Major heparin-binding proteins of the seminal plasma from Morada Nova rams

Small Ruminant Research

Volumn 113, Issue 1, 2013, Pages 115-127

  Martins, Jorge André Matias ^a   Souza, Carlos Eduardo Azevedo ^a   Silva, Fredy David Albuquerque ^a   Cadavid, Verónica Gonzalez ^a   Nogueira, Fabio César ^b   Domont, Gilberto Barbosa ^b   de Oliveira, José Tadeu Abreu ^a   Moura, Arlindo A ^a  

^a FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Heparin affinity chromatography; Ovine; Seminal plasma

Indexed keywords

BOVINAE; MAMMALIA; OVIS;

EID: 84878358933     PISSN: 09214488     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smallrumres.2013.01.005     Document Type: Article

References (128)

1. Albarracín J.L., Fernández-Novell J.M., Ballester J., Rauch M.C., Quintero-Moreno A., Peña A., Mogas T., Rigau T., Yañez A., Guinovart J.J., Slebe J.C., Concha I.I., Rodríguez-Gil J.E. Gluconeogenesis-linked glycogen metabolism is important in the achievement of in vitro capacitation of dog spermatozoa in a medium without glucose. Biol. Reprod. 2004, 71:1437-1445.
2. Bailey R., Griswold M.D. Clusterin in the male reproductive system: localization and possible function. Mol. Cell. Endocrinol. 1999, 151:17-23.
3. Belleannée 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. Proteomics 2011, 74:59-78.
4. Bellin M.E., Hawkins H.E., Ax R.L. Fertility of range beef bulls grouped according to presence or absence of heparin-binding proteins in sperm membranes and seminal fluid. J. Anim. Sci. 1994, 72:2441-2448.
5. 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.
6. 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.
7. 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.
8. Bratanov K., Efremova V., Doycheva M., Somlev B., Tornyov A. Effect of kallikrein on the motility of bull and ram spermatozoa after deep freezing. C R Acad. Bulg. Sci. 1978, 31:1337-1338.
9. Calvete J.J., Mann K., Schafer W., Raida M., Sanz L., Topfer-Petersen E. Boar spermadhesin PSP-II: location of posttranslational modifications, heterodimer formation with PSP-I glycoforms and effect of dimerization on the ligand-binding capabilities of the subunits. FEBS Lett. 1995, 365:179-182.
10. 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.
11. Cancilla B., Davies A., Ford-Perriss M., Risbridger G.P. Discrete cell- and stage-specific localisation of fibroblast growth factors and receptor expression during testis development. J. Endocrinol. 2000, 164:149-159.
12. Cao W., Aghajanian H.K., Haig-Ladewig L.A., Gerton G.L. Sorbitol can fuel mouse sperm motility and protein tyrosine phosphorylation via sorbitol dehydrogenase. Biol. Reprod. 2009, 80:124-133.
13. Cardin A.D., Weintraub H.J. Molecular modeling of protein-glycosaminoglycan interactions. Arterioscler. Thromb. Vasc. Biol. 1989, 9:21-32.
14. 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.
15. Carmo A.S. Avaliação do desenvolvimento testicular de machos da raça Guzerá do nascimento aos 30 meses de idade, através de ultrasonografia, biometria e avaliação espermática 2008, Escola de Veterinária. Universidade Federal de Minas Gerais, Belo Horizonte, p. 89.
16. Castellón E.A., Huidobro C.C. Androgen regulation of glycosidase secretion in epithelial cell cultures from human epididymis. Hum. Reprod. 1999, 14:1522-1527.
17. Chabory E., Damon C., Lenoir A., Henry-Berger J., Vernet P., Cadet R., Saez F., Drevet J.R. Mammalian glutathione peroxidases control acquisition and maintenance of spermatozoa integrity. J. Anim. Sci. 2010, 88:1321-1331.
18. Chakraborty G., Jain S., Behera R., Ahmed M., Sharma P., Kumar V., Kundu G.C. The multifaceted roles of osteopontin in cell signaling, tumor progression and angiogenesis. Curr. Mol. Med. 2006, 6:819-830.
19. 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.
20. Citarella F., Te Velthuis H., Helmer-Citterich M., Hack C.E. Identification of a putative binding site for negatively charged surfaces in the fibronectin type II domain of human factor XII-an immunochemical and homology modeling approach. Thromb. Haemost. 2000, 84:1057-1065.
21. 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.
22. 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, 82:36-45.
23. 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.
24. Dhanad O.P., Rao B.R., Razdan M.N. Sorbitol dehydrogenase and hyaluronidase activity in buffalo semen. Indian J. Exp. Biol. 1981, 19:286-289.
25. Dias J.C., Andrade V.J., Emerick L.L., Martins J.A.M., Vale Filho V.R., Silva M.A. Teste da libido em touros jovens Guzerá e suas associações com características reprodutivas e níveis séricos de testosterona. Arch. Vet. Sci. 2009, 14:204-213.
26. Dzugan M., Ksiazkiewicz J. Activity of alpha- and beta-mannosidases in semen and reproductive organs of the drake. Reprod. Biol. 2009, 9:25-37.
27. Ekhlasi-Hundrieser M., Gohr K., Wagner A., Tsolova M., Petrunkina A.M., Topfer-Petersen E. Spermadhesin AQN1 is a candidate receptor molecule involved in the formation of the oviductal sperm reservoir in the pig. Biol. Reprod. 2005, 73:536-545.
28. Erikson D.W., Chapman D.A., Ealy A.D., Killian G.J. Immunodetection of osteopontin on Holstein bull sperm and of alpha(v) and alpha(5) integrins on bovine oocytes. 36th Annual Meeting of the Society-for-the-Study-of-Reproduction 2003, p. 349.
29. Falkner J.A., Kachman M., Veine D.M., Walker A., Strahler J.R., Andrews P.C. Validated MALDI-TOF/TOF mass spectra for protein standards. J. Am. Soc. Mass Spectrom. 2007, 18:850-855.
30. Fang X., Zhang W.W. Affinity separation and enrichment methods in proteomic analysis. J. Proteomics 2008, 71:284-303.
31. Feng J., Mehta V.B., El-Assal O.N., Wu D., Besner G.E. Tissue distribution and plasma clearance of heparin-binding EGF-like growth factor (HB-EGF) in adult and newborn rats. Peptides 2006, 27:1589-1596.
32. Fernández-Juan M., Gallego M., Barrios B., Osada J., Cebrián-Pérez J.A., Muiño-Blanco T. Immunohistochemical localization of sperm-preserving proteins in the ram reproductive tract. J. Androl. 2006, 27:588-595.
33. Fouchécourt S., Métayer S., Locatelli A., Dacheux F., Dacheux J.L. Stallion epididymal fluid proteome: qualitative and quantitative characterization, secretion and dynamic changes of major proteins. Biol. Reprod. 2000, 62:1790-1803.
34. Frenette G., Lessard C., Sullivan R. Polyol pathway along the bovine epididymis. Mol. Reprod. Dev. 2004, 69:448-456.
35. Fujimoto N., Terlizzi J., Aho S., Brittingham R., Fertala A., Oyama N., Mcgrath J.A., Uitto J. Extracellular matrix protein 1 inhibits the activity of matrix metalloproteinase 9 through high-affinity protein/protein interactions. Exp. Dermatol. 2006, 15:300-307.
36. Gabrielli N.M., Veiga M.F., Matos M.L., Quintana S., Chemes H., Blanco G., Vazquez-Levin M.H. Expression of dysadherin in the human male reproductive tract and in spermatozoa. Fertil. Steril. 2011, 96:554-561.
37. Garcia J.M., Pinheiro L.E.L., Okuda H.T. Body development and semen physical and morphological characteristics of young Guzera bulls. Ars Vet. 1987, 3:47-53.
38. Gaviraghi A., Deriu F., Soggiu A., Galli A., Bonacina C., Bonizzi L., Roncada P. Proteomics to investigate fertility in bulls. Vet. Res. Commun. 2010, 34:33-36.
39. Gonçalves R.F., Chapman D.A., Bertolla R.P., Eder I., Killian G.J. Pre-treatment of cattle semen or oocytes with purified milk osteopontin affects in vitro fertilization and embryo development. Anim. Reprod. Sci. 2008, 108:375-383.
40. 5) and osteopontin on bovine sperm-egg binding, and fertilization in vitro. Theriogenology 2007, 67:468-474.
41. 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.
42. Hao Y., Mathialagan N., Walters E., Mao J., Lai L., Becker D., Li W., Critser J., Prather R.S. Osteopontin reduces polyspermy during in vitro fertilization of porcine oocytes. Biol. Reprod. 2006, 75:726-733.
43. Hao Y., Murphy C.N., Spate L., Wax D., Zhong Z., Samuel M., Mathialagan N., Schatten G., Prather R.S. Osteopontin improves in vitro development of porcine embryos and decreases apoptosis. Mol. Reprod. Dev. 2008, 75:291-298.
44. Hecht N., Cavalcanti M.C.O., Nayudu P., Behr R., Reichenbach M., Weidner W., Steger K. Protamine-1 represents a sperm specific gene transcript: a study in Callithrix jacchus and Bos taurus. Andrologia 2011, 43:167-173.
45. Horlacher T., Noti C., De Paz J.L., Bindschadler P., Hecht M.L., Smith D.F., Fukuda M.N., Seeberger P.H. Characterization of annexin A1 glycan binding reveals binding to highly sulfated glycans with preference for highly sulfated heparan sulfate and heparin. Biochemistry 2011, 50:2650-2659.
46. Ibarra B., Gonzalez-Quiroga G., Vaca G., Diaz M., Rivas F., Cantu J.M. Sorbitol dehydrogenase (EC.1.1.1.14) polymorphism in human seminal plasma. Ann. Genet. 1982, 25:53-55.
47. Ihalin R., Loimaranta V., Tenovuo J. Origin, structure, and biological activities of peroxidases in human saliva. Arch. Biochem. Biophys. 2006, 445:261-268.
48. Jauhiainen A., Vanha-Pertulla T. Characterization of acid and neutral a-mannosidases in bull semen and reproductive organs. Int. J. Biochem. 1987, 19:267-274.
49. Jones A.R., Montague M.D. Metabolism of fructose-1,6-bisphosphate by mature boar spermatozoa. Reprod. Fertil. Dev. 1991, 3:609-613.
50. Kanagawa M., Satoh T., Ikeda A., Nakano Y., Yagi H., Kato K., Kojima-Aikawa K., Yamaguchi Y. Crystal structures of human secretory proteins ZG16p and ZG16b reveal a Jacalin-related β-prism fold. Biochem. Biophys. Res. Commun. 2011, 404:201-205.
51. 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.
52. Killian G.J., Chapman D.A., Rogowski L.A. Fertility-associated proteins in Holstein bull seminal plasma. Biol. Reprod. 1993, 49:1202-1207.
53. Kumar V., Hassan M.D.I., Kashav T., Singh T.P., Yadav S. Heparin-binding proteins of human seminal plasma: purification and characterization. Mol. Reprod. Dev. 2008, 75:1767-1774.
54. Lee C.N., Ax R.L. Concentrations and composition of glycosaminoglycans in the female bovine reproductive tract. J. Dairy Sci. 1984, 67:2006-2009.
55. Lee C.N., Clayton M.K., Bushmeyer S.M., First N.L., Ax R.L. Glycosaminoglycans in ewe reproductive tracts and their influence on acrosome reactions in bovine spermatozoa in vitro. J. Anim. Sci. 1986, 63:861-867.
56. Leonardi A., Sathe S., Bortolotti M., Beaton A., Sack R. Cytokines, matrix metalloproteases, angiogenic and growth factors in tears of normal subjects and vernal keratoconjunctivitis patients. Allergy 2009, 64:710-717.
57. Lippolis J.D., Reinhardt T.A. Centennial paper: proteomics in animal science. J. Anim. Sci. 2008, 86:2430-2441.
58. Lippolis J.D., Reinhardt T.A. Utility, limitations, and promise of proteomics in animal science. Vet. Immunol. Immunopathol. 2010, 138:241-251.
59. Lusignan M.F., Bergeron A., Crête M.H., Lazure C., Manjunath P. Induction of epididymal boar sperm capacitation by pB1 and BSP-A1/-A2 proteins, members of the BSP protein family. Biol. Reprod. 2007, 76:424-432.
60. 165-induced angiogenesis by competing for heparin-like binding sites on endothelial cells. Am. J. Pathol. 2006, 169:1753-1766.
61. 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.
62. 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.
63. Manjunath P., Sairam M.R., Uma J. Purification of four gelatin-binding proteins from bovine seminal plasma by affinity chromatography. Biosci. Rep. 1987, 7:231-238.
64. Mann T. Secretory function of the prostate, seminal vesicle and other male accessory organs of reproduction. J. Reprod. Fertil. 1974, 37:179-188.
65. Mann T., Lutwak-Mann C. Studies on the metabolism of semen. 4. Aerobic and anaerobic utilization of fructose by spermatozoa and seminal vesicles. Biochem. J. 1948, 43:266-270.
66. Marín-Briggiler C.I., Veiga M.F., Matos M.L., González-Echeverría 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.
67. 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.
68. Melo L.M., Nascimento A.S.F., Silveira F.G., Cunha R.M.S., Tavares N., Teixeira A.C., Lima-Filho D.I.A., Freitas J.L., Cavada V.J.F., Rádis-Baptista B.S.G. 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.
69. Meri S., Jarva H. Complement regulatory proteins. Nat. Encycl. Life Sci. 2001, 1:1-8.
70. 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.
71. Miller D.J., Winer M.A., Ax R.L. Heparin-binding proteins from seminal plasma bind to bovine spermatozoa and modulate capacitation by heparin. Biol. Reprod. 1990, 42:899-915.
72. 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.
73. Molina R., Bolaños I., Galina C.S., Pérez E., Paniagua G., Estrada S. Sexual behaviour of Zebu bulls in the humid tropics of Costa Rica: single versus multiple-sire groups. Anim. Reprod. Sci. 2000, 64:139-148.
74. 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.
75. 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.
76. Moura A.A., Van Tilburg M.F., Souza C.E.A., Martins J.a.M., Lobo C.H., Moreno F.B., Monteiro-Moreira A.C., Moreira R.A., Figueiredo J.R. Major proteins of the ram seminal plasma: attributes and interaction with the sperm membrane. Reprod. Domest. Anim. 2012, 47:520-521.
77. Nagdas S.K., Hamilton S.L., Raychoudhury S. Identification of acrosomal matrix-specific hydrolases binding proteins of bovine cauda epididymal spermatozoa. J. Androl. 2010, 31:177-187.
78. Nel-Themaat L., Harding G.D., Chandler J.E., Chenevert J.F., Damiani P., Fernandez J.M., Humes P.E., Pope C.E., Godke R.A. Quality and freezing qualities of first and second ejaculates collected from endangered Gulf Coast Native rams. Anim. Reprod. Sci. 2006, 95:251-261.
79. Orosz F., Ovádi J. TPPP orthologs are ciliary proteins. FEBS Lett. 2008, 582:3757-3764.
80. Osaki A., Okida N., Ishikawa K., Tokumoto M., Nagahama Y., Lippert T.H., Voelter W., Tokumoto T. Identification of ubiquitin in seminal plasma from Tilapia, Oreochromis niloticus. Biomed. Res. Tokyo 1999, 20:249-252.
81. Parrish J.J., Susko-Parrish J., First N.L. Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH. Biol. Reprod. 1989, 41:683-699.
82. Parrish J.J., Susko-Parrish J., Winer M.A., First N.L. Capacitation of bovine sperm by heparin. Biol. Reprod. 1988, 38:1171-1180.
83. Peloille S., Esnard A., Dacheux J.L., Guillou F., Gauthier F., Esnard F. Interactions between ovine cathepsin L, cystatin C and a2-macroglobulin-potential role in the genital tract. Eur. J. Biochem. 1997, 244:140-146.
84. Philippe B., Rousseau G.G., Hue L. Fructose 2,6-bisphosphate and the control of glycolysis in bovine spermatozoa. FEBS Lett. 1986, 200:169-172.
85. Pilch B., Mann M. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol. 2006, 7:R40.
86. Pruneda A., Pinart E., Bonet S., Yeung C.H., Cooper T.G. Study of the polyol pathway in the porcine epididymis. Mol. Reprod. Dev. 2006, 73:859-865.
87. Rákos G., Kis Z., Nagy D., Lur G., Farkas T., Hortobágyi T., Vecsei L., Toldi J. Evans blue fluorescence permits the rapid visualization of non-intact cells in the perilesional rim of cold injured rat brain. Acta Neurobiol. Exp. (Warsz.) 2007, 67:149-154.
88. Ramanathan B., Davis E.G., Ross C.R., Blecha F. Cathelicidins: microbicidal activity, mechanisms of action, and roles in innate immunity. Microbes Infect. 2002, 4:361-372.
89. Rocha S.L.G, Neves-Ferreira A.G.C., Trugilho M.R.O., Chapeaurouge A., León I.R., Valente R.H., Domont G.B., Perales J. Crotalid snake venom subproteomes unraveled by the antiophidic protein DM43. J. Proteome Res. 2009, 8:2351-2360.
90. Rodrigues M.a.M., Souza C.E.A., Martins J.a.M., Rego J.P., Oliveira J.T.A., Domont G.B., Nogueira F.C., Moura A.A. Seminal plasma proteins and their relationship with sperm motility in Santa Ines rams. Small Ruminant Res. 2013, 109:94-100.
91. Sakaue T., Takeuchi K., Maeda T., Yamamoto Y., Nishi K., Ohkubo I. Factor H in porcine seminal plasma protects sperm against complement attack in genital tracts. J. Biol. Chem. 2010, 285:2184-2192.
92. Shibib B.A., Khan L.A., Rahman R. Hypoglycaemic activity of Coccinia indica and Momordica charantia in diabetic rats: depression of the hepatic gluconeogenic enzymes glucose-6-phosphatase and fructose-1,6-bisphosphatase and elevation of both liver and red-cell shunt enzyme glucose-6-phosphate dehydrogenase. Biochem. J. 1993, 292:267-270.
93. Somlev B., Helili K., Karcheva V. Tissue kallikrein activity in seminal plasma of bovine ejaculates with different quality. Theriogenology 1996, 45:471-475.
94. Sorensen O.E., Gram L., Johnsen A.H., Andersson E., Bangsboll S., Tjabringa G.S., Hiemstra P.S., Malm J., Egesten A., Borregaard N. Processing of seminal plasma hCAP-18 to ALL-38 by gastricsin: a novel mechanism of generating antimicrobial peptides in vagina. J. Biol. Chem. 2003, 278:28540-28546.
95. 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.
96. Souza C.E.A., Moura A.A., Monaco E., Killian G.J. Binding patterns of bovine seminal plasma proteins A1/A2, 30 kDa and osteopontin on ejaculated sperm before and after incubation with isthmic and ampullary oviductal fluid. Anim. Reprod. Sci. 2008, 105:72-89.
97. Souza C.E.A., Moura A.A., Oliveira J.T.A., Radis-Baptista G., Araújo A.A., Lima A.C.B. Seminal plasma proteins, testis development and semen criteria in the ram. 29th Annual Meeting of the American Society of Andrology 2004, p. 91.
98. Souza C.E.A., Rego J.P., Lobo C.H., Oliveira J.T.A., Nogueira F.C., Domont G.B., Fioramonte M., Gozzo F.C., Moreno F.B., Monteiro-Moreira A.C., Figueiredo J.R., Moura A.A. Proteomic analysis of the reproductive tract fluids from tropically-adapted Santa Ines rams. J. Proteomics 2012, 75:4436-4456.
99. Speight S.M., Estienne M.J., Harper A.F., Crawford R.J., Knight J.W., Whitaker B.D. Effects of dietary supplementation with an organic source of selenium on characteristics of semen quality and in vitro fertility in boars. J. Anim. Sci. 2012, 761-770.
100. Stefan N., Hennige A.M., Staiger H., Machann J., Schick F., Krober S.M., Machicao F., Fritsche A., Haring H.U. a2-Heremans-Schmid glycoprotein/Fetuin A is associated with insulin resistance and fat accumulation in the liver in humans. Diabetes Care 2006, 29:853-857.
101. 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.
102. Sylvester S.R., Morales C.R., 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.
103. Syntin P., Dacheux F., Druart X., Gatti J.L., Okamura N., Dacheux J.L. Characterization and identification of proteins secreted in the various regions of the adult boar epididymis. Biol. Reprod. 1996, 55:956-974.
104. Talevi R., Gualtieri R. Molecules involved in sperm-oviduct adhesion and release. Theriogenology 2010, 73:796-801.
105. Teixeira D.I.A., Melo L.M., Gadelha C.a.A., Cunha R.M.S., Bloch C., Rádis-Baptista G., Cavada B.S., Freitas V.J.F. Ion-exchange chromatography used to isolate a spermadhesin-related protein from domestic goat (Capra hircus) seminal plasma. Gen. Mol. Res. 2006, 5:79-87.
106. Thérien I., Bleau G., Manjunath P. Phosphatidylcholine-binding proteins of bovine seminal plasma modulate capacitation of spermatozoa by heparin. Biol. Reprod. 1995, 52:1372-1379.
107. Thérien I., Bousquet D., Manjunath P. Effect of seminal phospholipid-binding proteins and follicular fluid on bovine sperm capacitation. Biol. Reprod. 2001, 65:41-51.
108. Thimon V., Frenette G., Saez F., Thabet M., Sullivan R. Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach. Hum. Reprod. 2008, 23:1698-1707.
109. Tirián L., Hlavanda E., Oláh J., Horváth I., Orosz F., Szabó B., Kovács J., Szabad J., Ovádi J. TPPP/p25 promotes tubulin assemblies and blocks mitotic spindle formation. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13976-13981.
110. Topfer-Petersen E., Ekhlasi-Hundrieser M., Tsolova M. Glycobiology of fertilization in the pig. Int. J. Dev. Biol. 2008, 52:717-736.
111. Topfer-Petersen E., Petrunkina A.M., Ekhlasi-Hundrieser M. Oocyte-sperm interactions. Anim. Reprod. Sci. 2000, 60-61:653-662.
112. Topfer-Petersen E., Romero A., Varela P.F., Ekhlasi-Hundrieser M., Dostàlovà Z., Sanz L., Calvete J.J. Spermadhesins: a new protein family. Facts, hypotheses and perspectives. Andrologia 1998, 30:217-224.
113. Torres-Júnior J.R.S., Henry M. Sexual development of Guzerat (Bos taurus indicus) bulls raised in a tropical region. Anim. Reprod. 2005, 2:114-121.
114. Trocóniz J.F., Beltrán J., Bastidas H., Larreal H., Bastidas P. Testicular development, body weight changes, puberty and semen traits of growing Guzerat and Nellore bulls. Theriogenology 1991, 35:815-826.
115. Tsujioka H., Fukami T., Yotsumoto F., Ueda T., Hikita S., Takahashi Y., Kondo H., Kuroki M., Miyamoto S. A possible clinical adaptation of CRM197 in combination with conventional chemotherapeutic agents for ovarian cancer. Anticancer Res. 2011, 31:2461-2465.
116. Tulsiani D.R.P., 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. Fert. Suppl. 1998, 53:85-97.
117. Tulsiani D.R.P., Skudlarek M.D., Nagdas S.K., Orgebin-Crist M.C. Purification and characterization of rat epididymal fluid a-d-mannosidase: similarities to sperm plasma membrane a-d-mannosidase. Biochem. J. 1993, 290:427-436.
118. Tulsiani D.R.P., Skudlarek M.D., Orgebin-Crist M.C. Novel a-d-mannosidase of rat sperm plasma membranes: characterization and potential role in sperm-egg interaction. J. Cell Biol. 1989, 109:1257-1267.
119. Turner R.M. Tales from the tail: what do we really know about sperm motility. J. Androl. 2003, 24:790-803.
120. 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.
121. Villemure M., Lazure C., Manjunath P. Isolation and characterization of gelatin-binding proteins from goat seminal plasma. Reprod. Biol. Endocrinol. 2003, 1:39-48.
122. Vincze O., Tökési N., Oláh J., Hlavanda E., Zotter A., Horváth I., Lehotzky A., Tirián L., Medzihradszky K.F., Kovács J., Orosz F., Ovádi J. Tubulin polymerization promoting proteins (TPPPs): members of a new family with distinct structures and function. Biochemistry 2006, 45:13818-13826.
123. 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.
124. Wang B.C., Huang H.Y., Chen Y.C., Bristow R.E., Kassauei K., Cheng C.C., Roden R., Sokoll L.J., Chan D.W., Shih I.M. Increased plasma DNA integrity in cancer patients. Cancer Res. 2003, 63:3966-3968.
125. Ward W.S. Function of sperm chromatin structural elements in fertilization and development. Mol. Hum. Reprod. 2010, 16:30-36.
126. Xuan J.W., Hota C., Shigeyama Y., D'errico J.A., Somerman M.J., Chambers A.F. Site-directed mutagenesis of the arginine-glycine-aspartic acid sequence in osteopontin destroys cell adhesion and migration functions. J. Cell. Biochem. 1995, 57:680-690.
127. Yasuda T., Takeshita H., Tsubota E., Sawazaki K., Iida R., Nadano D., Kishi K. Alpha-2-HS-glycoprotein (AHSG) polymorphism in semen and saliva. Electrophoresis 1996, 17:793-796.
128. Zanetti M., Gennaro R., Romeo D. Cathelicidins: a novel protein family with a common proregion and a variable C-terminal antimicrobial domain. FEBS Lett. 1995, 374:1-5.