Why mitochondria must fuse to maintain their genome integrity

Antioxidants and Redox Signaling

Volumn 19, Issue 4, 2013, Pages 379-388

  Vidoni, Sara ^a,b,c   Zanna, Claudia ^b   Rugolo, Michela ^b   Sarzi, Emmanuelle ^a   Lenaers, Guy ^a  

^a Montpellier University Medical Center   (France)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MITOFUSIN 2; NUCLEOPROTEIN; OPTIC ATROPHY 1; PARKIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE INUDCED KINASE 1; UNCLASSIFIED DRUG;

CELL PROLIFERATION; DNA SEQUENCE; GENE DELETION; GENE DOSAGE; GENE MUTATION; HUMAN; MEMBRANE POTENTIAL; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL GENOME; MITOPHAGY; POINT MUTATION; PRIORITY JOURNAL; REVIEW;

ANIMALS; DNA, MITOCHONDRIAL; GENOME, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS;

BACTERIA (MICROORGANISMS);

EID: 84879874146     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4800     Document Type: Review

References (57)

1. Alavi MV, Bette S, Schimpf S, Schuettauf F, Schraermeyer U, Wehrl HF, Ruttiger L, Beck SC, Tonagel F, Pichler BJ, et al. A splice site mutation in the murine Opa1 gene features pathology of autosomal dominant optic atrophy. Brain 130: 1029-1042, 2007. (Pubitemid 47355593)
2. Amati-Bonneau P, Valentino ML, Reynier P, Gallardo ME, Bornstein B, Boissiere A, Campos Y, Rivera H, de la Aleja JG, Carroccia R, et al. OPA1 mutations induce mitochondrial DNA instability and optic atrophy 'plus' phenotypes. Brain 131: 338-351, 2008. (Pubitemid 351197609)
3. Baricault L, Segui B, Guegand L, Olichon A, Valette A, Larminat F, and Lenaers G. OPA1 cleavage depends on decreased mitochondrial ATP level and bivalent metals. Exp Cell Res 313: 3800-3808, 2007. (Pubitemid 47464239)
4. Bender A, Krishnan KJ, Morris CM, Taylor GA, Reeve AK, Perry RH, Jaros E, Hersheson JS, Betts J, Klopstock T, et al. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat Genet 38: 515-517, 2006.
5. Bereiter-Hahn J and Voth M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc Res Tech 27: 198-219, 1994. (Pubitemid 24062014)
6. Bleazard W, McCaffery JM, King EJ, Bale S, Mozdy A, Tieu Q, Nunnari J, and Shaw JM. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol 1: 298-304, 1999. (Pubitemid 129495781)
7. Cartoni R, Arnaud E, Medard JJ, Poirot O, Courvoisier DS, Chrast R, and Martinou JC. Expression of mitofusin 2(R94Q) in a transgenic mouse leads to Charcot-Marie-Tooth neuropathy type 2A. Brain 133: 1460-1469, 2010.
8. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, and Chan DC. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160: 189-200, 2003. (Pubitemid 36254953)
9. Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, and Chan DC. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141: 280-289, 2010.
10. Chevrollier A, Guillet V, Loiseau D, Gueguen N, de Crescenzo MA, Verny C, Eng MF, Dollfus H, Odent S, Milea D, et al. Hereditary optic neuropathies share a common mitochondrial coupling defect. Ann Neurol 63: 794-798, 2008. (Pubitemid 351945539)
11. Copeland WC. Defects in mitochondrial DNA replication and human disease. Crit Rev Biochem Mol Biol 47: 64-74, 2012.
12. Dawson TM, Ko HS, and Dawson VL. Genetic animal models of Parkinson's disease. Neuron 66: 646-661, 2010.
13. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, Pelloquin L, Grosgeorge J, Turc-Carel C, Perret E, et al. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26: 207-210, 2000.
14. Diot A, Guillou E, Daloyau M, Arnaune-Pelloquin L, Emorine LJ, and Belenguer P. Transmembrane segments of the dynamin Msp1p uncouple its functions in the control of mitochondrial morphology and genome maintenance. J Cell Sci 122: 2632-2639, 2009.
15. Elachouri G, Vidoni S, Zanna C, Pattyn A, Boukhaddaoui H, Gaget K, Yu-Wai-Man P, Gasparre G, Sarzi E, Delettre C, et al. OPA1 links human mitochondrial genome maintenance to mtDNA replication and distribution. Genome Res 21: 12-20, 2011.
16. Elliott HR, Samuels DC, Eden JA, Relton CL, and Chinnery PF. Pathogenic mitochondrial DNA mutations are common in the general population. Am J Hum Genet 83: 254-260, 2008.
17. Ferre M, Bonneau D, Milea D, Chevrollier A, Verny C, Dollfus H, Ayuso C, Defoort S, Vignal C, Zanlonghi X, et al. Molecular screening of 980 cases of suspected hereditary optic neuropathy with a report on 77 Novel OPA1 mutations. Hum Mutat 30: E692-E705, 2009.
18. Gilkerson RW, Schon EA, Hernandez E, and Davidson MM. Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation. J Cell Biol 181: 1117-1128, 2008. (Pubitemid 351915487)
19. Griparic L, Kanazawa T, and van der Bliek AM. Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J Cell Biol 178: 757-764, 2007. (Pubitemid 47347361)
20. Hudson G, Amati-Bonneau P, Blakely EL, Stewart JD, He L, Schaefer AM, Griffiths PG, Ahlqvist K, Suomalainen A, Reynier P, et al. Mutation of OPA1 causes dominant optic atrophy with external ophthalmoplegia, ataxia, deafness and multiple mitochondrial DNA deletions: a novel disorder of mtDNA maintenance. Brain 131: 329-337, 2008. (Pubitemid 351197604)
21. Jones BA and Fangman WL. Mitochondrial DNA maintenance in yeast requires a protein containing a region related to the GTP-binding domain of dynamin. Genes Dev 6: 380-389, 1992.
22. Kogelnik AM, Lott MT, Brown MD, Navathe SB, and Wallace DC. MITOMAP: a human mitochondrial genome database-1998 update. Nucleic Acids Res 26: 112-115, 1998.
23. Lenaz G, Baracca A, Carelli V, D'Aurelio M, Sgarbi G, and Solaini G. Bioenergetics of mitochondrial diseases associated with mtDNA mutations. Biochim Biophys Acta 1658: 89-94, 2004. (Pubitemid 39013238)
24. Liu P and Demple B. DNA repair in mammalian mitochondria: much more than we thought? Environ Mol Mutagen 51: 417-426, 2010.
25. Liu X, Weaver D, Shirihai O, and Hajnoczky G. Mitochondrial 'kiss-and-run': interplay between mitochondrial motility and fusion-fission dynamics. EMBO J 28: 3074-3089, 2009.
26. Loeb LA, Wallace DC, and Martin GM. The mitochondrial theory of aging and its relationship to reactive oxygen species damage and somatic mtDNA mutations. Proc Natl Acad Sci U S A 102: 18769-18770, 2005. (Pubitemid 43049521)
27. Loiseau D, Chevrollier A, Verny C, Guillet V, Gueguen N, Pou de Crescenzo MA, Ferre M, Malinge MC, Guichet A, Nicolas G, et al. Mitochondrial coupling defect in Charcot-Marie-Tooth type 2A disease. Ann Neurol 61: 315-323, 2007. (Pubitemid 46676731)
28. Malka F, Lombes A, and Rojo M. Organization, dynamics and transmission of mitochondrial DNA: focus on vertebrate nucleoids. Biochim Biophys Acta 1763: 463-472, 2006. (Pubitemid 44015946)
29. Matsuda N and Tanaka K. Uncovering the roles of PINK1 and parkin in mitophagy. Autophagy 6: 952-954, 2010.
30. McCorquodale DS, 3rd, Montenegro G, Peguero A, Carlson N, Speziani F, Price J, Taylor SW, Melanson M, Vance JM, and Zuchner S. Mutation screening of mitofusin 2 in Charcot-Marie-Tooth disease type J Neurol 258: 1234-1239, 2011.
31. Montoya J, Gaines GL, and Attardi G. The pattern of transcription of the human mitochondrial rRNA genes reveals two overlapping transcription units. Cell 34: 151-159, 1983. (Pubitemid 13045470)
32. Narendra D, Tanaka A, Suen DF, and Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183: 795-803, 2008.
33. Narendra DP and Youle RJ. Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid Redox Signal 14: 1929-1938, 2011.
34. Narra HP and Ochman H. Of what use is sex to bacteria? Curr Biol 16: R705-R710, 2006. (Pubitemid 44691791)
35. Olichon A, Baricault L, Gas N, Guillou E, Valette A, Belenguer P, and Lenaers G. Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J Biol Chem 278: 7743-7746, 2003. (Pubitemid 36800505)
36. Palade GE. An electron microscope study of the mitochondrial structure. J Histochem Cytochem 1: 188-211, 1953.
37. Payne BA, Wilson IJ, Hateley CA, Horvath R, Santibanez-Koref M, Samuels DC, Price DA, and Chinnery PF. Mitochondrial aging is accelerated by anti-retroviral therapy through the clonal expansion of mtDNA mutations. Nat Genet 43: 806-810, 2011.
38. Pelloquin L, Belenguer P, Menon Y, and Ducommun B. Identification of a fission yeast dynamin-related protein involved in mitochondrial DNA maintenance. Biochem Biophys Res Commun 251: 720-726, 1998. (Pubitemid 28512777)
39. Poole AC, Thomas RE, Andrews LA, McBride HM, Whitworth AJ, and Pallanck LJ. The PINK1/Parkin pathway regulates mitochondrial morphology. Proc Natl Acad Sci U S A 105: 1638-1643, 2008. (Pubitemid 351346567)
40. Rapaport D, Brunner M, Neupert W, and Westermann B. Fzo1p is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria in Saccharomyces cerevisiae. J Biol Chem 273: 20150-20155, 1998. (Pubitemid 28377572)
41. Renaldo F, Amati-Bonneau P, Slama A, Romana C, Forin V, Doummar D, Barnerias C, Bursztyn J, Mayer M, Khouri N, et al. MFN2, a new gene responsible for mitochondrial DNA depletion. Brain 135: e223, 2012.
42. Rojo M, Legros F, Chateau D, and Lombes A. Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo. J Cell Sci 115: 1663-1674, 2002. (Pubitemid 34520596)
43. Rothfuss O, Fischer H, Hasegawa T, Maisel M, Leitner P, Miesel F, Sharma M, Bornemann A, Berg D, Gasser T, et al. Parkin protects mitochondrial genome integrity and supports mitochondrial DNA repair. Hum Mol Genet 18: 3832-3850, 2009.
44. Rouzier C, Bannwarth S, Chaussenot A, Chevrollier A, Verschueren A, Bonello-Palot N, Fragaki K, Cano A, Pouget J, Pellissier JF, et al. The MFN2 gene is responsible for mitochondrial DNA instability and optic atrophy 'plus' phenotype. Brain 135: 23-34, 2012.
45. Sarzi E, Bourdon A, Chretien D, Zarhrate M, Corcos J, Slama A, Cormier-Daire V, de Lonlay P, Munnich A, and Rotig A. Mitochondrial DNA depletion is a prevalent cause of multiple respiratory chain deficiency in childhood. J Pediatr 150: 531-534, 2007.
46. Sarzi E, Goffart S, Serre V, Chretien D, Slama A, Munnich A, Spelbrink JN, and Rotig A. Twinkle helicase (PEO1) gene mutation causes mitochondrial DNA depletion. Ann Neurol 62: 579-587, 2007.
47. Srivastava S and Moraes CT. Double-strand breaks of mouse muscle mtDNA promote large deletions similar to multiple mtDNA deletions in humans. Hum Mol Genet 14: 893-902, 2005. (Pubitemid 40533100)
48. Suen DF, Narendra DP, Tanaka A, Manfredi G, and Youle RJ. Parkin overexpression selects against a deleterious mtDNA mutation in heteroplasmic cybrid cells. Proc Natl Acad Sci U S A 107: 11835-11840, 2010.
49. Takai D, Isobe K, and Hayashi J. Transcomplementation between different types of respiration-deficient mitochondria with different pathogenic mutant mitochondrial DNAs. J Biol Chem 274: 11199-11202, 1999.
50. Thanbichler M and Shapiro L. Chromosome organization and segregation in bacteria. J Struct Biol 156: 292-303, 2006. (Pubitemid 44666446)
51. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27: 433-446, 2008. (Pubitemid 351161653)
52. Twig G, Hyde B, and Shirihai OS. Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view. Biochim Biophys Acta 1777: 1092-1097, 2008.
53. Wallace DC. Mitochondrial DNA mutations in disease and aging. Environ Mol Mutagen 51: 440-450, 2010.
54. Waterham HR, Koster J, van Roermund CW, Mooyer PA, Wanders RJ, and Leonard JV. A lethal defect of mitochondrial and peroxisomal fission. N Engl J Med 356: 1736-1741, 2007. (Pubitemid 46658705)
55. Wei YH and Lee HC. Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp Biol Med (Maywood) 227: 671-682, 2002.
56. Yang Y, Ouyang Y, Yang L, Beal MF, McQuibban A, Vogel H, and Lu B. Pink1 regulates mitochondrial dynamics through interaction with the fission/fusion machinery. Proc Natl Acad Sci U S A 105: 7070-7075, 2008. (Pubitemid 351754531)
57. Yu-Wai-Man P, Davies VJ, Piechota MJ, Cree LM, Votruba M, and Chinnery PF. Secondary mtDNA defects do not cause optic nerve dysfunction in a mouse model of dominant optic atrophy. Invest Ophthalmol Vis Sci 50: 4561-4566, 2009.