Oocyte maturation and fertilization in marine nemertean worms: Using similar sorts of signaling pathways as in mammals, but often with differing results

Biological Bulletin

Volumn 224, Issue 3, 2013, Pages 137-155

  Stricker, Stephen A ^a   Cline, Cory ^a   Goodrich, David ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME ACTIVITY; FERTILIZATION (REPRODUCTION); INVERTEBRATE; MAMMAL; MARINE ECOSYSTEM; MATURATION; SIGNALING; SPATIOTEMPORAL ANALYSIS;

ANIMALIA; MAMMALIA; NEMERTEA; SIPUNCULUS NUDUS;

ANIMAL; ARTICLE; FEMALE; FERTILIZATION; HELMINTH; OOCYTE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; FEMALE; FERTILIZATION; HELMINTHS; OOCYTES; SIGNAL TRANSDUCTION;

EID: 84883401704     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.1086/bblv224n3p137     Document Type: Article

References (211)

1. Aarabi, M., Z. Qin, W. Xu, J. Mewburn, and R. Oko. 2010. Spermborne protein, PAWP, initiates zygotic development in Xenopus laevis by eliciting intracellular calcium release. Mol. Reprod. Dev. 77: 249- 256.
2. Aarabi, M., Y. Yu, W. Xu, M. Y. Tse, S. C. Pang, Y.-Y. Yia, P. Sutovsky, and R. Oko. 2012. The testicular and epididymal expression profile of PLCζ in mouse and human does not support its role as a sperm-borne oocyte activating factor. PLoS ONE 7: e33496; doi: 10.1371/journal.pone.0033496
3. Alessi, D. R., K. Sakamoto, and J. R. Bayascas. 2006. LKB1-dependent signaling pathways. Annu. Rev. Biochem. 75: 137-163.
4. Alexandre, H., and J. Mulnard. 1988. Time-lapse cinematography study of the germinal vesicle behaviour in mouse primary oocytes treated with activators of protein kinases A and C. Gamete Res. 21: 359-365.
5. Alm, H., and K. Hinrichs. 1996. Effect of cycloheximide on nuclear maturation of horse oocytes and its relation to initial cumulus morphology. J. Reprod. Fertil. 107: 215-220.
6. Bae, I. H., and C. P. Channing. 1985. Effect of calcium ion on the maturation of cumulus-enclosed pig follicular oocytes isolated from medium-sized Graafian follicles. Biol. Reprod. 33: 79-87.
7. Beckhelling, C., P. Chang, S. Chevalier, C. Ford, and E. Houliston. 2003. Pre-M phase-promoting factor associates with annulate lamellae in Xenopus oocytes and egg extracts. Mol. Biol. Cell 14: 1125-1137.
8. i) oscillations resulting from microinjection of mouse phospholipase C zeta mRNA into mare oocytes. Anim. Reprod. Sci. 94: 294-298.
9. Bilodeau-Goeseels, S., M. Sasseville, C. Guillemette, and F. J. Richard. 2007. Effects of adenosine monophosphate-activated kinase activators on bovine oocyte nuclear maturation in vitro. Mol. Reprod. Dev. 74: 1021-1034.
10. Bilodeau-Goeseels, S., P. L. Panic, and J. P. Kastelic. 2011. Activation of AMP-activated protein kinase may not be involved in AICAR- and metformin-mediated meiotic arrest in bovine denuded and cumulusenclosed oocytes in vitro. Zygote 19: 97-106.
11. Bornslaeger, E. A., W. T. Pouymirou, P. Mattei, and R. M. Schultz. 1986. Effects of protein kinase C activators on germinal vesicle breakdown and polar body emission of mouse oocytes. Exp. Cell Res. 165: 507-517.
12. Brown, A. J., T. Jones, and J. Shuttlesworth. 1994. Expression and activity of p40MO15, the catalytic subunit of cdk-activating kinase, during Xenopus oogenesis and embryogenesis. Mol. Biol. Cell 5: 921-932.
13. Byskov, A. G., C. Y. Andersen, and L. Leonardsen. 2002. Role of meiosis activating sterols, MAS, in induced oocyte maturation. Mol. Cell. Endocrinol. 187: 189-196.
14. 2+ oscillations driven by inositol trisphosphate occur during in vitro maturation of mouse oocytes. J. Biol. Chem. 267: 11196-11201.
15. Chausson, F., L. A. Paterson, K. A. Betteley, L. Hannah, L. Meijer, and M. G. Bentley. 2004. CDK1/cyclin B regulation during oocyte maturation in two closely related lugworm species, Arenicola marina and Arenicola defodiens. Dev. Growth Differ. 46: 71-82.
16. Chen, J., and S. M. Downs. 2008. AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro. Dev. Biol. 313: 47-57.
17. Chen, J., E. Hudson, M. M. Chi, A. S. Chang, K. H. Moley, D. G. Hardie, and S. M. Downs. 2006. AMPK regulation of mouse oocyte meiotic resumption in vitro. Dev. Biol. 291: 227-238.
18. Chen, J., M. M. Chi, K. H. Moley, and S. M. Downs. 2009. cAMP pulsing of denuded mouse oocytes increases meiotic resumption via activation of AMP-activated protein kinase. Reproduction 138: 759-770.
19. Choi, T., F. Aoki, M. Mori, M. Yamashita, Y. Nagahama, and K. Kohmoto. 1991. Activation of p34cdc2 protein kinase in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 113: 789-795.
20. Coe, W. R. 1899. On the development of the pilidium of certain nemerteans. Connecticut Acad. Arts Sci. 10: 235-262.
21. Conti, M., C. B. Andersen, F. Richard, C. Mehats, S. Y. Chun, K. Horner, C. Jin, and A. Tsafriri. 2002. Role of cyclic nucleotide signaling in oocyte maturation. Mol. Cell. Endocrinol. 187: 153-159.
22. Cooney, M. A., C. Malcuit, B. Cheon, M. K. Holland, R. A. Fissore, and N. T. D'Cruz. 2010. Species-specific differences in the activity and nuclear localization of murine and bovine phospholipase C zeta1. Biol. Reprod. 83: 92-101.
23. Coward, K., C. P. Ponting, H.-Y. Chang, O. Hibbitt, P. Savolainen, K. T. Jones, and J. Parrington. 2005. Phospholipase Cζ, the trigger of egg activation in mammals, is present in non-mammalian species. Reproduction 130: 157-163.
24. Coward, K., C. P. Ponting, N. Zhang, C. Young, C.-J. Huang, C.-M. Chou, J. Kashir, R. A. Fissore, and J. Parrington. 2011. Identification and functional analysis of an ovarian form of the egg activation factor phospholipase C zeta (PLCζ,) in pufferfish. Mol. Reprod. Dev. 78: 48-56.
25. 2+ influx in oocytes of limpets (Phylum Mollusca, Class Gastropoda). Dev. Biol. 304: 652-663.
26. 2+ release from inositol 1, 4, 5-trisphosphate-sensitive stores function at fertilization in oocytes of the marine bivalve Mytilus edulis. Development 122: 3651-3660.
27. 2+ oscillations in fertilized mouse eggs. Dev. Biol. 257: 166-176.
28. 2+ increases at fertilization in eggs of jellyfish (Phylum Cnidaria, Class Hydrozoa). Dev. Biol. 279: 291-307
29. Deguchi, R., N. Takeda, and S. A. Stricker. 2011. Comparative biology of cAMP-induced germinal vesicle breakdown in marine invertebrate oocytes. Mol. Reprod. Dev. 78: 708-725.
30. Dekel, N., D. Galiani, and I. Sherizly. 1988. Dissociation between the inhibitory and the stimulatory action of cAMP on maturation of rat oocytes. Mol. Cell. Endocrinol. 56: 115-121.
31. Denys, A., N. Avazeri, and B. Lefevre. 2007. 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. 74: 1575-1580.
32. Downs, S. M. 2010. Regulation of the G2/M transition in rodent oocytes. Mol. Reprod. Dev. 77: 566-585.
33. Downs, S. M. 2011. Mouse versus rat: profound differences in meiotic regulation at the level of the isolated oocyte. Mol. Reprod. Dev. 78: 778-794.
34. Downs, S. M., and M. Hunzicker-Dunn. 1995. Differential regulation of oocyte maturation and cumulus expansion in the mouse oocytecumulus cell complex by site-selective analogs of cyclic adenosine monophosphate. Dev. Biol. 172: 72-85.
35. Downs, S. M., J. Cottom, and M. Hunzicker-Dunn. 2001. Protein kinase C and meiotic regulation in isolated mouse oocytes. Mol. Reprod. Dev. 58: 101-115.
36. Downs, S. M., E. R. Hudson, and D. G. Hardie. 2002. A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Dev. Biol. 245: 200-212.
37. 2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev. Biol. 315: 257-279.
38. Dumollard, R., J. Carroll, G. Dupont, and C. Sardet. 2002. Calcium wave pacemakers in eggs. J. Cell Sci. 115: 3557-3564.
39. Dupont, G., and R. Dumollard, R. 2004. Simulation of calcium waves in ascidian eggs: insights into the origin of the pacemaker sites and the possible nature of the sperm factor. J. Cell Sci. 117: 4313-4323.
40. 2+ spiking. Biochem. J. 316: 583-591.
41. Edwards, R. G., and A. H. Gates. 1959. Timing of the stages of the maturation divisions, ovulation, fertilization and the first cleavage of eggs of adult mice treated with gonadotrophins. J. Endocrinol. 18: 292-304.
42. Eisen, A., and G. A. Reynolds. 1985. Sources and sinks for the calcium released during fertilization of single sea urchin eggs. J. Cell Biol. 100: 1522-1527.
43. Ekholm, C., and C. Magnusson. 1979. Rat oocyte maturation: effects of protein synthesis inhibitors. Biol. Reprod. 21: 1287-1293.
44. Esacalona, R., and S. A. Stricker. 2013. Immunoblotting analyses of changes in protein phosphorylations during oocyte maturation in marine nemertean worms. In Methods in Molecular Biology: Developmental Biology of the Sea Urchin and Other Marine Invertebrate Model Systems, D. J. Carroll and S. A. Stricker, eds. Humana Press, New York. In press.
45. Evans, J., and B. Gadella. 2011. Membrane fusions during mammalian fertilization. Adv. Exp. Med. Biol. 713: 65-80.
46. Faerge, I., B. Terry, J. Kalous, P. Wahl, M. Lessl, J. L. Ottesen, P. Hyttel, and C. Grondahl. 2001. Resumption of meiosis induced by meiosis-activating sterol has a different signal transduction pathway than spontaneous resumption of meiosis in denuded mouse oocytes cultured in vitro. Biol. Reprod. 65: 1751-1758.
47. Fan, H.-Y., and Q.-Y. Sun. 2004. Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol. Reprod. 70: 535-547.
48. Fan, H.-Y., L.-J. Huo, D.-Y. Chen, H. Schatten, and Q.-Y. Sun. 2004. Protein kinase C and mitogen-activated protein kinase cascade in mouse cumulus cells: cross talk and effect on meiotic resumption of oocyte. Biol. Reprod. 70: 1178-1187.
49. Fan, H.-Y., Z. Liu, M. Shimada, E. Sterneck, P. F. Johnson, S. M. Hedrick, and J. S. Richards. 2009. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 324: 938-941.
50. 2+ release in mouse oocytes and embryos. Mol. Biol. Cell 14: 288-301.
51. Freeman, G. 1978. The role of asters in the localization of the factors that specify the apical tuft and the gut of the nemertine Cerebratulus lacteus. J. Exp. Zool. 206: 81-107.
52. Freeman, G., and E. B. Ridgway. 1988. 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. 197: 197-211.
53. Fujii, W., T. Nishimura, K. Kano, K. Sugiura, and K. Naito. 2011. CDK7 and CCNH are components of CDK-activating kinase and are required for meiotic progression of pig oocytes. Biol. Reprod. 85: 1124-1132.
54. Fulka, J., Jr., J. Motlik, J. Fulka, and F. Jilek. 1986. Effect of cycloheximide on nuclear maturation of pig and mouse oocytes. J. Reprod. Fertil. 77: 281-285.
55. Gaffré, M., A. Martoriati, N. Belhachemi, J. P. Chambon, E. Houliston, C. Jessus, and A. Karaiskou. 2011. A critical balance between Cyclin B synthesis and Myt1 activity controls meiosis entry in Xenopus oocytes. Development 138: 3735-3744.
56. Gallicano, G. I., S. M. Schwarz, R. W. McGaughey, and D. G. Capco. 1993. Protein kinase C, a pivotal regulator of hamster egg activation, functions after elevation of intracellular free calcium. Dev. Biol. 156: 94-106.
57. Gilchrist, R. B. 2011. Recent insights into oocyte-follicle cell interactions provide opportunities for the development of new approaches to in vitro maturation. Reprod. Fertil. Dev. 23: 23-31.
58. Goren, S., Y. Oron, and N. Dekel. 1990. Rat oocyte maturation: role of calcium in hormone action. Mol. Cell. Endocrinol. 72: 131-138.
59. Grange, L. J., L. S. Peck, and P. A. Tyler. 2011. Reproductive ecology of the circumpolar Antarctic nemertean Parborlasia corrugatus: no evidence for inter-annual variation. J. Exp. Mar. Biol. Ecol. 404: 98-107.
60. Griffin, J., B. R. Emery, I. Huan, C. M. Peterson, and D. T. Carrell. 2006. Comparative analysis of follicle morphology in four mammalian species (mouse, hamster, pig, and human). J. Exp. Clin. Assist. Reprod. 3: doi:10.1186/1743-1050-3-2.
61. Harada, Y., T. Matsumoto, S. Hirahara, A. Nakashima, S. Ueno, S. Oda, S. Miyazaki, and Y. Iwao. 2007. Characterization of a sperm factor for egg activation at fertilization of the newt Cynops pyrrhogaster. Dev. Biol. 306: 797-808.
62. 2+ increase by the sperm factor in physiologically polyspermic newt fertilization: its signaling mechanism in egg cytoplasm and the speciesspecificity. Dev. Biol. 351: 266-276.
63. Hardie, D. G. 2007. AMP-activated/SNF1protein kinases: conserved guardians of cellular energy. Nat. Rev. Mol. Cell. Biol. 8: 774-785.
64. Hartman, C. G. 1929. How large is the mammalian egg?: A review. Q. Rev. Biol. 4: 373-388.
65. Hegele-Hartung, C., J. Kuhnke, M. Lessl, C. Grøndahl, J. Ottesen, H. M. Beier, S. Eisner, and U. Eichenlaub-Ritter. 1999. Nuclear and cytoplasmic maturation of mouse oocytes after treatment with synthetic meiosis-activating sterol in vitro. Biol. Reprod. 61: 1362-1372.
66. Heytens, E., J. Parrington, K. Coward, C. Young, S. Lambrecht, S.-Y. Yoon, R. A. Fissore, R. Hamer, C. M. Deane, M. Ruas, et al. 2009. Reduced amounts and abnormal forms of phospholipase C zeta (PLCζ) in spermatozoa from infertile men. Hum. Reprod. 24: 2417-2428.
67. Homa, S. T. 1995. Calcium and meiotic maturation of the mammalian oocyte. Mol. Reprod. Dev. 40: 122-134.
68. Ito, J., and N. Kashiwazaki. 2012. Molecular mechanisms of fertilization in the pig. Animal Sci. J. 83: 669-672.
69. 2+ channel, is a novel substrate of polo-like kinase 1 in eggs. Dev. Biol. 320: 402-413.
70. Ito, J., J. Parrington, and R. A. Fissore. 2011. PLCζæ and its role as a trigger of development in vertebrates. Mol. Reprod. Dev. 78: 846-853.
71. Jaffe, L., D. Kline, and R. Tucker. 1985. Fertilization potential and polyspermy prevention in the egg of the nemertean, Cerebratulus lacteus. J. Exp. Zool. 236: 45-52.
72. Jaffe, L. A., and R. P. Norris. 2010. Initiation of the meiotic prophaseto-metaphase transition in mammalian oocytes. Pp. 181-198 in Oogenesis: The Universal Process, M.-H. Verlhac and A. Villeneuve, eds. John Wiley, New York.
73. 2+ oscillations in the activation of the egg and development of the embryo in mammals. Int. J. Dev. Biol. 42: 1-10.
74. Jones, K. T. 2004. Turning it on and off: M-phase promoting factor during meiotic maturation and fertilization. Mol. Hum. Reprod. 10: 1-5.
75. Jones, K. T. 2007. Intracellular calcium in the fertilization and development of mammalian eggs. Clin. Exp. Pharmacol. Physiol. 34: 1084-1089.
76. Jones, K. T., J. Carroll, J. A. Merriman, D. G. Whittingham, and T. Kono. 1995. Repetitive sperm-induced calcium transients in mouse oocytes are cell cycle dependent. Development 121: 3259-3266.
77. Kajihara, H., A. V. Chernyshev, S.-C. Sun, P. Sundberg, and F. B. Crandall. 2008. Checklist of nemertean genera and species (Nemertea) published between 1995 and 2007. Species Diversity 13: 245-274.
78. Kang, M. K., and S. J. Han. 2011. Post-transcriptional and posttranslational regulation during mouse oocyte maturation. Biochem. Mol. Biol. Rep. 44: 147-157.
79. Kashir, J., B. Heindryckx, C. Jones, P. De Sutter, J. Parrington, and K. Coward. 2010. Oocyte activation, phospholipase C zeta and human infertility. Hum. Reprod. Update 16: 690-703.
80. Kashir, J., C. Jones, and K. Coward. 2012. Calcium oscillations, oocyte activation, and phospholipase C zeta. Adv. Exp. Med. Biol. 740: 1095-1121.
81. Kastrop, P. M. M., S. C. J. Sulshof, M. M. Bevers, O. H. J. Destree, and T. A. M. Kruip. 1991. The effects of α-amanitin and cycloheximide on nuclear progression, protein synthesis, and phosphorylation during bovine oocyte maturation in vivo. Mol. Reprod. Dev. 28: 249-254.
82. Kaufman, M. H. 1973. Timing of the first cleavage division of the mouse and the duration of its component stages: a study of living and fixed eggs. J. Cell Sci. 12: 799-808.
83. Kishimoto, T. 2003. Cell-cycle control during meiotic maturation. Curr. Opin. Cell Biol. 15: 654-663.
84. Kline, D. 2000. Attributes and dynamics of the endoplasmic reticulum in mammalian oocytes. Curr. Top. Dev. Biol. 50: 124-154.
85. Kovo, M., M. Kandli-Cohen, M. Ben-Haim, D. Galiani, D. W. Carr, and N. Dekel. 2006. An active protein kinase A (PKA) is involved in meiotic arrest of rat growing oocytes. Reproduction 132: 33-43.
86. Kyozuka, K., R. Deguchi, T. Mohri, and S. Miyazaki. 1998. Injection of sperm extract mimics spatiotemporal dynamics of calcium responses and progression of meiosis at fertilisation of ascidian oocytes. Development 125: 4099-4105.
87. Lambert, C. C. 2008. Signaling pathways in ascidian oocyte maturation: the role of cyclic AMP and follicle cells in germinal vesicle breakdown. Dev. Growth Differ. 50: 181-188.
88. 2+ oscillations in mouse embryos are regulated by nuclear targeting of PLCzeta. J. Cell Sci. 117: 2513-2521.
89. LaRosa, C., and S. M. Downs. 2006. Stress stimulates AMP-activated protein kinase and meiotic resumption in mouse oocytes. Biol. Reprod. 74: 585-592.
90. LaRosa, C., and S. M. Downs. 2007. Meiotic induction by heat stress in mouse oocytes: involvement of AMP-activated protein kinase and MAPK family members. Biol. Reprod. 76: 476-486.
91. i response at fertilization: a role for the MAP kinase pathway. Development 133: 4355-4365.
92. Le Gal, F., L. Gall, and V. De Smedt. 1992. Changes in protein synthesis pattern during in vitro maturation of goat oocytes. Mol. Reprod. Dev. 32: 1-8.
93. Lefevre, B., A. R. Pesty, K. Koziak, and J. Testart. 1992. Protein kinase C modulators influence meiosis kinetics but not fertilizability of mouse oocytes. J. Exp. Zool. 264: 206-213.
94. 2+ oscillations triggered by activation of ascidian eggs and has an absolute requirement for Cdk1 activity. J. Cell Sci. 120: 1763-1771.
95. Li, Y. X. 2003. Tango waves in a bidomain model of fertilization calcium waves. Physica D. 186: 27-49.
96. Liang, C.-G., Y.-Q. Su, H.-Y. Fan, H. Schatten, and Q.-Y. Sun. 2007. Mechanisms regulating oocyte meiotic resumption: roles of mitogenactivated protein kinase. Mol. Endocrinol. 21: 2037-2055.
97. Lu, Q., G. D. Smith, D.-Y. Chen, Z.-M. Han, H. Schatten, and Q.-Y. Sun. 2001. 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. 64: 1444-1450.
98. Luria, A, T. Tennenbaum, Q. Y. Sun, S. Rubinstein, and H. Breitbart. 2000. Differential localization of conventional protein kinase C isoforms during mouse oocyte development. Biol. Reprod. 62: 1564-1570.
99. 2+ release mechanisms during meiotic maturation of human oocytes. Biol. Reprod. 83: 578-583.
100. 2+ oscillations at fertilization in mammals are regulated by the formation of pronuclei. Development 130: 1461-1472.
101. Mattioli, M., G. Galeati, B. Barboni, and E. Seren. 1994. Concentration of cyclic AMP during the maturation of pig oocytes in vivo and in vitro. J. Reprod. Fertil. 100: 403-409.
102. Matzuk, M. H., K. H. Burns, M. M. Viveiros, and J. J. Eppig. 2002. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296: 2178-2180.
103. Mayes, M. A., M. F. Laforest, C. Guillemette, R. B. Gilchrist, and F. J. Richard. 2007. Adenosine 5'-monophosphate kinase-activated protein kinase (PRKA) activators delay meiotic resumption in porcine oocytes. Biol. Reprod. 76: 589-597.
104. 2+ waves induced by a cytosolic sperm extract in mature ascidian eggs mimic those observed at fertilization. J. Cell Sci. 113: 3453-3462.
105. McDougall, A., J. Chenevert, and R. Dumollard. 2012. Cell cycle control in oocytes and early embryonic cleavage cycles in ascidians. Int. Rev. Cell Mol. Biol. 297: 235-264.
106. McGinnis, L. K., D. J. Carroll, and W. H. Kinsey. 2011. Protein tyrosine kinase signaling during oocyte maturation and fertilization. Mol. Reprod. Dev. 78: 831-845.
107. Mehlmann, L. M. 2005. Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130: 791-799.
108. i family G protein or calcium in the mouse oocyte. Dev. Biol. 299: 345-355.
109. Meng, L., J. Luo, C. Li, and W. H. Kinsey. 2006. Role of Src homology 2 domain-mediated PTK signaling in mouse zygotic development. Reproduction 132: 413-422.
110. Miao, Y.-L., and C. J. Williams. 2012. Calcium signaling in mammalian egg activation and embryo development: the influence of subcellular localization. Mol. Reprod. Dev. 79: 742-756.
111. Miyata, K., T. Nakano, R. Kuroda, and H. Kuroda. 2006. Development of calcium releasing activity induced by inositol trisphosphate and cyclic ADP-ribose during in vitro maturation of sea urchin oocytes. Dev. Growth Differ. 48: 605-613.
112. Miyazaki, S. 2006. Thirty years of calcium signals at fertilization. Semin. Cell Dev. Biol. 17: 233-243.
113. 2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science 257: 251-255.
114. Motlik, J., J. Fulka Jr., R. Prochazka, Z. Rimkevicova, M. Kulbelka, and J. Fulka. 1989. RNA and protein synthesis requirements for the resumption of meiosis in rabbit oocytes: the role of cumulus cells. Reprod. Nutr. Dev. 29: 601-609.
115. Motoshima, H., B. J. Goldstein, M. Igata, and E. Araki. 2006. AMPK and cell proliferation-AMPK as a therapeutic target for atherosclerosis and cancer. J. Physiol. 574: 63-71
116. Nakamura, Y., Y. Yamagata, N. Sugino, H. Takayama, and H. Kato. 2002. Nitric oxide inhibits oocyte meiotic maturation. Biol. Reprod. 67: 1588-1592.
117. Nogueira, D., J. C. Sadeu, and J. Montagut. 2012. In vitro oocyte maturation: current status. Semin. Reprod. Med. 30: 199-213.
118. 2+ signal that induces egg activation and embryo development. Bioessays 34: 126-134
119. Norenburg, J. L., and S. A. Stricker. 2002. Phylum Nemertea. Pp. 163-179 in Atlas of Marine Invertebrate Larvae, C. Young, M. A. Sewel, and M. Rice, eds. Academic Press, San Diego.
120. Oh, J. S., S. J. Han, and M. Conti. 2010. Wee1B, Myt1, and Cdc25 function in distinct compartments of the mouse oocyte to control meiotic maturation. J. Cell Biol. 188: 199-207.
121. Paleos, G. A., and R. D. Powers. 1981. The effect of calcium on the first meiotic division of the mammalian oocyte. J. Exp. Zool. 217: 409-416.
122. Park, J. Y., Y. Q. Su, M. Ariga, E. Law, S. L. Jin, and M. Conti. 2004. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303: 682-684.
123. Parrington, J., L. C. Davis, A. Galione, and G. Wessel. 2007. Flipping the switch: how a sperm activates the egg at fertilization. Dev. Dyn. 236: 2027-2038.
124. Pirino, G., M. P. Wescott, and P. J. Donovan. 2009. Protein kinase A regulates resumption of meiosis by phosphorylation of Cdc25B in mammalian oocytes. Cell Cycle 8: 665-670.
125. Plancha, C. E., and D. F. Albertini. 1992. Protein synthesis requirements during resumption of meiosis in the hamster oocyte-early nuclear and microtubule configurations. Mol. Reprod. Dev. 33: 324-332.
126. Quan, H.-M., H.-Y. Fan, X.-Q. Meng, D.-Y. Chen, H. Schatten, P.-M. Yang, and Q.-Y. Sun. 2003. Effects of PKC activation of the meiotic maturation, fertilization and early development of mouse oocytes. Zygote 11: 329-337.
127. Ramadan, W. M., J. Kashir, C. Jones, and K. Coward. 2012. Oocyte activation and phospholipase C zeta (PLCζ): diagnostic and therapeutic implications for assisted reproductive technology. Cell Comm. Signal. 10: doi: 10.1186/1478-811X-10-12
128. Rodrigues, P., D. Limback, L. McGinnis, C. E. Plancha, and D. F. Albertini. 2008. Oogenesis: prospects and challenges for the future. J. Cell. Physiol. 216: 355-365.
129. 2+ release by the same pathway as fertilization. Development 127: 3227-3236.
130. Runft, L., L. A. Jaffe, and L. M. Mehlmann. 2002. Egg activation at fertilization: where it all begins. Dev. Biol. 245: 237-254.
131. Salustri, A., S. Petrungaro, M. De Felice, M. Conti, and G. Siracusa. 1985. Effect of follicle-stimulating hormone on cyclic adenosine monophosphate level and on meiotic maturation in mouse cumulus cell-enclosed oocytes cultured in vitro. Biol. Reprod. 33: 797-802.
132. Santella, L., F. Vasilev, and J. T. Chun. 2012. Fertilization in echinoderms. Biochim. Biophys. Res. Comm. 425: 588-594.
133. Sardet, C., F. Roegiers, R. Dumollard, C. Rouviere, and A. McDougall. 1998. Calcium waves and oscillations in eggs. Biophys. Chem. 72: 131-140.
134. Sasseville, M., N. Cote, C. Guillemette, and F. J. Richard. 2006. New insight into the role of phosphodiesterase 3A in porcine oocyte maturation. BMC Dev. Biol. 6: doi:10.1186/1471-213X-6-47
135. Schroeder, T. E., and S. A. Stricker. 1983. Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Dev. Biol. 98: 373-384.
136. Schultz, R. M., and P. M. Wassarman. 1977. Biochemical studies of mammalian oogenesis: protein synthesis during oocyte growth and meiotic maturation in the mouse. J. Cell Sci. 24: 167-194.
137. Sela-Abramovich, S., D. Galiani, N. Nevo, and N. Dekel. 2008. Inhibition of rat oocyte maturation and ovulation by nitric oxide: mechanism of action. Biol. Reprod. 78: 1111-1118.
138. Shalgi, R., R. Kaplan, and P. F. Kraicer. 1985. The influence of postovulatory age on the rate of cleavage in in vitro fertilized rat oocytes. Gamete Res. 11: 99-106.
139. 2+ signaling during maturation of cumulus-oocyte complex in mammals. Mol. Reprod. Dev. 78: 744-756.
140. Smythe, T. L., and S. A. Stricker. 2005. Germinal vesicle breakdown is not fully dependent on MAPK activation in maturing oocytes of marine nemertean worms. Mol. Reprod. Dev. 70: 91-102.
141. Sobinoff, A. P, J. M. Sutherland, and E. A. McLaughlin. 2012. Intracellular signalling during female gametogenesis. Mol. Hum. Reprod. doi: 10.1093/molehr/gas065
142. Solc, P., R. M. Schultz, and J. Motlik. 2010. Prophase I arrest and progression to metaphase I in mouse oocytes: comparison of resumption of meiosis and recovery from G2-arrest in somatic cells. Mol. Hum. Reprod. 16: 654-664.
143. Stricker, S. A. 1982. The morphology of Paranemertes sanjuanensis sp. n. (Nemertea, Monostilifera) from Washington, USA. Zool. Scr. 11: 107-115.
144. Stricker, S. A. 1985. A new species of Tetrastemma (Nemertea, Monostilifera) from San Juan Island, Washington, U.S.A. Can. J. Zool. 63: 682-690.
145. Stricker, S. A. 1986. An ultrastructural study of oogenesis, fertilization, and egg laying in a nemertean ectosymbiont of crabs, Carcinonemertes epialti (Nemertea, Hoplonemertea). Can. J. Zool. 64: 1256-1269.
146. Stricker, S. A. 1987. Phylum Nemertea. Pp. 129-137 in Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast, M. Strathmann, ed. Univ. Washington Press, Seattle.
147. Stricker, S. A. 1995. Time-lapse confocal imaging of calcium dynamics in starfish embryos. Dev. Biol. 170: 496-518.
148. Stricker, S. A. 1996. Repetitive calcium waves induced by fertilization in the nemertean worm Cerebratulus lacteus. Dev. Biol. 176: 243-363.
149. Stricker, S. A. 1997. Intracellular injections of a soluble sperm factor trigger calcium oscillations and meiotic maturation in the unfertilized oocytes of a marine worm. Dev. Biol. 186: 185-201.
150. Stricker, S. A. 1999. Comparative calcium signaling during fertilization and egg activation in animals. Dev. Biol. 211: 157-176.
151. Stricker, S. A. 2000. Confocal microscopy of intracellular calcium dynamics during fertilization. BioTechniques 29: 492-498.
152. Stricker, S. A. 2004. Dual-channel confocal ratioing of calcium dynamics in living eggs and oocytes. Pp. 137-148 in Germ Cell Protocols, Vol. 2, H. Schatten, ed. Humana Press, Totowa, NJ.
153. Stricker, S. A. 2004. Dual-channel confocal ratioing of calcium dynamics in living eggs and oocytes. Pp. 137-148 in Germ Cell Protocols, Vol. 2, H. Schatten, ed. Humana Press, Totowa, NJ.
154. Stricker, S. A. 2009a. Roles of protein kinase C isotypes during seawaterversus cAMP-induced oocyte maturation in a marine worm. Mol. Reprod. Dev. 76: 693-707.
155. Stricker, S. A. 2009b. 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.
156. Stricker, S. A. 2011. Potential upstream regulators and downstream targets of AMP-activated kinase (AMPK) during oocyte maturation in a marine worm. Reproduction 142: 29-39.
157. Stricker, S. A. 2012. Inhibition of germinal vesicle breakdown by antioxidants and the roles of signaling pathways related to nitric oxide and cGMP during meiotic resumption in oocytes of a marine worm. Reproduction 143: 261-270.
158. Stricker, S. A., and M. W. Folsom. 1998. A comparative ultrastructural analysis of spermatogenesis in nemertean worms. Hydrobiologia 365: 55-72.
159. Stricker, S. A., and T. L. Smythe. 2000. Multiple triggers of oocyte maturation in nemertean worms: the roles of calcium and serotonin. J. Exp. Zool. 287: 243-261.
160. Stricker, S. A., and T. L. Smythe 2001. 5-HT causes an increase in cAMP that stimulates, rather than inhibits, oocyte maturation in marine nemertean worms. Development 128: 1415-1427.
161. 2+ signaling in maturing and fertilized oocytes of marine protostome worms: the roles of MAPKs and MPF. Development 130: 2867-2879.
162. Stricker, S. A., and T. L. Smythe. 2006a. 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. 73: 1578-1590.
163. Stricker, S. A., and T. L. Smythe. 2006b. Differing mechanisms of cAMP- versus seawater-induced oocyte maturation in marine nemertean worms. II. The roles of tyrosine kinases and phosphatases. Mol. Reprod. Dev. 73: 1564-1577.
164. Stricker, S. A., and M. Whitaker. 1999. Confocal laser scanning microscopy of calcium dynamics in living cells. Micr. Res. Tech. 46: 356-369.
165. Stricker, S. A., V. E. Centonze, S. W. Paddock, and G. Schatten. 1992. Confocal microscopy of fertilization-induced calcium dynamics in sea urchin eggs. Dev. Biol. 149: 370-380.
166. Stricker, S. A., R. Silva, and T. Smythe. 1998. Calcium and endoplasmic reticulum dynamics during oocyte maturation and fertilization in the marine worm Cerebratulus lacteus. Dev. Biol. 203: 305-322.
167. Stricker, S. A., K. Swann, K. T. Jones, and R. A. Fissore. 2000. Injections of porcine sperm extracts trigger fertilization-like calcium oscillations in oocytes of a marine worm. Exp. Cell Res. 257: 341-347.
168. Stricker, S. A., T. L. Smythe, L. Miller, and J. L. Norenburg. 2001. Comparative biology of oogenesis in nemertean worms. Acta Zool. 82: 213-230.
169. Stricker, S. A., J. R. Escalona, S. Abernathy, and A. Marquardt. 2010a. Pharmacological analyses of protein kinases regulating egg maturation in marine nemertean worms: a review and comparison with mammalian eggs. Mar. Drugs 8: 2417-2434.
170. Stricker, S. A., L. Swiderek, and T. Nguyen. 2010b. 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. 77: 497-510.
171. Stricker, S. A., D. J. Carroll, and W. L. Tsui. 2010c. Roles of Src family kinases during fertilization and the first cell cycle in the marine protostome worm Cerebratulus. Int. J. Dev. Biol. 54: 787-793.
172. Struck, T., and F. Fisse. 2008. Phylogenetic position of Nemertea derived from phylogenomic data. Mol. Biol. Evol. 25: 728-736.
173. Su, Y. Q., G. L. Xia, A. G. Byskov, C. D. Fu, and C. R. Yang. 1999. Protein kinase C and intracellular calcium are involved in folliclestimulating hormone-mediated meiotic resumption of cumulus cellenclosed porcine oocytes in hypoxanthine-supplemented medium. Mol. Reprod. Dev. 53: 51-58.
174. Su, Y. Q., K. Sugiura, Q. Li, K. Wigglesworth, M. M. Matzuk, and J. J. Eppig. 2010. Mouse oocytes enable LH-induced maturation of the cumulus-oocyte complex via promoting EGF receptor-dependent signalling. Mol. Endocrinol. 24: 1230-1239.
175. Sun, Q. Y., Y. L. Miao, and H. Schatten. 2009. Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 8: 2741-2747.
176. Suwa, K., and M. Yamashita. 2007. Regulatory mechanisms of oocyte maturation and ovulation. Pp. 323-347 in The Fish Oocyte: From Basic Studies to Biotechnological Applications, P. J. Babin, J. Cerda, and E. Lubzens, eds. Springer, Dordrecht.
177. 2+ oscillations in fertilizing mammalian eggs. Cell Calcium doi: 10.1016/j.ceca.2012.11.001.
178. Swann, K., and Y. S. Yu. 2008. The dynamics of calcium oscillations that activate mammalian eggs. Int. J. Dev. Biol. 52: 585-594.
179. Takeda, N., K. Kyozuka, and R. Deguchi. 2006. Increase in intracellular cAMP is a prerequisite signal for initiation of physiological oocyte meiotic maturation in the hydrozoan Cytaeis uchidae. Dev. Biol. 298: 248-258.
180. Talmor-Cohen, A., R. Tomashov-Matar, E. Eliyahu, R. Shapiro, and R. Shalgi. 2004. Are Src family kinases involved in cell cycle resumption in rat eggs? Reproduction 127: 455-463.
181. Taylor, S. S., J. Yang, J. Wu, N. M. Haste, E. Radzio-Andzelm, and G. Annand. 2004. PKA: a portrait of protein kinase dynamics. Biochim. Biophys. Acta 1697: 259-269.
182. Terasaki, M., and L. A. Jaffe. 2004. Labeling of cell membranes and compartments for live cell fluorescence microscopy. Methods Cell Biol. 74: 469-489.
183. 2+ independent in the mouse oocyte. J. Cell Biol. 117: 799-811.
184. Tosca, L., S. Uzbekova, C. Chabrolle, and J. Dupont. 2007. 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. 77: 452-465.
185. Tosti, E. 2006. Calcium ion currents mediating oocyte maturation events. Reprod. Biol. Endocrinol. 4: 26-35.
186. Tripathi, A., S. Khatun, A. N. Pandey, S. K. Mishra, R. Chaube, T. G. Shrivastav, and S. K. Chaube. 2009. Intracellular levels of hydrogen peroxide and nitric oxide in oocytes at various stages of meiotic cell cycle and apoptosis. Free Radic. Res. 43: 287-294.
187. Tripathi, A., K. V. Kumar, and S. K. Chaube. 2010. Meiotic cell cycle arrest in mammalian oocytes. J. Cell. Physiol. 223: 592-600.
188. Tsafriri, A., and N. Dekel. 2010. Intra- and intercellular molecular mechanisms in regulation of meiosis in murid rodents. Pp. 38-63 in Oocyte Maturation and Fertilization: A Long History for a Short Event, E. Tosti and R. Boni, eds. Bentham Science Publishers. [Online.] Available: http://www.benthamscience.com/ebooks/9781608051823/ [2013, July 11].
189. Tsafriri, A., H. R. Lindner, U. Zor, and S. A. Lamprecht. 1972. In vitro induction of meiotic division in follicle-enclosed rat oocytes by LH, cAMP, and prostaglandin E. J. Reprod. Fertil. 31: 39-50.
190. Tsafriri, A., S.-Y. Chun, R. Zhang, A. J. W. Hsueh, and M. Conti. 1996. Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev. Biol. 178: 393-402.
191. Vacquier, V. D. 2011. Laboratory on sea urchin fertilization. Mol. Reprod. Dev. 78: 553-564.
192. Voronina, E., and G. M. Wessel. 2003. The regulation of oocyte maturation. Curr. Top. Dev. Biol. 58: 53-110.
193. 2+ signaling during mammalian fertilization: requirements, players, and adaptations. Cold Spring Harb. Perspect. Biol. doi: 10.1101/cshperspect.a006767
194. Webb, R. J., L. Tinworth, G. M. H. Thomas, M. Zaccolo, and J. Carroll. 2008. Developmentally acquired PKA localization in mouse oocytes and embryos. Dev. Biol. 317: 36-45.
195. Wessel, G., S. D. Conner, and L. Berg. 2002. Cortical granule translocation is microfilament mediated and linked to meiotic maturation in the sea urchin oocyte. Development 129: 4315-4325.
196. Whitaker, M. 2006. Calcium at fertilization and in early development. Physiol. Rev. 86: 25-88.
197. Whitaker, M., and K. Swann. 1993. Lighting the fuse at fertilization. Development 117: 1-12.
198. Wilson, C. B. 1900. The habits and early development of Cerebratulus lacteus (Verrill): a contribution to physiological morphology. Q. J. Microsc. 43: 97-198.
199. Wu, A. T., P. Sutovsky, G. Manandhar, W. Xu, M. Katayama, B. N. Day, K. W. Park, Y. J. Yi, Y. W. Xi, R. S. Prather, et al. 2007. PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J. Biol. Chem. 282: 12164-12175.
200. Xia, G.-L., A. G. Byskov, and Y. C. Andersen. 1994. Cumulus cells secrete a meiosis-inducing substance by stimulation with forskolin and dibutyric cyclic adenosine monophosphate. Mol. Reprod. Dev. 39: 17-24.
201. Yamada, M., and Y. Isaji. 2011. Structural and functional changes linked to, and factors promoting, cytoplasmic maturation in mammalian oocytes. Reprod. Med. Biol. 2: 69-79.
202. Yamagata, Y., Y. Nakamura, N. Sugino, A. Harad, H. Takayama, S. Kashida, and H. Kato. 2002. Alterations in nitrate/nitrite and nitric oxide synthase in preovulatory follicules of gonadotropin-primed immature rat. Endocr. J. 49: 219-226.
203. Yamashita, M. 2000. Toward modeling of a general mechanism of MPF formation during oocyte maturation in vertebrates. Zool. Sci. 17: 841-851.
204. Yi, J.-H., L. Lefièvre, C. Gagnon, M. Anctil, and F. Dubé. 2002. Increase of cAMP upon release from prophase arrest in surf clam oocytes. J. Cell. Sci. 115: 311-320.
205. 2+ oscillation-inducing phospholipase C zeta expressed in mouse eggs is accumulated to the pronucleus during egg activation. Dev. Biol. 268: 245-257.
206. 2+ oscillations in activation of ascidian eggs. Dev. Biol. 203: 122-133.
207. Yoshimura, Y., Y. Nakamura, M. Ando, M. Jinno, T. Oda, M. Karube, N. Koyama, and T. Nanno. 1992. Stimulatory role of cyclic adenosine monophosphate as a mediator of meiotic resumption in rabbit oocytes. Endocrinology 131, 351-356.
208. Zhang, M., Y. Tao, B. Zhou, H. Xie, F. Wang, L. Lei, L. Huo, Q. Sun, and G. Xia. 2005. Atrial natriuretic peptide inhibits the actions of FSH and forskolin in meiotic maturation of pig oocytes via different signalling pathways. J. Mol. Endocrinol. 34: 459-472.
209. Zhang, Y., Z. Zhang, X.-Y. Xu, X.-S. Li, M. Yu, A.-M. Yu, Z.-H. Zong, and B.-Z. Yu. 2008. Protein kinase A modulates Cdc25B activity during meiotic resumption of mouse oocytes. Dev. Dyn. 237: 3777-3786.
210. 2+ cascade and meiotic resumption of the caprine primary oocyte. Reprod. Domest. Anim. 42: 555-559.
211. Zuckerman, S. 1951. The number of oocytes in the mature ovary. Recent Prog. Horm. Res. 6: 63-109.