Literature DB >> 22421049

Barriers to male transmission of mitochondrial DNA in sperm development.

Steven Z DeLuca1, Patrick H O'Farrell.   

Abstract

Across the eukaryotic phylogeny, offspring usually inherit their mitochondrial genome from only one of two parents: in animals, the female. Although mechanisms that eliminate paternally derived mitochondria from the zygote have been sought, the developmental stage at which paternal transmission of mitochondrial DNA is restricted is unknown in most animals. Here, we show that the mitochondria of mature Drosophila sperm lack DNA, and we uncover two processes that eliminate mitochondrial DNA during spermatogenesis. Visualization of mitochondrial DNA nucleoids revealed their abrupt disappearance from developing spermatids in a process requiring the mitochondrial nuclease, Endonuclease G. In Endonuclease G mutants, persisting nucleoids are swept out of spermatids by a cellular remodeling process that trims and shapes spermatid tails. Our results show that mitochondrial DNA is eliminated during spermatogenesis, thereby removing the capacity of sperm to transmit the mitochondrial genome to the next generation. Copyright Â
© 2012 Elsevier Inc. All rights reserved.

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Year:  2012        PMID: 22421049      PMCID: PMC3306594          DOI: 10.1016/j.devcel.2011.12.021

Source DB:  PubMed          Journal:  Dev Cell        ISSN: 1534-5807            Impact factor:   12.270


  38 in total

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Journal:  Proc Natl Acad Sci U S A       Date:  1980-07       Impact factor: 11.205

6.  Selective and continuous elimination of mitochondria microinjected into mouse eggs from spermatids, but not from liver cells, occurs throughout embryogenesis.

Authors:  H Shitara; H Kaneda; A Sato; K Inoue; A Ogura; H Yonekawa; J I Hayashi
Journal:  Genetics       Date:  2000-11       Impact factor: 4.562

7.  Sustained elongation of sperm tail promoted by local remodeling of giant mitochondria in Drosophila.

Authors:  Tatsuhiko Noguchi; Michiko Koizumi; Shigeo Hayashi
Journal:  Curr Biol       Date:  2011-05-05       Impact factor: 10.834

8.  Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos.

Authors:  Miyuki Sato; Ken Sato
Journal:  Science       Date:  2011-10-13       Impact factor: 47.728

9.  The mitochondrial DNA of Drosophila melanogaster exists in two distinct and stable superhelical forms.

Authors:  J L Rubenstein; D Brutlag; D A Clayton
Journal:  Cell       Date:  1977-10       Impact factor: 41.582

10.  Manipulating the metazoan mitochondrial genome with targeted restriction enzymes.

Authors:  Hong Xu; Steven Z DeLuca; Patrick H O'Farrell
Journal:  Science       Date:  2008-07-25       Impact factor: 47.728

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  63 in total

Review 1.  Genotype to phenotype: Diet-by-mitochondrial DNA haplotype interactions drive metabolic flexibility and organismal fitness.

Authors:  Wen C Aw; Samuel G Towarnicki; Richard G Melvin; Neil A Youngson; Michael R Garvin; Yifang Hu; Shaun Nielsen; Torsten Thomas; Russell Pickford; Sonia Bustamante; Antón Vila-Sanjurjo; Gordon K Smyth; J William O Ballard
Journal:  PLoS Genet       Date:  2018-11-06       Impact factor: 5.917

2.  Paternal transmission of mitochondrial DNA as an integral part of mitochondrial inheritance in metapopulations of Drosophila simulans.

Authors:  J N Wolff; M Nafisinia; P Sutovsky; J W O Ballard
Journal:  Heredity (Edinb)       Date:  2012-09-26       Impact factor: 3.821

Review 3.  Mitochondrial matters: Mitochondrial bottlenecks, self-assembling structures, and entrapment in the female germline.

Authors:  Florence L Marlow
Journal:  Stem Cell Res       Date:  2017-03-15       Impact factor: 2.020

4.  The Mitochondrial DNA Polymerase Promotes Elimination of Paternal Mitochondrial Genomes.

Authors:  Zhongsheng Yu; Patrick H O'Farrell; Nikita Yakubovich; Steven Z DeLuca
Journal:  Curr Biol       Date:  2017-03-16       Impact factor: 10.834

5.  Long Oskar Controls Mitochondrial Inheritance in Drosophila melanogaster.

Authors:  Thomas Ryan Hurd; Beate Herrmann; Julia Sauerwald; Justina Sanny; Markus Grosch; Ruth Lehmann
Journal:  Dev Cell       Date:  2016-12-05       Impact factor: 12.270

6.  Ubiquitination is required for the initial removal of paternal organelles in C. elegans.

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Review 7.  Origins of eukaryotic sexual reproduction.

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Journal:  Cold Spring Harb Perspect Biol       Date:  2014-03-01       Impact factor: 10.005

Review 8.  Mitochondrial dynamics and inheritance during cell division, development and disease.

Authors:  Prashant Mishra; David C Chan
Journal:  Nat Rev Mol Cell Biol       Date:  2014-09-17       Impact factor: 94.444

9.  Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition.

Authors:  Mark S Sharpley; Christine Marciniak; Kristin Eckel-Mahan; Meagan McManus; Marco Crimi; Katrina Waymire; Chun Shi Lin; Satoru Masubuchi; Nicole Friend; Maya Koike; Dimitra Chalkia; Grant MacGregor; Paolo Sassone-Corsi; Douglas C Wallace
Journal:  Cell       Date:  2012-10-12       Impact factor: 41.582

Review 10.  You are what you eat: multifaceted functions of autophagy during C. elegans development.

Authors:  Peiguo Yang; Hong Zhang
Journal:  Cell Res       Date:  2013-12-03       Impact factor: 25.617

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