Full-term mouse development by abolishing Zn2+-dependent metaphase II arrest without Ca2+ release

T Suzuki, N Yoshida, E Suzuki, E Okuda, Anthony C F Perry

Research output: Contribution to journalArticle

46 Citations (Scopus)

Abstract

In vertebrates, a rise in intracellular free Ca2+ (Ca-i(2+)) levels during fertilization initiates second metaphase (mII) exit and the developmental programme. The Ca2+ rise has long been considered to be crucial for development, but verifying this contribution would benefit from defining its role during fertilization. Here, we delineate the role of Ca2+ release during mII exit in wild-type mouse eggs and show that it is dispensable for full-term development. Exit from mII can be induced by Zn2+-specific sequestration without Ca2+ release, eliciting Cyclin B degradation in a manner dependent upon the proteasome pathway and intact microtubules, but not accompanied by degradation of the meiotic regulator Emi2. Parthenogenotes generated by Zn2+ sequestration developed in vitro with normal expression of Ca2+-sensitive genes. Meiotic exit induced by either Ca2+ oscillations or a single Ca2+ rise in oocytes containing a signaling-deficient sperm resulted in comparable developmental rates. In the absence of Ca2+ release, full-term development occurred similar to 50% less efficiently, but at readily detectable rates, with the birth of 27 offspring. These results show in intact mouse oocytes that Zn2+ is essential for mII arrest and suggest that triggering meiotic exit is the sole indispensable developmental role of Ca2+ signaling in mammalian fertilization.
LanguageEnglish
Pages2659-2669
Number of pages11
JournalDevelopment
Volume137
Issue number16
Early online date29 Jun 2010
DOIs
StatusPublished - 15 Aug 2010

Fingerprint

Metaphase
Fertilization
Oocytes
Cyclin B
Birth Rate
Proteasome Endopeptidase Complex
Microtubules
Eggs
Vertebrates
Spermatozoa
Genes

Keywords

  • mouse
  • metaphase II exit
  • Zn2+
  • Ca2+

Cite this

Full-term mouse development by abolishing Zn2+-dependent metaphase II arrest without Ca2+ release. / Suzuki, T; Yoshida, N; Suzuki, E; Okuda, E; Perry, Anthony C F.

In: Development, Vol. 137, No. 16, 15.08.2010, p. 2659-2669.

Research output: Contribution to journalArticle

Suzuki, T ; Yoshida, N ; Suzuki, E ; Okuda, E ; Perry, Anthony C F. / Full-term mouse development by abolishing Zn2+-dependent metaphase II arrest without Ca2+ release. In: Development. 2010 ; Vol. 137, No. 16. pp. 2659-2669.
@article{0b098b9120014cbeb3fd66ab6b24a87d,
title = "Full-term mouse development by abolishing Zn2+-dependent metaphase II arrest without Ca2+ release",
abstract = "In vertebrates, a rise in intracellular free Ca2+ (Ca-i(2+)) levels during fertilization initiates second metaphase (mII) exit and the developmental programme. The Ca2+ rise has long been considered to be crucial for development, but verifying this contribution would benefit from defining its role during fertilization. Here, we delineate the role of Ca2+ release during mII exit in wild-type mouse eggs and show that it is dispensable for full-term development. Exit from mII can be induced by Zn2+-specific sequestration without Ca2+ release, eliciting Cyclin B degradation in a manner dependent upon the proteasome pathway and intact microtubules, but not accompanied by degradation of the meiotic regulator Emi2. Parthenogenotes generated by Zn2+ sequestration developed in vitro with normal expression of Ca2+-sensitive genes. Meiotic exit induced by either Ca2+ oscillations or a single Ca2+ rise in oocytes containing a signaling-deficient sperm resulted in comparable developmental rates. In the absence of Ca2+ release, full-term development occurred similar to 50{\%} less efficiently, but at readily detectable rates, with the birth of 27 offspring. These results show in intact mouse oocytes that Zn2+ is essential for mII arrest and suggest that triggering meiotic exit is the sole indispensable developmental role of Ca2+ signaling in mammalian fertilization.",
keywords = "mouse, metaphase II exit, Zn2+, Ca2+",
author = "T Suzuki and N Yoshida and E Suzuki and E Okuda and Perry, {Anthony C F}",
year = "2010",
month = "8",
day = "15",
doi = "10.1242/dev.049791",
language = "English",
volume = "137",
pages = "2659--2669",
journal = "Development",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "16",

}

TY - JOUR

T1 - Full-term mouse development by abolishing Zn2+-dependent metaphase II arrest without Ca2+ release

AU - Suzuki, T

AU - Yoshida, N

AU - Suzuki, E

AU - Okuda, E

AU - Perry, Anthony C F

PY - 2010/8/15

Y1 - 2010/8/15

N2 - In vertebrates, a rise in intracellular free Ca2+ (Ca-i(2+)) levels during fertilization initiates second metaphase (mII) exit and the developmental programme. The Ca2+ rise has long been considered to be crucial for development, but verifying this contribution would benefit from defining its role during fertilization. Here, we delineate the role of Ca2+ release during mII exit in wild-type mouse eggs and show that it is dispensable for full-term development. Exit from mII can be induced by Zn2+-specific sequestration without Ca2+ release, eliciting Cyclin B degradation in a manner dependent upon the proteasome pathway and intact microtubules, but not accompanied by degradation of the meiotic regulator Emi2. Parthenogenotes generated by Zn2+ sequestration developed in vitro with normal expression of Ca2+-sensitive genes. Meiotic exit induced by either Ca2+ oscillations or a single Ca2+ rise in oocytes containing a signaling-deficient sperm resulted in comparable developmental rates. In the absence of Ca2+ release, full-term development occurred similar to 50% less efficiently, but at readily detectable rates, with the birth of 27 offspring. These results show in intact mouse oocytes that Zn2+ is essential for mII arrest and suggest that triggering meiotic exit is the sole indispensable developmental role of Ca2+ signaling in mammalian fertilization.

AB - In vertebrates, a rise in intracellular free Ca2+ (Ca-i(2+)) levels during fertilization initiates second metaphase (mII) exit and the developmental programme. The Ca2+ rise has long been considered to be crucial for development, but verifying this contribution would benefit from defining its role during fertilization. Here, we delineate the role of Ca2+ release during mII exit in wild-type mouse eggs and show that it is dispensable for full-term development. Exit from mII can be induced by Zn2+-specific sequestration without Ca2+ release, eliciting Cyclin B degradation in a manner dependent upon the proteasome pathway and intact microtubules, but not accompanied by degradation of the meiotic regulator Emi2. Parthenogenotes generated by Zn2+ sequestration developed in vitro with normal expression of Ca2+-sensitive genes. Meiotic exit induced by either Ca2+ oscillations or a single Ca2+ rise in oocytes containing a signaling-deficient sperm resulted in comparable developmental rates. In the absence of Ca2+ release, full-term development occurred similar to 50% less efficiently, but at readily detectable rates, with the birth of 27 offspring. These results show in intact mouse oocytes that Zn2+ is essential for mII arrest and suggest that triggering meiotic exit is the sole indispensable developmental role of Ca2+ signaling in mammalian fertilization.

KW - mouse

KW - metaphase II exit

KW - Zn2+

KW - Ca2+

UR - http://www.scopus.com/inward/record.url?scp=77955743213&partnerID=8YFLogxK

UR - http://dx.doi.org/10.1242/dev.049791

U2 - 10.1242/dev.049791

DO - 10.1242/dev.049791

M3 - Article

VL - 137

SP - 2659

EP - 2669

JO - Development

T2 - Development

JF - Development

SN - 0950-1991

IS - 16

ER -