Evidence for the involvement of zinc in the association of CRISP1 with rat sperm during epididymal Maturation

Biology of Reproduction

Volumn 85, Issue 3, 2011, Pages 503-510

  Maldera, Julieta A ^a   Vasen, Gustavo ^a   Ernesto, Juan I ^a   Weigel Muñoz, Mariana ^a   Cohen, Débora J ^a   Cuasnicu, Patricia S ^a  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

Author keywords

Crisp1; Epididymis; Fertilization; Gamete biology; Sperm; Sperm maturation; Zinc

Indexed keywords

AVIDIN; CYSTEINE RICH SECRETORY PROTEIN 1; EDETIC ACID; EPIDIDYMAL SECRETORY PROTEIN; FLUORESCEIN ISOTHIOCYANATE; SODIUM CHLORIDE; TRYPTOPHAN; UNCLASSIFIED DRUG; ZINC;

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BIOTINYLATION; CONTROLLED STUDY; EPIDIDYMIS; EPIFLUORESCENCE MICROSCOPY; FLOW CYTOMETRY; IN VITRO STUDY; INCUBATION TIME; MALE; MOLECULAR WEIGHT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; RAT; SPERM; SPERMATOZOON TAIL; WESTERN BLOTTING;

ANIMALS; EPIDIDYMIS; MALE; MEMBRANE GLYCOPROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SPERMATOZOA; ZINC;

RATTUS;

EID: 80052537573     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.091439     Document Type: Article

References (55)

1. Cuasnicú PS, Cohen DJ, Ellerman DA, Busso D, Da Ros VG, Morgenfeld M. Changes in sperm proteins during epididymal maturation. In: Robaire B, Hinton BT (eds.), The Epididymis. From Molecules to Clinical Practice. New York: Kluwer Academic/Plenum Publishers; 2002:389-404.
2. Cornwall GA. New insights into epididymal biology and function. Hum Reprod Update 2009; 15:213-227.
3. Cameo MS, Blaquier JA. Androgen-controlled specific proteins in rat epididymis. J Endocrinol 1976; 69:317-324.
4. Hardy DM, Huang TTF, Driscoll WJ, Tung KSK, Wild GC. Purification and characterization of the primary acrosomal autoantigen of guinea pig epididymal spermatozoa. Biol Reprod 1988; 38:423-437.
5. Kasahara M, Gutknecht J, Brew K, Spurr N, Goodfellow PN. Cloning and mapping of a testis-specific gene with sequence similarity to a spermcoating glycoprotein gene. Genomics 1989; 5:527-534.
6. Mizuki N, Sarapata D, Garci{dotless}́a-Sanz JA, Kasahara M. The mouse male germ cell-specific gene Tpx-1: molecular structure, mode of expression in spermatogenesis, and sequence similarity to two nonmammalian genes. Mamm Genome 1992; 3:274-280.
7. Haendler B, Kratzschmar J, Theuring F, Schleuning WD. Transcripts for cysteine-rich secretory protein-1 (CRISP-1; DE/AEG) and the novel related CRISP-3 are expressed under androgen control in the mouse salivary gland. Endocrinology 1993; 133:192-198.
8. Kjeldsen L, Cowland JB, Johnsen AH, Borregaard N. SGP28, a novel matrix glycoprotein in specific granules of human neutrophils with similarity to a human testis-specific gene product and a rodent spermcoating glycoprotein. FEBS Lett 1996; 380:246-250.
9. Udby L, Bjartell A, Malm J, Egesten A, Lundwall A, Cowland JB, Borregaard N, Kjeldsen L. Characterization and localization of cysteinerich secretory protein 3 (CRISP-3) in the human male reproductive tract. J Androl 2005; 26:333-342.
10. Jalkanen J, Huhtaniemi I, Poutanen M. Mouse cysteine-rich secretory protein 4 (CRISP4): a member of the crisp family exclusively expressed in the epididymis in an androgen-dependent manner. Biol Reprod 2005; 72:1268-1274.
11. Nolan MA, Wu L, Bang HJ, Jelinsky SA, Roberts KP, Turner TT, Kopf GS, Johnston DS. Identification of rat cysteine-rich secretory protein 4 (Crisp4) as the ortholog to human CRISP1 and mouse Crisp4. Biol Reprod 2006; 74:984-991.
12. Morrissette J, Kratzschmar J, Haendler B, El-Hayek R, Mochca-Morales J, Martin BM, Jitandrakumar RP, Moss RL, Schleuning WD, Coronado R, Possani LD. Primary structure and properties of helothermine, a peptide that blocks ryanodine receptors. Biophys J 1995; 68:2280-2288.
13. Yamazaki Y, Morita T. Structure and function of snake venom cysteinerich secretory proteins. Toxicon 2004; 44:227-231.
14. Guo M, Teng M, Niu L, Liu Q, Huang Q, Hao Q. Crystal structure of the cysteine-rich secretory protein stecrisp reveals that the cysteine-rich domain has a K{thorn} channel inhibitor-like fold. J Biol Chem 2005; 280:12405-12412.
15. Gibbs GM, Roelants K, O'Bryan MK. The CAP superfamily: cysteinerich secretory proteins, antigen 5, and pathogenesis-related 1 proteins-roles in reproduction, cancer, and immune defense. Endocr Rev 2008; 29:865-897.
16. Kohane AC, Cameo MS, Piñeiro L, Garberi JC, Blaquier JA. Distribution and site of production of specific proteins in the rat epididymis. Biol Reprod 1980; 23:181-187.
17. Kohane AC, Gonzalez Echeverria F, Piñeiro L, Blaquier JA. Interaction of proteins of epididymal origin with spermatozoa. Biol Reprod 1980; 23:737-742.
18. Cameo MS, Gonzalez Echeverria MF, Blaquier JA, Burgos MH. Immunochemical localization of epididymal protein DE on rat spermatozoa: its fate after induced acrosome reaction. Gamete Res 1986; 15:247-258.
19. Roberts KP, Ensrud KM, Hamilton DW. A comparative analysis of expression and processing of the rat epididymal fluid and sperm-bound forms of proteins D and E. Biol Reprod 2002; 67:525-533.
20. Cohen DJ, Rochwerger L, Ellerman DA, Morgenfeld M, Busso D, Cuasnicu PS. Relationship between the association of rat epididymal protein DE with spermatozoa and the behavior and function of the protein. Mol Reprod Dev 2000; 56:180-188.
21. Roberts KP, Ensrud KM, Wooters JL, Nolan MA, Johnston DS, Hamilton DW. Epididymal secreted protein Crisp-1 and sperm function. Mol Cell Endocrinol 2006; 250:122-127.
22. Rochwerger L, Cuasnicu PS. Redistribution of a rat sperm epididymal glycoprotein after in vivo and in vitro capacitation. Mol Reprod Dev 1992; 31:34-41.
23. Busso D, Cohen DJ, Maldera JA, Dematteis A, Cuasnicu PS. A novel function for CRISP1 in rodent fertilization: involvement in sperm-zona pellucida interaction. Biol Reprod 2007; 77:848-854.
24. Rochwerger L, Cohen DJ, Cuasnicú PS. Mammalian sperm-egg fusion: the rat egg has complementary sites for a sperm protein that mediates gamete fusion. Dev Biol 1992; 153:83-90.
25. Da Ros VG, Maldera JA, Willis WD, Cohen DJ, Goulding EH, Gelman DM, Rubinstein M, Eddy EM, Cuasnicu PS. Impaired sperm fertilizing ability in mice lacking cysteine-rich secretory protein 1 (CRISP1). Dev Biol 2008; 320:12-18.
26. 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.
27. 2+ signaling. J Biol Chem 2006; 281:4156-4163.
28. Mawson CA, Fischer MI. Zinc content of the genital organs of the rat. Nature 1951; 167:859.
29. Stoltenberg M, Ernst E, Andreasen A, Danscher G. Histochemical localization of zinc ions in the epididymis of the rat. Histochem J 1996; 28:173-185.
30. 2+-channel blocker derived from snake venom. J Mol Biol 2005; 350:735-743.
31. Suzuki N, Yamazaki Y, Brown RL, Fujimoto Z, Morita T, Mizuno H Structures of pseudechetoxin and pseudecin, two snake-venom cysteinerich secretory proteins that target cyclic nucleotide-gated ion channels: implications for movement of the C-terminal cysteine-rich domain. Acta Crystallogr D Biol Crystallogr 2008; 64:1034-1042.
32. 2+- and heparan sulfate-dependent transcriptional regulation of endothelial cell adhesion molecules. J Biol Chem 2010; 285:37872-37883.
33. Sansone G, Martino M, Abrescia P. Binding of free and protein-associated zinc to rat spermatozoa. Comp Biochem Physiol C Toxicol Pharmacol 1991; 99:113-117.
34. Sansone G, Abrescia P. Zinc-protein from rat prostate fluid binds epididymal spermatozoa. J Exp Zool 1991; 259:379-385.
35. Garberi JC, Kohane AC, Cameo MS, Blaquier JA. Isolation and characterization of specific rat epididymal proteins. Mol Cell Endocrinol 1979; 13:73-82.
36. Garberi JC, Fontana JD, Blaquier JA. Carbohydrate composition of specific rat epididymal protein. Int J Androl 1982; 5:619-626.
37. Kohane AC, Piñeiro L, Blaquier JA. Androgen-controlled synthesis of specific protein in the rat epididymis. Endocrinology 1983; 112:1590- 1596.
38. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-685.
39. Hames BD. An introduction to polyacrylamide gel electrophoresis. In: Hames BD, Rickwood D (eds.), Gel Electrophoresis of Proteins. Oxford: IRL Press; 1981:1-86.
40. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 1979; 76:4350-4360.
41. Stray SJ, Ceres P, Zlotnick A. Zinc ions trigger conformational change and oligomerization of hepatitis B virus capsid protein. Biochemistry 2004; 43:9989-9998.
42. Glaser RW, Grune M, Wandelt C, Ulrich AS. Structure analysis of a fusogenic peptide sequence from the sea urchin fertilization protein bindin. Biochemistry 1999; 38:2560-2569.
43. Roberts KP, Ensrud-Bowlin KM, Piehl LB, Parent KR, Bernhardt ML, Hamilton DW. Association of the protein D and protein E forms of rat CRISP1 with epididymal sperm. Biol Reprod 2008; 79:1046-1053.
44. Saez F, Frenette G, Sullivan R. Epididymosomes and prostasomes: their roles in posttesticular maturation of the sperm cells. J Androl 2003; 24:149-154.
45. Oh JS, Han C, Cho C. ADAM7 is associated with epididymosomes and integrated into sperm plasma membrane. Mol Cells 2009; 28:441-446.
46. de Larminat MA, Cuasnicu PS, Blaquier JA. Changes in trophic and functional parameters of the rat epididymis during sexual maturation. Biol Reprod 1981; 25:813-819.
47. Saito S, Zeitz L, Bush IM, Lee R, Whitmore WF Jr. Zinc uptake in canine or rat spermatozoa. Am J Physiol 1969; 217:1039-1043.
48. Mawson CA, Fischer MI. Zinc and carbonic anhydrase in human semen. Biochem J 1953; 55:696-700.
49. Arver S, Eliasson R. Zinc and magnesium in bull and boar spermatozoa. J Reprod Fertil 1980; 60:481-484.
50. Andrews JC, Nolan JP, Hammerstedt RH, Bavister BD. Role of zinc during hamster sperm capacitation. Biol Reprod 1994; 51:1238-1247.
51. Huang YH, Chu ST, Chen YH. A seminal vesicle autoantigen of mouse is able to suppress sperm capacitation-related events stimulated by serum albumin. Biol Reprod 2000; 63:1562-1566.
52. Fornes MW, Burgos MH. Epididymal glycoprotein involved in rat sperm association. Mol Reprod Dev 1994; 38:43-47.
53. Huang YH, Luo CW, Yu LC, Chu ST, Chen YH. The protein conformation and a zinc-binding domain of an autoantigen from mouse seminal vesicle. Biophys J 1995; 69:2084-2089.
54. Ulrich AS, Otter M, Glabe CG, Hoekstra D. Membrane fusion is induced by a distinct peptide sequence of the sea urchin fertilization protein bindin. J Biol Chem 1998; 273:16748-16755.
55. Frenette G, Lessard C, Sullivan R. Selected proteins of "prostasome-like particles" from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol Reprod 2002; 67:308-313.