Insight into mammalian mitochondrial DNA segregation

Annals of Medicine

Volumn 45, Issue 2, 2013, Pages 149-155

  Jokinen, Riikka ^a   Battersby, Brendan J ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Autophagy; Disease; Genetics; Metabolism; Mitochondria; Mitochondrial DNA

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; PARKIN; SINGLE STRANDED DNA BINDING PROTEIN;

ARTICLE; ENZYME ACTIVE SITE; EXERCISE; GENE DOSAGE; GENE SEGREGATION; HUMAN; IMMUNOLOGICAL SYNAPSE; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; MAMMAL; MICROAUTOPHAGY; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE; MITOPHAGY; NIDATION; NONHUMAN; OVARY FOLLICLE DEVELOPMENT; POINT MUTATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REPLISOME; RNA SPLICING; SIGNAL TRANSDUCTION;

ANIMALS; CHROMOSOME SEGREGATION; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MUTATION;

EID: 84873380671     PISSN: 07853890     EISSN: 13652060     Source Type: Journal    
DOI: 10.3109/07853890.2012.693190     Document Type: Article

References (98)

1. Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, et al. Sequence and organization of the human mitochondrial genome. Nature. 1981;290:457-65.
2. Bibb MJ, Van Etten RA, Wright CT, Walberg MW, Clayton DA. Sequence and gene organization of mouse mitochondrial DNA. Cell. 1981;26: 167-80.
3. Falkenberg M, Larsson NG, Gustafsson CM. DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem. 2007;76:679-99.
4. Bogenhagen DF. Mitochondrial DNA nucleoid structure. Biochim Biophys Acta. 2011 Nov 27 [Epub ahead of print].
5. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong SE, et a l. Amitochondrial protein compendium elucidates complex I disease biology. Cell. 2008;134:112-23.
6. Taylor RW, Turnbull DM. Mitochondrial DNA mutations in human disease. Nat Rev Genet. 2005;6:389-402.
7. Cree LM, Samuels DC, de Sousa Lopes SC, Rajasimha HK, Wonnapinij P, Mann JR, et al. Areduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat Genet. 2008;40:249-54.
8. Wai T, Ao A, Zhang X, Cyr D, Dufort D, Shoubridge EA. The role of mitochondrial DNA copy number in mammalian fertility. Biol Reprod. 2010;83:52-62.
9. Wai T, Teoli D, Shoubridge EA. The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nat Genet. 2008;40:1484-8.
10. Korhonen JA, Pham XH, Pellegrini M, Falkenberg M. Reconstitution of a minimal mtDNA replisome in vitro. EMBO J. 2004;23:2423-9.
11. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet. 1998;18:231-6.
12. Kaufman BA, Durisic N, Mativetsky JM, Costantino S, Hancock MA, Grutter P, et al. The mitochondrial transcription factor TFAM coordinates the assembly of multiple DNA molecules into nucleoid-like structures. Mol Biol Cell. 2007;18:3225-36.
13. Kukat C, Wurm CA, Spahr H, Falkenberg M, Larsson NG, Jakobs S. Super-resolution microscopy reveals that mammalian mitochondrial nucleoids have a uniform size and frequently contain a single copy of mtDNA. Proc Natl Acad Sci USA. 2011;108:13534-9.
14. Spelbrink JN, Toivonen JM, Hakkaart GA, Kurkela JM, Cooper HM, Lehtinen SK, et al. In vivo functional analysis of the human mitochondrial DNA polymerase POLG expressed in cultured human cells. JBiol Chem. 2000;275:24818-28.
15. Ekstrand MI, Falkenberg M, Rantanen A, Park CB, Gaspari M, Hultenby K, et al. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Genet. 2004;13:935-44.
16. Tyynismaa H, Sembongi H, Bokori-Brown M, Granycome C, Ashley N, Poulton J, et al. Twinkle helicase is essential for mtDNA maintenance and regulates mtDNA copy number. Hum Mol Genet. 2004;13: 3219-27.
17. Ylikallio E, Tyynismaa H, Tsutsui H, Ide T, Suomalainen A. High mitochondrial DNA copy number has detrimental effects in mice. Hum Mol Genet. 2010;19:2695-705.
18. Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005;1: 361-70.
19. Clay Montier LL, Deng JJ, Bai Y. Number matters: control of mammalian mitochondrial DNA copy number. JGenet Genomics. 2009; 36:125-31.
20. Moraes CT. What regulates mitochondrial DNA copy number in animal cells? Trends Genet. 2001;17:199-205.
21. Giles RE, Blanc H, Cann HM, Wallace DC. Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci USA. 1980;77: 6715-9.
22. Kaneda H, Hayashi J, Takahama S, Taya C, Lindahl KF, Yonekawa H. Elimination of paternal mitochondrial DNA in intraspecifi c crosses during early mouse embryogenesis. Proc Natl Acad Sci USA. 1995;92:4542-6.
23. He Y, Wu J, Dressman DC, Iacobuzio-Donahue C, Markowitz SD, Velculescu VE, et al. Heteroplasmic mitochondrial DNA mutations in normal and tumour cells. Nature. 2010;464:610-4.
24. Hauswirth WW, Laipis PJ. Mitochondrial DNA polymorphism in a maternal lineage of Holstein cows. Proc Natl Acad Sci USA. 1982;79:4686-90.
25. Jenuth JP, Peterson AC, Fu K, Shoubridge EA. Random genetic drift in the female germline explains the rapid segregation of mammalian mitochondrial DNA. Nat Genet. 1996;14:146-51.
26. Cao L, Shitara H, Horii T, Nagao Y, Imai H, Abe K, et al. The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nat Genet. 2007;39:386-90.
27. Fan W, Waymire KG, Narula N, Li P, Rocher C, Coskun PE, et al. Amouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science. 2008;319:958-62.
28. Stewart JB, Freyer C, Elson JL, Wredenberg A, Cansu Z, Trifunovic A, et al. Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biol. 2008;6:e10.
29. Chinnery PF, Thorburn DR, Samuels DC, White SL, Dahl HM, Turnbull DM, et al. The inheritance of mitochondrial DNA heteroplasmy: random drift, selection or both? Trends Genet. 2000;16:500-5.
30. Monnot S, Gigarel N, Samuels DC, Burlet P, Hesters L, Frydman N, et al. Segregation of mtDNA throughout human embryofetal development: m.3243A ? G as a model system. Hum Mutat. 2011;32:116-25.
31. Hayashi J, Ohta S, Kikuchi A, Takemitsu M, Goto Y, Nonaka I. Introduction of disease-related mitochondrial DNA deletions into HeLa cells lacking mitochondrial DNA results in mitochondrial dysfunction. Proc Natl Acad Sci USA. 1991;88:10614-8.
32. Boulet L, Karpati G, Shoubridge EA. Distribution and threshold expression of the tRNA(Lys) mutation in skeletal muscle of patients with myoclonic epilepsy and ragged-red fi bers (MERRF). Am J Hum Genet. 1992;51:1187-200.
33. Dubeau F, De Stefano N, Zifk in BG, Arnold DL, Shoubridge EA. Oxidative phosphorylation defect in the brains of carriers of the tRNAleu(UUR) A3243G mutation in a MELAS pedigree. Ann Neurol. 2000;47:179-85.
34. Sacconi S, Salviati L, Nishigaki Y, Walker WF, Hernandez-Rosa E, Trevisson E, et al. Afunctionally dominant mitochondrial DNA mutation. Hum Mol Genet. 2008;17:1814-20.
35. Chinnery PF, Samuels DC. Relaxed replication of mtDNA: a model with implications for the expression of disease. Am J Hum Genet. 1999;64:1158-65.
36. Chinnery PF, Zwijnenburg PJ, Walker M, Howell N, Taylor RW, Lightowlers RN, et al. Nonrandom tissue distribution of mutant mtDNA. Am J Med Genet. 1999;85:498-501.
37. Fu K, Hartlen R, Johns T, Genge A, Karpati G, Shoubridge EA. Anovel heteroplasmic tRNAleu(CUN) mtDNA point mutation in a sporadic patient with mitochondrial encephalomyopathy segregates rapidly in skeletal muscle and suggests an approach to therapy. Hum Mol Genet. 1996;5:1835-40.
38. Takeda K, Takahashi S, Onishi A, Hanada H, Imai H. Replicative advantage and tissue-specifi c segregation of RR mitochondrial DNA between C57BL/6 and RR heteroplasmic mice. Genetics. 2000;155: 777-83.
39. Polyak K, Li Y, Zhu H, Lengauer C, Willson JK, Markowitz SD, et a l. Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat Genet. 1998;20:291-3.
40. Elson JL, Samuels DC, Turnbull DM, Chinnery PF. Random intracellular drift explains the clonal expansion of mitochondrial DNA mutations with age. Am J Hum Genet. 2001;68:802-6.
41. Coller HA, Khrapko K, Bodyak ND, Nekhaeva E, Herrero-Jimenez P, Thilly WG. High frequency of homoplasmic mitochondrial DNA mutations in human tumors can be explained without selection. Nat Genet. 2001;28:147-50.
42. Larsson NG. Somatic mitochondrial DNA mutations in mammalian aging. Annu Rev Biochem. 2010;79:683-706.
43. Pyle A, Taylor RW, Durham SE, Deschauer M, Schaefer AM, Samuels DC, et al. Depletion of mitochondrial DNA in leucocytes harbouring the 3243A-? G mtDNA mutation. JMed Genet. 2007;44:69-74.
44. Rahman S, Poulton J, Marchington D, Suomalainen A. Decrease of 3243 A-G mtDNA mutation from blood in MELAS syndrome: a longitudinal study. Am J Hum Genet. 2001;68:238-40.
45. -45.'t Hart LM, Jansen JJ, Lemkes HH, de KnijffP, Maassen JA. Heteroplasmy levels of a mitochondrial gene mutation associated with diabetes mellitus decrease in leucocyte DNA upon aging. Hum Mutat. 1996;7:193-7.
46. Weber K, Wilson JN, Taylor L, Brierley E, Johnson MA, Turnbull DM, et al. Anew mtDNA mutation showing accumulation with time and restriction to skeletal muscle. Am J Hum Genet. 1997;60:373-80.
47. Rajasimha HK, Chinnery PF, Samuels DC. Selection against pathogenic mtDNA mutations in a stem cell population leads to the loss of the 3243A-G mutation in blood. Am J Hum Genet. 2008;82: 333-43.
48. Shoubridge EA. Segregation of mitochondrial DNAs carrying a pathogenic point mutation (tRNA(leu3243)) in cybrid cells. Biochem Biophys Res Commun. 1995;213:189-95.
49. Jenuth JP, Peterson AC, Shoubridge EA. Tissue-specifi c selection for different mtDNA genotypes in heteroplasmic mice. Nat Genet. 1997;16:93-5.
50. Battersby BJ, Loredo-Osti JC, Shoubridge EA. Nuclear genetic control of mitochondrial DNA segregation. Nat Genet. 2003;33:183-6.
51. Battersby BJ, Shoubridge EA. 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;10:2469-79.
52. Jokinen R, Marttinen P, Sandell HK, Manninen T, Teerenhovi H, Wai T, et al. Gimap3 regulates tissue-specifi c mitochondrial DNA segregation. PLoS Genet. 2010;6:e1001161.
53. Battersby BJ, Redpath ME, Shoubridge EA. Mitochondrial DNA segregation in hematopoietic lineages does not depend on MHC presentation of mitochondrially encoded peptides. Hum Mol Genet. 2005;14:2587-94.
54. Schwefel D, Frohlich C, Eichhorst J, Wiesner B, Behlke J, Aravind L, et al. Structural basis of oligomerization in septin-like GTPase of immunity-associated protein 2 (GIMAP2). Proc Natl Acad Sci USA. 2010;107:20299-304.
55. Westermann B. Mitochondrial fusion and fi ssion in cell life and death. Nat Rev Mol Cell Biol. 2010;11:872-84.
56. Detmer SA, Chan DC. Functions and dysfunctions of mitochondrial dynamics. Nat Rev Mol Cell Biol. 2007;8:870-9.
57. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. JCell Biol. 2003;160:189-200.
58. Davies VJ, Hollins AJ, Piechota MJ, Yip W, Davies JR, White KE, et a l. Opa1 defi ciency in a mouse model of autosomal dominant optic atrophy impairs mitochondrial morphology, optic nerve structure and visual function. Hum Mol Genet. 2007;16:1307-18.
59. Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki SO, Masuda K, et al. Mitochondrial fi ssion factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol. 2009;11:958-66.
60. Chan DC. Mitochondria: dynamic organelles in disease, aging, and development. Cell. 2006;125:1241-52.
61. Chen H, Chomyn A, Chan DC. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. JBiol Chem. 2005;280: 26185-92.
62. Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, et al. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell. 2010;141:280-9.
63. Liu X, Weaver D, Shirihai O, Hajnoczky G. Mitochondrial'kiss-andrun': interplay between mitochondrial motility and fusion-fi ssion dynamics. EMBO J. 2009;28:3074-89.
64. Garrido N, Griparic L, Jokitalo E, Wartiovaara J, van der Bliek AM, Spelbrink JN. Composition and dynamics of human mitochondrial nucleoids. Mol Biol Cell. 2003;14:1583-96.
65. Nunnari J, Marshall WF, Straight A, Murray A, Sedat JW, Walter P. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fi ssion and the intramitochondrial segregation of mitochondrial DNA. Mol Biol Cell. 1997;8:1233-42.
66. Gilkerson RW, Schon EA, Hernandez E, Davidson MM. Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation. JCell Biol. 2008;181:1117-28.
67. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008;27:433-46.
68. Malena A, Loro E, Di Re M, Holt IJ, Vergani L. Inhibition of mitochondrial fi ssion favours mutant over wild-type mitochondrial DNA. Hum Mol Genet. 2009;18:3407-16.
69. Stowers RS, Megeath LJ, Gorska-Andrzejak J, Meinertzhagen IA, Schwarz TL. Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron. 2002;36:1063-77.
70. Guo X, Macleod GT, Wellington A, Hu F, Panchumarthi S, Schoenfi eld M, et al. The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron. 2005;47:379-93.
71. Wang X, Schwarz TL. The mechanism of Ca2 ffh-dependent regulation of kinesin-mediated mitochondrial motility. Cell. 2009;136:163-74.
72. Reis K, Fransson A, Aspenstr? P. The Miro GTPases: at the heart of the mitochondrial transport machinery. FEBS Lett. 2009;583:1391-8.
73. Li Z, Okamoto K, Hayashi Y, Sheng M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell. 2004;119:873-87.
74. Campello S, Lacalle RA, Bettella M, Manes S, Scorrano L, Viola A. Orchestration of lymphocyte chemotaxis by mitochondrial dynamics. JExp Med. 2006;203:2879-86.
75. Quintana A, Schwindling C, Wenning AS, Becherer U, Rettig J, Schwarz EC, et al. Tcell activation requires mitochondrial translocation to the immunological synapse. Proc Natl Acad Sci USA. 2007;104:14418-23.
76. Mizushima N. Autophagy: process and function. Genes Dev. 2007;21:2861-73.
77. Kanki T, Wang K, Cao Y, Baba M, Klionsky DJ. Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev Cell. 2009;17:98-109.
78. Okamoto K, Kondo-Okamoto N, Ohsumi Y. Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell. 2009;17:87-97.
79. Sandoval H, Thiagarajan P, Dasgupta SK, Schumacher A, Prchal JT, Chen M, et al. Essential role for Nix in autophagic maturation of erythroid cells. Nature. 2008;454:232-5.
80. Schweers RL, Zhang J, Randall MS, Loyd MR, Li W, Dorsey FC, et a l. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci USA. 2007;104:19500-5.
81. Zhang J, Randall MS, Loyd MR, Dorsey FC, Kundu M, Cleveland JL, et al. Mitochondrial clearance is regulated by Atg7-dependent and-independent mechanisms during reticulocyte maturation. Blood. 2009;114:157-64.
82. Ney PA. Normal and disordered reticulocyte maturation. Curr Opin Hematol. 2011;18:152-7.
83. Al Rawi S, Louvet-Vallee S, Djeddi A, Sachse M, Culetto E, Hajjar C, et al. Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science. 2011;334:1144-7.
84. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010;8:e1000298.
85. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 1998;392:605-8.
86. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science. 2004;304:1158-60.
87. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. JCell Biol. 2008;183:795-803.
88. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA, et a l. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. JCell Biol. 2010;189:211-21.
89. Neuspiel M, Schauss AC, Braschi E, Zunino R, Rippstein P, Rachubinski RA, et al. Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr Biol. 2008;18: 102-8.
90. Andrade-Navarro MA, Sanchez-Pulido L, McBride HM. Mitochondrial vesicles: an ancient process providing new links to peroxisomes. Curr Opin Cell Biol. 2009;21:560-7.
91. Renelli M, Matias V, Lo RY, Beveridge TJ. DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology. 2004;150:2161-9.
92. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, et a l. Circulating mitochondrial DAMPs cause infl ammatory responses to injury. Nature. 2010;464:104-7.
93. Carp H. Mitochondrial N-formylmethionyl proteins as chemoattractants for neutrophils. JExp Med. 1982;155:264-75.
94. Loveland B, Wang CR, Yonekawa H, Hermel E, Lindahl KF. Maternally transmitted histocompatibility antigen of mice: a hydrophobic peptide of a mitochondrially encoded protein. Cell. 1990;60:971-80.
95. Young L, Leonhard K, Tatsuta T, Trowsdale J, Langer T. Role of the ABC transporter Mdl1 in peptide export from mitochondria. Science. 2001;291:2135-8.
96. Haynes CM, Yang Y, Blais SP, Neubert TA, Ron D. The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans. Mol Cell. 2010;37:529-40.
97. Lindahl KF, Byers DE, Dabhi VM, Hovik R, Jones EP, Smith GP, et a l. H2-M3, a full-service class Ib histocompatibility antigen. Annu Rev Immunol. 1997;15:851-79.
98. Ishikawa K, Toyama-Sorimachi N, Nakada K, Morimoto M, Imanishi H, Yoshizaki M, et al. The innate immune system in host mice targets cells with allogenic mitochondrial DNA. JExp Med. 2010;207: 2297-305.