Seminal plasma proteome of electroejaculated Bos indicus bulls

Animal Reproduction Science

Volumn 148, Issue 1-2, 2014, Pages 1-17

  Rego, J P A ^a   Crisp, J M ^b   Moura, A A ^a   Nouwens, A S ^b   Li, Y ^c   Venus, B ^d   Corbet, N J ^d   Corbet, D H ^d   Burns, B M ^b   Boe Hansen, G B ^b   McGowan, M R ^b  

^a FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c CSIRO   (Australia)

^d DEPARTMENT OF AGRICULTURE AND FISHERIES   (Australia)

Author keywords

Bos indicus; Electrophoresis; Proteome; Seminal plasma; Sperm

Indexed keywords

PROTEOME; SEMINAL PLASMA PROTEIN;

ANIMAL; BOVINE; CHEMISTRY; EJACULATION; ELECTROSTIMULATION; MALE; PHYSIOLOGY; SPERM;

ANIMALS; CATTLE; EJACULATION; ELECTRIC STIMULATION; MALE; PROTEOME; SEMEN; SEMINAL PLASMA PROTEINS;

EID: 84903555929     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2014.04.016     Document Type: Article

References (169)

1. Abascal I., Skalaban S.R., Grimm K.M., Aviles M., Martinez-Menarguez J.A., Castells M.T., Ballesta J., Alhadeff J.A. Alteration of the isoform composition of plasma-membrane-associated rat sperm alpha-l-fucosidase during late epididymal maturation: comparative characterization of the acidic and neutral isoforms. Biochem. J. 1998, 333:201-207.
2. Abbasihormozi S., Shahverdi A., Kouhkan A., Cheraghi J., Akhlaghi A.A., Kheimeh A. Relationship of leptin administration with production of reactive oxygen species, sperm DNA fragmentation, sperm parameters and hormone profile in the adult rat. Arch. Gynecol. Obstet. 2012, 287(6):1241-1249.
3. Achilli A., Olivieri A., Pellecchia M., Uboldi C., Colli L., Al-Zahery N., Accetturo M., Pala M., Hooshiar Kashani B., Perego U.A., Battaglia V., Fornarino S., Kalamati J., Houshmand M., Negrini R., Semino O., Richards M., Macaulay V., Ferretti L., Bandelt H.J., Ajmone-Marsan P., Torroni A. Mitochondrial genomes of extinct aurochs survive in domestic cattle. Curr. Biol. 2008, 18:R157-R158.
4. Agarwal A., Prabakaran S.A., Said T.M. Prevention of oxidative stress injury to sperm. J. Androl. 2005, 26:654-660.
5. Alvarez J.G., Storey B.T. Differential incorporation of fatty-acids into and peroxidative loss of fatty-acids from phospholipids of human spermatozoa. Mol. Reprod. Dev. 1995, 42:334-346.
6. Alves Teixeira D.I., Melo L.M., de Almeida Gadelha C.A., Silva da Cunha R.M., Bloch C., Radis-Baptista G., Cavada B.S., de Figueiredo Freitas V.J. Ion-exchange chromatography used to isolate a spermadhesin-related protein from domestic goat (Capra hircus) seminal plasma. Genetics Mol. Res. 2006, 5:79-87.
7. Angst B.D., Marcozzi C., Magee A.I. The cadherin superfamily. J. Cell Sci. 2001, 114:625-626.
8. Armstrong J.S., Rajasekaran M., Hellstrom W.J., Sikka S.C. Antioxidant potential of human serum albumin: role in the recovery of high quality human spermatozoa for assisted reproductive technology. J. Androl. 1998, 19:412-419.
9. Arruda-Alencar J.M., Viana Neto A.M.V., Souza C.E.A., Martins J.A.M., Moreno F.B., Moreira A.C.O., Guerreiro M.E.F., Moura A.A.N.A. Major proteins of the seminal plasma of New Zealand white rabbits and association with semen criteria. 10th World Rabbit Congress 2012.
10. Assumpcao T.I., Fontes W., Sousa M.V., Ricart C.A. Proteome analysis of Nelore bull (Bos taurus indicus) seminal plasma. Protein Peptide Lett. 2005, 12:813-817.
11. Bals R., Wilson J.M. Cathelicidins - a family of multifunctional antimicrobial peptides. Cell. Mol. Life Sci. 2003, 60:711-720.
12. Barrett A.J. Cystatin, the egg-white inhibitor of cysteine proteinases. Methods Enzymol. 1981, 80:771-778.
13. Belleannee C., Labas V., Teixeira-Gomes A.-P., Gatti J.L., Dacheux J.-L., Dacheux F. Identification of luminal and secreted proteins in bull epididymis. J. Proteom. 2011, 74:59-78.
14. Benzaquen L.R., Nicholson-Weller A., Halperin J.A. Terminal complement proteins C5b-9 release basic fibroblast growth factor and platelet-derived growth factor from endothelial cells. J. Exp. Med. 1994, 179:985-992.
15. 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.
16. Bhatia 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.
17. 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.
18. Bortolussi G., McIvor J.G., Hodgkinson J.J., Coffey S.G., Holmes C.R. The northern Australian beef industry, a snapshot. 2. Breeding herd performance and management. Aust. J. Exp. Agric. 2005, 45:1075-1091.
19. Bradford M.M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
20. Bradley D.T., Zipfel P.F., Hughes A.E. Complement in age-related macular degeneration: a focus on function. Eye (Lond., Engl.) 2011, 25:683-693.
21. Brandtzaeg P., Prydz H. Direct evidence for an integrated function of J chain and secretory component in epithelial transport of immunoglobulins. Nature 1984, 311:71-73.
22. Breitbart H., Cohen G., Rubinstein S. Role of actin cytoskeleton in mammalian sperm capacitation and the acrosome reaction. Reproduction (Cambridge, Engl.) 2005, 129:263-268.
23. Burns B.M., Corbet N.J., Corbet D.H., Crisp J.M., Venus B.K., Johnston D.J., Li Y., McGowan M.R., Holroyd R.G. Male traits and herd reproductive capability in tropical beef cattle. 1. Experimental design and animal measures. Anim. Prod. Sci. 2013, 53:87-100.
24. Buttyan R., Olsson C.A., Pintar J., Chang C.S., Bandyk M., Ng P.Y., Sawczuk I.S. Induction of the TRPM-2 gene in cells undergoing programmed death. Mol. Cell. Biol. 1989, 9:3473-3481.
25. Byrne K., Leahy T., McCulloch R., Colgrave M.L., Holland M.K. Comprehensive mapping of the bull sperm surface proteome. Proteomics 2012, 12:3559-3579.
26. Calvete J.J., Raida M., Gentzel M., Urbanke C., Sanz L., TopferPetersen E. Elation 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.
27. Cancel A.M., Chapman D.A., Killian G.J. Osteopontin is the 55-kilodalton fertility-associated protein in Holstein bull seminal plasma. Biol. Reprod. 1997, 57:1293-1301.
28. Candiano G., Bruschi M., Musante L., Santucci L., Ghiggeri G.M., Carnemolla B., Orecchia P., Zardi L., Righetti P.G. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 2004, 25:1327-1333.
29. Chard T., Parslow J., Rehmann T., Dawnay A. The concentrations of transferrin, beta-2-microglobulin, and albumin in seminal plasma in relation to sperm count. Fertil. Steril. 1991, 55:211-213.
30. Choi N.H., Mazda T., Tomita M. A serum-protein sp40,40 modulates the formation of membrane attack complex of complement on erythrocytes. Mol. Immunol. 1989, 26:835-840.
31. Christmas P., Callaway J., Fallon J., Jones J., Haigler H.T. Selective secretion of annexin 1, a protein without a signal sequence, by the human prostate gland. J. Biol. Chem. 1991, 266:2499-2507.
32. Corbet N.J., Burns B.M., Johnston D.J., Wolcott M.L., Corbet D.H., Venus B.K., Li Y., McGowan M.R., Holroyd R.G. Male traits and herd reproductive capability in tropical beef cattle. 2. Genetic parameters of bull traits. Anim. Prod. Sci. 2013, 53:101-113.
33. 2+-dependent metalloprotease in mammalian gamete membrane fusion. Dev. Biol. 2000, 225:124-134.
34. Coulthard M.G., Morgan M., Woodruff T.M., Arumugam T.V., Taylor S.M., Carpenter T.C., Lackmann M., Boyd A.W. Eph/Ephrin signaling in injury and inflammation. Am. J. Pathol. 2012, 181:1493-1503.
35. Cunningham K.A., Carey A.J., Finnie J.M., Bao S., Coon C., Jones R., Wijburg O., Strugnell R.A., Timms P., Beagley K.W. Poly-immunoglobulin receptor-mediated transport of IgA into the male genital tract is important for clearance of Chlamydia muridarum infection. Am. J. Reprod. Immunol. (New York, N.Y.: 1989) 2008, 60:405-414.
36. D'Amours O., Frenette G., Fortier M., Leclerc P., Sullivan R. Proteomic comparison of detergent-extracted sperm proteins from bulls with different fertility indexes. Reproduction (Cambridge, Engl.) 2010, 139:545-556.
37. Dacheux J.L., Gatti J.L., Dacheux F. Contribution of epididymal secretory proteins for spermatozoa maturation. Microsc. Res. Tech. 2003, 61:7-17.
38. Danshina P.V., Geyer C.B., Dai Q., Goulding E.H., Willis W.D., Kitto G.B., McCarrey J.R., Eddy E.M., O'Brien D.A. Phosphoglycerate kinase 2 (PGK2) is essential for sperm function and male fertility in mice. Biol. Reprod. 2010, 82:136-145.
39. Davalieva K., Kiprijanovska S., Noveski P., Plaseski T., Kocevska B., Broussard C., Plaseska-Karanfilska D. Proteomic analysis of seminal plasma in men with different spermatogenic impairment. Andrologia 2012, 44:256-264.
40. Davrinche C., Abbal M., Clerc A. Molecular characterization of human complement factor B subtypes. Immunogenetics 1990, 32:309-312.
41. de Mateo S., Castillo J., Estanyol J.M., Ballesca J.L., Oliva R. Proteomic characterization of the human sperm nucleus. Proteomics 2011, 11:2714-2726.
42. De Paul A.L., Bonaterra M., Soler A.P., Knudsen K.A., Roth F.D., Aoki A. Soluble p-cadherin found in human semen. J. Androl. 2005, 26:44-47.
43. Denhardt D.T. The third international conference on osteopontin and related proteins, San Antonio, Texas, May 10-12, 2002. Calcif. Tissue Int. 2004, 74:213-219.
44. Desnoyers L., Manjunath P. Major proteins of bovine seminal plasma exhibit novel interactions with phospholipid. J. Biol. Chem. 1992, 267:10149-10155.
45. Ding Z., Qu F., Guo W., Ying X., Wu M., Zhang Y. Identification of sperm forward motility-related proteins in human seminal plasma. Mol. Reprod. Dev. 2007, 74:1124-1131.
46. Dostalova Z., Calvete J.J., Sanz L., Hettel C., Riedel D., Schoneck C., Einspanier R., Topfer-Petersen E. Immunolocalization and quantitation of acidic seminal fluid protein (aSFP) in ejaculated, swim-up, and capacitated bull spermatozoa. Biol. Chem. Hoppe-Seyler 1994, 375:457-461.
47. Drevet J.R. The antioxidant glutathione peroxidase family and spermatozoa: a complex story. Mol. Cell. Endocrinol. 2006, 250:70-79.
48. Druart X., Rickard J.P., Mactier S., Kohnke P.L., Kershaw-Young C.M., Bathgate R., Gibb Z., Crossett B., Tsikis G., Labas V., Harichaux G., Grupen C.G., de Graaf S.P. Proteomic characterization and cross species comparison of mammalian seminal plasma. J. Proteom. 2013, 91C:13-22.
49. Dube E., Chan P.T., Hermo L., Cyr D.G. Gene expression profiling and its relevance to the blood-epididymal barrier in the human epididymis. Biol. Reprod. 2007, 76:1034-1044.
50. Eddy E.M., Toshimori K., O'Brien D.A. Fibrous sheath of mammalian spermatozoa. Microsc. Res. Tech. 2003, 61:103-115.
51. Elsbach P., Weiss J. Oxygen-independent Antimicrobial Systems of Phagocytes 1992.
52. Evans J.P. The molecular basis of sperm-oocyte membrane interactions during mammalian fertilization. Hum. Reprod. Update 2002, 8:297-311.
53. Fellous M., Colle A., Tonnelle C. Expression of human beta2-microglobulin on human spermatozoa. Eur. J. Immunol. 1976, 6:21-24.
54. Fink E., Schill W.B., Miska W., Krassnigg F., Niederhauser H., Fink E., Frick J., Schill W.B. Kinin-containing kininogen is present in human seminal plasma. Angiotensin converting enzyme in human seminal plasma is synthesized by the testis, epididymis and prostate. Adv. Exp. Med. Biol. 1989, 247B:311-315.
55. Fitzpatrick L.A., Fordyce G., McGowan M.R., Bertram J.D., Doogan V.J., De Faveri J., Miller R.G., Holroyd R.G. Bull selection and use in northern Australia. Part 2. Semen traits. Anim. Reprod. Sci. 2002, 71:39-49.
56. Fordyce G., Entwistle K., Norman S., Perry V., Gardiner B., Fordyce P. Standardising bull breeding soundness evaluations and reporting in Australia. Theriogenology 2006, 66:1140-1148.
57. Fouchecourt S., Dacheux F., Dacheux J.L. Glutathione-independent prostaglandin D-2 synthase in ram and stallion epididymal fluids: origin and regulation. Biol. Reprod. 1999, 60:558-566.
58. Fouquet J.P., Kann M.L. Species-specific localization of actin in mammalian spermatozoa - fact or artifact. Microsc. Res. Tech. 1992, 20:251-258.
59. Franzen A., Heinegard D. Isolation and characterization of 2 sialoproteins present only in bone calcified matrix. Biochem. J. 1985, 232:715-724.
60. Fu Y., Fu J., Ren Q., Chen X., Wang A. Expression of Eph A molecules during swine embryo implantation. Mol. Biol. Rep. 2012, 39:2179-2185.
61. Fujiwara H., Yoshioka S., Tatsumi K., Kosaka K., Satoh Y., Nishioka Y., Egawa M., Higuchi T., Fujii S. Human endometrial epithelial cells express ephrin A1: possible interaction between human blastocysts and endometrium via Eph-ephrin system. J. Clin. Endocrinol. Metab. 2002, 87:5801-5807.
62. Gerena R.L., Irikura D., Urade Y., Eguchi N., Chapman D.A., Killian G.J. Identification of a fertility-associated protein in bull seminal plasma as lipocalin-type prostaglandin D synthase. Biol. Reprod. 1998, 58:826-833.
63. Go K.J., Wolf D.P. Albumin-mediated changes in sperm sterol content during capacitation. Biol. Reprod. 1985, 32:145-153.
64. Goncalves R.F., Staros A.L., Killian G.J. Oviductal fluid proteins associated with the bovine zona pellucida and the effect on in vitro sperm-egg binding, fertilization and embryo development. Reprod. Domest Anim. 2008, 43:720-729.
65. Goncalves R.F., Wolinetz C.D., Killian G.J. Influence of arginine-glycine-aspartic acid (RGD), integrins (alphaV and alpha5) and osteopontin on bovine sperm-egg binding, and fertilization in vitro. Theriogenology 2007, 67:468-474.
66. 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.
67. Hao Y., Murphy C.N., Spate L., Wax D., Zhong Z., Samuel M., Mathialagan N., Schatten H., Prather R.S. Osteopontin improves in vitro development of porcine embryos and decreases apoptosis. Mol. Reprod. Dev. 2008, 75:291-298.
68. Hassan M.I., Waheed A., Yadav S., Singh T.P., Ahmad F. Zinc alpha 2-glycoprotein: a multidisciplinary protein. Mol. Cancer Res. 2008, 6:892-906.
69. Holmes S.D., Lipshultz L.I., Smith R.G. Transferrin and gonadal dysfunction in man. Fertil. Steril. 1982, 38:600-604.
70. Hooper L.V., Stappenbeck T.S., Hong C.V., Gordon J.I. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat. Immunol. 2003, 4:269-273.
71. Hough S.R., Parks J.E. Platelet-activating-factor acetylhydrolase activity in seminal plasma from the bull, stallion, rabbit, and rooster. Biol. Reprod. 1994, 50:912-916.
72. Humphreys D.T., Carver J.A., Easterbrook-Smith S.B., Wilson M.R. Clusterin has chaperone-like activity similar to that of small heat shock proteins. J. Biol. Chem. 1999, 274:6875-6881.
73. Ignotz G.G., Cho M.Y., Suarez S.S. Annexins are candidate oviductal receptors for bovine sperm surface proteins and thus may serve to hold bovine sperm in the oviductal reservoir. Biol. Reprod. 2007, 77:906-913.
74. Ishitsuka R., Kojima K., Utsumi H., Ogawa H., Matsumoto I. Glycosaminoglycan binding properties of annexin IV, V, and VI. J. Biol. Chem. 1998, 273:9935-9941.
75. Ivanov A.I., Romanovsky A.A. Putative dual role of ephrin-Eph receptor interactions in inflammation. IUBMB Life 2006, 58:389-394.
76. Jarvi K., Langlais J., Gagnon C., Roberts K.D. Platelet-activating-factor acetylhydrolase in the male reproductive-tract - origin and properties. Int. J. Androl. 1993, 16:121-127.
77. Jha K.N., Shumilin I.A., Digilio L.C., Chertihin O., Zheng H., Schmitz G., Visconti P.E., Flickinger C.J., Minor W., Herr J.C. Biochemical and structural characterization of apolipoprotein A-I binding protein, a novel phosphoprotein with a potential role in sperm capacitation. Endocrinology 2008, 149:2108-2120.
78. Jobim M.I., Oberst E.R., Salbego C.G., Souza D.O., Wald V.B., Tramontina F., Mattos R.C. Two-dimensional polyacrylamide gel electrophoresis of bovine seminal plasma proteins and their relation with semen freezability. Theriogenology 2004, 61:255-266.
79. Johnston D.J., Barwick S.A., Corbet N.J., Fordyce G., Holroyd R.G., Williams P.J., Burrow H.M. Genetics of heifer puberty in two tropical beef genotypes in northern Australia and associations with heifer- and steer-production traits. Anim. Prod. Sci. 2009, 49:399-412.
80. Kaetzel C.S. The polymeric immunoglobulin receptor. eLS 2013, John Wiley & Sons, Ltd, Chichester.
81. Kamaruddin M., Kroetsch T., Basrur P.K., Hansen P.J., King W.A. Immunolocalization of heat shock protein 70 in bovine spermatozoa. Andrologia 2004, 36:327-334.
82. Kappler U., Nouwens A.S. The molybdoproteome of Starkeya novella - insights into the diversity and functions of molybdenum containing proteins in response to changing growth conditions. Metallomics: Integr. Biometal Sci. 2013, 5(4):325-334.
83. Kelly V.C., Kuy S., Palmer D.J., Xu Z., Davis S.R., Cooper G.J. Characterization of bovine seminal plasma by proteomics. Proteomics 2006, 6:5826-5833.
84. Kerkhoff C., Klempt M., Sorg C. Novel insights into structure and function of MRP8 (S100A8) and MRP14 (S100A9). Biochim. Biophys. Acta 1998, 1448:200-211.
85. Killian G.J., Chapman D.A., Rogowski L.A. Fertility-associated proteins in Holstein bull seminal plasma. Biol. Reprod. 1993, 49:1202-1207.
86. Kimura K., Asami K., Yamamoto M. Effect of heat shock treatment on the production of variant testosterone-repressed prostate message-2 (TRPM-2) mRNA in culture cells. Cell Biochem. Funct. 1997, 15:251-257.
87. Kirchhoff C., Osterhoff C., Pera I., Schroter S. Function of human epididymal proteins in sperm maturation. Andrologia 1998, 30:225-232.
88. Koga K., Osuga Y., Tsutsumi O., Momoeda M., Suenaga A., Kugu K., Fujiwara T., Takai Y., Yano T., Taketani Y. Evidence for the presence of angiogenin in human follicular fluid and the up-regulation of its production by human chorionic gonadotropin and hypoxia. J. Clin. Endocrinol. Metab. 2000, 85:3352-3355.
89. Koga K., Osuga Y., Tsutsumi O., Yano T., Yoshino O., Takai Y., Matsumi H., Hiroi H., Kugu K., Momoeda M., Fujiwara T., Taketani Y. Demonstration of angiogenin in human endometrium and its enhanced expression in endometrial tissues in the secretory phase and the decidua. J. Clin. Endocrinol. Metab. 2001, 86:5609-5614.
90. Koga K., Osuga Y., Yano T., Ikezuki Y., Yoshino O., Hirota Y., Hirata T., Horie S., Ayabe T., Tsutsumi O., Taketani Y. Evidence for the presence of angiogenin in human testis. J. Androl. 2004, 25:369-374.
91. Konczol K., Bodnar I., Zelena D., Pinter O., Papp R.S., Palkovits M., Nagy G.M., Toth Z.E. Nesfatin-1/NUCB2 may participate in the activation of the hypothalamic-pituitary-adrenal axis in rats. Neurochem. Int. 2010, 57:189-197.
92. Kraus M., Ticha M., Zelezna B., Peknicova J., Jonakova V. Characterization of human seminal plasma proteins homologous to boar AQN spermadhesins. J. Reprod. Immunol. 2005, 65:33-46.
93. Laki K. The action of thrombin on fibrinogen. Science (New York, N.Y.) 1951, 114:435-436.
94. Lev N., Ickowicz D., Barhum Y., Lev S., Melamed E., Offen D. DJ-1 protects against dopamine toxicity. J. Neural Transm. (Vienna, Austria: 1996) 2009, 116:151-160.
95. Lindquist S., Craig E.A. The heat-shock proteins. Annu. Rev. Genet. 1988, 22:631-677.
96. Luedtke C.C., McKee M.D., Cyr D.G., Gregory M., Kaartinen M.T., Mui J., Hermo L. Osteopontin expression and regulation in the testis, efferent ducts, and epididymis of rats during postnatal development through to adulthood. Biol. Reprod. 2002, 66:1437-1448.
97. Malm J., Sorensen O., Persson T., Frohm-Nilsson M., Johansson B., Bjartell A., Lilja H., Stahle-Backdahl M., Borregaard N., Egesten A. The human cationic antimicrobial protein (hCAP-18) is expressed in the epithelium of human epididymis, is present in seminal plasma at high concentrations, and is attached to spermatozoa. Infect. Immun. 2000, 68:4297-4302.
98. Manjunath P., Chandonnet L., Leblond E., Desnoyers L. Major proteins of bovine seminal-vesicles bind to spermatozoa. Biol. Reprod. 1994, 50. 977.
99. Manjunath P., Lefebvre J., Jois P.S., Fan J., Wright M.W. New nomenclature for mammalian BSP genes. Biol. Reprod. 2009, 80:394-397.
100. Manjunath P., Marcel Y.L., Uma J., Seidah N.G., Chretien M., Chapdelaine A. Apolipoprotein A-I binds to a family of bovine seminal plasma-proteins. J. Biol. Chem. 1989, 264:16853-16857.
101. Marin-Briggiler C.I., Veiga M.F., Matos M.L., Echeverria M.F., Furlong L.I., Vazquez-Levin M.H. Expression of epithelial cadherin in the human male reproductive tract and gametes and evidence of its participation in fertilization. Mol. Hum. Reprod. 2008, 14:561-571.
102. Marrs J.A., Nelson W.J. Cadherin cell adhesion molecules in differentiation and embryogenesis. Int. Rev. Cytol. 1996, 165:159-205.
103. Matousek J., Klaudy J. Qualitative and quantitative analyses of seminal ribonuclease in reproductive tract fluids of bulls. Anim. Reprod. Sci. 1998, 51:111-118.
104. 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.
105. Melian E.B., Hinzman E., Nagasaki T., Firth A.E., Wills N.M., Nouwens A.S., Blitvich B.J., Leung J., Funk A., Atkins J.F., Hall R., Khromykh A.A. NS1' of flaviviruses in the Japanese encephalitis virus serogroup is a product of ribosomal frameshifting and plays a role in viral neuroinvasiveness. J. Virol. 2010, 84:1641-1647.
106. Metayer 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.
107. Miller D., Brough S., Al-Harbi O. Characterization and cellular distribution of human spermatozoal heat shock proteins. Hum. Reprod. (Oxford, Engl.) 1992, 7:637-645.
108. Mollan T.L., Banerjee S., Wu G., Parker Siburt C.J., Tsai A.L., Olson J.S., Weiss M.J., Crumbliss A.L., Alayash A.I. Alpha-hemoglobin stabilizing protein (AHSP) markedly decreases the redox potential and reactivity of alpha subunits of human HbA with hydrogen peroxide. J. Biol. Chem. 2012, 288(6):4288-4298.
109. Monaco E., Gasparrini B., Boccia L., De Rosa A., Attanasio L., Zicarelli L., Killian G. Effect of osteopontin (OPN) on in vitro embryo development in cattle. Theriogenology 2009, 71:450-457.
110. Morales P., Kong M., Pizarro E., Pasten C. Participation of the sperm proteasome in human fertilization. Hum. Reprod. (Oxford, Engl.) 2003, 18:1010-1017.
111. Moreau R., Manjunath P. Characteristics of the cholesterol efflux induced by novel seminal phospholipid-binding proteins. Biochim. Biophys. Acta: Mol. Cell Biol. Lipids 2000, 1487:24-32.
112. Mortarino M., Tedeschi G., Negri A., Ceciliani F., Gottardi L., Maffeo G., Ronchi S. Two-dimensional polyacrylamide gel electrophoresis map of bull seminal plasma proteins. Electrophoresis 1998, 19:797-801.
113. Mostov K.E., Friedlander M., Blobel G. The receptor for transepithelial transport of IgA and IgM contains multiple immunoglobulin-like domains. Nature 1984, 308:37-43.
114. Moura A.A. Seminal plasma proteins and fertility indexes in the bull: the case for osteopontin. Anim. Reprod. 2005, 2:3-10.
115. 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.
116. 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.
117. 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.
118. Moura A.A., Souza C.E., Stanley B.A., Chapman D.A., Killian G.J. Proteomics of cauda epididymal fluid from mature Holstein bulls. J. Proteom. 2010, 73:2006-2020.
119. Murthy A.R.K., Lehrer R.I., Harwig S.S.L., Miyasaki K.T. In vitro candidastatic properties of the human neutrophil calprotectin complex. J. Immunol. 1993, 151:6291-6301.
120. Ochs D., Wolf D.P. Actin in ejaculated human sperm cells. Biol. Reprod. 1985, 33:1223-1226.
121. Peloille S., Esnard A., Dacheux J.L., Guillou F., Gauthier F., Esnard F. Interactions between ovine cathepsin L, cystatin C and alpha(2)-macroglobulin - potential role in the genital tract. Eur. J. Biochem. 1997, 244:140-146.
122. Petersen B.H., Lammel C.J., Stites D.P., Brooks G.F. Human seminal plasma inhibition of complement. J. Lab. Clin. Med. 1980, 96:582-591.
123. Petersson U., Somogyi E., Reinholt F.P., Karlsson T., Sugars R.V., Wendel M. Nucleobindin is produced by bone cells and secreted into the osteoid, with a potential role as a modulator of matrix maturation. Bone 2004, 34:949-960.
124. Purohit S., Brahmaraju M., Palta A., Shukla S., Laloraya M., Kumar P.G. Impaired E-cadherin expression in human spermatozoa in a male factor infertility subset signifies E-cadherin-mediated adhesion mechanisms operative in sperm-oolemma interactions. Biochem. Biophys. Res. Commun. 2004, 316:903-909.
125. Quayle A.J., James K. Immunosuppression by seminal plasma and its possible biological significance. Arch. Immunol. Ther. Exp. (Warsz) 1990, 38:87-100.
126. Raczek S., Yeung C.H., Hasilik A., Robenek H., Hertle L., Schulze H., Cooper T.G. Immunocytochemical localization of some lysosomal hydrolases, their presence in luminal fluid and their directional secretion by human epididymal cells in culture. Cell Tissue Res. 1995, 280:415-425.
127. Rader D.J. Molecular regulation of HDL metabolism and function: implications for novel therapies. J. Clin. Invest. 2006, 116:3090-3100.
128. Rawe V.Y., Diaz E.S., Abdelmassih R., Wojcik 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. (Oxford, Engl.) 2008, 23:573-580.
129. Red-Horse K., Kapidzic M., Zhou Y., Feng K.T., Singh H., Fisher S.J. EPHB4 regulates chemokine-evoked trophoblast responses: a mechanism for incorporating the human placenta into the maternal circulation. Development (Cambridge, Engl.) 2005, 132:4097-4106.
130. Rescher U., Gerke V. Annexins - unique membrane binding proteins with diverse functions. J. Cell Sci. 2004, 117:2631-2639.
131. Reyes-Moreno C., Boilard M., Sullivan R., Sirard M.A. Characterization and identification of epididymal factors that protect ejaculated bovine sperm during in vitro storage. Biol. Reprod. 2002, 66:159-166.
132. Ritonja A., Colic A., Dolenc I., Ogrinc T., Podobnik M., Turk V. The complete amino-acid-sequence of bovine cathepsin-S and a partial sequence of bovine cathepsin-L. FEBS Lett. 1991, 283:329-331.
133. Roth J., Burwinkel F., Vandenbos C., Goebeler M., Vollmer E., Sorg C. MRP 8 and MRP14, S-100-like proteins associated with myeloid differentiation, are translocated to plasma-membrane and intermediate filaments in a calcium-dependent manner. Blood 1993, 82:1875-1883.
134. Roudebush W.E., Diehl J.R. Platelet-activating factor content in boar spermatozoa correlates with fertility. Theriogenology 2001, 55:1633-1638.
135. Roudebush W.E., Purnell E.T. Platelet-activating factor content in human spermatozoa and pregnancy outcome. Fertil. Steril. 2000, 74:257-260.
136. Sanchez L.M., LopezOtin C., Bjorkman P.J. Biochemical characterization and crystalization of human Zn-alpha(2)-glycoprotein, a soluble class I major histocompatibility complex homolog. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:4626-4630.
137. Sankhala R.S., Swamy M.J. The major protein of bovine seminal plasma, PDC-109, is a molecular chaperone. Biochemistry 2010, 49:3908-3918.
138. Sanz L., Calvete J.J., Mann K., Schafer W., Schmid E.R., Amselgruber W., Sinowatz F., Ehrhard M., Topferpetersen E. The complete primary structure of the spermadhesin awn, a zona-pellucida-binding protein isolated from boar spermatozoa. FEBS Lett. 1992, 300:213-218.
139. Shao C., Zhang F., Kemp M.M., Linhardt R.J., Waisman D.M., Head J.F., Seaton B.A. Crystallographic analysis of calcium-dependent heparin binding to annexin A2. J. Biol. Chem. 2006, 281:31689-31695.
140. Shivaji S., Rukmini V., Gupta P.D., Scheit K.H., Bhargava P.M. Localization of bovine seminal plasma RNA-A BS1, on the surface of bovine spermatozoa. Cell. Mol. Biol. 1989, 35:285-291.
141. Silkensen J.R., Schwochau G.B., Rosenberg M.E. The role of clusterin in tissue-injury. Biochem. Cell Biol. 1994, 72:483-488.
142. Silkensen J.R., Skubitz K.M., Skubitz A.P.N., Chmielewski D.H., Manivel J.C., Dvergsten J.A., Rosenberg M.E. Clusterin promotes the aggregation and adhesion of renal porcine epithelial cells. J. Clin. Invest. 1995, 96:2646-2653.
143. Singleton C.L., Killian G.J. A study of phospholipase in albumin and its role in inducing the acrosome reaction of guinea pig spermatozoa in vitro. J. Androl. 1983, 4:150-156.
144. Sirigu P., Perra M.T., Turno F. Immunohistochemical study of secretory IgA in the human male reproductive tract. Andrologia 1995, 27:335-339.
145. Snel B., Lehmann G., Bork P., Huynen M.A. STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. Nucleic Acids Res. 2000, 28:3442-3444.
146. Solis D., Romero A., Jimenez M., Diaz-Maurino 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.
147. Sottrupjensen L. Alpha-macroglobulins - structure, shape, and mechanism of proteinase complex-formation. J. Biol. Chem. 1989, 264:11539-11542.
148. Souza C.E.A., Rego J.P.A., Lobo C.H., Oliveira J.T.A., Nogueira F.C.S., Domont G.B., Fioramonte M., Gozzo F.C., Moreno F.B., Monteiro-Moreira A.C.O., Figueiredo J.R., Moura A.A. Proteomic analysis of the reproductive tract fluids from tropically adapted Santa Ines rams. J. Proteom. 2012, 75:4436-4456.
149. Stafforini D.M., McIntyre T.M., Zimmermann G.A., Prescott S.M. Platelet-activating factor acetylhydrolases. J. Biol. Chem. 1997, 272:17895-17898.
150. Sutovsky P., Manandhar G., McCauley T.C., Caamano J.N., Sutovsky M., Thompson W.E., Day B.N. Proteasomal interference prevents zona pellucida penetration and fertilization in mammals. Biol. Reprod. 2004, 71:1625-1637.
151. Suzuki K., Kusumoto H., Nishioka J., Komiyama Y. Bovine plasma protein-C inhibitor with structural and functional homologous properties to human plasma protein-C inhibitor. J. Biochem. 1990, 107:381-388.
152. Sylvester S.R., Morales C., Oko R., Griswold M.D. Localization of sulfated glycoprotein-2 (clusterin) on spermatozoa and in the reproductive-tract of the male-rat. Biol. Reprod. 1991, 45:195-207.
153. Tada T., Ohkubo I., Niwa M., Sasaki M., Tateyama H., Eimoto T. Immunohistochemical localization of Zn-alpha-2-glycoprotein in normal human tissues. J. Histochem. Cytochem. 1991, 39:1221-1226.
154. Therien 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.
155. Therien I., Moreau R., Manjunath P. Bovine seminal plasma phospholipid-binding proteins stimulate phospholipid efflux from epididymal sperm. Biol. Reprod. 1999, 61:590-598.
156. Tjabringa G.S., Vos J.B., Olthuis D., Ninaber D.K., Rabe K.F., Schalkwijk J., Hiemstra P.S., Zeeuwen P.L. Host defense effector molecules in mucosal secretions. FEMS Immunol. Med. Microbiol. 2005, 45:151-158.
157. 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.
158. Tulsiani D.R., Orgebin-Crist M.C., Skudlarek M.D. Role of luminal fluid glycosyltransferases and glycosidases in the modification of rat sperm plasma membrane glycoproteins during epididymal maturation. J. Reprod. Fertil. Suppl. 1998, 53:85-97.
159. Urade Y., Watanabe K., Hayaishi O. Prostaglandin-D, prostaglandin-E, and prostaglandin-F synthases. J. Lipid Mediators Cell Signal. 1995, 12:257-273.
160. Utleg A.G., Yi E.C., Xie T., Shannon P., White J.T., Goodlett D.R., Hood L., Lin B. Proteomic analysis of human prostasomes. Prostate 2003, 56:150-161.
161. Valencia C.A., Cotten S.W., Duan J., Liu R. Modulation of nucleobindin-1 and nucleobindin-2 by caspases. FEBS Lett. 2008, 582:286-290.
162. Villemure M., Lazure C., Manjunath P. Isolation and characterization of gelatin-binding proteins from goat seminal plasma. Reprod. Biol. Endocrinol. 2003, 1:39.
163. Yanagimachi R. Fertility of mammalian spermatozoa: its development and relativity. Zygote (Cambridge, Engl.) 1994, 2:371-372.
164. Yoshida H., Satoh K., Imaizumi T. Activity of platelet-activating-factor acetylhydrolase exists in red-cell membrane. Am. J. Hematol. 1992, 40:61-63.
165. Yu H.H., Xu Q., Chen H.P., Wang S., Huang X.S., Huang Q.R., He M. Stable overexpression of DJ-1 protects H9c2 cells against oxidative stress under a hypoxia condition. Cell Biochem. Funct. 2013, 31(8):643-651.
166. Yuasa H., Tanaka H., Hayashi T., Wakita T., Nakamura H., Nishioka J., Kawarada Y., Suzuki K. Bovine protein C inhibitor has a unique reactive site and can transiently inhibit plasmin. Thromb. Haemost. 2000, 83:262-267.
167. Zalata A., Hafez T., Schoonjans F., Comhaire F. The possible meaning of transferrin and its soluble receptors in seminal plasma as markers of the seminiferous epithelium. Hum. Reprod. 1996, 11:761-764.
168. Zhou W., Freed C.R. DJ-1 up-regulates glutathione synthesis during oxidative stress and inhibits A53T alpha-synuclein toxicity. J. Biol. Chem. 2005, 280:43150-43158.
169. Ziv S., Rufas O., Shalgi R. Cadherins expression during gamete maturation and fertilization in the rat. Mol. Reprod. Dev. 2002, 62:547-556.