A novel recurrent mitochondrial DNA mutation in ND3 gene is associated with isolated complex I deficiency causing leigh syndrome and dystonia

American Journal of Medical Genetics, Part A

Volumn 143, Issue 1, 2007, Pages 33-41

  Sarzi, Emmanuelle ^a   Brown, Michael D ^b   Lebon, Sophie ^a   Chretien, Dominique ^a   Munnich, Arnold ^a   Rotig, Agnès ^a   Procaccio, Vincent ^c,d  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

^b MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Complex I; Dystonia; Leigh syndrome; Mitochondrial genome; mtDNA; ND3

Indexed keywords

ALANINE; MITOCHONDRIAL DNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); THREONINE;

ADULT; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; DYSTONIA; FEMALE; GENE FUNCTION; GENE MUTATION; GENETIC ASSOCIATION; GENOTYPE PHENOTYPE CORRELATION; HETEROPLASMY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYBRID CELL; HYDROPHILICITY; HYDROPHOBICITY; INFANT; LEIGH DISEASE; LYMPHOBLASTOID CELL; MALE; MITOCHONDRIAL GENE; MUSCLE TISSUE; ND3 GENE; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PRIORITY JOURNAL; RESPIRATORY CHAIN;

ADULT; AMINO ACID SEQUENCE; BASE SEQUENCE; CHILD; CHILD, PRESCHOOL; DNA MUTATIONAL ANALYSIS; DNA, MITOCHONDRIAL; DYSTONIA; ELECTRON TRANSPORT COMPLEX I; FEMALE; HUMANS; INFANT; LEIGH DISEASE; MALE; MOLECULAR SEQUENCE DATA; MUTATION; PEDIGREE; PROTEINS;

EID: 33846008430     PISSN: 15524825     EISSN: 15524833     Source Type: Journal    
DOI: 10.1002/ajmg.a.31565     Document Type: Article

References (37)

1. Alves PC, Videira A. 1998. The membrane domain of complex I is not assembled in the stopper mutant E35 of Neurospora. Biochem Cell Biol 76:139-143.
2. Bannwarth S, Procaccio V, Paquis-Flucklinger V. 2005. Surveyor nuclease: A new strategy for a rapid identification of heteroplasmic mitochondrial DNA mutations in patients with respiratory chain defects. Hum Mutat 25:575-582.
3. Brandon MC, Lott MT, Nguyen KC, Spolim S, Navathe SB, Baldi P, Wallace DC. 2005. MITOMAP: A human mitochondrial genome database-2004 update. Nucleic Acids Res 33:D611-D613.
4. Brink J, Hovmoller S, Ragan CI, Cleeter MW, Boekema EJ, van Bruggen EF. 1987. The structure of NADH:ubiquinone oxidoreductase from beef-heart mitochondria. Crystals containing an octameric arrangement of iron-sulphur protein fragments. Eur J Biochem 166:287-294.
5. Bykhovskaya Y, Mengesha E, Wang D, Yang H, Estivill X, Shohat M, Fischel-Ghodsian N. 2004. Phenotype of non-syndromic deafness associated with the mitochondrial A1555G mutation is modulated by mitochondrial RNA modifying enzymes MTO1 and GTPBP3. Mol Genet Metab 83:199-206.
6. Chol M, Lebon S, Benit P, Chretien D, de Lonlay P, Goldenberg A, Odent S, Hertz-Pannier L, Vincent-Delorme C, Cormier-Daire V, Rustin P, Rotig A, Munnich A. 2003. The mitochondrial DNA G13513A MELAS mutation in the NADH dehydrogenase 5 gene is a frequent cause of Leigh-like syndrome with isolated complex I deficiency. J Med Genet 40:188-191.
7. Chomyn A, Cleeter MW, Ragan CI, Riley M, Doolittle RF, Attardi G. 1986. URF6, last unidentified reading frame of human mtDNA, codes for an NADH dehydrogenase subunit. Science 234:614-618.
8. Crimi M, Papadimitriou A, Galbiati S, Palamidou P, Fortunato F, Bordoni A, Papandreou U, Papadimitriou D, Hadjigeorgiou GM, Drogari E, Bresolin N, Comi GP. 2004. A new mitochondrial DNA mutation in ND3 gene causing severe Leigh syndrome with early lethality. Pediatr Res 55:842-846.
9. Fischel-Ghodsian N, Kopke RD, Ge X. 2004. Mitochondrial dysfunction in hearing loss. Mitochondrion 4:675-694.
10. Gigarel N, Ray PF, Burlet P, Frydman N, Royer G, Lebon S, Bonnefont JP, Frydman R, Munnich A, Steffann J. 2005. Single cell quantification of the 8993T>G NARP mitochondrial DNA mutation by fluorescent PCR. Mol Genet Metab 84:289-292.
11. Guenebaut V, Schlitt A, Weiss H, Leonard K, Friedrich T. 1998. Consistent structure between bacterial and mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 276:105-112.
12. Hirst J, Carroll J, Fearnley IM, Shannon RJ, Walker JE. 2003. The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim Biophys Acta 1604:135-150.
13. Kirby DM, Kahler SG, Freckmann ML, Reddihough D, Thorburn DR. 2000. Leigh disease caused by the mitochondrial DNA G14459A mutation in unrelated families. Ann Neurol 48:102-104.
14. Kirby DM, Boneh A, Chow CW, Ohtake A, Ryan MT, Thyagarajan D, Thorburn DR. 2003. Low mutant load of mitochondrial DNA G13513A mutation can cause Leigh's disease. Ann Neurol 54:473-478.
15. Kirby DM, McFarland R, Ohtake A, Dunning C, Ryan MT, Wilson C, Ketteridge D, Turnbull DM, Thorburn DR, Taylor RW. 2004a. Mutations of the mitochondrial ND1 gene as a cause of MELAS. J Med Genet 41:784-789.
16. Kirby DM, Salemi R, Sugiana C, Ohtake A, Parry L, Bell KM, Kirk EP, Boneh A, Taylor RW, Dahl HH, Ryan MT, Thorburn DR. 2004b. NDUFS6 mutations are a novel cause of lethal neonatal mitochondrial complex I deficiency. J Clin Invest 114:837-845.
17. Lebon S, Chol M, Benit P, Mugnier C, Chretien D, Giurgea I, Kern I, Girardin E, Hertz-Pannier L, de Lonlay P, Rotig A, Rustin P, Munnich A. 2003. Recurrent de novo mitochondrial DNA mutations in respiratory chain deficiency. J Med Genet 40:896-899.
18. Leshinsky-Silver E, Lev D, Tzofi-Berrnan Z, Cohen S, Saada A, Yanoov-Sharav M, Gilad E, Lerman-Sagie T. 2005. Fulminant neurological deterioration in a neonate with Leigh syndrome due to a maternally transmitted missense mutation in the mitochondrial ND3 gene. Biochem Biophys Res Commun 334:582-587.
19. Letellier T, Heinrich R, Malgat M, Mazat JP. 1994. The kinetic basis of threshold effects observed in mitochondrial diseases: A systemic approach. Biochemical J 302:171-174.
20. Loeffen J, Elpeleg O, Smeitink J, Smeets R, Stockler-Ipsiroglu S, Mandel H, Sengers R, Trijbels F, van den Heuvel L. 2001. Mutations in the complex I NDUFS2 gene of patients with cardiomyopathy and encephalomyopathy. Ann Neurol 49:195-201.
21. Malgat M, Letellier T Jouaville SL, Mazat JP. 1995. Value of control theory in the study of cellular metabolism-Biomedical implications. J Biol Syst 3:165-175.
22. McFarland R, Kirby DM, Fowler KJ, Ohtake A, Ryan MT, Amor DJ, Fletcher JM, Dixon JW, Collins FA, Turnbull DM, Taylor RW, Thorburn DR. 2004. De novo mutations in the mitochondrial ND3 gene as a cause of infantile mitochondrial encephalopathy and complex I deficiency. Ann Neurol 55:58-64.
23. Mitchell AL, Elson JL, Howell N, Taylor RW, Turnbull DM. 2006. Sequence variation in mitochondrial complex I genes: Mutation or polymorphism? J Med Genet 43:175-179.
24. Rahman S, Poulton J, Marchington D, Suomalainen A. 2001. Decrease of 3243 A→G mtDNA mutation from blood in MELAS syndrome: A longitudinal study. Am J Hum Genet 68:238-240.
25. Rubio-Gozalbo ME, Sengers RC, Trijbels JM, Doesburg WH, Janssen AJ, Verbeek AL, Smeitink JA. 2000. A prognostic index as diagnostic strategy in children suspected of mitochondriocytopathy. Neuropediatrics 31:114-121.
26. Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC. 2004. Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303:223-226.
27. Rustin P, Chretien D, Bourgeron T, Gerard B, Rötig A, Saudubray JM, Munnich A. 1994. Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 228:35-51.
28. Shoffner JM, Brown MD, Stugard C, Jun AS, Pollok S, Haas RH, Kaufman A, Koontz D, Kim Y, Graham JR, et al. 1995. Leber's hereditary optic neuropathy plus dystonia is caused by a mitochondrial DNA point mutation in a complex I subunit. Ann Neurol 38:163-169.
29. Sudo A, Honzawa S, Nonaka I, Goto Y. 2004. Leigh syndrome caused by mitochondrial DNA G13513A mutation: Frequency and clinical features in Japan. J Hum Genet 49:92-96.
30. Taylor RW, Singh-Kler R, Hayes CM, Smith PE, Turnbull DM. 2001. Progressive mitochondrial disease resulting from a novel missense mutation in the mitochondrial DNA ND3 gene. Ann Neural 50:104-107.
31. Taylor RW, Morris AA, Hutchinson M, Turnbull DM. 2002. Leigh disease associated with a novel mitochondrial DNA ND5 mutation. Eur J Hum Genet 10:141-144.
32. Triepels RH, Van Den Heuvel LP, Trijbels JM, Smeitink JA. 2001. Respiratory chain complex I deficiency. Am J Med Genet 106:37-45.
33. Trounce I, Neill S, Wallace DC. 1994. Cytoplasmic transfer of the mtDNA nt 8993 T→G (ATP6) point mutation associated with Leigh syndrome into mtDNA-less cells demonstrates cosegregation with a decrease in state III respiration and ADP/O ratio. Proc Natl Acad Sci USA 91:8334-8338.
34. Trounce IA, Kim YL, Jun AS, Wallace DC. 1996. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol 264:484-509.
35. Ugalde C, Triepels RH, Coenen MJ, van den Heuvel LP, Smeets R, Uusimaa J, Briones P, Campistol J, Majamaa K, Smeitink JA, Nijtmans LG. 2003. Impaired complex I assembly in a Leigh syndrome patient with a novel missense mutation in the ND6 gene. Ann Neurol 54:665-669.
36. Von Kleist-Retzow JC, Cormier-Daire V, de Lonlay P, Parfait B, Chretien D, Rustin P, Feingold J, Rötig A, Munnich A. 1998. A high rate (20%-30%) of parental consanguinity in cytochrome-oxidase deficiency. Am J Hum Genet 63:428-435.
37. Wallace DC, Lott MT, Procaccio V. 2006. Mitochondrial genes in degenerative diseases, cancer and aging. In: Rimoin DL, Connor JM, Pyeritz RE, Korf BR, editors. Emery and Rimoin's principles and practice of medical genetics, 5th edition. London: Churchill Livingstone (in press).