Quantitative mapping of zinc fluxes in the mammalian egg reveals the origin of fertilization-induced zinc sparks

Emily L. Que; Reiner Bleher; Francesca E. Duncan; Betty Y. Kong; Sophie C. Gleber; Stefan Vogt; Si Chen; Seth A. Garwin; Amanda R. Bayer; Vinayak P. Dravid; Teresa K. Woodruff; Thomas V. O'Halloran

doi:10.1038/nchem.2133

Quantitative mapping of zinc fluxes in the mammalian egg reveals the origin of fertilization-induced zinc sparks

Emily L. Que, Reiner Bleher, Francesca E. Duncan, Betty Y. Kong, Sophie C. Gleber, Stefan Vogt, Si Chen, Seth A. Garwin, Amanda R. Bayer, Vinayak P. Dravid, Teresa K. Woodruff^*, Thomas V. O'Halloran

^*Corresponding author for this work

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

171 Scopus citations

Abstract

Fertilization of a mammalian egg initiates a series of 'zinc sparks' that are necessary to induce the egg-to-embryo transition. Despite the importance of these zinc-efflux events little is known about their origin. To understand the molecular mechanism of the zinc spark we combined four physical approaches that resolve zinc distributions in single cells: a chemical probe for dynamic live-cell fluorescence imaging and a combination of scanning transmission electron microscopy with energy-dispersive spectroscopy, X-ray fluorescence microscopy and three-dimensional elemental tomography for high-resolution elemental mapping. We show that the zinc spark arises from a system of thousands of zinc-loaded vesicles, each of which contains, on average, 10 ⁶ zinc atoms. These vesicles undergo dynamic movement during oocyte maturation and exocytosis at the time of fertilization. The discovery of these vesicles and the demonstration that zinc sparks originate from them provides a quantitative framework for understanding how zinc fluxes regulate cellular processes.

Original language	English (US)
Pages (from-to)	130-139
Number of pages	10
Journal	Nature chemistry
Volume	7
Issue number	2
DOIs	https://doi.org/10.1038/nchem.2133
State	Published - 2015

Funding

The authors thank members of the O’Halloran, Woodruff and Dravid labs for scientific discussions and advice. We thank E. W. Roth for the preparation of electron microscopy samples and J-H. Chung and J. Shangguan for help with chemical syntheses. Equipment and experimental guidance were provided by the following core facilities at Northwestern University: the Integrated Molecular Structure Education and Research Center, the Biological Imaging Facility, the Quantitative Bioelemental Imaging Center, the Electron Probe Instrumentation Centre and the Keck Biophysics Facility. 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. This work was supported by a Medical Research Award from the W. M. Keck Foundation, a SPARK Award from the Chicago Biomedical Consortium and the National Institutes of Health (P01 HD021921, GM38784, U54HD076188 and T32GM105538).

ASJC Scopus subject areas

General Chemical Engineering
General Chemistry

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title = "Quantitative mapping of zinc fluxes in the mammalian egg reveals the origin of fertilization-induced zinc sparks",

abstract = "Fertilization of a mammalian egg initiates a series of 'zinc sparks' that are necessary to induce the egg-to-embryo transition. Despite the importance of these zinc-efflux events little is known about their origin. To understand the molecular mechanism of the zinc spark we combined four physical approaches that resolve zinc distributions in single cells: a chemical probe for dynamic live-cell fluorescence imaging and a combination of scanning transmission electron microscopy with energy-dispersive spectroscopy, X-ray fluorescence microscopy and three-dimensional elemental tomography for high-resolution elemental mapping. We show that the zinc spark arises from a system of thousands of zinc-loaded vesicles, each of which contains, on average, 10 6 zinc atoms. These vesicles undergo dynamic movement during oocyte maturation and exocytosis at the time of fertilization. The discovery of these vesicles and the demonstration that zinc sparks originate from them provides a quantitative framework for understanding how zinc fluxes regulate cellular processes.",

author = "Que, {Emily L.} and Reiner Bleher and Duncan, {Francesca E.} and Kong, {Betty Y.} and Gleber, {Sophie C.} and Stefan Vogt and Si Chen and Garwin, {Seth A.} and Bayer, {Amanda R.} and Dravid, {Vinayak P.} and Woodruff, {Teresa K.} and O'Halloran, {Thomas V.}",

note = "Funding Information: The authors thank members of the O{\textquoteright}Halloran, Woodruff and Dravid labs for scientific discussions and advice. We thank E. W. Roth for the preparation of electron microscopy samples and J-H. Chung and J. Shangguan for help with chemical syntheses. Equipment and experimental guidance were provided by the following core facilities at Northwestern University: the Integrated Molecular Structure Education and Research Center, the Biological Imaging Facility, the Quantitative Bioelemental Imaging Center, the Electron Probe Instrumentation Centre and the Keck Biophysics Facility. 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. This work was supported by a Medical Research Award from the W. M. Keck Foundation, a SPARK Award from the Chicago Biomedical Consortium and the National Institutes of Health (P01 HD021921, GM38784, U54HD076188 and T32GM105538).",

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doi = "10.1038/nchem.2133",

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AU - Bleher, Reiner

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AU - Kong, Betty Y.

AU - Gleber, Sophie C.

AU - Vogt, Stefan

AU - Chen, Si

AU - Garwin, Seth A.

AU - Bayer, Amanda R.

AU - Dravid, Vinayak P.

AU - Woodruff, Teresa K.

AU - O'Halloran, Thomas V.

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AB - Fertilization of a mammalian egg initiates a series of 'zinc sparks' that are necessary to induce the egg-to-embryo transition. Despite the importance of these zinc-efflux events little is known about their origin. To understand the molecular mechanism of the zinc spark we combined four physical approaches that resolve zinc distributions in single cells: a chemical probe for dynamic live-cell fluorescence imaging and a combination of scanning transmission electron microscopy with energy-dispersive spectroscopy, X-ray fluorescence microscopy and three-dimensional elemental tomography for high-resolution elemental mapping. We show that the zinc spark arises from a system of thousands of zinc-loaded vesicles, each of which contains, on average, 10 6 zinc atoms. These vesicles undergo dynamic movement during oocyte maturation and exocytosis at the time of fertilization. The discovery of these vesicles and the demonstration that zinc sparks originate from them provides a quantitative framework for understanding how zinc fluxes regulate cellular processes.

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Quantitative mapping of zinc fluxes in the mammalian egg reveals the origin of fertilization-induced zinc sparks

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