TY - JOUR
T1 - Zinc availability during germline development impacts embryo viability in Caenorhabditis elegans
AU - Mendoza, Adelita D.
AU - Woodruff, Teresa K.
AU - Wignall, Sarah M.
AU - O'Halloran, Thomas V.
N1 - Funding Information:
This research was supported by National Institutes of Health grants GM038784 (TVO) and GM115848 (TVO & TKW), the Chicago Biomedical Consortium with support from the Searle Funds at The Chicago Community Trust (SMW, AM), and training grants T32CA009560 and F31GM112478 in support of AM.
Funding Information:
We acknowledge C. Schiffer and S. Cheung for technical assistance. We thank A. Sue and S. Siepka for assistance in data analysis and manuscript preparation, and the Morimoto lab for providing the worm strain fog-1(q253) . Some strains were provided by the CGC, which is funded by the NIH Office of Research Infrastructure Programs ( P40 OD010440 ). Imaging work was performed at the Northwestern University Biological Imaging Facility generously supported by the Chemistry of Life Processes Institute and the NU Office for Research. Confocal microscopy was performed on a Leica TCS SP5 laser scanning confocal microscope system purchased with funds from the NU Office for Research. Metal analysis was performed at the Northwestern University Quantitative Bio-element Imaging Center with support from NASA Ames Research Center Grant NNA04CC36G .
Publisher Copyright:
© 2016 Elsevier Inc.
PY - 2017/1/1
Y1 - 2017/1/1
N2 - Zinc is an essential metal that serves as a cofactor in a variety of cellular processes, including meiotic maturation. Cellular control of zinc uptake, availability and efflux is closely linked to meiotic progression in rodent and primate reproduction where large fluctuations in zinc levels are critical at several steps in the oocyte-to-embryo transition. Despite these well-documented roles of zinc fluxes during meiosis, only a few of the genes encoding key zinc receptors, membrane-spanning transporters, and downstream signaling pathway factors have been identified to date. Furthermore, little is known about analogous roles for zinc fluxes in the context of a whole organism. Here, we evaluate whether zinc availability regulates germline development and oocyte viability in the nematode Caenorhabditis elegans, an experimentally flexible model organism. We find that similar to mammals, mild zinc limitation in C. elegans profoundly impacts the reproductive axis: the brood size is significantly reduced under conditions of zinc limitation where other physiological functions are not perturbed. Zinc limitation in this organism has a more pronounced impact on oocytes than sperm and this leads to the decrease in viable embryo production. Moreover, acute zinc limitation of isolated zygotes prevents extrusion of the second polar body during meiosis and leads to aneuploid embryos. Thus, the zinc-dependent steps in C. elegans gametogenesis roughly parallel those described in meiotic-to-mitotic transitions in mammals.
AB - Zinc is an essential metal that serves as a cofactor in a variety of cellular processes, including meiotic maturation. Cellular control of zinc uptake, availability and efflux is closely linked to meiotic progression in rodent and primate reproduction where large fluctuations in zinc levels are critical at several steps in the oocyte-to-embryo transition. Despite these well-documented roles of zinc fluxes during meiosis, only a few of the genes encoding key zinc receptors, membrane-spanning transporters, and downstream signaling pathway factors have been identified to date. Furthermore, little is known about analogous roles for zinc fluxes in the context of a whole organism. Here, we evaluate whether zinc availability regulates germline development and oocyte viability in the nematode Caenorhabditis elegans, an experimentally flexible model organism. We find that similar to mammals, mild zinc limitation in C. elegans profoundly impacts the reproductive axis: the brood size is significantly reduced under conditions of zinc limitation where other physiological functions are not perturbed. Zinc limitation in this organism has a more pronounced impact on oocytes than sperm and this leads to the decrease in viable embryo production. Moreover, acute zinc limitation of isolated zygotes prevents extrusion of the second polar body during meiosis and leads to aneuploid embryos. Thus, the zinc-dependent steps in C. elegans gametogenesis roughly parallel those described in meiotic-to-mitotic transitions in mammals.
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U2 - 10.1016/j.cbpc.2016.09.007
DO - 10.1016/j.cbpc.2016.09.007
M3 - Article
C2 - 27664515
AN - SCOPUS:85000898338
SN - 1532-0456
VL - 191
SP - 194
EP - 202
JO - Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology
JF - Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology
ER -