Ca2+ homeostasis regulates Xenopus oocyte maturation

Biology of Reproduction

Volumn 78, Issue 4, 2008, Pages 726-735

  Sun, Lu ^b   Hodeify, Rawad ^b   Haun, Shirley ^b   Charlesworth, Amanda ^b   MacNicol, Angus M ^b,d   Ponnappan, Subramaniam ^c   Ponnappan, Usha ^b,c,d   Prigent, Claude ^e   Machaca, Khaled ^a,b,d  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^e UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Aurora kinase A; Calcium; Gamete biology; Meiosis; Oocyte development

Indexed keywords

AURORA A KINASE; CALCIUM; CALMODULIN; PROTEIN KINASE (CALCIUM,CALMODULIN) II; AURORA KINASE; PROTEASOME; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION; GERMINAL VESICLE; MEIOSIS; MITOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE MATURATION; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; SPINDLE CELL; VERTEBRATE; XENOPUS; ANIMAL; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; METABOLISM; OOCYTE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

VERTEBRATA;

ANIMALS; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CALMODULIN; FEMALE; HOMEOSTASIS; MEIOSIS; OOCYTES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; XENOPUS;

EID: 41549140994     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.107.063693     Document Type: Article

References (84)

1. Eppig JJ, Viveiros MM, Marin-Bivens C, De La Fuente R. Regulation of mammalian oocyte maturation. In: Adashi EY, Leung PCK (eds.), The Ovary. San Diego: Elsevier Press; 2004:113-129.
2. Voronina E, Wessel GM. The regulation of oocyte maturation. Curr Top Dev Biol 2003; 58:53-110.
3. Nebreda AR, Ferby I. Regulation of the meiotic cell cycle in oocytes. Curr Opin Cell Biol 2000; 12:666-675.
4. Baitinger C, Alderton J, Poenie M, Schulman H, Steinhardt RA. Multifunctional Ca2+/calmodulin-dependent protein kinase is necessary for nuclear envelope breakdown. J Cell Biol 1990; 111:1763-1773.
5. Morin N, Abrieu A, Lorca T, Martin F, Doree M. The proteolysis-dependent metaphase to anaphase transition: calcium/calmodulin-dependent protein kinase II mediates onset of anaphase in extracts prepared from unfertilized Xenopus eggs. EMBO J 1994; 13:4343-4352.
6. Poenie M, Alderton J, Tsien RY, Steinhardt RA. Changes of free calcium levels with stages of the cell division cycle. Nature 1985; 315:147-149.
7. Means AR. Calcium, calmodulin and cell cycle regulation. FEBS Lett 1994; 347:1-4.
8. Whitaker M. Regulation of the cell division cycle by inositol trisphosphate and the calcium signaling pathway. Adv Sec Mess Phosph Res 1995; 30: 299-310.
9. Stricker SA. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 2000; 211:157-176.
10. 2+. Dev Genes Evol 1996; 206:110-124.
11. Homa ST, Carroll J, Swann K. The role of calcium in mammalian oocyte maturation and egg activation. Hum Reprod 1993; 8:1274-1281.
12. 2+ independent in the mouse oocyte. J Cell Biol 1992; 117:799-811.
13. Wasserman WJ, Masui Y. Initiation of meiotic maturation in Xenopus laevis oocytes by the combination of divalent cations and ionophore A23187. J Exp Zool 1975; 193:369-375.
14. Moreau M, Doree M, Guerrier P. Electrophoretic introduction of calcium into the cortex of Xenopus laevis oocytes triggers meiosis reinitiation. J Exp Zool 1976; 197:443-449.
15. Schorderet-Slatkine S, Schorderet M, Baulieu EE. Initiation of meiotic maturation in Xenopus laevis oocytes by lanthanum. Nature 1976; 262: 289-290.
16. O'Connor CM, Robinson KR, Smith LD. Calcium, potassium, and sodium exchange by full-grown and maturing Xenopus laevis oocytes. Dev Biol 1977; 61:28-40.
17. Wasserman WJ, Pinto LH, O'Connor CM, Smith LD. Progesterone induces a rapid increase in [Ca2+]in of Xenopus laevis oocytes. Proc Natl Acad Sci U S A 1980; 77:1534-1536.
18. Moreau M, Vilain JP, Guerrier P. Free calcium changes associated with hormone action in amphibian oocytes. Dev Biol 1980; 78:201-214.
19. Robinson KR. Maturation of Xenopus oocytes is not accompanied by electrode-detectable calcium changes. Dev Biol 1985; 109:504-508.
20. Cork RJ, Cicirelli MF, Robinson KR. A rise in cytosolic calcium is not necessary for maturation of Xenopus laevis oocytes. Dev Biol 1987; 121:41-47.
21. Carroll J, Swann K. Spontaneous cytosolic calcium oscillations driven by inositol trisphosphate occur during in vitro maturation of mouse oocytes. J Biol Chem 1992; 267:11196-11201.
22. Sun L, Machaca K. Ca2+cyt negatively regulates the initiation of oocyte maturation. J Cell Biol 2004; 165:63-75.
23. 2+ entry. J Cell Biol 2002; 156:75-85.
24. Roghi C, Giet R, Uzbekov R, Morin N, Chartrain I, Le Guellec R, Couturier A, Doree M, Philippe M, Prigent C. The Xenopus protein kinase pEg2 associates with the centrosome in a cell cycle-dependent manner, binds to the spindle microtubules and is involved in bipolar mitotic spindle assembly. J Cell Sci 1998; 111:557-572.
25. Rassa JC, Wilson GM, Brewer GA, Parks GD. Spacing constraints on reinitiation of paramyxovirus transcription: the gene end U tract acts as a spacer to separate gene end from gene start sites. Virology 2000; 274:438-449.
26. Charlesworth A, Cox LL, MacNicol AM. Cytoplasmic polyadenylation element (CPE)- and CPE-binding protein (CPEB)-independent mechanisms regulate early class maternal mRNA translational activation in Xenopus oocytes. J Biol Chem 2004; 279:17650-17659.
27. Hudmon A, Schulman H. Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem J 2002; 364:593-611.
28. Mak DO, McBride SM, Petrenko NB, Foskett JK. Novel regulation of calcium inhibition of the inositol 1,4,5-trisphosphate receptor calcium-release channel. J Gen Physiol 2003; 122:569-581.
29. Kessler BM, Tortorella D, Altun M, Kisselev AF, Fiebiger E, Hekking BG, Ploegh HL, Overkleeft HS. Extended peptide-based inhibitors efficiently target the proteasome and reveal overlapping specificities of the catalytic beta-subunits. Chem Biol 2001; 8:913-929.
30. Zhu Y, Bond J, Thomas P. Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor. Proc Natl Acad Sci U S A 2003; 100:2237-2242.
31. Sadler SE, Maller JL. Identification of a steroid receptor on the surface of Xenopus oocytes by photoaffinity labeling. J Biol Chem 1982; 257:355-361.
32. Maller JL, Butcher FR, Krebs EG. Early effect of progesterone on levels of cyclic adenosine 3′:5′-monophosphate in Xenopus oocytes. J Biol Chem 1979; 254:579-582.
33. Sagata N, Oskarsson M, Copeland T, Brumbaugh J, Vande Woude GF. Function of the c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature 1988; 335:519-525.
34. Barkoff A, Ballantyne S, Wickens M. Meiotic maturation in Xenopus requires polyadenylation of multiple mRNAs. EMBO J 1998; 17:3168-3175.
35. Coleman TR, Dunphy WG. Cdc2 regulatory factors. Curr Opin Cell Biol 1994; 6:877-882.
36. Mendez R, Richter JD. Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol 2001; 2:521-529.
37. Charlesworth A, Wilczynska A, Thampi P, Cox LL, MacNicol AM. Musashi regulates the temporal order of mRNA translation during Xenopus oocyte maturation. EMBO J 2006; 25:2792-2801.
38. Johnson J, Bierle BM, Gallicano GI, Capco DG. Calcium/calmodulin- dependent protein kinase II and calmodulin: regulators of the meiotic spindle in mouse eggs. Dev Biol 1998; 204:464-477.
39. Madgwick S, Levasseur M, Jones KT. Calmodulin-dependent protein kinase II, and not protein kinase C, is sufficient for triggering cell-cycle resumption in mammalian eggs. J Cell Sci 2005; 118:3849-3859.
40. Su YQ, Eppig JJ. Evidence that multifunctional calcium/calmodulin- dependent protein kinase II (CaM KII) participates in the meiotic maturation of mouse oocytes. Mol Reprod Dev 2002; 61:560-569.
41. Ishida A, Kameshita I, Okuno S, Kitani T, Fujisawa H. A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem Biophys Res Commun 1995; 212:806-812.
42. Waldmann R, Hanson PI, Schulman H. Multifunctional Ca2+/calmodulin- dependent protein kinase made Ca2+ independent for functional studies. Biochem 1990; 29:1679-1684.
43. Chin D, Means AR. Calmodulin: a prototypical calcium sensor. Trends Cell Biol 2000; 10:322-328.
44. Welsh MJ, Dedman JR, Brinkley BR, Means AR. Calcium-dependent regulator protein: localization in mitotic apparatus of eukaryotic cells. Proc Natl Acad Sci U S A 1978; 75:1867-1871.
45. Hisanaga S, Pratt MM. Calmodulin interaction with cytoplasmic and flagellar dynein: calcium-dependent binding and stimulation of adenosinetriphosphatase activity. Biochem 1984; 23:3032-3037.
46. Blum JJ, Hayes A, Jamieson GA Jr, Vanaman TC. Calmodulin confers calcium sensitivity on ciliary dynein ATPase. J Cell Biol 1980; 87:386-397.
47. Pfarr CM, Coue M, Grissom PM, Hays TS, Porter ME, McIntosh JR. Cytoplasmic dynein is localized to kinetochores during mitosis. Nature 1990; 345:263-265.
48. Steuer ER, Wordeman L, Schroer TA, Sheetz MP. Localization of cytoplasmic dynein to mitotic spindles and kinetochores. Nature 1990; 345:266-268.
49. Verde F, Berrez JM, Antony C, Karsenti E. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein. J Cell Biol 1991; 112:1177-1187.
50. Becker BE, Romney SJ, Gard DL. XMAP215, XKCM1, NuMA, and cytoplasmic dynein are required for the assembly and organization of the transient microtubule array during the maturation of Xenopus oocytes. Dev Biol 2003; 261:488-505.
51. Geiser JR, Sundberg HA, Chang BH, Muller EG, Davis TN. The essential mitotic target of calmodulin is the 110-kilodalton component of the spindle pole body in Saccharomyces cerevisiae. Mol Cell Biol 1993; 13:7913-7924.
52. Stirling DA, Rayner TF, Prescott AR, Stark MJ. Mutations which block the binding of calmodulin to Spc110p cause multiple mitotic defects. J Cell Sci 1996; 109:1297-1310.
53. Sundberg HA, Goetsch L, Byers B, Davis TN. Role of calmodulin and Spc110p interaction in the proper assembly of spindle pole body compenents. J Cell Biol 1996; 133:111-124.
54. Cartaud A, Ozon R, Walsh MP, Haiech J, Demaille JG. Xenopus laevis oocyte calmodulin in the process of meiotic maturation. J Biol Chem 1980; 255:9404-9408.
55. Cicirelli MF, Smith LD. Do calcium and calmodulin trigger maturation in amphibian oocytes? Dev Biol 1987; 121:48-57.
56. Wasserman WJ, Smith LD. Calmodulin triggers the resumption of meiosis in amphibian oocytes. J Cell Biol 1981; 89:389-394.
57. Huchon D, Ozon R, Fischer EH, Demaille JG. The pure inhibitor of cAMP-dependent protein kinase initiates Xenopus laevis meiotic maturation. A 4-step scheme for meiotic maturation. Mol Cell Endocrinol 1981; 22:211-222.
58. el Saleh SC, Solaro RJ. Calmidazolium, a calmodulin antagonist, stimulates calcium-troponin C and calcium-calmodulin-dependent activation of striated muscle myofilaments. J Biol Chem 1987; 262:17240-17246.
59. Weiss B, Levin RM. Mechanism for selectively inhibiting the activation of cyclic nucleotide phosphodiesterase and adenylate cyclase by antipsychotic agents. Adv Cyclic Nucleotide Res 1978; 9:285-303.
60. Cartaud A, Huchon D, Marot J, Ozon R, Demaille JG. Calmodulin is involved in the first step of oocyte maturation: effects of the antipsychotic drug fluphenazine and of anticalmodulin antibodies on the progesterone-induced maturation of xenopus laevis oocyte. Cell Differ 1981; 10:357-363.
61. Baulieu EE, Godeau F, Schorderet M, Schorderet-Slatkine S. Steroid-induced meiotic division in Xenopus laevis oocytes: surface and calcium. Nature 1978; 275:593-598.
62. Hollinger TG, Alvarez IM. The effect of trifluoperazine on maturation of Xenopus laevis oocytes. J Exp Zool 1984; 230:427-441.
63. Zuhlke RD, Pitt GS, Deisseroth K, Tsien RW, Reuter H. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature 1999; 399:159-162.
64. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, Keen JE, Ishii T, Hirschberg B, Bond CT, Lutsenko S, Maylie J, Adelman JP. Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 1998; 395:503-507.
65. Gross SD, Schwab MS, Taieb FE, Lewellyn AL, Qian YW, Maller JL. The critical role of the MAP kinase pathway in meiosis II in Xenopus oocytes is mediated by p90(Rsk). Curr Biol 2000; 10:430-438.
66. Nakajo N, Yoshitome S, Iwashita J, Iida M, Uto K, Ueno S, Okamoto K, Sagata N. Absence of Wee1 ensures the meiotic cell cycle in Xenopus oocytes. Genes Dev 2000; 14:328-338.
67. xe protooncogene. Proc Natl Acad Sci U S A 1991; 88:5794-5798.
68. Schumacher JM, Golden A, Donovan PJ. AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos. J Cell Biol 1998; 143:1635-1646.
69. Castro A, Mandart E, Lorca T, Galas S. Involvement of Aurora A kinase during meiosis I-II transition in Xenopus oocytes. J Biol Chem 2003; 278:2236-2241.
70. Ma C, Cummings C, Liu XJ. Biphasic activation of Aurora-A kinase during the meiosis I- meiosis II transition in Xenopus oocytes. Mol Cell Biol 2003; 23:1703-1716.
71. Frank-Vaillant M, Haccard O, Thibier C, Ozon R, Arlot-Bonnemains Y, Prigent C, Jessus C. Progesterone regulates the accumulation and the activation of Eg2 kinase in Xenopus oocytes. J Cell Sci 2000; 113:1127-1138.
72. Paris J, Swenson K, Piwnica-Worms H, Richter JD. Maturation-specific polyadenylation: in vitro activation by p34cdc2 and phosphorylation of a 58-kD CPE-binding protein. Genes Dev 1991; 5:1697-1708.
73. Kawahara H, Yokosawa H. Intracellular calcium mobilization regulates the activity of 26 S proteasome during the metaphase-anaphase transition in the ascidian meiotic cell cycle. Dev Biol 1994; 166:623-633.
74. Aizawa H, Kawahara H, Tanaka K, Yokosawa H. Activation of the proteasome during Xenopus egg activation implies a link between proteasome activation and intracellular calcium release. Biochem Biophys Res Commun 1996; 218:224-228.
75. Josefsberg LB, Galiani D, Dantes A, Amsterdam A, Dekel N. The proteasome is involved in the first metaphase-to-anaphase transition of meiosis in rat oocytes. Biol Reprod 2000; 62:1270-1277.
76. Reverte CG, Ahearn MD, Hake LE. CPEB degradation during Xenopus oocyte maturation requires a PEST domain and the 26S proteasome. Dev Biol 2001; 231:447-458.
77. Ishida N, Tanaka K, Tamura T, Nishizawa M, Okazaki K, Sagata N, Ichihara A. Mos is degraded by the 26S proteasome in a ubiquitin-dependent fashion. FEBS Lett 1993; 324:345-348.
78. Weisenberg RC. Microtubule formation in vitro in solutions containing low calcium concentrations. Science 1972; 177:1104-1105.
79. Kirschner MW, Williams RC, Weingarten M, Gerhart JC. Microtubules from mammalian brain: some properties of their depolymerization products and a proposed mechanism of assembly and disassembly. Proc Natl Acad Sci U S A 1974; 71:1159-1163.
80. Eyers PA, Maller JL. Regulating the regulators: Aurora A activation and mitosis. Cell Cycle 2003; 2:287-289.
81. Nigg EA. Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2001; 2:21-32.
82. Gruss OJ, Vernos I. The mechanism of spindle assembly: functions of Ran and its target TPX2. J Cell Biol 2004; 166:949-955.
83. Martinez SE, Yuan L, Lacza C, Ransom H, Mahon GM, Whitehead IP, Hake LE. XGef mediates early CPEB phosphorylation during Xenopus oocyte meiotic maturation. Mol Biol Cell 2005; 16:1152-1164.
84. Keady BT, Kuo P, Martinez SE, Yuan L, Hake LE. MAPK interacts with XGef and is required for CPEB activation during meiosis in Xenopus oocytes. J Cell Sci 2007; 120:1093-1103.