Tyrosine phosphorylation generates multiple isoforms of the mitochondrial capsule protein, phospholipid hydroperoxide glutathione peroxidase (PHGPx), during hamster sperm capacitation

Biology of Reproduction

Volumn 72, Issue 1, 2005, Pages 164-171

  NagDas, Subir K ^a   Winfrey, Virginia P ^a   Olson, Gary E ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

PHCPx; Signal transduction; Sperm; Sperm capacitation; Sperm mitochondria; Tyrosine phosphorylation

Indexed keywords

DISULFIDE; DITHIOTHREITOL; ISOPROTEIN; MITOCHONDRIAL PROTEIN; MONOCLONAL ANTIBODY; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; PHOSPHOTYROSINE; POLYPEPTIDE; TRITON X 100;

ANIMAL CELL; ANION EXCHANGE CHROMATOGRAPHY; ARTICLE; BIBLIOGRAPHIC DATABASE; CONTROLLED STUDY; CROSS LINKING; FERTILIZATION; HAMSTER; IMMUNOAFFINITY CHROMATOGRAPHY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; ISOELECTRIC FOCUSING; ISOELECTRIC POINT; MALE; MITOCHONDRION; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; SEXUAL MATURATION; SIGNAL TRANSDUCTION; SOLUBILIZATION; SPERMATOZOON CAPACITATION; SPERMATOZOON TAIL; TANDEM MASS SPECTROMETRY;

AMINO ACID SEQUENCE; ANIMALS; CRICETINAE; EPIDIDYMIS; FLUORESCENT ANTIBODY TECHNIQUE; GLUTATHIONE PEROXIDASE; ISOENZYMES; MALE; MESOCRICETUS; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHOSPHORYLATION; SPERM CAPACITATION; SPERM TAIL; TYROSINE;

ANIMALIA; BOVINAE; CRICETINAE;

EID: 10944240463     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.104.033530     Document Type: Article

References (56)

1. Yanagimachi R. Mammalian Fertilization. In: Knobil E, Neill JD (eds.), The Physiology of Reproduction, 2nd ed. New York: Raven Press; 1993: 189-317.
2. Cross NL. Role of cholesterol in sperm capacitation. Biol Reprod 1998; 59:7-11.
3. Visconti PE, Kopf GS. Regulation of protein phosphorylation during sperm capacitation. Biol Reprod 1998; 59:1-6.
4. 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.
5. Cohen-Dayag A, Eisenbach M. Potential assays for sperm capacitation in mammals. Am J Physiol Cell Physiol 1994; 267:C1167-1176.
6. Chang MC. Development of fertilizing capacity of rabbit spermatozoa in the uterus. Nature 1955; 175:1036-1037.
7. Chang MC. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 1951; 168:697-698.
8. Austin CR. Observations on the penetration of the sperm into the mammalian egg. Aust J Sci Res 1951; 4:581-596.
9. Austin CR. The "capacitation" of the mammalian sperm. Nature 1952; 170:326.
10. 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.
11. 2 is not required for zona pellucidaor progesterone-induced acrosomal exocytosis of mouse spermatozoa but is essential for capacitation. Biol Reprod 1995; 52:540-546.
12. Yanagimachi R. The movement of golden hamster spermatozoa before and after capacitation. J Reprod Fertil 1970; 23:193-196.
13. Ho H-C, Suarez SS. Hyperactivation of mammalian spermatozoa: function and regulation. Reproduction 2000; 122:519-526.
14. Florman HM, Babcock DF. Progress Toward Understanding the Molecular Basis of Capacitation. Boca Raton, FL: CRC Press; 1991.
15. Travis AJ, Kopf GS. The role of cholesterol efflux in regulating the fertilization potential of mammalian spermatozoa. J Clin Invest 2002; 110:731-736.
16. Visconti PE, Galantinohomer H, Moore GD, Bailey JL, Ning X, Fornes M, Kopf GS. The molecular basis of sperm capacitation. J Androl 1998; 19:242-248.
17. Visconti PE, Westbrook VA, Chertihin O, Demarco I, Sleight S, Diekman AB. Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 2002; 53:133-150.
18. Wolf D, Hagopian S, Ishijima S. Changes in sperm plasma membrane lipid diffusibility after hyperactivation during in vitro capacitation in the mouse. J Cell Biol 1986; 102:1372-1377.
19. Langlais J, Roberts KD. A molecular membrane model of sperm capacitation and the acrosome reaction of mammalian spermatozoa. Gamete Res 1985; 12:183-224.
20. Suzuki F, Yanagimachi R. Changes in the distribution of intramembranous particles and filipin-reactive membrane sterols during in vitro capacitation of golden hamster spermatozoa. Gamete Res 1989; 23: 335-347.
21. Go K, Wolf D. Albumin-mediated changes in sperm sterol content during capacitation. Biol Reprod 1985; 32:145-153.
22. Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P, Kopf GS. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 1995; 1121:1129-1137.
23. DasGupta S, Mills C, Fraser L. Ca(2+)-related changes in the capacitation state of human spermatozoa assessed by a chlortetracycline fluorescence assay. J Reprod Fertil 1993; 99:135-143.
24. Baker MA, Hetherington L, Ecroyd H, Roman SD, Aitken RJ. Analysis of the mechanism by which calcium negatively regulates the tyrosine phosphorylation cascade associated with sperm capacitation. J Cell Sci 2004; 117:211-222.
25. Visconti PE, Stewart-Savage J, Blasco A, Battaglia L, Miranda P, Kopf GS, Tezon JG. Roles of bicarbonate, cAMP, and protein tyrosine phosphorylation on capacitation and the spontaneous acrosome reaction of hamster sperm. Biol Reprod 1999; 61:76-84.
26. Carrera A, Moos J, Ning XP, Gerton GL, Kopf GS, Moss SB. Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin- dependent mechanism: identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation. Dev Biol 1996; 180:284-296.
27. Galantino-Homer HL, Visconti PE, Kopf GS. Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3,′ 5′-monophosphate-dependent pathway. Biol Reprod 1997; 56:707-719.
28. Emiliozzi C, Fenichel P. Protein tyrosine phosphorylation is associated with capacitation of human sperm in vitro but is not sufficient for its completion. Biol Reprod 1997; 56:674-679.
29. Leclerc P, de Lamirande E, Gagnon C. Cyclic adenosine 3′,5′monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol Reprod 1996; 55:684-692.
30. Kopf GS, Visconti PE, Galantino-Homer H. Capacitation of the mammalian spermatozoon. Adv Dev Biochem 1999; 5:83-107.
31. Jaiswal BS, Eisenbach M. Capacitation. San Diego, CA: Academic Press; 2002.
32. Aitken R, Paterson M, Fisher H, Buckingham D, van Duin M. Redox regulation of tyrosine phosphorylation in human spermatozoa and its role in the control of human sperm function. J Cell Sci 1995; 108: 2017-2025.
33. Naaby-Hansen S, Mandai A, Wolkowicz MJ, Sen B, Westbrook VA, Shetty J, Coonrod SA, Klotz KL, Kim Y-H, Bush LA, Flickinger CJ, Herr JC. CABYR, a novel calcium-binding tyrosine phosphorylation-regulated fibrous sheath protein involved in capacitation. Dev Biol 2002; 242:236-254.
34. Ficarro S, Chertihin O, Westbrook VA, White F, Jayes F, Kalab P, Marto JA, Shabanowitz J, Herr JC, Hunt DF, Visconti PE. Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/n97 during capacitation. J Biol Chem 2003; 278:11579-11589.
35. Visconti PE, Johnson LR, Oyaski M, Fornes M, Moss SB, Gerton GL, Kopf GS. Regulation, localization, and anchoring of protein kinase A subunits during mouse sperm capacitation. Dev Biol 1997; 192:351-363.
36. Carrera A, Gerton GL, Moss SB. The major fibrous sheath polypeptide of mouse sperm: structural and functional similarities to the A-kinase anchoring proteins. Dev Biol 1994; 165:272-284.
37. Vijayaraghavan S, Gouelis SA, Davey MP, Carr DW. Protein kinase A-anchoring inhibitor peptides arrest mammalian sperm motility. J Biol Chem 1997; 272:4747-4752.
38. Ursini F, Heim S, Kiess M, Maiorino M, Roveri A, Wissing J, Flohe L. Dual function of the selenoprotein PHGPx during sperm maturation. Science 1999; 285:1393-1396.
39. Kopf GS. Zona pellucida-mediated signal transduction in mammalian spermatozoa. J Reprod Fertil Suppl 1990; 42:33-49.
40. Ohzu E, Yanagimachi R. Acceleration of acrosome reaction in hamster spermatozoa by lysolecithin. J Exp Zool 1982; 224:259-263.
41. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 1976; 72:248-254.
42. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-685.
43. Fairbanks G, Steck TL, Wallach DFH. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry 1971; 10:2606-2617.
44. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci 1979; 76:4350-4354.
45. NagDas SK, Winfrey VP, Olson GE. Proacrosin-acrosomal matrix binding interactions in ejaculated bovine spermatozoa. Biol Reprod 1996; 54:111-121.
46. Si Y, Okuno M. Role of tyrosine phosphorylation of flagellar proteins in hamster sperm hyperactivation. Biol Reprod 1999; 61:240-246.
47. Kalab P, Peknicova J, Geussova G, Moos J. Regulation of protein tyrosine phosphorylation in boar sperm through a cAMP-dependent pathway. Mol Reprod Devel 1998; 51:304-314.
48. Roveri A, Flohe L, Maiorino M, Ursini F. Phospholipid-hydroperoxide glutathione peroxidase in sperm. Meth Enzymol 2002; 347:208-212.
49. Roveri A, Maiorino M, Ursini F. Enzymatic and immunological measurements of soluble and membrane-bound phospholipid-hydroperoxide glutathione peroxidase. Meth Enzymol 1994; 233:202-212.
50. Nam SY, Fujisawa M, Kim JS, Kurohmaru M, Hayashi Y. Expression pattern of phospholipid hydroperoxide glutathione peroxidase messenger ribonucleic acid in mouse testis. Biol Reprod 1998; 58:1272-1276.
51. Calvin HI, Grosshans K, Musicant-Shikora SR, Turner SI. A developmental study of rat sperm and testis selenoproteins. J Reprod Fertil 1987; 81:1-11.
52. Roveri A, Ursini F, Flohe L, Maiorino M. PHGPx and spermatogenesis. Biofactors 2001; 14:213-222.
53. Imai H, Suzuki K, Ishizaka K, Ichinose S, Oshima H, Okayasu I, Emoto K, Umeda M, Nakagawa Y. Failure of the expression of phospholipid hydroperoxide glutathione peroxidase in the spermatozoa of human infertile males. Biol Reprod 2001; 64:674-683.
54. Foresta C, Flohe L, Garolla A, Roveri A, Ursini F, Maiorino M. Male fertility is linked to the selenoprotein phospholipid hydroperoxide glutathione peroxidase. Biol Reprod 2002; 67:967-971.
55. Hiraoka J-I, Hirao Y-H. Fate of sperm tail components after incorporation into the hamster egg. Gamete Res 1988; 19:369-380.
56. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Intracellular compartments and protein sorting. In: Molecular Biology of the Cell, 4th ed. New York: Garland Science; 2002:659-710.