PTK2b Function During Fertilization of the Mouse Oocyte

Overview

Journal Biochem Biophys Res Commun

Publisher Elsevier

Specialty Biochemistry

Date 2014 Mar 27

PMID 24667605

Citations 5

Authors

Jinping Luo

Lynda K McGinnis

Carol Carlton

Hilary E Beggs

William H Kinsey

Affiliations

Soon will be listed here.

Abstract

Fertilization triggers rapid changes in intracellular free calcium that serve to activate multiple signaling events critical to the initiation of successful development. Among the pathways downstream of the fertilization-induced calcium transient is the calcium-calmodulin dependent protein tyrosine kinase PTK2b or PYK2 kinase. PTK2b plays an important role in fertilization of the zebrafish oocyte and the objective of the present study was to establish whether PTK2b also functions in mammalian fertilization. PTK2b was activated during the first few hours after fertilization of the mouse oocyte during the period when anaphase resumption was underway and prior to the pronuclear stage. Suppression of PTK2b kinase activity in oocytes blocked sperm incorporation and egg activation although sperm-oocyte binding was not affected. Oocytes that failed to incorporate sperm after inhibitor treatment showed no evidence of a calcium transient and no evidence of anaphase resumption suggesting that egg activation did not occur. The results indicate that PTK2b functions during the sperm-egg fusion process or during the physical incorporation of sperm into the egg cytoplasm and is therefore critical for successful development.

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References

Owen K, Thomas K, Bouton A . The differential expression of Yersinia pseudotuberculosis adhesins determines the requirement for FAK and/or Pyk2 during bacterial phagocytosis by macrophages. Cell Microbiol. 2006; 9(3):596-609. DOI: 10.1111/j.1462-5822.2006.00811.x. View

Okigaki M, Davis C, Falasca M, Harroch S, Felsenfeld D, Sheetz M . Pyk2 regulates multiple signaling events crucial for macrophage morphology and migration. Proc Natl Acad Sci U S A. 2003; 100(19):10740-5. PMC: 196873. DOI: 10.1073/pnas.1834348100. View

Owen K, Pixley F, Thomas K, Vicente-Manzanares M, Ray B, Horwitz A . Regulation of lamellipodial persistence, adhesion turnover, and motility in macrophages by focal adhesion kinase. J Cell Biol. 2007; 179(6):1275-87. PMC: 2140030. DOI: 10.1083/jcb.200708093. View

Boschelli D, Wu B, Ye F, Wang Y, Golas J, Lucas J . Synthesis and Src kinase inhibitory activity of a series of 4-[(2,4-dichloro-5-methoxyphenyl)amino]-7-furyl-3-quinolinecarbonitriles. J Med Chem. 2006; 49(26):7868-76. DOI: 10.1021/jm061031t. View

Gui P, Chao J, Wu X, Yang Y, Davis G, Davis M . Coordinated regulation of vascular Ca2+ and K+ channels by integrin signaling. Adv Exp Med Biol. 2010; 674:69-79. DOI: 10.1007/978-1-4419-6066-5_7. View

Tengowski M . Microscopic techniques for studying sperm-oocyte interaction during fertilization and early embryonic development. Methods Mol Biol. 2004; 253:165-99. DOI: 10.1385/1-59259-744-0:165. View

Gui P, Wu X, Ling S, Stotz S, Winkfein R, Wilson E . Integrin receptor activation triggers converging regulation of Cav1.2 calcium channels by c-Src and protein kinase A pathways. J Biol Chem. 2006; 281(20):14015-25. DOI: 10.1074/jbc.M600433200. View

Wu S, Jacamo R, Vong S, Rozengurt E . Differential regulation of Pyk2 phosphorylation at Tyr-402 and Tyr-580 in intestinal epithelial cells: roles of calcium, Src, Rho kinase, and the cytoskeleton. Cell Signal. 2006; 18(11):1932-40. DOI: 10.1016/j.cellsig.2006.02.013. View

McGinnis L, Luo J, Kinsey W . Protein tyrosine kinase signaling in the mouse oocyte cortex during sperm-egg interactions and anaphase resumption. Mol Reprod Dev. 2013; 80(4):260-72. PMC: 3891396. DOI: 10.1002/mrd.22160. View

10.

Gardner A, Williams C, Evans J . Establishment of the mammalian membrane block to polyspermy: evidence for calcium-dependent and -independent regulation. Reproduction. 2007; 133(2):383-93. DOI: 10.1530/REP-06-0304. View

11.

Wakai T, Vanderheyden V, Fissore R . Ca2+ signaling during mammalian fertilization: requirements, players, and adaptations. Cold Spring Harb Perspect Biol. 2011; 3(4). PMC: 3062211. DOI: 10.1101/cshperspect.a006767. View

12.

Sharma D, Kinsey W . PYK2: a calcium-sensitive protein tyrosine kinase activated in response to fertilization of the zebrafish oocyte. Dev Biol. 2012; 373(1):130-40. PMC: 3510262. DOI: 10.1016/j.ydbio.2012.10.015. View

13.

Li X, Dy R, Cance W, Graves L, Earp H . Interactions between two cytoskeleton-associated tyrosine kinases: calcium-dependent tyrosine kinase and focal adhesion tyrosine kinase. J Biol Chem. 1999; 274(13):8917-24. DOI: 10.1074/jbc.274.13.8917. View

14.

Luo J, McGinnis L, Kinsey W . Role of Fyn kinase in oocyte developmental potential. Reprod Fertil Dev. 2010; 22(6):966-76. PMC: 3933928. DOI: 10.1071/RD09311. View

15.

Swann K, Saunders C, Rogers N, Lai F . PLCzeta(zeta): a sperm protein that triggers Ca2+ oscillations and egg activation in mammals. Semin Cell Dev Biol. 2006; 17(2):264-73. DOI: 10.1016/j.semcdb.2006.03.009. View

16.

Dikic I, Tokiwa G, Lev S, Courtneidge S, Schlessinger J . A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature. 1996; 383(6600):547-50. DOI: 10.1038/383547a0. View

17.

Sun C, Ng K, Lim Z, Cheng Q, Lo C, Poon R . Proline-rich tyrosine kinase 2 (Pyk2) promotes cell motility of hepatocellular carcinoma through induction of epithelial to mesenchymal transition. PLoS One. 2011; 6(4):e18878. PMC: 3080371. DOI: 10.1371/journal.pone.0018878. View

18.

Beggs H, Schahin-Reed D, Zang K, Goebbels S, Nave K, Gorski J . FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron. 2003; 40(3):501-14. PMC: 2758566. DOI: 10.1016/s0896-6273(03)00666-4. View

19.

Yu Y, Nomikos M, Theodoridou M, Nounesis G, Lai F, Swann K . PLCζ causes Ca(2+) oscillations in mouse eggs by targeting intracellular and not plasma membrane PI(4,5)P(2). Mol Biol Cell. 2011; 23(2):371-80. PMC: 3258180. DOI: 10.1091/mbc.E11-08-0687. View

20.

Mitaka T, Shindoh M, Mochizuki Y, Sasaki H, Ishino M, Matsuya M . Restricted expression of cell adhesion kinase-beta in rat tissues. Am J Pathol. 1997; 150(1):267-81. PMC: 1858543. View