Regulation of Mitochondrial Genome Inheritance by Autophagy and Ubiquitin-proteasome System: Implications for Health, Fitness, and Fertility

Overview

Journal Biomed Res Int

Publisher Wiley

Specialties Biomedical Engineering
Biotechnology
General Medicine

Date 2014 Jul 17

PMID 25028670

Citations 20

Authors

Won-Hee Song

John William Oman Ballard

Young-Joo Yi

Peter Sutovsky

Affiliations

Soon will be listed here.

Abstract

Mitochondria, the energy-generating organelles, play a role in numerous cellular functions including adenosine triphosphate (ATP) production, cellular homeostasis, and apoptosis. Maternal inheritance of mitochondria and mitochondrial DNA (mtDNA) is universally observed in humans and most animals. In general, high levels of mitochondrial heteroplasmy might contribute to a detrimental effect on fitness and disease resistance. Therefore, a disposal of the sperm-derived mitochondria inside fertilized oocytes assures normal preimplantation embryo development. Here we summarize the current research and knowledge concerning the role of autophagic pathway and ubiquitin-proteasome-dependent proteolysis in sperm mitophagy in mammals, including humans. Current data indicate that sperm mitophagy inside the fertilized oocyte could occur along multiple degradation routes converging on autophagic clearance of paternal mitochondria. The influence of assisted reproductive therapies (ART) such as intracytoplasmic sperm injection (ICSI), mitochondrial replacement (MR), and assisted fertilization of oocytes from patients of advanced reproductive age on mitochondrial function, inheritance, and fitness and for the development and health of ART babies will be of particular interest to clinical audiences. Altogether, the study of sperm mitophagy after fertilization has implications in the timing of evolution and developmental and reproductive biology and in human health, fitness, and management of mitochondrial disease.

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References

Kraft C, Peter M, Hofmann K . Selective autophagy: ubiquitin-mediated recognition and beyond. Nat Cell Biol. 2010; 12(9):836-41. DOI: 10.1038/ncb0910-836. View

Kimonis V, Mehta S, Fulchiero E, Thomasova D, Pasquali M, Boycott K . Clinical studies in familial VCP myopathy associated with Paget disease of bone and frontotemporal dementia. Am J Med Genet A. 2008; 146A(6):745-57. PMC: 2467391. DOI: 10.1002/ajmg.a.31862. View

Karbowski M, Youle R . Regulating mitochondrial outer membrane proteins by ubiquitination and proteasomal degradation. Curr Opin Cell Biol. 2011; 23(4):476-82. PMC: 3155757. DOI: 10.1016/j.ceb.2011.05.007. View

Gershoni M, Templeton A, Mishmar D . Mitochondrial bioenergetics as a major motive force of speciation. Bioessays. 2009; 31(6):642-50. DOI: 10.1002/bies.200800139. View

Bogenhagen D . Mitochondrial DNA nucleoid structure. Biochim Biophys Acta. 2011; 1819(9-10):914-20. DOI: 10.1016/j.bbagrm.2011.11.005. View

Chinnery P, Hudson G . Mitochondrial genetics. Br Med Bull. 2013; 106:135-59. PMC: 3675899. DOI: 10.1093/bmb/ldt017. View

Sutovsky P, McCauley T, Sutovsky M, Day B . Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biol Reprod. 2003; 68(5):1793-800. DOI: 10.1095/biolreprod.102.012799. View

Steinborn R, Schinogl P, Wells D, Bergthaler A, Muller M, Brem G . Coexistence of Bos taurus and B. indicus mitochondrial DNAs in nuclear transfer-derived somatic cattle clones. Genetics. 2002; 162(2):823-9. PMC: 1462299. DOI: 10.1093/genetics/162.2.823. View

Liau W, Gonzalez-Serricchio A, Deshommes C, Chin K, LaMunyon C . A persistent mitochondrial deletion reduces fitness and sperm performance in heteroplasmic populations of C. elegans. BMC Genet. 2007; 8:8. PMC: 1852114. DOI: 10.1186/1471-2156-8-8. View

10.

Chinnery P, Howell N, Lightowlers R, Turnbull D . Molecular pathology of MELAS and MERRF. The relationship between mutation load and clinical phenotypes. Brain. 1997; 120 ( Pt 10):1713-21. DOI: 10.1093/brain/120.10.1713. View

11.

Wallace D . Mitochondrial DNA sequence variation in human evolution and disease. Proc Natl Acad Sci U S A. 1994; 91(19):8739-46. PMC: 44682. DOI: 10.1073/pnas.91.19.8739. View

12.

Bruderer R, Brasseur C, Meyer H . The AAA ATPase p97/VCP interacts with its alternative co-factors, Ufd1-Npl4 and p47, through a common bipartite binding mechanism. J Biol Chem. 2004; 279(48):49609-16. DOI: 10.1074/jbc.M408695200. View

13.

Hiraoka J, Hirao Y . Fate of sperm tail components after incorporation into the hamster egg. Gamete Res. 1988; 19(4):369-80. DOI: 10.1002/mrd.1120190408. View

14.

Bohr V, Dianov G . Oxidative DNA damage processing in nuclear and mitochondrial DNA. Biochimie. 1999; 81(1-2):155-60. DOI: 10.1016/s0300-9084(99)80048-0. View

15.

Craven L, Tuppen H, Greggains G, Harbottle S, Murphy J, Cree L . Pronuclear transfer in human embryos to prevent transmission of mitochondrial DNA disease. Nature. 2010; 465(7294):82-5. PMC: 2875160. DOI: 10.1038/nature08958. View

16.

Coskun P, Wyrembak J, Schriner S, Chen H, Marciniack C, LaFerla F . A mitochondrial etiology of Alzheimer and Parkinson disease. Biochim Biophys Acta. 2011; 1820(5):553-64. PMC: 3270155. DOI: 10.1016/j.bbagen.2011.08.008. View

17.

Gyllensten U, Wharton D, Josefsson A, Wilson A . Paternal inheritance of mitochondrial DNA in mice. Nature. 1991; 352(6332):255-7. DOI: 10.1038/352255a0. View

18.

Margulis L . The origin of plant and animal cells. Am Sci. 1971; 59(2):230-5. View

19.

Campello S, Strappazzon F, Cecconi F . Mitochondrial dismissal in mammals, from protein degradation to mitophagy. Biochim Biophys Acta. 2013; 1837(4):451-60. DOI: 10.1016/j.bbabio.2013.11.010. View

20.

DeLuca S, OFarrell P . Barriers to male transmission of mitochondrial DNA in sperm development. Dev Cell. 2012; 22(3):660-8. PMC: 3306594. DOI: 10.1016/j.devcel.2011.12.021. View