Proteomic analysis of the reproductive tract fluids from tropically-adapted Santa Ines rams

Journal of Proteomics

Volumn 75, Issue 14, 2012, Pages 4436-4456

  Souza, Carlos Eduardo A ^a   Rego, João Paulo A ^a   Lobo, Carlos H ^a   Oliveira, José Tadeu A ^a   Nogueira, Fábio C S ^b   Domont, Gilberto B ^b   Fioramonte, Mariana ^c   Gozzo, Fabio C ^c   Moreno, Frederico B ^d   Monteiro Moreira, Ana Cristina O ^d   Figueiredo, José Ricardo ^e   Moura, Arlindo A ^a  

^a FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c UNIVERSITY OF CAMPINAS   (Brazil)

^d UNIVERSITY OF FORTALEZA   (Brazil)

^e STATE UNIVERSITY OF CEARÁ   (Brazil)

Author keywords

Binder of Sperm Protein; Ram; Seminal plasma; Sperm; Spermadhesin

Indexed keywords

ALBUMIN; ALPHA ENOLASE; BETA GALACTOSIDASE; BODHESIN 1; BODHESIN 2; CELL PROTEIN; CLUSTERIN; CYTOSOL AMINOPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE; GAMMA GLUTAMYL HYDROLASE; GELATINASE A; LACTOFERRIN; PEROXIREDOXIN; PROTEOME; TISSUE INHIBITOR OF METALLOPROTEINASE 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODHESIN 1 GENE; BODHESIN 2 GENE; BODY FLUID; EJACULATION; ELECTROPHORESIS; EPIDIDYMIS; EPIDIDYMIS TAIL; GENE; GENE EXPRESSION; GENE ONTOLOGY; GENETIC ANALYSIS; MALE; MALE GENITAL SYSTEM; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; RAM (SHEEP); SEMINAL PLASMA; SPERM; VESICULAR GLAND; WESTERN BLOTTING;

ACCLIMATIZATION; ANIMALS; BODY FLUIDS; EPIDIDYMIS; MALE; PROTEOME; SEMEN; SEMINAL VESICLES; SHEEP; TISSUE DISTRIBUTION; TROPICAL CLIMATE;

ANIMALIA;

EID: 84863828044     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.05.039     Document Type: Article

References (111)

1. Florman H.M., Ducibella T. Fertilization in mammals. Knobil and Neill's physiology of reproduction 2006, 55-112. Elsevier Inc., New York. 3rd ed. J.D. Neill, T.M. Plant, D.W. Pfaff, J.R.G. Challis, D.M. De Kretser, J.S. Richards (Eds.).
2. D'Amours O., Frenette G., Fortier M.A., Leclerc P., Sullivan R. Proteomic comparison of detergent-extracted sperm proteins from bulls with different fertility indexes. Reproduction 2010, 139:545-556.
3. Ward W.S. Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod 2010, 16:30-36.
4. Lalancette C., Miller D., Li Y., Krawetz S.A. Paternal contributions: new functional insights for spermatozoal RNA. J Cell Biochem 2008, 104:1570-1579.
5. Rodriguez-Martinez H., Kvist U., Ernerudh J., Sanz L., Calvete J.J. Seminal plasma proteins: what role do they play?. Am J Reprod Immunol 2011, 66:11-22.
6. Moura A.A., Chapman D.A., Killian G.J. Proteins of the accessory sex glands associated with the oocyte-penetrating capacity of cauda epididymal sperm from Holstein bulls of documented fertility. Mol Reprod Dev 2007, 74:214-222.
7. Killian G.J., Chapman D.A., Rogowski L.A. Fertility-associated proteins in Holstein bull seminal plasma. Biol Reprod 1993, 49:1202-1207.
8. McCauley T.C., Zhang H.M., Bellin M.E., Ax R.L. Identification of a heparin-binding protein in bovine seminal fluid as tissue inhibitor of metalloproteinases-2. Mol Reprod Dev 2001, 58:336-341.
9. Moura A.A., Chapman D.A., Koc H., Killian G.J. Proteins of the cauda epididymal fluid associated with fertility of mature dairy bulls. J Androl 2006, 27:534-541.
10. Moura A.A., Koc H., Chapman D.A., Killian G.J. Identification of proteins in the accessory sex gland fluid associated with fertility indexes of dairy bulls: a proteomic approach. J Androl 2006, 27:201-211.
11. Sousa W.H., Lobo R.N.B., Morais O.R. Ovinos Santa Inês: estado da arte e perspectivas. II Simpósio Internacional sobre Caprinos e Ovinos de Corte 2003, 7-19. EMEPA, João Pessoa.
12. Souza C.E.A., Araújo A.A., Oliveira J.T.A., Lima-Souza A.C.B., Neiva J.N.M., Moura A.A. Reproductive development of Santa Inês rams during the first year of life: body and testis growth, testosterone concentrations, sperm parameters, age at puberty and seminal plasma proteins. Reprod Domest Anim 2010, 45:644-653.
13. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
14. Candiano G., Bruschi M., Musante L., Santucci L., Ghiggeri G.M., Carnemolla B., et al. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 2004, 25:1327-1333.
15. Moura A.A., Souza C.E.A., Stanley B.A., Chapman D.A., Killian G.J. Proteomics of cauda epididymal fluid from mature Holstein bulls. J Proteomics 2010, 73:2006-2020.
16. Moura A.A., Chapman D.A., Koc H., Killian G.J. A comprehensive proteomic analysis of the accessory sex gland fluid from mature Holstein bulls. Anim Reprod Sci 2007, 98:169-188.
17. Rocha S.L.G., Neves-Ferreira A.G.C., Trugilho M.R.O., Chapeaurouge A., León I.R., Valente R.H., et al. Crotalid snake venom subproteomes unraveled by the antiophidic protein DM43. J Proteome Res 2009, 8:2351-2360.
18. Carvalho P.C., Junqueira M., Valente R.H., Domont G.B. Caititu: a tool to graphically represent peptide sequence coverage and domain distribution. J Proteomics 2008, 71:486-489.
19. Soares M.R., Facincani A.P., Ferreira R.M., Moreira L.M., Oliveira J.C.F., Ferro J.A., et al. Proteome of the phytopatogen Xanthomonas citri subsp. citri: a global expression profile. Proteome Sci 2010, 8:55.
20. Perkins D.N., Pappin D.J.C., Creasy D.M., Cottrell J.S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20:3551-3567.
21. Bathia V.N., Perlman D.H., Costello C.E., Mccomb M.E. Software tool for researching annotations of proteins: open-source protein annotation software with data visualization. Anal Chem 2009, 81:9819-9823.
22. Manjunath P., Sairam M.R. Purification and biochemical characterization of three major acidic proteins (BSP-A1, BSP-A2 and BSP-A3) from bovine seminal plasma. Biochem J 1987, 241:685-692.
23. Cardozo J.A., Fernández-Juan M., Cebrián-Pérez J.A., Muiño-Blanco T. Identification of RSVP14 and RSVP20 components by two-dimensional electrophoresis and western-blotting. Reprod Domest Anim 2008, 43:15-21.
24. Souza C.E.A., Moura A.A., Monaco E., Killian G.J. Binding patterns of bovine seminal plasma proteins A1/A2, 30kDa and osteopontin on ejaculated sperm before and after incubation with isthmic and ampullary oviductal fluid. Anim Reprod Sci 2008, 105:72-89.
25. 2 synthase in ram and stallion epididymal fluids: origin and regulation. Biol Reprod 1999, 60:558-566.
26. Melo L.M., Teixeira D.I.A., Havt A., Cunha R.M.S., Martins D.B.G., Castelletti C.H.M., et al. Buck (Capra hircus) genes encode new members of the spermadhesin family. Mol Reprod Dev 2008, 75:8-16.
27. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
28. Manjunath P., Lefebvre J., Jois P.S., Fan J., Wright M.W. New nomenclature for mammalian BSP genes. Biol Reprod 2009, 80:394-397.
29. Manjunath P., Chandonnet L., Leblond E., Desnoyers L. Major proteins of bovine seminal vesicles bind to spermatozoa. Biol Reprod 1994, 49:27-37.
30. Villemure M., Lazure C., Manjunath P. Isolation and characterization of gelatin-binding proteins from goat seminal plasma. Reprod Biol Endocrinol 2003, 1:39-48.
31. Boisvert M., Bergeron A., Lazure C., Manjunath P. Isolation and characterization of gelatin-binding bison seminal vesicle secretory proteins. Biol Reprod 2004, 70:656-661.
32. Lobo C.H., Martins J.A.M., Rego J.P., Silva G.M., Figueiredo J.R., Moura A.A. Expressão do gene da ram seminal vesicle protein 14kDa no trato reprodutivo de carneiros adultos da raça Morada Nova. 48a Reunião Anual da Sociedade Brasileira de Zootecnia 2011, 1-3. Sociedade Brasileira de Zootecnia, Belém-PA.
33. Lefebvre J., Fan J., Chevalier S., Sullivan R., Carmona E., Manjunath P. Genomic structure and tissue-specific expression of human and mouse genes encoding homologues of the major bovine seminal plasma proteins. Mol Hum Reprod 2007, 13:45-53.
34. Sankhala R.S., Swamy M.J. The major protein of bovine seminal plasma, PDC-109, is a molecular chaperone. Biochemistry 2010, 49:3908-3918.
35. Ménard M., Nauc V., Lazure C., Vaillancourt D., Manjunath P. Novel purification method for mammalian seminal plasma phospholipid-binding proteins reveals the presence of a novel member of this family of protein in stallion seminal fluid. Mol Reprod Dev 2003, 66:349-357.
36. Calvete J.J., Raida M., Gentzel M., Urbanke C., Sanz L., Topfer-Petersen E. Isolation and characterization of heparin- and phosphorylcholine-binding proteins of boar and stallion seminal plasma. Primary structure of porcine pB1. FEBS Lett 1997, 407:201-206.
37. Thérien I., Moreau R., Manjunath P. Major proteins of bovine seminal plasma and high-density lipoprotein induce cholesterol efflux from epididymal sperm. Biol Reprod 1998, 59:768-776.
38. Pérez-Pé R., Cebrián-Pérez J.A., Muiño-Blanco T. Semen plasma proteins prevent cold-shock membrane damage to ram spermatozoa. Theriogenology 2001, 56:425-434.
39. Gwathmey T.M., Ignotz G.G., Mueller J.L., Manjunath P., Suarez S.S. Bovine seminal plasma proteins PDC-109, BSP-A3, and BSP-30-kDa share functional roles in storing sperm in the oviduct. Biol Reprod 2006, 75:501-507.
40. Sahin E., Petrunkina A.M., Ekhlasi-Hundrieser M., Hettel C., Waberski D., Harrison R.A., et al. Fibronectin type II-module proteins in the bovine genital tract and their putative role in cell volume control during sperm maturation. Reprod Fertil Dev 2009, 21:479-488.
41. Martins J.A.M., Souza C.E.A., Silva F.D.A., Rego J.P., Cadavid V.G., Lobo C.H., et al. Partial proteome of native brazilian northeastern rams seminal plasma heparin-binding proteins. 36th annual meeting of the American Society of Andrology 2011, 89. American Society of Andrology, Montréal-QC.
42. Chandonnet L., Roberts K.D., Chapdelaine A., Manjunath P. Identification of heparin-binding proteins in bovine seminal plasma. Mol Reprod Dev 1990, 26:313-318.
43. Melo L.M., Nascimento A.S.F., Silveira F.G., Cunha R.M.S., Tavares N.A.C., Teixeira D.I.A., et al. Quantitative expression analysis of bodhesin genes in the buck (Capra hircus) reproductive tract by real-time polymerase chain reaction (qRT-PCR). Anim Reprod Sci 2009, 110:245-255.
44. Sanz L., Calvete J.J., Mann K., Schafer W., Schmid E.R., Amselgruber W., et al. The complete primary structure of the spermadhesin AWN, a zona pellucida-binding protein isolated from boar spermatozoa. FEBS Lett 1992, 300:213-218.
45. Topfer-Petersen E., Ekhlasi-Hundrieser M., Kirchhoff C., Leeb T., Sieme H. The role of stallion seminal proteins in fertilisation. Anim Reprod Sci 2005, 89:159-170.
46. Solís D., Romero A., Jiménez M., Díaz-Mauriño T., Calvete J.J. Binding of mannose-6-phosphate and heparin by boar seminal plasma PSP-II, a member of the spermadhesin protein family. FEBS Lett 1998, 431:273-278.
47. Dostàlovà Z., Calvete J.J., Sanz L., Topfer-Petersen E. Boar spermadhesin AWN-1: oligosaccharide and zona pellucida binding characteristics. Eur J Biochem 1995, 230:329-336.
48. Bork P., Beckmann G. The CUB domain: a widespread module in developmentally regulated proteins. J Mol Biol 1993, 231:539-545.
49. Topfer-Petersen E., Romero A., Varela P.F., Ekhlasi-Hundrieser M., Dostàlovà Z., Sanz L., et al. Spermadhesins: a new protein family. Facts, hypotheses and perspectives. Andrologia 1998, 30:217-224.
50. Talevi R., Gualtieri R. Molecules involved in sperm-oviduct adhesion and release. Theriogenology 2010, 73:796-801.
51. Bergeron A., Villemure M., Lazure C., Manjunath P. Isolation and characterization of the major proteins of ram seminal plasma. Mol Reprod Dev 2005, 71:461-470.
52. Roche M., Rondeau P., Singh N.R., Tarnus E., Bourdon E. The antioxidant properties of serum albumin. FEBS Lett 2008, 582:1783-1787.
53. Rhee S.G., Chae H.Z., Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med 2005, 38:1543-1552.
54. Drevet J.R. The antioxidant glutathione peroxidase family and spermatozoa: a complex story. Mol Cell Endocrinol 2006, 250:70-79.
55. Vernet P., Aitken R.J., Drevet J.R. Antioxidant strategies in the epididymis. Mol Cell Endocrinol 2004, 216:31-39.
56. Wakabayashi H., Matsumoto H., Hashimoto K., Teraguchi S., Takase M., Hayasawa H. Inhibition of iron/ascorbate induced lipid peroxidation by an N-terminal peptide of bovine lactoferrin and its acylated derivatives. Biosci Biotechnol Biochem 1999, 63:955-957.
57. Farnaud S., Evans R.W. Lactoferrin - a multifunctional protein with antimicrobial properties. Mol Immunol 2003, 40:395-405.
58. Bingle C.D., Craven C.J. PLUNC: a novel family of candidate host defence proteins expressed in the upper airways and nasopharynx. Hum Mol Genet 2002, 11:937-943.
59. Kirchhoff C., Osterhoff C., Young L. Molecular cloning and characterization of HE1, a major secretory protein of the human epididymis. Biol Reprod 1996, 54:847-856.
60. Manjunath P., Marcel Y.L., Uma J., Seidah N.G., Chrétien M., Chapdelaine A. Apolipoprotein A-1 binds to a family of bovine seminal plasma proteins. J Biol Chem 1989, 264:16853-16857.
61. Jha K.N., Shumilin I.A., Digilio L.C., Chertihin O., Zheng H., Schmitz G., et al. Biochemical and structural characterization of apolipoprotein A-1 binding protein, a novel phosphoprotein with a potential role in sperm capacitation. Endocrinology 2008, 149:2108-2120.
62. Beere H.M. 'The stress of dying': the role of heat shock proteins in the regulation of apoptosis. J Cell Sci 2004, 117:2641-2651.
63. Signorelli J., Diaz E.S., Morales P. Kinases, phosphatases and proteases during sperm capacitation. Cell Tissue Res Mar 20 2012, [Electronic publication ahead of print]. 10.1007/s00441-012-1370-3.
64. Fàbrega A., Guyonnet B., Dacheux J.L., Gatti J.L., Puigmulé M., Bonet S., et al. Expression, immunolocalization and processing of fertilins ADAM-1 and ADAM-2 in the boar (Sus domesticus) spermatozoa during epididymal maturation. Reprod Biol Endocrinol 2011, 9:96.
65. Barrett A.J., Kirschke H. Cystatin, the egg white inhibitor of cysteine proteinases. Methods Enzymol 1981, 80:771-778.
66. Igdoura S.A., Morales C.R., Hermo L. Differential expression of cathepsins B and D in testis and epididymis of adult rats. J Histochem Cytochem 1995, 43:545-557.
67. Tomomasa H., Waguri S., Umeda T., Koiso K., Kominami E., Uchiyama Y. Lysosomal cysteine proteinases in rat epididymis. J Histochem Cytochem 1994, 42:417-425.
68. Dalet-Fumeron V., Guinec N., Pagano M. In vitro activation of pro-cathepsin B by three serine proteinases: leucocyte elastase, cathepsin G, and the urokinase-type plasminogen-activator. FEBS Lett 1993, 332:251-254.
69. Carlsson L., Ronquist G., Ronquist G., Eliasson R., Egberg N., Larsson A. Association of cystatin C with prostasomes in human seminal plasma. Int J Androl 2011, 34:363-368.
70. Peloille S., Esnard A., Dacheux J.L., Guillou F., Gauthier F., Esnard F. Interactions between ovine cathepsin L, cystatin C and α2-macroglobulin - potential role in the genital tract. Eur J Biochem 1997, 244:140-146.
71. Thimon V., Métayer S., Belghazi M., Dacheux F., Dacheux J.L., Gatti J.L. Shedding of the germinal angiotensin I-converting enzyme (gACE) involves a serine protease and is activated by epididymal fluid. Biol Reprod 2005, 73:881-890.
72. Yamaguchi R., Yamagata K., Ikawa M., Moss S.B., Okabe M. Aberrant distribution of ADAM3 in sperm from both angiotensin-converting enzyme (Ace)- and calmegin (Clgn)-deficient mice. Biol Reprod 2006, 75:760-766.
73. Kohn F.M., Muller C., Drescher D., Neukamm C., El Mulla K.F., Henkel R., et al. Effect of angiotensin converting enzyme (ACE) and angiotensins on human sperm functions. Andrologia 1998, 30:207-215.
74. Hagaman J.R., Moyer J.S., Bachman E.S., Sibony M., Magyar P.L., Welch J.E., et al. Angiotensin-converting enzyme and male fertility. Proc Natl Acad Sci U S A 1998, 95:2552-2557.
75. Baumgart E., Lenk S.V., Loening S.A., Jung K. Quantitative differences in matrix metalloproteinase (MMP)-2, but not in MMP-9, tissue inhibitor of metalloproteinase (TIMP)-1 or TIMP-2, in seminal plasma of normozoospermic and azoospermic patients. Hum Reprod 2002, 17:2919-2923.
76. Métayer S., Dacheux F., Dacheux J.L., Gatti J.L. Comparison, characterization, and identification of proteases and protease inhibitors in epididymal fluids of domestic mammals. Matrix metalloproteinases are major fluid gelatinases. Biol Reprod 2002, 66:1219-1229.
77. Hedrich J., Lottaz D., Meyer K., Yiallouros I., Jahnen-Dechent W., Stocker W., et al. Fetuin-A and Cystatin C are endogenous inhibitors of human meprin metalloproteases. Biochemistry 2010, 49:8599-8607.
78. Yasuda T., Takeshita H., Tsubota E., Sawazaki K., Iida R., Nadano D., et al. Alpha-2-HS-glycoprotein (AHSG) polymorphism in semen and saliva. Electrophoresis 1996, 17:793-796.
79. Stefan N., Hennige A.M., Staiger H., Machann J., Schick F., Krober S.M., et al. α2-Heremans-Schmid glycoprotein/fetuin A is associated with insulin resistance and fat accumulation in the liver in humans. Diabetes Care 2006, 29:853-857.
80. Voros K., Graf L., Prohaszka Z., Graf L., Szenthe P., Kaszas E., et al. Serum fetuin-A in metabolic and inflammatory pathways in patients with myocardial infarction. Eur J Clin Invest 2011, 41:703-709.
81. Sakwe A.M., Koumangoye R., Goodwin S.J., Ochieng J. Fetuin-A (α2HS-glycoprotein) is a major serum adhesive protein that mediates growth signaling in breast tumor cells. J Biol Chem 2010, 285:41827-41835.
82. Pillai S., Rust P.F., Howard L. Effects of antibodies to transferrin and alpha 2-HS glycoprotein on in vitro sperm motion: implications in infertility associated with endometriosis. Am J Reprod Immunol 1998, 39:235-242.
83. Togo T., Morisawa M. GPI-anchored aminopeptidase is involved in the acrosome reaction in sperm of the mussel mytilusedulis. Mol Reprod Dev 2004, 67:465-471.
84. Tantibhedhyangkul J., Weerachatyanukul W., Carmona E., Xu H., Anupriwan A., Michaud D., et al. Role of sperm surface arylsulfatase A in mouse sperm-zona pellucida binding. Biol Reprod 2002, 67:212-219.
85. Tulsiani D.R.P. Glycan modifying enzymes in luminal fluid of rat epididymis: are they involved in altering sperm surface glycoproteins during maturation?. Microsc Res Tech 2003, 61:18-27.
86. Miranda P.V., Gonzalez-Echeverría F., Marín-Briggiler C.I., Brandelli A., Blaquier J.A., Tezón J.G. Glycosidic residues involved in human sperm-zona pellucida binding in vitro. Mol Hum Reprod 1997, 3:399-404.
87. Frenette G., Lessard C., Sullivan R. Polyol pathway along the bovine epididymis. Mol Reprod Dev 2004, 69:448-456.
88. Manásková P., Liberda J., Tichá M., Jonáková V. Isolation of non-heparin-binding and heparin-binding proteins of boar prostate. J Chromatogr B 2002, 770:137-143.
89. Kikuchi M., Mizoroki S., Kubo T., Ohiwa Y., Kubota M., Yamada N., et al. Seminal plasma lactoferrin but not transferrin reflects gonadal function in dogs. J Vet Med Sci 2003, 65:679-684.
90. Souza C.E.A., Moura A.A., Lima-Souza A.C.B., Killian G.J. Binding patterns of seminal plasma proteins on bovine epididymal and ejaculated sperm membrane. Arq Bras Med Vet Zoot 2011, 63:535-543.
91. Leone M.G., Haq H.A., Saso L. Lipocalin type prostaglandin D-synthase: which role in male fertility?. Contraception 2002, 65:293-295.
92. Yin H.L., Kwiatkowski D.J., Mole J.E., Cole F.S. Structure and biosynthesis of cytoplasmic and secreted variants of gelsolin. J Biol Chem 1984, 259:5271-5276.
93. Lee W.M., Galbraith R.M. The extracellular actin-scavenger system and actin toxicity. N Engl J Med 1992, 326:1335-1341.
94. Kjarland E., Keen T.J., Kleppe R. Does isoform diversity explain functional differences in the 14-3-3 protein family?. Curr Pharm Biotechnol 2006, 7:217-223.
95. Huang Z., Myers K., Khatra B., Vijayaraghavan S. Protein 14-3-3ζ binds to protein phosphatase PP1γ2 in bovine epididymal spermatozoa. Biol Reprod 2004, 71:177-184.
96. Sun S., Wong E.W.P., Li M.W.M., Lee W.M., Cheng C.Y. 14-3-3 and its binding partners are regulators of protein-protein interactions during spermatogenesis. J Endocrinol 2009, 202:327-336.
97. Shankardas J., Senchyna M., Dimitrijevich S.D. Presence and distribution of 14-3-3 proteins in human ocular surface tissues. Mol Vis 2008, 14:2604-2615.
98. Bochtler M., Ditzel L., Groll M., Hartmann C., Huber R. The proteasome. Annu Rev Biophys Biomol Struct 1999, 28:295-317.
99. Sixt S.U., Dahlmann B. Extracellular, circulating proteasomes and ubiquitin - incidence and relevance. Biochim Biophys Acta, Mol Basis Dis 2008, 1782:817-823.
100. Hershko A., Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998, 67:425-479.
101. Osaki A., Okida N., Ishikawa K., Tokumoto M., Nagahama Y., Lippert T.H., et al. Identification of ubiquitin in seminal plasma from tilapia, Oreochromis niloticus. Biomed Res 1999, 20:249-252.
102. Lippert T.H., Seeger H., Schieferstein G., Voelter W. Immunoreactive ubiquitin in human seminal plasma. J Androl 1993, 14:130-131.
103. Fraile B., Martin R., De Miguel M.P., Arenas M.I., Bethencourt F.R., Peinado F., et al. Light and electron microscopic immunohistochemical localization of protein gene product 9.5 and ubiquitin immunoreactivities in the human epididymis and vas deferens. Biol Reprod 1996, 55:291-297.
104. Hermo L., Jacks D. Nature's ingenuity: bypassing the classical secretory route via apocrine secretion. Mol Reprod Dev 2002, 63:394-410.
105. Sutovsky P. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone. Microsc Res Tech 2003, 61:88-102.
106. Kwon J., Wang Y.L., Setsuie R., Sekiguchi S., Sato Y., Sakurai M., et al. Two closely related ubiquitin C-terminal hydrolase isoenzymes function as reciprocal modulators of germ cell apoptosis in cryptorchid testis. Am J Pathol 2004, 165:1367-1374.
107. Yi Y.J., Manandhar G., Sutovsky M., Li R., Jonáková V., Oko R., et al. Ubiquitin C-terminal hydrolase-activity is involved in sperm acrosomal function and anti-polyspermy defense during porcine fertilization. Biol Reprod 2007, 77:780-793.
108. Bohring C., Krause E., Habermann B., Krause W. Isolation and identification of sperm membrane antigens recognized by antisperm antibodies, and their possible role in immunological infertility disease. Mol Hum Reprod 2001, 7:113-118.
109. Morales P., Díaz E.S., Kong M. Proteasome activity and its relationship with protein phosphorylation during capacitation and acrosome reaction in human spermatozoa. Soc Reprod Fertil Suppl 2007, 65:269-273.
110. Sutovsky P., Manandhar G., McCauley T.C., Caamano J.N., Sutovsky M., Thompson W.E. Proteasomal interference prevents zona pellucida penetration and fertilization in mammals. Biol Reprod 2004, 71:1625-1637.
111. Sutovsky P., Moreno R., Ramalho-Santos J., Dominko T., Thompson W.E., Schatten G. A putative, ubiquitin-dependent mechanism for the recognition and elimination of defective spermatozoa in the mammalian epididymis. J Cell Sci 2001, 114:1665-1675.