XB-ART-36964
Biol Reprod
2008 Apr 01;784:726-35. doi: 10.1095/biolreprod.107.063693.
Show Gene links
Show Anatomy links
Ca2+ homeostasis regulates Xenopus oocyte maturation.
Sun L
,
Hodeify R
,
Haun S
,
Charlesworth A
,
MacNicol AM
,
Ponnappan S
,
Ponnappan U
,
Prigent C
,
Machaca K
.
???displayArticle.abstract???
In contrast to the well-defined role of Ca2+ signals during mitosis, the contribution of Ca2+ signaling to meiosis progression is controversial, despite several decades of investigating the role of Ca2+ and its effectors in vertebrate oocyte maturation. We have previously shown that during Xenopus oocyte maturation, Ca2+ signals are dispensable for entry into meiosis and for germinal vesicle breakdown. However, normal Ca2+ homeostasis is essential for completion of meiosis I and extrusion of the first polar body. In this study, we test the contribution of several downstream effectors in mediating the Ca2+ effects during oocyte maturation. We show that calmodulin and calcium-calmodulin-dependent protein kinase II (CAMK2) are not critical downstream Ca2+ effectors during meiotic maturation. In contrast, accumulation of Aurora kinase A (AURKA) protein is disrupted in cells deprived of Ca2+ signals. Since AURKA is required for bipolar spindle formation, failure to accumulate AURKA may contribute to the defective spindle phenotype following Ca2+ deprivation. These findings argue that Ca2+ homeostasis is important in establishing the oocyte's competence to undergo maturation in preparation for fertilization and embryonic development.
???displayArticle.pubmedLink??? 18094360
???displayArticle.pmcLink??? PMC2587222
???displayArticle.link??? Biol Reprod
???displayArticle.grants??? [+]
AG13081 NIA NIH HHS , GM-61829 NIGMS NIH HHS , HD35688 NICHD NIH HHS , R01 GM061829-07 NIGMS NIH HHS , R01 GM061829-08 NIGMS NIH HHS , R01 HD035688-08A2 NICHD NIH HHS , RR20146 NCRR NIH HHS , R01 HD035688 NICHD NIH HHS
Species referenced: Xenopus
Genes referenced: aurka
References [+] :
Aizawa,
Activation of the proteasome during Xenopus egg activation implies a link between proteasome activation and intracellular calcium release.
1996, Pubmed,
Xenbase
Aizawa, Activation of the proteasome during Xenopus egg activation implies a link between proteasome activation and intracellular calcium release. 1996, Pubmed , Xenbase
Baitinger, Multifunctional Ca2+/calmodulin-dependent protein kinase is necessary for nuclear envelope breakdown. 1990, Pubmed
Barkoff, Meiotic maturation in Xenopus requires polyadenylation of multiple mRNAs. 1998, Pubmed , Xenbase
Baulieu, Steroid-induced meiotic division in Xenopus laevis oocytes: surface and calcium. 1978, Pubmed , Xenbase
Becker, XMAP215, XKCM1, NuMA, and cytoplasmic dynein are required for the assembly and organization of the transient microtubule array during the maturation of Xenopus oocytes. 2003, Pubmed , Xenbase
Blum, Calmodulin confers calcium sensitivity on ciliary dynein ATPase. 1980, Pubmed
Carroll, Spontaneous cytosolic calcium oscillations driven by inositol trisphosphate occur during in vitro maturation of mouse oocytes. 1992, Pubmed
Cartaud, Xenopus laevis oocyte calmodulin in the process of meiotic maturation. 1980, Pubmed , Xenbase
Cartaud, 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. 1981, Pubmed , Xenbase
Castro, Involvement of Aurora A kinase during meiosis I-II transition in Xenopus oocytes. 2003, Pubmed , Xenbase
Charlesworth, Cytoplasmic polyadenylation element (CPE)- and CPE-binding protein (CPEB)-independent mechanisms regulate early class maternal mRNA translational activation in Xenopus oocytes. 2004, Pubmed , Xenbase
Charlesworth, Musashi regulates the temporal order of mRNA translation during Xenopus oocyte maturation. 2006, Pubmed , Xenbase
Chin, Calmodulin: a prototypical calcium sensor. 2000, Pubmed
Cicirelli, Do calcium and calmodulin trigger maturation in amphibian oocytes? 1987, Pubmed , Xenbase
Coleman, Cdc2 regulatory factors. 1994, Pubmed
Cork, A rise in cytosolic calcium is not necessary for maturation of Xenopus laevis oocytes. 1987, Pubmed , Xenbase
Duesbery, The role of Ca(2+) in progesterone-induced germinal vesicle breakdown of Xenopus laevis oocytes: the synergic effects of microtubule depolymerization and Ca(2+). 1996, Pubmed , Xenbase
el-Saleh, Calmidazolium, a calmodulin antagonist, stimulates calcium-troponin C and calcium-calmodulin-dependent activation of striated muscle myofilaments. 1987, Pubmed
Eyers, Regulating the regulators: Aurora A activation and mitosis. 2003, Pubmed , Xenbase
Frank-Vaillant, Progesterone regulates the accumulation and the activation of Eg2 kinase in Xenopus oocytes. 2000, Pubmed , Xenbase
Geiser, The essential mitotic target of calmodulin is the 110-kilodalton component of the spindle pole body in Saccharomyces cerevisiae. 1993, Pubmed
Gross, The critical role of the MAP kinase pathway in meiosis II in Xenopus oocytes is mediated by p90(Rsk). 2000, Pubmed , Xenbase
Gruss, The mechanism of spindle assembly: functions of Ran and its target TPX2. 2004, Pubmed
Hisanaga, Calmodulin interaction with cytoplasmic and flagellar dynein: calcium-dependent binding and stimulation of adenosinetriphosphatase activity. 1984, Pubmed
Hollinger, The effect of trifluoperazine on maturation of Xenopus laevis oocytes. 1984, Pubmed , Xenbase
Homa, The role of calcium in mammalian oocyte maturation and egg activation. 1993, Pubmed
Huchon, The pure inhibitor of cAMP-dependent protein kinase initiates Xenopus laevis meiotic maturation. A 4-step scheme for meiotic maturation. 1981, Pubmed , Xenbase
Hudmon, Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. 2002, Pubmed
Ishida, Mos is degraded by the 26S proteasome in a ubiquitin-dependent fashion. 1993, Pubmed , Xenbase
Ishida, A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. 1995, Pubmed
Johnson, Calcium/calmodulin-dependent protein kinase II and calmodulin: regulators of the meiotic spindle in mouse eggs. 1998, Pubmed
Josefsberg, The proteasome is involved in the first metaphase-to-anaphase transition of meiosis in rat oocytes. 2000, Pubmed
Kanki, Progression from meiosis I to meiosis II in Xenopus oocytes requires de novo translation of the mosxe protooncogene. 1991, Pubmed , Xenbase
Kawahara, Intracellular calcium mobilization regulates the activity of 26 S proteasome during the metaphase-anaphase transition in the ascidian meiotic cell cycle. 1994, Pubmed
Keady, MAPK interacts with XGef and is required for CPEB activation during meiosis in Xenopus oocytes. 2007, Pubmed , Xenbase
Kessler, Extended peptide-based inhibitors efficiently target the proteasome and reveal overlapping specificities of the catalytic beta-subunits. 2001, Pubmed
Kirschner, Microtubules from mammalian brain: some properties of their depolymerization products and a proposed mechanism of assembly and disassembly. 1974, Pubmed
Ma, Biphasic activation of Aurora-A kinase during the meiosis I- meiosis II transition in Xenopus oocytes. 2003, Pubmed , Xenbase
Machaca, Induction of maturation-promoting factor during Xenopus oocyte maturation uncouples Ca(2+) store depletion from store-operated Ca(2+) entry. 2002, Pubmed , Xenbase
Madgwick, Calmodulin-dependent protein kinase II, and not protein kinase C, is sufficient for triggering cell-cycle resumption in mammalian eggs. 2005, Pubmed
Mak, Novel regulation of calcium inhibition of the inositol 1,4,5-trisphosphate receptor calcium-release channel. 2003, Pubmed , Xenbase
Maller, Early effect of progesterone on levels of cyclic adenosine 3':5'-monophosphate in Xenopus oocytes. 1979, Pubmed , Xenbase
Martínez, XGef mediates early CPEB phosphorylation during Xenopus oocyte meiotic maturation. 2005, Pubmed , Xenbase
Means, Calcium, calmodulin and cell cycle regulation. 1994, Pubmed
Mendez, Translational control by CPEB: a means to the end. 2001, Pubmed , Xenbase
Moreau, Electrophoretic introduction of calcium ions into the cortex of Xenopus laevis oocytes triggers meiosis neinitiation. 1976, Pubmed , Xenbase
Moreau, Free calcium changes associated with hormone action in amphibian oocytes. 1980, Pubmed , Xenbase
Morin, The proteolysis-dependent metaphase to anaphase transition: calcium/calmodulin-dependent protein kinase II mediates onset of anaphase in extracts prepared from unfertilized Xenopus eggs. 1994, Pubmed , Xenbase
Nakajo, Absence of Wee1 ensures the meiotic cell cycle in Xenopus oocytes. 2000, Pubmed , Xenbase
Nebreda, Regulation of the meiotic cell cycle in oocytes. 2000, Pubmed , Xenbase
Nigg, Mitotic kinases as regulators of cell division and its checkpoints. 2001, Pubmed
O'Connor, Calcium, potassium, and sodium exchange by full-grown and maturing Xenopus laevis oocytes. 1977, Pubmed , Xenbase
Paris, Maturation-specific polyadenylation: in vitro activation by p34cdc2 and phosphorylation of a 58-kD CPE-binding protein. 1991, Pubmed , Xenbase
Pfarr, Cytoplasmic dynein is localized to kinetochores during mitosis. 1990, Pubmed
Poenie, Changes of free calcium levels with stages of the cell division cycle. , Pubmed
Rassa, Spacing constraints on reinitiation of paramyxovirus transcription: the gene end U tract acts as a spacer to separate gene end from gene start sites. 2000, Pubmed
Reverte, CPEB degradation during Xenopus oocyte maturation requires a PEST domain and the 26S proteasome. 2001, Pubmed , Xenbase
Robinson, Maturation of Xenopus oocytes is not accompanied by electrode-detectable calcium changes. 1985, Pubmed , Xenbase
Roghi, 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. 1998, Pubmed , Xenbase
Sadler, Identification of a steroid receptor on the surface of Xenopus oocytes by photoaffinity labeling. 1982, Pubmed , Xenbase
Sagata, Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. 1988, Pubmed , Xenbase
Schorderet-Slatkine, Initiation of meiotic maturation in Xenopus laevis oocytes by lanthanum. 1976, Pubmed , Xenbase
Schumacher, 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. 1998, Pubmed
Steuer, Localization of cytoplasmic dynein to mitotic spindles and kinetochores. 1990, Pubmed
Stirling, Mutations which block the binding of calmodulin to Spc110p cause multiple mitotic defects. 1996, Pubmed
Stricker, Comparative biology of calcium signaling during fertilization and egg activation in animals. 1999, Pubmed
Su, Evidence that multifunctional calcium/calmodulin-dependent protein kinase II (CaM KII) participates in the meiotic maturation of mouse oocytes. 2002, Pubmed
Sun, Ca(2+)(cyt) negatively regulates the initiation of oocyte maturation. 2004, Pubmed , Xenbase
Sundberg, Role of calmodulin and Spc110p interaction in the proper assembly of spindle pole body compenents. 1996, Pubmed
Tombes, Meiosis, egg activation, and nuclear envelope breakdown are differentially reliant on Ca2+, whereas germinal vesicle breakdown is Ca2+ independent in the mouse oocyte. 1992, Pubmed
Verde, Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein. 1991, Pubmed , Xenbase
Voronina, The regulation of oocyte maturation. 2003, Pubmed
Waldmann, Multifunctional Ca2+/calmodulin-dependent protein kinase made Ca2+ independent for functional studies. 1990, Pubmed , Xenbase
Wasserman, Initiation of meiotic maturation in Xenopus laevis oocytes by the combination of divalent cations and ionophore A23187. 1975, Pubmed , Xenbase
Wasserman, Calmodulin triggers the resumption of meiosis in amphibian oocytes. 1981, Pubmed , Xenbase
Wasserman, Progesterone induces a rapid increase in [Ca2+]in of Xenopus laevis oocytes. 1980, Pubmed , Xenbase
Weisenberg, Microtubule formation in vitro in solutions containing low calcium concentrations. 1972, Pubmed
Weiss, Mechanism for selectively inhibiting the activation of cyclic nucleotide phosphodiesterase and adenylate cyclase by antipsychotic agents. 1978, Pubmed
Welsh, Calcium-dependent regulator protein: localization in mitotic apparatus of eukaryotic cells. 1978, Pubmed
Whitaker, Regulation of the cell division cycle by inositol trisphosphate and the calcium signaling pathway. 1995, Pubmed
Xia, Mechanism of calcium gating in small-conductance calcium-activated potassium channels. 1998, Pubmed , Xenbase
Zhu, Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor. 2003, Pubmed , Xenbase
Zühlke, Calmodulin supports both inactivation and facilitation of L-type calcium channels. 1999, Pubmed , Xenbase