Rare primary mitochondrial DNA mutations and probable synergistic variants in leber's hereditary optic neuropathy

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Achilli, Alessandro ^a   Iommarini, Luisa ^b   Olivieri, Anna ^c   Pala, Maria ^c   Hooshiar Kashani, Baharak ^c   Reynier, Pascal ^d,e,f   La Morgia, Chiara ^b   Valentino, Maria Lucia ^b   Liguori, Rocco ^b   Pizza, Fabio ^b   Barboni, Piero ^b,g   Sadun, Federico ^h   de Negri, Anna Maria ⁱ   Zeviani, Massimo ^j   Dollfus, Helene ^k   Moulignier, Antoine ^l   Ducos, Ghislaine ^m   Orssaud, Christophe ⁿ   Bonneau, Dominique ^d,e,f   Procaccio, Vincent ^d,e,f   Leo Kottler, Beate ^o   Fauser, Sascha ^p   Wissinger, Bernd ^o   Amati Bonneau, Patrizia ^d,f   Torroni, Antonio ^c   Carelli, Valerio ^b   more..

^a UNIVERSITY OF PERUGIA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

^d INSERM   (France)

^e UNIVERSITÉ D'ANGERS   (France)

^f ANGERS UNIVERSITY HOSPITAL   (France)

^g Studio Oculistico d'Azeglio   (Italy)

^h Ospedale San Giovanni Evangelista   (Italy)

ⁱ Azienda San Camillo Forlanini   (Italy)

^j DEPARTMENT OF NEUROSURGERY   (Italy)

^k UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^l Service de Neurologie   (France)

^m Saint Jean Languedoc Clinic   (France)

ⁿ HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^o UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^p UNIVERSITY OF COLOGNE   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; AMINO ACID; CYTOSINE; GUANINE; MITOCHONDRIAL DNA;

ARTICLE; FRANCE; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC VARIABILITY; GERMANY; HAPLOTYPE; HUMAN; ITALY; LEBER HEREDITARY OPTIC NEUROPATHY; MITOCHONDRIAL GENOME; NUCLEOTIDE SEQUENCE; PHYLOGENY; POINT MUTATION;

AMINO ACID SEQUENCE; BASE SEQUENCE; CONSERVED SEQUENCE; DNA, MITOCHONDRIAL; FAMILY; HUMANS; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; OPTIC ATROPHY, HEREDITARY, LEBER; PHYLOGENY; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY;

EID: 84864554107     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042242     Document Type: Article

References (62)

1. Carelli V, Ross-Cisneros FN, Sadun AA, ((2004)) Mitochondrial dysfunction as a cause of optic neuropathies. Prog Retin Eye Res 23:: 53--89.
2. Newman NJ (2005) Leber's hereditary optic neuropathy. In: Miller NR, Newman NJ, Valerie B, Kerrison JB (eds). Walsh and Hoyt's Clinical Neuro-Ophthalmology. Baltimore: Lippincott Williams & Wilkins. 482-484.
3. Yu-Wai-Man P, Griffiths PG, Chinnery PF, ((2011)) Mitochondrial optic neuropathies- Disease mechanisms and therapeutic strategies. Prog Retin Eye Res 30:: 81--114.
4. Torroni A, Petrozzi M, D'Urbano L, Sellitto D, Zeviani M, et al. ((1997)) Haplotype and phylogenetic analyses suggest that one European-specific mtDNA background plays a role in the expression of Leber hereditary optic neuropathy by increasing the penetrance of the primary mutations 11778 and 14484. Am J Hum Genet 60:: 1107--1121.
5. Carelli V, Achilli A, Valentino ML, Rengo C, Semino O, et al. ((2006)) Haplogroup effects and recombination of mitochondrial DNA: novel clues from the analysis of Leber hereditary optic neuropathy pedigrees. Am J Hum Genet 78:: 564--574.
6. Hudson G, Carelli V, Spruijt L, Gerards M, Mowbray C, et al. ((2007)) Clinical expression of Leber hereditary optic neuropathy is affected by the mitochondrial DNA-haplogroup background. Am J Hum Genet 81:: 228--233.
7. Chinnery PF, Brown DT, Andrews RM, Singh-Kler R, Riordan-Eva P, et al. ((2001)) The mitochondrial ND6 gene is a hot spot for mutations that cause Leber's hereditary optic neuropathy. Brain 124:: 209--218.
8. Valentino ML, Barboni P, Ghelli A, Bucchi L, Rengo C, et al. ((2004)) The ND1 gene of complex I is a mutational hot spot for Leber's hereditary optic neuropathy. Ann Neurol 56:: 631--641.
9. Howell N, Bogolin C, Jamieson R, Marenda DR, Mackey DA, ((1998)) mtDNA mutations that cause optic neuropathy: how do we know? Am J Hum Genet 62:: 196--202.
10. Luberichs J, Leo-Kottler B, Besch D, Fauser S, ((2002)) A mutational hot spot in the mitochondrial ND6 gene in patients with Leber's hereditary optic neuropathy. Graefes Arch Clin Exp Ophthalmol 240:: 96--100.
11. Valentino ML, Avoni P, Barboni P, Pallotti F, Rengo C, et al. ((2002)) Mitochondrial DNA nucleotide changes C14482G and C14482A in the ND6 gene are pathogenic for Leber's hereditary optic neuropathy. Ann Neurol 51:: 774--778.
12. Wissinger B, Besch D, Baumann B, Fauser S, Christ-Adler M, et al. ((1997)) Mutation analysis of the ND6 gene in patients with Lebers hereditary optic neuropathy. Biochem Biophys Res Commun 234:: 511--515.
13. Besch D, Leo-Kottler B, Zrenner E, Wissinger B, ((1999)) Leber's hereditary optic neuropathy: clinical and molecular genetic findings in a patient with a new mutation in the ND6 gene. Graefes Arch Clin Exp Ophthalmol 237:: 745--752.
14. Fauser S, Leo-Kottler B, Besch D, Luberichs J, ((2002)) Confirmation of the 14568 mutation in the mitochondrial ND6 gene as causative in Leber's hereditary optic neuropathy. Ophthalmic Genet 23:: 191--197.
15. Kim JY, Hwang JM, Park SS, ((2002)) Mitochondrial DNA C4171A/ND1 is a novel primary causative mutation of Leber's hereditary optic neuropathy with a good prognosis. Ann Neurol 51:: 630--634.
16. Cui SL, Yang L, Wang W, Shang J, Zhang XJ, ((2007)) Rare primary mtDNA mutations in Leber hereditary optic neuropathy. Ophthalmology in China 16:: 382--385.
17. Yang J, Zhu Y, Chen L, Zhang H, Tong Y, et al. ((2009)) Novel A14841G mutation is associated with high penetrance of LHON/C4171A family. Biochem Biophys Res Comm 386:: 693--696.
18. Brown MD, Zhadanov S, Allen JC, Hosseini S, Newman NJ, et al. ((2001)) Novel mtDNA mutations and oxidative phosphorylation dysfunction in Russian LHON families. Hum Genet 109:: 33--39.
19. Zhang AM, Zou Y, Guo X, Jia X, Zhang Q, et al. ((2009)) Mitochondrial DNA mutation m.3635G>A may be associated with Leber hereditary optic neuropathy in Chinese. Biochem Biophys Res Commun 386:: 392--395.
20. Yang J, Zhu Y, Tong Y, Chen L, Liu L, et al. ((2009)) Confirmation of the mitochondrial ND1 gene mutation G3635A as a primary LHON mutation. Biochem Biophys Res Commun 386:: 50--54.
21. Jia X, Li S, Wang P, Guo X, Zhang Q, ((2010)) mtDNA m.3635G>A may be classified as a common primary mutation for Leber hereditary optic neuropathy in the Chinese population. Biochem Biophys Res Commun 403:: 237--241.
22. Brown MD, Torroni A, Reckord CL, Wallace DC, ((1995)) Phylogenetic analysis of Leber's hereditary optic neuropathy mitochondrial DNA's indicates multiple independent occurrences of the common mutations Hum Mutat. 6:: 311--325.
23. Brown MD, Starikovskaya E, Derbeneva O, Hosseini S, Allen JC, et al. ((2002)) The role of mtDNA background in disease expression: a new primary LHON mutation associated with Western Eurasian haplogroup. Hum Genet 110:: 130--138.
24. Abu-Amero KK, Bosley TM, ((2006)) Mitochondrial abnormalities in patients with LHON-like optic neuropathies. Invest Ophthalmol Vis Sci 47:: 4211--4220.
25. Fraser JA, Biousse V, Newman NJ, ((2010)) The neuro-ophthalmology of mitochondrial disease.Surv Ophthalmol. 55:: 299--334.
26. MITOMAP. A Human Mitochondrial Genome Database. Available: http://www.mitomap.org. Accessed 2012 Mar 2.
27. Fauser S, Luberichs J, Besch D, Leo-Kottler B, ((2002)) Sequence analysis of the complete mitochondrial genome in patients with Leber's hereditary optic neuropathy lacking the three most common pathogenic DNA mutations. Biochem Biophys Res Commun 295:: 342--347.
28. Jun AS, Brown MD, Wallace DC, ((1994)) A mitochondrial DNA mutation at nucleotide pair 14459 of the NADH dehydrogenase subunit 6 gene associated with maternally inherited Leber hereditary optic neuropathy and dystonia. Proc Natl Acad Sci USA 91:: 6206--6210.
29. Novotny EJ Jr, Singh G, Wallace DC, Dorfman LJ, Louis A, et al. ((1986)) Leber's disease and dystonia: a mitochondrial disease. Neurology 36:: 1053--1060.
30. Kirby DM, Kahler SG, Freckmann M-L, Reddihough D, Thorburn DR, ((2000)) Leigh disease caused by the mitochondrial DNA G14459A mutation in unrelated families. Ann Neurol 48:: 102--104.
31. Valentino ML, Barboni P, Rengo C, Achilli A, Torroni A, et al. ((2006)) The 13042G A/ND5 mutation in mtDNA is pathogenic and can be associated also with a prevalent ocular phenotype. J Med Genet 43:: e38.
32. Naini AB, Lu J, Kaufmann P, Bernstein RA, Mancuso M, et al. ((2005)) Novel mitochondrial DNA ND5 mutation in a patient with clinical features of MELAS and MERRF. Arch Neurol 62:: 473--476.
33. Blok MJ, Spruijt L, de Coo IF, Schoonderwoerd K, Hendrickx A, et al. ((2007)) Mutations in the ND5 subunit of complex I of the mitochondrial DNA are a frequent cause of oxidative phosphorylation disease. J Med Genet 44:: e74.
34. Achilli A, Rengo C, Magri C, Battaglia V, Olivieri A, et al. ((2004)) The molecular dissection of mtDNA haplogroup H confirms that the Franco-Cantabrian glacial refuge was a major source for the European gene pool. Am J Hum Genet 75:: 910--918.
35. van Oven M, Kayser M, ((2009)) Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum Mutat 30:: E386--394.
36. Uusimaa J, Finnilä S, Remes AM, Rantala H, Vainionpää L, et al. ((2004)) Molecular epidemiology of childhood mitochondrial encephalomyopathies in a Finnish population: sequence analysis of entire mtDNA of 17 children reveals heteroplasmic mutations in tRNAArg, tRNAGlu, and tRNALeu(UUR) genes. Pediatrics 114:: 443--450.
37. Lertrit P, Noer AS, Jean-Francois MJ, Kapsa R, Dennett X, et al. ((1992)) A new disease-related mutation for mitochondrial encephalopathy lactic acidosis and strokelike episodes (MELAS) syndrome affects the ND4 subunit of the respiratory complex I. Am J Hum Genet. 51:: 457--468.
38. Zhao F, Guan M, Zhou X, Yuan M, Liang M, et al. ((2009)) Leber's hereditary optic neuropathy is associated with mitochondrial ND6 T14502C mutation. Biochem Biophys Res Commun 389:: 466--472.
39. Zhang S, Wang L, Hao Y, Wang P, Hao P, et al. ((2008)) T14484C and T14502C in the mitochondrial ND6 gene are associated with Leber's hereditary optic neuropathy in a Chinese family. Mitochondrion 8:: 205--210.
40. Zhang J, Zhou X, Zhou J, Li C, Zhao F, et al. ((2010)) Mitochondrial ND6 T14502C variant may modulate the phenotypic expression of LHON-associated G11778A mutation in four Chinese families. Biochem Biophys Res Commun 399:: 647--653.
41. Tarnopolsky MA, Baker SK, Myint T, Maxner CE, Robitaille J, et al. ((2004)) Clinical variability in maternally inherited Leber Hereditary Optic Neuropathy with the G14459A mutation. Am J Med Genet 124A:: 372--376.
42. Gropman A, Chen TJ, Perng CL, Krasnewich D, Chernoff E, et al. ((2004)) Variable clinical manifestation of homoplasmic G14459A mitochondrial DNA mutation. Am J Med Genet 124A:: 377--382.
43. Ferré M, Bonneau D, Milea D, Chevrollier A, Verny C, et al. ((2009)) Molecular screening of 980 cases of suspected hereditary optic neuropathy with a report on 77 novel OPA1 mutations. Hum Mutat 30:: E692--705.
44. Olivieri A, Achilli A, Pala M, Battaglia V, Fornarino S, et al. ((2006)) The mtDNA legacy of the Levantine Early Upper Palaeolithic in Africa. Science 314:: 1767--1770.
45. Riordan-Eva P, Sanders MD, Govan GG, Sweeney MG, Da Costa J, et al. ((1995)) The clinical features of Leber's hereditary optic neuropathy defined by the presence of a pathogenic mitochondrial DNA mutation. Brain 118:: 319--337.
46. Brown MD, Allen JC, Van Stavern GP, Newman NJ, Wallace DC, ((2001)) Clinical, genetic, and biochemical characterization of a Leber hereditary optic neuropathy family containing both the 11778 and 14484 primary mutations. Am J Med Genet 104:: 331--228.
47. Howell N, Miller NR, Mackey DA, Arnold A, Herrnstadt C, et al. ((2002)) Lightning strikes twice: Leber hereditary optic neuropathy families with two pathogenic mtDNA mutations. J Neuroophthalmol 22:: 262--269.
48. Vergani L, Martinuzzi A, Carelli V, Cortelli P, Montagna P, et al. ((1995)) MtDNA mutations associated with Leber's hereditary optic neuropathy: studies on cytoplasmic hybrid (cybrid) cells. Biochem Biophys Res Commun 210:: 880--888.
49. Efremov RG, Baradaran R, Sazanov LA, ((2010)) The architecture of respiratory complex I. Nature. 465:: 441--445.
50. Hunte C, Zickermann V, Brandt U, ((2010)) Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science. 329:: 448--451.
51. Carelli V, Ghelli A, Ratta M, Bacchilega E, Sangiorgi S, et al. ((1997)) Leber's hereditary optic neuropathy: biochemical effect of 11778/ND4 and 3460/ND1 mutations and correlation with the mitochondrial genotype. Neurology 48:: 1623--1632.
52. Carelli V, Ghelli A, Bucchi L, Montagna P, De Negri A, et al. ((1999)) Biochemical features of mtDNA 14484 (ND6/M64V) point mutation associated with Leber's hereditary optic neuropathy. Ann Neurol 45:: 320--328.
53. Gonzalez-Halphen D, Ghelli A, Iommarini L, Carelli V, Esposti MD, ((2011)) Mitochondrial complex I and cell death: a semi-automatic shotgun model. Cell Death Dis 2:: e222.
54. Pala M, Olivieri A, Achilli A, Accetturo M, Metspalu E, et al. ((2012)) Mitochondrial DNA signals of Late Glacial re-colonisation of Europe from Near Eastern refugia. Am J Hum Genet 90:: 915--924.
55. Mackey D, Howell N, ((1992)) A variant of Leber hereditary optic neuropathy characterized by recovery of vision and by an unusual mitochondrial genetic etiology. Am J Hum Genet 51:: 1218--1228.
56. Ji F, Sharpley MS, Derbeneva O, Alves LS, Qian P, et al. ((2012)) Mitochondrial DNA variant associated with Leber hereditary optic neuropathy and high-altitude Tibetans. Proc Natl Acad Sci U S A 109:: 7391--7396.
57. Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, et al. ((1999)) Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet 23:: 147.
58. La Morgia C, Achilli A, Iommarini L, Barboni P, Pala M, et al. ((2008)) Rare mtDNA variants in Leber hereditary optic neuropathy families with recurrence of myoclonus. Neurology 70:: 762--770.
59. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. ((2010)) A method and server for predicting damaging missense mutations. Nat Methods 7:: 248--249.
60. Kumar P, Henikoff S, Ng PC, ((2009)) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protocols 4:: 1073--1081.
61. Calabrese R, Capriotti E, Fariselli P, Martelli PL, Casadio R, ((2009)) Functional annotations improve the predictive score of human disease-related mutations in proteins. Hum Mutat 30:: 1237--1244.
62. PROVEAN. Protein Variation Effect Analyzer. Available: http://provean.jcvi.org/index.php. Accessed 2012 Jun 2.