Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Modern tools applied to classic structures: Approaches for mammalian male germ cell RNA granule research

Modern tools applied to classic structures: Approaches for mammalian male germ cell RNA granule... INTRODUCTIONGerm cell RNA granules are cytoplasmic regions, RNA‐rich and nonmembrane bound, found in germ cells across a wide range of phyla from Caenorhabditis elegans and Drosophila to mammals including mice, rats, and humans. These granules appear to be sites of crucial and complex RNA biology including small RNA processing,1 mRNA storage,2 and translation regulation.3,4 Granules are essential structures for successful spermatogenesis as loss of key granule components has catastrophic results for germ cell development and the organism's fertility.5–8 Given their importance, there has been great interest in defining the components and functions of germ cell granules, particularly in mammals.Though first observed via light microscopy as early as the late 19th century,9 a full account of germ cell granules in mammalian spermatocytes was not be conducted until nearly a century later. In 1964, Gardner employed electron microscopy (EM) to assess the seminiferous tubules of the mouse and briefly discussed the chromatoid body (CB) in spermatids.10 In 1978, six distinct granules, referred therein as “nuage,” were defined in the rat testis via EM.11 Five of these were observed primarily in spermatocytes and one, the CB, in spermatids.11 Over the subsequent decades, the field has utilized myriad models and methodologies to further http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Andrology Wiley

Modern tools applied to classic structures: Approaches for mammalian male germ cell RNA granule research

Chukrallah, Lauren G.; Snyder, Elizabeth M.
Andrology , Volume 11 (5) – Jul 1, 2023
Download PDF
12 pages

Loading next page...
 
/lp/wiley/modern-tools-applied-to-classic-structures-approaches-for-mammalian-g76xwSRrbu
Publisher
Wiley
Copyright
© 2023 American Society of Andrology and European Academy of Andrology.
ISSN
2047-2919
eISSN
2047-2927
DOI
10.1111/andr.13320
Publisher site
See Article on Publisher Site

Abstract

INTRODUCTIONGerm cell RNA granules are cytoplasmic regions, RNA‐rich and nonmembrane bound, found in germ cells across a wide range of phyla from Caenorhabditis elegans and Drosophila to mammals including mice, rats, and humans. These granules appear to be sites of crucial and complex RNA biology including small RNA processing,1 mRNA storage,2 and translation regulation.3,4 Granules are essential structures for successful spermatogenesis as loss of key granule components has catastrophic results for germ cell development and the organism's fertility.5–8 Given their importance, there has been great interest in defining the components and functions of germ cell granules, particularly in mammals.Though first observed via light microscopy as early as the late 19th century,9 a full account of germ cell granules in mammalian spermatocytes was not be conducted until nearly a century later. In 1964, Gardner employed electron microscopy (EM) to assess the seminiferous tubules of the mouse and briefly discussed the chromatoid body (CB) in spermatids.10 In 1978, six distinct granules, referred therein as “nuage,” were defined in the rat testis via EM.11 Five of these were observed primarily in spermatocytes and one, the CB, in spermatids.11 Over the subsequent decades, the field has utilized myriad models and methodologies to further

Journal

Andrology – Wiley

Published: Jul 1, 2023

Keywords: granules; male; mammalian; nuage; RNA; spermatocytes

References

  • Cytoplasmic compartmentalization of the fetal piRNA pathway in mice
    Aravin, AA; Heijden, GW; Castaneda, J; Vagin, VV; Hannon, GJ; Bortvin, A
  • The chromatoid body in spermatogenesis
    Parvinen, M
  • Germ cell ribonucleoprotein granules in different clades of life: from insects to mammals
    Mukherjee, N; Mukherjee, C
  • Transcriptional silencing and translational control: key features of early germline development
    Leatherman, JL; Jongens, TA
  • Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression
    Vasileva, A; Tiedau, D; Firooznia, A; Muller‐Reichert, T; Jessberger, R
  • MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline
    Watanabe, T; Chuma, S; Yamamoto, Y
  • Tdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germline
    Saxe, JP; Chen, M; Zhao, H; Lin, H
  • RNF17, a component of the mammalian germ cell nuage, is essential for spermiogenesis
    Pan, J; Goodheart, M; Chuma, S; Nakatsuji, N; Page, D; Wang, P
  • Die betheiligung von centralkörper und sphäre am aufbau des samenfadens bei säugethieren
    Niessing, C
  • Fine structure of the seminiferous tubule of the Swiss mouse. The spermatid
    Gardiner, P
  • Ultrastructural characterization of nuage in spermatocytes of the rat
    Russell, L; Frank, B
  • An atlas of chromatoid body components
    Meikar, O; Vagin, VV; Chalmel, F
  • Historical survey on chromatoid body research
    Yokota, S
  • Perspectives on mammalian chromatoid body research
    Peruquetti, RL
  • Beiträge zur entwicklungsgeschichte der samenkörper
    Brunn, A
  • Neue mittheilungen über die entwickelung der genitadrüsen und über die metamorphose der samenzellen (histogenese der spermatozoen)
    Benda, C
  • Studies on the fine structure of the mammalian testis
    Burgos, M; Fawcett, D
  • The ‘chromatoid body’ in spermatogenesis
    Sud, B
  • The development and morphology of the gonads of the mouse.–IV. The post‐natal growth of the testis
    Rowlands, I; Rogers Brambell, F
  • Distribution of nucleic acids in germ cells during the cycle of the seminiferous epithelium in the rat
    Daoust, R; Clermont, Y
  • Morphological and histochemical studies of the chromatoid body and related elements in the spermatogenesis of the rat
    Sud, B
  • High‐resolution electron microscopy, 4th ed., John C.H. Spence, Oxford University Press, Oxford, UK; 2013, Hardcover, 432 pp., ISBN: 978‐0‐19‐966863‐2; 3rd ed., John C.H. Spence, Oxford University Press, 2009, Paperback, 401 pp., ISBN: 978‐0‐19‐955275‐7
    Zuo, J‐M
  • Transmission electron microscopy, diffraction, imaging, and spectroscopy
    Carter, HPCB; Williams, DB
  • Transmission electron microscopy; diffraction, imaging, and spectrometry. C. Barry Carter and David B. Williams (eds.). Springer International Publishing, Switzerland 2016, 518 pp. ISBN: 978‐3‐3‐319‐26649‐7
    Bell, DC
  • Biological field emission scanning electron microscopy. Roland A. Fleck and Bruno M. Humbel (eds.), Wiley, Hoboken, NJ, 2019. 752 pp. ISBN: 1118654064
    Qvortrup, K
  • Molecular Biology of the Cell
    Alberts, B; Johnson, A; Lewis, J
  • Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis
    Fawcett, D; Eddy, E; Phillips, D
  • Expression of MAEL in nuage and non‐nuage compartments of rat spermatogenic cells and colocalization with DDX4, DDX25 and MIWI
    Takebe, M; Onohara, Y; Yokota, S
  • Localization of mouse vasa homolog protein in chromatoid body and related nuage structures of mammalian spermatogenic cells during spermatogenesis
    Onohara, Y; Fujiwara, T; Yasukochi, T; Himeno, M; Yokota, S
  • Chromatoid body and small RNAs in male germ cells
    Meikar, O; Da Ros, M; Korhonen, H; Kotaja, N
  • Nuage proteins: their localization in subcellular structures of spermatogenic cells as revealed by immunoelectron microscopy
    Yokota, S
  • The structure of the eukaryotic ribosome at 3.0 Å resolution
    Ben‐Shem, A; Loubress, G; Melnikov, S; Jenner, L; Yusupova, G; Yusupov, M
  • DDX6 localizes to nuage structures and the annulus of mammalian spermatogenic cells
    Kawahara, C; Yokota, S; Fujita, H
  • Human‐specific subcellular compartmentalization of P‐element induced wimpy testis‐like (PIWIL) granules during germ cell development and spermatogenesis
    Gomes Fernandes, M; He, N; Wang, F
  • A common lipid links Mfn‐mediated mitochondrial fusion and SNARE‐regulated exocytosis
    Choi, SY; Huang, P; Jenkins, GM; Chan, DC; Schiller, J; Frohman, MA
  • GPAT2, a mitochondrial outer membrane protein, in piRNA biogenesis in germline stem cells
    Shiromoto, Y; Kuramochi‐Miyagawa, S; Daiba, A
  • Cellular and subcellular localization of endogenous phospholipase D6 in seminiferous tubules of mouse testes
    Riew, TR; Kim, S; Jin, X
  • Expression of DDX25 in nuage components of mammalian spermatogenic cells: immunofluorescence and immunoelectron microscopic study
    Onohara, Y; Yokota, S
  • Argonaute2 protein in rat spermatogenic cells is localized to nuage structures and LAMP2‐positive vesicles surrounding chromatoid bodies
    Fujii, Y; Onohara, Y; Fujita, H; Yokota, S
  • ADAD1 and ADAD2, testis‐specific adenosine deaminase domain‐containing proteins, are required for male fertility
    Snyder, E; Chukrallah, L; Seltzer, K; Goodwin, L; Braun, RE
  • Localization of BRUNOL2 in rat spermatogenic cells as revealed by immunofluorescence and immunoelectron microscopic techniques
    Yonetamari, H
  • GASZ is essential for male meiosis and suppression of retrotransposon expression in the male germline
    Ma, L; Buchold, GM; Greenbaum, MP
  • Mili, a mammalian member of piwi family gene, is essential for spermatogenesis
    Kuramochi‐Miyagawa, S; Kimura, T; Ijiri, TW
  • Subcellular localization of the mouse PRAMEL1 and PRAMEX1 reveals multifaceted roles in the nucleus and cytoplasm of germ cells during spermatogenesis
    Liu, WS; Lu, C; Mistry, BV
  • A novel testis‐specific protein, PRAMEY, is involved in spermatogenesis in cattle
    Liu, WS; Zhao, Y; Lu, C
  • PRKRA localizes to nuage structures and the ectoplasmic specialization and tubulobulbar complexes in rat and mouse testis
    Suzuki, J; Yokota, S
  • Tdrd1/Mtr‐1, a tudor‐related gene, is essential for male germ‐cell differentiation and nuage/germinal granule formation in mice
    Chuma, S; Hosokawa, M; Kitamura, K
  • Tudor‐related proteins TDRD1/MTR‐1, TDRD6 and TDRD7/TRAP: domain composition, intracellular localization, and function in male germ cells in mice
    Hosokawa, M; Shoji, M; Kitamura, K
  • STK31(TDRD8) is dynamically regulated throughout mouse spermatogenesis and interacts with MIWI protein
    Bao, J; Wang, L; Lei, J
  • UHRF1 suppresses retrotransposons and cooperates with PRMT5 and PIWI proteins in male germ cells
    Dong, J; Wang, X; Cao, C
  • Cytochemical observations of the chromatoid body of the male germ cell
    Eddy, E
  • Mechanisms of translational repression of the Smcp mRNA in round spermatids
    Cullinane, DL; Chowdhury, TA; Kleene, KC
  • Independent and coordinate trafficking of single Drosophila germ plasm mRNAs
    Little, SC; Sinsimer, KS; Lee, JJ; Wieschaus, EF; Gavis, ER
  • Aggregation, segregation, and dispersal of homotypic germ plasm RNPs in the early zebrafish embryo
    Eno, C; Hansen, CL; Pelegri, F
  • Accumulation of piRNAs in the chromatoid bodies purified by a novel isolation protocol
    Meikar, O; Da Ros, M; Liljenback, H; Toppari, J; Kotaja, N
  • Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis
    Vourekas, A; Zheng, Q; Alexiou, P
  • The RNA binding protein SAM68 transiently localizes in the chromatoid body of male germ cells and influences expression of select microRNAs
    Messina, V; Meikar, O; Paronetto, MP
  • Mouse Piwi interactome identifies binding mechanism of Tdrkh Tudor domain to arginine methylated Miwi
    Chen, C; Jin, J; James, DA
  • Isolation of chromatoid bodies from mouse testis as a rich source of short RNAs
    Meikar, O; Kotaja, N
  • Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis
    Soper, SF; Heijden, GW; Hardiman, TC
  • An optimised STAPUT method for the purification of mouse spermatocyte and spermatid populations
    Dunleavy, JEM; O'Connor, AE; O'Bryan, MK
  • Separation of cells by velocity sedimentation
    Miller, R; Phillips, R
  • Transcriptome analysis of highly purified mouse spermatogenic cell populations: gene expression signatures switch from meiotic‐to postmeiotic‐related processes at pachytene stage
    da Cruz, I; Rodriguez‐Casuriaga, R; Santinaque, FF
  • A standardized approach for multispecies purification of mammalian male germ cells by mechanical tissue dissociation and flow cytometry
    Lima, AC; Jung, M; Rusch, J; Usmani, A; Lopes, AM; Conrad, DF
  • An expanded mouse testis transcriptome and mass spectrometry defines novel proteins
    Gamble, J; Chick, J; Seltzer, K
  • Proteomics: technologies and their applications
    Aslam, B; Basit, M; Nisar, MA; Khurshid, M; Rasool, MH
  • A short review on proteomics and its applications
    Chandrasekhar, K; Dileep, A; Lebonah, DE; Kumari, JP
  • A critical review of bottom‐up proteomics: the good, the bad, and the future of this field
    Dupree, EJ; Jayathirtha, M; Yorkey, H; Mihasan, M; Petre, BA; Darie, CC
  • Recent advances in mass‐spectrometry based proteomics software, tools and databases
    Halder, A; Verma, A; Biswas, D; Srivastava, S
  • The CRISPR tool kit for genome editing and beyond
    Adli, M
  • Molecular biology at the cutting edge: a review on CRISPR/CAS9 gene editing for undergraduates
    Thurtle‐Schmidt, DM; Lo, TW
  • Expression and intracellular localization of mouse Vasa‐homologue protein during germ cell development
    Toyooka, Y; Tsunekawa, N; Takahashi, Y; Matsui, Y; Satoh, M; Noce, T
  • Principles and properties of stress granules
    Protter, DSW; Parker, R
  • Molecular mechanisms of stress granule assembly and disassembly
    Hofmann, S; Kedersha, N; Anderson, P; Ivanov, P
  • The use of markers for correlative light electron microscopy
    Brown, E; Verkade, P
  • Mitochondrial RNA granules are fluid condensates positioned by membrane dynamics
    Rey, T; Zaganelli, S; Cuillery, E
  • The mitochondrial RNA‐binding protein GRSF1 localizes to RNA granules and is required for posttranscriptional mitochondrial gene expression
    Antonicka, H; Sasarman, F; Nishimura, T; Paupe, V; Shoubridge, EA
  • Visualization of podocyte substructure with structured illumination microscopy (SIM): a new approach to nephrotic disease
    Pullman, JM; Nylk, J; Campbell, EC; Gunn‐Moore, FJ; Prystowsky, MB; Dholakia, K
  • Super‐resolution microscopy demystified
    Schermelleh, L; Ferrand, A; Huser, T
  • STED super‐resolved microscopy
    Vicidomini, G; Bianchini, P; Diaspro, A
  • Fluorescence microscopy light sources
    Aswani, K; Jinadasa, T; Brown, CM
  • From Animaculum to single molecules: 300 years of the light microscope
    Wollman, AJ; Nudd, R; Hedlund, EG; Leake, MC
  • TIA1 mutations in amyotrophic lateral sclerosis and frontotemporal dementia promote phase separation and alter stress granule dynamics
    Mackenzie, IR; Nicholson, AM; Sarkar, M
  • Concepts for nanoscale resolution in fluorescence microscopy
    Hell, SW; Dyba, M; Jakobs, S
  • Distinct stages in stress granule assembly and disassembly
    Wheeler, JR; Matheny, T; Jain, S; Abrisch, R; Parker, R
  • The TRAPP complex mediates secretion arrest induced by stress granule assembly
    Zappa, F; Wilson, C; Di Tullio, G
  • Beyond light's limits: fluorescence imaging at the nanoscale
    Spence, M
  • Coaligned dual‐channel STED nanoscopy and molecular diffusion analysis at 20 nm resolution
    Gottfert, F; Wurm, CA; Mueller, V
  • Stochastic optical reconstruction microscopy (STORM) in comparison with stimulated emission depletion (STED) and other imaging methods
    Tam, J; Merino, D
  • Stochastic optical reconstruction microscopy (STORM)
    Xu, J; Ma, H; Liu, Y
  • ATPase‐modulated stress granules contain a diverse proteome and substructure
    Jain, S; Wheeler, JR; Walters, RW; Agrawal, A; Barsic, A; Parker, R
  • The White Confocal Microscopic Optical Sectioning in all Colors
    Borlinghaus, RT
  • The stress granule transcriptome reveals principles of mRNA accumulation in stress granules
    Khong, A; Matheny, T; Jain, S; Mitchell, SF; Wheeler, JR; Parker, R
  • It's just a phase: exploring the relationship between mRNA, biomolecular condensates, and translational control
    Parker, DM; Winkenbach, LP; Osborne Nishimura, E
  • Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles
    Nott, TJ; Petsalaki, E; Farber, P
  • Role of microtubules in stress granule assembly: microtubule dynamical instability favors the formation of micrometric stress granules in cells
    Chernov, KG; Barbet, A; Hamon, L; Ovchinnikov, LP; Curmi, PA; Pastre, D
  • Microtubules govern stress granule mobility and dynamics
    Nadezhina, E; Lomakin, A; Shpilman, A; Chudinova, E; Ivanov, P
  • Germ granules and gene regulation in the Caenorhabditis elegans germline
    Phillips, C; Updike, D
  • Francis Aston and the mass spectrograph
    Squires, G
  • Elektronmikroskopische befunde an versilberten kollagen fibrillen
    Dettmer, N; Neckel, I; Ruska, H
  • Immunological properties of an antibody containing a fluorescent group
    Coons, A; Creech, H; Jones, R
  • A simple method for quantitation of serum beta‐lipoproteins by means of the immunocrit
    Heiskell, C; Fisk, R; Florsheim, W; Tachi, A; Goodman, J; Carpenter, C
  • Breaking the diffraction resolution limit by stimulated emission: stimulated‐emission‐depletion fluorescence microscopy
    Hell, S; Wichmann, J
  • Fluorescence photooxidation with eosin: a method for high resolution immunolocalization and in situ hybridization detection for light and electron microscopy
    Deerinck, T; Martone, M; Lev‐Ram, V
  • Noise analysis of a white‐light supercontinuum light source for multiple wavelength confocal laser scanning fluorescence microscopy
    McConnell, G
  • Sub‐diffraction‐limit imaging by stochastic optical reconstruction microscopy (STORM)
    Rust, MJ; Bates, M; Zhuang, X
  • Method of obtaining optical sectioning by using structured light in a conventional microscope
    Neil, M; Jaskaitis, R; Wilson, T
  • A brief history of mass spectrometry
    Griffiths, J
  • Immunoprecipitation analysis of soluble complement‐fixing antigens of dengue viruses
    Russell, P; Chiewsilp, D; Brandt, W