skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Bovine eggs release zinc in response to parthenogenetic and sperm-induced egg activation

Abstract

Upon fertilization or parthenogenesis, zinc is released into the extracellular space through a series of exocytic events termed zinc sparks, which are tightly coordinated with intracellular calcium transients. The zinc spark reduces the total amount of intracellular zinc, and this reduction is necessary and sufficient to induce egg activation even in the absence of calcium transients. In addition, this zinc release contributes to the block to polyspermy through modification of the zona pellucida. The zinc spark has been documented in all organisms examined to date including the mouse, two species of nonhuman primates, and human. Here we determined whether zinc sparks occur in the bovine, an important model of gamete development in mono-ovulatory mammalian species. We obtained metaphase II-arrested (MII) bovine eggs following in vitro maturation. Total zinc, assessed in single cells using X-Ray Fluorescence Microscopy, was significantly more abundant in the bovine egg compared to iron and copper. Studies with intracellular fluorescent probes revealed that labile zinc pools are localized to discrete cytoplasmic punctae enriched at the cortex. To determine whether zinc undergoes dynamic fluxes during egg activation, we parthenogenetically activated bovine eggs using two approaches: ionomycin or bovine phospholipase C zeta (bPlcζ) Both these methods induced zinc sparksmore » coordinately with intracellular calcium transients. The zinc spark was also observed in bovine eggs following intracytoplasmic sperm injection. Furthermore, these results establish that zinc is the most abundant transition metal in the bovine egg, and zinc flux during egg activation-induced by chemical activation or sperm-is a highly conserved event across mammalian species.« less

Authors:
 [1];  [2];  [2];  [2];  [3];  [4];  [1];  [5]
  1. Northwestern Univ., Evanston, IL (United States)
  2. Northwestern Univ., Chicago, IL (United States)
  3. Argonne National Lab. (ANL), Argonne, IL (United States)
  4. Univ. of Massachusetts, Amherst, MA (United States)
  5. 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.:
Ferring International Centers S.A. (Ferring Pharmaceuticals); National Institutes of Health (NIH); USDOE Office of Science (SC)
OSTI Identifier:
1528925
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Theriogenology
Additional Journal Information:
Journal Volume: 127; Journal Issue: C; Journal ID: ISSN 0093-691X
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; bovine; calcium; egg activation; gamete; zinc

Citation Formats

Que, Emily L., Duncan, Francesca E., Lee, Hoi Chang, Hornick, Jessica E., Vogt, Stefan, Fissore, Rafael A., O'Halloran, Thomas V., and Woodruff, Teresa K.. Bovine eggs release zinc in response to parthenogenetic and sperm-induced egg activation. United States: N. p., 2018. Web. https://doi.org/10.1016/j.theriogenology.2018.12.031.
Que, Emily L., Duncan, Francesca E., Lee, Hoi Chang, Hornick, Jessica E., Vogt, Stefan, Fissore, Rafael A., O'Halloran, Thomas V., & Woodruff, Teresa K.. Bovine eggs release zinc in response to parthenogenetic and sperm-induced egg activation. United States. https://doi.org/10.1016/j.theriogenology.2018.12.031
Que, Emily L., Duncan, Francesca E., Lee, Hoi Chang, Hornick, Jessica E., Vogt, Stefan, Fissore, Rafael A., O'Halloran, Thomas V., and Woodruff, Teresa K.. Mon . "Bovine eggs release zinc in response to parthenogenetic and sperm-induced egg activation". United States. https://doi.org/10.1016/j.theriogenology.2018.12.031. https://www.osti.gov/servlets/purl/1528925.
@article{osti_1528925,
title = {Bovine eggs release zinc in response to parthenogenetic and sperm-induced egg activation},
author = {Que, Emily L. and Duncan, Francesca E. and Lee, Hoi Chang and Hornick, Jessica E. and Vogt, Stefan and Fissore, Rafael A. and O'Halloran, Thomas V. and Woodruff, Teresa K.},
abstractNote = {Upon fertilization or parthenogenesis, zinc is released into the extracellular space through a series of exocytic events termed zinc sparks, which are tightly coordinated with intracellular calcium transients. The zinc spark reduces the total amount of intracellular zinc, and this reduction is necessary and sufficient to induce egg activation even in the absence of calcium transients. In addition, this zinc release contributes to the block to polyspermy through modification of the zona pellucida. The zinc spark has been documented in all organisms examined to date including the mouse, two species of nonhuman primates, and human. Here we determined whether zinc sparks occur in the bovine, an important model of gamete development in mono-ovulatory mammalian species. We obtained metaphase II-arrested (MII) bovine eggs following in vitro maturation. Total zinc, assessed in single cells using X-Ray Fluorescence Microscopy, was significantly more abundant in the bovine egg compared to iron and copper. Studies with intracellular fluorescent probes revealed that labile zinc pools are localized to discrete cytoplasmic punctae enriched at the cortex. To determine whether zinc undergoes dynamic fluxes during egg activation, we parthenogenetically activated bovine eggs using two approaches: ionomycin or bovine phospholipase C zeta (bPlcζ) Both these methods induced zinc sparks coordinately with intracellular calcium transients. The zinc spark was also observed in bovine eggs following intracytoplasmic sperm injection. Furthermore, these results establish that zinc is the most abundant transition metal in the bovine egg, and zinc flux during egg activation-induced by chemical activation or sperm-is a highly conserved event across mammalian species.},
doi = {10.1016/j.theriogenology.2018.12.031},
journal = {Theriogenology},
number = C,
volume = 127,
place = {United States},
year = {2018},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 5 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Zinc Requirement During Meiosis I–Meiosis II Transition in Mouse Oocytes Is Independent of the MOS-MAPK Pathway1
journal, March 2011


A Zinc-Dependent Mechanism Regulates Meiotic Progression in Mammalian Oocytes1
journal, April 2012


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
  • DOI: 10.1038/srep24737

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
  • DOI: 10.1021/cb200084y

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
  • DOI: 10.1038/nchembio.419

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
  • DOI: 10.1093/molehr/gau066

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
  • DOI: 10.1002/dvdy.24285

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
  • DOI: 10.1038/nchem.2133

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
  • DOI: 10.1242/dev.049791

Preconception Zinc Deficiency Disrupts Postimplantation Fetal and Placental Development in Mice1
journal, April 2014


Zinc Depletion Causes Multiple Defects in Ovarian Function during the Periovulatory Period in Mice
journal, February 2012


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
  • DOI: 10.1038/srep22772

Zinc availability during germline development impacts embryo viability in Caenorhabditis elegans
journal, January 2017

  • Mendoza, Adelita D.; Woodruff, Teresa K.; Wignall, Sarah M.
  • Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, Vol. 191
  • DOI: 10.1016/j.cbpc.2016.09.007

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
  • DOI: 10.3892/mmr.2015.4125

Pig oocyte activation using a Zn2+ chelator, TPEN
journal, October 2015


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
  • DOI: 10.1007/s11626-014-9784-8

Large animal models for the study of ovarian follicular dynamics in women
journal, November 2012


Bovine Model for the Study of Reproductive Aging in Women: Follicular, Luteal, and Endocrine Characteristics1
journal, July 2005


Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human)
journal, March 2006

  • Griffin, Jeanine; Emery, Benjamin R.; Huang, Ivan
  • Journal of Experimental & Clinical Assisted Reproduction, Vol. 3, Issue 1
  • DOI: 10.1186/1743-1050-3-2

Bovine oocyte diameter in relation to developmental competence
journal, October 1997


Positioning to get out of meiosis: the asymmetry of division
journal, September 2010


Asymmetric division of spindle microtubules and microfilaments during bovine meiosis from metaphase I to metaphase III
journal, January 2005

  • Li, Guang-Peng; Liu, Ying; Bunch, Thomas D.
  • Molecular Reproduction and Development, Vol. 71, Issue 2
  • DOI: 10.1002/mrd.20255

Four zona pellucida glycoproteins are expressed in the human
journal, July 2004


Identification of bovine zona pellucida glycoproteins
journal, March 1997


Quantitative elemental analysis of bovine ovarian follicles using X-ray fluorescence imaging
journal, January 2015

  • Ceko, M. J.; Hummitzsch, K.; Hatzirodos, N.
  • Metallomics, Vol. 7, Issue 5
  • DOI: 10.1039/C5MT00035A

The Importance of Having Zinc During In Vitro Maturation of Cattle Cumulus-Oocyte Complex: Role of Cumulus Cells
journal, August 2014

  • Anchordoquy, Jm; Anchordoquy, Jp; Sirini, Ma
  • Reproduction in Domestic Animals, Vol. 49, Issue 5
  • DOI: 10.1111/rda.12385

Effect of increasing zinc sulphate concentration during in vitro maturation of bovine oocytes
journal, October 2010


NIH Image to ImageJ: 25 years of image analysis
journal, June 2012

  • Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2089

MAPS : A set of software tools for analysis and visualization of 3D X-ray fluorescence data sets
journal, March 2003


Patterns of Intracellular Ca2+ Concentrations in Fertilized Bovine Eggs1
journal, December 1992

  • Fissore, Rafael A.; Dobrinsky, John R.; Balise, John J.
  • Biology of Reproduction, Vol. 47, Issue 6
  • DOI: 10.1095/biolreprod47.6.960

Human sperm devoid of PLC, zeta 1 fail to induce Ca2+ release and are unable to initiate the first step of embryo development
journal, November 2008

  • Yoon, Sook-Young; Jellerette, Teru; Salicioni, Ana Maria
  • Journal of Clinical Investigation, Vol. 118, Issue 11
  • DOI: 10.1172/JCI36942

Capacitation of Bovine Sperm by Heparin1
journal, June 1988


Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]i responses and oocyte activation
journal, January 2006

  • Malcuit, Christopher; Maserati, Marc; Takahashi, Yoshiyuki
  • Reproduction, Fertility and Development, Vol. 18, Issue 2
  • DOI: 10.1071/RD05131

An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro
journal, July 1989

  • Chatot, C. L.; Ziomek, C. A.; Bavister, B. D.
  • Reproduction, Vol. 86, Issue 2
  • DOI: 10.1530/jrf.0.0860679

Analysis of Mouse Oocyte Activation Suggests the Involvement of Sperm Perinuclear Material1
journal, June 1998


Defective sperm head decondensation undermines the success of ICSI in the bovine
journal, September 2017

  • Águila, Luis; Felmer, Ricardo; Arias, María Elena
  • Reproduction, Vol. 154, Issue 3
  • DOI: 10.1530/REP-17-0270

Development of Parthenogenetic and Cloned Ovine Embryos: Effect of Activation Protocols1
journal, May 1998


From egg to embryo: a peripatetic journey
journal, December 2005


PLCζ and its role as a trigger of development in vertebrates: ROLES OF PLCζ IN VERTEBRATES
journal, August 2011

  • Ito, Junya; Parrington, John; Fissore, Rafael A.
  • Molecular Reproduction and Development, Vol. 78, Issue 10-11
  • DOI: 10.1002/mrd.21359

Parthenogenetic activation of bovine oocytes using bovine and murine phospholipase C zeta
journal, January 2008

  • Ross, Pablo J.; Beyhan, Zeki; Iager, Amy E.
  • BMC Developmental Biology, Vol. 8, Issue 1
  • DOI: 10.1186/1471-213X-8-16

Activation of bovine somatic cell nuclear transfer embryos by PLCZ cRNA injection
journal, March 2009

  • Ross, Pablo J.; Rodriguez, Ramon M.; Iager, Amy E.
  • REPRODUCTION, Vol. 137, Issue 3
  • DOI: 10.1530/REP-08-0419

Recombinant human phospholipase C zeta 1 induces intracellular calcium oscillations and oocyte activation in mouse and human oocytes
journal, March 2012


Role of calcium signals in early development
journal, April 2006


Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term
journal, December 2006


Egg activation events are regulated by the duration of a sustained [Ca2+]cyt signal in the mouse
journal, June 2005


Mechanisms underlying oocyte activation and postovulatory ageing
journal, December 2002


Intracellular Calcium Oscillations Signal Apoptosis Rather than Activation in In Vitro Aged Mouse Eggs1
journal, June 2002


Distinctions in Meiotic Spindle Structure and Assembly During In Vitro and In Vivo Maturation of Mouse Oocytes1
journal, December 2003


Meiotic spindle morphogenesis in in vivo and in vitro matured mouse oocytes: insights into the relationship between nuclear and cytoplasmic quality
journal, December 2004

  • Sanfins, Alexandra; Plancha, Carlos E.; Overstrom, Eric W.
  • Human Reproduction, Vol. 19, Issue 12
  • DOI: 10.1093/humrep/deh528

Cortical granules behave differently in mouse oocytes matured under different conditions
journal, September 2005

  • Liu, Xin-Yong; Mal, Suo-Feng; Miao, De-Qiang
  • Human Reproduction, Vol. 20, Issue 12
  • DOI: 10.1093/humrep/dei265

TRPV3 channels mediate Ca2+ influx induced by 2-APB in mouse eggs
journal, January 2016


PLCζ(zeta): A sperm protein that triggers Ca2+ oscillations and egg activation in mammals
journal, April 2006


An Obscure Rider Obstructing Science: The Conflation of Parthenotes with Embryos in the Dickey–Wicker Amendment
journal, March 2011

  • Rodriguez, Sarah; Campo-Engelstein, Lisa; Tingen, Candace
  • The American Journal of Bioethics, Vol. 11, Issue 3
  • DOI: 10.1080/15265161.2010.546472

Politics and Parthenotes
journal, October 2010


Practical Parthenote Policy and the Practice of Science
journal, March 2011

  • Campo-Engelstein, Lisa; Rodriguez, Sarah; Tingen, Candace
  • The American Journal of Bioethics, Vol. 11, Issue 3
  • DOI: 10.1080/15265161.2011.563162

Fate of fertilized human oocytes
journal, December 2010

  • Benagiano, Giuseppe; Farris, Manuela; Grudzinskas, Gedis
  • Reproductive BioMedicine Online, Vol. 21, Issue 6
  • DOI: 10.1016/j.rbmo.2010.08.011

A Review of Outcome Data concerning Children Born following Assisted Reproductive Technologies
journal, June 2012

  • Dupont, Charlotte; Sifer, Christophe
  • ISRN Obstetrics and Gynecology, Vol. 2012
  • DOI: 10.5402/2012/405382

Genomic Imprinting and Assisted Reproductive Technology: Connections and Potential Risks
journal, August 2005

  • Thompson, Jennifer R.; Williams, Carmen J.
  • Seminars in Reproductive Medicine, Vol. 23, Issue 03
  • DOI: 10.1055/s-2005-872457

Preserving fertility during cancer treatment
journal, October 2009


From the bench to bedside to babies: translational medicine made possible by funding multidisciplinary team science
journal, August 2013


    Works referencing / citing this record:

    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
    • DOI: 10.1007/s10815-019-01679-4

    A biophotonic approach to measure pH in small volumes in vitro: Quantifiable differences in metabolic flux around the cumulus‐oocyte‐complex (COC)
    journal, December 2019

    • McLennan, Hanna J.; Saini, Avishkar; Sylvia, Georgina M.
    • Journal of Biophotonics, Vol. 13, Issue 3
    • DOI: 10.1002/jbio.201960038