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

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

*Corresponding author for this work

Research output: Contribution to journalArticle

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 sparks coordinately with intracellular calcium transients. The zinc spark was also observed in bovine eggs following intracytoplasmic sperm injection. 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.

Original languageEnglish (US)
Pages (from-to)41-48
Number of pages8
JournalTheriogenology
Volume127
DOIs
StatePublished - Mar 15 2019

Fingerprint

Eggs
Ovum
Spermatozoa
Zinc
zinc
spermatozoa
cattle
Calcium
calcium
transition elements
Parthenogenesis
polyspermy
intracytoplasmic sperm injection
Zona Pellucida
Ionomycin
Intracytoplasmic Sperm Injections
zona pellucida
phospholipase C
parthenogenesis
extracellular space

Keywords

  • Bovine
  • Calcium
  • Egg activation
  • Gamete
  • Zinc

ASJC Scopus subject areas

  • Small Animals
  • Food Animals
  • Animal Science and Zoology
  • Equine

Cite this

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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 sparks coordinately with intracellular calcium transients. The zinc spark was also observed in bovine eggs following intracytoplasmic sperm injection. 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.",
keywords = "Bovine, Calcium, Egg activation, Gamete, Zinc",
author = "Que, {Emily L.} and Duncan, {Francesca Elizabeth} and Lee, {Hoi Chang} and Hornick, {Jessica Elizabeth} and Stefan Vogt and Fissore, {Rafael A.} and O'Halloran, {Thomas V} and Woodruff, {Teresa K}",
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Bovine eggs release zinc in response to parthenogenetic and sperm-induced egg activation. / Que, Emily L.; Duncan, Francesca Elizabeth; Lee, Hoi Chang; Hornick, Jessica Elizabeth; Vogt, Stefan; Fissore, Rafael A.; O'Halloran, Thomas V; Woodruff, Teresa K.

In: Theriogenology, Vol. 127, 15.03.2019, p. 41-48.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Bovine eggs release zinc in response to parthenogenetic and sperm-induced egg activation

AU - Que, Emily L.

AU - Duncan, Francesca Elizabeth

AU - Lee, Hoi Chang

AU - Hornick, Jessica Elizabeth

AU - Vogt, Stefan

AU - Fissore, Rafael A.

AU - O'Halloran, Thomas V

AU - Woodruff, Teresa K

PY - 2019/3/15

Y1 - 2019/3/15

N2 - 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. 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.

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