Dynamic Regulation of Mitochondrial Genome Maintenance in Germ Cells

Overview

Journal Reprod Med Biol

Specialty Biology

Date 2014 Feb 1

PMID 24482608

Citations 6

Authors

Katsumi Kasashima

Yasumitsu Nagao

Hitoshi Endo

Affiliations

Soon will be listed here.

Abstract

Mitochondria play a crucial role in the development and function of germ cells. Mitochondria contain a maternally inherited genome that should be transmitted to offspring without reactive oxygen species-induced damage during germ line development. Germ cells are also involved in the mitochondrial DNA (mtDNA) bottleneck; thus, the appropriate regulation of mtDNA in these cells is very important for this characteristic transmission. In this review, we focused on unique regulation of the mitochondrial genome in animal germ cells; paternal elimination and the mtDNA bottleneck in females. We also summarized the mitochondrial nucleoid factors involved in various mtDNA regulation pathways. Among them, mitochondrial transcription factor A (TFAM), which has pleiotropic and essential roles in mtDNA maintenance, appears to have putative roles in germ cell regulation.

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References

Garrido N, Griparic L, Jokitalo E, Wartiovaara J, van der Bliek A, Spelbrink J . Composition and dynamics of human mitochondrial nucleoids. Mol Biol Cell. 2003; 14(4):1583-96. PMC: 153124. DOI: 10.1091/mbc.e02-07-0399. View

Stuart J, Mayard S, Hashiguchi K, Souza-Pinto N, Bohr V . Localization of mitochondrial DNA base excision repair to an inner membrane-associated particulate fraction. Nucleic Acids Res. 2005; 33(12):3722-32. PMC: 1174906. DOI: 10.1093/nar/gki683. View

Lu B, Lee J, Nie X, Li M, Morozov Y, Venkatesh S . Phosphorylation of human TFAM in mitochondria impairs DNA binding and promotes degradation by the AAA+ Lon protease. Mol Cell. 2012; 49(1):121-32. PMC: 3586414. DOI: 10.1016/j.molcel.2012.10.023. View

Merkwirth C, Langer T . Prohibitin function within mitochondria: essential roles for cell proliferation and cristae morphogenesis. Biochim Biophys Acta. 2008; 1793(1):27-32. DOI: 10.1016/j.bbamcr.2008.05.013. View

Rantanen A, Jansson M, Oldfors A, Larsson N . Downregulation of Tfam and mtDNA copy number during mammalian spermatogenesis. Mamm Genome. 2001; 12(10):787-92. DOI: 10.1007/s00335-001-2052-8. View

Wang Y, Bogenhagen D . Human mitochondrial DNA nucleoids are linked to protein folding machinery and metabolic enzymes at the mitochondrial inner membrane. J Biol Chem. 2006; 281(35):25791-802. DOI: 10.1074/jbc.M604501200. View

Amikura R, Sato K, Kobayashi S . Role of mitochondrial ribosome-dependent translation in germline formation in Drosophila embryos. Mech Dev. 2005; 122(10):1087-93. DOI: 10.1016/j.mod.2005.06.003. View

Van Blerkom J . Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion. 2010; 11(5):797-813. DOI: 10.1016/j.mito.2010.09.012. View

Thompson W, Ramalho-Santos J, Sutovsky P . Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biol Reprod. 2003; 69(1):254-60. DOI: 10.1095/biolreprod.102.010975. View

10.

Dairaghi D, Shadel G, Clayton D . Addition of a 29 residue carboxyl-terminal tail converts a simple HMG box-containing protein into a transcriptional activator. J Mol Biol. 1995; 249(1):11-28. DOI: 10.1006/jmbi.1995.9889. View

11.

Dellinger M, Geze M . Detection of mitochondrial DNA in living animal cells with fluorescence microscopy. J Microsc. 2002; 204(Pt 3):196-202. DOI: 10.1046/j.1365-2818.2001.00954.x. View

12.

Merkwirth C, Martinelli P, Korwitz A, Morbin M, Bronneke H, Jordan S . Loss of prohibitin membrane scaffolds impairs mitochondrial architecture and leads to tau hyperphosphorylation and neurodegeneration. PLoS Genet. 2012; 8(11):e1003021. PMC: 3493444. DOI: 10.1371/journal.pgen.1003021. View

13.

Nishimura Y, Yoshinari T, Naruse K, Yamada T, Sumi K, Mitani H . Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers. Proc Natl Acad Sci U S A. 2006; 103(5):1382-7. PMC: 1360526. DOI: 10.1073/pnas.0506911103. View

14.

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

15.

Matsushima Y, Matsumura K, Ishii S, Inagaki H, Suzuki T, Matsuda Y . Functional domains of chicken mitochondrial transcription factor A for the maintenance of mitochondrial DNA copy number in lymphoma cell line DT40. J Biol Chem. 2003; 278(33):31149-58. DOI: 10.1074/jbc.M303842200. View

16.

Ankel-Simons F, Cummins J . Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc Natl Acad Sci U S A. 1996; 93(24):13859-63. PMC: 19448. DOI: 10.1073/pnas.93.24.13859. View

17.

Farge G, Laurens N, Broekmans O, van den Wildenberg S, Dekker L, Gaspari M . Protein sliding and DNA denaturation are essential for DNA organization by human mitochondrial transcription factor A. Nat Commun. 2012; 3:1013. DOI: 10.1038/ncomms2001. View

18.

Zhang H, Pommier Y . Mitochondrial topoisomerase I sites in the regulatory D-loop region of mitochondrial DNA. Biochemistry. 2008; 47(43):11196-203. PMC: 2597090. DOI: 10.1021/bi800774b. View

19.

Laipis P, Van de Walle M, Hauswirth W . Unequal partitioning of bovine mitochondrial genotypes among siblings. Proc Natl Acad Sci U S A. 1988; 85(21):8107-10. PMC: 282364. DOI: 10.1073/pnas.85.21.8107. View

20.

Sharpley M, Marciniak C, Eckel-Mahan K, McManus M, Crimi M, Waymire K . Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition. Cell. 2012; 151(2):333-343. PMC: 4175720. DOI: 10.1016/j.cell.2012.09.004. View