Sperm proteasome and fertilization

Reproduction

Volumn 142, Issue 1, 2011, Pages 1-14

  Sutovsky, Peter ^a  

^a University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIBODY; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; PROTEASOME; UBIQUITIN;

ACROSOME REACTION; EXOCYTOSIS; FERTILIZATION; GENETICS; HUMAN; MEDICAL RESEARCH; NONHUMAN; POLYSPERMY; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SPERMATOZOON; SPERMATOZOON CAPACITATION; VITELLINE MEMBRANE; ZONA PELLUCIDA;

ANIMALS; ENZYME INHIBITORS; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; HUMANS; MALE; OVUM; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; SPERMATOZOA; UBIQUITIN;

ANIMALIA; ASCIDIACEA; ECHINODERMATA; ECHINOIDEA; MAMMALIA;

EID: 79960447102     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-11-0041     Document Type: Review

References (97)

1. Arcelay E, Salicioni AM, Wertheimer E & Visconti PE 2008 Identification of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation. International Journal of Developmental Biology 52 463-472. (doi:10.1387/ijdb.072555ea)
2. Austin CR & Bishop MW 1958 Role of the rodent acrosome and perforatorium in fertilization. Proceedings of the Royal Society of London. Series B. Biological Sciences 149 241-248. (doi:10.1098/rspb.1958.0066)
3. Azzu V & Brand MD 2010 Degradation of an intramitochondrial protein by the cytosolic proteasome. Journal of Cell Science 123 578-585. (doi:10.1242/jcs.060004)
4. Baarends WM, van der Laan R & Grootegoed JA 2000 Specific aspects of the ubiquitin system in spermatogenesis. Journal of Endocrinological Investigation 23 597-604.
5. Baba T, Azuma S, Kashiwabara S & Toyoda Y 1994 Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. Journal of Biological Chemistry 269 31845-31849. (Pubitemid 24379557)
6. Bailey JL 2010 Factors regulating sperm capacitation. Systems Biology in Reproductive Medicine 56 334-348. (doi:10.3109/19396368.2010.512377)
7. Baker MA, Hetherington L, Reeves G, Muller J & Aitken RJ 2008 The rat sperm proteome characterized via IPG strip prefractionation and LCKMS/MS identification. Proteomics 8 2312-2321. (doi:10.1002/pmic.200700876)
8. Baker MA, Smith ND, Hetherington L, Taubman K, Graham ME, Robinson PJ & Aitken RJ 2010 Label-free quantitation of phosphopeptide changes during rat sperm capacitation. Journal of Proteome Research 9 718-729. (doi:10.1021/pr900513d)
9. Bedard N, Yang Y, Gregory M, Cyr DG, Suzuki J, Yu X, Chian RC, Hermo L, O'Flaherty C, Smith CE et al. 2011 Mice lacking the USP2 deubiquitinating enzyme have severe male subfertility associated with defects in fertilization and sperm motility. Biology of Reproduction [in press]. (doi:10.1095/biolreprod.110. 088542)
10. Bedford JM 1998 Mammalian fertilization misread? Sperm penetration of the eutherian zona pellucida is unlikely to be a lytic event Biology of Reproduction 59 1275-1287. (doi:10.1095/biolreprod59.6.1275)
11. Bedford JM 2008 Puzzles of mammalian fertilization - and beyond. International Journal of Developmental Biology 52 415-426. (doi:10.1387/ijdb. 072551jb)
12. Bohring C & Krause W 2003 Characterization of spermatozoa surface antigens by antisperm antibodies and its influence on acrosomal exocytosis. American Journal of Reproductive Immunology 50 411-419. (doi:10.1034/j.1600- 0897.2003.00103.x)
13. Chakravarty S, Bansal P, Sutovsky P & Gupta SK 2008 Role of proteasomal activity in the induction of acrosomal exocytosis in human spermatozoa. Reproductive Biomedicine Online 16 391-400. (doi:10.1016/S1472- 6483(10)60601-3)
14. Choi YJ, Uhm SJ, Song SJ, Song H, Park JK, Kim T, Park C & Kim JH 2008 Cytochrome c upregulation during capacitation and spontaneous acrosome reaction determines the fate of pig sperm cells: linking proteome analysis. Journal of Reproduction and Development 54 68-83. (doi:10.1262/jrd.19116)
15. Ciechanover A 2009 Tracing the history of the ubiquitin proteolytic system: the pioneering article. Biochemical and Biophysical Research Communications 387 1-10. (doi:10.1016/j.bbrc.2009.06.065)
16. Coux O, Nothwang HG, Silva Pereira I, Recillas Targa F, Bey F & Scherrer K 1994 Phylogenic relationships of the amino acid sequences of prosome (proteasome, MCP) subunits. Molecular & General Genetics 245 769-780. (doi:10.1007/BF00297284)
17. Diaz ES, Kong M & Morales P 2007 Effect of fibronectin on proteasome activity, acrosome reaction, tyrosine phosphorylation and intracellular calcium concentrations of human sperm. Human Reproduction 22 1420-1430. (doi:10.1093/humrep/dem023)
18. Ellederova Z, Halada P, Man P, Kubelka M, Motlik J & Kovarova H 2004 Protein patterns of pig oocytes during in vitro maturation. Biology of Reproduction 71 1533-1539. (doi:10.1095/biolreprod.104.030304)
19. Gadella BM & Visconti PE 2006 Regulation of capacitation. In The Sperm Cell, pp 134-169. Eds C De Jonge & CL Barratt. Cambridge, UK: Cambridge University Press.
20. Gerton G 2002 Function of the sperm acrosome. In Fertilization, pp 265-302. Ed. D Hardy. San Diego: Academic Press.
21. Geussova G, Kalab P & Peknicova J 2002 Valosine containing protein is a substrate of cAMP-activated boar sperm tyrosine kinase. Molecular Reproduction and Development 63 366-375. (doi:10.1002/mrd.10156)
22. Glickman MH & Ciechanover A 2002 The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiological Reviews 82 373-428. (doi:10.1152/physrev.00027.2001)
23. Green DP 1987 Mammalian sperm cannot penetrate the zona pellucida solely by force. Experimental Cell Research 169 31-38. (doi:10.1016/0014-4827(87)90221- 7)
24. Gupta SK, Bagavant H, Chadha K, Gupta M, Yurewicz EC & Sacco AG 1993 Mapping of immunogenic domains on porcine zona pellucida 3 alpha and beta glycoproteins by murine monoclonal antibodies. American Journal of Reproductive Immunology 30 95-100. (Pubitemid 24014463)
25. Guterman A & Glickman MH 2004 Deubiquitinating enzymes are IN/(trinsic to proteasome function). Current Protein & Peptide Science 5 201-211. (doi:10.2174/1389203043379756)
26. Hedrick JL 2008 Anuran and pig egg zona pellucida glycoproteins in fertilization and early development. International Journal of Developmental Biology 52 683-701. (doi:10.1387/ijdb.082580jh)
27. Hermo L, Pelletier RM, Cyr DG & Smith CE 2010 Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 4: intercellular bridges, mitochondria, nuclear envelope, apoptosis, ubiquitination, membrane/voltage-gated channels, methylation/acetylation, and transcription factors. Microscopy Research and Technique 73 364-408. (doi:10.1002/jemt.20783)
28. Jin M, Fujiwara E, Kakiuchi Y, Okabe M, Satouh Y, Baba SA, Chiba K & Hirohashi N 2011 Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. PNAS 108 4892-4896. (doi:10.1073/pnas.1018202108)
29. Kato JY & Yoneda-Kato N 2009 Mammalian COP9 signalosome. Genes to Cells 14 1209-1225. (doi:10.1111/j.1365-2443.2009.01349.x)
30. Kawano N, Kang W, Yamashita M, Koga Y, Yamazaki T, Hata T, Miyado K & Baba T 2010 Mice lacking two sperm serine proteases, ACR and PRSS21, are subfertile, but the mutant sperm are infertile in vitro. Biology of Reproduction 83 359-369. (doi:10.1095/biolreprod.109.083089)
31. Khor B, Bredemeyer AL, Huang CY, Turnbull IR, Evans R, Maggi LB Jr, White JM, Walker LM, Carnes K, Hess RA et al. 2006 Proteasome activator PA200 is required for normal spermatogenesis. Molecular and Cellular Biology 26 2999-3007. (doi:10.1128/MCB.26.8.2999-3007.2006)
32. Kim ST, Zhang K, Dong J & Lord EM 2006 Exogenous free ubiquitin enhances lily pollen tube adhesion to an in vitro stylar matrix and may facilitate endocytosis of SCA. Plant Physiology 142 1397-1411. (doi:10.1104/pp.106.086801)
33. Kloetzel PM & Ossendorp F 2004 Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Current Opinion in Immunology 16 76-81. (doi:10.1016/j.coi.2003.11.004)
34. Kong M, Diaz ES & Morales P 2009 Participation of the human sperm proteasome in the capacitation process and its regulation by protein kinase A and tyrosine kinase. Biology of Reproduction 80 1026-1035. (doi:10.1095/ biolreprod.108.073924)
35. Kurihara LJ, Semenova E, Levorse JM & Tilghman SM 2000 Expression and functional analysis of Uch-L3 during mouse development. Molecular and Cellular Biology 20 2498-2504. (doi:10.1128/MCB.20.7.2498-2504.2000)
36. Kwon J, Mochida K, Wang YL, Sekiguchi S, Sankai T, Aoki S, Ogura A, Yoshikawa Y & Wada K 2005 Ubiquitin C-terminal hydrolase L-1 is essential for the early apoptotic wave of germinal cells and for sperm quality control during spermatogenesis. Biology of Reproduction 73 29-35. (doi:10.1095/ biolreprod.104.037077)
37. Kwon J, Sekiguchi S, Wang YL, Setsuie R, Yoshikawa Y & Wada K 2006 The region-specific functions of two ubiquitin C-terminal hydrolase isozymes along the epididymis. Experimental Animals 55 35-43. (doi:10.1538/expanim.55.35)
38. van Leeuwen FW, de Kleijn DP, van den Hurk HH, Neubauer A, Sonnemans MA, Sluijs JA, Koycu S, Ramdjielal RD, Salehi A, Martens GJ et al. 1998 Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients. Science 279 242-247. (doi:10.1126/science.279.5348.242)
39. van Leeuwen FW, Kros JM, Kamphorst W, van Schravendijk C & de Vos RA 2006 Molecular misreading: the occurrence of frameshift proteins in different diseases. Biochemical Society Transactions 34 738-742. (doi:10.1042/BST0340738)
40. Lerer-Goldshtein T, Bel S, Shpungin S, Pery E, Motro B, Goldstein RS, Bar-Sheshet SI, Breitbart H & Nir U 2010 TMF/ARA160: a key regulator of sperm development. Developmental Biology 348 12-21. (doi:10.1016/j.ydbio.2010. 07.033)
41. Massicotte L, Coenen K, Mourot M & Sirard MA 2006 Maternal housekeeping proteins translated during bovine oocyte maturation and early embryo development. Proteomics 6 3811-3820. (doi:10.1002/pmic.200500803)
42. de Mateo S, Martinez-Heredia J, Estanyol JM, Dominguez-Fandos D, Vidal- Taboada JM, Ballesca JL & Oliva R 2007 Marked correlations in protein expression identified by proteomic analysis of human spermatozoa. Proteomics 7 4264-4277. (doi:10.1002/pmic.200700521)
43. Mochida K, Tres LL & Kierszenbaum AL 2000 Structural features of the 26S proteasome complex isolated from rat testis and sperm tail. Molecular Reproduction and Development 57 176-184. (doi:10.1002/1098-2795(200010)57: 2〈176::AID-MRD9〉3.0.CO;2-O)
44. Moore K, Lovercamp K, Feng D, Antelman J, Sutovsky M, Manandhar G, van Leyen K, Safranski T & Sutovsky P 2010 Altered epididymal sperm maturation and cytoplasmic droplet migration in subfertile male Alox15 mice. Cell and Tissue Research 340 569-581. (doi:10.1007/s00441-010-0972-x)
45. Morales P, Kong M, Pizarro E & Pasten C 2003 Participation of the sperm proteasome in human fertilization. Human Reproduction 18 1010-1017. (doi:10.1093/humrep/deg111)
46. Morales P, Pizarro E, Kong M & Jara M 2004 Extracellular localization of proteasomes in human sperm. Molecular Reproduction and Development 68 115-124. (doi:10.1002/mrd.20052)
47. Morales P, Diaz ES & Kong M 2007 Proteasome activity and its relationship with protein phosphorylation during capacitation and acrosome reaction in human spermatozoa. Society of Reproduction and Fertility Supplement 65 269-273.
48. Mtango NR, Sutovsky M, Zhong Z, Vande Voort CA, Latham KE & Sutovsky P 2009 Roles of deubiquitnating enzymes UCHL1 and UCHL3 in oocyte maturation, fertilization and zygotic development. Biology of Reproduction 81 (Special Issue) 329.
49. Nakagawa T, Shirane M, Iemura S, Natsume T & Nakayama KI 2007 Anchoring of the 26S proteasome to the organellar membrane by FKBP38. Genes to Cells 12 709-719. (doi:10.1111/j.1365-2443.2007.01086.x)
50. Naz RK & Dhandapani L 2010 Identification of human sperm proteins that interact with human zona pellucida3 (ZP3) using yeast two-hybrid system. Journal of Reproductive Immunology 84 24-31. (doi:10.1016/j.jri.2009.10.006)
51. Olds-Clarke P 2003 Unresolved issues in mammalian fertilization. International Review of Cytology 232 129-184. (doi:10.1016/S0074-7696(03)32004- 2)
52. Pasten C, Morales P & Kong M 2005 Role of the sperm proteasome during fertilization and gamete interaction in the mouse. Molecular Reproduction and Development 71 209-219. (doi:10.1002/mrd.20280)
53. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, Marsischky G, Roelofs J, Finley D & Gygi SP 2003 A proteomics approach to understanding protein ubiquitination. Nature Biotechnology 21 921-926. (doi:10.1038/nbt849)
54. Platts AE, Dix DJ, Chemes HE, Thompson KE, Goodrich R, Rockett JC, Rawe VY, Quintana S, Diamond MP, Strader LF et al. 2007 Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs. Human Molecular Genetics 16 763-773. (doi:10.1093/hmg/ddm012)
55. de Pril R, Fischer DF, Maat-Schieman ML, Hobo B, de Vos RA, Brunt ER, Hol EM, Roos RA & van Leeuwen FW 2004 Accumulation of aberrant ubiquitin induces aggregate formation and cell death in polyglutamine diseases. Human Molecular Genetics 13 1803-1813. (doi:10.1093/hmg/ddh188)
56. Rawe VY, Diaz ES, Abdelmassih R, Wojcik C, Morales P, Sutovsky P & Chemes HE 2008 The role of sperm proteasomes during sperm aster formation and early zygote development: implications for fertilization failure in humans. Human Reproduction 23 573-580. (doi:10.1093/humrep/dem385)
57. Rechsteiner M & Hill CP 2005 Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends in Cell Biology 15 27-33. (doi:10.1016/j.tcb.2004.11.003)
58. Rivkin E, Kierszenbaum AL, Gil M & Tres LL 2009 Rnf19a, a ubiquitin protein ligase, and Psmc3, a component of the 26S proteasome, tether to the acrosome membranes and the head-tail coupling apparatus during rat spermatid development. Developmental Dynamics 238 1851-1861. (doi:10.1002/dvdy.22004)
59. Rodriguez CI & Stewart CL 2007 Disruption of the ubiquitin ligase HERC4 causes defects in spermatozoon maturation and impaired fertility. Developmental Biology 312 501-508. (doi:10.1016/j.ydbio.2007.09.053)
60. Rodriguez-Miranda E, Buffone MG, Edwards SE, Ord TS, Lin K, Sammel MD, Gerton GL, Moss SB & Williams CJ 2008 Extracellular adenosine 50-triphosphate alters motility and improves the fertilizing capability of mouse sperm. Biology of Reproduction 79 164-171. (doi:10.1095/biolreprod.107.065565)
61. Roest HP, van Klaveren J, de Wit J, van Gurp CG, Koken MH, Vermey M, van Roijen JH, Hoogerbrugge JW, Vreeburg JT, Baarends WM et al. 1996 Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell 86 799-810. (doi:10.1016/S0092- 8674(00)80154-3)
62. Saigoh K, Wang YL, Suh JG, Yamanishi T, Sakai Y, Kiyosawa H, Harada T, Ichihara N, Wakana S, Kikuchi T et al. 1999 Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gadmice. Nature Genetics 23 47-51. (doi:10.1038/12647)
63. Saitoh Y, Sawada H & Yokosawa H 1993 High-molecular-weight protease complexes (proteasomes) of sperm of the ascidian, Halocynthia roretzi: isolation, characterization, and physiological roles in fertilization. Developmental Biology 158 238-244. (doi:10.1006/dbio.1993.1182)
64. Sakai N, Sawada H & Yokosawa H 2003 Extracellular ubiquitin system implicated in fertilization of the ascidian, Halocynthia roretzi: isolation and characterization. Developmental Biology 264 299-307. (doi:10.1016/j.ydbio.2003. 07.016)
65. Sakai N, Sawada MT & Sawada H 2004 Non-traditional roles of ubiquitin-proteasome system in fertilization and gametogenesis. International Journal of Biochemistry & Cell Biology 36 776-784. (doi:10.1016/S1357- 2725(03)00263-2)
66. Sanchez R, Deppe M, Schulz M, Bravo P, Villegas J, Morales P & Risopatron J 2011 Participation of the sperm proteasome during in vitro fertilisation and the acrosome reaction in cattle. Andrologia 43 114-120. (doi:10.1111/j.1439-0272.2009.01031.x)
67. Sawada H, Pinto MR & De Santis R 1998 Participation of sperm proteasome in fertilization of the phlebobranch ascidian Ciona intestinalis. Molecular Reproduction and Development 50 493-498. (doi:10.1002/(SICI)1098- 2795(199808)50:4〈493::AID-MRD13〉3.0.CO;2-3)
68. Sawada H, Sakai N, Abe Y, Tanaka E, Takahashi Y, Fujino J, Kodama E, Takizawa S & Yokosawa H 2002a Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. PNAS 99 1223-1228. (doi:10.1073/pnas.032389499)
69. Sawada H, Takahashi Y, Fujino J, Flores SY & Yokosawa H 2002b Localization and roles in fertilization of sperm proteasomes in the ascidian Halocynthia roretzi. Molecular Reproduction and Development 62 271-276. (doi:10.1002/mrd.10089)
70. Sekiguchi S, Kwon J, Yoshida E, Hamasaki H, Ichinose S, Hideshima M, Kuraoka M, Takahashi A, Ishii Y, Kyuwa S et al. 2006 Localization of ubiquitin C-terminal hydrolase L1 in mouse ova and its function in the plasma membrane to block polyspermy. American Journal of Pathology 169 1722-1729. (doi:10.2353/ajpath.2006.060301)
71. Stone M, Hartmann-Petersen R, Seeger M, Bech-Otschir D, Wallace M & Gordon C 2004 Uch2/Uch37 is the major deubiquitinating enzyme associated with the 26S proteasome in fission yeast. Journal of Molecular Biology 344 697-706. (doi:10.1016/j.jmb.2004.09.057)
72. Sun QY, Fuchimoto D & Nagai T 2004 Regulatory roles of ubiquitin-proteasome pathway in pig oocyte meiotic maturation and fertilization. Theriogenology 62 245-255. (doi:10.1016/j.theriogenology.2003.10.015)
73. Susor A, Liskova L, Toralova T, Pavlok A, Pivonkova K, Karabinova P, Lopatarova M, Sutovsky P & Kubelka M 2010 Role of ubiquitin C-terminal hydrolase-L1 in antipolyspermy defense of mammalian oocytes. Biology of Reproduction 82 1151-1161. (doi:10.1095/biolreprod.109.081547)
74. Sutovsky P 2009 Sperm-egg adhesion and fusion in mammals. Expert Reviews in Molecular Medicine 11 e11. (doi:10.1017/S1462399409001045)
75. Sutovsky P 2010 Fertilization. In Reproductive Endocrinology and Infertility: the Practical Clinic and Laboratory. Eds D Carrell & M Peterson. Totowa, NJ: The Humana Press.
76. Sutovsky P, McCauley TC, Sutovsky M & Day BN 2003 Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biology of Reproduction 68 1793-1800. (doi:10.1095/biolreprod.102.012799)
77. Sutovsky P, Manandhar G, McCauley TC, Caamano JN, Sutovsky M, Thompson WE & Day BN 2004 Proteasomal interference prevents zona pellucida penetration and fertilization in mammals. Biology of Reproduction 71 1625-1637. (doi:10.1095/biolreprod.104.032532)
78. Tanaka K 2009 The proteasome: overview of structure and functions. Proceedings of the Japan Academy. Series B, Physical and Biological Sciences 85 12-36. (doi:10.2183/pjab.85.12)
79. Tengowski MW, Feng D, Sutovsky M & Sutovsky P 2007 Differential expression of genes encoding constitutive and inducible 20S proteasomal core subunits in the testis and epididymis of theophylline- or 1,3- dinitrobenzene-exposed rats. Biology of Reproduction 76 149-163. (doi:10.1095/biolreprod.106.053173)
80. Tipler CP, Hutchon SP, Hendil K, Tanaka K, Fishel S & Mayer RJ 1997 Purification and characterization of 26S proteasomes from human and mouse spermatozoa. Molecular Human Reproduction 3 1053-1060. (doi:10.1093/molehr/3.12. 1053)
81. Voges D, Zwickl P & Baumeister W 1999 The 26S proteasome: a molecular machine designed for controlled proteolysis. Annual Review of Biochemistry 68 1015-1068. (doi:10.1146/annurev.biochem.68.1.1015)
82. Wang H, Song C, Duan C, Shi W, Li C, Chen D & Wang Y 2002 Effects of ubiquitin-proteasome pathway on mouse sperm capacitation, acrosome reaction and in vitro fertilization. Chinese Science Bulletin 47 127-132. (doi:10.1360/02tb9029)
83. Wilkinson CR, Ferrell K, Penney M, Wallace M, Dubiel W & Gordon C 2000 Analysis of a gene encoding Rpn10 of the fission yeast proteasome reveals that the polyubiquitin-binding site of this subunit is essential when Rpn12/Mts3 activity is compromised. Journal of Biological Chemistry 275 15182-15192. (doi:10.1074/jbc.275.20.15182)
84. Wing SS, Bedard N, Morales C, Hingamp P & Trasler J 1996 A novel rat homolog of the Saccharomyces cerevisiae ubiquitin-conjugating enzymes UBC4 and UBC5 with distinct biochemical features is induced during spermatogenesis. Molecular and Cellular Biology 16 4064-4072. (Pubitemid 26251205)
85. Yanagimachi R 1994 Mammalian fertilization. In The Physiology of Reproduction, 2nd edn, pp 189-317. Eds E Knobil & J Neill. New York: Raven Press.
86. Yanagimachi R 2009 Germ cell research: a personal perspective. Biology of Reproduction 80 204-218. (doi:10.1095/biolreprod.108.071993)
87. Yi YJ, Manandhar G, Oko RJ, Breed WG & Sutovsky P 2007a Mechanism of sperm-zona pellucida penetration during mammalian fertilization: 26S proteasome as a candidate egg coat lysin. Society of Reproduction and Fertility Supplement 63 385-408.
88. Yi YJ, Manandhar G, Sutovsky M, Li R, Jonakova V, Oko R, Park CS, Prather RS & Sutovsky P 2007b Ubiquitin C-terminal hydrolase-activity is involved in sperm acrosomal function and anti-polyspermy defense during porcine fertilization. Biology of Reproduction 77 780-793. (doi:10.1095/biolreprod.107. 061275)
89. Yi YJ, Manandhar G, Sutovsky M, Jonakova V, Park CS & Sutovsky P 2009a Inhibition of 19S proteasomal regulatory complex subunit PSMD8 increases polyspermy during porcine fertilization in vitro. Journal of Reproductive Immunology 84 154-163. (doi:10.1016/j.jri.2009.11.002)
90. Yi YJ, Park CS, Kim ES, Song ES, Jeong JH & Sutovsky P 2009b Spermsurface ATP in boar spermatozoa is required for fertilization: relevance to sperm proteasomal function. Systems Biology in Reproductive Medicine 55 85-96. (doi:10.1080/19396360802699074)
91. Yi YJ, Manandhar G, Sutovsky M, Zimmerman SW, Jonakova V, van Leeuwen FW, Oko R, Park CS & Sutovsky P 2010 Interference with the 19S proteasomal regulatory complex subunit PSMD4 on the sperm surface inhibits sperm-zona pellucida penetration during porcine fertilization. Cell and Tissue Research 341 325-340. (doi:10.1007/s00441-010-0988-2)
92. Yokota N & Sawada H 2007a Effects of proteasome inhibitors on fertilization of the sea urchin Anthocidaris crassispina. Biological & Pharmaceutical Bulletin 30 1332-1335. (doi:10.1248/bpb.30.1332)
93. Yokota N & Sawada H 2007b Sperm proteasomes are responsible for the acrosome reaction and sperm penetration of the vitelline envelope during fertilization of the sea urchin Pseudocentrotus depressus. Developmental Biology 308 222-231. (doi:10.1016/j.ydbio.2007.05.025)
94. Yokota N, Harada Y & Sawada H 2010 Identification of testis-specific ubiquitin-conjugating enzyme in the ascidian Ciona intestinalis. Molecular Reproduction and Development 77 640-647. (doi:10.1002/mrd.21198)
95. Young P, Deveraux Q, Beal RE, Pickart CM & Rechsteiner M 1998 Characterization of two polyubiquitin binding sites in the 26 S protease subunit 5a. Journal of Biological Chemistry 273 5461-5467. (doi:10.1074/jbc.273.10. 5461)
96. Zimmerman S & Sutovsky P 2009 The sperm proteasome during sperm capacitation and fertilization. Journal of Reproductive Immunology 83 19-25. (doi:10.1016/j.jri.2009.07.006)
97. Zimmerman SW, Manandhar G, Yi Y-J, Gupta SK, Sutovsky M, Odhiambo JF, Powell MD, Miller DJ & Sutovsky P 2011 Sperm proteasomes degrade sperm receptor on the egg zona pellucida during mammalian fertilization. PLoS ONE 6 e17256. (doi:10.1371/journal.pone.0017256)