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Title: Zinc sparks induce physiochemical changes in the egg zona pellucida that prevent polyspermy

Abstract

During fertilization or chemically-induced egg activation, the mouse egg releases billions of zinc atoms in brief bursts known as ‘zinc sparks.’ The zona pellucida (ZP), a glycoprotein matrix surrounding the egg, is the first structure zinc ions encounter as they diffuse away from the plasma membrane. Following fertilization, the ZP undergoes changes described as ‘hardening’, which prevent multiple sperm from fertilizing the egg and thereby establish a block to polyspermy. A major event in zona hardening is cleavage of ZP2 proteins by ovastacin; however, the overall physiochemical changes contributing to zona hardening are not well understood. Using x-ray fluorescence microscopy, transmission and scanning electron microscopy, and biological function assays, we tested the hypothesis that zinc release contributes to ZP hardening. We found that the zinc content in the ZP increases by 300% following activation and that zinc exposure modulates the architecture of the ZP matrix. Importantly, zinc-induced structural changes of the ZP have a direct biological consequence; namely, they reduce the ability of sperm to bind to the ZP. These results provide a paradigm-shifting model in which fertilization-induced zinc sparks contribute to the polyspermy block by altering conformations of the ZP matrix. Finally, this adds a previously unrecognized factor, namelymore » zinc, to the process of ZP hardening.« less

Authors:
ORCiD logo [1];  [1];  [1];  [1]; ORCiD logo [2];  [2];  [3];  [3];  [4];  [1]
  1. Northwestern Univ., Evanston, IL (United States)
  2. Northwestern Univ., Evanston, IL (United States); Northwestern Univ. Atomic and Nanoscale Characterization Experimental Center, Evanston, IL (United States)
  3. Argonne National Lab. (ANL), Argonne, IL (United States)
  4. Northwestern Univ., Evanston, IL (United States); Northwestern Univ., Chicago, IL (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Science Foundation (NSF); National Institutes of Health (NIH); W.M. Keck Foundation; Chicago Biomedical Consortium; USDOE
OSTI Identifier:
1369059
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Integrative Biology
Additional Journal Information:
Journal Volume: 9; Journal Issue: 2; Journal ID: ISSN 1757-9694
Publisher:
Royal Society of Chemistry
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Que, Emily L., Duncan, Francesca E., Bayer, Amanda R., Philips, Steven J., Roth, Eric W., Bleher, Reiner, Gleber, Sophie C., Vogt, Stefan, Woodruff, Teresa K., and O’Halloran, Thomas V. Zinc sparks induce physiochemical changes in the egg zona pellucida that prevent polyspermy. United States: N. p., 2017. Web. doi:10.1039/C6IB00212A.
Que, Emily L., Duncan, Francesca E., Bayer, Amanda R., Philips, Steven J., Roth, Eric W., Bleher, Reiner, Gleber, Sophie C., Vogt, Stefan, Woodruff, Teresa K., & O’Halloran, Thomas V. Zinc sparks induce physiochemical changes in the egg zona pellucida that prevent polyspermy. United States. doi:10.1039/C6IB00212A.
Que, Emily L., Duncan, Francesca E., Bayer, Amanda R., Philips, Steven J., Roth, Eric W., Bleher, Reiner, Gleber, Sophie C., Vogt, Stefan, Woodruff, Teresa K., and O’Halloran, Thomas V. Thu . "Zinc sparks induce physiochemical changes in the egg zona pellucida that prevent polyspermy". United States. doi:10.1039/C6IB00212A. https://www.osti.gov/servlets/purl/1369059.
@article{osti_1369059,
title = {Zinc sparks induce physiochemical changes in the egg zona pellucida that prevent polyspermy},
author = {Que, Emily L. and Duncan, Francesca E. and Bayer, Amanda R. and Philips, Steven J. and Roth, Eric W. and Bleher, Reiner and Gleber, Sophie C. and Vogt, Stefan and Woodruff, Teresa K. and O’Halloran, Thomas V.},
abstractNote = {During fertilization or chemically-induced egg activation, the mouse egg releases billions of zinc atoms in brief bursts known as ‘zinc sparks.’ The zona pellucida (ZP), a glycoprotein matrix surrounding the egg, is the first structure zinc ions encounter as they diffuse away from the plasma membrane. Following fertilization, the ZP undergoes changes described as ‘hardening’, which prevent multiple sperm from fertilizing the egg and thereby establish a block to polyspermy. A major event in zona hardening is cleavage of ZP2 proteins by ovastacin; however, the overall physiochemical changes contributing to zona hardening are not well understood. Using x-ray fluorescence microscopy, transmission and scanning electron microscopy, and biological function assays, we tested the hypothesis that zinc release contributes to ZP hardening. We found that the zinc content in the ZP increases by 300% following activation and that zinc exposure modulates the architecture of the ZP matrix. Importantly, zinc-induced structural changes of the ZP have a direct biological consequence; namely, they reduce the ability of sperm to bind to the ZP. These results provide a paradigm-shifting model in which fertilization-induced zinc sparks contribute to the polyspermy block by altering conformations of the ZP matrix. Finally, this adds a previously unrecognized factor, namely zinc, to the process of ZP hardening.},
doi = {10.1039/C6IB00212A},
journal = {Integrative Biology},
number = 2,
volume = 9,
place = {United States},
year = {2017},
month = {1}
}

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