Protein tyrosine phosphorylation in sperm during capacitation
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1 Chinese Bulletin of Life Sciences Vol. 18, No. 3 Jun., (2006) sac/camp/pka Q25 A Protein tyrosine phosphorylation in sperm during capacitation ZHOU Si-Chang, NI Ya, SHI Qi-Xian* (Zhejiang Academy of Medical Sciences, Hangzhou, China ) Abstract: Mammalian sperm are required to undergo a process known as capacitation before they can undertake the fertilization process. The protein phosphorylation especially at tyrosine residues is one of the most important events that occur during capacitation. The increase in protein tyrosine phosphorylation during capacitation has been shown to be regulated by camp/pka-dependent pathway, receptor tyrosine kinase pathway, and non-receptor protein tyrosine kinase pathway. It has been observed that the tyrosine phosphorylated proteins are localized in various regions of spermatozoon, and that the tyrosine phosphorylation of sperm proteins link to the different sperm functions. Key words: sperm sperm capacitation protein tyrosine phosphorylation; signal transduction (capacitation) (hyperactive motility) (acrosome reaction) ph Ca 2+ camp [1] / / (G ) ( ) (1980 ) (1961 ) (1936 ) *
2 286 Tash Means [2] / (Ser) (Thr) (Tyr) Ser/Thr Visconti [3] 40~120kDa Leyton Saling [4] (2-D) (Western blot) (MS/ MS) [5] 1 (sac)/ (camp)/ A(PKA) AC/cAMP/PKA 1.1 sac/camp/pka ( HCO 3 ) (soluble adenylate cyclase, sac) camp PKA A (AKAPs) ( ) camp H89(PKA ) / camp [6] PKA Ser/Thr [1] camp-pka 1.2 (receptor tyrosine kinases, RTKs) ( EGF IGF-1 p190 c-met c-abl ) (adapter protein)( Shc) Ras Raf MEK(MAPKK /extracellular signal-regulated kinase kinase) (mitogen-activated protein kinases, MAPK) ( ) MEK 1(extracellular signal-regulated protein kinase1 ERK1) ERK2 MAPK MAPK MAPK ERK2 Shc Ras [7] 1.3 ( c-yes TK-32) ( ) 2 [8] Urner [9] - Carrera [10] Naaby-Hansen [11] (CABYR) CABYR Ca 2+ [11] CABYR (pi4.0) 86kDa CABYR CABYR [11] Naz [12]
3 287 (endoplasmin, Erp99) 60(Hsp60) [13] [14] - 3 Leyton Saling [4] 52kDa 75kDa 95kDa 95kDa Naz [12] (95/94 3kDa 46 3kDa 25 7kDa 12 2kDa) 46 3 kda -1(FA-1) FA-1 - FA kda 46 3 kda(fa-1 ) [15] Flesch [16] (27kDa 37kDa 40kDa) (34kDa 47kDa 55kDa) Flesch [17] 34kDa 47kDa Hsp90 Ecroyd [18] Hsp90 Hsp86 Hsp86 ansamycin antibiotic geldanamycin Asquith [19] HspD1 TRA1(tumor rejection antigen, gp96) HspD1 Hsp60 TRA1 Erp99 Hsp60 Erp99 Erp99 Hsp90 Erp99 N (Grp94) Grp94 gp96 Erp 99 TRA1 Hsp90 Toll IgGs Asquith [13] Erp99 Hsp60, AKAPs AKAPs PKA Carrera [10] AKAP82 pro-akap82 AKAP3 AKAP4 [5] AKAPs ( ) - Luconi [20] HCO 3 sac AKAP3 PKA AKAP3 81kDa 95kDa 105kDa AKAP (FSP95) AKAP82 32% C II Mandal [21] FSP95 NagDas [22] (PHGPx) PHGPx PHGPx
4 288 PDC A PDC [23] (5-methoxyindole-2-carboxylic acid) Mitra Shivaji [24] Ras p21 MAPKs ERKs Ras/ERK Luconi [25] ERK-1 ERK-2 ERKs A23187 ERKs ERKs 42kDa 44kDa ERK-2 ERK-1 ERKs ERK-1 ERK-2 MAPK PD ERK ERKs AAA(ATPases associated with various cellular activities)p97 VCP(valosin-containing protein) VCP/p97 N- (NSF) NSF VCP/p97 T VCP/ p97 ATP T p97 Ficarro [5] -VCP VCP/p97 NSF(SNARE) SNARE- t-snare syntaxin 5 VCP/p97 NSF SNARE VCP/p97 4 [1] Leclerc P, de Lamirande E, Gagnon C. Interaction between Ca 2+, cyclic 3',5'-adenosine monophosphate, the superoxide anion, and tyrosine phosphorylation pathways in the regulation of human sperm capacitation. J Androl, 1998, 19(4): 434~443 [2] Tash J S, Means A R. Cyclic adenosine 3', 5' monophosphate, calcium and protein phosphorylation in flagellar motility. Biol Reprod, 1983, 28(1): 75~104 [3] Visconti P E, Bailey J L, Moore G D, et al. Capacitation of mouse spermatozoa: I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development, 1995, 121(4): 1129~1137 [4] Leyton L, Saling P. 95 kd sperm proteins bind ZP3 and serve as tyrosine kinase substrates in response to zona binding. Cell, 1989, 57(7): 1123~1130 [5] Ficarro S, Chertihin O, Westbrook V A, et al. Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J Biol Chem, 2003, 278(13): 11579~11589 [6] Thundathil J, de Lamirande E, Gagnon C. Different signal transduction pathways are involved during human sperm capacitation induced by biological and pharmacological agents. Mol Hum Reprod, 2002, 8(9): 811~816 [7] de Lamirande E, Gagnon C. The extracellular signal-regulated kinase (ERK) pathway is involved in human sperm function and modulated by the superoxide anion. Mol Hum Reprod, 2002, 8(2): 124~135 [8] Urner F, Sakkas D. Protein phosphorylation in mammalian spermatozoa. Reproduction, 2003, 125(1): 17~26 [9] Urner F, Leppens-Luisier G, Sakkas D. Protein tyrosine phosphorylation in sperm during gamete interaction in the mouse: the influence of glucose. Biol Reprod, 2001, 64(5): 1350~1357 [10] Carrera A, Moos J, Ning X P, et al. 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(1): 284~296 [11] Naaby-Hansen S, Mandal A, Wolkowicz M J, et al. CABYR, a novel calcium binding tyrosine phosphorylation-regulated fibrous sheath protein involved in capacitation. Dev Biol, 2002, 242(2): 236~254
5 289 [12] Naz R K, Ahmad K, Kumar R. Role of membrane phosphotyrosine proteins in human spermatozoal function. J Cell Sci, 1991, 99(Pt 1): 157~165 [13] Asquith K L, Baleato R M, McLaughlin E A, et al. Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci, 2004, 117(Pt 16): 3645~3657 [14] Sakkas D, Leppens-Luisier G, Lucas H, et al. Localization of tyrosine phosphorylated proteins in human sperm and relation to capacitation and zona pellucida binding. Biol Reprod, 2003, 68(4): 1463~1469 [15] Naz R K, Ahmad K. Molecular identities of human sperm proteins that bind human zona pellucida: nature of spermzona interaction, tyrosine kinase activity, and involvement of FA-1. Mol Reprod Dev, 1994, 39(4): 397~408 [16] Flesch F M, Colenbrander B, van Golde L M, et al. Capacitation induces tyrosine phosphorylation of proteins in the boar sperm plasma membrane. Biochem Biophys Res Commun, 1999, 262(3): 787~792 [17] Flesch F M, Wijnand E, van de Lest C H, et al. Capacitation dependent activation of tyrosine phosphorylation generates two sperm head plasma membrane proteins with high primary binding affinity for the zona pellucida. Mol Reprod Dev, 2001, 60(1): 107~115 [18] Ecroyd H, Jones R C, Aitken R J. Tyrosine phosphorylation of HSP-90 during mammalian sperm capacitation. Biol Reprod, 2003, 69(6): 1801~1807 [19] Asquith K L, Harman A J, McLaughlin E A, et al. Localization and significance of molecular chaperones, heat shock protein 1, and tumor rejection antigen gp96 in the male reproductive tract and during capacitation and acrosome reaction. Biol Reprod, 2005, 72(2): 328~337 [20] Luconi M, Porazzi I, Ferruzzi P, et al. 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, 2005, 72 (1): 22~32 [21] Mandal A, Naaby-Hansen S, Wolkowicz M J, et al. FSP95, a testis-specific 95-kilodalton fibrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa. Biol Reprod, 1999, 61(5): 1184~1197 [22] NagDas S K, Winfrey V P, Olson G E. Tyrosine phosphorylation generates multiple isoforms of the mitochondrial capsule protein, phospholipid hydroperoxide glutathione peroxidase (PHGPx), during hamster sperm capacitation. Biol Reprod, 2005, 72(1): 164~171 [23] Ciszak E M, Korotchkina L G, Dominiak P M, et al. Structural basis for flip-flop action of thiamin pyrophosphatedependent enzymes revealed by human pyruvate dehydrogenase. J Biol Chem, 2003, 278(23): 21240~21246 [24] Mitra K, Shivaji S. Novel tyrosine-phosphorylated post-pyruvate metabolic enzyme, dihydrolipoamide dehydrogenase, involved in capacitation of hamster spermatozoa. Biol Reprod, 2004, 70(4): 887~899 [25] Luconi M, Barni T, Vannelli G B, et al. Extracellular-signal regulated kinases (ERKs) modulate capacitation of human spermatozoa. Biol Reprod, 1998, 58(6): 1476~ Archakov Alexander Konstantin G. Skryabin Victor V. Godin 19 http: //
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