Characterization of recombinant murine binder of sperm protein homolog 1 and its: Role in capacitation

Biology of Reproduction

Volumn 87, Issue 1, 2012, Pages 20-

  Plante, Genevie've ^a,b   Thérien, Isabelle ^a   Manjunath, Puttaswamy ^a,b  

^a UNIVERSITY OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Binder of sperm (BSP) proteins; Epididymal protein; Fibronectin (Fn) 2 domains; Murine sperm capacitation; Recombinant protein expression

Indexed keywords

BINDER OF SPERM PROTEIN HOMOLOG 1 PROTEIN; BOVINE SERUM ALBUMIN; GELATIN; HEPARIN; LIPOSOME; PHOSPHATIDYLCHOLINE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; BSPH 1 PROTEIN, MOUSE; BSPH-1 PROTEIN, MOUSE; PRIMER DNA; SEMINAL VESICLE SECRETORY PROTEIN;

ACROSOME REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; DNA SEQUENCE; EPIDIDYMIS; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SECRETION; SEMINAL VESICLE; SEQUENCE HOMOLOGY; SPERMATOZOON CAPACITATION; SPERMATOZOON HEAD; SPERMATOZOON MIDPIECE; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; FEMALE; GENETICS; IMMUNOHISTOCHEMISTRY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN BINDING;

BOVINAE; MURINAE; UNGULATA;

ACROSOME REACTION; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; DNA PRIMERS; EPIDIDYMIS; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED ICR; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RECOMBINANT PROTEINS; SEMINAL VESICLE SECRETORY PROTEINS; SPERM CAPACITATION; SPERM HEAD; SPERM MIDPIECE;

EID: 84869213420     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.096644     Document Type: Article

References (60)

1. Chang MC. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 1951; 168:697-698.
2. Austin CR. Observations on the penetration of the sperm in the mammalian egg. Aust J Sci Res B 1951; 4:581-596.
3. Langlais J, Roberts KD. A molecular membrane model of sperm capacitation and the acrosome reaction of mammalian spermatozoa. Gamete Res 1985; 12:183-224.
4. Go KJ, Wolf DP. The role of sterols in sperm capacitation. Adv Lipid Res 1983; 20:317-330.
5. Suarez SS. Hyperactivated motility in sperm. J Androl 1996; 17:331-335.
6. Visconti PE, Kopf GS. Regulation of protein phosphorylation during sperm capacitation. Biol Reprod 1998; 59:1-6.
7. de Lamirande E, Leclerc P, Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 1997; 3:175-194.
8. Xia J, Ren D. The BSA-induced Ca2{thorn} influx during sperm capacitation is CATSPER channel-dependent. Reprod Biol Endocrinol 2009; 7:119.
9. Salicioni AM, Platt MD, Wertheimer EV, Arcelay E, Allaire A, Sosnik J, Visconti PE. Signalling pathways involved in sperm capacitation. Soc Reprod Fertil Suppl 2007; 65:245-259.
10. Manjunath P, Lefebvre J, Jois PS, Fan J, Wright MW. New nomenclature for mammalian BSP genes. Biol Reprod 2009; 80:394-397.
11. Manjunath P. Gonadotropin release stimulatory and inhibitory proteins in bull seminal plasma. In: Sairam MR, Atkinson LE (eds.), Gonadal Proteins and Peptides and Their Biological Significance. Singapore: World Science Publishing; 1984:49-61.
12. Manjunath P, Sairam MR. Purification and biochemical characterization of three major acidic proteins (BSP-A1, BSP-A2 et BSP-A3) from bovine seminal plasma. Biochem J 1987; 241:685-692.
13. Manjunath P, Sairam MR, Uma J. Purification of four gelatin-binding proteins from bovine seminal plasma by affinity chromatography. Biosci Rep 1987; 7:231-238.
14. Desnoyers L, Manjunath P. Major proteins of bovine seminal plasma exhibit novel interactions with phospholipid. J Biol Chem 1992; 267: 10149-10155.
15. Therien I, Soubeyrand S, Manjunath P. Major proteins of bovine seminal plasma modulate sperm capacitation by high-density lipoprotein. Biol Reprod 1997; 57:1080-1088.
16. Therien I, Bleau G, Manjunath P. Phosphatidylcholine-binding proteins of bovine seminal plasma modulate capacitation of spermatozoa by heparin. Biol Reprod 1995; 52:1372-1379.
17. Therien I, Bergeron A, Bousquet D, Manjunath P. Isolation and characterization of glycosaminoglycans from bovine follicular fluid and their effect on sperm capacitation. Mol Reprod Dev 2005; 71:97-106.
18. Gwathmey TM, Ignotz GG, Suarez SS. 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.
19. Sankhala RS, Swamy MJ. The major protein of bovine seminal plasma, PDC-109, is a molecular chaperone. Biochemistry 2010; 49:3908-3918.
20. Menard 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.
21. Calvete JJ, 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.
22. Villemure M, Lazure C, Manjunath P. Isolation and characterization of gelatin-binding proteins from goat seminal plasma. Reprod Biol Endocrinol 2003; 1:39.
23. 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.
24. 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.
25. Calvete JJ, 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 gelatinbinding capabilities. Biochem J 1995; 310:615-622.
26. Lusignan M-F, Bergeron A, 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.
27. Manjunath P, Nauc V, Bergeron A, Menard M. Major proteins of bovine seminal plasma bind to the low-density lipoprotein fraction of hen's egg yolk. Biol Reprod 2002; 67:1250-1258.
28. Fan J, Lefebvre J, Manjunath P. Bovine seminal plasma proteins and their relatives: a new expanding superfamily in mammals. Gene 2006; 375: 63-74.
29. Lefebvre J, Fan J, Chevalier S, Sullivan R, Carmona E, Manjunath P. Genomic structure and tissue-specific expression of human and mouse genes encoding homologs of the major bovine seminal plasma proteins. Mol Hum Reprod 2007; 13:45-53.
30. Lane M, Therien I, Moreau R, Manjunath P. Heparin and high-density lipoprotein mediate bovine sperm capacitation by different mechanisms. Biol Reprod 1999; 60:169-175.
31. Gwathmey TM, Ignotz GG, Mueller JL, Manjunath P, Suarez SS. Bovine seminal plasma proteins PDC-109, BSP-A3, and BSP-30-kDa share functional roles in storing sperm in the oviduct. Biol Reprod 2006; 74: 501-507.
32. Lemercier G, Bakalara N, Santarelli X. On-column refolding of an insoluble histidine tag recombinant exopolyphosphatase from Trypanosoma brucei overexpressed in Escherichia coli. J Chromatogr B Analyt Technol Biomed Life Sci 2003; 786:305-309.
33. Havlis J, Thomas H, Sebela M, Shevchenko A. Fast-response proteomics by accelerated in-gel digestion of proteins. Anal Chem 2003; 75: 1300-1306.
34. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-685.
35. Lefebvre J, Boileau G, Manjunath P. Recombinant expression and affinity purification of a novel epididymal human sperm-binding protein, BSPH1. Mol Hum Reprod 2009; 15:105-114.
36. Moore GD, Ayabe T, Visconti PE, Schultz RM, Kopf GS. Roles of heterotrimeric and monomeric G proteins in sperm-induced activation of mouse eggs. Development 1994; 120:3313-3323.
37. Moller CC, Bleil JD, Kinloch RA, Wassarman PM. Structural and functional relationships between mouse and hamster zona pellucida glycoproteins. Dev Biol 1990; 137:276-286.
38. Ward CR, Storey BT. Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay. Dev Biol 1984; 104:287-296.
39. Gasset M, Saiz JL, Laynez J, Sanz L, Gentzel M, Topper-Petersen E, Calvete JJ. Conformational features and thermal stability of bovine seminal plasma protein PDC-109 oligomers and phosphorylcholine-bound complexes. Eur J Biochem 1997; 250:735-744.
40. Calvete JJ, Reinert M, Sanz L, Topfer-Petersen E. Effect of glycosylation on the heparin-binding capability of boar and stallion seminal plasma proteins. J Chromatogr A 1995; 711:167-173.
41. Salek-Ardakani S, Arrand JR, Shaw D, Mackett M. Heparin and heparan sulfate bind interleukin-10 and modulate its activity. Blood 2000; 96: 1879-1888.
42. Hileman RE, Fromm JR, Weiler JM, Linhardt RJ. Glycosaminoglycanprotein interactions: definition of consensus sites in glycosaminoglycan binding proteins. Bioessays 1998; 20:156-167.
43. Leblond E, Desnoyers L, Manjunath P. Phosphorylcholine-binding proteins from the seminal fluids of different species share antigenic determinants with the major proteins of bovine seminal plasma. Mol Reprod Dev 1993; 34:443-449.
44. Wah DA, Fernandez-Tornero C, Sanz L, Romero A, Calvete JJ. Sperm coating mechanism from the 1.8 A crystal structure of PDC-109-phosphorylcholine complex. Structure (Camb) 2002; 10:505-514.
45. Rejraji H, Sion B, Prensier G, Carreras M, Motta C, Frenoux JM, Vericel E, Grizard G, Vernet P, Drevet JR. Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol Reprod 2006; 74:1104-1113.
46. Manjunath P, Chandonnet L, Leblond E, Desnoyers L. Major proteins of bovine seminal vesicles bind to spermatozoa. Biol Reprod 1994; 50: 27-37.
47. Calvete JJ, Raida M, Sanz L, Wempe F, Scheit KH, 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.
48. Souza CE, Moura AA, Monaco E, Killian GJ. 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.
49. Sanchez-Luengo S, Aumuller G, Albrecht M, Sen PC, Rohm K, Wilhelm B. Interaction of PDC-109, the major secretory protein from bull seminal vesicles, with bovine sperm membrane Ca2{thorn}-ATPase. J Androl 2004; 25: 234-244.
50. Manjunath P, Bergeron A, Lefebvre J, Fan J. Seminal plasma proteins: functions and interaction with protective agents during semen preservation. Soc Reprod Fertil Suppl 2007; 65:217-228.
51. Roberts KP, Wamstad JA, Ensrud KM, Hamilton DW. Inhibition of capacitation-associated tyrosine phosphorylation signaling in rat sperm by epididymal protein Crisp-1. Biol Reprod 2003; 69:572-581.
52. Zhou Y, Zheng M, Shi Q, Zhang L, Zhen W, Chen W, Zhang Y. An epididymis-specific secretory protein HongrES1 critically regulates sperm capacitation and male fertility. PLoS One 2008; 3:e4106.
53. Katkov II, Mazur P. Influence of centrifugation regimes on motility, yield, and cell associations of mouse spermatozoa. J Androl 1998; 19:232-241.
54. Therien I, Bousquet D, Manjunath P. Effect of seminal phospholipidbinding proteins and follicular fluid on bovine sperm capacitation. Biol Reprod 2001; 65:41-51.
55. 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.
56. Zhao C, Guo XJ, Shi ZH, Wang FQ, Huang XY, Huo R, Zhu H, Wang XR, Liu JY, Zhou ZM, Sha JH. Role of translation by mitochondrial-type ribosomes during sperm capacitation: an analysis based on a proteomic approach. Proteomics 2009; 9:1385-1399.
57. Kawai Y, Takeiri A, Suzuki T, Suzuki Y, Miyake M. Anti-mouse sperm monoclonal antibody, A-1, inhibits sperm capacitation, acrosome reaction and calcium influx into spermatocytes. Biol Pharm Bull 2000; 23: 922-925.
58. Jonas A. Interaction of phosphatidylcholine with bovine serum albumin. Specificity and properties of the complexes. Biochim Biophys Acta 1976; 427:325-336.
59. Manjunath P, Therien I. Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. J Reprod Immunol 2002; 53:109-119.
60. Muller P, Erlemann KR, Muller K, Calvete JJ, Topfer-Petersen E, Marienfeld K, Herrmann A. Biophysical characterization of the interaction of bovine seminal plasma protein PDC-109 with phospholipid vesicles. Eur Biophys J 1998; 27:33-41.