Mitochondrial DNA segregation and replication restrict the transmission of detrimental mutation.


Journal

The Journal of cell biology
ISSN: 1540-8140
Titre abrégé: J Cell Biol
Pays: United States
ID NLM: 0375356

Informations de publication

Date de publication:
06 07 2020
Historique:
received: 22 05 2019
revised: 15 11 2019
accepted: 10 04 2020
entrez: 7 5 2020
pubmed: 7 5 2020
medline: 18 3 2021
Statut: ppublish

Résumé

Although mitochondrial DNA (mtDNA) is prone to accumulate mutations and lacks conventional DNA repair mechanisms, deleterious mutations are exceedingly rare. How the transmission of detrimental mtDNA mutations is restricted through the maternal lineage is debated. Here, we demonstrate that mitochondrial fission, together with the lack of mtDNA replication, segregate mtDNA into individual organelles in the Drosophila early germarium. After mtDNA segregation, mtDNA transcription begins, which activates respiration. Mitochondria harboring wild-type genomes have functional electron transport chains and propagate more vigorously than mitochondria containing deleterious mutations in hetreoplasmic cells. Therefore, mtDNA expression acts as a stress test for the integrity of mitochondrial genomes and sets the stage for replication competition. Our observations support selective inheritance at the organelle level through a series of developmentally orchestrated mitochondrial processes. We also show that the Balbiani body has a minor role in mtDNA selective inheritance by supplying healthy mitochondria to the pole plasm. These two mechanisms may act synergistically to secure the transmission of functional mtDNA through Drosophila oogenesis.

Identifiants

pubmed: 32375181
pii: 151740
doi: 10.1083/jcb.201905160
pmc: PMC7337505
pii:
doi:

Substances chimiques

DNA, Mitochondrial 0
Electron Transport Chain Complex Proteins 0

Types de publication

Journal Article Research Support, N.I.H., Intramural

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply.

Références

Science. 2014 Nov 7;346(6210):748-51
pubmed: 25378625
J Cell Sci. 2004 Mar 1;117(Pt 7):1201-10
pubmed: 14996942
Science. 2008 Feb 15;319(5865):958-62
pubmed: 18276892
Nat Genet. 2014 Apr;46(4):389-92
pubmed: 24614072
Trends Microbiol. 2018 Oct;26(10):815-832
pubmed: 29843923
Sci Rep. 2019 Aug 27;9(1):12419
pubmed: 31455826
Proc Natl Acad Sci U S A. 1982 Aug;79(15):4686-90
pubmed: 6289312
Nucleic Acids Res. 2003 Mar 15;31(6):1640-5
pubmed: 12626705
Exp Cell Res. 1991 Sep;196(1):137-40
pubmed: 1715276
PLoS Biol. 2010 Jan 26;8(1):e1000298
pubmed: 20126261
EMBO J. 2016 May 17;35(10):1045-57
pubmed: 27053724
J Cell Biol. 2008 Jun 30;181(7):1117-28
pubmed: 18573913
Proc Natl Acad Sci U S A. 2006 Oct 31;103(44):16325-30
pubmed: 17056713
Dev Cell. 2001 Oct;1(4):515-25
pubmed: 11703942
Cell Tissue Res. 2016 Oct;366(1):191-201
pubmed: 27164893
Curr Biol. 2014 Jan 20;24(2):144-55
pubmed: 24388847
Biophys J. 1999 Jan;76(1 Pt 1):469-77
pubmed: 9876159
Nat Rev Genet. 2008 Sep;9(9):657-62
pubmed: 18695671
Mech Dev. 1998 Nov;78(1-2):113-8
pubmed: 9858703
Proc Natl Acad Sci U S A. 2011 Aug 16;108(33):13534-9
pubmed: 21808029
Nat Genet. 2008 Feb;40(2):249-54
pubmed: 18223651
Nat Rev Microbiol. 2008 Oct;6(10):741-51
pubmed: 18794912
Annu Rev Genet. 2005;39:359-407
pubmed: 16285865
Genetics. 1974 Oct;78(2):737-56
pubmed: 4448362
Nature. 1983 Nov 24-30;306(5941):400-2
pubmed: 6646218
EMBO J. 2004 Jun 16;23(12):2423-9
pubmed: 15167897
Development. 2003 Mar;130(6):1159-70
pubmed: 12571107
Proc Natl Acad Sci U S A. 2007 Jan 2;104(1):187-92
pubmed: 17189423
J Cell Sci. 2004 Jun 1;117(Pt 13):2653-62
pubmed: 15138283
Proc Natl Acad Sci U S A. 2012 Sep 18;109(38):15109-14
pubmed: 22949706
Cell. 2006 Jun 30;125(7):1241-52
pubmed: 16814712
PLoS Biol. 2008 Jan;6(1):e10
pubmed: 18232733
Development. 2003 Apr;130(8):1579-90
pubmed: 12620983
Mol Biol Cell. 2000 Nov;11(11):3977-91
pubmed: 11071921
Development. 2007 Mar;134(6):1071-80
pubmed: 17287246
Nat Rev Genet. 2005 May;6(5):389-402
pubmed: 15861210
Dev Cell. 2016 Dec 5;39(5):560-571
pubmed: 27923120
Mol Cell. 2019 Mar 21;73(6):1127-1137.e5
pubmed: 30772175
Curr Genet. 2010 Apr;56(2):101-7
pubmed: 20179933
Mol Biol Cell. 2015 Feb 15;26(4):674-84
pubmed: 25501370
Nat Commun. 2018 Nov 30;9(1):5111
pubmed: 30504768
Nature. 2019 Jun;570(7761):380-384
pubmed: 31092924
EMBO J. 2006 Jul 12;25(13):2966-77
pubmed: 16778770
Elife. 2019 Oct 15;8:
pubmed: 31612862
Dev Growth Differ. 2006 Jan;48(1):49-57
pubmed: 16466393
Development. 2006 Sep;133(17):3371-7
pubmed: 16887820
Nat Genet. 2014 Apr;46(4):393-7
pubmed: 24614071
Nat Protoc. 2017 Jul;12(7):1326-1348
pubmed: 28594816
J Vis Exp. 2011 Nov 23;(57):e3266
pubmed: 22143245
Mol Cell. 1999 Nov;4(5):815-26
pubmed: 10619028
PLoS Pathog. 2005 Oct;1(2):e14
pubmed: 16228015
Annu Rev Cell Dev Biol. 1996;12:365-91
pubmed: 8970731
Nat Genet. 1996 Oct;14(2):146-51
pubmed: 8841183
Sci Rep. 2018 Jun 22;8(1):9500
pubmed: 29934612
Cold Spring Harb Perspect Biol. 2013 Nov 01;5(11):a021220
pubmed: 24186072
Proc Natl Acad Sci U S A. 2014 Oct 28;111(43):15474-9
pubmed: 25313049
PLoS Genet. 2014 Oct 09;10(10):e1004670
pubmed: 25299061
Genetics. 2017 Apr;205(4):1473-1488
pubmed: 28159754

Auteurs

Zhe Chen (Z)

National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD.

Zong-Heng Wang (ZH)

National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD.

Guofeng Zhang (G)

National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, MD.

Christopher K E Bleck (CKE)

National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD.

Dillon J Chung (DJ)

National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD.

Grey P Madison (GP)

National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD.

Eric Lindberg (E)

National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD.

Christian Combs (C)

National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD.

Robert S Balaban (RS)

National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD.

Hong Xu (H)

National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD.

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Classifications MeSH