Role of Ubiquitin-proteasome system in Espematogenesis
Main Article Content
Abstract
Spermatogenesis is a series of events that constitute programmed cell differentiation, with dramatic changes in morphology, biochemistry and gene expression which are regulated by temporal and especially endocrine, paracrine and autocrine mechanisms. During the various stages of spermatogenesis and particularly during the differentiation of spermatids, there is massive degradation of cytosolic proteins, nuclear and membrane due to the elimination of much of the cytoplasm which has round spermatid. This protein degradation occurs within the seminiferous epithelium and is mediated by cellular systems described for this purpose. The proteasome is a multienzyme complex responsible for degrading the majority of nuclear and cytosolic proteins, after they are marked for destruction by covalent attachment of ubiquitin molecules. This selective destruction of cellular proteins is a key mechanism in the process of spermatogenesis. This article discusses the basics of male gonadal physiological process and the current understanding of the role of the ubiquitin proteasome system in the functional maintenance of spermatogenesis are reviewed.
References
Adler, I. D. Comparison o f the duration o f spermatogenesis between male rodents and humans. Mutat. Res., 352(1-2):169-72, 1996.
Agell, N. & Mezquita, C. Cellular content of ubiquitin and formation of ubiquitin conjugates during chicken spermatogenesis. Biochem. J., 250(3):883-9, 1988.
Arrigo, A. P.; Simon, M.; Darlix, J. L. & Spahr, P. F. A 20S particle ubiquitous from yeast to human. J. Mol. Evol., 25(2):141-50, 1987.
Baarends, W. M.; Hoogerbrugge, J. W.; Roest, H. P.; Ooms, M.; Vreeburg, J.; Hoeijmakers, J. H. & Grootegoed, J. A. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev. Biol., 207(2):322-33,1999a.
Baarends, W. M.; Roest, H. P. & Grootegoed, J. A. The ubiquitin system in gametogenesis. Mol. Cell. Endocrinol., 151(1-5):5-16, 1999b.
Bajorek, M. & Glickman, M. H. Keepers at the final gates: regulatory complexes and gating of the proteasome channel. Cell. Mol. Life Sci., 61(13):1579-88, 2004.
Barton, L. F.; Runnels, H. A.; Schell, T. D.; Cho, Y.; Gibbons, R.; Tevethia, S. S.; Deepe, G. S. Jr. & Monaco, J. J. Immune defects in 28-kDa proteasome activator gamma-deficient mice. J. Immunol., 172(6):3948-54, 2004.
Bebington, C.; Doherty, F. J. & Fleming, S. D. The possible biological and reproductive functions of ubiquitin. Hum. Reprod. Update, 7(1):102-11, 2001.
Bedard, N.; Hingamp, P.; Pang, Z.; Karaplis, A.; Morales, C.; Trasler, J.; Cyr, D.; Gagnon, C. & Wing, S. S. Mice lacking the UBC4-testis gene have a delay in postnatal testis development but normal spermatogenesis and fertility. Mol. Cell. Biol., 25(15):6346-54, 2005.
Bellvé, A. R.; Cavicchia, J. C.; Millette, C. F.; O'Brien, D. A.; Bhatnagar, Y. M. & Dym, M. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell Biol., 74(1):68-85, 1977.
Bialy, L. P.; Ziemba, H. T.; Marianowski, P.; Fracki, S.; Bury, M. & Wójcik, C. Localization of a proteasomal antigen in human spermatozoa: immunohistochemical electron microscopic study. Folia Histochem. Cytobiol., 39(2):129-30, 2001.
Bousquet-Dubouch, M. P.; Fabre, B.; Monsarrat, B. & Burlet-Schiltz, O. Proteomics to study the diversity and dynamics of proteasome complexes: from fundamentals to the clinic. Expert Rev. Proteomics, 8(4):459-81, 2011.
Ciechanover, A. Intracellular protein degradation: from a vague idea, through the lysosome and the ubiquitin-proteasome system, and onto human diseases and drug targeting (Nobel lecture). Angew. Chem. Int. Ed. Engl., 44(37):5944-67, 2005a.
Ciechanover, A. Intracellular protein degradation: from a vague idea, through the lysosome and the ubiquitin-proteasome system, and onto human diseases and drug targeting (Nobel lecture). Angew. Chem. Int. Ed. Engl., 44(37):5944-67, 2005b.
Ciechanover, A. The ubiquitin proteolytic system: from an idea to the patient bed. Proc. Am. Thorac. Soc., 3(1):21-31, 2006.
Claverol, S.; Burlet-Schiltz, O.; Girbal-Neuhauser, E.; Gairin, J. E. & Monsarrat, B. Mapping and structural dissection of human 20 S proteasome using proteomic approaches. Mol. Cell. Proteomics, 1(8):567-78, 2002.
Clermont, Y. Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol. Rev., 52(1):198-236, 1972
Clermont, Y. & Bustos-Obregon, E. Re-examination of spermatogonial renewal in the rat by means of seminiferous tubules mounted "in toto". Am. J. Anat., 122(2):237-47, 1968.
Chen, H. Y.; Sun, J. M.; Zhang, Y.; Davie, J. R. & Meistrich, M. L. Ubiquitination of histone H3 in elongating spermatids of rat testes. J. Biol. Chem., 273(21):13165-9, 1998
de Bie, P. & Ciechanover, A. Ubiquitination of E3 ligases: self-regulation of the ubiquitin system via proteolytic and non-proteolytic mechanisms. Cell. Death Differ., 18(9):1393-402, 2011.
Diaz, E. S.; Kong, M. & Morales, P. Effect of fibronectin on proteasome activity, acrosome reaction, tyrosine phosphorylation and intracellular calcium concentrations of human sperm. Hum. Reprod., 22(5):1420-30, 2007.
Eddy, E. M. Male germ cell gene expression. Recent Prog. Horm. Res., 57:103-28, 2002.
Fang, S. & Weissman, A. M. A Field Guide to Ubiquitylation. Cell. Mol. Life Sci., 61(13):1546- 61, 2004.
Feist, E.; Brychcy, M.; Hausdorf, G.; Hoyer, B.; Egerer, K.; Dörner, T.; Kuckelkorn, U. & Burmester, G. R. Anti-proteasome autoantibodies contribute to anti-nuclear antibody patterns on human larynx carcinoma cells. Ann. Rheum. Dis., 66(1):5-11, 2007.
Fouquet, J. P. & Dadoune, J. P. Renewal of spermatogonia in the monkey (Macaca fascicularis). Biol. Reprod., 35(1):199-207, 1986.
Fraile, B.; Martin, R.; De Miguel, M. P.; Arenas, M. I.; Bethencourt, F. R.; Peinado, F.; Paniagua, R. & Santamaria, L. Light and electron microscopic immunohistochemical localization of protein gene product 9.5 and ubiquitin immunoreactivities in the human epididymis and vas deferens. Biol. Reprod., 55(2):291-7, 1996.
França, L. R.; Ogawa, T.; Avarbock, M. R.; Brinster, R. L. & Russell, L. D. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol. Reprod., 59(6):1371-7, 1998.
Glickman, M. H. & Ciechanover, A. The ubiquitinproteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev., 82(2):373- 428, 2002.
Grillari, J.; Katinger, H. & Voglauer, R. Aging and the ubiquitinome: traditional and non-traditional functions of ubiquitin in aging cells and tissues. Exp. Gerontol., 41(11):1067-79, 2006.
Haraguchi, C. M.; Mabuchi, T.; Hirata, S.; Shoda, T.; Tokumoto, T.; Hoshi, K. & Yokota, S. Possible function of caudal nuclear pocket: degradation of nucleoproteins by ubiquitin-proteasome system in rat spermatids and human sperm. J. Histochem. Cytochem., 55(6):585-95, 2007.
He, C. & Klionsky, D. J. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet., 43:67-93, 2009.
Hegerl, R.; Pfeifer, G.; Pühler, G.; Dahlmann, B. & Baumeister, W. The three-dimensional structure of proteasomes from Thermoplasma acidophilum as determined by electron microscopy using random conical tilting. F. E. B. S. Lett., 283(1):117-21, 1991.
Hermo, L.; Pelletier, R. M.; Cyr, D. G. & Smith, C. E. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: background to spermatogenesis, spermatogonia, and spermatocytes. Microsc. Res. Tech., 73(4):241-78, 2010.
Hershko, A. & Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem., 67:425-79, 1998.
Hogarth, C. A. & Griswold, M. D. The key role of vitamin A in spermatogenesis. J. Clin. Invest., 120(4):956-62, 2010.
Inaba, K.; Akazome, Y. & Morisawa, M. Purification of proteasomes from salmonid fish sperm and their localization along sperm flagella. J. Cell. Sci., 104(Pt. 3):907-15, 1993.
Jakob, C.; Egerer, K.; Liebisch, P.; Türkmen, S.; Zavrski, I.; Kuckelkorn, U.; Heider, U.; Kaiser, M.; Fleissner, C.; Sterz, J.; Kleeberg, L.; Feist, E.; Burmester, G. R.; Kloetzel, P. M. & Sezer, O. Circulating proteasome levels are an independent prognostic factor for survival in multiple myeloma. Blood, 109(5):2100-5,2007.
Jung, T.; Catalgol, B. & Grune, T. The proteasomal system. Mol. Aspects Med., 30(4):191-296, 2009.
Kerr, J. B.; Loveland, K. L.; O'Bryan, M. K. & De Kretser, D. M. Citology of the Testis and Intrinsic Control Mechanisms. En: Neill, J. D. (Ed.). Knobil and Neill's Physiology of Reproduction. 3rd ed.New York, Elsevier, 2006.
Khor, B.; Bredemeyer, A. L.; Huang, C. Y.; Turnbull, I. R.; Evans, R.; Maggi, L. B. Jr.; White, J. M.;Walker, L. M.; Carnes, K.; Hess, R. A. &Sleckman, B. P. Proteasome activator PA200 isrequired for normal spermatogenesis. Mol. Cell.Biol., 26(8):2999-3007, 2006.
Kim, H. M.; Yu, Y. & Cheng, Y. Structure characterization of the 26S proteasome. Biochim. Biophys. Acta, 1809(2):67-79, 2011.
Kinyamu, H. K.; Chen, J. & Archer, T. K. Linking the ubiquitin-proteasome pathway to chromatin remodeling/modification by nuclear receptors. J. Mol. Endocrinol., 34(2):281-97, 2005.
Kirschner, M. Intracellular proteolysis. Trends Cell. Biol., 9(1):M42-5, 1999.
Kloetzel, P. M. Antigen processing by the proteasome. Nat. Rev. Mol. Cell Biol., 2(3):179-87, 2001.
Kniepert, A. & Groettrup, M. The unique functions of tissue-specific proteasomes. Trends Biochem. Sci., 39(1):17-24, 2014.
Kon, Y.; Endoh, D. & Iwanaga, T. Expression of protein gene product 9.5, a neuronal ubiquitin C-terminal hydrolase, and its developing changein sertoli cells of mouse testis. Mol. Reprod. Dev.,54(4):333-41, 1999.
Konstantinova, I. M.; Tsimokha, A. S. & Mittenberg,A. G. Role of proteasomes in cellular regulation. Int. Rev. Cell. Mol. Biol., 267:59-124, 2008.
Kroemer, G.; Mariño, G. & Levine, B. Autophagy and the integrated stress response. Mol. Cell.,40(2):280-93, 2010.
Kwiatkowska, M.; Wojtczak, A.; Pop?on´ska, K. & Teodorczyk, M. The influence of epoxomicin, inhibitor of proteasomal proteolytic activity, on spermiogenesis in Chara vulgaris. Folia Histochem. Cytobiol., 41(1):51-4, 2003.
Leblond, C. P. & Clermont, Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann. N. Y. Acad. Sci., 55(4):548-73,1952.
Lui, W. Y. & Lee, W. M. Ubiquitin system in male reproduction and its relevance to contraception. Immunol. Endocr. Metab. Agents Med. Chem., 8(1):14-9, 2008.
Ma, J.; Katz, E. & Belote, J. M. Expression of proteasome subunit isoforms during spermatogenesis in Drosophila melanogaster. Insect Mol. Biol., 11(6):627-39, 2002.
Matsumoto, A. M. & Bremner, W. J. Endocrine control of human spermatogenesis. J. Steroid Biochem., 33(4B):789-90, 1989.
Matsumura, K. & Aketa, K. Proteasome (multicatalytic proteinase) of sea urchin sperm and its possible participation in the acrosome reaction. Mol. Reprod. Dev., 29(2):189-99, 1991.
Mochida, K.; Tres, L. L. & Kierszenbaum, A. L. Structural features of the 26S proteasome complex isolated from rat testis and sperm tail.Mol. Reprod. Dev., 57(2):176-84, 2000.
Morales, P.; Kong, M.; Pizarro, E. & Pasten, C. Participation of the sperm proteasome in human fertilization. Hum. Reprod., 18(5):1010-7, 2003.
Morales, P.; Pizarro, E.; Kong, M. & Jara, M. Extracellular localization of proteasomes in human sperm. Mol. Reprod. Dev., 68(1):115-24, 2004.
Murata, S.; Kawahara, H.; Tohma, S.; Yamamoto, K.; Kasahara, M.; Nabeshima, Y.; Tanaka, K. & Chiba, T. Growth retardation in mice lacking the proteasome activator PA28gamma. J. Biol. Chem., 274(53):38211-5, 1999.
Murata, S.; Udono, H.; Tanahashi, N.; Hamada, N.; Watanabe, K.; Adachi, K.; Yamano, T.; Yui, K.; Kobayashi, N.; Kasahara, M.; Tanaka, K. & Chiba, T. Immunoproteasome assembly and antigen presentation in mice lacking both PA28alpha and PA28beta. E. M. B. O. J., 20(21):5898-907,2001.
Nandi, D.; Tahiliani, P.; Kumar, A. & Chandu, D. The ubiquitin-proteasome system. J. Biosci., 31(1):137-55, 2006.
Nederlof, P. M.; Wang, H. R. & Baumeister, W. Nuclear localization signals of human and Thermoplasma proteasomal alpha subunits are functional in vitro. Proc. Natl. Acad. Sci. U. S. A., 92(26):12060-4, 1995.
Orlowski, M. The multicatalytic proteinase complex, a major extralysosomal proteolytic system. Biochemistry, 29(45):10289-97, 1990.
Ortega, J.; Heymann, J. B.; Kajava, A. V.; Ustrell, V.; Rechsteiner, M. & Steven, A. C. The axial channel of the 20S proteasome opens upon binding of the PA200 activator. J. Mol. Biol., 346(5):1221-7, 2005.
Parvinen, M. Regulation of the seminiferous epithelium. Endocr. Rev., 3(4):404-17, 1982.
Pickart, C. M. Back to the future with ubiquitin. Cell, 116(2):181-90, 2004.
Pickart, C. M. & Cohen, R. E. Proteasomes and their kin: proteases in the machine age. Nat. Rev. Mol. Cell. Biol., 5(3):177-87, 2004.
Pickart, C. M. & Eddins, M. J. Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta, 1695(1-3):55-72, 2004.
Pickart, C. M. & Fushman, D. Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol.,8(6):610-6, 2004.
Qian, M. X.; Pang, Y.; Liu, C. H.; Haratake, K.; Du, B. Y.; Ji, D. Y.; Wang, G. F.; Zhu, Q. Q.; Song, W.; Yu, Y.; Zhang, X. X.; Huang, H. T.; Miao, S.; Chen, L. B.; Zhang, Z. H.; Liang, Y. N.; Liu, S.; Cha, H.; Yang, D.; Zhai, Y.; Komatsu, T.; Tsuruta, F.; Li, H.; Cao, C.; Li, W.; Li, G. H.; Cheng, Y.; Chiba, T.;Wang, L.; Goldberg, A. L.; Shen, Y. & Qiu, X. B.Acetylation-mediated proteasomal degradation ofcore histones during DNA repair andspermatogenesis. Cell, 153(5):1012-24, 2013.
Rawe, V. Y.; Díaz, E. S.; Abdelmassih, R.; Wójcik, C.; Morales, P.; Sutovsky, P. & Chemes, H. E. The role of sperm proteasomes during sperm aster formation and early zygote development: implications for fertilization failure in humans. Hum. Reprod., 23(3):573-80, 2008.
Rechsteiner, M. & Hill, C. P. Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends Cell. Biol., 15(1):27-33, 2005.
Reid, A. T.; Redgrove, K.; Aitken, R. J. & Nixon, B. Cellular mechanisms regulating sperm-zona pellucida interaction. Asian J. Androl., 13(1):88-96, 2011.
Rock, K. L.; Gramm, C.; Rothstein, L.; Clark, K.; Stein, R.; Dick, L.; Hwang, D. & Goldberg, A. L. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell, 78(5):761-71, 1994.
Rodriguez, C. I. & Stewart, C. L. Disruption of the ubiquitin ligase HERC4 causes defects in spermatozoon maturation and impaired fertility. Dev. Biol., 312(2):501-8, 2007.
Russell, L.; Ettlin, R.; Sinha Hikim, A. & Clegg, E. Histological And Histopathological Evaluation Of The Testis. Clearwater, Cache River Press, 1990.
Ryu, K. Y.; Sinnar, S. A.; Reinholdt, L. G.; Vaccari, S.; Hall, S.; Garcia, M. A.; Zaitseva, T. S.; Bouley, D. M.; Boekelheide, K.; Handel, M. A.; Conti, M. & Kopio, R. R. The mouse polyubiquitin gene Ubb is essential for meiotic progression. Mol. Cell. Biol., 28(3):1136-46, 2008.
Saitoh, Y.; Sawada, H. & Yokosawa, H. High-molecularweight protease complexes (proteasomes) of sperm of the ascidian, Halocynthia roretzi: isolation, characterization, and physiological roles in fertilization. Dev. Biol., 158(1):238-44, 1993.
Santamaría, L.; Martín, R.; Paniagua, R.; Fraile, B.; Nistal, M.; Terenghi, G. & Polak, J. M. Protein gene product 9.5 and ubiquitin immunoreactivities in rat epididymis epithelium. Histochemistry, 100(2):131- 8, 1993.
Savulescu, A. F. & Glickman, M. H. Proteasome activator 200: the heat is on... Mol. Cell. Proteomics, 10(5):R110.006890, 2011.
Sawada, H.; Iwasaki, K.; Kihara-Negishi, F.; Ariga, H. & Yokosawa, H. Localization, expression, and the role in fertilization of spermosin, an ascidian sperm trypsin-like protease. Biochem. Biophys. Res. Commun., 222(2):499-504, 1996.
Sawada, H.; Sakai, N.; Abe, Y.; Tanaka, E.; Takahashi, Y.; Fujino, J.; Kodama, E.; Takizawa, S. & Yokosawa, H. Extracellular ubiquitination and proteasomemediated degradation of the ascidian sperm receptor. Proc. Natl. Acad. Sci. U. S. A., 99(3):1223-8, 2002.
Sawada, H.; Yokosawa, H.; Hoshi, M. & Ishii, S. Ascidian sperm chymotrypsin-like enzyme; participation in fertilization. Experientia, 39(4):377-8, 1983.
Sawada, H.; Yokosawa, H. & Ishii, S. Purification and characterization of two types of trypsin-like enzymes from sperm of the ascidian (Prochordata) Halocynthia roretzi. Evidence for the presence of spermosin, a novel acrosin-like enzyme. J. Biol. Chem., 259(5):2900-4, 1984.
Schlesinger, D. H.; Goldstein, G. & Niall, H. D. The complete amino acid sequence of ubiquitin, an adenylate cyclase stimulating polypeptide probably universal in living cells. Biochemistry, 14(10):2214-8, 1975.
Skerget, S.; Rosenow, M.; Polpitiya, A.; Petritis, K.; Dorus, S. & Karr, T. L. The Rhesus macaque (Macaca mulatta) sperm proteome. Mol. Cell. Proteomics, 12(11):3052-67, 2013.
Sorokin, A. V.; Kim, E. R. & Ovchinnikov, L. P. Nucleocytoplasmic transport of proteins. Biochemistry (Mosc.), 72(13):1439-57, 2007.
Spiteri-Grech, J. & Nieschlag, E. Paracrine factors relevant to the regulation of spermatogenesis--a review. J. Reprod. Fertil., 98(1):1-14, 1993.
Steinberger, E.; Steinberger, A. & Sanborn, B. Endocrine control of spermatogenesis. Basic Life Sci., 4(Part A):163-81, 1974.
Sutovsky, P.; Manandhar, G.; McCauley, T. C.; Caamaño, J. N.; Sutovsky, M.; Thompson, W. E. & Day, B. N. Proteasomal interference prevents zona pellucida penetration and fertilization in mammals. Biol. Reprod., 71(5):1625-37, 2004.
Tapia, S.; Rojas, M.; Morales, P.; Ramirez, M. A. & Diaz, E. S. The laminin-induced acrosome reaction in human sperm is mediated by Src kinases and the proteasome. Biol. Reprod., 85(2):357-66, 2011.
Tipler, C. P.; Hutchon, S. P.; Hendil, K.; Tanaka, K.; Fishel, S. & Mayer, R. J. Purification and characterization of 26S proteasomes from human and mouse spermatozoa. Mol. Hum. Reprod., 3(12):1053-60, 1997.
Ustrell, V.; Hoffman, L.; Pratt, G. & Rechsteiner, M. PA200, a nuclear proteasome activator involved in DNA repair. E. M. B. O. J., 21(13):3516-25, 2002
Ventii, K. H. & Wilkinson, K. D. Protein partners of deubiquitinating enzymes. Biochem. J., 414(2):161-75, 2008.
Verhoeven, G.; Willems, A.; Denolet, E.; Swinnen, J. V. & De Gendt, K. Androgens and spermatogenesis: lessons from transgenic mouse models. Philos. Trans. R. Soc. Lond. B Biol. Sci., 365(1546):1537-56, 2010.
Vogl, A. W.; Vaid, K. S. & Guttman, J. A. The Sertoli cell cytoskeleton. Adv. Exp. Med. Biol., 636:186- 211, 2008.
Wada, M.; Kosaka, M.; Saito, S.; Sano, T.; Tanaka, K. & Ichihara, A. Serum concentration and localization in tumor cells of proteasomes in patients with hematologic malignancy and their pathophysiologic significance. J. Lab. Clin. Med., 121(2):215-23, 1993.
Walz, J.; Erdmann, A.; Kania, M.; Typke, D.; Koster, A. J. & Baumeister, W. 26S proteasome structure revealed by three-dimensional electron microscopy. J. Struct. Biol., 121(1):19-29, 1998.
Wilk, S. & Orlowski, M. Cation-sensitive neutral endopeptidase: isolation and specificity of the bovine pituitary enzyme. J. Neurochem., 35(5):1172-82, 1980.
Wilk, S. & Orlowski, M. Evidence that pituitary cationsensitive neutral endopeptidase is a multicatalytic protease complex. J. Neurochem., 40(3):842-9,1983.
Wing, S. S.; Bédard, N.; Morales, C.; Hingamp, P. & Trasler, J. A novel rat homolog o f the Saccharomyces cerevisiae ubiquitin-conjugating enzymes UBC4 and UBC5 with distinct biochemical features is induced during spermatogenesis. Mol. Cell. Biol., 16(8):4064-72, 1996.
Wojcik, C.; Benchaib, M.; Lornage, J.; Czyba, J. C. & Guerin, J. F. Proteasomes in human spermatozoa. Int. J. Androl., 23(3):169-77, 2000.
Wojtczak, A. & Kwiatkowska, M. Immunocytochemical and ultrastructural analyses of the function of the ubiquitin-proteasome system during spermiogenesis with the use of the inhibitors of proteasome proteolytic activity in the alga, Chara vulgaris. Biol. Reprod., 78(4):577-85, 2008.
Yokota, N.; Harada, Y. & Sawada, H. Identification of testis-specific ubiquitin-conjugating enzyme in the ascidian Ciona intestinalis. Mol. Reprod. Dev., 77(7):640-7, 2010.
Yokota, N. & Sawada, H. Sperm proteasomes are responsible for the acrosome reaction and sperm penetration of the vitelline envelope during fertilization of the sea urchin Pseudocentrotus depressus. Dev. Biol., 308(1):222-31, 2007.
Yuan, X.; Miller, M. & Belote, J. M. Duplicated proteasome subunit genes in Drosophila melanogaster encoding testes-specific isoforms. Genetics, 144(1):147-57, 1996.