Bovine seminal PDC-109 protein: An overview of biochemical and functional properties

Animal Reproduction Science

Volumn 138, Issue 1-2, 2013, Pages 1-13

  Srivastava, N ^a   Jerome, A ^b   Srivastava, S K ^a   Ghosh, S K ^a   Kumar, Amit ^a  

^a INDIAN VETERINARY RESEARCH INSTITUTE   (India)

^b CENTRAL INSTITUTE FOR RESEARCH ON BUFFALOES   (India)

Author keywords

Bovine; BSP A1 A2 protein; Cryoinjury; Cryopreservation; Sequestration

Indexed keywords

BOVINAE;

PROTEIN BINDING; SEMINAL VESICLE SECRETORY PROTEIN; SEMINAL VESICLE SECRETORY PROTEIN 109, BOS TAURUS;

ACROSOME REACTION; AMINO ACID SEQUENCE; ANIMAL; BOVINE; CHEMISTRY; CRYOPRESERVATION; MALE; PHYSIOLOGY; PROCEDURES; SPERM; SPERMATOZOON; SPERMATOZOON CAPACITATION; VETERINARY;

ACROSOME REACTION; AMINO ACID SEQUENCE; ANIMALS; CATTLE; CRYOPRESERVATION; MALE; PROTEIN BINDING; SEMEN; SEMINAL VESICLE SECRETORY PROTEINS; SPERM CAPACITATION; SPERMATOZOA;

EID: 84880042492     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2013.02.008     Document Type: Review

References (91)

1. Amann R.P., Seidel G.E., Brink Z.A. Exposure of thawed frozen bull sperm to a synthetic peptide before artificial insemination increases fertility. J. Androl. 1999, 20:42-46.
2. Anbazhagan V., Damai R.S., Paul A., Swamy M.J. Interaction of the major protein from bovine seminal plasma, PDC-109 with phospholipid membranes and soluble ligands investigated by fluorescence approaches. Biochim. Biophys. Acta 2008, 1784:891-899.
3. Anbazhagan V., Sankhala R.S., Singh B.P., Swamy M.J. Isothermal titration calorimetric studies on the interaction of the major bovine seminal plasma protein, PDC-109 with phospholipid membranes. PLoS ONE 2011, 6(10):e25993. 10.1371/journal.pone.0025993.
4. Arangasamy A., Singh L.P., Ahmad N., Ansari M.R., Ram G.C. Isolation and characterization of heparin and gelatin binding buffalo seminal plasma proteins and their effect on cauda epididymal spermatozoa. Anim. Reprod. Sci. 2005, 90:243-254.
5. Arnoult C., Zeng Y., Florman H.M. ZP3-dependent of activation of sperm cation channels regulate acrosomal secretion during mammalian fertilization. J. Cell Biol. 1996, 134:637-645.
6. Aumuller G., Vesper M., Seitz J., Kemme M., Scheit K.-H. Binding of a major secretory protein from bull seminal vesicles to bovine spermatozoa. Cell Tissue Res. 1988, 252:377-384.
7. Baas J.W., Mohan P.C., Shannon P. Factors in seminal plasma of bull that affect the viability and motility of spermatozoa. J. Reprod. Fertil. 1983, 68:275-280.
8. Bergeron A., Brindle Y., Blondin P., Manjunath P. Milk caseins decrease the binding of the major bovine seminal plasma proteins to sperm and prevent lipid loss from the sperm membrane during sperm storage. Biol. Reprod. 2007, 77:120-126.
9. Bergeron A., Crete M.-H., Brindle Y., Manjunath P. Low-density lipoprotein fraction from hen's egg yolk decreases the binding of the major proteins of bovine seminal plasma to sperm and prevents lipid efflux from the sperm membrane. Biol. Reprod. 2004, 70:708-717.
10. Bergeron A., Villemure M., Lazure C., Manjunath P. Isolation and characterization of the major proteins of ram seminal plasma. Mol. Reprod. Dev. 2005, 71(4):461-470.
11. Breitbart H., Darshan R., Rubinstein S. Evidence for the presence of ATP-dependent calcium pump and ATPase activities in bull sperm head membranes. Biochem. Biophys. Res. Commun. 1984, 122:479-484.
12. 2+-ATPase in maintaining motility in ram spermatozoa. J. Biol. Chem. 1985, 122:11548-11553.
13. Calvete J.J., Mann K., Sanz L., Raida M., Topfer-Petersen E. The primary structure of BSP-30kDa, a major lipid-, gelatin-, and heparin-binding glycoprotein of bovine seminal plasma. FEBS Lett. 1996, 399:147-152.
14. Calvete J.J., Mann K., Schafer W., Sanz L., Reinert M., Nessau S., Raida M., Topfer-Petersen E. Amino acid sequence of HSP-1, a major protein of stallion seminal plasma: effect of glycosylation on its heparin- and gelatin-binding capabilities. Biochem. J. 1995, 310:616-622.
15. Calvete J.J., Raida M., Sanz L., Wempe F., Scheit K.H., Romero A., Topfer-Petersen E. Localization and structural characterization of an oligosaccharide O-linked to bovine PDC-109: quantitation of the glycoprotein in seminal plasma and on the surface of ejaculated and capacitated spermatozoa. FEBS Lett. 1994, 350:203-206.
16. Calvete J.J., Raida M., Gentzel M., Urbanke C., Sanz L., Toepfer-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.
17. Calvete J.J., Topfer-Petersen E., Sanz L. Spermadhesin-a novel class of mammalian lectins?. Lectins Biology, Biochemistry, Clinical Biochemistry 1996, 185-192. Textop, Helkrup. E. Van Driessche, P. Rouge, C. Beeckmans, T.C. Bog-Hansen (Eds.).
18. Calvete J.J., Varela P.F., Sanz L., Romero A., Mann K., Topfer-Petersen E. A procedure for the large-scale isolation of major bovine seminal plasma proteins. Protein Expr. Purif. 1995, 8:48-56.
19. Cardin E., Weintraub H.J. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 1989, 9:21-32.
20. Damai R.S., Anbazhagan V., Babu Rao K., Swamy M.J. Fluorescence studies on the interaction of choline-binding domain B of the major bovine seminal plasma protein, PDC-109 with phospholipid membranes. Biochim. Biophys. Acta 2009, 1794:1725-1733.
21. Damai R.S., Sankhala R.S., Anbazhagan V., Swamy M.J. P NMR and AFM studies on the destabilization of cell and model membranes by the major bovine seminal plasma protein, PDC-109. IUBMB Life 2010, 62(11):841-851.
22. Darin-Bennett A., White I.G. Influence of the cholesterol content of mammalian spermatozoa on susceptibility to cold shock. Cryobiology 1977, 14:466-477.
23. DeMott R.P., Lefebvre R., Suarez S.S. Carbohydrates mediates the adherence of hamster sperm to oviductal epithelium. Biol. Reprod. 1995, 52:1395-1403.
24. Desnoyers L., Manjunath P. Major proteins of bovine seminal plasma exhibit novel interaction with phospholipids. J. Biol. Chem. 1992, 267:10149-10155.
25. Desnoyers L., Therien I., Manjunath P. Characterization of the major proteins of bovine seminal fluid by two-dimensional polyacrylamide gel electrophoresis. Mol. Reprod. Dev. 1994, 37:425-435.
26. Dobrinski I., Suarez S.S., Ball B.A. Intracellular calcium concentration in equine spermatozoa attached to oviductal epithelial cells in vitro. Biol. Reprod. 1996, 54:783-788.
27. Ehrenwald E., Parks J.E., Foote R.H. Cholesterol efflux from bovine sperm. I. Induction of acrosome reaction with lysophosphatidylcholine after reducing sperm cholesterol. Gamete Res. 1988, 20:145-157.
28. Esch F.S., Ling N.C., Bohlen P., Ying S.Y., Guillemin R. Primary structure of PDC-109, a major protein constituent of bovine seminal plasma. Biochem. Biophys. Res. Commun. 1983, 113:861-867.
29. Galantino-Homer H.L., Visconti P.E., Kopf G.S. Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3'5'-monophosphate-dependent pathway. Biol. Reprod. 1997, 56:707-719.
30. Gasset M., Magdaleno L., Calvete J.J. Biophysical study of the perturbation of model membrane structure caused by seminal plasma protein PDC-109. Arch. Biochem. Biophys. 2000, 374(2):241-247.
31. Gasset M., Saiz J.L., Laynez J., Sanz L., Gentzel M., Peterson E.T., Calvete J.J. Conformational features and thermal stability of bovine seminal plasma protein PDC-109 oligomers and phosphorycholine-bound complexes. Eur. J. Biochem. 1997, 250:735-744.
32. Green C.E., Bredl J., Holt W.V., Watson P.F., Fazeli A. Carbohydrate mediation of boar sperm binding to oviductal epithelial cells in vitro. Reproduction 2001, 122:305-315. (Abstract).
33. 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.
34. Gwathmey T.M., Ignotz G.G., Suarez S.S. PDC-109 (BSP-A1/-A2) promotes bull sperm binding to oviductal epithelium in vitro and may be involved in forming the oviductal sperm reservoir. Biol. Reprod. 2003, 69:809-815.
35. Handrove R.R., First N.L., Parrish J.J. Calcium requirement and increased association with bovine sperm during capacitation by heparin. J. Exp. Zool. 1989, 252:174-182.
36. Harshan, H.M., 2007. Modulation of structural and functional properties of buffalo cauda epididymal spermatozoa by sperm binding seminal plasma protein (PDC-109). Ph.D. Thesis submitted to deemed university. IVRI, Izatnagar.
37. Harshan H.M., Sankar S., Singh L.P., Singh M.K., Sudharani S., Ansari M.R., Singh S.K., Majumdar A.C., Joshi P. Identification of PDC-109-like protein(s) in buffalo seminal plasma. Anim. Reprod. Sci. 2009, 115(1-4):306-311.
38. Ignotz G.G., Lo M.C., Perez C.L., Gwathmay T.M., Suarez S.S. Characterization of fucose-binding protein from bull sperm and seminal plasma that may be responsible for formation of the oviductal sperm reservoir. Biol. Reprod. 2001, 64:1806-1811.
39. Jeyendran R.S., Vander Ven H.H., Parez-Pelaez M., Crabo B.G., Zaneweld L.J.D. Development of an assay to assess the functional integrity of the sperm membrane and its relationship to other semen characteristics. J. Reprod. Fertil. 1984, 70:219-228.
40. Kosanović M.M., Jankovi M.M. Molecular heterogeneity of gelatin-binding proteins from human seminal plasma. Asian J. Androl. 2010, 12:363-375.
41. Kulkarni B.A., Dhande S.G., Patnakar D.D. Seminal plasma protein profiles of Holstein Friesian, Jersey and cross bred bulls. Indian J. Anim. Sci. 1996, 11:133-137.
42. Kumar A., Singh L.P., Harshan M.H., Majumdar A.C. Seminal plasma non-heparin binding proteins (NHBP) reduce the cryoinjury to buffalo cauda epididymal spermatozoa induced by heparin binding proteins (HBPs). Anim. Reprod. Sci. 2007, 104(2-4):220-226.
43. Langlais J., Roberts K.D. A molecular membrane model of sperm capacitation and acrosome reaction of mammalian spermatozoa. Gamete Res. 1985, 12:183-224.
44. Lasley J.F., Bogart R. A comparative study of epididymal and ejaculated spermatozoa of boar. J. Anim. Sci. 1942, 3:360-370.
45. Leblond E., Desnoyers L., Manjunath P. Phosphorycholine-binding proteins form the seminal fluids of different species, share antigenic determinants with the major proteins of bovine seminal plasma. Mol. Reprod. Dev. 1993, 34:443-449.
46. Leclerc P., de Lamirande E., Gagnon C. Regulation of protein-tyrosine phosphorylation and human sperm capacitation by reactive oxygen derivatives. Free Radic. Biol. Med. 1997, 22:643-656.
47. Lefebvre R., DeMott R.P., Suarez S.S., Samper J.C. Specific inhibition of equine sperm binding to oviductal epithelium. Equine Reproduction VI 1995, 689-696. Society for the study of Reproduction. D.C. Sharp, F.W. Bazer, W.I. Madison (Eds.).
48. Lefebvre R., Lo M., Suarez S.S. Bovine sperm binding to oviductal epithelium involves fucose recognition. Biol. Reprod. 1997, 56:1198-1204.
49. Manjunath P., Baillargeon L., Marcel Y., Seidah N., Chrétien M., Chapdelaine A. Diversity of novel proteins in gonadal fluids. Molecular Biology of Brain and Endocrine Peptidergic Systems 1988, 259-273. Plenum Press, New York. M. Chrétien (Ed.).
50. Manjunath P., Marcel Y.L., Uma J., Seidah N.G., Chrétien M., Chapdelaine A. Apolylipopotein A-I binds to a family of bovine seminal plasma proteins. Biochem. J. 1989, 264:16853-16857.
51. Manjunath P., Sairam M.R. Purification and biochemical characterization of major acidic proteins (BSP-A1, BSP-A2 and BSP-A3) from bovine seminal plasma. Biochem. J. 1987, 241:685-692.
52. Manjunath P., Sairam M.R., Uma J. Purification of four gelatin binding proteins from bovine seminal plasma by affinity chromatography. Biosci. Rep. 1987, 7:231-237.
53. 2. Biochem. J. 1994, 303:121-128.
54. Martinus R.D., Molan P.C., Shannon P. Deleterious effect of seminal plasma in the cryo-preservation of bovine spermatozoa. N. Z. J. Agric. Res. 1991, 34:281-286.
55. 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.
56. Moreau R., Therien L., Lazure C., Manjunath P. Type II domains of BSP-A1/-A2 proteins: binding properties, lipid efflux, and sperm capacitation potential. Biochem. Biophys. Res. Commun. 1998, 246:148-154.
57. Muller P., Erlemann K.-R., Muller K., Calvete J.J., Topfer-Petersen E., Marienfeld K., Herrmann A. Biophysical characterization of the interaction of bovine seminal plasma protein PDC-109 with phospholipids vesicles. Eur. Biophys. J. 1998, 27:33-41.
58. Muller P., Greube A., Topfer-Petersen E., Herrmann A. Influence of the bovine seminal plasma protein PDC-109 on cholesterol in the presence of phospholipids. Eur. Biophys. J. 2002, 31:438-447.
59. Nauc V., Manjunath P. Radio immunoassays for bull seminal plasma proteins (BSP-A1/A2, BSP-A3, and BSP-30-kilo Daltons) and their quantification in seminal plasma and sperm. Biol. Reprod. 2000, 63:1058-1066.
60. Parrish J.J., Susko-Parrish J.L., First N.L. Capacitation of bovine spermatozoa by heparin: inhibitory effect of glucose and role of intracellular pH. Biol. Reprod. 1989, 41:683-699.
61. Peitz B. Effects of seminal vesicle fluid components on sperm motility in the house mouse. J. Reprod. Fertil. 1988, 83:169-176.
62. Pommer A.C., Rutlant J., Meyers S.A. Phosphorylation of protein tyrosine residues in fresh and cryopreserved stallion spermatozoa under capacitating conditions. Biol. Reprod. 2003, 68:1208-1214.
63. Ramakrishnan M., Anbazhagan V., Pratap T.V., Marsh D., Swamy M.J. Membrane insertion and lipid-protein interactions of bovine seminal plasma protein PDC-109 investigated by spin-label electron spin resonance spectroscopy. Biophys. J. 2001, 81:2215-2225.
64. Saacke R.G., Nadir S., Nebel R.L. Relationship of semen quality to sperm quality, fertilization and embryo quality in ruminants. Theriogenology 1994, 40:1207-1214.
65. +)-ATPase. J. Androl. 2004, 25(2):234-244.
66. Sankhala R.S., Damai R.S., Anbazhagan V., Sudheer Kumar C., Bulusu G., Swamy M.J. Biophysical investigations on the interaction of the major bovine seminal plasma protein, PDC-109, with heparin. J. Phys. Chem. B 2011, 115(44):12954-12962.
67. Sankhala R.S., Damai R.S., Swamy M.J. Correlation of membrane binding and hydrophobicity to the chaperone-like activity of PDC-109, the major protein of bovine seminal plasma. PLoS ONE 2011, 6(3):e17330. 10.1371/journal.pone.0017330.
68. Scolari S., Muller K., Bittman R., Herrmann A., Muller P. Interaction of mammalian seminal plasma protein PDC-109 with cholesterol: implications for a putative CRAC domain. Biochemistry 2010, 49(42):9027-9031.
69. Seidah N.G., Manjunath P., Rochemont J., Sairam M.R., Chrétien M. Complete amino acid sequence of BSP-A3 from bovine seminal plasma. Homology to PDC-109 and to the collagen-binding domain of fibronectin. Biochem. J. 1987, 243:195-203.
70. Singh L.P., Harshan H.M., Ansari M.R. Effect of egg yolk and seminal plasma heparin binding protein interaction on the freezability of buffalo cauda epididymal spermatozoa. Anim. Reprod. Sci. 2007, 99:395-400.
71. 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.
72. Srivastava, N., 2011. Studies on sequestration of PDC-109 protein on cryodamage and in vitro fertility of crossbred bull spermatozoa. Ph.D. Thesis submitted to Deemed University. IVRI, Izat nagar, UP, India.
73. Srivastava N., Srivastava S.K., Ghosh S.K., Singh L.P., Prasad J.K., Amit Kumar, Peru mal P., Jerome A., Thamizharasan A. Sequestration of PDC-109 protein improves freezability of crossbred bull spermatozoa. Anim. Reprod. Sci. 2012, 131:54-62.
74. Suarez S.S. Sperm transport and motility in the mouse oviduct: observations in situ. Biol. Reprod. 1987, 36:203-210.
75. Suarez S.S., Ho H.C. Hyperactivated motility in sperm. Reprod. Domest. Anim. 2003, 38:119-124.
76. Swamy M.J. Interaction of bovine seminal plasma proteins with model membranes and sperm plasma membranes. Curr. Sci. 2004, 87:203-211.
77. Tannert A., Kurz A., Erlemann, Karl-Rudolf, Müller K., Herrmann A., Schiller J., Töpfer-Petersen E., Manjunath P., Müller P. The bovine seminal plasma protein PDC-109 extracts phosphorylcholine-containing lipids from the outer membrane leaf let. Eur. Biophys. J. 2007, 36:461-475.
78. Tannert A., Töpfer-Petersen E., Herrmann A., Müller K., Müller P. The lipid composition modulates the influence of the bovine seminal plasma protein PDC-109 on membrane stability. Biochemistry 2007, 46(41):11621-11629.
79. Triphan J., Aumü ller G., Brandenburger T., Wilhelm B. Localization and regulation of plasma membrane Ca2+-ATPase in bovine spermatozoa. Eur. J. Cell Biol. 2007, 86:265-273.
80. Tatemoto K., Mutt V. Isolation of two novel candidate hormones using a chemical method for finding naturally occurring polypeptides. Nature 1980, 285(5):417-418.
81. Therien I., Bleau G., Manjunath P. Phosphatidylcholine-binding proteins of bovine seminal plasma modulates capacitation of spermatozoa by heparin. Biol. Reprod. 1995, 52:1372-1379.
82. 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.
83. Therien I., Moreau R., Manjunath P. Bovine seminal plasma phospholipids binding proteins stimulate phospholipids efflux from epididymal sperm. Biol. Reprod. 1999, 61:590-598.
84. Therien I., Souberyrand S., Manjunath P. Major proteins of bovine seminal plasma modulate sperm capacitation by high-density lipoprotein. Biol. Reprod. 1997, 57:1080-1088.
85. Thomas C.J., Anbazhagan V., Ramakrishna M., Sultan N., Surolia I., Swamy M.J. Mechanism of membrane binding by the bovine seminal plasma protein, PDC-109: a surface resonance study. Biophys. J. 2003, 84:3037-3044.
86. Villemoure M., Lazure C., Manjunath P. Isolation and characterization of gelatin-binding proteins from goat seminal plasma. Reprod. Biol. Endocrinol. 2003, 1:39.
87. Vishwanath R., Shannon P., Curson B. Cationic extracts of egg yolk and their effect on motility, survival and fertilizing ability of bull sperm. Anim. Reprod. Sci. 1992, 29:185-194.
88. Wah D.A., Fernandez-Tornero C., Sanz L., Romero L., Calvete J.J. Sperm coating mechanisms from the 1.8Å crystal structure of PDC-109 phosphorylcholine complex. Structure 2002, 10:505-514.
89. Watson P.F. Use of Giemsa stain to detect changes in the acrosome of frozen ram spermatozoa. Vet. Rec. 1975, 97:12-15.
90. Watson P.F. The effect of cold shock on sperm cell membrane. Effects of Low Temperature on Biological Membranes 1981, 189-218. Academic Press, London. G.J. Morris, A. Clarke (Eds.).
91. Witte T.S., Schafer-Somi S. Involvement of cholesterol, calcium and progesterone in the induction of capacitation and acrosome reaction of mammalian spermatozoa. Anim. Reprod. Sci. 2007, 102:181-193.