Dynamic zinc fluxes regulate meiotic progression in Caenorhabditis elegans

Adelita D. Mendoza; Aaron Sue; Olga Antipova; Stefan Vogt; Teresa K Woodruff; Sarah M. Wignall; Thomas V O'Halloran

doi:10.1093/biolre/ioac064

Dynamic zinc fluxes regulate meiotic progression in Caenorhabditis elegans

Adelita D. Mendoza, Aaron Sue, Olga Antipova, Stefan Vogt, Teresa K Woodruff, Sarah M. Wignall, Thomas V O'Halloran

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

Abstract

Zinc influx and efflux events are essential for meiotic progression in oocytes of several mammalian and amphibian species, but it is less clear whether this evolutionary conservation of zinc signals is also important in late-stage germline development in invertebrates. Using quantitative, single cell elemental mapping methods, we find that Caenorhabditis elegans oocytes undergo significant stage-dependent fluctuations in total zinc content, rising by over sevenfold from Prophase I through the beginning of mitotic divisions in the embryo. Live imaging of the rapid cell cycle progression in C. elegans enables us to follow changes in labile zinc pools across meiosis and mitosis in single embryo. We find a dynamic increase in labile zinc prior to fertilization that then decreases from Anaphase II through pronuclear fusion and relocalizes to the eggshell. Disruption of these zinc fluxes blocks extrusion of the second polar body, leading to a range of mitotic defects. We conclude that spatial temporal zinc fluxes are necessary for meiotic progression in C. elegans and are a conserved feature of germ cell development in a broad cross section of metazoa.

Original language	English (US)
Pages (from-to)	406-418
Number of pages	13
Journal	Biology of reproduction
Volume	107
Issue number	2
DOIs	https://doi.org/10.1093/biolre/ioac064
State	Published - Aug 1 2022

Funding

This project was supported by NIH grants R01GM115848 to TVO and TKW, R01GM038784, P41GM181350 to TVO, and R01GM124354 to SMW. ADM was supported by the Ruth L. Kirchenstein F31 NRSA (F31GM112478) and the Chicago Biomedical Consortium Scholarship (A2011-00985). Elemental analysis was performed at the Northwestern University Quantitative Bio-element Imaging Center supported by the Office of the Director, National Institutes of Health via NIH grants S10OD026786 and S10OD020118. Research at the Advanced Photon Source, a U.S. Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory was supported under Contract No. DE-AC02-06CH11357.

Keywords

C. elegans
X-ray fluorescence microscopy
egg activation
meiosis
oogenesis
zinc

ASJC Scopus subject areas

Reproductive Medicine

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10.1093/biolre/ioac064

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abstract = "Zinc influx and efflux events are essential for meiotic progression in oocytes of several mammalian and amphibian species, but it is less clear whether this evolutionary conservation of zinc signals is also important in late-stage germline development in invertebrates. Using quantitative, single cell elemental mapping methods, we find that Caenorhabditis elegans oocytes undergo significant stage-dependent fluctuations in total zinc content, rising by over sevenfold from Prophase I through the beginning of mitotic divisions in the embryo. Live imaging of the rapid cell cycle progression in C. elegans enables us to follow changes in labile zinc pools across meiosis and mitosis in single embryo. We find a dynamic increase in labile zinc prior to fertilization that then decreases from Anaphase II through pronuclear fusion and relocalizes to the eggshell. Disruption of these zinc fluxes blocks extrusion of the second polar body, leading to a range of mitotic defects. We conclude that spatial temporal zinc fluxes are necessary for meiotic progression in C. elegans and are a conserved feature of germ cell development in a broad cross section of metazoa.",

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AU - Wignall, Sarah M.

AU - O'Halloran, Thomas V

N1 - Publisher Copyright: © The Author(s) 2022. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: [email protected].

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N2 - Zinc influx and efflux events are essential for meiotic progression in oocytes of several mammalian and amphibian species, but it is less clear whether this evolutionary conservation of zinc signals is also important in late-stage germline development in invertebrates. Using quantitative, single cell elemental mapping methods, we find that Caenorhabditis elegans oocytes undergo significant stage-dependent fluctuations in total zinc content, rising by over sevenfold from Prophase I through the beginning of mitotic divisions in the embryo. Live imaging of the rapid cell cycle progression in C. elegans enables us to follow changes in labile zinc pools across meiosis and mitosis in single embryo. We find a dynamic increase in labile zinc prior to fertilization that then decreases from Anaphase II through pronuclear fusion and relocalizes to the eggshell. Disruption of these zinc fluxes blocks extrusion of the second polar body, leading to a range of mitotic defects. We conclude that spatial temporal zinc fluxes are necessary for meiotic progression in C. elegans and are a conserved feature of germ cell development in a broad cross section of metazoa.

AB - Zinc influx and efflux events are essential for meiotic progression in oocytes of several mammalian and amphibian species, but it is less clear whether this evolutionary conservation of zinc signals is also important in late-stage germline development in invertebrates. Using quantitative, single cell elemental mapping methods, we find that Caenorhabditis elegans oocytes undergo significant stage-dependent fluctuations in total zinc content, rising by over sevenfold from Prophase I through the beginning of mitotic divisions in the embryo. Live imaging of the rapid cell cycle progression in C. elegans enables us to follow changes in labile zinc pools across meiosis and mitosis in single embryo. We find a dynamic increase in labile zinc prior to fertilization that then decreases from Anaphase II through pronuclear fusion and relocalizes to the eggshell. Disruption of these zinc fluxes blocks extrusion of the second polar body, leading to a range of mitotic defects. We conclude that spatial temporal zinc fluxes are necessary for meiotic progression in C. elegans and are a conserved feature of germ cell development in a broad cross section of metazoa.

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Dynamic zinc fluxes regulate meiotic progression in Caenorhabditis elegans

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