Use of transmitochondrial cybrids to assign a complex I defect to the mitochondrial DNA-encoded NADH dehydrogenase subunit 6 gene mutation at nucleotide pair 14459 that causes Leber hereditary optic neuropathy and dystonia

Molecular and Cellular Biology

Volumn 16, Issue 3, 1996, Pages 771-777

  Jun, Albert S ^a   Trounce, Ian A ^a   Brown, Michael D ^a   Shoffner, John M ^a   Wallace, Douglas C ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Dept of Genet and Molec Medicine ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

AMINO ACID SUBSTITUTION; ARTICLE; BASE MISPAIRING; CONTROLLED STUDY; DYSTONIA; ENZYME ACTIVITY; ENZYME SUBUNIT; GENE MUTATION; HEREDITARY OPTIC ATROPHY; HUMAN; HUMAN CELL; MITOCHONDRIAL RESPIRATION; PRIORITY JOURNAL;

CELL LINE, TRANSFORMED; DNA, MITOCHONDRIAL; HERPESVIRUS 4, HUMAN; HUMANS; HYBRID CELLS; MUTATION; NADH DEHYDROGENASE; OPTIC ATROPHIES, HEREDITARY;

HUMAN HERPESVIRUS 4;

EID: 0030060823     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.3.771     Document Type: Article

References (63)

1. Anderson, S., A. T. Bankier, B. G. Barrell, M. H. L. de Bruijn, A. R. Coulson, J. Drouin, I. C. Eperon, D. P. Nierlich, B. A. Roe, F. Sanger, P. H. Schreier, A. J. H. Smith, R. Staden, and I. G. Young. 1981. Sequence and organization of the human mitochandrial genome. Nature (London) 290:457-465.
2. Beal, M. F. 1992. Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann. Neurol 31:119-130.
3. Benecke, R., P. Strumper, and H. Weiss. 1992. Electron transfer complex I defect in idiopaihic dystonia. Ann Neurol. 32:683-686.
4. Berkovic, S. F., G. Karpati, S. Carpenter, and A. E. Lang. 1987. Progressive dystonia with bilateral putaminal hypodensities. Arch. Neurol. 44:1185-1187.
5. Bindoff, L. A., M. Birch-Machin, N. E. F. Cartlidge, W. D. J. Parker, and D. M. Turnbull. 1989. Mitochondrial function in Parkinson's disease. Lancet ii:49.
6. Bindoff, L. A., M. A. Birch-Machin, N. E. F. Cartlidge, W. D. J. Parker, and D. M. Turnbull. 1991. Respiratory chain abnormalities in skeletal muscle from patients with Parkinson's disease. J. Neurol. Sci. 104:203-208.
7. Blin, O., C. Desnuelle, O. Rascol, M. Borg, H. Peyro Saint Paul, J. P. Azulay, F. Bille, D. Figarella, F. Coulom, J. F. Pellissier, J. L. Montastruc, M. Chatel, and G. Serratrice. 1994. Mitochondrial respiratory failure in skeletal muscle from patients with Parkinson's disease and multiple system atrophy. J. Neurol. Sci. 125:95-101.
8. Brown, M. D., and D. C. Wallace. 1994. Spectrum of mitochondrial DNA mutations in Leber's hereditary optic neuropathy. Clin. Neurosci. 2:138-145
9. Bruyn, G. W., G. T. A. M. Bots, L. N. Went, and P. J. J. M. Klinkhamer. 1992 Hereditary spastic dystonia with Leber's hereditary optic neuropathy: neuropathological findings. J. Neurol. Sci. 113:55-61.
10. Bruyn, G. W., G. J. Vielvoye, and L. N. Went. 1991. Hereditary spastic dystonia: a new mitochondrial encephalopathy? J. Neurol. Sci. 103:195-202.
11. Chomyn, A., M. W. J. Cleeter, C. I. Ragan, M. Riley, R. F. Doolittle, and G. Attardi. 1986. URF 6, last unidentified reading frame of human mtDNA, codes for an NADH dehydrogenase subunit. Science 234:614-618.
12. Lys mutation causing myoclonic epilepsy and ragged red fibers Am. J. Hum. Genet. 54:966-974.
13. Chomyn, A., G. Meola, N. Bresolin, S. T. Lai, G. Scarlato, and G. Attardi. 1991. In vitro genetic transfer of protein synthesis and respiration defects to mitochondrial DNA-less cells with myopathy-patient mitochondria. Mol. Cell. Biol. 11:2236-2244.
14. Fearnley, I. M., and J. E. Walker. 1992. Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins. Biochim. Biophys. Acta 1140:105-134
15. Goto, Y., I. Nonaka, and S. Horai. 1990. A mutation in the tRNA(Leu) (UUR) gene associated with the MELAS subgroup of mitochondrial encephalomyopathies. Nature (London) 348:651-653.
16. Gregoire, M., R. Morais, M. Quilliam, and D. Gravel. 1984. On auxotrophy for pyrimidines of respiration-deficient chick embryo cells. Eur. J. Biochem 142:49-55.
17. Hayashi, J.-I., S. Ohta, A. Kikuchi, M. Takemitsu, Y.-I. Goto, and I. Nonaka. 1991. Introduction of disease-related mitochondrial DNA deletions into HeLa cells lacking mitochondrial DNA results in mitochondrial dysfunction. Proc. Natl. Acad Sci. USA 88:10614-10018.
18. Heinrich, H., J. E. Azevedo, and S. Werner. 1992. Characterization of the 9.5 kDa ubiquinone-binding protein of NADH:ubiquinone oxidoreductase (complex I) from Neurospora crassa. Biochemistry 31:11420-11424.
19. Heinrich, H., and S. Werner. 1992. Identification of the ubiquinone-binding site of NADH:ubiquinone oxidoreductase (complex I) from Neurospora crassa. Biochemistry 31:11413-11419.
20. Howell, N., I. Kubacka, M. Xu, and D. A. McCullough. 1991. Leber hereditary optic neuropathy: involvement of the mitochondrial ND1 gene and evidence for an intragenic suppressor mutation. Am. J. Hum. Genet. 48:935-942.
21. Ichiki, T., M. Tanaka, M. Nishikimi, H. Suzuki, T. Ozawa, M. Kobayasbi, and Y. Wada. 1988. Deficiency of subunits of complex I and mitochondrial encephalomyopathy Ann. Neurol. 23:287-294.
22. Johns, D. R., K. L. Heher, N. R. Miller, and K. H. Smith. 1993 Leber's hereditary optic neuropathy. Clinical manifestations of the 14484 mutation. Arch. Ophthalmol. 111:495-498.
23. Johns, D. R., M. J. Neufeld, and R. D. Park. 1992. An ND-6 mitochondrial DNA mutation associated with Leber hereditary optic neuropathy. Biochem Biophys. Res. Commun. 187:1551-1557.
24. Jun, A. S., M. D. Brown, and D. C. Wallace. 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.
25. King, M. P., and G. Attardi. 1989. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246:500-503.
26. Leu(UUR) mutation associated with mitochondrial myopathy, encephalopathy, lactic acidosis, and strokelike episodes. Mol. Cell. Biol. 12:480-490.
27. Larsson, N.-G., O. Andersen, E. Holme, A. Oldfors, and J. Wahlstrom. 1991. Leber's hereditary optic neuropathy and complex I deficiency in muscle. Ann Neurol. 30:701-708
28. Letellier, T., R. Heinrich, M. Malgat, and J.-P. Mazat. 1994. The kinetic basis of threshold effects observed in mitochondrial diseases: a systemic approach. Biochem. J. 302:171-174
29. Levy, J. A., M. Virolainen, and V. Defendi. 1968. Human lymphoblastoid lines from lymph node and spleen. Cancer 22:517-524.
30. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
31. Mackey, D., and N. Howell. 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.
32. Majander, A., K. Huoponen, M.-L. Savontaus, E. Nikoskelainen, and M. Wikstrom. 1991. Electron transfer properties of NADH:ubiquinone reductase in the ND1/3460 and the ND4/11778 mutations of the Leber hereditary optic neuroretinopathy (LHON). FEBS Lett. 292:289-292.
33. Malgat, M., T. Letellier, S. L. Jouaville, and J.-P. Mazat. 1995. Value of control theory in the study of cellular metabolism - biomedical implications. J. Biol. Syst. 3:165-175.
34. Marsden, C. D., A. E. Lang, N. P. Quinn, W. I. McDonald, A. Abdallat, and S. Nimri. 1986 Familial dystonia and visual failure with striatal CT lucencies. J. Neurol Neurosurg. Psychiatry 49:500-509.
35. Mizuno, Y., S. Ohta, M. Tanaka, S. Takayima, K. Suzuki, T. Sato, H. Oya, T. Ozawa, and Y. Kagawa. 1989. Deficiencies in complex I subunits of the respiratory chain in Parkinson's disease Biochem Biophys. Res. Commun 163:1450-1455.
36. Novotny, E. J., G. Singh, D. C. Wallace, L. J. Dorfman, A. Louis, R. L. Sogg, and L. Steimnan. 1986. Leber's disease and dystonia: a mitochondrial disease. Neurology 36:1053-1060.
37. Parker, W. D., S. J. Boyson, A. S. Luder, and J. K. Parks. 1990. Evidence for a defect in NADH.ubiquinone oxidoreductase (complex I) in Huntington's disease. Neurology 40:1231-1234
38. Parker, W. D., S. J. Boyson, and J. K. Parks. 1989 Abnormalities of the electron transport chain in idiopathic Parkinson's disease. Ann. Neurol. 26:719-723.
39. Parker, W. D., C. A. Oley, and J. K. Parks. 1989. A defect in mitochondrial electron-transport activity (NADH-coenzyme O oxidoreductase) in Leber's hereditary optic neuropathy. N. Engl. J. Med. 320:1331-1333.
40. Pilkington, S. J., J. M. Arizmendi, I. M. Fearnley, M. J. Runswick, J. M. Skehel, and J. E. Walker. 1993. Structural organization of complex I from bovine mitochondria. Biochem. Soc. Trans. 21:26-31.
41. Schapira, A. H. V., J. M. Cooper, D. Dexter, J. B. Clark, P. Jenner, and C. D. Marsden. 1990. Mitochondrial complex I deficiency in Parkinson's disease. J. Neurochem. 54:823-827.
42. Schapira, A. H. V., J. M. Cooper, D. Dexter, P. Jenner, J. B. Clark, and C. D. Marsden. 1989. Mitochondrial complex I deficiency in Parkinson's disease Lancet i:1269.
43. Schapira, A. H. V., V. M. Mann, J. M. Cooper, D. Dexter, S. E. Daniel, P. Jenner, J. B. Clark, and C. D. Marsden. 1990. Anatomic and disease specificity of NADH CoQ1 reductase (complex I) deficiency in Parkinson's disease. J. Neurochem 55:2142-2145.
44. Schapira, A. H. V., J. A. Morgan-Hughes, M. J. W. Cleeter, J. M. Cooper, S. D. Patel, C. I. Ragan, and J. B. Clark. 1988. Molecular basis of mitochondrial myopathies: polypeptide analysis in complex I-deficiency. Lancet i:500-503.
45. Schulz, J. B., and M. F. Beal. 1994. Mitochondrial dysfunction in movement disorders. Curr. Opin Neurol. 7:333-339.
46. Shoffner, J. M., M. D. Brown, C. Stugard, A. S. Jun, S. Pollock, R. H. Haas, A. Kaufman, D. Koontz, V. Kim, J. R. Graham, E. Smith, J. Dixon, and D. C. Wallace. 1995. Leber's hereditary' optic neuropathy plus dystonia is caused by a mitochondrial DNA point mutation. Ann. Neurol. 38:163-169.
47. Shoffner, J. M., and D. C. Wallace. 1994. Oxidative phosphorylation diseases and mitochondrial DNA mutations, diagnosis and treatment. Annu. Rev. Nutr. 14:535-568.
48. Shoffner, J. M., R. L. Watts, J. L. Juncos, A. Torroni, and D. C. Wallace. 1991. Mitochondrial oxidative phosphorylation defects in Parkinson's disease. Ann Neurol. 30:332-339.
49. Smith, P. R., J. M. Cooper, G. G. Govan, A. E. Harding, and A. H. V. Schapira. 1994. Platelet mitochondrial function in Leber's hereditary optic neuropathy. J. Neurol Sci. 122:80-83.
50. Suzuki, H., and T. Ozawa. 1986. An ubiquinone-binding protein in mitochondrial NADH-ubiquinone reductase (complex I). Biochem. Biophys. Res. Commun. 138:1237-1242.
51. Trounce, I. A., Y. L. Kim, A. S. Jun, and D. C. Wallace. 1996. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol 264:484-509.
52. Trounce, I. A., S. A. Neill, and D. C. Wallace. 1994. Cytoplasmic transfer of the mtDNA nt 8993 T to 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
53. Vinogradov, A. D. 1993. Kinetics, control, and mechanism of ubiquinone reduction by the mammalian respiratory chain-linked NADH-ubiquinone reductase J. Bioenerg. Biomembr. 25:367-375.
54. Wallace, D. C. 1970. A new manifestation of Leber's disease and a new explanation for the agency responsible for its unusual pattern of inheritance. Brain 93:121-132.
55. Wallace, D. C. 1992. Diseases of the mitochondrial DNA. Annu. Rev. Biochem. 61:1175-1212
56. Wallace, D. C. 1994. Mitochondrial DNA mutations in diseases of energy metabolism J. Bioenerg. Biomembr. 26:241-249.
57. Wallace, D. C. 1994. Mitochondrial DNA sequence variation in human evolution and disease. Proc Natl. Acad Sci. USA 91:8739-8746.
58. Wallace, D. C., C. L. Bunn, and J. M. Eisenstadt. 1975. Cytoplasmic transfer of chloramphenicol resistance in human tissue culture cells. J. Cell Biol. 67:174-188.
59. Wallace, D. C., J. M. Shoffner, I. Trounce, M. D. Brown, S. W. Ballinger, M. Corral-Debrinski, T. Horton, A. S. Jun, and M. L. Lett. 1995. Mitochondrial DNA mutations in human degenerative diseases and aging. Biochim. Biophys. Acta 1271:141-151.
60. Wallace, D. C., J. Yang, J. Ye, M. T. Lott, N. A. Oliver, and J. McCarthy. 1986. Computer prediction of peptide maps: assignment of polypeptides to human and mouse mitochondrial DNA genes by analysis of two-dimensional-proteolytic digest gels Am. J Hum Genet. 38:461-481.
61. Walsh, P. S., D. A. Metzger, and R. Higuchi. 1991. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material BioTechniques 10:506-513.
62. Yoneda, M., A. Chomyn, A. Martinuzzi, O. Hurko, and G. Attardi. 1992 Marked replicative advantage of human mtDNA carrying a point mutation that causes the MELAS encephatomyopathy. Proc. Natl. Acad. Sci. USA 89:11164-11168.
63. Zheng, X. X., J. M. Shoffner, A. S. Voljavec, and D. C. Wallace. 1990 Evaluation of procedures for assaying oxidative phosphorylation enzyme activities in mitochondrial myopathy muscle biopsies. Biochim. Biophys. Acta 1019:1-10