TY - JOUR
T1 - Zinc Dynamics during Drosophila Oocyte Maturation and Egg Activation
AU - Hu, Qinan
AU - Duncan, Francesca E.
AU - Nowakowski, Andrew B.
AU - Antipova, Olga A.
AU - Woodruff, Teresa K.
AU - O'Halloran, Thomas V.
AU - Wolfner, Mariana F.
N1 - Funding Information:
This research used resources of the Advanced Photon Source, a US Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. We thank Cornell's graduate school travel award (to Q.H.) and George P. Hess travel award (to Q.H.); National Institutes of Health grants R01-GM115848 (to T.K.W. and T.V.O.), R01-GM038784 (to T.V.O.), and R21-HD088744 (to M.F.W.); Postdoctoral Individual National Research Service Award F32-GM115052 (to A.B.N.); and Stephen H. Weiss Presidential Fellowship (to M.F.W.) and Barbara Payne Memorial Funds (to M.F.W.) for funding this study. We thank Dr. Robert A. Holmgren for rearing flies for some of the experiments. We thank Dr. Yasir Ahmed-Braimah for suggesting the egg centrifugation experiment and Drs. J. Liu, =C. Han, S. Garwin, and three anonymous reviewers for helpful comments on the manuscript. We thank Adriana N. Vélez-Avilés for assistance with znt35C 1 mutant strain screening and Lauryn A. Worley for assistance with the TPEN fertility assays, and the Society for Developmental Biology's “Choose Development!” fellows' program ( NSF grants IOS-1239422 and REU DBI-1156528 ) and Cornell Molecular Biology and Genetics department's Research Experience for Undergraduates (NSF grant REU DBI-1659534 ) program for supporting them. We thank Cornell's Statistical Consulting Unit for assistance with data analysis. The diagrams for the Graphical Abstract were created using Biorender.
Funding Information:
This research used resources of the Advanced Photon Source, a US Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. We thank Cornell's graduate school travel award (to Q.H.) and George P. Hess travel award (to Q.H.); National Institutes of Health grants R01-GM115848 (to T.K.W. and T.V.O.), R01-GM038784 (to T.V.O.), and R21-HD088744 (to M.F.W.); Postdoctoral Individual National Research Service Award F32-GM115052 (to A.B.N.); and Stephen H. Weiss Presidential Fellowship (to M.F.W.) and Barbara Payne Memorial Funds (to M.F.W.) for funding this study. We thank Dr. Robert A. Holmgren for rearing flies for some of the experiments. We thank Dr. Yasir Ahmed-Braimah for suggesting the egg centrifugation experiment and Drs. J. Liu, =C. Han, S. Garwin, and three anonymous reviewers for helpful comments on the manuscript. We thank Adriana N. V?lez-Avil?s for assistance with znt35C1 mutant strain screening and Lauryn A. Worley for assistance with the TPEN fertility assays, and the Society for Developmental Biology's ?Choose Development!? fellows' program (NSF grants IOS-1239422 and REU DBI-1156528) and Cornell Molecular Biology and Genetics department's Research Experience for Undergraduates (NSF grant REU DBI-1659534) program for supporting them. We thank Cornell's Statistical Consulting Unit for assistance with data analysis. The diagrams for the Graphical Abstract were created using Biorender. Conceptualization, Q.H. F.E.D. and M.F.W; Investigation, Q.H. F.E.D. A.B.N. and O.A.A.; Data Analysis, Q.H. O.A.A. F.E.D. M.F.W. T.K.W. and T.V.O.; Writing, Q.H.; Editing, Q.H. F.E.D. A.B.N. O.A.A. T.K.W. T.V.O. and M.F.W.; Funding Acquisition, T.K.W. T.V.O. and M.F.W. The authors declare no conflict of interests.
Publisher Copyright:
© 2020 The Author(s)
PY - 2020/7/24
Y1 - 2020/7/24
N2 - Temporal fluctuations in zinc concentration are essential signals, including during oogenesis and early embryogenesis. In mammals, zinc accumulation and release are required for oocyte maturation and egg activation, respectively. Here, we demonstrate that zinc flux occurs in Drosophila oocytes and activated eggs, and that zinc is required for female fertility. Our synchrotron-based X-ray fluorescence microscopy reveals zinc as the most abundant transition metal in Drosophila oocytes. Its levels increase during oocyte maturation, accompanied by the appearance of zinc-enriched intracellular granules in the oocyte, which depend on transporters. Subsequently, in egg activation, which mediates the transition from oocyte to embryo, oocyte zinc levels decrease significantly, as does the number of zinc-enriched granules. This pattern of zinc dynamics in Drosophila oocytes follows a similar trajectory to that in mammals, extending the parallels in female gamete processes between Drosophila and mammals and establishing Drosophila as a model for dissecting reproductive roles of zinc.
AB - Temporal fluctuations in zinc concentration are essential signals, including during oogenesis and early embryogenesis. In mammals, zinc accumulation and release are required for oocyte maturation and egg activation, respectively. Here, we demonstrate that zinc flux occurs in Drosophila oocytes and activated eggs, and that zinc is required for female fertility. Our synchrotron-based X-ray fluorescence microscopy reveals zinc as the most abundant transition metal in Drosophila oocytes. Its levels increase during oocyte maturation, accompanied by the appearance of zinc-enriched intracellular granules in the oocyte, which depend on transporters. Subsequently, in egg activation, which mediates the transition from oocyte to embryo, oocyte zinc levels decrease significantly, as does the number of zinc-enriched granules. This pattern of zinc dynamics in Drosophila oocytes follows a similar trajectory to that in mammals, extending the parallels in female gamete processes between Drosophila and mammals and establishing Drosophila as a model for dissecting reproductive roles of zinc.
KW - Biotechnology
KW - Embryology
KW - Evolutionary Developmental Biology
UR - http://www.scopus.com/inward/record.url?scp=85087018784&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85087018784&partnerID=8YFLogxK
U2 - 10.1016/j.isci.2020.101275
DO - 10.1016/j.isci.2020.101275
M3 - Article
C2 - 32615472
AN - SCOPUS:85087018784
SN - 2589-0042
VL - 23
JO - iScience
JF - iScience
IS - 7
M1 - 101275
ER -