OPA1 links human mitochondrial genome maintenance to mtDNA replication and distribution

Genome Research

Volumn 21, Issue 1, 2011, Pages 12-20

  Elachouri, Ghizlane ^a,i   Vidoni, Sara ^a,b,i   Zanna, Claudia ^b   Pattyn, Alexandre ^a,i   Boukhaddaoui, Hassan ^a,i   Gaget, Karen ^a,i   Yu Wai Man, Patrick ^c   Gasparre, Giuseppe ^d   Sarzi, Emmanuelle ^e   Delettre, Cécile ^a,i   Olichon, Aurélien ^f   Loiseau, Dominique ^g   Reynier, Pascal ^g   Chinnery, Patrick F ^c   Rotig, Agnès ^e   Carelli, Valerio ^b   Hamel, Christian P ^a,h,i   Rugolo, Michela ^b   Lenaers, Guy ^a,i  

^a Montpellier University Medical Center   (France)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF BARI   (Italy)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f INSTITUT CLAUDIUS REGAUD   (France)

^g ANGERS UNIVERSITY HOSPITAL   (France)

^h MONTPELLIER UNIVERSITY HOSPITAL   (France)

ⁱ UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; MITOCHONDRIAL DNA; PEPTIDE; SMALL INTERFERING RNA;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EUKARYOTE; EXON; GENE; GENE LOCATION; GENE SILENCING; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MITOCHONDRIAL DNA DEPLETION; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL GENOME; MITOCHONDRIAL MEMBRANE; NONHUMAN; OPA1 GENE; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION;

DNA REPLICATION; DNA, MITOCHONDRIAL; GENE SILENCING; GENOME, HUMAN; GENOME, MITOCHONDRIAL; GTP PHOSPHOHYDROLASES; HELA CELLS; HEP G2 CELLS; HUMANS; RNA, SMALL INTERFERING;

EUKARYOTA; VERTEBRATA;

EID: 78651480831     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.108696.110     Document Type: Article

References (44)

1. Albring M, Griffith J, Attardi G. 1977. Association of a protein structure of probable membrane derivation with HeLa cell mitochondrial DNA near its origin of replication. Proc Natl Acad Sci 74: 1348-1352.
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. 2008. OPA1 mutations induce mitochondrial DNA instability and optic atrophy 'plus' phenotypes. Brain 131: 338-351.
3. Ashley N, Harris D, Poulton J. 2005. Detection of mitochondrial DNA depletion in living human cells using PicoGreen staining. Exp Cell Res 303: 432-446.
4. Ashley N, Adams S, Slama A, Zeviani M, Suomalainen A, Andreu AL, Naviaux RK, Poulton J. 2007. Defects in maintenance of mitochondrial DNA are associated with intramitochondrial nucleotide imbalances. Hum Mol Genet 16: 1400-1411.
5. Bogenhagen DF, Rousseau D, Burke S. 2008. The layered structure of human mitochondrial DNA nucleoids. J Biol Chem 283: 3665-3675.
6. Capaldi RA, Aggeler R, Gilkerson R, Hanson G, Knowles M, Marcus A, Margineantu D, Marusich M, Murray J, Oglesbee D, et al. 2002. A replicating module as the unit of mitochondrial structure and functioning. Biochim Biophys Acta 1555: 192-195.
7. Chen H, Chan DC. 2006. Critical dependence of neurons on mitochondrial dynamics. Curr Opin Cell Biol 18: 453-459.
8. Chen H, McCaffery JM, Chan DC. 2007. Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130: 548-562.
9. Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, Chan DC. 2010. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141: 280-289.
10. Copeland WC. 2008. Inherited mitochondrial diseases of DNA replication. Annu Rev Med 59: 131-146.
11. Cornille K, Milea D, Amati-Bonneau P, Procaccio V, Zazoun L, Guillet V, El Achouri G, Delettre C, Gueguen N, Loiseau D, et al. 2008. Reversible optic neuropathy with OPA1 exon 5b mutation. Ann Neurol 63: 667-671.
12. D'Aurelio M, Gajewski CD, Lin MT, Mauck WM, Shao LZ, Lenaz G, Moraes CT, Manfredi G. 2004. Heterologous mitochondrial DNA recombination in human cells. Hum Mol Genet 13: 3171-3179.
13. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, Pelloquin L, Grosgeorge J, Turc-Carel C, Perret E, et al. 2000. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26: 207-210.
14. Delettre C, Griffoin JM, Kaplan J, Dollfus H, Lorenz B, Faivre L, Lenaers G, Belenguer P, Hamel CP. 2001. Mutation spectrum and splicing variants in the OPA1 gene. Hum Genet 109: 584-591.
15. Diot A, Guillou E, Daloyau M, Arnaune-Pelloquin L, Emorine LJ, Belenguer P. 2009. Transmembrane segments of the dynamin Msp1p uncouple its functions in the control of mitochondrial morphology and genome maintenance. J Cell Sci 122: 2632-2639.
16. Duvezin-Caubet S, Koppen M, Wagener J, Zick M, Israel L, Bernacchia A, Jagasia R, Rugarli EI, Imhof A, Neupert W, et al. 2007. OPA1 processing reconstituted in yeast depends on the subunit composition of the m-AAA protease in mitochondria. Mol Biol Cell 18: 3582-3590.
17. Ferre M, Bonneau D, Milea D, Chevrollier A, Verny C, Dollfus H, Ayuso C, Defoort S, Vignal C, Zanlonghi X, et al. 2009. Molecular screening of 980 cases of suspected hereditary optic neuropathywith a report on 77 novel OPA1 mutations. Hum Mutat 30: E692-E705.
18. Garrido N, Griparic L, Jokitalo E, Wartiovaara J, van der Bliek AM, Spelbrink JN. 2003. Composition and dynamics of human mitochondrial nucleoids. Mol Biol Cell 14: 1583-1596.
19. Gilkerson RW, Schon EA, Hernandez E, Davidson MM. 2008. Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation. J Cell Biol 181: 1117-1128.
20. Griparic L, Kanazawa T, van der Bliek AM. 2007. Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J Cell Biol 178: 757-764.
21. Guan K, Farh L, Marshall TK, Deschenes RJ. 1993. Normal mitochondrial structure and genome maintenance in yeast requires the dynamin-like product of the MGM1 gene. Curr Genet 24: 141-148.
22. He J, Mao CC, Reyes A, Sembongi H, Di Re M, Granycome C, Clippingdale AB, Fearnley IM, Harbour M, Robinson AJ, et al. 2007. The AAA+ protein ATAD3 has displacement loop binding properties and is involved in mitochondrial nucleoid organization. J Cell Biol 176: 141-146.
23. Herlan M, Vogel F, Bornhovd C, Neupert W, Reichert AS. 2003. Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA. J Biol Chem 278: 27781-27788.
24. Holt IJ, He J, Mao CC, Boyd-Kirkup JD, Martinsson P, Sembongi H, Reyes A, Spelbrink JN. 2007. Mammalian mitochondrial nucleoids: Organizing an independently minded genome. Mitochondrion 7: 311-321.
25. Hudson G, Amati-Bonneau P, Blakely EL, Stewart JD, He L, Schaefer AM, Griffiths PG, Ahlqvist K, Suomalainen A, Reynier P, et al. 2008. 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.
26. Jones BA, Fangman WL. 1992. Mitochondrial DNA maintenance in yeast requires a protein containing a region related to the GTP-binding domain of dynamin. Genes Dev 6: 380-389.
27. Lenaers G, Pelloquin L, Olichon A, Emorine LJ, Guillou E, Delettre C, Hamel CP, Ducommun B, Belenguer P. 2002. What similarity between human and fission yeast proteins is required for orthology? Yeast 19: 1125-1126.
28. Loiseau D, Morvan D, Chevrollier A, Demidem A, Douay O, Reynier P, Stepien G. 2009. Mitochondrial bioenergetic background confers a survival advantage to HepG2 cells in response to chemotherapy. Mol Carcinog 48: 733-741.
29. Malka F, Lombes A, Rojo M. 2006. Organization, dynamics and transmission of mitochondrial DNA: Focus on vertebrate nucleoids. Biochim Biophys Acta 1763: 463-472.
30. Meeusen S, DeVay R, Block J, Cassidy-Stone A, Wayson S, McCaffery JM, Nunnari J. 2006. Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell 127: 383-395.
31. Nass MM. 1969. Mitochondrial DNA. I. Intramitochondrial distribution and structural relations of single- and double-length circular DNA. J Mol Biol 42: 521-528.
32. Nowak DE, Tian B, Brasier AR. 2005. Two-step cross-linking method for identification of NF-kB gene network by chromatin immunoprecipitation. Biotechniques 39: 715-725.
33. Olichon A, Emorine LJ, Descoins E, Pelloquin L, Brichese L, Gas N, Guillou E, Delettre C, Valette A, Hamel CP, et al. 2002. The human dynaminrelated protein OPA1 is anchored to themitochondrial inner membrane facing the inter-membrane space. FEBS Lett 523: 171-176.
34. Olichon A, Elachouri G, Baricault L, Delettre C, Belenguer P, Lenaers G. 2007. OPA1 alternate splicing uncouples an evolutionary conserved function in mitochondrial fusion from a vertebrate restricted function in apoptosis. Cell Death Differ 14: 682-692.
35. Parone PA, Da Cruz S, Tondera D, Mattenberger Y, James DI, Maechler P, Barja F, Martinou JC. 2008. Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS ONE 3: e3257. doi: 10.1371/journal.pone.0003257.
36. Pelloquin L, Belenguer P, Menon Y, Ducommun B. 1998. Identification of a fission yeast dynamin-related protein involved inmitochondrial DNA maintenance. Biochem Biophys Res Commun 251: 720-726.
37. Pelloquin L, Belenguer P, Menon Y, Gas N, Ducommun B. 1999. Fission yeast Msp1 is a mitochondrial dynamin-related protein. J Cell Sci 112: 4151-4161.
38. Sambrook J, Russell DW. 2001. Molecular cloning: A laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Sarzi E, Bourdon A, Chretien D, Zarhrate M, Corcos J, Slama A, Cormier- Daire V, de Lonlay P, Munnich A, Rotig A. 2007. Mitochondrial DNA depletion is a prevalent cause of multiple respiratory chain deficiency in childhood. J Pediatr 150: 531-536.
40. Song Z, Chen H, Fiket M, Alexander C, Chan DC. 2007. OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J Cell Biol 178: 749-755.
41. Spinazzola A, Zeviani M. 2009. Disorders from perturbations of nuclear- mitochondrial intergenomic cross-talk. J Intern Med 265: 174-192.
42. Thanbichler M, Shapiro L. 2006. Chromosome organization and segregation in bacteria. J Struct Biol 156: 292-303.
43. Wong ED, Wagner JA, Scott SV, Okreglak V, Holewinske TJ, Cassidy-Stone A, Nunnari J. 2003. The intramitochondrial dynamin-related GTPase, Mgm1p, is a component of a protein complex that mediates mitochondrial fusion. J Cell Biol 160: 303-311.
44. Zanna C, Ghelli A, Porcelli AM, Karbowski M, Youle RJ, Schimpf S, Wissinger B, Pinti M, Cossarizza A, Vidoni S, et al. 2008. OPA1 mutations associated with dominant optic atrophy impair oxidative phosphorylation and mitochondrial fusion. Brain 131: 352-367.