Protein tyrosine kinase signaling in the mouse oocyte cortex during sperm-egg interactions and anaphase resumption

Molecular Reproduction and Development

Volumn 80, Issue 4, 2013, Pages 260-272

  Mcginnis, Lynda K ^a   Luo, Jinping ^a   Kinsey, William H ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOTYROSINE; PROTEIN TYROSINE KINASE;

ANAPHASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOACCUMULATION; ENZYME ACTIVATION; FEMALE; FERTILIZATION; FERTILIZATION IN VITRO; IMMUNOFLUORESCENCE MICROSCOPY; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; OOCYTE; OOCYTE CORTEX; PRIORITY JOURNAL; PROTEIN BINDING; SPERM;

ANIMALS; CYTOPLASM; FEMALE; FOCAL ADHESION KINASE 2; MALE; MICE; OOCYTES; SIGNAL TRANSDUCTION; SPERM-OVUM INTERACTIONS; SPERMATOZOA;

MAMMALIA;

EID: 84876416317     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.22160     Document Type: Article

References (80)

1. Allingham MJ, van Buul JD, Burridge K. 2007. ICAM-1-mediated, Src- and Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J Immunol 179:4053-4064.
2. Andersen J, Orntoft TF, Poulsen HS. 1988. Immunohistochemical demonstration of estrogen receptors (ER) in formalin-fixed, paraffin-embedded human breast cancer tissue by use of a monoclonal antibody to ER. J Histochem Cytochem 36:1553-1560.
3. Antoine AF, Faure JE, Cordeiro S, Dumas C, Rougier M, Feijo JA. 2000. A calcium influx is triggered and propagates in the zygote as a wavefront during in vitro fertilization of flowering plants. Proc Natl Acad Sci USA 97:10643-10648.
4. 2+ influx to gamete fusion and egg activation in maize. Nat Cell Biol 3:1120-1123.
5. Barraud-Lange V, Chalas BC, Serres C, Auer J, Schmitt A, Lefevre B, Wolf JP, Ziyyat A. 2012. Membrane transfer from oocyte to sperm occurs in two CD9-independent ways that do not supply the fertilizing ability of Cd9-deleted oocytes. Reproduction 44:53-66.
6. Basile JR, Afkhami T, Gutkind JS. 2005. Semaphorin 4D/plexin-B1 induces endothelial cell migration through the activation of PYK2, Src, and the phosphatidylinositol 3-kinase-Akt pathway. Mol Cell Biol 25:6889-6898.
7. Berditchevski F, Odintsova E. 1999. Characterization of integrin-tetraspanin adhesion complexes: Role of tetraspanins in integrin signaling. J Cell Biol 146:477-492.
8. Bromfield EG, Nixon B. 2013. The function of chaperone proteins in the assemblage of protein complexes involved in gamete adhesion and fusion processes. Reproduction 145:R31-R42.
9. Bruce-Staskal PJ, Weidow CL, Gibson JJ, Bouton AH. 2002. Cas, Fak and Pyk2 function in diverse signaling cascades to promote Yersinia uptake. J Cell Sci 115:2689-2700.
10. Burnett LA, Washburn CA, Sugiyama H, Xiang X, Olson JH, Al-Anzi B, Bieber AL, Chandler DE. 2012. Allurin, an amphibian sperm chemoattractant having implications for mammalian sperm physiology. Int Rev Cell Mol Biol 295:1-61.
11. Cain RJ, Vanhaesebroeck B, Ridley AJ. 2010. The PI3K p110alpha isoform regulates endothelial adherens junctions via Pyk2 and Rac1. J Cell Biol 188:863-876.
12. 2+ signalling at fertilization in mammals. Semin Cell Dev Biol 12:37-43.
13. Clark GF. 2011. The molecular basis of mouse sperm-zona pellucida binding: A still unresolved issue in developmental biology. Reproduction 142:377-381.
14. Conover JC, Gwatkin RB. 2008. Pre-loading of mouse oocytes with DNA-specific fluorochrome (Hoechst 33342) permits rapid detection of sperm-oocyte fusion. J Reprod Fertil 82:681-690.
15. Cross NL, Elinson RP. 1980. A fast block to polyspermy in frogs mediated by changes in the membrane potential. Dev Biol 75:187-198.
16. Dikic I, Tokiwa G, Lev S, Courtneidge SA, Schlessinger J. 1996. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 383:547-550.
17. Gadella BM, Evans JP. 2011. Membrane fusions during mammalian fertilization. Adv Exp Med Biol 713:65-80.
18. Gardner AJ, Williams CJ, Evans JP. 2007. Establishment of the mammalian membrane block to polyspermy: Evidence for calcium-dependent and -independent regulation. Reproduction 133:383-393.
19. Gil-Henn H, Destaing O, Sims NA, Aoki K, Alles N, Neff L, Sanjay A, Bruzzaniti A, De Camilli P, Baron R, Schlessinger J. 2007. Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J Cell Biol 178:1053-1064.
20. Giusti AF, Carroll DJ, Abassi YA, Terasaki M, Foltz KR, Jaffe LA. 1999. Requirement of a Src family kinase for initiating calcium release at fertilization in starfish eggs. J Biol Chem 274:29318-29322.
21. Giusti AF, Xu WQ, Hinkle B, Terasaki M, Jaffe LA. 2000. Evidence that fertilization activates starfish eggs by sequential activation of a Src-like kinase and phospholipase Cgamma. J Biol Chem 275:16788-16794.
22. Glahn D, Nuccitelli R. 2003. Voltage-clamp study of the activation currents and fast block to polyspermy in the egg of Xenopus laevis. Dev Growth Differ 45:187-197.
23. Glazar AI, Evans JP. 2009. Immunoglobulin superfamily member IgSF8 (EWI-2) and CD9 in fertilisation: Evidence of distinct functions for CD9 and a CD9-associated protein in mammalian sperm-egg interaction. Reprod Fertil Dev 21:293-303.
24. Gupta SK, Bhandari B, Shrestha A, Biswal BK, Palaniappan C, Malhotra SS, Gupta N. 2012. Mammalian zona pellucida glycoproteins: Structure and function during fertilization. Cell Tissue Res 349:665-678.
25. 2+ lightning conveys cell-cell contact information inside the cells. EMBO Rep 7:1117-1123.
26. Institute of Laboratory Animal Resources (U.S., ). Committee on Care and Use of Laboratory Animals 1996 Guide for the care and use of laboratory animals. In NIH Publication Bethesda, MD.
27. Ivankovic-Dikic I, Gronroos E, Blaukat A, Barth BU, Dikic I. 2000. Pyk2 and FAK regulate neurite outgrowth induced by growth factors and integrins. Nat Cell Biol 2:574-581.
28. Jiang X, Jacamo R, Zhukova E, Sinnett-Smith J, Rozengurt E. 2006. RNA interference reveals a differential role of FAK and Pyk2 in cell migration, leading edge formation and increase in focal adhesions induced by LPA in intestinal epithelial cells. J Cell Physiol 207:816-828.
29. Jin M, Fujiwara E, Kakiuchi Y, Okabe M, Satouh Y, Baba SA, Chiba K, Hirohashi N. 2011. Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc Natl Acad Sci USA 108:4892-4896.
30. Kalive M, Faust JJ, Koeneman BA, Capco DG. 2010. Involvement of the PKC family in regulation of early development. Mol Reprod Dev 77:95-104.
31. Kim S, Spike C, Greenstein D. 2013. Control of oocyte growth and meiotic maturation in Caenorhabditis elegans. Adv Exp Med Biol 757:277-320.
32. Kinsey WH. 2013. Intersecting roles of protein tyrosine kinase and calcium signaling during fertilization. Cell Calcium 53:32-40.
33. Krauchunas AR, Horner VL, Wolfner MF. 2012. Protein phosphorylation changes reveal new candidates in the regulation of egg activation and early embryogenesis in D. melanogaster. Dev Biol 370:125-134.
34. 2+]i oscillations in mouse eggs. Reproduction 127:441-454.
35. Lawrence Y, Whitaker M, Swann K. 1997. Sperm-egg fusion is the prelude to the initial Ca2+ increase at fertilization in the mouse. Development 124:233-241.
36. Levi M, Maro B, Shalgi R. 2011. The conformation and activation of Fyn kinase in the oocyte determine its localisation to the spindle poles and cleavage furrow. Reprod Fert Dev 23:846-857.
37. Liu Y, Zhang GY, Hou XY, Xu TL. 2003. Two types of calcium channels regulating activation of proline-rich tyrosine kinase 2 induced by transient brain ischemia in rat hippocampus. Neurosci Lett 348:127-130.
38. Longo FJ, Lynn JW, McCulloh DH, Chambers EL. 1986. Correlative ultrastructural and electrophysiological studies of sperm-egg interactions of the sea urchin, Lytechinus variegatus. Dev Biol 118:155-166.
39. Longo FJ, Cook S, McCulloh DH, Ivonnet PI, Chambers EL. 1994. Stages leading to and following fusion of sperm and egg plasma membranes. Zygote 2:317-331.
40. Mahbub Hasan AK, Sato K, Sakakibara K, Ou Z, Iwasaki T, Ueda Y, Fukami Y. 2005. Uroplakin III, a novel Src substrate in Xenopus egg rafts, is a target for sperm protease essential for fertilization. Dev Biol 286:483-492.
41. McCulloh DH, Chambers EL. 1992. Fusion of membranes during fertilization. Increases of the sea urchin egg's membrane capacitance and membrane conductance at the site of contact with the sperm. J Gen Physiol 99:137-175.
42. McGinnis LK, Albertini DF, Kinsey WH. 2007. Localized activation of Src-family protein kinases in the mouse egg. Dev Biol 306:241-254.
43. McGinnis LK, Carroll DJ, Kinsey WH. 2011a. Protein tyrosine kinase signaling during oocyte maturation and fertilization. Mol Reprod Dev 78:831-845.
44. McGinnis LK, Hong X, Christenson LK, Kinsey WH. 2011b. Fer tyrosine kinase is required for germinal vesicle breakdown and meiosis-I in mouse oocytes. Mol Reprod Dev 78:33-47.
45. 2+ release at fertilization in mouse eggs. Reproduction 129:557-564.
46. Meng XQ, Zheng KG, Yang Y, Jiang MX, Zhang YL, Sun QY, Li YL. 2006. Proline-rich tyrosine kinase2 is involved in F-actin organization during in vitro maturation of rat oocyte. Reproduction 132:859-867.
47. Mitaka T, Shindoh M, Mochizuki Y, Sasaki H, Ishino M, Matsuya M, Ninomiya T, Sasaki T. 1997. Restricted expression of cell adhesion kinase-beta in rat tissues. Am J Pathol 150:267-281.
48. Miyado K, Yoshida K, Yamagata K, Sakakibara K, Okabe M, Wang X, Miyamoto K, Akutsu H, Kondo T, Takahashi Y, Ban T, Ito C, Toshimori K, Nakamura A, Ito M, Miyado M, Mekada E, Umezawa A. 2008. The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proc Natl Acad Sci USA 105:12921-12926.
49. Naruse M, Ishikawa R, Sakaya H, Moriyama H, Hoshi M, Matsumoto M. 2011. Novel conserved structural domains of acrosome reaction-inducing substance are widespread in invertebrates. Mol Reprod Dev 78:57-66.
50. Nolan K, Lacoste J, Parsons JT. 1999. Regulated expression of focal adhesion kinase-related nonkinase, the autonomously expressed C-terminal domain of focal adhesion kinase. Mol Cell Biol 19:6120-6129.
51. National Research Council (US). 2011. Guide for the care and use of laboratory animals. Washington, DC: Committee for the Update of the guide for the care and use of laboratory animals. p 220.
52. Ohnami N, Nakamura A, Miyado M, Sato M, Kawano N, Yoshida K, Harada Y, Takezawa Y, Kanai S, Ono C, Takahashi Y, Kimura K, Shida T, Miyado K, Umezawa A. 2012. CD81 and CD9 work independently as extracellular components upon fusion of sperm and oocyte. Biol Open 1:640-647.
53. Okamoto H, Takahashi K, Yamashita N. 1977. Ionic currents through the membrane of the mammalian oocyte and their comparison with those in the tunicate and sea urchin. J.Physiol 267:465-495.
54. Okigaki M, Davis C, Falasca M, Harroch S, Felsenfeld DP, Sheetz MP, Schlessinger J. 2003. Pyk2 regulates multiple signaling events crucial for macrophage morphology and migration. Proc Natl Acad Sci USA 100:10740-10745.
55. Owen KA, Pixley FJ, Thomas KS, Vicente-Manzanares M, Ray BJ, Horwitz AF, Parsons JT, Beggs HE, Stanley ER, Bouton AH. 2007a. Regulation of lamellipodial persistence, adhesion turnover, and motility in macrophages by focal adhesion kinase. J Cell Biol 179:1275-1287.
56. Owen KA, Thomas KS, Bouton AH. 2007b. The differential expression of Yersinia pseudotuberculosis adhesins determines the requirement for FAK and/or Pyk2 during bacterial phagocytosis by macrophages. Cell Microbiol 9:596-609.
57. Parrington J, Davis LC, Galione A, Wessel G. 2007. Flipping the switch: How a sperm activates the egg at fertilization. Dev Dyn 236:2027-2038.
58. Powner D, Kopp PM, Monkley SJ, Critchley DR, Berditchevski F. 2011. Tetraspanin CD9 in cell migration. Biochem Soc Trans 39:563-567.
59. Qian D, Lev S, van Oers NS, Dikic I, Schlessinger J, Weiss A. 1997. Tyrosine phosphorylation of Pyk2 is selectively regulated by Fyn during TCR signaling. J Exp Med 185:1253-1259.
60. Runft LL, Jaffe LA, Mehlmann LM. 2002. Egg activation at fertilization: Where it all begins. Dev Biol 245:237-254.
61. Schaller MD. 2010. Cellular functions of FAK kinases: Insight into molecular mechanisms and novel functions. J Cell Sci 123:1007-1013.
62. Sharma D, Kinsey WH. 2006. Fertilization triggers localized activation of Src-family protein kinases in the zebrafish egg. Dev Biol 295:604-614.
63. Sharma D, Kinsey WH. 2008. Regionalized calcium signaling in zebrafish fertilization. Int J Dev Biol 52:561-570.
64. Sharma D, Kinsey WH. 2013. PYK2: A calcium-sensitive protein tyrosine kinase activated in response to fertilization of the zebrafish oocyte. Dev Biol 373:130-140.
65. Stricker SA. 2009. Interactions between mitogen-activated protein kinase and protein kinase C signaling during oocyte maturation and fertilization in a marine worm. Mol Reprod Dev 76:708-721.
66. Summers MC, McGinnis LK, Lawitts JA, Raffin M, Biggers JD. 2000. IVF of mouse ova in a simplex optimized medium supplemented with amino acids. Human Reprod 15:1791-1801.
67. Sun CK, Ng KT, Lim ZX, Cheng Q, Lo CM, Poon RT, Man K, Wong N, Fan ST. 2011. Proline-rich tyrosine kinase 2 (Pyk2) promotes cell motility of hepatocellular carcinoma through induction of epithelial to mesenchymal transition. PLoS ONE 6:e18878.
68. 2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCzeta. Reproduction 127:431-439.
69. Tengowski MW. 2004. Microscopic techniques for studying sperm-oocyte interaction during fertilization and early embryonic development. Methods Mol Biol 253:165-199.
70. Tokmakov A, Iwasaki T, Itakura S, Sato K, Shirouzu M, Fukami Y, Yokoyama S. 2005. Regulation of Src kinase activity during Xenopus oocyte maturation. Dev Biol 278:289-300.
71. Tokmakov AA, Iwasaki T, Sato K, Fukami Y. 2010. Analysis of signal transduction in cell-free extracts and rafts of Xenopus eggs. Methods 51:177-182.
72. Totani L, Piccoli A, Manarini S, Federico L, Pecce R, Martelli N, Cerletti C, Piccardoni P, Lowell CA, Smyth SS, Berton G, Evangelista V. 2006. Src-family kinases mediate an outside-in signal necessary for beta2 integrins to achieve full activation and sustain firm adhesion of polymorphonuclear leucocytes tethered on E-selectin. Biochem J 396:89-98.
73. 2+ release at fertilization. Dev Biol 327:465-477.
74. Vacquier VD, Swanson WJ. 2011. Selection in the rapid evolution of gamete recognition proteins in marine invertebrates. Cold Spring Harb Perspect Biol 3:a002931.
75. Vomaske J, Varnum S, Melnychuk R, Smith P, Pasa-Tolic L, Shutthanandan JI, Streblow DN. 2010. HCMV pUS28 initiates pro-migratory signaling via activation of Pyk2 kinase. Herpesviridae 1:2.
76. Voronina E, Wessel GM. 2006. Activator of G-protein signaling in asymmetric cell divisions of the sea urchin embryo. Dev Growth Differ 48:549-557.
77. Watanabe A, Fukutomi K, Kubo H, Ohta M, Takayama-Watanabe E, Onitake K. 2009. Identification of egg-jelly substances triggering sperm acrosome reaction in the newt, Cynops pyrrhogaster. Mol Reprod Dev 76:399-406.
78. Wu W, Kinsey W. 2000. Fertilization triggers activation of Fyn kinase in the zebrafish egg. Int J Dev Biol 44:837-841.
79. Wu SS, Jacamo RO, Vong SK, Rozengurt E. 2006 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 18:1932-1940.
80. Xiong WC, Macklem M, Parsons JT. 1998. Expression and characterization of splice variants of PYK2, a focal adhesion kinase-related protein. J Cell Sci 111:1981-1991.