Zinc Availability Regulates Exit from Meiosis in Maturing Mammalian Oocytes

Overview

Journal Nat Chem Biol

Specialties Biochemistry
Biology
Chemistry

Date 2010 Aug 10

PMID 20693991

Citations 117

Authors

Alison M Kim

Stefan Vogt

Thomas V OHalloran

Teresa K Woodruff

Affiliations

Soon will be listed here.

Abstract

Cellular metal ion fluxes are known in alkali and alkaline earth metals but are not well documented in transition metals. Here we describe major changes in the zinc physiology of the mammalian oocyte as it matures and initiates embryonic development. Single-cell elemental analysis of mouse oocytes by synchrotron-based X-ray fluorescence microscopy (XFM) revealed a 50% increase in total zinc content within the 12-14-h period of meiotic maturation. Perturbation of zinc homeostasis with a cell-permeable small-molecule chelator blocked meiotic progression past telophase I. Zinc supplementation rescued this phenotype when administered before this meiotic block. However, after telophase arrest, zinc triggered parthenogenesis, suggesting that exit from this meiotic step is tightly regulated by the availability of a zinc-dependent signal. These results implicate the zinc bolus acquired during meiotic maturation as an important part of the maternal legacy to the embryo.

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References

Falchuk K, Montorzi M . Zinc physiology and biochemistry in oocytes and embryos. Biometals. 2002; 14(3-4):385-95. DOI: 10.1023/a:1012994427351. View

Yamasaki S, Sakata-Sogawa K, Hasegawa A, Suzuki T, Kabu K, Sato E . Zinc is a novel intracellular second messenger. J Cell Biol. 2007; 177(4):637-45. PMC: 2064209. DOI: 10.1083/jcb.200702081. View

Wickramasinghe D, Ebert K, Albertini D . Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes. Dev Biol. 1991; 143(1):162-72. DOI: 10.1016/0012-1606(91)90063-9. View

Stitzel M, Seydoux G . Regulation of the oocyte-to-zygote transition. Science. 2007; 316(5823):407-8. DOI: 10.1126/science.1138236. View

Brunet S, Maro B . Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction. 2005; 130(6):801-11. DOI: 10.1530/rep.1.00364. View

Gandolfi T, Gandolfi F . The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology. 2001; 55(6):1255-76. DOI: 10.1016/s0093-691x(01)00481-2. View

Beyersmann D, Haase H . Functions of zinc in signaling, proliferation and differentiation of mammalian cells. Biometals. 2002; 14(3-4):331-41. DOI: 10.1023/a:1012905406548. View

Barrett S, Albertini D . Allocation of gamma-tubulin between oocyte cortex and meiotic spindle influences asymmetric cytokinesis in the mouse oocyte. Biol Reprod. 2007; 76(6):949-57. DOI: 10.1095/biolreprod.106.057141. View

Toth S, Huneau D, Banrezes B, Ozil J . Egg activation is the result of calcium signal summation in the mouse. Reproduction. 2006; 131(1):27-34. DOI: 10.1530/rep.1.00764. View

10.

Kambe T, Weaver B, Andrews G . The genetics of essential metal homeostasis during development. Genesis. 2008; 46(4):214-28. PMC: 2366893. DOI: 10.1002/dvg.20382. View

11.

Ajduk A, Malagocki A, Maleszewski M . Cytoplasmic maturation of mammalian oocytes: development of a mechanism responsible for sperm-induced Ca2+ oscillations. Reprod Biol. 2008; 8(1):3-22. DOI: 10.1016/s1642-431x(12)60001-1. View

12.

Erickson G, Sorensen R . In vitro maturation of mouse oocytes isolated from late, middle, and pre-antral graafian follicles. J Exp Zool. 1974; 190(1):123-7. DOI: 10.1002/jez.1401900112. View

13.

Santos F, Hendrich B, Reik W, Dean W . Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol. 2002; 241(1):172-82. DOI: 10.1006/dbio.2001.0501. View

14.

Finney L, OHalloran T . Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science. 2003; 300(5621):931-6. DOI: 10.1126/science.1085049. View

15.

Sorensen R, Wassarman P . Relationship between growth and meiotic maturation of the mouse oocyte. Dev Biol. 1976; 50(2):531-6. DOI: 10.1016/0012-1606(76)90172-x. View

16.

Eide D . Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta. 2006; 1763(7):711-22. DOI: 10.1016/j.bbamcr.2006.03.005. View

17.

Taki M, Wolford J, OHalloran T . Emission ratiometric imaging of intracellular zinc: design of a benzoxazole fluorescent sensor and its application in two-photon microscopy. J Am Chem Soc. 2004; 126(3):712-3. DOI: 10.1021/ja039073j. View

18.

Suhy D, Simon K, Linzer D, OHalloran T . Metallothionein is part of a zinc-scavenging mechanism for cell survival under conditions of extreme zinc deprivation. J Biol Chem. 1999; 274(14):9183-92. DOI: 10.1074/jbc.274.14.9183. View

19.

Valko M, Morris H, Cronin M . Metals, toxicity and oxidative stress. Curr Med Chem. 2005; 12(10):1161-208. DOI: 10.2174/0929867053764635. View

20.

Perreault S, Barbee R, Slott V . Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol. 1988; 125(1):181-6. DOI: 10.1016/0012-1606(88)90070-x. View