Access the full text.
Sign up today, get DeepDyve free for 14 days.
Ann Microbiol (2017) 67:343–358 DOI 10.1007/s13213-017-1261-7 REVIEW ARTICLE 1 1 Michelle S. Fernandes & Savita Kerkar Received: 5 August 2016 /Accepted: 21 February 2017 /Published online: 12 March 2017 Springer-Verlag Berlin Heidelberg and the University of Milan 2017 Abstract Tyrosinase is the main enzyme responsible for roseum, Bacillus thuringiensis, Pseudomonas putida F6 and enzymatic browning of fruits post-harvest and melanogenesis Ralstonia solanacearum (Liu et al. 2004;Ruan et al. 2005; in mammals, an undesirable phenomenon. This encouraged Claus and Decker 2006; Dalfard et al. 2006; Hernández- researchers to seek potent tyrosinase inhibitors for application Romero et al. 2006; McMahon et al. 2007; Shuster and in the food and cosmetics industries. Despite an increased Fishman 2009). In eukaryotes, they serve several other func- knowledge of tyrosinase inhibitors from plants and synthetic tions apart from melanin production. They are important for sources in the past few years, inhibitors of microbial origin are wound healing and serve as primary immune response in under-explored. Thus, this article surveys tyrosinase inhibitors plants, sponges, and many invertebrates (Van Gelder et al. produced by microorganisms and hence, serves as an updated 1997; Cerenius and Söderhäll 2004;Müller et al. 2004), and database of tyrosinase inhibitors from microbial sources. are also involved in sclerotization in arthropods (García‐ Borrón and Solano 2002). Recently, enzyme inhibitors have been gaining attention as . . . . Keywords Inhibitor Melanogenesis Bacteria Fungi indispensable tools, not only for the study of the respective Tyrosinase enzyme structure but also for their potential in pharmaceuticals and agriculture (Imada 2004). Tyrosinase plays a key role in melanogenesis in mammals and enzymatic browning in fruits Introduction and fungi, through a series of reactions leading to the formation of a dark pigment, melanin (Chang 2009). Although melanin Over the past several years, tyrosinase (EC 184.108.40.206) has plays an important role in the phytoprotection of human skin been studied extensively in a wide area of research. from UV rays, depigmentation is an esthetic problem in a wide Tyrosinase enzyme is ubiquitous in nature, found in both range of human populations (Solano et al. 2006;Brenner and prokaryotes as well as eukaryotes. There are several examples Hearing 2008). In addition, browning of fruits and mushrooms of well-characterized tyrosinases from prokaryotes. The first post-harvest is undesirable, as it reduces the commercial value well-described tyrosinase was reported in Streptomyces sp. of the product. The development of tyrosinase inhibitors has (Lerch and Ettinger 1972; Katz et al. 1983); however, this also become a better alternative in controlling insect pests, as enzyme has also been reported from other genera, such as the enzyme also plays an important role in developmental and Bacillus megaterium, Rhizobium sp., Symbiobacterium defensive functions in insects (Sugumaran 2002). Due to these thermophilum, Pseudomonas maltophilia, Sinorhizobium varied applications, tyrosinase inhibitors have been gaining meliloti, Marinomonas mediterranea, Thermomicrobium importance as the best alternative for these approaches. Tyrosinase inhibitors have been discovered and reviewed from various natural and synthetic sources (Kim and Uyama * Savita Kerkar 2005;Khan 2007;Parvez etal. 2007; Schurink et al. 2007; email@example.com Likhitwitayawuid 2008; Lin et al. 2008;Chang 2009, 2012a; Loizzo et al. 2012;Chanetal. 2014;Chenet al. 2015; Department of Biotechnology, Goa University, Taleigao Plateau, Goa 403206, India Kilimnik and Dembitsky 2016). However, limited literature 344 Ann Microbiol (2017) 67:343–358 has been reviewed about tyrosinase inhibitors produced by activity of type 3 copper proteins. Asn and Glu residues microorganisms. Microorganisms produce several bioactive are highly conserved in type 3 copper proteins and are compounds and have potential as important new sources of assumed to play a role in the activation of the conserved water tyrosinase inhibitors. Hence, this article reviews several tyros- molecule. We have listed in Table 1 tyrosinases from different inase inhibitors produced by microorganisms in the literature microbial sources. for use in the depigmentation of hyperpigmented skin and other applications. Melanogenesis in mammals Biochemical characteristics of tyrosinase Melanin is an important pigment in mammals, synthesized and distributed in the skin and hair bulbs, that absorb free radicals In this section, we give a brief overview of tyrosinase from generated within the cytoplasm and also protect the host from bacteria, plants and fungi, with more emphasis on mushroom various types of ionizing radiation (Seiberg et al. 2000; tyrosinase. Because of difficulties in producing tyrosinase from Schaffer and Bolognia 2001). In mammals, a mixture of two humans in large quantities, its three-dimensional structure is types of melanin, eumelanin (brown or black pigment) and still unknown. Tyrosinase is a polyphenol oxidase enzyme pheomelanin (red or yellow pigment), are found. The for- which uses molecular oxygen to catalyze sequential reactions, mation of melanin occurs through a series of oxidative such as (i) hydroxylation of monophenols to o-diphenols, reaction, where tyrosine is converted to dihydroxyphenylalanine followed by (ii) oxidation of o-diphenols to o-quinones. The (DOPA) and, further, to dopaquinone by tyrosinase. quinones self-polymerize or react with other substances to form Dopaquinone is further auto-oxidized to dihydroxyindole or to melanin. They belong to a large group of proteins, namely type dihydroxyindole-2-carboxylic acid (DHICA) by dopachrome 3 copper proteins, responsible mainly for the first step in tautomerase and DHICA oxidase to form eumelanin. melanin synthesis. Both copper atoms are coordinated by Subsequently, pheomelanin is formed (Raper 1928;Kobayashi conserved three histidine residues. In melanin synthesis, three et al. 1995;Borgeset al. 2001). types of tyrosinase, namely oxy, met, and deoxy, with different Melanogenesis is regulated by three different signaling path- binuclear copper structures are involved. The resting form of ways: protein kinase C-mediated pathway, cAMP-mediated tyrosinase consists of a mixture of met and oxy forms, with pathway, and mitogen-activated protein kinase (MAPK) path- 85% of the met form (Sánchez-Ferrer et al. 1995;Kim and way. Although there are three enzymes active in the process of Uyama 2005; Claus and Decker 2006). melanogenesis, tyrosinase plays the key role in the formation of The first crystal structure of tyrosinase was determined from melanin, whereas the rest adjust the type of pigment formed Streptomyces castaneoglobisporus (Matoba et al. 2006). The (Kobayashi et al. 1995). Microphthalmia-associated transcrip- low sequence homology between tyrosinase of different tion factor (MITF) is phosphorylated by MAPK, which is sources can be related to the differences in their structure and essential for its activation as well as degradation. cAMP serves function. In fungal tyrosinases, one histidine residue is linked as a starting point of several interacting signaling cascades in by thioether bond to the side chain of a cysteine residue. This melanin synthesis as well as regulating melanin production and feature is not found in bacterial tyrosinase. Haudecoeur et al. PI3K. Stimulation with cAMP inhibits PI3K signaling, thereby (2014) reported that there was some similarity and difference increasing the synthesis of melanin via increased transcription between the binding sites of tyrosinase from different origins of tyrosinase and TRP-1 (tyrosinase-related protein 1). using the same set of molecules. Selinheimo et al. (2007)also Therefore, the activation of PI3K or protein kinase B (AKT) compared the characteristics of fungal and plant tyrosinases and signaling reduces melanogenesis via the downregulation of suggested that the enzymes showed different features in terms MITF expression, as AKT is an effector of PI3K (Bertolotto of substrate specificity, stereo-specificity, inhibition, and ability et al. 1998; Hemesath et al. 1998; Meinkoth et al. 1991;Xu to crosslink the model protein; however, they had similar reac- et al. 2000; Hennessy et al. 2005). tion mechanisms to produce identical quinone radicals. In a Due to the increased treatments for skin fairness, there has recent study, it was found that, although monophenols and been a demand for the prevention of skin pigmentation in the diphenols bind and orient identically at the active site, only cosmetics industry. This has lead to an increased interest on monophenols rotate during the reaction, thus enabling enzymes potent tyrosinase inhibitors, to prevent melanogenesis. with only diphenolase activity to have two constraints to pre- Although several tyrosinase inhibitors have been reported vent monophenolase activity. They also proposed a conserved from natural and synthetic sources, only a few of them are water molecule at the active site that mediates deprotonation of used as skin-whitening agents. Solano et al. (2006)suggests monophenol at the active site (Goldfeder et al. 2014). Kanteev that, although tyrosinase inhibition is the most common et al. (2015) also suggested that the active site flexibility and approach, a new innovative combined approach improved substrate deprotonation is crucial for the monophenolase the transdermal delivery system and enabled efficient Ann Microbiol (2017) 67:343–358 345 Table 1 Tyrosinase of different origins Source Molecular weight (kDa) pI References Gram-positive bacteria Streptomyces glaucescens 30.9 – Lerch and Ettinger (1972); Kim and Uyama (2005) Streptomyces antibioticus 30.6 7.17 Katz et al. (1983); Claus and Decker (2006) 14.9 6.54 Streptomyces avermitilis 33.5 9.33 Claus and Decker (2006) 13.6 6.64 Streptomyces nigrifaciens 18 – Nambudiri et al. (1972); Claus and Decker (2006) Streptomyces castaneoglobisporus 31 6.20 Matoba et al. (2006) 13 6.42 Streptomyces coelicolor 33.1 9.66 Claus and Decker (2006) 19.3 7.15 Streptomyces galbus 31.3 9.33 Claus and Decker (2006) 12.9 6.69 Streptomyces griseus 35.5 8.90 Claus and Decker (2006) 13.7 11.8 Streptomyces lincolnensis 30.7 6.84 Michalik et al. (1975); Claus and Decker (2006) 14.2 7.10 Streptomyces lavendulae 31 6.8 Claus and Decker (2006) 17 11.9 Streptomyces tanashiensis 31.3 6.84 Claus and Decker (2006) 12.5 9.39 Streptomyces sp. KY-453 29 9.9 Yoshimoto et al. (1985); Claus and Decker (2006) Streptomyces michiganensis 32 9.0 Philipp et al. (1991); Claus and Decker (2006) 34.5 Bacillus cereus 28.5 5.47 Claus and Decker (2006) Bacillus thuringiensis 16.8 4.87 Liu et al. (2004); Ruan et al. (2005) Corynebacterium efficiens 46.4 5.16 Claus and Decker (2006) Bacillus megaterium 31 – Shuster and Fishman (2009) Gram-negative bacteria Marinomonas mediterranea 74.5 4.84 Claus and Decker (2006) Marinomonas mediterranea 53.1 4.85 Claus and Decker (2006) Marinomonas mediterranea 28.6 9.89 Claus and Decker (2006) Nitrosomonas europaea 53.9 5.26 Claus and Decker (2006) Rhizobium etli (Rh.e.) 67.4 7.28 Claus and Decker (2006); Cabrera-Valladares et al. (2006) Sinorhizobium meliloti 54.1 4.65 Claus and Decker (2006) Ralstonia solanacearum 44 8.44 Hernández-Romero et al. (2005); Claus and Decker (2006) Stenotrophomonas maltophilia 18.6 9.27 Claus and Decker (2006) Pseudomonas melanogenum –– Yoshida et al. (1974); Claus and Decker (2006) Thermomicrobium roseum 43 4.9 Kong et al. (2000); Claus and Decker (2006) Vibrio tyrosinaticus 38.5 – Pomerantz and Murthy (1974); Claus and Decker (2006) Fungi Pycnoporus sanguineus 45 4.5–5.0 Halaouli et al. (2005); Halaouli et al. (2006) Trichoderma reesei 43.5 9.0 Selinheimo et al. (2006) Aspergillus oryzae 67 – Ichishima et al. (1984); Halaouli et al. (2006) Lentinula edodes 54–55 4.3–4.7 Kanda et al. (1996); Halaouli et al. (2006) 15–50 Neurospora crassa 46 8.3–8.5 Lerch (1983); Halaouli et al. (2006) Agaricus bisporus 13.4 4.7–5.0 Solomon et al. (1996) Mammals Human melanocyte 66.7 – Solomon et al. (1996) 346 Ann Microbiol (2017) 67:343–358 screening tests for validating their efficacy and safety. et al. 2008). Some authors use Bmelanogenesis inhibitors^ as Currently, arbutin, gentisic acid, hydroquinone, and aloesin the terminology for tyrosinase inhibitors; however, this is isolated from plants as well as 4-n-butylresorcinol, attributed to the inhibition of melanin synthesis, regardless deoxyarbutin, kojic acid, ascorbic acid, and azelaic acid are of its mode of action. Thus, tyrosinase inhibition could be used in the cosmetics industry, with strong inhibition against due to one of the following reasons, which could mislead tyrosinase (Solano et al. 2006;Parvezet al. 2007; Lin et al. the definition of an enzyme inhibitor: 2008; Gillbro and Olsson 2011). 1. Reducing agents causing chemical reduction of dopaquinone, e.g., ascorbic acid Enzymatic browning of plant-derived foods 2. o-Dopaquinone scavengers which react with dopaquinone to form a colorless product, e.g., thio-containing The browning of fruit and vegetables is of great concern in the compounds food industry, as it reduces its economic value. Browning 3. Alternative substrate with good affinity for the enzyme occurs due to various reasons, such as microbial spoilage, forming a different product, e.g., phenolic compounds mechanical damage and enzymatic reactions. Due to their thin 4. Non-specific enzyme inactivators such as acids and bases and epidermal layer, the respiration rate of vegetables and which inactivate the enzyme fruits is high; hence, they tend to lose their quality post-har- 5. Specific enzyme inactivators or suicide substrates vest. Enzymatic browning is a major concern in damaged 6. True inhibitors which bind to the enzyme and inhibit its fruits during post-harvest handling and processing, where activity tyrosinase enzyme plays a key role (Mayer 1987). Tyrosinase causes oxidation of the phenolic compounds in fruits, causing The true inhibitors can be subdivided further into three undesirable changes in color, flavor and texture, thereby categories based on their mode of inhibition, such as compet- reducing its marketability. The extent of browning depends on itive inhibitors, mixed type inhibitors, and non-competitive various factors, such as concentration of the enzyme and sub- inhibitors (Chang 2009, 2012b). The inhibitors mainly com- strate, oxygen availability, pH and temperature (Zheng et al. prise copper-binding agents and compounds binding on active 2008). Tyrosinase catalyzes the hydroxylation of phenolic sites (Mayer and Harel 1979;Robb 1984). Substrate ana- substrate tyrosine to DOPA via its monophenolase activity, logues include numerous aromatic acids, phenols and their which is further oxidized to dopaquinone by its diphenolase derivatives, and a few non-aromatic compounds, which main- activity. Further, these quinones are powerful electrophiles, ly behave as competitive inhibitors (Walker and McCallion which can be attacked by water, other polyphenols, amino 1980; Menon et al. 1990; Nicolas et al. 1994). As the enzyme is a metalloenzyme, metal chelaters such as carbon monoxide, acids, peptides and proteins, leading to Michael-type addi- tions. This is further converted to melanin through a series cyanide, azide ions, thiourea derivatives, kojic acid, tropolone, of reactions (Busch 1999). etc. could inhibit its activity. Inhibitors from natural sources The appearance of a product has been an essential attribute have been preferred over synthetic sources, with microbial in the food industry and, therefore, several methods have been sources being an important area for exploration of some novel incorporated to reduce or stop enzymatic browning, such as and safe inhibitors for application in various sectors. blanching, microwave, autoclaving, application of chemicals, modified atmospheric packing, controlled atmospheric Tyrosinase inhibitors from fungi control, etc. (Singh et al. 2010; Ioannou and Ghoul 2013). However, these processes alter the quality, texture, and nutrient Fungi produce diverse bioactive compounds, including content of the product. Several enzyme inhibitors, namely antibiotics, enzymes, enzyme inhibitors, growth promoters, citric acid, ascorbic acid and kojic acid, have been used for etc., exploited in the agriculture, food, and pharmaceutical the prevention of browning (Loizzo et al. 2012; Ioannou and industries. Fungi from different genera have been found to Ghoul 2013). However, since safety is the main concern in the demonstrate anti-tyrosinase activity. One of the genera, food industry, the search for a considerably safe tyrosinase Aspergillus, was found to produce several compounds having inhibitor from a natural source is an eminent topic of research. tyrosinase inhibitory activity (Fig. 1). Kojic acid (5-hydroxy- 2-(hydroxymethyl)-gamma-pyrone), a well-studied tyrosinase inhibitor, was reported from A. albus (Saruno et al. 1979), Tyrosinase inhibitors A. candidus (Wei et al. 1991), A. niger (Vasantha et al. 2014), and Penicillium sp., a good chelator and also a scavenger of free Tyrosinase inhibitors are widely used in cosmetology and radicals. Saruno et al. (1979) reported kojic acid with 80% agriculture. There are several tyrosinase inhibitors derived inhibition by A. albus, whereas Vasantha et al. (2014)reported A. niger S16 producing kojic acid that showed 84% from natural and synthetic sources (Parvez et al. 2007;Lin Ann Microbiol (2017) 67:343–358 347 Compound Structures Mechanism IC = n.d Down regulation MITF via induction of ERK 50 OH Terrein activity. OH Inhibtion of MITF promoter activity. H C O O HO Chelate copper at its active site. IC = 61.9 μM Competitive inhibition Kojic acid OH O OH OH Not Known IC = 74 μM OH Decumbenone A O OH OH H Not Known OH Decumbenone C IC = 0.9 μM OH R1 R1=R4=H, Competitive inhibition of monophenolase R2 O O IC = 9 μM R2=R3=OH activity R3 R4 OH R1 IC = 191 μM; R2 O O Irreversible inhibition of monophenolase R1=R2=OH, and diphenolase activity. 181 μM R3=R4=H R3 R4 OH R1 R2 O O Irreversible inhibition of monophenolase R1=R2=R4=OH, IC = 184 μM; R3 R3=H and diphenolase activity. R4 OH 212 μM R1 Daidzein Competitive inhibition of monophenolase R2 O O R1=R3=R4=H, IC = 203 μM activity. R2=OH R3 R4 OH R1 Glyceitein Competitive inhibition of monophenolase R2 O O R1=R4=H, activity. IC = 218 μM R2=OH, (6-Methoxy ,7,4’- 50 R3 R3=OCH3 R4 OH R1 Daidzin Competitive inhibition of monophenolase R2 O O R1=R3=R4=H, activity. IC = 267 μM 50 R2=OGlc R3 R4 OH glucoside) R1 Genistin R1=R3=H, Competitive inhibition of monophenolase R2 O O R2=OGlc, IC = 343 μM activity. R4=OH R3 O-glucoside) R4 OH Fig. 1 Structures of tyrosinase inhibitors from Aspergillus sp. (n.d not defined) competitive inhibition of mushroom tyrosinase with an IC P. decumbens and A. sulphureus; in addition, the Aspergillus value of 61.9 μM. Based on several studies, kojic acid at a genus also produced a new potent decaline derivative, minimum level of exposure or consumption was found to have decumbenone C, showing cytotoxic activity against human negligible toxicity to humans (Burdock et al. 2001; Nohynek melanoma cells with an IC value of 0.9 μM (Fujii et al. et al. 2004). Apart from kojic acid, the Aspergillus genus pro- 2002; Zhurayleva et al. 2012). Terrein was isolated for the first duces diverse compounds with anti-tyrosinase activity. time from A. terreus, which inhibited melanin synthesis by the Aspergillus niger produces metallothioneins, which are strong downregulation of MITF via the induction of ERK activity and tyrosinase inhibitors having strong avidity to chelate copper at inhibition of MITF promoter activity (Raistrick and Smith its active site (Goetghebeur and Kermasha 1996). An inhibitor 1935; Kim et al. 2007, 2008). A melanogenesis inhibitor iso- of melanin formation, decumbenone A, was isolated from lated from Penicillium sp. 20135 was also identified as terrein, 1’ 3’ 2’ 348 Ann Microbiol (2017) 67:343–358 which inhibited melanin formation in B16 melanoma cells; different melanogenesis inhibitors, with not all of them show- however, neither inhibited mushroom tyrosinase nor demon- ing inhibition of tyrosinase (Tsuchiya et al. 2008). strated cytotoxic activity in a cell-based assay (Park et al. Marine fungi live in a unique environment with stressful 2004; Kim et al. 2005). In addition, Chang et al. (2007)report- conditions of pH, temperature, salinity, oxygen nutrients, and ed seven isoflavones from soygerm koji fermented with light, and, therefore, serve as promising candidates for novel A. oryzae BCRC 32288 having anti-tyrosinase activity. Five bioactive compounds. On investigation, few known and novel compounds, 6,7,4′-trihyroxyisoflavone (IC =9 μM), compounds with tyrosinase inhibition activity have been re- daidzein (IC = 203 μM), glycitein (IC = 218 μM), ported from marine-derived fungi (Fig. 3). Two derivatives of 50 50 daidzin (IC = 267 μM), and genistin (IC =343 μM), showed kojic acid, kojic acid dimethyl ether and kojic acid 50 50 inhibitory activity against the monophenolase activity of tyros- monomethyl ether, as well as phomaligol A, were identified inase by competitive inhibition. The other two compounds, from broth of marine-derived fungi Alternaria sp. isolated 7,8,4′-trihyroxyisoflavone and 5,7,8,4′-tetrahydroxyisoflavone, from marine green algae having tyrosinase inhibitory activity irreversibly inhibited both monophenolase with IC values of (Li et al. 2003). Similarly, two compounds, 6-n-pentyl-α- 191 μM and 184 μM, respectively, as well as diphenolase ac- pyrone and myrothenone A, identified from marine-derived tivity with IC values of 181 μM and 212 μM, respectively, of fungi Myrothecium sp. MFA 58 isolated from algae were tyrosinase. Additionally, dietary daidzein, a phytoestrogen com- stronger than kojic acid (IC =7.7 μM), with IC values of 50 50 ponent of soy, did not show toxicity to the female reproductive 0.8 and 6.6 μM, respectively (Li et al. 2005). Zhang et al. tract in rats (Lamartiniere et al. 2002). Tyrosinase inhibition 2007 reported a pyrone derivative, 6-[(E)-hept-1-enyl]-α- activity (56.18%) was also found in rice bran fermented with pyrone, exhibiting anti-tyrosinase activity (IC = 4.5 μM) A. oryzae (Razak et al. 2015). isolated from Botrytis sp. Two sesquiterpene compounds were Another genus found to produce diverse compounds having isolated from a marine-derived fungi Pestalotiopsis sp. Z233, anti-tyrosinase activity is Trichoderma (Fig. 2). Lee et al. isolated from algae, 1β,5α,6α,14-tetraacetoxy-9α- (1995) reported a particular strain of T. harzianum MR304 to benzoyloxy-7βH-eudesman-2β,11-diol and 4α,5α-diacetoxy- produce a melanin synthesis inhibitor, MR304-1, identified as 9α-benzoyloxy-7βH-eudesman-1β,2β,11-tetraol, having ty- an isocyanide compound, which inhibited melanogenesis in- rosinase inhibitory activity. These compounds were induced hibition in S. bikinienesis, B16 melanoma cells [minimum by abiotic stress elicitation by CuCl with IC values of 2 50 inhibitory concentration (MIC) = 0.05 μg/mL], and mushroom 14.8 μM and 22.3 μM, respectively (Wu et al. 2013). tyrosinase (IC = 0.25 μg/mL). Trichoderma harzianum iso- Apart from marine fungi, several other fungal groups are lated from soil was also reported to produce several melanin reported for anti-tyrosinase activity (Fig. 4). Azelaic acid (1,7- synthesis inhibitors. Two new tyrosinase inhibitors, MR566A heptanedicarboxylic acid) produced by yeast, Pityrosporum (IC =1.72 μM) and MR566B (IC =47 μM), along with a ovale, has a cytotoxic effect on the melanocytes of primary cu- 50 50 new oxazole compound MR93B (IC >6000 μM), six taneous melanoma. It is a straight chain, saturated dicarboxylic known isocyanide compounds, and MR93A (IC > acid which inhibits tyrosinase by competing for the α- 6000 μM), were isolated showing inhibition against mush- carboxylate binding site of the L-tyrosine substrate of the en- room tyrosinase, melanogenesis inhibition in S. bikinienesis, zyme (Schallreuter and Wood 1990). Nevertheless, azelaic acid and B16 melanoma cells. The isocyanide compounds were is a known compound that has been previously reported as non- identified as 1-(1,4,5-trihydroxy-3-isocyanocyclopenten-2- toxic (Töpert et al. 1989). In addition, yeasts also produce cyto- enyl)ethanol, 2-hydroxy-4-isocyano-α-methyl-6- solic proteins, metallothioneins characterized by the selective oxabiocyclo[3.1.0]hex-3-ene-3methanol, 4-hydroxy-8- binding of a large amount of heavy metal ions and high cysteine isocyano-1-oxaspiro[4.4]cyclonon-8-en-2-one, MR304A, content. Neurospora crassa is also reported to produce a copper methyl-3-(1,5-dihydroxy-3-isocyanocyclopent-3-enyl)prop-2- metallothionein, which serves as a metal donor for apotyrosinase enoate, and an unidentified compound with IC values of 3.6, (Lerch 1981). Tanaka et al. (1996) reported an anti-melanoma 4.9, 0.089, 47, 1.72, and 0.0014 μM, respectively (Lee et al. compound from Talaromyces sp. FO-3182, which reduced the 1997a, b). Lee et al. (1997a, b) proposed that the isocyano melanin content of B16 melanoma cells. Melanocin A was iso- group in the compounds plays a vital role in inhibiting the lated from the fermentation broth and mycelia extract of activity of mushroom tyrosinase enzyme. Imada et al. (2001) Eupenicillium shearii F80695, showing inhibition against mush- reported mushroom tyrosinase inhibitor produced by room tyrosinase (IC =0.009 μM) and B16 melanoma cells Trichoderma sp. H1-7 isolated from a marine environment as (MIC = 0.9 μM) due to the presence of isocyanide group in the having 1000–2500 U/mL inhibitory activity. A competitive compound (Kim et al. 2003). Two steroids were isolated from inhibitor of tyrosinase (5.4 × 10 U/mL) similar to the structure the fungus Cunninghamella elegans,17α-ethynyl-11α,17β- of homothallin II was isolated from T. viridae strain H1-7 from dihyroxyandrost-4-en-3-one (IC = 5950 μM) and 17α-ethyl- marine sediments which inhibited the enzyme by binding to 11α,17β-dihyroxyandrost-4-en-3-one (IC = 1720 μM), hav- the copper active site. In addition, this strain produced seven ing tyrosinase inhibition activity (Choudhary et al. 2005). Ann Microbiol (2017) 67:343–358 349 Compound Structures Mechanism HO MR566A 2 1 Me IC = 1.72 μM Isocyano group in the compound plays role 4 3 OH 1-(3-chloro-1,2-dihydroxy-4-isocyano- in inhibition of the enzyme 4-cyclopenten-1-yl)ethanol CN OH CI MR566B HO IC = 47 μM Isocyano group in the compound plays role HO Me OH 1-(1,2,3-trihydroxy-3-isocyano-4- HO in inhibition of the enzyme cyclopenten-1-yl)ethanol CN HO Me 1-(1,4,5-Trihydroxy-3- Isocyano group in the compound plays role OH IC = 3.6 μM isocyanocyclopenten-2-enyl)ethanol in inhibition of the enzyme CN OH OH HO 2-Hydroxy-4-isocyano-α-methyl-6- Me Isocyano group in the compound plays role IC = 4.9 μM OH oxabicyclo[3.1.0]hex-3-ene-3- in inhibition of the enzyme CN methanol 4-Hydroxy-8-isocyano-1- O O 5 2 Isocyano group in the compound plays role IC = 0.089 μM oxaspiro[4.4]cyclonon-8-en-2-one 3 50 in inhibition of the enzyme CN 6 OH 9 7 HO HO Me Isocyano group in the compound plays role MR304A IC = 47 μM OH in inhibition of the enzyme CN OH Methyl-3-(1,5-dihydroxy-3- COOMe Isocyano group in the compound plays role isocyanocyclopent-3-enyl)prop-2 OH IC = 1.72 μM in inhibition of the enzyme enoate CN OH COOH Isocyano group in the compound plays role IC = 0.0014 μM in inhibition of the enzyme CN 5’ 1’ MR93B N O CH OH 2’ 2 Not Known IC >6000 μM 4 50 4-[(1Z)-3-hydroxy-2-hydroxymethyl- O O 4’ 1 3’ Me OH 1-propen-1-yl]oxazole OH Not Known MR93A N O Me IC >6000 μM O O OH NC 5 IC = 5.4 x 10 Competitive inhibition HO Homothallin II 1 Units/mL Fig. 2 Structures of tyrosinase inhibitors from Trichoderma sp. Entomopathogenic fungi are a source of several potential bioac- skin. We have reviewed compounds serving as tyrosinase or tive compounds. Three new polyphenolic tyrosinase inhibitors melanogenesis inhibitors isolated from mycelia or fruiting were isolated from an entomopathogenic fungi Paecilomyces bodies of mushrooms (Fig. 4). Two tyrosinase inhibitors gunnii, paecilomycones A, B, and C, having IC values of have been isolated, purified, and characterized from the 110, 170, and 140 μM, respectively, which compete for the mushroom Agaricus hortensis with competitive and non- active binding site of the enzyme and, in addition, the number competitive inhibition, respectively (Madhosingh and of hydroxyl groups present in these compounds also plays a vital Sundberg 1974). Similarly, two isomeric compounds hav- role in its inhibitory activity (Lu et al. 2014). ing tyrosinase inhibitory activity were isolated from the There have been several studies of secondary metabolites lipophilic fractions Albatrellus confluens and identified as from Basidiomycetes with different biological activities, with neogrifolin (IC =25 μM) and grifolin (IC = 760 μM), 50 50 few studies on tyrosinase inhibition and depigmentation of the activities of which are affected by the position of the IC = n.d R = CHO IC = 6.6 μM IC = n.d R = Me IC = n.d R = H 350 Ann Microbiol (2017) 67:343–358 Compound Structures Mechanism HO MeO Not Known Phomaligol A NH-R HO Not Known Myrothenone A Not Known Kojic acid di-methyl ether OMe Not Known Kojic acid monomethyl ether OMe 1 IC = 0.8 μM O O O 50 6-n-pentyl-α-pyrone Not Known 1’ 3’ 5’ 24 18 23 O 26 21 16 22 1β,5α,6α,14-tetraacetocy-9α- O 14 O benzolyloxy-7βH-eudesman- O 10 HO 2 B IC = 14.8 μM Not Known 2β,11-diol 12 50 4 6 OH O 13 15 27 O O 4α,5α-diacetoxy-9α- OH 16 22 benzoyloxy-7βH-eudesman- 14 HO O 10 9 IC = 22.3 μM Not Known 1β,2β,11-tetraol 8 50 HO O 7 3 11 4 6 O OH 24 O 25 O 15 13 6-[(E)-hept-1-enyl]-a-pyrone O O IC = 4.5 μM Not Known Fig. 3 Structures of tyrosinase inhibitors from marine-derived fungi (n.d not defined) farnesyl group on the aromatic ring (Misasa et al. 1992). and possibly chelating the copper in tyrosinase, whereas Neogrifolin was also isolated from mushroom Polyporus 5-hydroxymethyl-2-furaldehyde is a non-competitive in- confluens, which showed 100% tyrosinase inhibition at hibitor which may form a Schiff base with primary amino 50 ppm (Minosasa et al. 1991). Melanogenesis inhibitor, groups in the enzyme, rather than binding to the active 2-amino-3H-phenoxazin-3-one was identified from the site (Kang et al. 2004). A chromene type compound, mushroom A. bisporus (Lu et al. 2002). Sharma et al. daedalin A (IC = 194 μM), was reported from the (2004) reported the methanolic extract of an edible mushroom mycelia culture broth of the mushroom Daedalea Dictyophora indusiata non-competitively inhibiting mushroom dickinsii, which competitively inhibited tyrosinase, for tyrosinase activity and was identified as 5-hydroxymethyl-2- its substrate L-tyrosine. Further studies on the application furfural (HMF). However, the carcinogenic potential of HMF of this compound in an in vitro human skin model sub- in food was found to be contradictory due to limited data from stantiated its activity on suppressing melanogenesis with- toxicity studies and, therefore, there is a need for improvement out affecting cell viability by directly inhibiting tyrosinase in the risk assessment for HMF (Abraham et al. 2011; activity in melanocytes (Morimura et al. 2007, 2009). Capuano and Fogliano 2011). Two tyrosinase inhibitors, 5-hydroxymethyl-2-furaldehyde (IC =720 μM) and Tyrosinase inhibitors from bacteria protocatechualdehyde (IC = 2.896 μM), were isolated from the fruiting body of a medicinal mushroom Bacterial metabolites represent a diverse array of chemical Phellinus linteus. Protocatechualdehyde competitively compounds with different biological activities. Several reports binds to the copper active site with its hydroxyl group of tyrosinase inhibition by bacteria have been discussed in this Ann Microbiol (2017) 67:343–358 351 Compound Structures Mechanism HO CH IC = 25 μM Not Known CH 50 3 Neogrifolin OH CH CH CH 3 3 3 H C 3 OH Grifolin CH Not Known IC = 760 μM CH CH CH 50 OH 3 3 3 HO NC Isocyanide group in the compound plays a role Melanocins A OH HO in inhibition of the enzyme IC = 0.009 μM 50 NH OHC OH NH O N 2-amino-3H-phenoxazin-3-one IC = n.d Not Known O O 8a O O 2 OH Competes with the substrate L-tyrosine of IC = 194 μM Daedalin A 50 4a the enzyme tyrosinase. HO 6 NC IC = n.d Not Known COOH H H 7 9 6a 9a O O Paecilomycones B IC = 170 μM Competes for the active binding site of the 3b 5 2 3a enzyme. 4 3 OR HO R R1=OH Paecilomycones A HO Competes for the active binding site of the IC = 110 μM R2=H enzyme. OR HO R R1=NH HO Paecilomycones C IC = 140 μM Competes for the active binding site of the R2=H enzyme. HO IC = 2.9 μM Competes with copper active site of the enzyme Protocatechualdehyde 50 O HO with its hydroxyl group. Chelates copper in the active site of the wnzyme. O O IC = n.d 5-Hydroxymethyl-1,2-furfural 50 HOH C CHO base with primary amino groups in the enzyme. (HMF) IC = n.d Competes for the α-carboxylate binding site of HOOC COOH Azelaic acid 50 L-tyrosine substrate of the enzyme. OH 1 R 11 13 H R=-C C, IC = 5950 μM 9 14 50 15 Not known 17 α-ethynyl-11 α,17β- 2 10 8 H R1=OH 3 7 dihydroxyandrost-4-en-3-one 4 6 o R2=H OH 1 R 11 13 17 α-ethyl-11 α,17β- IC = 1720 μM R=-H C CH , 9 14 50 2 3 15 Not known 2 10 8 dihydroxyandrost-4-en-3-one H R1=OH 3 7 4 6 o R2=H O O O 5-Hydroxy-xymethyl-2- IC = 720 μM Not-competitive inhibition furaldehyde OH Fig. 4 Structures of tyrosinase inhibitors from other fungi (n.d not defined) article (Fig. 5). Among them, Streptomyces sp. serves as a enzyme inhibitors (Umezawa 1972). There have been several potential source of several bioactive compounds, including reports on tyrosinase inhibition from the genus Streptomyces. 10’ 8’ 6’ 8’ 6’ 8’ 6’ OH OH O O O O C H 5 11 - - C C6 6H H12 12 O O O O OX C C6 4H H12 8 C C6 7H H12 15 352 Ann Microbiol (2017) 67:343–358 Compound Structures Mechanism O H O O N O Inhibits tyrosinase through post-translational NH 2 IC > 703.3 μM O H 50 Melanostatin N O O N H O COOH COOH IC = 6.8 μM O H 3 18 13 O N Inhibits tyrosinase through post-translational O N 16 15 14 11 10 7 6 4 H N O N Amphistin 9 2 2 H H NH O 8 COOH N O Cyclo(-L-Pro-L-Tyr-L-Pro-L-Val-) H O N O Not Known O N IC = n.d O 50 O N OH 1 3 NC 3’ 1’ Byelyankacin IC = 0.0021 μM; Isocyanide group binds to copper active site of the O O 5’ 50 5’’ 1’’ O O enzyme. HO 3’’ 0.03 μM HO OH H C 8 3 6 CH 9 5 OH IC = n.d Albocycline K3 OH 4 50 Not Known 11 3 CH 12 2 H C 13 1 3 O O O OCH3 H C 8 7 6 9 5 OH-3984 K1 4 CH IC = n.d Not Known 10 50 CH 3 O O 12 2 1 H C O OCH H C CH R=H 3 IC = n.d OH-3984 K2 50 CH Not Known 3 O O H C OR 3 3 A: 1 R 4 2 1 2’ 4’ NH Thalassotalic acid A HO 7 IC = 130 μM 6 Not Known R 50 R1=OH , R2=A B: 1 2’ 4’ 4 2 R Thalassotalic acid B 1 NH IC = 470 μM 5 Not Known HO 7 6 R 2 R1=OH , R2=B C: 4 1 R Thalassotalic acid C 2 1 2’ 4’ Not Known IC = 280 μM 5 NH 7 50 HO 2 R1=OH , R2=C O N Cl O O Competitive inhibition 12815 A IC = 9 μM N O (Streptochlorin) O N O O Not Known IC = 1086 μM 12815 B O N Suppresses gene encoding melanocortin receptor-1. IC = n.d OH O O 50 Interferes with phosphorylation MAPK, extracellular signal Daidzein regulated kinase and glycogen synthase kinase. HO O O Decreases expression of tyrosinase, TRP-1 and TRP-2. Suppresses gene encoding melanocortin receptor-1. OH Interferes with phosphorylation MAPK, extracellular signal IC = n.d Equol 50 regulated kinase and glycogen synthase kinase. HO O O Decreases expression of tyrosinase, TRP-1 and TRP-2. IC = n.d Suppresses tyrosinase activity and expression through Genistein positive regulator, MITF and MAPK inactivation. HO O O Reduces activity and expression of tyrosinase. OPO P O O O O O O O O O O O O O O O O O O O O Lipoteichoic acid O O O O XO O O O O O O Degrades MITF via regulation of signaling and RNA O O IC = n.d X=H;D-ala stability of proteins involved in melanogenesis. OOO O Down-regulation of transcription gene encoding melanocortin 1 receptor. NH NH Decreases phosphorylation of cAMP response element- Uracil IC = n.d N N 50 binding protein. H H Represses expression of MITF 9’ 9’ Ann Microbiol (2017) 67:343–358 353 Fig. 5 Structures of tyrosinase inhibitors from bacterial source (n.d not partially purified methanol extract of the metabolite exhibited defined) an IC value of 2 μg/mL (Hsu et al. 2014; Liang et al. 2015). In addition, tyrosinase inhibitors are reported from a marine Gram-negative bacterium, Thalassotalea sp. PP2-459 isolated Melanostatin isolated from the fermentation broth of from a marine bivalve and identified as thalassotalic acid A, B, S. claviver N924-2 inhibited melanin formation in B16 mela- and C, with IC values of 130, 470, and 280 μM, respective- noma cells (IC >703.34 μM) (Ishihara et al. 1991). Three ly. Thalassotalic acids are N-acyl dehydrotyrosine derivatives compounds, OH-3984 K1, OH-3984 K3, and albocycline K3, produced by this bacterium, thalassotalic acid A being compa- a macrocyclic compound isolated from Streptomyces sp. OH- rable to the inhibitory activity of arbutin and could be used as a 3984, inhibited melanogenesis of B16 melanoma cells at con- whitening agent or in preventing browning of foods. They centrations of 7.5, 3.8, and 15 μg/mL respectively; however suggest that the presence of a carboxylic acid and a straight the mechanism of action is unknown (Takamatsu et al. 1993, aliphatic chain increased enzyme inhibition within this struc- 1996). Arai et al. (1997) reported melanogenesis inhibitor tural class of inhibitors (Deering et al. 2016). produced by Streptomyces sp. KP-3052, which was identified Probiotics such as Lactobacillus sp. and Bifidobacterium as amphistin with IC =6.8 μMagainst thegrowth of B16 sp. have been used in several fermented food products. In melanoma cells. Amphistin is a pseudotripeptide with activity addition, the fermented by-products of such probiotic bacteria similar to melanostatin and feldamycin, which inhibits tyros- have been recently explored for bioactive compounds with inase through post-translational modification of the enzyme or applications in cosmetics. Several investigators have reported other modulatory proteins. Imada et al. (2001) screened and fermented substrates that inhibit tyrosinase activity and mela- reported two bacterial isolates, one being actinobacteria pro- nogenesis. Lactobacilli and bifidobacteria are the two major ducing tyrosinase inhibitor, having 19 and 6 U/mL inhibitory bacteria involved in fermentation, resulting in producing me- activity, respectively. Chang and Tseng (2006)isolated and tabolites suppressing melanogenesis. Lactobacillus helveticus screened actinobacteria from forest soil for anti-tyrosinase ac- produced a novel tyrosinase inhibitor, identified as a cyclic tivity; one bacterial strain, Streptomyces sp. TI-B10, showed tetra peptide, cyclo(-L-Pro-L-Tyr-L-Pro-L-Val-), by the highest tyrosinase activity (46 U/mL), which was further Kawagishi et al. (1993). Lactobacillus plantarum M23 isolat- improved to 73 U/mL when cultured in YMG medium at ed from raw milk showed better tyrosinase inhibitory activity pH 8.0 and 30 °C. Chang et al. (2008)reported as compared to commercial lactic acid bacteria, showing S. hiroshimensis TI-C3 isolated from soil, showing anti- 52.1% tyrosinase inhibition and 32% inhibition of melanoma tyrosinase activity (498 U/mL) with enhanced activity (905 B16 cells. Tyrosinase inhibition activity was enhanced to U/mL) using glucose and malt extract as the sole carbon and 84.05% in fermented milk by the addition of yeast extract nitrogen sources, respectively. Streptomyces roseolilacinus and grape, incubated at 37.1 °C for 14.8 h (Heo et al. 2007; NBRC 12815 produced two compounds, 12815 A (IC = Lim and Kim 2012). In addition, Kuwaki et al. (2012)report- 9 μM) and B (IC =1086 μM), showing anti-tyrosinase ac- ed a plant-based paste fermented by a lactic acid bacteria and tivity against mushroom and mammalian tyrosinases. yeast, and extracted with PBS, which demonstrated anti- However, 12815 A was further identified as streptochlorin, tyrosinase activity with an IC value 58.5 mg/mL. which was found to be a competitive inhibitor of tyrosinase Bifidobacterium adolescentis culture filtrate was found to de- with anti-nematode activity and cytotoxicity (Nakashima et al. crease melanogenesis of melanoma cell by inhibiting tyrosi- 2009). This study also suggested that compound 12815 A nase activity mediated by its antioxidant property (Huang and produced by S. roseolilacinus and its companions could be a Chang 2012). Tsai et al. (2013)reported L. rhamnosus spent common feature in related species. culture supernatant showing 71.3% tyrosinase inhibitory ac- Several studies on melanogenesis inhibitors have been re- tivity, where the supernatant showed no difference in ac- ported from Gram-negative bacteria. Takahashi et al. (2007) tivity on heating at 100 °C for 30 min. Chen et al. (2013) reported an Enterobacter sp. B20 isolated from soil produced reported extracts from L. plantarum TWK10 fermented soy a novel potent melanogenesis inhibitor, byelyankacin, which milk to inhibit tyrosinase activity (38.33%) and melanin pro- inhibited tyrosinase (IC = 0.0021 μM) by binding its duction in B16F0 melanocytes (27.56%) compared to non- isocyanide group to the copper active site of the enzyme, fermented soy milk, structurally elucidated as an aglycone iso- and also inhibited melanogenesis of B16-2D2 melanoma cells flavone similar to daidzein, equol, or genistein. These (IC =0.03 μM). Burkholderia cepacia TKU025, a Gram- isoflavones have been known to be non-toxic to the reproduc- negative bacteria isolated from soil, also produced tyrosinase tive tract of female rats (Fritz et al. 1998; Lamartiniere et al. inhibitor (2890 U/mL) in nutrient broth, which was maxi- 2002). Chen et al. (2013) further report the inhibition of mela- mized after cultivation in 1% squid pen as a sole C/N source nogenesis by suppressing tyrosinase activity and expression to 5000 U/mL. The inhibitor was stable at varying pH condi- through a positive regulator, microphthalmia-associated tran- tions (pH 2–12) and thermostable at 100 °C for 60 min. The scription factor (MITF) and p38 MAPK inactivation. Daidzein 354 Ann Microbiol (2017) 67:343–358 and equol reduced the melanin content by suppressing gene and steroids, inhibitors isolated from fungi are structurally encoding melanocortin receptor-1, interfering with phosphor- comparable to those from plant sources. Tyrosinase inhibitors ylation of p38 MAPK, phosphorylation of extracellular signal from fungi are derivatives of isoflavones and pyrones, along regulated kinase and glycogen synthase kinase, and decreasing with terpenes, steroids, and alkaloids, which may reversibly or the expression of tyrosinase, TRP-1, and TRP-2 (Chang irreversibly inactivate the enzyme. In contrast, tyrosinase and Tsai 2016). Kim et al. (2015) further report a cell wall inhibitors from bacteria comprise a smaller group, belonging to component of L. plantarum, lipoteichoic acid, to inhibit alkaloids, macrolides, and polyphenols, which competitively melanogenesis in B16F10 mouse melanoma cells by re- inhibit the enzyme. However, profound work on the mecha- ducing the activity and expression of tyrosinase and, also, nism of these compounds needs to be established. To conclude, likely by degrading MITF via the regulation of signaling the information provided could serve as leads in the search for and RNA stability of proteins involved in melanogenesis. new inhibitors from microorganisms with increased efficiency Interestingly, the metabolite had no effect on mushroom and safety in the food and cosmetics industries. tyrosinase. Lactobacillus plantarum TWK10, an organism Acknowledgements The authors wish to thank the Head of the responsible for fermenting soy milk, contained a metabolite Department of Biotechnology for the facilities provided and UGC- exhibiting anti-melanogenesis in B16F0 mouse melanoma MANF scholarship for the funds provided (MANF-2012-13-CHR- cells, where the melanogenic inhibitor was identified as GOA-12673 to M.S.F.). uracil. Its activity was found to be due to the downregu- lation of a transcription gene encoding melanocortin 1 Compliance with ethical standards receptor, decreasing phosphorylation of cAMP response Funding This work was supported by the UGC-Maulana Azad fellowship element-binding protein, and repressing the expression of (MANF-2012-13-CHR-GOA-12673 to M.S.F.). MITF (Chang et al. 2015). Exopolysaccharides (EPS) isolated from L. sakei Probio 65 have also been reported, with tyrosi- Conflict of interest The authors declare that there is no conflict of nase inhibiting activity in the range 13.17–62.85% (Bajpai interest regarding the publication of this manuscript. et al. 2016). Wang et al. (2016) reported tyrosinase inhibition activity in walnuts, Moutan Cortex Radicis, and asparagus root Research involving human participants and/or animals This article does not contain any studies with human participants or animals per- extract fermented by B. bifidum with IC values of 420, 380, formed by any of the authors. and 260 μg/mL, respectively. The study also reports the fermented extract to have low cytotoxic activity as com- pared to unfermented extracts. References Abraham K, Gürtler R, Berg K, Heinemeyer G, Lampen A, Appel KE Conclusions (2011) Toxicology and risk assessment of 5-Hydroxymethylfurfural in food. Mol Nutr Food Res 55:667–678. doi:10.1002/mnfr. Tyrosinase plays a vital role in the enzymatic browning of 201000564 Arai N, Shiomi K, Takamatsu S, Komiyama K, Shinose M, Takahashi Y, food and depigmentation disorders in humans. Thus, targeting Tanaka Y, Iwai Y, Liu JR, Omura S (1997) Amphistin, a new mela- tyrosinase inhibitors could be the best solution in preventing nogenesis inhibitor, produced by an actinomycete. J Antibiot such problems. Natural product research still has an enormous 50(10):808–814 unexplored potential with microorganisms representing prom- Bajpai VK, Rather IA, Park YH (2016) Partially purified exo- ising sources producing anti-tyrosinase metabolites in high polysaccharide from Lactobacillus sakei Probio 65 with antioxidant, α-glucosidase and tyrosinase inhibitory potential. J Food Biochem yields with feasible extraction methods at a reasonable cost. 40(3):264–274. doi:10.1111/jfbc.12230 Thousands of bacterial metabolites have been reported with Bertolotto C, Abbe P, Hemesath TJ, Bille K, Fisher DE, Ortonne JP, wide application in varied sectors. However, the chemical Ballotti R (1998) Microphthalmia gene product as a signal transduc- diversity in the metabolites produced by microorganisms re- er in cAMP-induced differentiation of melanocytes. J Cell Biol 142: 827–835 mains an unparalleled resource for the discovery of new com- Borges CR, Roberts JC, Wilkins DG, Rollins DE (2001) Relationship of pounds for application in the agriculture, cosmetics, and phar- melanin degradation products to actual melanin content: application maceutical industries. This review, therefore, compiles an up- to human hair. Anal Biochem 290:116–125 dated database of tyrosinase or melanogenesis inhibitors re- Brenner M, Hearing VJ (2008) The protective role of melanin against UV ported from microbial sources. Tyrosinase inhibitors isolated damage in human skin. Photochem Photobiol 84(3):539–549 Burdock GA, Soni MG, Carabin IG (2001) Evaluation of health aspects from natural sources comprise a small group, with the majority of kojic acid in food. Regul Toxicol Pharmacol 33(1):80–101 of the compounds identified from plant sources and marginally Busch JM (1999) Enzymic browning in potatoes: a simple assay for a from microbial sources. Although tyrosinase inhibitors isolated polyphenol oxidase catalysed reaction. Biochem Educ 27:171–173 from plant sources are diverse, belonging to the family of Cabrera-Valladares N, Martínez A, Piñero S, Lagunas-Munoz VH, Tinoco R, De Anda R, Vázquez-Duhalt R, Bolívar F, Gosset G polyphenol, benzaldehyde derivatives, anthraquinones, lipids, Ann Microbiol (2017) 67:343–358 355 (2006) Expression of the melA gene from Rhizobium etli CFN42 in Goldfeder M, Kanteev M, Isaschar-Ovdat S, Adir N, Fishman A (2014) Determination of tyrosinase substrate-binding modes reveals mech- Escherichia coli and characterization of the encoded tyrosinase. Enzym Microb Technol 38:772–779 anistic differences between type-3 copper proteins. Nat Commun 5: Capuano E, Fogliano V (2011) Acrylamide and 5-hydroxymethylfurfural 4505. doi:10.1038/ncomms5505 (HMF): a review on metabolism, toxicity, occurrence in food and Halaouli S, Asther M, Kruus K, Guo L, Hamdi M, Sigoillot JC, Asther M, mitigation strategies. Food Sci Technol 44:793–810 Lomascolo A (2005) Characterization of a new tyrosinase from Cerenius L, Söderhäll K (2004) The prophenoloxidase-activating system Pycnoporus species with high potential for food technological ap- in invertebrates. Immunol Rev 198:116–126 plications. J Appl Microbiol 98:332–343 Chan CF, Huang CC, Lee MY, Lin YS (2014) Fermented broth in tyros- Halaouli S, Asther M, Sigoillot JC, Hamdi M, Lomascolo A (2006) inase and melanogenesis inhibition. Molecules 19:13122–13135 Fungal tyrosinases: new prospects in molecular characteristics, bio- Chang TS (2009) An updated review of tyrosinase inhibitors. Int J Mol engineering and biotechnological applications. J Appl Microbiol Sci 10:2440–2475 100(2):219–232 Chang TS (2012a) Natural melanogenesis inhibitors acting through the Haudecoeur R, Gouron A, Dubois C, Jamet H, Lightbody M, Hardré R, down-regulation of tyrosinase activity. Materials 5:1661–1685 Milet A, Bergantino E, Bubacco L, Belle C, Réglier M, Boumendjel Chang TM (2012b) Tyrosinase and tyrosinase inhibitors. J Biocatal A (2014) Investigation of binding-site homology between mush- Biotransfor 1:2 room and bacterial tyrosinases by using aurones as effectors. Chang CJ, Tsai TY (2016) Antimelanogenic effects of the novel Chembiochem 15(9):1325–1333. doi:10.1002/cbic.201402003 melanogenic inhibitors daidzein and equol, derived from soymilk Hemesath TJ, Price ER, Takemoto C, Badalian T, Fisher DE (1998) MAP fermented with Lactobacillus plantarum strain TWK10, in B16F0 kinase links the transcription factor Microphthalmia to c-Kit signal- mouse melanoma cells. J Funct Foods 22:211–223 ling in melanocytes. Nature 391:298–301 Chang TS, Tseng M (2006) Preliminary screening of soil actinomycetes Hennessy BT, Smith DL, Ram PT, Lu Y, Mills GB (2005) Exploiting the for anti-tyrosinase activity. J Mar Sci Technol 14(3):190–193 PI3K/AKT pathway for cancer drug discovery. Nat Rev Drug Chang TS, Ding HY, Tai SS, Wu CY (2007) Mushroom tyrosinase in- Discov 4:988–1004 hibitory effects of isoflavones isolated from soygerm koji fermented Heo IS, Kim KS, Yang SY, Lee NH, Lim SD (2007) Physiological char- with Aspergillus oryzae BCRC 32288. Food Chem 105:1430–1438 acteristics and tyrosinase inhibitory activity of Lactobacillus Chang TS, Tseng M, Ding HY, Tai SS (2008) Isolation and characteriza- plantarum M23 isolated from raw milk. Korean J Food Sci Anim tion of Streptomyces hiroshimensis strain TI-C3 with anti-tyrosinase Resour 27(4):501–508 activity. J Cosmet Sci 59:33–40 Hernández-Romero D, Solano F, Sanchez-Amat A (2005) Polyphenol Chang CJ, Dai RY, Leu YL, Tsai TY (2015) Effects of the melanogenic oxidase activity expression in Ralstonia solanacearum.Appl inhibitor, uracil, derived from Lactobacillus plantarum TWK10- Environ Microbiol 71(11):6808–6815. doi:10.1128/AEM.71.11. fermented soy milk on anti-melanogenesis in B16F0 mouse mela- 6808-6815.2005 noma cells. J Funct Foods 17:314–327 Hernández-Romero D, Sanchez-Amat A, Solano F (2006) A tyrosinase Chen YM, Shih TW, Chiu CP, Pan TM, Tsai TY (2013) Effects of lactic with an abnormally high tyrosine hydroxylase/dopa oxidase ratio. acid bacteria-fermented soy milk on melanogenesis in B16F0 mela- FEBS J 273:257–270 nocytes. J Funct Foods 5:395–405 Hsu CH, Nguyen AD, Chen YW, Wang SL (2014) Tyrosinase inhibitors Chen CY, Lin LC, Yang WF, Bordon J, Wang HMD (2015) An updated and insecticidal materials produced by Burkholderia cepacia using organic classification of tyrosinase inhibitors on melanin biosynthesis. squid pen as the sole carbon and nitrogen source. Res Chem Curr Org Chem 19:4–18 Intermed 40:2249–2258. doi:10.1007/s11164-014-1602-0 Choudhary MI, Sultan S, Khan MTH, Atta-ur-Rahman (2005) Microbial Huang HC, Chang TM (2012) Antioxidative properties and inhibitory transformation of 17α-ethynyl- and 17α-ethylsteroids, and tyrosinase effect of Bifidobacterium adolescentis on melanogenesis. World J inhibitory activity of transformed products. Steroids 70:798–802 Microbiol Biotechnol 28(9):2903–2912 Claus H, Decker H (2006) Bacterial tyrosinases. Syst Appl Microbiol 29: Ichishima E, Maeba H, Amikura T, Sakata H (1984) Multiple forms of 3–14 pr otyrosinase from Aspergillus oryzae and their mode of activation Dalfard AB, Khajeh K, Soudi MR, Naderi-Manesh H, Ranjbar B, Sajedi at pH 3.0. Biochim Biophys Acta 786:25–31 RH (2006) Isolation and biochemical characterization of laccase and Imada C (2004) Enzyme inhibitors of marine microbial origin with tyrosinase activities in a novel melanogenic soil bacterium. Enzym pharmaceutical importance. Mar Biotechnol 6:193–198 Microb Technol 39:1409–1416 Imada C, Sugimoto Y, Makimura T, Kobayashi T, Hamada N, Watanabe Deering RW, Chen J, Sun J, Ma H, Dubert J, Barja JL, Seeram NP, Wang E (2001) Isolation and characterization of tyrosinase inhibitor- H, Rowley DC (2016) N-acyl dehydrotyrosines, tyrosinase inhibi- producing microorganisms from marine environment. Fish Sci 67: tors from the marine bacterium Thalassotalea sp. PP2-459. J Nat 1151–1156 Prod 79:447–450. doi:10 .1021/acs.jnatprod.5b00972 Ioannou I, Ghoul M (2013) Prevention of enzymatic browning in fruit Fritz WA, Coward L, Wang J, Lamartiniere CA (1998) Dietary genistein: and vegetables. Eur Sci J 9(30):310–341 perinatal mammary cancer prevention, bioavailability and toxicity Ishihara Y, Oka M, Tsunakawa M, Tomita K, Hatori M, Yamamoto testing in the rat. Carcinogenesis 19(12):2151–2158 H, Kamei H, Miyaki T, Konishi M, Oki T (1991) Melanostatin, Fujii Y, Asahara M, Ichinoe M, Nakajima H (2002) Fungal melanin a new melanin synthesis inhibitor. Production, isolation, chem- inhibitor and related compounds from Penicillium decumbens. ical properties, structure and biological activity. J Antibiot Phytochemistry 60(7):703–708 44(1):25–32 García‐Borrón JC, Solano F (2002) Molecular anatomy of tyrosi- Kanda K, Sato T, Ishii S, Enei H, Ejiri S (1996) Purification and proper- nase and its related proteins: beyond the histidine-bound metal ties of tyrosinase isozymes from the gill of Lentinus edodes fruiting catalytic center. Pigment Cell Res 15:162–173 body. Biosci Biotechnol Biochem 60:1273–1278 Goetghebeur M, Kermasha S (1996) Inhibition of polyphenol oxidase by Kang HS, Choi JH, Cho WK, Park JC, Choi JS (2004) A sphingolipid copper-metallothionein from Aspergillus niger.Phytochemistry42: and tyrosinase inhibitors from the fruiting body of Phellinus linteus. 935–940 Arch Pharm Res 27(7):742–750 Gillbro JM, Olsson MJ (2011) The melanogenesis and mechanisms of skin-lightening agents—existing and new approaches. Int J Cosmet Kanteev M, Goldfeder M, Fishman A (2015) Structure–function correla- Sci 33:210–221. doi:10.1111/j.1468-2494.2010.00616.x tions in tyrosinases. Protein Sci 24:1360–1369 356 Ann Microbiol (2017) 67:343–358 Katz E, Thompson CJ, Hopwood DA (1983) Cloning and expression of Li X, Jeong JH, Lee KT, Rho JR, Choi HD, Kang JS, Son BW (2003) Gamma-pyrone derivatives, kojic acid methyl ethers from a marine- the tyrosinase gene from Streptomyces antibioticus in Streptomyces lividans. J Gen Microbiol 129:2703–2714 derived fungus Alternaria sp. Arch Pharm Res 26(7):532–534 Kawagishi H, Somoto A, Kuranari J, Kimura A, Chiba S (1993) A novel Li X, Kim MK, Lee U, Kim SK, Kang JS, Choi HD, Son BW (2005) cyclotetrapeptide produced by Lactobacillus helveticus as a tyrosi- Myrothenones A and B, cyclopentenone derivatives with tyrosinase nase inhibitor. Tetrahedron Lett 34(21):3439–3440 inhibitory activity from the marine-derived fungus Myrothecium sp. Chem Pharm Bull 53(4):453–455 Khan MTH (2007) Molecular design of tyrosinase inhibitors: a critical Liang TW, Lee YC, Wang SL (2015) Tyrosinase inhibitory activity of review of promising novel inhibitors from synthetic origins. Pure supernatant and semi-purified extracts from squid pen fermented Appl Chem 79(12):2277–2295 with Burkholderia cepacia TKU025. Res Chem Intermed 41(9): Kilimnik A, Dembitsky VM (2016) Anti-melanoma agents derived from 6105–6116 fungal species. Mathews J Pharm Sci 1(1):002 Likhitwitayawuid K (2008) Stilbenes with tyrosinase inhibitory activity. Kim YJ, Uyama H (2005) Tyrosinase inhibitors from natural and synthetic Curr Sci 94(1):44–52 sources: structure, inhibition mechanism and perspective for Lim SD, Kim KS (2012) Optimization of tyrosinase inhibitory activity in the future. Cell Mol Life Sci 62:1707–1723 the fermented milk by Lactobacillus plantarum M23. Korean J Kim JP, Kim BK, Yun BS, Ryoo IJ, Lee CH, Lee IK, Kim WG, Lee S, Food Sci Anim Resour 32(5):678–684 Pyun YR, Yoo ID (2003) Melanocins A, B and C, new melanin synthesis inhibitors produced by Eupenicillium shearii I. Lin JW, Chiang HM, Lin YC, Wen KC (2008) Natural products with Taxonomy, fermentation, isolation and biological properties. J skin-whitening effects. J Food Drug Anal 16(2):1–10 Antibiot 56(12):993–999 Liu N, Zhang T, Wang YJ, Huang YP, Ou JH, Shen P (2004) A heat inducible tyrosinase with distinct properties from Bacillus Kim WG, Ryoo IJ, Park SH, Kim DS, Lee S, Park KC, Yoo ID (2005) thuringiensis. Lett Appl Microbiol 39:407–412 Terrein, a melanin biosynthesis inhibitor, from Penicillium sp. 20135. J Microbiol Biotechnol 15(4):891–894 Loizzo MR, Tundis R, Menichini F (2012) Natural and synthetic tyrosi- Kim DS, Cho HJ, Lee HK, Lee WH, Park ES, Youn SW, Park KC (2007) nase inhibitors as antibrowning agents: an update. Compr Rev Food Terrein, a fungal metabolite, inhibits the epidermal proliferation of Sci Food Saf 11:378–398 skin equivalents. J Dermatol Sci 46(1):65–68 Lu Q, Tian M, Liu Y, Yu D (2002) Isolation and structure elucidation of melanin biosynthesis inhibitors H7264 A and B. Zhongguo Kim DS, Lee HK, Park SH, Lee S, Ryoo IJ, Kim WG, Yoo ID, Na JI, Kangshengsu Zazhi 27(7):385–386 Kwon SB, Park KC (2008) Terrein inhibits keratinocyte prolifera- tion via ERK inactivation and G2/M cell cycle arrest. Exp Dermatol Lu R, Liu X, Gao S, Zhang W, Peng F, Hu F, Huang B, Chen L, Bao G, Li 17(4):312–317 C, Li Z (2014) New tyrosinase inhibitors from Paecilomyces gunnii. Kim HR, Kim H, Jung BJ, You GE, Jang S, Chung DK (2015) J Agric Food Chem 62(49):11917–11923. doi:10.1021/jf504128c Lipoteichoic acid isolated from Lactobacillus plantarum inhibits Madhosingh C, Sundberg L (1974) Purification and properties of tyrosi- melanogenesis in B16F10 mouse melanoma cells. Mol Cells nase inhibitor from mushroom. FEBS Lett 49:156–158 38(2):163–170 Matoba Y, Kumagai T, Yamamoto A, Yoshitsu H, Sugiyama M Kobayashi T, Vieira WD, Potterf B, Sakai C, Imokawa G (1995) (2006) Crystallographic evidence that the dinuclear copper cen- Modulation of melanogenic protein expression during the switch ter of tyrosinase is flexible during catalysis. J Biol Chem 281: from eu- to pheomelanogenesis. J Cell Sci 108:2301–2309 8981–8990 Kong KH, Hong MP, Choi SS, Kim YT, Cho SH (2000) Purification and Mayer AM (1987) Polyphenol oxidases in plants—recent progress. characterization of a highly stable tyrosinase from Phytochemistry 26:11–20 Thermomicrobium roseum. Biotechnol Appl Biochem 31(2):113– Mayer AM, Harel E (1979) Polyphenol oxidases in plants. Phytochemistry 118. doi:10.1042/BA19990096 18:193–215 Kuwaki S, Nakajima N, Tanaka H, Ishihara K (2012) Plant-based paste McMahon AM, Doyle EM, Brooks S, O’Connor KE (2007) Biochemical fermented by lactic acid bacteria and yeast: functional analysis and characterisation of the coexisting tyrosinase and laccase in the soil possibility of application to functional foods. Biochem Insights 5: bacterium Pseudomonas putida F6. Enzym Microb Technol 40: 21–29. doi: 10.4137/BCI.S10529 1435–1441 Lamartiniere CA, Wang J, Smith-Johnson M, Eltoum IE (2002) Daidzein: Meinkoth JL, Montminy MR, Fink JS, Feramisco JR (1991) Induction of bioavailability, potential for reproductive toxicity, and breast cancer a cyclic AMP-responsive gene in living cells requires the nuclear chemoprevention in female rats. Toxicol Sci 65:228–238 factor CREB. Mol Cell Biol 11:1759–1764 Lee CH, Chung MC, Lee HJ, Kho YH, Lee KH (1995) MR304-1, a Menon S, Fleck RW, Yong G, Strothkamp KG (1990) Benzoic acid melanin synthesis inhibitor produced by Trichoderma harzianum. inhibition of the α, β,and γ isozymes of Agaricus bisporus tyros- Korean J Appl Microbiol Biotechnol 23(6):641–646 inase. Arch Biochem Biophys 280:27–32 Lee CH, Chung MC, Lee HJ, Bae KS, Kho YH (1997a) MR566A and Michalik J, Emilianowicz-Czerska W, Switalski L, Raczynska- MR566B, new melanin synthesis inhibitors produced by Bojanowska K (1975) Monophenol monooxygenase and Trichoderma harzianum. I. Taxonomy, fermentation, isolation and lincomysin biosynthesis in Streptomyces lincolnensis. Antimicrob biological activities. J Antibiot 50(6):469–473 Agents Chemother 8(5):526–531 Lee CH, Koshino H, Chung MC, Lee HJ, Hong JK, Yoon JS, Kho YH Minosasa J, Matsui K, Uehara H, Tanaka H (1991) Tyrosinase inhibitors (1997b) MR566A and MR566B, new melanin synthesis inhibitors containing neogrifolin. Jpn Kokai Tokkyo Koho, 15 Japanese produced by Trichoderma harzianum. II. Physico-chemical proper- Patent: JP 03109319 A 19910509 Heisei ties and structural elucidation. J Antibiot 50(6):474–478 Misasa H, Matsui Y, Uehara H, Tanaka H, Ishihara M, Shibata H (1992) Lerch K (1981) Copper monooxygenases: tyrosinase and dopamine β- Tyrosinase inhibitors from Albatrellus confluens. Biosci Biotechnol monooxygenase. In: Sigel H (ed) Metal ions in biological systems. Biochem 56(10):1660–1661 Marcel Dekker, New York, pp 143–186 Morimura K, Yamazaki C, Hattori Y, Makabe H, Kamo T, Hirota M (2007) Lerch K (1983) Neurospora tyrosinase: structural, spectroscopic and A tyrosinase inhibitor, Daedalin A, from mycelial culture of Daedalea catalytic properties. Mol Cell Biochem 52:125–138 dickinsii. Biosci Biotechnol Biochem 71(11):2837–2840 Morimura K, Hiramatsu K, Yamazaki C, Hattori Y, Makabe H, Hirota M Lerch K, Ettinger L (1972) Purification and characterization of a tyrosi- nase from Streptomyces glaucescens.Eur JBiochem 31:427–437 (2009) Daedalin A, a metabolite of Daedalea dickinsii, inhibits Ann Microbiol (2017) 67:343–358 357 melanin synthesis in an in vitro human skin model. Biosci Selinheimo E, Nieidhin D, Steffensen C, Nielsen J, Lomascolo A, Halaouli S, Record E, O’Beirne D, Buchert J, Kruus K (2007) Biotechnol Biochem 73(3):627–632. doi:10.1271/bbb.80695 Comparison of the characteristics of fungal and plant tyrosi- Müller WE, Grebenjuk VA, Thakur NL, Thakur AN, Batel R, Krasko A, nases. J Biotechnol 130:471–480 Müller IM, Breter HJ (2004) Oxygen-controlled bacterial growth in the sponge Suberites domuncula: toward a molecular understanding Sharma VK, Choi J, Sharma N, Choi M, Seo SY (2004) In vitro of the symbiotic relationships between sponge and bacteria. Appl anti-tyrosinase activity of 5-(hydroxymethyl)-2-furfural iso- Environ Microbiol 70:2332–2341 lated from Dictyophora indusiata. Phytother Res 18(10): Nakashima T, Anzai K, Kuwahara N, Komaki H, Miyadoh S, Harayama 841–844 S, Tianero MDB, Tanaka J, Kanamoto A, Ando K (2009) Shuster V, Fishman A (2009) Isolation, cloning and characteriza- Physicochemical characters of a tyrosinase inhibitor produced by tion of a tyrosinase with improved activity in organic solvents Streptomyces roseolilacinus NBRC 12815. Biol Pharm Bull 32(5): from Bacillus megaterium. J Mol Microbiol Biotechnol 17: 832–836 188–200 Nambudiri AMD, Bhat JV, Rao PVS (1972) Conversion of p-coumarate Singh P, Langowski HC, Wani AA, Saengerlaub S (2010) Recent ad- into caffeate by Streptomyces nigrifaciens: purification and proper- vances in extending the shelf life of fresh Agaricus mushrooms: a ties of the hydroxylating enzyme. Biochem J 130:425–433 review. J Sci Food Agric 90:1393–1402 Nicolas JJ, Richard-Forget FC, Goupy PM, Amiot MJ, Aubert SY (1994) Solano F, Briganti S, Picardo M, Ghanem G (2006) Hypopigmenting Enzymatic browning reactions in apple and apple products. Crit Rev agents: an updated review on biological, chemical and clinical as- Food Sci Nutr 34:109–157 pects. Pigment Cell Res 19:550–571. doi:10.1111/j.1600-0749. Nohynek GJ, Kirkland D, Marzin D, Toutain H, Leclerc-Ribaud C, Jinnai 2006.00334.x H (2004) An assessment of the genotoxicity and human health risk Solomon EI, Sundaram UM, Machonkin TE (1996) Multicopper oxi- of topical use of kojic acid [5-hydroxy-2-(hydroxymethyl)-4H-py- dases and oxygenases. Chem Rev 96:2563–2605 ran-4-one]. Food Chem Toxicol 42:93–105 Sugumaran M (2002) Comparative biochemistry of Eumelanogenesis Park SH, Kim DS, Kim WG, Ryoo IJ, Lee DH, Huh CH, Youn SW, Yoo and the protective roles of phenoloxidase and melanin in insects. ID, Park KC (2004) Terrein: a new melanogenesis inhibitor and its Pigment Cell Res 15:2–9 mechanism. Cell Mol Life Sci 61:2878–2885 Takahashi S, Iwai H, Kosaka K, Miyazaki T, Osanai Y, Arao N, Tanaka Parvez S, Kang M, Chung HS, Bae H (2007) Naturally occurring tyros- K, Nagai K, Nakagawa A (2007) Byelyankacin: a novel melano- inase inhibitors: mechanism and applications in skin health, cos- genesis inhibitor produced by Enterobacter sp. B20. J Antibiot metics and agriculture industries. Phytother Res 21:805–816 60(11):717–720 Philipp S, Held T, Kutzner HJ (1991) Purification and characterization of Takamatsu S, Rho MC, Hayashi M, Komiyama K, Tanaka H, the tyrosinase of Streptomyces michiganensis DSM 40015. J Basic Omura S, Imokawa G (1993) New inhibitors of melanogenesis, Microbiol 31:293–300 OH-3984 K1 and K2. II. Physico-chemical properties and Pomerantz SH, Murthy VV (1974) Purification and properties of tyrosinases structural elucidation. J Antibiot 46(10):1526–1529 from Vibrio tyrosinaticus. Arch Biochem Biophys 160(1):73–82 Takamatsu S, Kim YP, Hayashi M, Komiyama K, Imokawa G, Omura S Raistrick H, Smith G (1935) Studies in the biochemistry of micro-organ- (1996) A new inhibitor of melanogenesis, Albocycline K3, pro- isms: the metabolic products of Aspergillus terreus Thom. A new duced by Streptomyces sp. OH-3984. J Antibiot 49(5):485–486 mould metabolic product—terrein. Biochem J 29(3):606–611 Tanaka N, Naganuma M, Fukuda M, Wati Y, Komatsu K, Yoshida S, Raper HS (1928) The anaerobic oxidases. Physiol Rev 8:245–282 Komiyama K, Omura S (1996) Novel inhibitor of melanogenesis Razak DLA, Rashid NYA, Jamaluddin A, Sharifudin SA, Kahar AA, produced by Talaromyces FO-3182. Nippon Koshohin Kagakkaishi Long K (2015) Cosmeceutical potentials and bioactive compounds 20(1):3–6 of rice bran fermented with single and mix culture of Aspergillus Töpert M, Rach P, Siegmund F (1989) Pharmacology and toxicology of oryzae and Rhizopus oryzae. J Saudi Soc Agric Sci. doi:10.1016/j. azelaic acid. Acta Derm Venereol Suppl 143:14–19 jssas.2015.04.001 TsaiCC,Chan CF,Huang WY,Lin JS,ChanP,Liu HY,Lin YS(2013) Robb DA (1984) Tyrosinase. In: Lontie R (ed) Copper proteins and cop- Applications of Lactobacillus rhamnosus spent culture supernatant in per enzymes, vol 2. CRC Press, Boca Raton, pp 207–241 cosmetic antioxidation, whitening and moisture retention applications. Ruan L, He W, He J, Sun M, Yu Z (2005) Cloning and expression of mel Molecules 18:14161–14171. doi:10.3390/molecules181114161 gene from Bacillus thuringiensis in Escherichia coli. Antonie van Tsuchiya T, Yamada K, Minoura K, Miyamoto K, Usami Y, Kobayashi T, Leeuwenhoek 87:283–288 Hamada-Sato N, Imada C, Tsujibo H (2008) Purification and deter- Sánchez-Ferrer Á, Rodríguez-López JN, García-Cánovas F, García- mination of the chemical structure of the tyrosinase inhibitor pro- Carmona F (1995) Tyrosinase: a comprehensive review of its mech- duced by Trichoderma viride strain H1-7 from a marine environ- anism. Biochim Biophys Acta 1247:1–11 ment. Biol Pharm Bull 31(8):1618–1620 Saruno R, Kato F, Ikeno T (1979) Kojic acid, a tyrosinase inhibitor from Umezawa H (1972) Enzyme inhibitors of microbial origin. University of Aspergillus albus. Agric Biol Chem 43(6):1337–1338 Tokyo Press, Tokyo, Japan Schaffer JV, Bolognia JL (2001) The melanocortin-1 receptor: red hair Van Gelder CW, Flurkey WH, Wichers HJ (1997) Sequence and struc- and beyond. Arch Dermatol 137:1477–1485 tural features of plant and fungal tyrosinases. Phytochemistry 45: Schallreuter KU, Wood JW (1990) A possible mechanism of action for 1309–1323 azelaic acid in the human epidermis. Arch Dermatol Res 282:168–171 Vasantha KY, Murugesh CS, Sattur AP (2014) A tyrosinase in- Schurink M, van Berkel WJH, Wichers HJ, Boeriu CG (2007) Novel hibitor from Aspergillus niger. J Food Sci Technol 51(10): peptides with tyrosinase inhibitory activity. Peptides 28:485–495 2877–2880 Seiberg M, Paine C, Sharlow E, Eisinger M, Shapiro SS, Andrade- Walker JRL, McCallion RF (1980) The selective inhibition of ortho- and Gordon P, Costanzo M (2000) Inhibition of melanosome transfer para-diphenol oxidases. Phytochemistry 19:373–377 resultsinskinlightening. J Invest Dermatol115:162–167 Wang GH, Chen CY, Lin CP, Huang CL, Lin CH, Cheng CY, Chung YC Selinheimo E, Saloheimo M, Ahola E, Westerholm-Parvinen A, (2016) Tyrosinase inhibitory and antioxidant activities of three Kalkkinen N, Buchert J, Kruus K (2006) Production and character- Bifidobacterium bifidum-fermented herb extracts. Ind Crop Prod ization of a secreted, C-terminally processed tyrosinase from the 89:376–382 filamentous fungus Trichoderma reesei. FEBS J 273:4322–4335 358 Ann Microbiol (2017) 67:343–358 Wei CI, Huang TS, Chen JS, Marshall MR, Chung KT (1991) Production Zhang D, Li X, Kang JS, Choi HD, Son BW (2007) A new a-pyrone derivative, 6-[(E)-hept-1-enyl]-a-pyrone, with tyrosinase inhibitory of kojic acid by Aspergillus candidus in three culture media. J Food Prot 54(7):546–548 activity from a marine isolate of the fungus Botrytis. Bull Kor Chem Wu B, Wu X, Sun M, Li M (2013) Two novel tyrosinase inhibitory Soc 28(5):887–888 sesquiterpenes induced by CuCl from a marine-derived fungus Zheng ZP, Cheng KW, Chao J, Wu J, Wang M (2008) Tyrosinase inhib- Pestalotiopsis sp. Z233. Mar Drugs 11:2713–2721 itors from paper mulberry (Broussonetia papyrifera). Food Chem Xu W, Gong L, Haddad MM, Bischof O, Campisi J, Yeh ET, Medrano EE 106:529–535 (2000) Regulation of microphthalmia-associated transcription factor Zhuravleva OI, Afiyatullov SS, Vishchuk OS, Denisenko VA, MITF protein levels by association with the ubiquitin-conjugating Slinkina NN, Smetanina OF (2012) Decumbenone C, a new enzyme hUBC9. Exp Cell Res 255:135–143 cytotoxic decaline derivative from the marine fungus Yoshida H, Tanaka Y, Nakayama K (1974) Properties of tyrosinase from Aspergillus sulphureus KMM 4640. Arch Pharm Res 35(10): Pseudomonas melanogenum. Agric Biol Chem 38(3):627–632 1757–1762 Yoshimoto T, Yamamoto K, Tsuru D (1985) Extracellular tyrosinase from Streptomyces sp. KY-453: purification and some enzymatic proper- ties. J Biochem 97(6):1747–1754
Annals of Microbiology – Springer Journals
Published: Mar 12, 2017
Access the full text.
Sign up today, get DeepDyve free for 14 days.