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

Que, Emily L.; Duncan, Francesca E.; Lee, Hoi Chang; Hornick, Jessica E.; Vogt, Stefan; Fissore, Rafael A.; O'Halloran, Thomas V.; Woodruff, Teresa K.

doi:10.1016/j.theriogenology.2018.12.031

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

Journal Article · Mon Dec 24 00:00:00 EST 2018 · Theriogenology

DOI:https://doi.org/10.1016/j.theriogenology.2018.12.031· OSTI ID:1528925

Que, Emily L. ^[1]; Duncan, Francesca E. ^[2]; Lee, Hoi Chang ^[2]; Hornick, Jessica E. ^[2]; Vogt, Stefan ^[3]; Fissore, Rafael A. ^[4]; O'Halloran, Thomas V. ^[1]; Woodruff, Teresa K. ^[5]

Northwestern Univ., Evanston, IL (United States)
Northwestern Univ., Chicago, IL (United States)
Argonne National Lab. (ANL), Argonne, IL (United States)
Univ. of Massachusetts, Amherst, MA (United States)
Northwestern Univ., Evanston, IL (United States); Northwestern Univ., Chicago, IL (United States)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Organization:: Ferring International Centers S.A. (Ferring Pharmaceuticals); National Institutes of Health (NIH); USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1528925

Journal Information:: Theriogenology, Vol. 127, Issue C; ISSN 0093-691X

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 24 works

Citation information provided by
Web of Science

References (62)

Zinc Requirement During Meiosis I–Meiosis II Transition in Mouse Oocytes Is Independent of the MOS-MAPK Pathway1 Bernhardt, Miranda L.; Kim, Alison M.; O'Halloran, Thomas V. Biology of Reproduction, Vol. 84, Issue 3 https://doi.org/10.1095/biolreprod.110.086488	journal	March 2011
A Zinc-Dependent Mechanism Regulates Meiotic Progression in Mammalian Oocytes1 Bernhardt, Miranda L.; Kong, Betty Y.; Kim, Alison M. Biology of Reproduction, Vol. 86, Issue 4 https://doi.org/10.1095/biolreprod.111.097253	journal	April 2012
The zinc spark is an inorganic signature of human egg activation Duncan, Francesca E.; Que, Emily L.; Zhang, Nan Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep24737	journal	April 2016
Zinc Sparks Are Triggered by Fertilization and Facilitate Cell Cycle Resumption in Mammalian Eggs Kim, Alison M.; Bernhardt, Miranda L.; Kong, Betty Y. ACS Chemical Biology, Vol. 6, Issue 7 https://doi.org/10.1021/cb200084y	journal	April 2011
Zinc availability regulates exit from meiosis in maturing mammalian oocytes Kim, Alison M.; Vogt, Stefan; O'Halloran, Thomas V. Nature Chemical Biology, Vol. 6, Issue 9 https://doi.org/10.1038/nchembio.419	journal	August 2010
Maternally-derived zinc transporters ZIP6 and ZIP10 drive the mammalian oocyte-to-egg transition Kong, B. Y.; Duncan, F. E.; Que, E. L. MHR: Basic science of reproductive medicine, Vol. 20, Issue 11 https://doi.org/10.1093/molehr/gau066	journal	August 2014
The inorganic anatomy of the mammalian preimplantation embryo and the requirement of zinc during the first mitotic divisions: Zinc Requirement in Embryo Development Kong, Betty Y.; Duncan, Francesca E.; Que, Emily L. Developmental Dynamics, Vol. 244, Issue 8 https://doi.org/10.1002/dvdy.24285	journal	July 2015
Quantitative mapping of zinc fluxes in the mammalian egg reveals the origin of fertilization-induced zinc sparks Que, Emily L.; Bleher, Reiner; Duncan, Francesca E. Nature Chemistry, Vol. 7, Issue 2 https://doi.org/10.1038/nchem.2133	journal	December 2014
Full-term mouse development by abolishing Zn2+-dependent metaphase II arrest without Ca2+ release Suzuki, T.; Yoshida, N.; Suzuki, E. Development, Vol. 137, Issue 16 https://doi.org/10.1242/dev.049791	journal	June 2010
Preconception Zinc Deficiency Disrupts Postimplantation Fetal and Placental Development in Mice1 Tian, Xi; Anthony, Kate; Neuberger, Thomas Biology of Reproduction, Vol. 90, Issue 4 https://doi.org/10.1095/biolreprod.113.113910	journal	April 2014
Zinc Depletion Causes Multiple Defects in Ovarian Function during the Periovulatory Period in Mice Tian, X.; Diaz, F. J. Endocrinology, Vol. 153, Issue 2 https://doi.org/10.1210/en.2011-1599	journal	February 2012
Acute dietary zinc deficiency before conception compromises oocyte epigenetic programming and disrupts embryonic development Tian, X.; Diaz, F. J. Developmental Biology, Vol. 376, Issue 1 https://doi.org/10.1016/j.ydbio.2013.01.015	journal	April 2013
The fertilization-induced zinc spark is a novel biomarker of mouse embryo quality and early development Zhang, Nan; Duncan, Francesca E.; Que, Emily L. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep22772	journal	March 2016
Zinc availability during germline development impacts embryo viability in Caenorhabditis elegans Mendoza, Adelita D.; Woodruff, Teresa K.; Wignall, Sarah M. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, Vol. 191 https://doi.org/10.1016/j.cbpc.2016.09.007	journal	January 2017
Zinc deficiency during in vitro maturation of porcine oocytes causes meiotic block and developmental failure Jeon, Yubyeol; Yoon, Junchul David; Cai, Lian Molecular Medicine Reports, Vol. 12, Issue 4 https://doi.org/10.3892/mmr.2015.4125	journal	July 2015
Pig oocyte activation using a Zn2+ chelator, TPEN Lee, Kiho; Davis, Alyssa; Zhang, Lu Theriogenology, Vol. 84, Issue 6 https://doi.org/10.1016/j.theriogenology.2015.05.036	journal	October 2015
Zinc depletion activates porcine metaphase II oocytes independently of the protein kinase C pathway Zhao, Ming-Hui; Kim, Nam-Hyung; Cui, Xiang-Shun In Vitro Cellular & Developmental Biology - Animal, Vol. 50, Issue 10 https://doi.org/10.1007/s11626-014-9784-8	journal	August 2014
Large animal models for the study of ovarian follicular dynamics in women Adams, G. P.; Singh, J.; Baerwald, A. R. Theriogenology, Vol. 78, Issue 8 https://doi.org/10.1016/j.theriogenology.2012.04.010	journal	November 2012
Bovine Model for the Study of Reproductive Aging in Women: Follicular, Luteal, and Endocrine Characteristics1 Malhi, Pritpal S.; Adams, Gregg P.; Singh, Jaswant Biology of Reproduction, Vol. 73, Issue 1 https://doi.org/10.1095/biolreprod.104.038745	journal	July 2005
Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human) Griffin, Jeanine; Emery, Benjamin R.; Huang, Ivan Journal of Experimental & Clinical Assisted Reproduction, Vol. 3, Issue 1 https://doi.org/10.1186/1743-1050-3-2	journal	March 2006
Bovine oocyte diameter in relation to developmental competence Otoi, T.; Yamamoto, K.; Koyama, N. Theriogenology, Vol. 48, Issue 5 https://doi.org/10.1016/S0093-691X(97)00300-2	journal	October 1997
Positioning to get out of meiosis: the asymmetry of division Brunet, S.; Verlhac, M. H. Human Reproduction Update, Vol. 17, Issue 1 https://doi.org/10.1093/humupd/dmq044	journal	September 2010
Asymmetric division of spindle microtubules and microfilaments during bovine meiosis from metaphase I to metaphase III Li, Guang-Peng; Liu, Ying; Bunch, Thomas D. Molecular Reproduction and Development, Vol. 71, Issue 2 https://doi.org/10.1002/mrd.20255	journal	January 2005
Four zona pellucida glycoproteins are expressed in the human Lefievre, L. Human Reproduction, Vol. 19, Issue 7 https://doi.org/10.1093/humrep/deh301	journal	July 2004
Identification of bovine zona pellucida glycoproteins Topper, E. K.; Kruijt, L.; Calvete, J. Molecular Reproduction and Development, Vol. 46, Issue 3 https://doi.org/10.1002/(SICI)1098-2795(199703)46:3<344::AID-MRD13>3.0.CO;2-Z	journal	March 1997
Quantitative elemental analysis of bovine ovarian follicles using X-ray fluorescence imaging Ceko, M. J.; Hummitzsch, K.; Hatzirodos, N. Metallomics, Vol. 7, Issue 5 https://doi.org/10.1039/C5MT00035A	journal	January 2015
The Importance of Having Zinc During In Vitro Maturation of Cattle Cumulus-Oocyte Complex: Role of Cumulus Cells Anchordoquy, Jm; Anchordoquy, Jp; Sirini, Ma Reproduction in Domestic Animals, Vol. 49, Issue 5 https://doi.org/10.1111/rda.12385	journal	August 2014
Effect of increasing zinc sulphate concentration during in vitro maturation of bovine oocytes Picco, S. J.; Anchordoquy, J. M.; de Matos, D. G. Theriogenology, Vol. 74, Issue 7 https://doi.org/10.1016/j.theriogenology.2010.05.015	journal	October 2010
NIH Image to ImageJ: 25 years of image analysis Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W. Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2089	journal	June 2012
MAPS : A set of software tools for analysis and visualization of 3D X-ray fluorescence data sets Vogt, S. Journal de Physique IV (Proceedings), Vol. 104 https://doi.org/10.1051/jp4:20030160	journal	March 2003
Patterns of Intracellular Ca2+ Concentrations in Fertilized Bovine Eggs1 Fissore, Rafael A.; Dobrinsky, John R.; Balise, John J. Biology of Reproduction, Vol. 47, Issue 6 https://doi.org/10.1095/biolreprod47.6.960	journal	December 1992
Human sperm devoid of PLC, zeta 1 fail to induce Ca2+ release and are unable to initiate the first step of embryo development Yoon, Sook-Young; Jellerette, Teru; Salicioni, Ana Maria Journal of Clinical Investigation, Vol. 118, Issue 11 https://doi.org/10.1172/JCI36942	journal	November 2008
Capacitation of Bovine Sperm by Heparin1 Parrish, J. J.; Susko-Parrish, J.; Winer, M. A. Biology of Reproduction, Vol. 38, Issue 5 https://doi.org/10.1095/biolreprod38.5.1171	journal	June 1988
ICSI-generated mouse zygotes exhibit altered calcium oscillations, inositol 1,4,5-trisphosphate receptor-1 down-regulation, and embryo development Kurokawa, M. Molecular Human Reproduction, Vol. 9, Issue 9 https://doi.org/10.1093/molehr/gag072	journal	September 2003
Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]i responses and oocyte activation Malcuit, Christopher; Maserati, Marc; Takahashi, Yoshiyuki Reproduction, Fertility and Development, Vol. 18, Issue 2 https://doi.org/10.1071/RD05131	journal	January 2006
An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro Chatot, C. L.; Ziomek, C. A.; Bavister, B. D. Reproduction, Vol. 86, Issue 2 https://doi.org/10.1530/jrf.0.0860679	journal	July 1989
Analysis of Mouse Oocyte Activation Suggests the Involvement of Sperm Perinuclear Material1 Kimura, Y.; Yanagimachi, R.; Kuretake, S. Biology of Reproduction, Vol. 58, Issue 6 https://doi.org/10.1095/biolreprod58.6.1407	journal	June 1998
Defective sperm head decondensation undermines the success of ICSI in the bovine Águila, Luis; Felmer, Ricardo; Arias, María Elena Reproduction, Vol. 154, Issue 3 https://doi.org/10.1530/REP-17-0270	journal	September 2017
Development of Parthenogenetic and Cloned Ovine Embryos: Effect of Activation Protocols1 Loi, P.; Ledda, S.; Fulka, J. Biology of Reproduction, Vol. 58, Issue 5 https://doi.org/10.1095/biolreprod58.5.1177	journal	May 1998
From egg to embryo: a peripatetic journey Schultz, Richard M. Reproduction, Vol. 130, Issue 6 https://doi.org/10.1530/rep.1.00902	journal	December 2005
PLCζ and its role as a trigger of development in vertebrates: ROLES OF PLCζ IN VERTEBRATES Ito, Junya; Parrington, John; Fissore, Rafael A. Molecular Reproduction and Development, Vol. 78, Issue 10-11 https://doi.org/10.1002/mrd.21359	journal	August 2011
Parthenogenetic activation of bovine oocytes using bovine and murine phospholipase C zeta Ross, Pablo J.; Beyhan, Zeki; Iager, Amy E. BMC Developmental Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-213X-8-16	journal	January 2008
Activation of bovine somatic cell nuclear transfer embryos by PLCZ cRNA injection Ross, Pablo J.; Rodriguez, Ramon M.; Iager, Amy E. REPRODUCTION, Vol. 137, Issue 3 https://doi.org/10.1530/REP-08-0419	journal	March 2009
Recombinant human phospholipase C zeta 1 induces intracellular calcium oscillations and oocyte activation in mouse and human oocytes Yoon, S. -Y.; Eum, J. H.; Lee, J. E. Human Reproduction, Vol. 27, Issue 6 https://doi.org/10.1093/humrep/des092	journal	March 2012
Role of calcium signals in early development Ducibella, T.; Schultz, R.; Ozil, J. Seminars in Cell & Developmental Biology, Vol. 17, Issue 2 https://doi.org/10.1016/j.semcdb.2006.02.010	journal	April 2006
Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term Ozil, Jean-Pierre; Banrezes, Bernadette; Tóth, Szabolcs Developmental Biology, Vol. 300, Issue 2 https://doi.org/10.1016/j.ydbio.2006.08.041	journal	December 2006
Egg activation events are regulated by the duration of a sustained [Ca2+]cyt signal in the mouse Ozil, Jean-Pierre; Markoulaki, Styliani; Toth, Szabolcs Developmental Biology, Vol. 282, Issue 1 https://doi.org/10.1016/j.ydbio.2005.02.035	journal	June 2005
Mechanisms underlying oocyte activation and postovulatory ageing Fissore, Ra; Kurokawa, M.; Knott, J. Reproduction https://doi.org/10.1530/rep.0.1240745	journal	December 2002
Intracellular Calcium Oscillations Signal Apoptosis Rather than Activation in In Vitro Aged Mouse Eggs1 Gordo, Ana Carla; Rodrigues, Patricia; Kurokawa, Manabu Biology of Reproduction, Vol. 66, Issue 6 https://doi.org/10.1095/biolreprod66.6.1828	journal	June 2002
Distinctions in Meiotic Spindle Structure and Assembly During In Vitro and In Vivo Maturation of Mouse Oocytes1 Sanfins, Alexandra; Lee, Gloria Y.; Plancha, Carlos E. Biology of Reproduction, Vol. 69, Issue 6 https://doi.org/10.1095/biolreprod.103.020537	journal	December 2003
Meiotic spindle morphogenesis in in vivo and in vitro matured mouse oocytes: insights into the relationship between nuclear and cytoplasmic quality Sanfins, Alexandra; Plancha, Carlos E.; Overstrom, Eric W. Human Reproduction, Vol. 19, Issue 12 https://doi.org/10.1093/humrep/deh528	journal	December 2004
Cortical granules behave differently in mouse oocytes matured under different conditions Liu, Xin-Yong; Mal, Suo-Feng; Miao, De-Qiang Human Reproduction, Vol. 20, Issue 12 https://doi.org/10.1093/humrep/dei265	journal	September 2005
TRPV3 channels mediate Ca2+ influx induced by 2-APB in mouse eggs Lee, Hoi Chang; Yoon, Sook-Young; Lykke-Hartmann, Karin Cell Calcium, Vol. 59, Issue 1 https://doi.org/10.1016/j.ceca.2015.12.001	journal	January 2016
PLCζ(zeta): A sperm protein that triggers Ca2+ oscillations and egg activation in mammals Swann, K.; Saunders, C.; Rogers, N. Seminars in Cell & Developmental Biology, Vol. 17, Issue 2 https://doi.org/10.1016/j.semcdb.2006.03.009	journal	April 2006
An Obscure Rider Obstructing Science: The Conflation of Parthenotes with Embryos in the Dickey–Wicker Amendment Rodriguez, Sarah; Campo-Engelstein, Lisa; Tingen, Candace The American Journal of Bioethics, Vol. 11, Issue 3 https://doi.org/10.1080/15265161.2010.546472	journal	March 2011
Politics and Parthenotes Tingen, C.; Rodriguez, S.; Campo-Engelstein, L. Science, Vol. 330, Issue 6003 https://doi.org/10.1126/science.1196881	journal	October 2010
Practical Parthenote Policy and the Practice of Science Campo-Engelstein, Lisa; Rodriguez, Sarah; Tingen, Candace The American Journal of Bioethics, Vol. 11, Issue 3 https://doi.org/10.1080/15265161.2011.563162	journal	March 2011
Fate of fertilized human oocytes Benagiano, Giuseppe; Farris, Manuela; Grudzinskas, Gedis Reproductive BioMedicine Online, Vol. 21, Issue 6 https://doi.org/10.1016/j.rbmo.2010.08.011	journal	December 2010
A Review of Outcome Data concerning Children Born following Assisted Reproductive Technologies Dupont, Charlotte; Sifer, Christophe ISRN Obstetrics and Gynecology, Vol. 2012 https://doi.org/10.5402/2012/405382	journal	June 2012
Genomic Imprinting and Assisted Reproductive Technology: Connections and Potential Risks Thompson, Jennifer R.; Williams, Carmen J. Seminars in Reproductive Medicine, Vol. 23, Issue 03 https://doi.org/10.1055/s-2005-872457	journal	August 2005
Preserving fertility during cancer treatment Woodruff, Teresa K. Nature Medicine, Vol. 15, Issue 10 https://doi.org/10.1038/nm1009-1124	journal	October 2009
From the bench to bedside to babies: translational medicine made possible by funding multidisciplinary team science Woodruff, Teresa K. Journal of Assisted Reproduction and Genetics, Vol. 30, Issue 10 https://doi.org/10.1007/s10815-013-0082-2	journal	August 2013

Cited By (2)

Perfect date—the review of current research into molecular bases of mammalian fertilization Trebichalská, Zuzana; Holubcová, Zuzana Journal of Assisted Reproduction and Genetics, Vol. 37, Issue 2 https://doi.org/10.1007/s10815-019-01679-4	journal	January 2020
A biophotonic approach to measure pH in small volumes in vitro: Quantifiable differences in metabolic flux around the cumulus‐oocyte‐complex (COC) McLennan, Hanna J.; Saini, Avishkar; Sylvia, Georgina M. Journal of Biophotonics, Vol. 13, Issue 3 https://doi.org/10.1002/jbio.201960038	journal	December 2019

Similar Records

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

Journal Article · Thu Jan 19 00:00:00 EST 2017 · Integrative Biology · OSTI ID:1528925

Que, Emily L.; Duncan, Francesca E.; Bayer, Amanda R.; +7 more

Autoradiographic visualization of the mouse egg's sperm receptor bound to sperm

Journal Article · Tue Apr 01 00:00:00 EST 1986 · J. Cell Biol.; (United States) · OSTI ID:1528925

Bleil, J D; Wassarman, P M

PTK2b function during fertilization of the mouse oocyte

Journal Article · Fri Aug 01 00:00:00 EDT 2014 · Biochemical and Biophysical Research Communications · OSTI ID:1528925

Luo, Jinping; McGinnis, Lynda K.; Carlton, Carol; +1 more

Related Subjects

60 APPLIED LIFE SCIENCES
59 BASIC BIOLOGICAL SCIENCES
bovine
calcium
egg activation
gamete
zinc

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

Citation Formats

References (62)

Cited By (2)

Similar Records

Related Subjects