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/lp/springer-journals/biomacromolecular-localization-in-bacterial-cells-by-the-diffusion-and-L6bl6tH0YQ
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- Springer Journals
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- Copyright © 2012 by Springer-Verlag Berlin Heidelberg and the University of Milan
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- Life Sciences; Microbiology; Microbial Genetics and Genomics; Microbial Ecology; Fungus Genetics; Medical Microbiology; Applied Microbiology
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- 1590-4261
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- 1869-2044
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- 10.1007/s13213-012-0596-3
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Abstract
Ann Microbiol (2013) 63:825–832 DOI 10.1007/s13213-012-0596-3 REVIEW ARTICLE Biomacromolecular localization in bacterial cells by the diffusion and capture mechanism Miguel Angel Pérez Rodriguez & Xianwu Guo Received: 7 June 2012 /Accepted: 17 December 2012 /Published online: 6 January 2013 Springer-Verlag Berlin Heidelberg and the University of Milan 2013 Abstract Subcellular localization of biomacromolecules Emanuelsson et al. 2007;Ramamurthi etal. 2009). The (nucleotides and proteins) is the base for their proper func- proteins contain some parts in the polypeptide chain which tion in bacterial cells. One model to explain the localization allow the transferring of the proteins themselves outside the of biomacromolecules, particularly proteins, is “diffusion cell or to other intracellular membranes, locations, or com- and capture”. In this model, proteins are localized by diffu- partments. This part of the peptide sequence that directs the sion through the cytoplasm or the membrane until binding to protein to a specific intracellular location is called the signal another protein or proteins that were already previously peptide (Blobel 1980). The peptide secretion signals are the sequestered in cells. The use of fusions with fluorescent best documented: they target the protein for translocation proteins to follow the fate of biomacromolecules has given across the plasma membrane in prokaryotes or across the new insight into the molecular localization mechanisms in endoplasmic reticulum (ER) membrane in eukaryotes (von living cells. Here, several proteins following a diffusion and Heijne 1990; Emanuelsson et al. 2007). One example of capture mechanism to reach their proper location in the cells peptide secretion signals is from the protein AphA in E. coli. are presented. Some RNAs also seem to localize by this The first 25 residues of AphA (237 amino acids) after mechanism. It is an intrinsic feature that the information for translation were cleaved and deleted after export, resulting molecular localization should exist in the sequences of in a 212-residue chain (Calderone et al. 2004). Commonly, protein itself. However, very little information has been the peptide secretion signals have 15–30 amino acids that available in this field to date. are cleaved off during translocation of the protein across the membrane (Emanuelsson et al. 2007). . . . Keywords Diffusion Capture Localization Protein It is clear that eukaryotic cells have sorting protein mech- anisms based on vesicles, and the cytoskeleton releases the protein to the correct location (Shapiro et al. 2009). However, such vesicles-based mechanisms to locate the Introduction protein do not exist in some bacteria or are at least not common as they work in eukaryotic cells. How to localize The essential activities for cellular life are principally real- the proteins in bacterial cells is a central topic in bacterial ized by proteins which are located at specific sites in cell.s cell biology. Several models have been put forward to The feature of protein localization is thus the pedestal of explain the subcellular localization (Collier and Shapiro protein functions (Blobel 1980; Chou and Shen 2007; 2007; Thanbichler and Shapiro 2008). In the targeted inser- tion model, a protein is directly and selectively inserted into M. A. Pérez Rodriguez Centro de Investigacion en Ciencia Aplicada y Tecnología the site where it is required. In the selective degradation Avanzada, Instituto Politécnico Nacional, Unidad Altamira, model, the proteins randomly insert into all membranes or Tamaulipas, Mexico stay in the cytoplasm, and then follow with proteolytic elimination except in the proper destination. In the diffusion M. A. Pérez Rodriguez X. Guo (*) Centro de Biotecnología Genómica, Instituto Politécnico Nacional, and capture model, the proteins also randomly insert into all Boulevard del Maestro membranes or into cytoplasm, reach their proper localiza- S/N esq. Elías Piña, Col. Narciso Mendoza, tion by diffusion, and are then captured at the site where C.P. 88710, Cd. Reynosa, Tamaulipas, Mexico they ultimately reside (Rudner et al. 2002; Deich et al. 2004; e-mail: xguo@ipn.mx 826 Ann Microbiol (2013) 63:825–832 Thanbichler and Shapiro 2008; Shapiro et al. 2009; Komeili et al. 2002; Mignot and Shaevitz 2008). In the absence of 2012). We focus on the mechanism of diffusion and capture SpoIVFA, SpoIVFB was mislocalized at all membranes because diffusion is the main way for intracellular move- within the mother cell while SpoIVFA localized properly ment (Elowitz et al. 1999; Mika and Poolman 2011) and the in the absence of SpoIVFB (Rudner and Losick 2002). The proteins produced in the cytoplasm reach their proper local- selective degradation model cannot explain this phenome- ization mainly via diffusion and capture (Rudner et al. 2002; non because the incorrectly localized protein, SpoIVFB, did Shapiro et al. 2002; Deich et al. 2004; Bowman et al. 2008; not show degradation. SpoIVFA is not responsible for the Mignot and Shaevitz 2008; Shapiro et al. 2009; Hughes et degradation of SpoIVFB because SpoIVFA is restricted to al. 2010; Loose et al. 2011). This model has been confirmed the engulfing forespore membrane where the fluorescent in several organisms (Table 1). signal of SpoIVFB-GFP was shown (Rudner et al. 2002). The fate of SpoIVFB produced after completion of en- gulfment was tracked to test whether the location of SpoIVFB was realized by means of targeted insertion. If Localization of proteins in the sporulation targeted insertion occurs, the SpoIVFB molecules should be only localized at the outer forespore membrane. However, in A good model to study subcellular localization has been provided by Bacillus subtilis sporulation, during which most cases, SpoIVFB was present exclusively in the cyto- plasmic membrane of the mother cell. and in some cases many membrane proteins localize to the polar septum where they participate in morphogenesis and signal transduction. was observed in both the cytoplasmic membrane of the mother cell and the outer forespore membranes. This result The formation of the polar septum results in the occurrence of two cells, the forespore and the mother cell. The fore- is compatible with the diffusion and capture model. It is spore is later engulfed by the mother cell. During engulf- present in the cytoplasmic membrane of the mother cell and the outer forespore membranes before specific localization ment, two topologically distinct membranes are present in the mother cell: the cytoplasmic membrane, and the outer on the outer forespore membranes (Fig. 1) (Rudner et al. 2002). forespore membrane, which is the membrane originating from the mother cell membrane and surrounding the fore- The localization of two other proteins, SpoIIE and SpoIIIAH, showed a similar pattern. Their distribution spore (Stragier and Losick 1996). The outer forespore membrane contains many specific depends on the presence of another protein, SpoIIQ, during sporulation (Rubio and Pogliano 2004). SpoIIE co-localizes proteins, one of which is SpoIVFB, a proprotein processing enzyme, which is involved in the activation of a transcrip- with FtsZ at the polar septum in the early stages of sporu- lation (Ben-Yehuda and Losick 2002). SpoIIE-GFP fusion tion factor at a late stage of development (Yu and Kroos showed that it was released into the membranes of the 2000; Rudner et al. 2002). The mother cell synthesizes SpoIVFB during the engulfment (Cutting et al. 1991). It forespore, but when σ is activated, SpoIIE-GFP was relo- calized to the septal membrane in a SpoIIQ-dependent man- has been observed that SpoIVFB exhibited a high specific subcellular localization by using a functional fusion of ner, indicating that the re-location of SpoIIE to the engulfing septal membrane did not result from the selective degrada- SpoIVFB to the green fluorescent protein (GFP). The SpoIVFB-GFP was consistently in the outer forespore mem- tion but from diffusion (Campo et al. 2008). SpoIIIAH is initially randomly distributed in the mother cell cytoplasmic brane. However, the correct localization of SpoIVFB depends on another membrane protein, SpoIVFA (Shapiro membrane (Rubio and Pogliano 2004), and then reaches the Table 1 The proteins from different bacterial species that showed the pattern of diffusion and capture Organism Protein Function References Caulobacter crescentus DivJ Membrane-bound histidine kinase Lin et al. 2010 Bacillus subtilis ComGA During transformability, mediate the uptake DNA at the cell Hahn et al. 2009 poles and their recombination Streptomyces coelicolor SffA FtsK-family ATPase in sporulation septa Flardh and Buttner 2009 Vibrio cholerae ParC Partitioning chemotaxis, promotes the efficiency of Ringgaard et al. 2011 chemotactic signaling Escherichia coli MurG Mediates the last step in peptidoglycan subunit biosynthesis Michaelis and Gitai 2010 Bacillus subtilis RacA Drive oriC movement to the cell pole during sporulation Errington 2010; Ben-Yehuda et al. 2003 Bacillus subtilis BofA Membrane protein, stabilizes SpoIVFA Shapiro et al. 2009; Yu and Kroos 2000 Ann Microbiol (2013) 63:825–832 827 Fig. 1 The diffusion and capture model for the sporulation protein freely through the cytoplasmic membrane, c capture by interaction SpoIVFB in Bacillus subtilis. a SpoIVFB is produced and diffused to with SpoIVFA in the septal membrane, d spore engulfment the cytoplasmic membrane during sporulation, b SpoIVFB diffuses sporulation septum by diffusion from the cytoplasmic mem- segregation and cytokinesis. In particular, the ParB protein brane and is targeted by SpoIIQ, via the interaction of binds to newly replicated sequences adjacent to the origin of extracytoplasmic domains of SpoIIQ. It is a stage of the replication, forming the ori/ParB complex, which travels zipper-like interaction, by which more proteins can be across the cell and is localized in the cell pole (Figge et al. recruited to the septum (Blaylock et al. 2004; Thanbichler 2003). and Shapiro 2008). SpoIIIAH is in turn required for the The proline-rich polar protein PopZ was fused to the localization of SpoIVFA (Doan et al. 2005). yellow fluorescent protein for observation in vivo (Bowman et al. 2008). The PopZ-YFP individual molecules diffuse randomly through the cytoplasm and, subsequently, bind directly to the ori/ParB complex to be localized at the Localization of PleC cell pole. In vitro, PopZ showed self-assembly of a network of filaments, forming an adhesive network for the ori/ParB In Caulobacter crescentus, the cell division produces motile complex. These results suggest that there was no direct swarmer cells (SW) with a single flagellum located at a transport or targeted insertion (Bowman et al. 2008). On specific pole, and stalked cells (ST), which have an adhesive the other hand, it has been reported that the actin-like MreB holdfast at the end of the stalk. The membrane histidine protein affected PopZ to be localized in the cell pole (Gitai kinase, PleC, is the regulator for the formation of polar et al. 2005), however, many aspects of such MreB partici- organelles, cell motility and asymmetric cell division pation remains unclear. (Burton et al. 1997; Viollier et al. 2002). The cells with mutations in PleC did not form stalks or pili, but showed symmetric cell division and paralyzed flagella (Ohta et al. 1992). The movement of PleC was tracked in living Localization of StpX Caulobacter cells by expressing PleC labeled with the en- hanced yellow fluorescent protein (PleC-EYFP) with the The stalk in C. crescentus is a polar surface organelle as a help of time-lapse imaging (Deich et al. 2004). PleC- cylindrical protrusion of all envelope layers, lacking the chro- EYFP was present in two forms: dimer, localized at the pole mosomal DNA and the ribosomes (Ireland et al. 2002). The of ST and SW cells, and individual, free molecules of PleC- absence of ribosomes in the stalk has provided an interesting EYFP moving throughout the cell. The existence of the free model for studying how proteins are localized, because it molecule form and localized dimers argues against an active eliminates the possibility of a co-translational protein targeting transport mechanism but supports the diffusion and capture mechanism within the stalk (Hughes et al. 2010). mechanism for the polar localization of PleC-EYFP (Deich The StpX is a bitopic membrane protein that modulates et al. 2004). the stalk elongation and is sequestered to the stalk (Hughes et al. 2010). StpX was found by generating libraries of C. crescentus with translational fusions with the GFP gene to Localization of PopZ genomic sequences at random positions. A strain was obtained that expressed the GFP fusion in the stalk com- In C. crescentus, the segregation of newly replicated chro- partment. In stalkless cells, StpX-GFP is dispersed through- mosomes to proper positions in the new daughter cells is a out the cell body and in the steady state; the levels of StpX- highly ordered event. In the C. crescentus chromosomes, the GFP are comparable to wild-type. In long stalk strains, origin of replication and the ParS sequences are localized StpX-GFP was scattered throughout the stalk. Within the specifically in the cell pole (Fogel and Waldor 2006). ParA stalk, immobile StpX was distinguished near the stalk base and ParB are essential proteins involved in chromosome and mobile StpX near the stalk tip. Because stalks lack 828 Ann Microbiol (2013) 63:825–832 ribosomes, StpX might be translated outside the stalk and bacterial counterparts: the tubulin-like protein FtsZ, the then diffuse into the stalk as mobile StpX protein molecules, actin-like protein MreB, and the intermediate filament-like where they are subsequently retained (Fig. 2). Continued protein Crescentin, which also play a key role in determin- insertion of StpX during the stalk elongation results in stalk- ing the cell morphogenesis (or regulation of cell shape). specific localization of StpX (Hughes et al. 2010). However, These proteins can be located as polymeric assemblies in- it is interesting that the inhibition of MreB can stop the stalk side the cell. Those polymeric assemblies or filaments are elongation, resulting in stalkless cells, which suggests a role formed by diffusion and capture (Rudner and Losick 2010). of MreB in the StpX localization at the stalk (Wagner et al. With single-molecule tracking by photoactivatable fluores- 2005). Therefore, it is still not able to negate the possibility cent protein, we investigated the mobility of intracellular of active transportation in this process. FtsZ protein molecules in living E. coli cells. The dynamics of distinct diffusions of FtsZ was observed. Some FtsZ molecules stayed near the center of StpX– Localization of DivIVA GFPcell (forming the Z ring) and the rest showed a random movement present in the whole cell. The FtsZ The division septa and the poles are the most negatively out of the Z ring formed a weaker periodical filamen- curved regions within the cell. DivIVA is localized in the tous helical structure underneath the membrane (Niu and membranes that are negatively curved at the cell poles and Yu 2008;Vatsetal. 2009). Similarly, Kim et al. (2006) to cell division sites (Cha and Stewart 1997; Lenarcic et al. tracked the MreB protein that was fused to the fluores- 2009), forming complexes with the DNA, and recruits the cent yellow protein. It was found that a group of mol- cell division inhibitors, MinC and MinD, to give rise to a ecules formed MreB filaments and another group did gradient directed toward the midcell for inhibiting cell divi- not show polymerization (MreB monomers). The mole- sion near the poles (Patrick and Kearns 2008). The assembly cule of unpolymerized MreB has fast diffusion random- of MinCD proteins with DivIVA in B. subtilis was recently ly, whereas the molecules of polymerized MreB confirmed in vivo (Eswaramoorthy et al. 2011). The DivIVA filaments showed very slow movement and exhibited protein is also required to anchor the chromosome origin to treadmilling directed behavior. the cell pole during B. subtilis sporulation (Ben-Yehuda et al. 2003; Bowman et al. 2008). The DivIVa protein recruits MinJ, and these two proteins The Z-ring assembly colocalize in a double ring flanking the division septum. The recruitment of MinJ and MinCD by DivIVA keeps them Z ring occurs during bacterial cell division, which is com- away from its target FtsZ (Eswaramoorthy et al. 2011). posed of the tubulin-like FtsZ protein that polymerizes Therefore, DivIVA can be regarded as the spatial regulator under the membrane at the middle of cell with the help of other division proteins such as FtsA, ZipA, and ZapA (Bi of cell division in B. subtilis, which spatially and temporally regulated the Min system activity. DivIVA diffuses through and Lutkenhaus 1991;Ueharaet al. 2010). The Z ring the cytoplasm and specifically binds to the cell poles to form shrinks to begin the process of division (Bi and a DivIVa ring (Lenarcic et al. 2009; Ramamurthi and Losick Lutkenhaus 1991). The division proteins bind to the Z ring 2009; Loose et al. 2011), which collapses in the rounded in a specific ordered sequence, each of which diffuses freely poles from the new separate daughter cells after cell division until it finds and adheres to the Z-ring, or binds to another (Eswaramoorthy et al. 2011). protein that has already assembled into the divisome (Rudner and Losick 2010), finally forming a protein com- plex consisting of 14 proteins: FtsZ, FtsA, and ZapA in Localization of cytoskeletal elements cytoplasm; ZipA, FtsE, FtsX, FtsK, FtsQ, FtsL, FtsB, FtsW, FtsI, and FtsN at the inner membrane, and AmiC in In the eukaryotic world, cytoskeletal proteins are tubulin, the periplasmic region (Scheffers et al. 2007; Rudner and actin, and intermediate filament; these proteins have Losick 2010) (Fig. 3). Fig. 2 The diffusion and capture model for a stalk-specific protein in Caulobacter crescentus. a StpX translation and random insertion in the cytoplasmic membrane, b random insertion in the cytoplasmic membrane, c capture in the free-of-ribosomes stalk Ann Microbiol (2013) 63:825–832 829 Fig. 3 Sketch to describe the cellular localization of the proteins in the assembly of divisome in E. coli. The Z ring is attached to the cytoplasmic membrane by FtsA and ZipA. ZapA aids the Z ring assembly. The proteins are captured at divisome in a linear hierarchical manner, where the assembly of each protein requires the presence of another specific protein at the position The Z ring is a structure fixed to the cell membrane; for the cell division or to no FtsZ ring formed (Hale and de however, ftsZ filaments showed no affinity with the mem- Boer 1997; Liu et al. 1999; Pichoff and Lutkenhaus 2002). brane. The Z ring stabilization is achieved by the FtsA and The proteins FtsA and ZipA bind to the extreme carboxy- ZipA proteins (Hale and de Boer 1997; van den Ent and terminal tail domains of FtsZ (Liu et al. 1999; Haney et al. Lowe 2000; Pichoff and Lutkenhaus 2007), which anchor 2001; Pichoff and Lutkenhaus 2007). In E. coli, the FtsA the FtsZ filaments to the cell membrane. The absence of protein has a conserved C-terminal domain, which forms an FtsA or ZipA leads to the formation of nonfunctional rings amphipathic motif helix called the membrane targeting Fig. 4 Tracking of mRNAs in E. coli. One vector carrying MS2/GFP fusion and other carrying a reporter mRNA containing tandemly repeated MS2-binding sites, after coex- pression the GFP-fusion protein binds to the RNA, forming bright fluorescent particles 830 Ann Microbiol (2013) 63:825–832 sequence (MTS) (Pichoff and Lutkenhaus 2005). The MTS bacterial cells, which, at least, depends on two conditions: is required to anchor FtsA to the membrane, which conse- first, the specific characteristics for an intracellular location quently helps the Z ring to attach to the membrane. The Z is unique in the whole cell, which contains specific proteins ring generates force to contract the cell envelope and divides or a specific secretion apparatus (Alley et al. 1992), and the cell (Errington et al. 2003; Anderson et al. 2004; Pichoff second, the signal peptide is present in the protein amino and Lutkenhaus 2005; Li et al. 2007; Osawa et al. 2008), acid sequence which directs the protein itself to a specific without the participation of other proteins (Osawa et al. location (Emanuelsson et al. 2007; Ramamurthi 2011). It 2008). means that this intrinsic feature is composed of a specific amino acid sequence within the protein that allows binding in the correct subcellular localization through its recognition mRNA localization by the proteins or the protein complex. Therefore, the local- ization information should exist in the sequences of the In bacteria, the mRNAs are generally translated into proteins protein itself. The specific regions for the determination of at the same time or a short time after the transcription. the localization have been identified for a few proteins. However, the tracking of some mRNA molecules in E. coli Much more information is needed to elucidate the complete showed free diffusion through the cytoplasm until they protein functions. reached a specific localization (Golding and Cox 2004). Nevo-Dinur et al. (2011) recently reported that some Acknowledgment This work was supported by Secretaría de Inves- mRNA is specific to the subcellular location where the tigación y Posgrado del Instituto Politécnico Nacional, México. corresponding protein will occupy in E. coli. By tracking (http://www.sip.ipn.mx/WPS/WCM/CONNECT/SIP/SIP/INICIO/ INDEX.HTM) (Grant numbers: 20080390 and 20091288) and by the some mRNAs of interest, their genes were fused to a spe- Consejo Nacional de Ciencia y Tecnología-México (Convocatoria de cific nucleotide sequence, which was recognized by a RNA- Ciencias Básica 2011, grant number: 168541). The authors have de- binding protein fused to a green fluorescent protein so that clared that no competing interests exist. Xianwu Guo holds a scholar- the labeling is not translation-dependent (Fig. 4). Their ship from Comisión de Operación y Fomento de Actividades Académicas/Instituto Politécnico Nacional. observations indicate that the non-translation-dependent la- beling sequence gives the mRNA ability to migrate to a particular region in the cell (Nevo-Dinur et al. 2011). To determine the mRNA element that targets the transcripts to the membrane, truncated mRNA was also fused, encoding References the hydrophilic or the hydrophobic domain (B and C domains), respectively. Only the part encoding the mem- Alley MR, Maddock JR et al (1992) Polar localization of a bacterial brane C domain were detected at the membrane, suggesting chemoreceptor. Genes Dev 6(5):825–836 that the cis regulatory sequences within the coding sequence Anderson DE, Gueiros-Filho FJ et al (2004) Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of of protein membranes lead the mRNA to the membrane FtsZ-regulating proteins. 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Journal
Annals of Microbiology – Springer Journals
Published: Jan 6, 2013