Protein kinases A and C and phosphatidylinositol 3 kinase regulate glycogen synthase kinase-3A serine 21 phosphorylation in boar spermatozoa

Journal of Cellular Biochemistry

Volumn 109, Issue 1, 2010, Pages 65-73

  Bragado, Maria J ^a   Aparicio, Ines M ^a   Gil, Maria C ^a   Garcia Marin, Luis J ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

Author keywords

GSK3; Motility; Phosphorylation; PI3K; PKA; PKC; Spermatozoa

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 3 [8 [(DIMETHYLAMINO)METHYL] 6,7,8,9 TETRAHYDROPYRIDO[1,2 A]INDOL 10 YL] 4 (1 METHYL 1H INDOL 3 YL) 1H PYRROLE 2,5 DIONE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLYCOGEN SYNTHASE KINASE 3ALPHA; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; SERINE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL LEVEL; CELL VIABILITY; ENZYME PHOSPHORYLATION; GERM CELL; MALE; NONHUMAN; PRIORITY JOURNAL; SPERMATOZOON; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; SWINE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BLOTTING, WESTERN; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GLYCOGEN SYNTHASE KINASE 3; MALE; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; SIGNAL TRANSDUCTION; SPERM MOTILITY; SPERMATOZOA; SUS SCROFA;

SUS;

EID: 73849141006     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22393     Document Type: Article

References (39)

1. Aparicio IM, Garcia-Marin LJ, Andreolotti AG, Bodega G, Jensen RT, Bragado MJ. 2003. Hepatocyte growth factor activates several transduction pathways in rat pancreatic acini. Biochim Biophys Acta 1643:37-46.
2. Aparicio IM, Gil MC, Garcia-Herreros M, Pena FJ, Garcia-Marin LJ. 2005. Inhibition of phosphatidylinositol 3-kinase modifies boar sperm motion parameters. Reproduction 129:283-289.
3. Aparicio IM, Bragado MJ, Gil MC, Garcia-Herreros M, Gonzalez-Fernandez L, Tapia JA, Garcia-Marin LJ. 2007. Porcine sperm motility is regulated by serine phosphorylation of the glycogen synthase kinase-3alpha. Reproduction 134:435-444.
4. Bajpai M, Doncel GF. 2003. Involvement of tyrosine kinase and cAMP-dependent kinase cross-talk in the regulation of human sperm motility. Reproduction 126:183-195.
5. Breitbart H. 2003. Signaling pathways in sperm capacitation and acrosome reaction. Cell Mol Biol (Noisy -le-grand) 49:321-327.
6. Carlson AE, Hille B, Babcock DF. 2007. External Ca2+ acts upstream of adenylyl cyclase SACY in the bicarbonate signaled activation of sperm motility. Dev Biol 312:183-192.
7. Carrera A, Gerton GL, Moss SB. 1994. The major fibrous sheath polypeptide of mouse sperm: Structural and functional similarities to the A-kinase anchoring proteins. Dev Biol 165:272-284.
8. Chen RH, Ding WV, McCormick F. 2000. Wnt signaling to beta-catenin involves two interactive components. Glycogen synthase kinase-3beta inhibition and activation of protein kinase C. J Biol Chem 275:17894-17899.
9. Cook D, Fry MJ, Hughes K, Sumathipala R, Woodgett JR, Dale TC. 1996. Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C. EMBO J 15:4526-4536.
10. du Plessis SS, Franken DR, Baldi E, Luconi M. 2004. Phosphatidylinositol 3-kinase inhibition enhances human sperm motility and sperm-zona pellucida binding. Int J Androl 27:19-26.
11. Duronio V, Scheid MP, Ettinger S. 1998. Downstream signalling events regulated by phosphatidylinositol 3-kinase activity. Cell Signal 10:233-239.
12. Espada S, Rojo AI, Salinas M, Cuadrado A. 2009. The muscarinic M1 receptor activates Nrf2 through a signaling cascade that involves protein kinase C and inhibition of GSK-3beta: Connecting neurotransmission with neuroprotection. J Neurochem 110:1107-1119.
13. Fang X, Yu SX, Lu Y, Bast RC, Jr., Woodgett JR, Mills GB. 2000. Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci USA 97:11960-11965.
14. Goode N, Hughes K, Woodgett JR, Parker PJ. 1992. Differential regulation of glycogen synthase kinase-3 beta by protein kinase C isotypes. J Biol Chem 267:16878-16882.
15. Harayama H, Miyake M. 2006. A cyclic adenosine 3′,5′- monophosphate-dependent protein kinase C activation is involved in the hyperactivation of boar spermatozoa. Mol Reprod Dev 73:1169-1178.
16. Harayama H, Nakamura K. 2008. Changes of PKA and PDK1 in the principal piece of boar spermatozoa treated with a cell-permeable cAMP analog to induce flagellar hyperactivation. Mol Reprod Dev 75:1396-1407.
17. Hemmings BA. 1997. Akt signaling: Linking membrane events to life and death decisions. Science 275:628-630.
18. Hess KC, Jones BH, Marquez B, Chen Y, Ord TS, Kamenetsky M, Miyamoto C, Zippin JH, Kopf GS, Suarez SS, Levin LR, Williams CJ, Buck J, Moss SB. 2005. The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Dev Cell 9:249-259.
19. Holt WV, Harrison RA. 2002. Bicarbonate stimulation of boar sperm motility via a protein kinase A- dependent pathway: Between-cell and between-ejaculate differences are not due to deficiencies in protein kinase A activation. J Androl 23:557-565.
20. King TD, Gandy JC, Bijur GN. 2006. The protein phosphatase-1/inhibitor-2 complex differentially regulates GSK3 dephosphorylation and increases sarcoplasmic/endoplasmic reticulum calcium ATPase 2 levels. Exp Cell Res 312:3693-3700.
21. Lefievre L, de LE, Gagnon C. 2002. Presence of cyclic nucleotide phosphodiesterases PDE1A, existing as a stable complex with calmodulin, and PDE3A in human spermatozoa. Biol Reprod 67:423-430.
22. Luconi M, Marra F, Gandini L, Filimberti E, Lenzi A, Forti G, Baldi E. 2001. Phosphatidylinositol 3-kinase inhibition enhances human sperm motility. Hum Reprod 16:1931-1937.
23. Luconi M, Carloni V, Marra F, Ferruzzi P, Forti G, Baldi E. 2004. Increased phosphorylation of AKAP by inhibition of phosphatidylinositol 3-kinase enhances human sperm motility through tail recruitment of protein kinase A. J Cell Sci 117:1235-1246.
24. Luconi M, Porazzi I, Ferruzzi P, Marchiani S, Forti G, Baldi E. 2005. Tyrosine phosphorylation of the a kinase anchoring protein 3 (AKAP3) and soluble adenylate cyclase are involved in the increase of human sperm motility by bicarbonate. Biol Reprod 72:22-32.
25. NagDas SK, Winfrey VP, Olson GE. 2002. Identification of ras and its downstream signaling elements and their potential role in hamster sperm motility. Biol Reprod 67:1058-1066.
26. Nauc V, de Lamirande E, Leclerc P, Gagnon C. 2004. Inhibitors of phosphoinositide 3-kinase, LY294002 and wortmannin, affect sperm capacitation and associated phosphorylation of proteins differently: Ca(2+)-dependent divergences. J Androl 25:573-585.
27. Okamura N, Tajima Y, Soejima A, Masuda H, Sugita Y. 1985. Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylate cyclase. J Biol Chem 260:9699-9705.
28. Reinton N, Collas P, Haugen TB, Skalhegg BS, Hansson V, Jahnsen T, Tasken K. 2000. Localization of a novel human A-kinase-anchoring protein, hAKAP220, during spermatogenesis. Dev Biol 223:194-204.
29. Rodriguez-Martinez H. 2007. Role of the oviduct in sperm capacitation. Theriogenology 68(Suppl 1):S138-S146.
30. Si Y, Okuno M. 1999. Role of tyrosine phosphorylation of flagellar proteins in hamster sperm hyperactivation. Biol Reprod 61:240-246.
31. Somanath PR, Jack SL, Vijayaraghavan S. 2004. Changes in sperm glycogen synthase kinase-3 serine phosphorylation and activity accompany motility initiation and stimulation. J Androl 25:605-617.
32. Tanji C, Yamamoto H, Yorioka N, Kohno N, Kikuchi K, Kikuchi A. 2002. A-kinase anchoring protein AKAP220 binds to glycogen synthase kinase-3beta (GSK-3beta) and mediates protein kinase A-dependent inhibition of GSK-3beta. J Biol Chem 277:36955-36961.
33. Tsujio I, Tanaka T, Kudo T, Nishikawa T, Shinozaki K, Grundke-Iqbal I, Iqbal K, Takeda M. 2000. Inactivation of glycogen synthase kinase-3 by protein kinase C delta: Implications for regulation of tau phosphorylation. FEBS Lett 469:111-117.
34. Vijayaraghavan S, Trautman KD, Goueli SA, Carr DW. 1997. A tyrosine-phosphorylated 55-kilodalton motility-associated bovine sperm protein is regulated by cyclic adenosine 3′,5′-monophosphates and calcium. Biol Reprod 56:1450-1457.
35. Vijayaraghavan S, Liberty GA, Mohan J, Winfrey VP, Olson GE, Carr DW. 1999. Isolation and molecular characterization of AKAP110, a novel, sperm-specific protein kinase A-anchoring protein. Mol Endocrinol 13:705-717.
36. Vijayaraghavan S, Mohan J, Gray H, Khatra B, Carr DW. 2000. A role for phosphorylation of glycogen synthase kinase-3alpha in bovine sperm motility regulation. Biol Reprod 62:1647-1654.
37. Woodgett JR. 1990. Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J 9:2431-2438.
38. Wuttke MS, Buck J, Levin LR. 2001. Bicarbonate-regulated soluble adenylyl cyclase. J Pancreas 2:154-158.
39. Xie F, Garcia MA, Carlson AE, Schuh SM, Babcock DF, Jaiswal BS, Gossen JA, Esposito G, van Duin M. Conti M. 2006. Soluble adenylyl cyclase (sAC) is indispensable for sperm function and fertilization. Dev Biol 296:353-362.