Pharmacological analyses of protein kinases regulating egg maturation in marine nemertean worms: A review and comparison with mammalian eggs

Marine Drugs

Volumn 8, Issue 8, 2010, Pages 2417-2434

  Stricker, Stephen A ^a   Escalona, Jose R ^a   Abernathy, Samuel ^a   Marquardt, Alicia ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

AMPK; GVBD; MPF

Indexed keywords

CYCLIC AMP; CYCLIN DEPENDENT KINASE 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ISOENZYME; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE; PROTEIN KINASE C; PROTEIN TYROSINE KINASE;

ANTIBODY SPECIFICITY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; IMMUNOBLOTTING; MAMMAL; MARINE SPECIES; NEMERTEAN; NONHUMAN; OOCYTE MATURATION; PROTEIN FAMILY; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; WORM; WORM EGG;

ANIMALIA; MAMMALIA; NEMERTEA;

EID: 77956418748     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md8082417     Document Type: Review

References (92)

1. Stricker, S.A. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev. Biol. 1999, 211, 157-176.
2. Maller J.L. Maturation-promoting factor in the early days. Trends Biochem. Sci. 1995, 20, 524-528.
3. Nebreda, A.R.; Ferby, I. Regulation of the meiotic cell cycle in oocytes. Curr. Opin. Cell Biol. 2000, 12, 666-675.
4. Kishimoto, T. Cell-cycle control during meiotic maturation. Curr. Opin. Cell Biol. 2003, 15, 654-663.
5. Voronina, E.; Wessel, G.M. The regulation of oocyte maturation. Curr. Top. Dev. Biol. 2003, 58, 53-110.
6. Jones, K.T. Turning it on and off: M-phase promoting factor during meiotic maturation and fertilization. Mol. Hum. Reprod. 2004, 10, 1-5.
7. Nagahama, Y.; Yamashita, M. Regulation of oocyte maturation in fish. Dev. Growth Differ. 2008, 50, S195-S219.
8. Gibson, A. Nemerteans, 1st ed.; Hutchinson & Co. Ltd.: London, UK, 1972.
9. Stricker, S.A. Phylum Nemertea. In Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast, 1st ed.; Strathmann, M.F., Ed.; University of Washington Press: Seattle, WA, USA, 1987; pp. 129-137.
10. Stricker, S.A.; Smythe, T.L.; Miller, L.; Norenburg, J.L. Comparative biology of oogenesis in nemertean worms. Acta Zool. 2001, 82, 213-230.
11. Stricker, S.A.; Smythe, T.L. Multiple triggers of oocyte maturation in nemertean worms: the roles of calcium and serotonin. J. Exp. Zool. 2000, 287, 243-261.
12. Mehlmann, L.M. Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 2005, 130, 791-799.
13. Tsafriri, A.; Cao, X.; Ashkenazi, H.; Motola, S.; Popliker, M.; Pomerantz, S.H. Resumption of oocyte meiosis in mammals: on models, meiosis activating sterols, steroids and EGF-like factors. Mol. Cell Endocrinol. 2005, 234, 37-45.
14. Sun, Q.Y.; Miao, Y.L.; Schatten, H. Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 2009, 8, 2741-2747.
15. Zhang, M.; Ouyang, H.; Xia, G. The signal pathway of gonadotropins- induced mammalian oocyte meiotic resumption. Mol. Hum. Reprod. 2009, 15, 399-409.
16. Stricker, S.A.; Smythe, T.L. 5-HT causes an increase in cAMP that stimulates, rather than inhibits, oocyte maturation in marine nemertean worms. Development 2001, 128, 1415-1427.
17. Cho, W.K.; Sterns, S.; Biggers, J.D. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J. Exp. Zool. 1974, 187, 383-386.
18. Eppig, J.J.; Freter, R.R.; Ward-Bailey, P.F.; Schultz, R.M. Inhibition of oocyte maturation in the mouse: participation of cAMP, steroid hormones and a putative maturation-inhibitory factor. Dev. Biol. 1983, 100, 39-49.
19. Dekel, N. Regulation of oocyte maturation. The role of cAMP. Ann. N.Y. Acad. Sci. 1988, 541, 211-216.
20. Downs, S.M.; Daniel, S.A.J.; Eppig, J.J. Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin. J. Exp. Zool. 1988, 245, 86-96.
21. Tornell, J.; Billig, H.; Hillensjo, T. Regulation of oocyte maturation by changes in ovarian levels of cyclic nucleotides. Hum. Reprod. 1991, 6, 411-422.
22. Norris, R.P.; Ratzan, W.J.; Freudzon, M.; Mehlmann, L.M.; Krall, J.; Movsesian, M.A.; Wang, H.; Ke, H.; Nidolaev, V.O.; Jaffe, L.A. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 2009, 136, 1869-1878.
23. Downs, S.M.; Hunzicker-Dunn, M. Differential regulation of oocyte maturation and cumulus expansion in the mouse oocyte-cumulus cell complex by site-selective analogs of cyclic adenosine monophosphate. Dev. Biol. 1995, 172, 72-85.
24. Webb, R.J.; Marshall, F.; Swann, K.; Carroll, J. Follicle-stimulating hormone induces a gap junction-dependent dynamic change in [cAMP] and protein kinase A in mammalian oocytes. Dev. Biol. 2002, 246, 441-454.
25. Sela-Abramovich, S.; Edry, I.; Galiani, D.; Nevo, N.; Dekel, N. Disruption of gap junctional communication within the ovarian follicle induces oocyte maturation. Endocrinology 2006, 147, 2280-2286.
26. Norris, R.P.; Freudzon, M.; Mehlmann, L.M.; Cowan, A.E.; Simon, A.M.; Paul, D.L.; Lampe, P.D.; Jaffe, L.A. Luteinizing hormone causes MAP kinase-dependent phosphorylation and closure of connexin 43 gap junctions in mouse ovarian follicles: one of two paths to meiotic resumption. Development 2008, 135, 3229-3238.
27. Sasseville, M.; Gagnon, M.C.; Guillemette, C.; Sullivan, R.; Gilchrist, R.B.; Richard, F.J. Regulation of gap junctions in porcine cumulus-oocyte complexes: contributions of granulosa cell contact, gonadotropins, and lipid rafts. Mol. Endocrinol. 2009, 23, 700-710.
28. Chen, J.; Chi, M.M.; Moley, K.H.; Downs, S.M. cAMP pulsing of denuded mouse oocytes increases meiotic resumption via activation of AMP-activated protein kinase. Reproduction 2009, 138, 759-770.
29. Freeman, G.; Ridgway, E.B. The role of cAMP in oocyte maturation and the role of the germinal vesicle contents in mediating maturation and subsequent developmental events in hydrozoans. Roux's Arch. Dev. Biol. 1988, 197, 197-211.
30. Yamashita, M. Involvement of cAMP in initiating maturation of the brittle-star Amphipholis kochii oocytes: induction of oocyte maturation by inhibitors of cyclic nucleotide phosphodiesterase and activators of adenylate cyclase. Dev. Biol. 1988, 125, 109-114.
31. Yi, J.H.; Lefièvre, L.; Gagnon, C.; Anctil, M.; Dubé, F. Increase of cAMP upon release from prophase arrest in surf clam oocytes. J. Cell. Sci. 2002, 115, 311-320.
32. Takeda, N.; Kyozuka, K.; Deguchi, R. Increase in intracellular cAMP is a prerequisite signal for initiation of physiological oocyte meiotic maturation in the hydrozoan Cytaeis uchidae. Dev. Biol. 2006, 298, 248-258.
33. Lambert, C.C. Signaling pathways in ascidian oocyte maturation: the role of cyclic AMP and follicle cells in germinal vesicle breakdown. Dev. Growth Differ. 2008, 50, 181-188.
34. Webb, R.J.; Tinworth, L.; Thomas, G.M.; Zaccolo, M.; Carroll, J. Developmentally acquired PKA localisation in mouse oocytes and embryos. Dev. Biol. 2008, 317, 36-45.
35. Stricker, S.A.; Smythe, T.L. Differing mechanisms of cAMP- versus seawater-induced oocyte maturation in marine nemertean worms. II. The roles of tyrosine kinases and phosphatases. Mol. Reprod. Dev. 2006, 73, 1564-1577.
36. Stricker, S.A. Roles of protein kinase C isotypes during seawater- versus cAMP-induced oocyte maturation in a marine worm. Mol. Reprod. Dev. 2009, 76, 693-707.
37. Wilkinson, M.G.; Millar, J.B. Control of the eukaryotic cell cycle by MAP kinase signaling pathways. FASEB J. 2000, 14, 2147-2157.
38. Chang, L.; Karin, M. Mammalian MAP kinase signalling cascades. Nature 2001, 410, 37-40. (Pubitemid 32225829)
39. Raman, M.; Chen, W.; Cobb, M.H. Differential regulation and properties of MAPKs. Oncogene 2007, 26, 3100-3112.
40. Sturgill, T.W. MAP kinase: it's been longer than fifteen minutes. Biochem. Biophys. Res. Commun. 2008, 371, 1-4.
41. 2+ signaling in maturing and fertilized oocytes of marine protostome worms: The roles of MAPKs and MPF. Development 2003, 130, 2867-2879.
42. Smythe, T.L.; Stricker, S.A. Germinal vesicle breakdown is not fully dependent on MAPK activation in maturing oocytes of marine nemertean worms. Mol. Reprod. Dev. 2005, 70, 91-102.
43. Stricker, S.A.; Smythe, T.L. Differing mechanisms of cAMP- versus seawater-induced oocyte maturation in marine nemertean worms I. The roles of serine/threonine kinases and phosphatases. Mol. Reprod. Dev. 2006, 73, 1578-1590.
44. Stricker, S.A. Interactions between mitogen-activated protein kinase and protein kinase C signaling during oocyte maturation and fertilization in a marine worm. Mol. Reprod. Dev. 2009, 76, 708-721.
45. Fan, H.Y.; Sun, Q.Y. Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol. Reprod. 2004, 70, 535-547.
46. Liang, C.G.; Su, Y.Q.; Fan, H.Y.; Schatten, H.; Sun, Q.Y. Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase. Mol. Endocrin. 2007, 21, 2037-2055.
47. Fan, H.Y.; Liu, Z.; Shimada, M.; Sterneck, E.; Johnson, P.F.; Hedrick, S.M.; Richards, J.S. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 2009, 324, 938-941.
48. Yamashita, Y.; Hishinuma, M.; Shimada, M. Activation of PKA, p38 MAPK and ERK1/2 by gonadotropins in cumulus cells is critical for induction of EGF-like factor and TACE/ADAM17 gene expression during in vitro maturation of porcine COCs. J. Ovarian Res. 2009, 2, 20:1-20:9.
49. Spivack, J.G.; Maller, J.L. Phosphorylation and protein synthetic events in Xenopus laevis oocytes microinjected with pp60v-src. Mol. Cell. Biol. 1985, 5, 3629-3633.
50. Stricker, S.A.; Carroll, D.J.; Tsui, W.L. Roles of Src family kinase signaling during fertilization and the first cell cycle in the marine protostome worm Cerebratulus. Int. J. Dev. Biol. 2010, 54, 787-793.
51. McGinnis, L.K.; Kinsey, W.H.; Albertini, D.F. Functions of Fyn kinase in the completion of meiosis in mouse oocytes. Dev. Biol. 2009, 327, 280-287.
52. Zheng, K.G.; Meng, X.Q.; Yang, Y.; Yu, Y.S.; Liu, D.C.; Li, Y.L. Requirements of Src family kinase during meiotic maturation in mouse oocyte. Mol. Reprod. Dev. 2007, 74, 125-130.
53. Sette, C.; Paronetto, M.P.; Barchi, M.; Bevilacqua, A.; Geremia, R.; Rossi, P. Tr-kit-induced resumption of the cell cycle in mouse eggs requires activation of a Src-like kinase. EMBO J. 2002, 21, 5386-5395. (Pubitemid 35231018)
54. Talmor-Cohen, A.; Tomashov-Matar, R.; Eliyahu, E.; Shapiro, R.; Shalgi, R. Are Src family kinases involved in cell cycle resumption in rat eggs? Reproduction 2004, 127, 455-463.
55. McGinnis, L.K.; Albertini, D.F.; Kinsey, W.H. Localized activation of Src-family protein kinases in the mouse egg. Dev. Biol. 2007, 306, 241-254.
56. Reut, T.M.; Mattan, L.; Dafna, T.; Ruth, K.K.; Ruth, S. The role of Src family kinases in egg activation. Dev. Biol. 2007, 312, 77-89.
57. Mellor, H.; Parker, P.J. The extended protein kinase C superfamily. Biochem. J. 1998, 332, 281-292.
58. Webb, L.J.; Hirst, S.J.; Giembycz, M.A. Protein kinase C isoenzymes: a review of their structure, regulation, and role in regulating airways smooth muscle tone and mitogenesis. Br. J. Pharmcol. 2000, 130, 1433-1452.
59. Kalive, M.; Faust, J.J.; Koeneman, B.A.; Capco, D.G. Involvement of the PKC family in regulation of early development. Mol. Reprod. Dev. 2010, 77, 95-104.
60. Downs, S.M.; Cottom, J.; Hunzicker-Dunn, M. Protein kinase C and meiotic regulation in isolated mouse oocytes. Mol. Reprod. Dev. 2001, 58, 101-115.
61. Avazeri, N.; Courtot, A.M.; Lefevre, B. Regulation of spontaneous meiosis resumption in mouse oocytes by various conventional PKC isozymes depends on cellular compartmentalization. J. Cell Sci. 2004, 117, 4969-4978.
62. Bornslaeger, E.A.; Pouymirou, W.T.; Mattei, P.; Schultz, R.M. Effects of protein kinase C activators on germinal vesicle breakdown and polar body emission of mouse oocytes. Exp. Cell Res. 1986, 165, 507-517.
63. Lefevre, B.; Pesty, A.R.; Koziak, K.; Testart, J. Protein kinase C modulators influence meiosis kinetics but not fertilizability of mouse oocytes. J. Exp. Zool. 1992, 264, 206-213.
64. Luria, A.; Tennenbaum, T.; Sun, Q.Y.; Rubinstein, S.; Breitbart, H. Differential localization of conventional protein kinase C isoforms during mouse oocyte development. Biol. Reprod. 2000, 62, 1564-1570.
65. Lu, Q.; Smith, G.D.; Chen, D.Y.; Yang, Z.; Han, Z.M.; Schatten, H.; Sun, Q.Y. Phosphorylation of mitogen-activated protein kinase is regulated by protein kinase C, cyclic 3′5′-adenosine monophosphate, and protein phosphatase modulators during meiosis resumption in rat oocytes. Biol. Reprod. 2001, 64, 1444-1450.
66. Denys, A.; Avazeri, N.; Lefevre, B. The PKC pathway and in particular its beta 1 isoform is clearly involved in meiotic arrest maintenance but poorly in FSH-induced meiosis resumption of the mouse cumulus cell enclosed oocyte. Mol. Reprod. Dev. 2007, 74, 1575-1580.
67. Gallicano, G.I.; McGaughey, R.W.; Capco, D.G. Activation of protein kinase C after fertilization is required for remodeling the mouse egg into zygote. Mol. Reprod. Dev. 1997, 46, 587-601.
68. Quan, H.M.; Fan, H.Y.; Meng, X.Q.; Chen, D.Y.; Schatten, H.; Yang, P.M.; Sun, Q.Y. Effects of PKC activation of the meiotic maturation, fertilization and early development of mouse oocytes. Zygote 2003, 11, 329-337.
69. 2+ oscillations at fertilization in mouse eggs. J. Cell Biol. 2004, 164, 1033-1044.
70. Ducibella, T.; LeFevre, L. Study of protein kinase C antagonists on cortical granule exocytosis and cell cycle resumption in fertilized mouse eggs. Mol. Reprod. Dev. 1997, 46, 216-226.
71. Carling, D. AMP-activated protein kinase: balancing the scales. Biochimie 2005, 87, 87-91. (Pubitemid 40298770)
72. Alessi, D.R.; Sakamoto, K.; Bayascas, J.R. LKB1-dependent signaling pathways. Ann. Rev. Biochem. 2006, 75, 137-163.
73. Hardie, D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat. Rev. Cell Mol. Biol. 2007, 8, 774-785.
74. Stricker, S.A.; Swiderek, L.; Nguyen, T. Stimulators of AMP-activated kinase inhibit seawater- but not cAMP-induced oocyte maturation in a marine worm: implications for interactions between cAMP and AMPK signaling. Mol. Reprod. Dev. 2010, 77, 497-510.
75. Downs, S.M.; Hudson, E.R.; Hardie, D.G. A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Dev. Biol. 2002, 245, 200-212.
76. Chen, J.; Hudson, E.; Chi, M.M.; Chang, A.S.; Moley, K.H.; Hardie, D.G.; Downs, S.M. AMPK regulation of mouse oocyte meiotic resumption in vitro. Dev. Biol. 2006, 291, 227-238.
77. Chen, J.; Downs, S.M. AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro. Dev. Biol. 2008, 313, 47-57.
78. Bilodeau-Goeseels, S.; Sasseville, M.; Guillemette, C.; Richard, F.J. Effects of adenosine monophosphate-activated kinase activators on bovine oocyte nuclear maturation in vitro. Mol. Reprod. Dev. 2007, 74, 1021-1034.
79. Mayes, M.A.; Laforest, M.F.; Guillemette, C.; Gilchrist, R.B.; Richard, F.J. Adenosine 5′-monophosphate kinase-activated protein kinase (PRKA) activators delay meiotic resumption in porcine oocytes. Biol. Reprod. 2007, 76, 589-597.
80. Tosca, L.; Uzbekova, S.; Chabrolle, C.; Dupont, J. Possible role of 5′ AMP-activated protein kinase in the metformin-mediated arrest of bovine oocytes at the germinal vesicle stage during in vitro maturation. Biol. Reprod. 2007, 77, 452-465.
81. Bilodeau-Goeseels, S. Review: The regulation of meiotic maturation in bovine oocytes. Can. J. Anim. Sci. 2008, 88, 343-349.
82. cdc2 binding and activating protein that is necessary and sufficient to trigger G2/M preogression in Xenopus oocytes. Genes Dev. 1999, 13, 2177-2189.
83. Kume, S.; Endo, T.; Nishimura, Y.; Kano, K.; Naito, K. Porcine SPDYA2 (RINGOA2) stimulates CDC2 activity and accelerates meiotic maturation of porcine oocytes. Biol. Reprod. 2007, 76, 440-447.
84. Yamashita, M.; Mita, K.; Yoshida, N.; Kondo, T. Molecular mechanisms of the initiation of oocyte maturation: General and species specific aspects. Prog. Cell Cycle Res. 2000, 4, 115-129.
85. Lincoln, A.J.; Wickramasinghe, D.; Stein, P.; Schultz, R.M.; Palko, M.E.; De Miguel, M.P.; Tessarollo, L.; Donovan, P.J. Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat. Gen. 2002, 30, 446-449.
86. Oh, J.S.; Han, J.S.; Conti, M. Wee 1B, Myt1, and Cdc25 function in distinct compartment of the mouse oocyte to control meiotic resumption. J. Cell Biol. 2010, 188, 199-207.
87. Alexandre, H.; van Cauwenberge, A.; Tsukitani, Y.; Mulnard, J. Pleiotropic effect of okadaic acid on maturing mouse oocytes. Development 1991, 112, 971-980. (Pubitemid 21900299)
88. Lu, Q.; Smith, G.D.; Chen, D.Y.; Yang, Z.; Han, Z.M.; Schatten, H.; Sun, Q.Y. Phosphorylation of mitogen-activated protein kinase is regulated by protein kinase C, cyclic 3′5′-adenosine monophosphate, and protein phosphatase modulators during meiosis resumption in rat oocytes. Biol. Reprod. 2001, 64, 1444-1450.
89. Stricker, S.A.; Silva, R.; Smythe, T.L. Calcium and endoplasmic reticulum dynamics during oocyte maturation and fertilization in the marine worm Cerebratulus lacteus. Dev. Biol. 1998, 203, 305-322.
90. Schroeder, T.E.; Stricker, S.A. Morphological changes during maturation of starfish oocytes: Surface ultrastructure and cortical actin. Dev. Biol. 1983, 98, 373-384.
91. Stricker, S.A.; Schatten, G. Nuclear envelope disassembly and nuclear lamina depolymerization during germinal vesicle breakdown in starfish. Dev. Biol. 1989, 135, 87-98.
92. Davies, S.P.; Reddy, H.; Caivano, M.; Cohen, P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 2000, 351, 95-105.