Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis

H. Kaneda, J. I. Hayashi, S. Takahama, C. Taya, K. F. Lindahl, H. Yonekawa

Research output: Contribution to journalArticle

352 Citations (Scopus)

Abstract

To examine whether mtDNA is uni- or biparentally transmitted in mice, we developed an assay that can detect sperm mtDNA in a single mouse embryo. In intraspecific hybrids of Mus musculus, paternal mtDNA was detected only through the early pronucleus stage, and its disappearance coincided with loss of membrane potential in sperm-derived mitochondria. By contrast, in interspecific hybrids between M. musculus and Mus spretus, paternal mtDNA was detected throughout development from pronucleus stage to neonates. We propose that oocyte cytoplasm has a species-specific mechanism that recognizes and eliminates sperm mitochondria and mtDNA. This mechanism must recognize nuclearly encoded proteins in the sperm midpiece, and not the mtDNA or the proteins it encodes, because sperm mitochondria from the congenic strain B6.mt(spr), which carries M. spretus mtDNA on background of M. musculus (B6) nuclear genes, were eliminated early by B6 oocytes as in intraspecific crosses. We conclude that cytoplasmic genomes are transmitted uniparentally in intraspecific crosses in mammals as in Chlamydomonas and that leakage of parental mtDNA is limited to interspecific crosses, which rarely occur in nature.

Original languageEnglish (US)
Pages (from-to)4542-4546
Number of pages5
JournalProceedings of the National Academy of Sciences of the United States of America
Volume92
Issue number10
StatePublished - 1995

Fingerprint

Mitochondrial DNA
Embryonic Development
Spermatozoa
Mitochondria
Oocytes
Sperm Midpiece
Chlamydomonas
Membrane Potentials
Mammals
Cytoplasm
Proteins
Embryonic Structures
Genome
Genes

ASJC Scopus subject areas

  • General
  • Genetics

Cite this

Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. / Kaneda, H.; Hayashi, J. I.; Takahama, S.; Taya, C.; Lindahl, K. F.; Yonekawa, H.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 92, No. 10, 1995, p. 4542-4546.

Research output: Contribution to journalArticle

Kaneda, H. ; Hayashi, J. I. ; Takahama, S. ; Taya, C. ; Lindahl, K. F. ; Yonekawa, H. / Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. In: Proceedings of the National Academy of Sciences of the United States of America. 1995 ; Vol. 92, No. 10. pp. 4542-4546.
@article{f4c46d2c4084409b98ed5b86574d1c89,
title = "Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis",
abstract = "To examine whether mtDNA is uni- or biparentally transmitted in mice, we developed an assay that can detect sperm mtDNA in a single mouse embryo. In intraspecific hybrids of Mus musculus, paternal mtDNA was detected only through the early pronucleus stage, and its disappearance coincided with loss of membrane potential in sperm-derived mitochondria. By contrast, in interspecific hybrids between M. musculus and Mus spretus, paternal mtDNA was detected throughout development from pronucleus stage to neonates. We propose that oocyte cytoplasm has a species-specific mechanism that recognizes and eliminates sperm mitochondria and mtDNA. This mechanism must recognize nuclearly encoded proteins in the sperm midpiece, and not the mtDNA or the proteins it encodes, because sperm mitochondria from the congenic strain B6.mt(spr), which carries M. spretus mtDNA on background of M. musculus (B6) nuclear genes, were eliminated early by B6 oocytes as in intraspecific crosses. We conclude that cytoplasmic genomes are transmitted uniparentally in intraspecific crosses in mammals as in Chlamydomonas and that leakage of parental mtDNA is limited to interspecific crosses, which rarely occur in nature.",
author = "H. Kaneda and Hayashi, {J. I.} and S. Takahama and C. Taya and Lindahl, {K. F.} and H. Yonekawa",
year = "1995",
language = "English (US)",
volume = "92",
pages = "4542--4546",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "10",

}

TY - JOUR

T1 - Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis

AU - Kaneda, H.

AU - Hayashi, J. I.

AU - Takahama, S.

AU - Taya, C.

AU - Lindahl, K. F.

AU - Yonekawa, H.

PY - 1995

Y1 - 1995

N2 - To examine whether mtDNA is uni- or biparentally transmitted in mice, we developed an assay that can detect sperm mtDNA in a single mouse embryo. In intraspecific hybrids of Mus musculus, paternal mtDNA was detected only through the early pronucleus stage, and its disappearance coincided with loss of membrane potential in sperm-derived mitochondria. By contrast, in interspecific hybrids between M. musculus and Mus spretus, paternal mtDNA was detected throughout development from pronucleus stage to neonates. We propose that oocyte cytoplasm has a species-specific mechanism that recognizes and eliminates sperm mitochondria and mtDNA. This mechanism must recognize nuclearly encoded proteins in the sperm midpiece, and not the mtDNA or the proteins it encodes, because sperm mitochondria from the congenic strain B6.mt(spr), which carries M. spretus mtDNA on background of M. musculus (B6) nuclear genes, were eliminated early by B6 oocytes as in intraspecific crosses. We conclude that cytoplasmic genomes are transmitted uniparentally in intraspecific crosses in mammals as in Chlamydomonas and that leakage of parental mtDNA is limited to interspecific crosses, which rarely occur in nature.

AB - To examine whether mtDNA is uni- or biparentally transmitted in mice, we developed an assay that can detect sperm mtDNA in a single mouse embryo. In intraspecific hybrids of Mus musculus, paternal mtDNA was detected only through the early pronucleus stage, and its disappearance coincided with loss of membrane potential in sperm-derived mitochondria. By contrast, in interspecific hybrids between M. musculus and Mus spretus, paternal mtDNA was detected throughout development from pronucleus stage to neonates. We propose that oocyte cytoplasm has a species-specific mechanism that recognizes and eliminates sperm mitochondria and mtDNA. This mechanism must recognize nuclearly encoded proteins in the sperm midpiece, and not the mtDNA or the proteins it encodes, because sperm mitochondria from the congenic strain B6.mt(spr), which carries M. spretus mtDNA on background of M. musculus (B6) nuclear genes, were eliminated early by B6 oocytes as in intraspecific crosses. We conclude that cytoplasmic genomes are transmitted uniparentally in intraspecific crosses in mammals as in Chlamydomonas and that leakage of parental mtDNA is limited to interspecific crosses, which rarely occur in nature.

UR - http://www.scopus.com/inward/record.url?scp=0029076820&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0029076820&partnerID=8YFLogxK

M3 - Article

VL - 92

SP - 4542

EP - 4546

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 10

ER -