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 »
- Authors:
-
[1];
[2];
- Northwestern Univ., Evanston, IL (United States)
- Northwestern Univ., Evanston, IL (United States); Northwestern Univ. Atomic and Nanoscale Characterization Experimental Center, Evanston, IL (United States)
- Argonne National Lab. (ANL), Argonne, IL (United States)
- Northwestern Univ., Evanston, IL (United States); Northwestern Univ., Chicago, IL (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (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. https://doi.org/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. https://doi.org/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 = {Thu Jan 19 00:00:00 EST 2017},
month = {Thu Jan 19 00:00:00 EST 2017}
}
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Works referenced in this record:
The mouse zona pellucida: folliculogenesis, fertility and pre-implantation development
journal, May 2000
- Rankin, Tracy; Soyal, Selma; Dean, Jurrien
- Molecular and Cellular Endocrinology, Vol. 163, Issue 1-2
A role for zinc in postsynaptic density asSAMbly and plasticity?
journal, July 2006
- Gundelfinger, Eckart D.; Boeckers, Tobias M.; Baron, Marisa K.
- Trends in Biochemical Sciences, Vol. 31, Issue 7
Izumo meets Juno: Preventing polyspermy in fertilization
journal, June 2014
- Bianchi, Enrica; Wright, Gavin J.
- Cell Cycle, Vol. 13, Issue 13
Juno is the egg Izumo receptor and is essential for mammalian fertilization
journal, April 2014
- Bianchi, Enrica; Doe, Brendan; Goulding, David
- Nature, Vol. 508, Issue 7497
Cellular and molecular mechanisms leading to cortical reaction and polyspermy block in mammalian eggs
journal, June 2003
- Sun, Qing-Yuan
- Microscopy Research and Technique, Vol. 61, Issue 4
BoneJ: Free and extensible bone image analysis in ImageJ
journal, December 2010
- Doube, Michael; Kłosowski, Michał M.; Arganda-Carreras, Ignacio
- Bone, Vol. 47, Issue 6
The inorganic anatomy of the mammalian preimplantation embryo and the requirement of zinc during the first mitotic divisions: Zinc Requirement in Embryo Development
journal, July 2015
- Kong, Betty Y.; Duncan, Francesca E.; Que, Emily L.
- Developmental Dynamics, Vol. 244, Issue 8
Zinc Regulates Meiotic Resumption in Porcine Oocytes via a Protein Kinase C-Related Pathway
journal, July 2014
- Zhao, Ming-Hui; Kwon, Jung-Woo; Liang, Shuang
- PLoS ONE, Vol. 9, Issue 7
Metals in Protein–Protein Interfaces
journal, May 2014
- Song, Woon Ju; Sontz, Pamela A.; Ambroggio, Xavier I.
- Annual Review of Biophysics, Vol. 43, Issue 1
Cellular basis for paracrine regulation of ovarian follicle development
journal, May 2001
- Albertini, Df; Combelles, Cm; Benecchi, E.
- Reproduction
Zona Pellucida Glycoproteins
journal, June 2008
- Wassarman, Paul M.
- Journal of Biological Chemistry, Vol. 283, Issue 36
Mammalian membrane block to polyspermy: new insights into how mammalian eggs prevent fertilisation by multiple sperm
journal, January 2006
- Gardner, Allison J.; Evans, Janice P.
- Reproduction, Fertility and Development, Vol. 18, Issue 2
The fertilization-induced zinc spark is a novel biomarker of mouse embryo quality and early development
journal, March 2016
- Zhang, Nan; Duncan, Francesca E.; Que, Emily L.
- Scientific Reports, Vol. 6, Issue 1
Insights into Egg Coat Assembly and Egg-Sperm Interaction from the X-Ray Structure of Full-Length ZP3
journal, October 2010
- Han, Ling; Monné, Magnus; Okumura, Hiroki
- Cell, Vol. 143, Issue 3
Surface Ultrastructural Alterations of Bovine Oocytes after Parthenogenetic Activation
journal, October 2000
- Suzuki, Hiroyuki; Ju, Jyh-Cherng; Yang, Xiangzhong
- Cloning, Vol. 2, Issue 2
Mammalian cortical granules: Contents, fate, and function
journal, December 1994
- Hoodbhoy, Tanya; Talbot, P.
- Molecular Reproduction and Development, Vol. 39, Issue 4
Localization of cortical granule constituents before and after exocytosis in the hamster egg
journal, April 1988
- Cherr, Gary N.; Drobnis, Erma Z.; Katz, David F.
- Journal of Experimental Zoology, Vol. 246, Issue 1
Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat
journal, January 1985
- Greve, Jeffrey M.; Wassarman, Paul M.
- Journal of Molecular Biology, Vol. 181, Issue 2
The zinc spark is an inorganic signature of human egg activation
journal, April 2016
- Duncan, Francesca E.; Que, Emily L.; Zhang, Nan
- Scientific Reports, Vol. 6, Issue 1
Patterns of intercellular connectivity in the mammalian cumulus-oocyte complex
journal, February 1994
- Albertini, David F.; Rider, Virginia
- Microscopy Research and Technique, Vol. 27, Issue 2
Mammalian Sperm Acrosome: Formation, Contents, and Function
journal, July 2000
- Abou-Haila, Aida; Tulsiani, Daulat R. P.
- Archives of Biochemistry and Biophysics, Vol. 379, Issue 2
Identification of distinctive interdomain interactions among ZP-N, ZP-C and other domains of zona pellucida glycoproteins underlying association of chicken egg-coat matrix
journal, January 2015
- Okumura, Hiroki; Sato, Takahiro; Sakuma, Rio
- FEBS Open Bio, Vol. 5, Issue 1
Role of Zinc during Hamster Sperm Capacitation1
journal, December 1994
- Andrews, Jane C.; Nolan, John P.; Hammerstedt, Roy H.
- Biology of Reproduction, Vol. 51, Issue 6
Zinc availability regulates exit from meiosis in maturing mammalian oocytes
journal, August 2010
- Kim, Alison M.; Vogt, Stefan; O'Halloran, Thomas V.
- Nature Chemical Biology, Vol. 6, Issue 9
Mammalian sperm-egg interaction: Fertilization of mouse eggs triggers modification of the major zona pellucida glycoprotein, ZP2
journal, August 1981
- Bleil, Jeffrey D.; Beall, Clifford F.; Wassarman, Paul M.
- Developmental Biology, Vol. 86, Issue 1
Video image analysis of labile zinc in viable pancreatic islet cells using a specific fluorescent probe for zinc.
journal, July 1994
- Zalewski, P. D.; Millard, S. H.; Forbes, I. J.
- Journal of Histochemistry & Cytochemistry, Vol. 42, Issue 7
Zinc is a novel intracellular second messenger
journal, May 2007
- Yamasaki, Satoru; Sakata-Sogawa, Kumiko; Hasegawa, Aiko
- The Journal of Cell Biology, Vol. 177, Issue 4
A Zinc-Dependent Mechanism Regulates Meiotic Progression in Mammalian Oocytes1
journal, April 2012
- Bernhardt, Miranda L.; Kong, Betty Y.; Kim, Alison M.
- Biology of Reproduction, Vol. 86, Issue 4
ZnT-3, a putative transporter of zinc into synaptic vesicles
journal, December 1996
- Palmiter, R. D.; Cole, T. B.; Quaife, C. J.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 25
The cortical reaction and development of activation competence in mammalian oocytes
journal, January 1996
- Ducibella, T.
- Human Reproduction Update, Vol. 2, Issue 1
A structured interdomain linker directs self-polymerization of human uromodulin
journal, January 2016
- Bokhove, Marcel; Nishimura, Kaoru; Brunati, Martina
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 6
Quantitative mapping of zinc fluxes in the mammalian egg reveals the origin of fertilization-induced zinc sparks
journal, December 2014
- Que, Emily L.; Bleher, Reiner; Duncan, Francesca E.
- Nature Chemistry, Vol. 7, Issue 2
Polyspermy prevention: facts and artifacts?
journal, November 2010
- Dale, Brian; DeFelice, Louis
- Journal of Assisted Reproduction and Genetics, Vol. 28, Issue 3
Zinc concentrations in serum and follicular fluid during ovarian stimulation and expression of Zn2+ transporters in human oocytes and cumulus cells
journal, June 2011
- Ménézo, Yves; Pluntz, Laurène; Chouteau, Jacques
- Reproductive BioMedicine Online, Vol. 22, Issue 6
Acrosome intact and acrosome-reacted human sperm can initiate binding to the zona pellucida
journal, June 1989
- Morales, Patricio; Cross, Nicholas L.; Overstreet, James W.
- Developmental Biology, Vol. 133, Issue 2
Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during meiotic maturation
journal, November 1988
- Ducibella, Tom; Anderson, Everett; Albertini, David F.
- Developmental Biology, Vol. 130, Issue 1
Maternally-derived zinc transporters ZIP6 and ZIP10 drive the mammalian oocyte-to-egg transition
journal, August 2014
- Kong, B. Y.; Duncan, F. E.; Que, E. L.
- MHR: Basic science of reproductive medicine, Vol. 20, Issue 11
Influence of the zona pellucida of the mouse egg on folliculogenesis and fertility
journal, January 2012
- Wassarman, Paul M.; Litscher, Eveline S.
- The International Journal of Developmental Biology, Vol. 56, Issue 10-11-12
The Timing of Cortical Granule Fusion, Content Dispersal, and Endocytosis during Fertilization of the Hamster Egg: An Electrophysiological and Histochemical Study
journal, March 1994
- Kline, Douglas; Stewart-Savage, J.
- Developmental Biology, Vol. 162, Issue 1
Oocyte specific oolemmal SAS1B involved in sperm binding through intra-acrosomal SLLP1 during fertilization
journal, March 2012
- Sachdev, Monika; Mandal, Arabinda; Mulders, Sabine
- Developmental Biology, Vol. 363, Issue 1
Acute dietary zinc deficiency before conception compromises oocyte epigenetic programming and disrupts embryonic development
journal, April 2013
- Tian, X.; Diaz, F. J.
- Developmental Biology, Vol. 376, Issue 1
Identification and Cloning of a -Cell-Specific Zinc Transporter, ZnT-8, Localized Into Insulin Secretory Granules
journal, August 2004
- Chimienti, F.; Devergnas, S.; Favier, A.
- Diabetes, Vol. 53, Issue 9
Zinc Depletion Causes Multiple Defects in Ovarian Function during the Periovulatory Period in Mice
journal, February 2012
- Tian, X.; Diaz, F. J.
- Endocrinology, Vol. 153, Issue 2
GPR39 is region-specifically expressed in mouse oviduct correlating with the Zn2+ distribution
journal, January 2017
- Qiao, Jingqiao; Zhao, Huashan; Zhang, Ying
- Theriogenology, Vol. 88
A Structural View of Egg Coat Architecture and Function in Fertilization1
journal, October 2011
- Monné, Magnus; Jovine, Luca
- Biology of Reproduction, Vol. 85, Issue 4
To err (meiotically) is human: the genesis of human aneuploidy
journal, April 2001
- Hassold, Terry; Hunt, Patricia
- Nature Reviews Genetics, Vol. 2, Issue 4
Structural changes of the zona pellucida during fertilization and embryo development
journal, January 2008
- Familiari, Giuseppe
- Frontiers in Bioscience, Vol. Volume, Issue 13
Zinc depletion activates porcine metaphase II oocytes independently of the protein kinase C pathway
journal, August 2014
- Zhao, Ming-Hui; Kim, Nam-Hyung; Cui, Xiang-Shun
- In Vitro Cellular & Developmental Biology - Animal, Vol. 50, Issue 10
New perspectives of zinc coordination environments in proteins
journal, June 2012
- Maret, Wolfgang
- Journal of Inorganic Biochemistry, Vol. 111
Fetuin Inhibits Zona Pellucida Hardening and Conversion of ZP2 to ZPZ during Spontaneous Mouse Oocyte Maturation in Vitro in the Absence of Serum1
journal, November 1990
- Schroeder, Allen C.; Schultz, Richard M.; Kopf, Gregory S.
- Biology of Reproduction, Vol. 43, Issue 5
Parthenogenetic activation of mouse oocytes by strontium chloride: A search for the best conditions
journal, September 2005
- Ma, Suo-Feng; Liu, Xin-Yong; Miao, De-Qiang
- Theriogenology, Vol. 64, Issue 5
Human Follicular Fluid Levels of Calcium, Copper and Zinc
journal, January 1987
- Ng, S. C.; Karunanithy, R.; Edirisinghe, W. R.
- Gynecologic and Obstetric Investigation, Vol. 23, Issue 2
Full-term mouse development by abolishing Zn2+-dependent metaphase II arrest without Ca2+ release
journal, June 2010
- Suzuki, T.; Yoshida, N.; Suzuki, E.
- Development, Vol. 137, Issue 16
Pig oocyte activation using a Zn2+ chelator, TPEN
journal, October 2015
- Lee, Kiho; Davis, Alyssa; Zhang, Lu
- Theriogenology, Vol. 84, Issue 6
Mussel-Inspired Histidine-Based Transient Network Metal Coordination Hydrogels
journal, January 2013
- Fullenkamp, Dominic E.; He, Lihong; Barrett, Devin G.
- Macromolecules, Vol. 46, Issue 3
Time course and pattern of cortical granule breakdown in hamster eggs after sperm fusion
journal, December 1991
- Stewart-Savage, J.; Bavister, Barry D.
- Molecular Reproduction and Development, Vol. 30, Issue 4
Crystal structure of the ZP-N domain of ZP3 reveals the core fold of animal egg coats
journal, December 2008
- Monné, Magnus; Han, Ling; Schwend, Thomas
- Nature, Vol. 456, Issue 7222
Fertility and Taxon-Specific Sperm Binding Persist after Replacement of Mouse Sperm Receptors with Human Homologs
journal, July 2003
- Rankin, Tracy L.; Coleman, Jenell S.; Epifano, Olga
- Developmental Cell, Vol. 5, Issue 1
Fertilization-Associated Changes in the Murine Zona Pellucida: A Time Sequence Study
journal, December 1975
- Inoue, Masato; Wolf, Don P.
- Biology of Reproduction, Vol. 13, Issue 5
Role of zinc trafficking in male fertility: from germ to sperm
journal, April 2014
- Foresta, Carlo; Garolla, Andrea; Cosci, Ilaria
- Human Reproduction, Vol. 29, Issue 6
Human zona pellucida during in vitro fertilization: An ultrastructural study using saponin, ruthenium red, and osmium-thiocarbohydrazide
journal, May 1992
- Familiari, Giuseppe; Nottola, Stefania A.; Macchiarelli, Guido
- Molecular Reproduction and Development, Vol. 32, Issue 1
Zinc in Mammalian Sperm: A Review
journal, June 1984
- Hidiroglou, M.; Knipfel, J. E.
- Journal of Dairy Science, Vol. 67, Issue 6
Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy
journal, April 2012
- Burkart, Anna D.; Xiong, Bo; Baibakov, Boris
- The Journal of Cell Biology, Vol. 197, Issue 1
Preconception Zinc Deficiency Disrupts Postimplantation Fetal and Placental Development in Mice1
journal, April 2014
- Tian, Xi; Anthony, Kate; Neuberger, Thomas
- Biology of Reproduction, Vol. 90, Issue 4
Effect of zinc on human sperm motility and the acrosome reaction
journal, June 1992
- Riffo, M.; Leiva, S.; Astudillo, J.
- International Journal of Andrology, Vol. 15, Issue 3
Three-dimensional structure of the zona pellucida
journal, September 1997
- Green, D.
- Reviews of Reproduction, Vol. 2, Issue 3
Zinc deficiency during in vitro maturation of porcine oocytes causes meiotic block and developmental failure
journal, July 2015
- Jeon, Yubyeol; Yoon, Junchul David; Cai, Lian
- Molecular Medicine Reports, Vol. 12, Issue 4
An Overview of a Wide Range of Functions of ZnT and Zip Zinc Transporters in the Secretory Pathway
journal, June 2011
- Kambe, Taiho
- Bioscience, Biotechnology, and Biochemistry, Vol. 75, Issue 6
Identification and Characterization of Human and Mouse Ovastacin: A NOVEL METALLOPROTEINASE SIMILAR TO HATCHING ENZYMES FROM ARTHROPODS, BIRDS, AMPHIBIANS, AND FISH
journal, April 2004
- Quesada, Víctor; Sánchez, Luis M.; Álvarez, Jesús
- Journal of Biological Chemistry, Vol. 279, Issue 25
Zinc Sparks Are Triggered by Fertilization and Facilitate Cell Cycle Resumption in Mammalian Eggs
journal, April 2011
- Kim, Alison M.; Bernhardt, Miranda L.; Kong, Betty Y.
- ACS Chemical Biology, Vol. 6, Issue 7
The role of Hv1 and CatSper channels in sperm activation: Hv1 and CatSper channels in sperm activation
journal, November 2010
- Lishko, Polina V.; Kirichok, Yuriy
- The Journal of Physiology, Vol. 588, Issue 23
Gamete Recognition in Mice Depends on the Cleavage Status of an Egg's Zona Pellucida Protein
journal, July 2010
- Gahlay, G.; Gauthier, L.; Baibakov, B.
- Science, Vol. 329, Issue 5988
Supplementation of zinc on oocyte in vitro maturation improves preimplatation embryonic development in pigs
journal, October 2014
- Jeon, Yubyeol; Yoon, Junchul David; Cai, Lian
- Theriogenology, Vol. 82, Issue 6
Zinc Maintains Prophase I Arrest in Mouse Oocytes Through Regulation of the MOS-MAPK Pathway1
journal, July 2012
- Kong, Betty Y.; Bernhardt, Miranda L.; Kim, Alison M.
- Biology of Reproduction, Vol. 87, Issue 1
Metal-Mediated Molecular Self-Healing in Histidine-Rich Mussel Peptides
journal, April 2014
- Schmidt, Stephan; Reinecke, Antje; Wojcik, Felix
- Biomacromolecules, Vol. 15, Issue 5
Calcium and The Control of Mammalian Cortical Granule Exocytosis
journal, January 2001
- Abbott, Allison, L.
- Frontiers in Bioscience, Vol. 6, Issue 1
Micro-CT data of early physiological cancellous bone formation in the lumbar spine of female C57BL/6 mice
journal, May 2021
- Zenzes, Michael; Zaslansky, Paul
- Scientific Data, Vol. 8, Issue 1
Three-dimensional structure of the zona pellucida
journal, September 1997
- Green, D.
- Reviews of Reproduction, Vol. 2, Issue 3
Mammalian Fertilization
book, January 2006
- Litscher, Eveline S.; Wassarman, Paul M.
- Encyclopedic Reference of Genomics and Proteomics in Molecular Medicine
Zona Pellucida Glycoproteins
journal, June 1988
- Wassarman, Paul M.
- Annual Review of Biochemistry, Vol. 57, Issue 1
Calcium and The Control of Mammalian Cortical Granule Exocytosis
journal, January 2001
- Ducibella, Tom
- Frontiers in Bioscience, Vol. 6, Issue 3
Re: A Structured Interdomain Linker Directs Self-Polymerization of Human Uromodulin
journal, September 2016
- Atala, Anthony
- Journal of Urology, Vol. 196, Issue 3
Works referencing / citing this record:
Strategic Advances in Formation of Cell-in-Shell Structures: From Syntheses to Applications
journal, February 2018
- Kim, Beom Jin; Cho, Hyeoncheol; Park, Ji Hun
- Advanced Materials, Vol. 30, Issue 14
Perfect date—the review of current research into molecular bases of mammalian fertilization
journal, January 2020
- Trebichalská, Zuzana; Holubcová, Zuzana
- Journal of Assisted Reproduction and Genetics, Vol. 37, Issue 2
Zinc ion flux during mammalian sperm capacitation
journal, May 2018
- Kerns, Karl; Zigo, Michal; Drobnis, Erma Z.
- Nature Communications, Vol. 9, Issue 1
Sperm chemorepulsion, a supplementary mechanism to regulate fertilization
journal, June 2017
- Guidobaldi, H. A.; Cubilla, M.; Moreno, A.
- Human Reproduction, Vol. 32, Issue 8
The molecular mechanisms mediating mammalian fertilization
journal, August 2019
- Bhakta, Hanisha H.; Refai, Fares H.; Avella, Matteo A.
- Development, Vol. 146, Issue 15
Zinc in Cellular Regulation: The Nature and Significance of “Zinc Signals”
journal, October 2017
- Maret, Wolfgang
- International Journal of Molecular Sciences, Vol. 18, Issue 11
Zinc: A Necessary Ion for Mammalian Sperm Fertilization Competency
journal, December 2018
- Kerns, Karl; Zigo, Michal; Sutovsky, Peter
- International Journal of Molecular Sciences, Vol. 19, Issue 12
Disruption of O ‐GlcNAc homeostasis during mammalian oocyte meiotic maturation impacts fertilization
journal, February 2019
- Zhou, Luhan T.; Romar, Raquel; Pavone, Mary Ellen
- Molecular Reproduction and Development, Vol. 86, Issue 5
Mammalian egg coat modifications and the block to polyspermy
journal, March 2020
- Fahrenkamp, Eileen; Algarra, Blanca; Jovine, Luca
- Molecular Reproduction and Development, Vol. 87, Issue 3
Molecular basis of egg coat cross-linking sheds light on ZP1-associated female infertility
journal, March 2019
- Nishimura, Kaoru; Dioguardi, Elisa; Nishio, Shunsuke
- Nature Communications
Zinc: A Necessary Ion for Mammalian Sperm Fertilization Competency
journal, January 2018
- Kerns, Karl; Zigo, Michal; Sutovsky, Peter
- International Journal of Molecular Sciences
Molecular basis of egg coat cross-linking sheds light on ZP1-associated female infertility
journal, July 2019
- Nishimura, Kaoru; Dioguardi, Elisa; Nishio, Shunsuke
- Nature Communications, Vol. 10, Issue 1