Progesterone-induced reorganisation of NOX-2 components in membrane rafts is critical for sperm functioning in Capra hircus

Andrologia

Volumn 42, Issue 6, 2010, Pages 356-365

  Shoeb, M ^a   Laloraya, M ^a   Kumar, P G ^a  

^a RAJIV GANDHI CENTRE FOR BIOTECHNOLOGY   (India)

Author keywords

Acrosome reaction; Capacitation; NOX; Raft; Spermatozoa; Superoxide

Indexed keywords

CAVEOLIN; ESTRADIOL; METHYL BETA CYCLODEXTRIN; PROGESTERONE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SUPEROXIDE;

ACROSOME REACTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAPRA HIRCUS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME SUBUNIT; GOAT; IMMUNOFLUORESCENCE; IN VITRO STUDY; LIPID RAFT; MALE; NONHUMAN; SPERM; SPERM MEMBRANE RAFT; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MATURATION;

ACROSOME REACTION; ANIMALS; BETA-CYCLODEXTRINS; CAVEOLIN 1; GOATS; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE MICRODOMAINS; NADPH OXIDASE; PROGESTERONE; REACTIVE OXYGEN SPECIES; SPERM CAPACITATION; SPERMATOZOA;

EID: 78649555283     PISSN: 03034569     EISSN: 14390272     Source Type: Journal    
DOI: 10.1111/j.1439-0272.2009.01024.x     Document Type: Article

References (76)

1. Aitken RJ, Clarkson JS (1987) Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil 81:459-469.
2. Aitken RJ, Clarkson JS, Fishel S (1989) Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod 41:183-197.
3. Aitken RJ, Paterson M, Fisher H, Buckingham DW, Van DM (1995) Redox regulation of tyrosine phosphorylation in human spermatozoa and its role in the control of human sperm function. J Cell Sci 108:2017-2025.
4. Aitken RJ, Buckingham DW, Harkiss D, Paterson M, Fisher H, Irvine DS (1996) The extragenomic action of progesterone on human spermatozoa is influenced by redox regulated changes in tyrosine phosphorylation during capacitation. Mol Cell Endocrinol 117:83-93.
5. Aitken RJ, Harkiss D, Knox W, Paterson M, Irvine DS (1998) A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation. J Cell Sci 111:645-656.
6. Alvarez JG, Touchstone JC, Blasco L, Storey BT (1987) Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa. Superoxide dismutase as major enzyme protectant against oxygen toxicity. J Androl 8:338-348.
7. Aquila S, Sisci D, Gentile M, Middea E, Catalano S, Carpino A, Rago V, Ando S (2004) Estrogen receptor (ER)alpha and ER beta are both expressed in human ejaculated spermatozoa: evidence of their direct interaction with phosphatidylinositol-3-OH kinase/Akt pathway. J Clin Endocrinol Metab 89:1443-1451.
8. Babior BM (1999) NADPH oxidase: an update. Blood 93:1464-1476.
9. Baldi E, Luconi M, Muratori M, Marchiani S, Tamburrino L, Forti G (2009) Nongenomic activation of spermatozoa by steroid hormones: facts and fictions. Mol Cell Endocrinol 308:39-46.
10. Barnett-Norris J, Lynch D, Reggio PH (2005) Lipids, lipid rafts and caveolae: their importance for GPCR signaling and their centrality to the endocannabinoid system. Life Sci 77:1625-1639.
11. Baumber J, Sabeur K, Vo A, Ball BA (2003) Reactive oxygen species promote tyrosine phosphorylation and capacitation in equine spermatozoa. Theriogenology 60:1239-1247.
12. Borras C, Gambini J, Lopez-Grueso R, Pallardo FV, Vina J (2009) Direct antioxidant and protective effect of estradiol on isolated mitochondria. Biochim Biophys Acta (in press).
13. Botto L, Masserini M, Palestini P (2007) Changes in the composition of detergent-resistant membrane domains of cultured neurons following protein kinase C activation. J Neurosci Res 85:443-450.
14. Breitbart H, Naor Z (1999) Protein kinases in mammalian sperm capacitation and the acrosome reaction. Rev Reprod 4:151-159.
15. Brown DA, London E (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14:111-136.
16. Carreau S, Delalande C, Galeraud-Denis I (2009) Mammalian sperm quality and aromatase expression. Microsc Res Tech 72:552-557.
17. El-Benna J, Dang PM, Gougerot-Pocidalo MA, Marie JC, Braut-Boucher F (2009) p47phox, the phagocyte NADPH oxidase/NOX2 organizer: structure, phosphorylation and implication in diseases. Exp Mol Med 41:217-225.
18. Field KA, Holowka D, Baird B (1997) Compartmentalized activation of the high affinity immunoglobulin E receptor within membrane domains. J Biol Chem 272:4276-4280.
19. Fisher HM, Aitken RJ (1997) Comparative analysis of the ability of precursor germ cells and epididymal spermatozoa to generate reactive oxygen metabolites. J Exp Zool 277:390-400.
20. Furuya S, Endo Y, Oba M, Matsui Y, Nozawa S, Suzuki S (1992) Protein phosphorylation regulates the mouse sperm acrosome reaction induced by the zona pellucida. J Assist Reprod Genet 9:384-390.
21. (2+)-dependent isoenzymes of protein kinase C. Arch Biochem Biophys 348:25-36.
22. Griveau JF, Renard P, Le LD (1994) An in vitro promoting role for hydrogen peroxide in human sperm capacitation. Int J Androl 17:300-307.
23. Hamden K, Silandre D, Delalande C, El FA, Carreau S (2008a) Age-related decrease in aromatase and estrogen receptor (ERalpha and ERbeta) expression in rat testes: protective effect of low caloric diets. Asian J Androl 10:177-187.
24. Hamden K, Silandre D, Delalande C, Elfeki A, Carreau S (2008b) Protective effects of estrogens and caloric restriction during aging on various rat testis parameters. Asian J Androl 10:837-845.
25. Hayashi T, Juliet PA, Miyazaki A, Ignarro LJ, Iguchi A (2007) High glucose downregulates the number of caveolae in monocytes through oxidative stress from NADPH oxidase: implications for atherosclerosis. Biochim Biophys Acta 1772:364-372.
26. Herrero MB, De LE, Gagnon C (2003) Nitric oxide is a signaling molecule in spermatozoa. Curr Pharm Des 9:419-425.
27. Holland MK, Alvarez JG, Storey BT (1982) Production of superoxide and activity of superoxide dismutase in rabbit epididymal spermatozoa. Biol Reprod 27:1109-1118.
28. Hu G, Ye RD, Dinauer MC, Malik AB, Minshall RD (2008) Neutrophil caveolin-1 expression contributes to mechanism of lung inflammation and injury. Am J Physiol Lung Cell Mol Physiol 294:L178-L186.
29. Janes PW, Ley SC, Magee AI, Kabouridis PS (2000) The role of lipid rafts in T cell antigen receptor (TCR) signalling. Semin Immunol 12:23-34.
30. (2+) increase in response to progesterone and cyclic nucleotides in mouse spermatozoa. Biol Reprod 63:113-120.
31. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
32. DeLamirande E, Gagnon C (1993a) Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Radic Biol Med 14:157-166.
33. DeLamirande E, Gagnon C (1993b) A positive role for the superoxide anion in triggering hyperactivation and capacitation of human spermatozoa. Int J Androl 16:21-25.
34. DeLamirande E, Gagnon C (2002) The extracellular signal-regulated kinase (ERK) pathway is involved in human sperm function and modulated by the superoxide anion. Mol Hum Reprod 8:124-135.
35. DeLamirande E, Jiang H, Zini A, Kodama H, Gagnon C (1997) Reactive oxygen species and sperm physiology. Rev Reprod 2:48-54.
36. DeLamirande E, Harakat A, Gagnon C (1998a) Human sperm capacitation induced by biological fluids and progesterone, but not by NADH or NADPH, is associated with the production of superoxide anion. J Androl 19:215-225.
37. DeLamirande E, Tsai C, Harakat A, Gagnon C (1998b) Involvement of reactive oxygen species in human sperm arcosome reaction induced by A23187, lysophosphatidylcholine, and biological fluid ultrafiltrates. J Androl 19:585-594.
38. Leclerc P, De LE, Gagnon C (1996) Cyclic adenosine 3', 5'monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol Reprod 55:684-692.
39. Leclerc P, De LE, Gagnon C (1997) Regulation of protein-tyrosine phosphorylation and human sperm capacitation by reactive oxygen derivatives. Free Radic Biol Med 22:643-656.
40. Lefievre L, Jha KN, De LE, Visconti PE, Gagnon C (2002) Activation of protein kinase A during human sperm capacitation and acrosome reaction. J Androl 23:709-716.
41. Leshchyns'ka I, Sytnyk V, Morrow JS, Schachner M (2003) Neural cell adhesion molecule (NCAM) association with PKCbeta2 via betaI spectrin is implicated in NCAM-mediated neurite outgrowth. J Cell Biol 161:625-639.
42. Leyton L, Saling P (1989) 95 kd sperm proteins bind ZP3 and serve as tyrosine kinase substrates in response to zona binding. Cell 57:1123-1130.
43. Liguori L, DeLamirande E., Minelli A, Gagnon C (2005) Various protein kinases regulate human sperm acrosome reaction and the associated phosphorylation of Tyr residues and of the Thr-Glu-Tyr motif. Mol Hum Reprod 11:211-221.
44. Luconi M, Barni T, Vannelli GB, Krausz C, Marra F, Benedetti PA, Evangelista V, Francavilla S, Properzi G, Forti G, Baldi E (1998) Extracellular signal-regulated kinases modulate capacitation of human spermatozoa. Biol Reprod 58:1476-1489.
45. Luconi M, Muratori M, Forti G, Baldi E (1999) Identification and characterization of a novel functional estrogen receptor on human sperm membrane that interferes with progesterone effects. J Clin Endocrinol Metab 84:1670-1678.
46. Mongrand S, Morel J, Laroche J, Claverol S, Carde JP, Hartmann MA, Bonneu M, Simon-Plas F, Lessire R, Bessoule JJ (2004) Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J Biol Chem 279:36277-36286.
47. Moran M, Miceli MC (1998) Engagement of GPI-linked CD48 contributes to TCR signals and cytoskeletal reorganization: a role for lipid rafts in T cell activation. Immunity 9:787-796.
48. Natarajan V, Taher MM, Roehm B, Parinandi NL, Schmid HH, Kiss Z, Garcia JG (1993) Activation of endothelial cell phospholipase D by hydrogen peroxide and fatty acid hydroperoxide. J Biol Chem 268:930-937.
49. Nolan JP, Hammerstedt RH (1997) Regulation of membrane stability and the acrosome reaction in mammalian sperm. FASEB J 11:670-682.
50. O'Flaherty C, De LE, Gagnon C (2004) Phosphorylation of the arginine-X-X-(serine/threonine) motif in human sperm proteins during capacitation: modulation and protein kinase A dependency. Mol Hum Reprod 10:355-363.
51. Orito A, Kumanogoh H, Yasaka K, Sokawa J, Hidaka H, Sokawa Y, Maekawa S (2001) Calcium-dependent association of annexin VI, protein kinase C alpha, and neurocalcin alpha on the raft fraction derived from the synaptic plasma membrane of rat brain. J Neurosci Res 64:235-241.
52. Ostrom RS, Liu X, Head BP, Gregorian C, Seasholtz TM, Insel PA (2002) Localization of adenylyl cyclase isoforms and G protein-coupled receptors in vascular smooth muscle cells: expression in caveolin-rich and noncaveolin domains. Mol Pharmacol 62:983-992.
53. Parinandi NL, Scribner WM, Vepa S, Shi S, Natarajan V (1999) Phospholipase D activation in endothelial cells is redox sensitive. Antioxid Redox Signal 1:193-210.
54. Park JW, Benna JE, Scott KE, Christensen BL, Chanock SJ, Babior BM (1994) Isolation of a complex of respiratory burst oxidase components from resting neutrophil cytosol. Biochemistry 33:2907-2911.
55. Patel HH, Murray F, Insel PA (2008) G-protein-coupled receptor-signaling components in membrane raft and caveolae microdomains. Handb Exp Pharmacol 186:167-184.
56. Petrie RJ, Schnetkamp PP, Patel KD, Wasthi-Kalia M, Deans JP (2000) Transient translocation of the B cell receptor and Src homology 2 domain-containing inositol phosphatase to lipid rafts: evidence toward a role in calcium regulation. J Immunol 165:1220-1227.
57. Rashba-Step J, Tatoyan A, Duncan R, Ann D, Pushpa-Rehka TR, Sevanian A (1997) Phospholipid peroxidation induces cytosolic phospholipase A2 activity: membrane effects versus enzyme phosphorylation. Arch Biochem Biophys 343:44-54.
58. Rivlin J, Mendel J, Rubinstein S, Etkovitz N, Breitbart H (2004) Role of hydrogen peroxide in sperm capacitation and acrosome reaction. Biol Reprod 70:518-522.
59. Roy SC, Atreja SK (2008) Production of superoxide anion and hydrogen peroxide by capacitating buffalo (Bubalus bubalis) spermatozoa. Anim Reprod Sci 103:260-270.
60. Shao D, Segal AW, Dekker LV (2003) Lipid rafts determine efficiency of NADPH oxidase activation in neutrophils. FEBS Lett 550:101-106.
61. Shukla S, Jha RK, Laloraya M, Kumar PG (2005) Identification of non-mitochondrial NADPH oxidase and the spatio-temporal organization of its components in mouse spermatozoa. Biochem Biophys Res Commun 331:476-483.
62. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569-572.
63. Tan CM, Xenoyannis S, Feldman RD (1995) Oxidant stress enhances adenylyl cyclase activation. Circ Res 77:710-717.
64. 2+ influx. Biochem J 264:539-546.
65. Thundathil J, De LE, Gagnon C (2002) Different signal transduction pathways are involved during human sperm capacitation induced by biological and pharmacological agents. Mol Hum Reprod 8:811-816.
66. Torgersen KM, Vang T, Abrahamsen H, Yaqub S, Tasken K (2002) Molecular mechanisms for protein kinase A-mediated modulation of immune function. Cell Signal 14:1-9.
67. Travis AJ, Merdiushev T, Vargas LA, Jones BH, Purdon MA, Nipper RW, Galatioto J, Moss SB, Hunnicutt GR, Kopf GS (2001) Expression and localization of caveolin-1, and the presence of membrane rafts, in mouse and Guinea pig spermatozoa. Dev Biol 240:599-610.
68. Vang T, Torgersen KM, Sundvold V, Saxena M, Levy FO, Skalhegg BS, Hansson V, Mustelin T, Tasken K (2001) Activation of the COOH-terminal Src kinase (Csk) by cAMP-dependent protein kinase inhibits signaling through the T cell receptor. J Exp Med 193:497-507.
69. Vernet P, Fulton N, Wallace C, Aitken RJ (2001) Analysis of reactive oxygen species generating systems in rat epididymal spermatozoa. Biol Reprod 65:1102-1113.
70. Vignais PV (2002) The superoxide-generating NADPH oxidase: structural aspects and activation mechanism. Cell Mol Life Sci 59:1428-1459.
71. Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P, Kopf GS (1995a) Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121:1129-1137.
72. Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, Olds-Clarke P, Kopf GS (1995b) Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121:1139-1150.
73. 2+ wave propagation in glial cells. Cell Calcium 41:155-167.
74. Xavier R, Brennan T, Li Q, McCormack C, Seed B (1998) Membrane compartmentation is required for efficient T cell activation. Immunity 8:723-732.
75. Yang B, Rizzo V (2007) TNF-alpha potentiates protein-tyrosine nitration through activation of NADPH oxidase and eNOS localized in membrane rafts and caveolae of bovine aortic endothelial cells. Am J Physiol Heart Circ Physiol 292:H954-H962.
76. Zhang AY, Yi F, Zhang G, Gulbins E, Li PL (2006) Lipid raft clustering and redox signaling platform formation in coronary arterial endothelial cells. Hypertension 47:74-80.