The implications of mitochondrial DNA copy number regulation during embryogenesis

Mitochondrion

Volumn 11, Issue 5, 2011, Pages 686-692

  Carling, Phillippa J ^a   Cree, Lynsey M ^a   Chinnery, Patrick F ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Copy number; Genetic bottleneck; Inheritance; Mitochondrial biogenesis; MtDNA replication; Transcription

Indexed keywords

MITOCHONDRIAL DNA; NUCLEOSIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR;

BIOGENESIS; BOTTLENECK POPULATION; EMBRYO DEVELOPMENT; GENE MUTATION; GENETIC REGULATION; HETEROPLASMY; HUMAN; INHERITANCE; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL GENOME; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; DNA COPY NUMBER VARIATIONS; DNA REPLICATION; EMBRYONIC DEVELOPMENT; GENOME, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; NUCLEOSIDES; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTORS;

EID: 79961211249     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2011.05.004     Document Type: Review

References (92)

1. Achanta G., Sasaki R., Feng L., Carew J.S., Lu W., Pelicano H., Keating M.J., Huang P. Novel role of p53 in maintaining mitochondrial genetic stability through interaction with DNA Pol gamma. EMBO J. 2005, 24:3482-3492.
2. Aiken C.E., Cindrova-Davies T., Johnson M.H. Variations in mouse mitochondrial DNA copy number from fertilization to birth are associated with oxidative stress. Reprod. Biomed. Online 2008, 17:806-813.
3. Battersby B.J., Shoubridge E.A. Selection of a mtDNA sequence variant in hepatocytes of heteroplasmic mice is not due to differences in respiratory chain function or efficiency of replication. Hum. Mol. Genet. 2001, 10:2469-2479.
4. Bergstrom C.T., Pritchard J. Germline bottlenecks and the evolutionary maintenance of mitochondrial genomes. Genetics 1998, 149:2135-2146.
5. Blok R.B., Gook D.A., Thorburn D.R., Dahl H.H. Skewed segregation of the mtDNA nt 8993 (T→G) mutation in human oocytes. Am. J. Hum. Genet. 1997, 60:1495-1501.
6. Bogenhagen D.F., Rousseau D., Burke S. The layered structure of human mitochondrial DNA nucleoids. J. Biol. Chem. 2008, 283:3665-3675.
7. Bourdon A., Minai L., Serre V., Jais J.P., Sarzi E., Aubert S., Chretien D., De Lonlay P., Paquis-Flucklinger V., Arakawa H., Nakamura Y., Munnich A., Rotig A. Mutation of RRM2B, encoding p53-controlled ribonucleotide reductase (p53R2), causes severe mitochondrial DNA depletion. Nat. Genet. 2007, 39:776-780.
8. Brown W.M., George M., Wilson A.C. Rapid evolution of animal mitochondrial DNA. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:1967-1971.
9. Brown D.T., Samuels D.C., Michael E.M., Turnbull D.M., Chinnery P.F. Random genetic drift determines the level of mutant mtDNA in human primary oocytes. Am. J. Hum. Genet. 2001, 68:533-536.
10. Cao L., Shitara H., Horii T., Nagao Y., Imai H., Abe K., Hara T., Hayashi J., Yonekawa H. The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nat. Genet. 2007, 39:386-390.
11. Cao L., Shitara H., Sugimoto M., Hayashi J., Abe K., Yonekawa H. New evidence confirms that the mitochondrial bottleneck is generated without reduction of mitochondrial DNA content in early primordial germ cells of mice. PLoS Genet. 2009, 5:e1000756.
12. Cavelier L., Johannisson A., Gyllensten U. Analysis of mtDNA copy number and composition of single mitochondrial particles using flow cytometry and PCR. Exp. Cell Res. 2000, 259:79-85.
13. Chen H., Vermulst M., Wang Y.E., Chomyn A., Prolla T.A., Mccaffery J.M., Chan D.C. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 2010, 141:280-289.
14. Chinnery P.F., Howell N., Lightowlers R.N., Turnbull D.M. Molecular pathology of MELAS and MERRF. The relationship between mutation load and clinical phenotypes. Brain 1997, 120(Pt 10):1713-1721.
15. Chinnery P.F., Thorburn D.R., Samuels D.C., White S.L., Dahl H.M., Turnbull D.M., Lightowlers R.N., Howell N. The inheritance of mitochondrial DNA heteroplasmy: random drift, selection or both?. Trends Genet. 2000, 16:500-505.
16. Clayton D.A. Replication of animal mitochondrial DNA. Cell 1982, 28:693-705.
17. Cree L.M., Samuels D.C., De Sousa Lopes S.C., Rajasimha H.K., Wonnapinij P., Mann J.R., Dahl H.H., Chinnery P.F. A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat. Genet. 2008, 40:249-254.
18. Drachman D.A. Ophthalmoplegia plus. The neurodegenerative disorders associated with progressive external ophthalmoplegia. Arch. Neurol. 1968, 18:654-674.
19. Ekstrand M.I., Falkenberg M., Rantanen A., Park C.B., Gaspari M., Hultenby K., Rustin P., Gustafsson C.M., Larsson N.G. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum. Mol. Genet. 2004, 13:935-944.
20. Elson J.L., Andrews R.M., Chinnery P.F., Lightowlers R.N., Turnbull D.M., Howell N. Analysis of European mtDNAs for recombination. Am. J. Hum. Genet. 2001, 68:145-153.
21. Falkenberg M., Gaspari M., Rantanen A., Trifunovic A., Larsson N.G., Gustafsson C.M. Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat. Genet. 2002, 31:289-294.
22. Fan W., Waymire K.G., Narula N., Li P., Rocher C., Coskun P.E., Vannan M.A., Narula J., Macgregor G.R., Wallace D.C. A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science 2008, 319:958-962.
23. Farr C.L., Wang Y., Kaguni L.S. Functional interactions of mitochondrial DNA polymerase and single-stranded DNA-binding protein. Template-primer DNA binding and initiation and elongation of DNA strand synthesis. J. Biol. Chem. 1999, 274:14779-14785.
24. Felsenstein J. The evolutionary advantage of recombination. Genetics 1974, 78:737-756.
25. Fukuhara N., Tokiguchi S., Shirakawa K., Tsubaki T. Myoclonus epilepsy associated with ragged-red fibres (mitochondrial abnormalities): disease entity or a syndrome? Light- and electron-microscopic studies of two cases and review of literature. J. Neurol. Sci. 1980, 47:117-133.
26. Gaspari M., Falkenberg M., Larsson N.G., Gustafsson C.M. The mitochondrial RNA polymerase contributes critically to promoter specificity in mammalian cells. EMBO J. 2004, 23:4606-4614.
27. Gilkerson R.W., Schon E.A., Hernandez E., Davidson M.M. Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation. J. Cell Biol. 2008, 181:1117-1128.
28. Ginsburg M., Snow M.H., Mclaren A. Primordial germ cells in the mouse embryo during gastrulation. Development 1990, 110:521-528.
29. Hauswirth W.W., Laipis P.J. Mitochondrial DNA polymorphism in a maternal lineage of Holstein cows. Proc. Natl. Acad. Sci. U. S. A. 1982, 79:4686-4690.
30. Hirose F., Yamaguchi M., Kuroda K., Omori A., Hachiya T., Ikeda M., Nishimoto Y., Matsukage A. Isolation and characterization of cDNA for DREF, a promoter-activating factor for Drosophila DNA replication-related genes. J. Biol. Chem. 1996, 271:3930-3937.
31. Holt I.J. Mitochondrial DNA replication and repair: all a flap. Trends Biochem. Sci. 2009, 34:358-365.
32. Holt I.J., Miller D.H., Harding A.E. Genetic heterogeneity and mitochondrial DNA heteroplasmy in Leber's hereditary optic neuropathy. J. Med. Genet. 1989, 26:739-743.
33. Holt I.J., Lorimer H.E., Jacobs H.T. Coupled leading- and lagging-strand synthesis of mammalian mitochondrial DNA. Cell 2000, 100:515-524.
34. Howell N., Halvorson S., Kubacka I., Mccullough D.A., Bindoff L.A., Turnbull D.M. Mitochondrial gene segregation in mammals: is the bottleneck always narrow?. Hum. Genet. 1992, 90:117-120.
35. Jacobs H.T., Lehtinen S.K., Spelbrink J.N. No sex please, we're mitochondria: a hypothesis on the somatic unit of inheritance of mammalian mtDNA. Bioessays 2000, 22:564-572.
36. Jenuth J.P., Peterson A.C., Fu K., Shoubridge E.A. Random genetic drift in the female germline explains the rapid segregation of mammalian mitochondrial DNA. Nat. Genet. 1996, 14:146-151.
37. Jenuth J.P., Peterson A.C., Shoubridge E.A. Tissue-specific selection for different mtDNA genotypes in heteroplasmic mice. Nat. Genet. 1997, 16:93-95.
38. Jokinen R., Marttinen P., Sandell H.K., Manninen T., Teerenhovi H., Wai T., Teoli D., Loredo-Osti J.C., Shoubridge E.A., Battersby B.J. Gimap3 regulates tissue-specific mitochondrial DNA segregation. PLoS Genet. 2010, 6:e1001161.
39. Korhonen J.A., Gaspari M., Falkenberg M. TWINKLE has 5'→3' DNA helicase activity and is specifically stimulated by mitochondrial single-stranded DNA-binding protein. J. Biol. Chem. 2003, 278:48627-48632.
40. Laipis P.J., Van De Walle M.J., Hauswirth W.W. Unequal partitioning of bovine mitochondrial genotypes among siblings. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:8107-8110.
41. Larsson N.G., Tulinius M.H., Holme E., Oldfors A., Andersen O., Wahlstrom J., Aasly J. Segregation and manifestations of the mtDNA tRNA(Lys) Ararr;G(8344) mutation of myoclonus epilepsy and ragged-red fibers (MERRF) syndrome. Am. J. Hum. Genet. 1992, 51:1201-1212.
42. Larsson N.G., Oldfors A., Holme E., Clayton D.A. Low levels of mitochondrial transcription factor A in mitochondrial DNA depletion. Biochem. Biophys. Res. Commun. 1994, 200:1374-1381.
43. Larsson N.G., Wang J., Wilhelmsson H., Oldfors A., Rustin P., Lewandoski M., Barsh G.S., Clayton D.A. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 1998, 18:231-236.
44. Lebedeva M.A., Eaton J.S., Shadel G.S. Loss of p53 causes mitochondrial DNA depletion and altered mitochondrial reactive oxygen species homeostasis. Biochim. Biophys. Acta 2009, 1787:328-334.
45. Lefai E., Fernandez-Moreno M.A., Alahari A., Kaguni L.S., Garesse R. Differential regulation of the catalytic and accessory subunit genes of Drosophila mitochondrial DNA polymerase. J. Biol. Chem. 2000, 275:33123-33133.
46. Lenaz G. The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life 2001, 52:159-164.
47. Malena A., Loro E., Di Re M., Holt I.J., Vergani L. Inhibition of mitochondrial fission favours mutant over wild-type mitochondrial DNA. Hum. Mol. Genet. 2009, 18:3407-3416.
48. Mandel H., Szargel R., Labay V., Elpeleg O., Saada A., Shalata A., Anbinder Y., Berkowitz D., Hartman C., Barak M., Eriksson S., Cohen N. The deoxyguanosine kinase gene is mutated in individuals with depleted hepatocerebral mitochondrial DNA. Nat. Genet. 2001, 29:337-341.
49. Maniura-Weber K., Goffart S., Garstka H.L., Montoya J., Wiesner R.J. Transient overexpression of mitochondrial transcription factor A (TFAM) is sufficient to stimulate mitochondrial DNA transcription, but not sufficient to increase mtDNA copy number in cultured cells. Nucleic Acids Res. 2004, 32:6015-6027.
50. Mclaren A., Lawson K.A. How is the mouse germ-cell lineage established?. Differentiation 2005, 73:435-437.
51. Meirelles F.V., Smith L.C. Mitochondrial genotype segregation in a mouse heteroplasmic lineage produced by embryonic karyoplast transplantation. Genetics 1997, 145:445-451.
52. Moreno-Loshuertos R., Acin-Perez R., Fernandez-Silva P., Movilla N., Perez-Martos A., Rodriguez De Cordoba S., Gallardo M.E., Enriquez J.A. Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nat. Genet. 2006, 38:1261-1268.
53. Motohashi H., Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol. Med. 2004, 10:549-557.
54. Muller H.J. The relation of recombination to mutational advance. Mutat. Res. 1964, 106:2-9.
55. Nishino I., Spinazzola A., Hirano M. Thymidine phosphorylase gene mutations in MNGIE, a human mitochondrial disorder. Science 1999, 283:689-692.
56. Olivo P., Van De Walle M., Laipis P., Hauswirth W. Nucleotide sequence evidence for rapid genotypic shifts in the bovinemitochondrial DNA D-loop. Nature 1983, 306:400-402.
57. Olson W., Engel W.K., Walsh G.O., Einaugler R. Oculocraniosomatic neuromuscular disease with "ragged-red" fibers. Arch. Neurol. 1972, 26:193-211.
58. Olson M.W., Wang Y., Elder R.H., Kaguni L.S. Subunit structure of mitochondrial DNA polymerase from Drosophila embryos. Physical and immunological studies. J. Biol. Chem. 1995, 270:28932-28937.
59. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., Hill D.E., Vidal M., Evans J.G., Thorburn D.R., Carr S.A., Mootha V.K. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
60. Pavlakis S.G., Phillips P.C., Dimauro S., De Vivo D.C., Rowland L.P. Mitochondrial myopathy, encephalopathy, lactic acidosis, and strokelike episodes: a distinctive clinical syndrome. Ann. Neurol. 1984, 16:481-488.
61. Payer B., Chuva De Sousa Lopes S.M., Barton S.C., Lee C., Saitou M., Surani M.A. Generation of stella-GFP transgenic mice: a novel tool to study germ cell development. Genesis 2006, 44:75-83.
62. Petty R.K., Harding A.E., Morgan-Hughes J.A. The clinical features of mitochondrial myopathy. Brain 1986, 109(Pt 5):915-938.
63. Piko L., Taylor K.D. Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos. Dev. Biol. 1987, 123:364-374.
64. Pillar T.M., Seitz H.J. Thyroid hormone and gene expression in the regulation of mitochondrial respiratory function. Eur. J. Endocrinol. 1997, 136:231-239.
65. Poe B.G., Duffy C.F., Greminger M.A., Nelson B.J., Arriaga E.A. Detection of heteroplasmy in individual mitochondrial particles. Anal. Bioanal. Chem. 2010, 397:3397-3407.
66. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., Spiegelman B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998, 92:829-839.
67. Rampazzo C., Ferraro P., Pontarin G., Fabris S., Reichard P., Bianchi V. Mitochondrial deoxyribonucleotides, pool sizes, synthesis, and regulation. J. Biol. Chem. 2004, 279:17019-17026.
68. Ropp P.A., Copeland W.C. Cloning and characterization of the human mitochondrial DNA polymerase, DNA polymerase gamma. Genomics 1996, 36:449-458.
69. Rotig A., Poulton J. Genetic causes of mitochondrial DNA depletion in humans. Biochim. Biophys. Acta 2009, 1792:1103-1108.
70. Ruiz De Mena I., Lefai E., Garesse R., Kaguni L.S. Regulation of mitochondrial single-stranded DNA-binding protein gene expression links nuclear and mitochondrial DNA replication in Drosophila. J. Biol. Chem. 2000, 275:13628-13636.
71. Saada A., Shaag A., Mandel H., Nevo Y., Eriksson S., Elpeleg O. Mutant mitochondrial thymidine kinase in mitochondrial DNA depletion myopathy. Nat. Genet. 2001, 29:342-344.
72. Samuels D.C., Wonnapinij P., Cree L.M., Chinnery P.F. Reassessing evidence for a postnatal mitochondrial genetic bottleneck. Nat. Genet. 2010, 42:471-472. (author reply 472-3).
73. Schon E.A., Bonilla E., Dimauro S. Mitochondrial DNA mutations and pathogenesis. J. Bioenerg. Biomembr. 1997, 29:131-149.
74. Schultz R.A., Swoap S.J., Mcdaniel L.D., Zhang B., Koon E.C., Garry D.J., Li K., Williams R.S. Differential expression of mitochondrial DNA replication factors in mammalian tissues. J. Biol. Chem. 1998, 273:3447-3451.
75. Spelbrink J.N., Toivonen J.M., Hakkaart G.A., Kurkela J.M., Cooper H.M., Lehtinen S.K., Lecrenier N., Back J.W., Speijer D., Foury F., Jacobs H.T. In vivo functional analysis of the human mitochondrial DNA polymerase POLG expressed in cultured human cells. J. Biol. Chem. 2000, 275:24818-24828.
76. Spelbrink J.N., Li F.Y., Tiranti V., Nikali K., Yuan Q.P., Tariq M., Wanrooij S., Garrido N., Comi G., Morandi L., Santoro L., Toscano A., Fabrizi G.M., Somer H., Croxen R., Beeson D., Poulton J., Suomalainen A., Jacobs H.T., Zeviani M., Larsson C. Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nat. Genet. 2001, 28:223-231.
77. Stewart J.B., Freyer C., Elson J.L., Wredenberg A., Cansu Z., Trifunovic A., Larsson N.G. Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biol. 2008, 6:e10.
78. Sugimoto M., Abe K. X chromosome reactivation initiates in nascent primordial germ cells in mice. PLoS Genet. 2007, 3:e116.
79. Tam P.P., Snow M.H. Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J. Embryol. Exp. Morphol. 1981, 64:133-147.
80. Taylor R.W., Turnbull D.M. Mitochondrial DNA mutations in human disease. Nat. Rev. Genet. 2005, 6:389-402.
81. Trong-Tue N., Thao D.T., Yamaguchi M. Role of DREF in transcriptional regulation of the Drosophila p53 gene. Oncogene 2010, 29:2060-2069.
82. Twig G., Elorza A., Molina A.J., Mohamed H., Wikstrom J.D., Walzer G., Stiles L., Haigh S.E., Katz S., Las G., Alroy J., Wu M., Py B.F., Yuan J., Deeney J.T., Corkey B.E., Shirihai O.S. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008, 27:433-446.
83. Tyynismaa H., Sembongi H., Bokori-Brown M., Granycome C., Ashley N., Poulton J., Jalanko A., Spelbrink J.N., Holt I.J., Suomalainen A. Twinkle helicase is essential for mtDNA maintenance and regulates mtDNA copy number. Hum. Mol. Genet. 2004, 13:3219-3227.
84. Virbasius J.V., Scarpulla R.C. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:1309-1313.
85. Wai T., Teoli D., Shoubridge E.A. The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nat. Genet. 2008, 40:1484-1488.
86. Weitzel J.M., Iwen K.A., Seitz H.J. Regulation of mitochondrial biogenesis by thyroid hormone. Exp. Physiol. 2003, 88:121-128.
87. Wonnapinij P., Chinnery P.F., Samuels D.C. The distribution of mitochondrial DNA heteroplasmy due to random genetic drift. Am. J. Hum. Genet. 2008, 83:582-593.
88. Wonnapinij P., Chinnery P.F., Samuels D.C. Previous estimates of mitochondrial DNA mutation level variance did not account for sampling error: comparing the mtDNA genetic bottleneck in mice and humans. Am. J. Hum. Genet. 2010, 86:540-550.
89. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
90. Yeom Y.I., Fuhrmann G., Ovitt C.E., Brehm A., Ohbo K., Gross M., Hubner K., Scholer H.R. Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development 1996, 122:881-894.
91. Yoshida Y., Izumi H., Torigoe T., Ishiguchi H., Itoh H., Kang D., Kohno K. P53 physically interacts with mitochondrial transcription factor A and differentially regulates binding to damaged DNA. Cancer Res. 2003, 63:3729-3734.
92. Zhu L., Wang Q., Zhang L., Fang Z., Zhao F., Lv Z., Gu Z., Zhang J., Wang J., Zen K., Xiang Y., Wang D., Zhang C.Y. Hypoxia induces PGC-1alpha expression and mitochondrial biogenesis in the myocardium of TOF patients. Cell Res. 2010, 20:676-687.