Mutations in cytochrome c oxidase subunit VIa cause neurodegeneration and motor dysfunction in Drosophila

Genetics

Volumn 176, Issue 2, 2007, Pages 937-946

  Liu, Wensheng ^a,c   Gnanasambandam, Radhakrishnan ^b   Benjamin, Jeffery ^b   Kaur, Gunisha ^a,d   Getman, Patricia B ^a   Siegel, Alan J ^b   Shortridge, Randall D ^b   Singh, Satpal ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE;

ARTICLE; CELL TRANSFORMATION; DROSOPHILA; ENZYME ACTIVITY; GENE MUTATION; GERM LINE; MOTOR DYSFUNCTION; NERVE DEGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ANIMALS; CITRATE (SI)-SYNTHASE; DROSOPHILA; ELECTRON TRANSPORT COMPLEX IV; GERM-LINE MUTATION; HUMANS; MITOCHONDRIA; MOTOR ACTIVITY; MUTAGENESIS; NERVE DEGENERATION; PARALYSIS; PHENOTYPE;

EID: 34250716562     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.071688     Document Type: Article

References (74)

1. ABOU-SLEIMAN, P. M., M. M. MUQIT and N. W. WOOD, 2006 Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat. Rev. Neurosci. 7: 207-219.
2. AGOSTINO, A., F. INVERNIZZI, C. TIVERON, G. FAGIOLARI, A. PRELLE et al., 2003 Constitutive knockout of Surf1 is associated with high embryonic lethality, mitochondrial disease and cytochrome c oxidase deficiency in mice. Hum. Mol. Genet. 12: 399-413.
3. ASHBURNER, M., 1989 Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. ATAMNA, H., and K. BOYLE, 2006 Amyloid-beta peptide binds with heme to form a peroxidase: relationship to the cytopathologies of Alzheimer's disease. Proc. Natl. Acad. Sci. USA 103: 3381-3386.
5. BARRIENTOS, A., M. H. BARROS, I. VALNOT, A. ROTIG, P. RUSTIN et al., 2002 Cytochrome oxidase in health and disease. Gene 286: 53-63.
6. BEAL, M. F., 2000 Energetics in the pathogenesis of neurodegenerative diseases. Trends Neurosci. 23: 298-304.
7. BELLEN, H. J., R. W. LEVIS, G. LIAO, Y. HE, J. W. CARLSON et al., 2004 The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167: 761-781.
8. BENCHOUA, A., Y. TRIOULIER, D. ZALA, M. C. GAILLARD, N. LEFORT et al., 2006 Involvement of mitochondrial complex II defects in neuronal death produced by N-terminus fragment of mutated huntingtin. Mol. Biol. Cell 17: 1652-1663.
9. BHATTACHARYA, A., G. G. GU and S. SINGH, 1999 Modulation of dihydropyridine-sensitive calcium channels in Drosophila by a cAMP-mediated pathway. J. Neurobiol. 39: 491-500.
10. BHATTACHARYA, A., S. S. LAKHMAN and S. SINGH, 2004 Modulation of L-type calcium channels in Drosophila via a pituitary adenylyl cyclase-activating polypeptide (PACAP)-mediated pathway. J. Biol. Chem. 279: 37291-37297.
11. BONINI, N. M., and M. E. FORTINI, 2003 Human neurodegenerative disease modeling using Drosophila. Annu. Rev. Neurosci. 26: 627-656.
12. + channels in apoptosis. J. Membr. Biol. 209: 3-20.
13. CARROZZO, R., A. TESSA, M. E. VAZQUEZ- MEMIJE, F. PIEMONTE, C. PATRONO et al., 2001 The T9176G mtDNA mutation severely affects ATP production and results in Leigh syndrome. Neurology 56: 687-690.
14. CELOTTO, A. M., A. C. FRANK, S. W. MCGRATH, T. FERGESTAD, W. A. VAN VOORHIES et al., 2006 Mitochondrial encephalomyopathy in Drosophila. J. Neurosci. 26: 810-820.
15. CHEN, B., T. CHU, E. HARMS, J. P. GERGEN and S. STRICKLAND, 1998 Mapping of Drosophila mutations using site-specific male recombination. Genetics 149: 157-163.
16. CHINOPOULOS, C., and V. ADAM-VIZI, 2006 Calcium, mitochondria and oxidative stress in neuronal pathology. Novel aspects of an enduring theme. FEBS J. 273: 433-450.
17. CHOO, Y. S., G. V. JOHNSON, M. MACDONALD, P. J. DETLOFF and M. LESORT, 2004 Mutant huntingtin directly increases susceptibility of mitochondria to the calcium-induced permeability transition and cytochrome c release. Hum. Mol. Genet. 13: 1407-1420.
18. CHOPRA, M., and S. SINGH, 1994 Developmental temperature selectively regulates a voltage-activated potassium current in Drosophila. J. Neurobiol. 25: 119-126.
19. CHOPRA, M., G.-G. GU and S. SINGH, 2000 Mutations affecting the delayed rectifier potassium current in Drosophila. J. Neurogenet. 14: 107-123.
20. CHOVNICK, A., G. H. BALLANTYNE, D. L. BAILLIE and D. G. HOLM, 1970 Gene conversion in higher organisms: half-tetrad analysis of recombination within the rosy cistron of Drosophila melanogaster. Genetics 66: 315-329.
21. CRITTENDEN, J. R., E. M. SKOULAKIS, K. A. Han, D. KALDERON and R. L. DAVIS, 1998 Tripartite mushroom body architecture revealed by antigenic markers. Learn. Mem. 5: 38-51.
22. DAHL, H. H., 1998 Getting to the nucleus of mitochondrial disorders: identification of respiratory chain-enzyme genes causing Leigh syndrome. Am. J. Hum. Genet. 63: 1594-1597.
23. DARBIN, O., J. J. RISSO, E. CARRE, M. LONJON and D. K. NARITOKU, 2005 Metabolic changes in rat striatum following convulsive seizures. Brain Res. 1050: 124-129.
24. DARIN, N., A. OLDFORS, A. R. MOSLEMI, E. HOLME and M. TULINIUS, 2001 The incidence of mitochondrial encephalomyopathies in childhood: clinical features and morphological, biochemical, and DNA anbormalities. Ann. Neurol. 49: 377-383.
25. DEFRANCE, J. F., and D. W. MCCANDLESS, 1991 Energy metabolismin rat hippocampus during and following seizure activity. Metab. Brain Dis. 6: 83-91.
26. DIAS-SANTAGATA, D., T. A. FULGA, A. DUTTAROY and M. B. FEANY, 2007 Oxidative stress mediates tau-induced neurodegeneration in Drosophila. J. Clin. Invest. 117: 236-245.
27. DIMAURO, S., 2004 Mitochondrial diseases. Biochim. Biophys. Acta 1658: 80-88.
28. DIMAURO, S., and M. HIRANO, 2005 Mitochondrial encephalomyopathies: an update. Neuromuscul. Disord. 15: 276-286.
29. DIMAURO, S., and E. A. SCHON, 2003 Mitochondrial respiratorychain diseases. N. Engl. J. Med. 348: 2656-2668.
30. DURANTEAU, J., N. S. CHANDEL, A. KULISZ, Z. SHAO and P. T. SCHUMACKER, 1998 Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes. J. Biol. Chem. 273: 11619-11624.
31. ESPOSITO, L., J. RABER, L. KEKONIUS, F. YAN, G. Q. YU et al., 2006 Reduction in mitochondrial superoxide dismutase modulates Alzheimer's disease-like pathology and accelerates the onset of behavioral changes in human amyloid precursor protein transgenic mice. J. Neurosci. 26: 5167-5179.
32. FABRIZI, G. M., R. RIZZUTO, H. NAKASE, S. MITA, B. KADENBACH et al., 1989 Sequence of a cDNA specifying subunit VIa of human cytochrome c oxidase. Nucleic Acids Res. 17: 6409.
33. FERGUSON, M., R. J. MOCKETT, Y. SHEN, W. C. ORR and R. S. SOHAL, 2005 Age-associated decline inmitochondrial respirationandelectrontransport in Drosophila melanogaster. Biochem. J. 390: 501-511.
34. FORTINI, M. E., and N. M. BONINI, 2000 Modeling human neurodegenerative diseases in Drosophila: on a wing and a prayer. Trends Genet. 16: 161-167.
35. GANETZKY, B., 2000 Genetic analysis of ion channel dysfunction in Drosophila. Kidney Int. 57: 766-771.
36. GANETZKY, B., and C. F. WU, 1982 Indirect suppression involving behavioral mutants with altered nerve excitability in Drosophila melanogaster. Genetics 100: 597-614.
37. GIELOW, M. L., G. G. GU and S. SINGH, 1995 Resolution and pharmacological analysis of the voltage-dependent calcium channels of Drosophila larval muscles. J. Neurosci. 15: 6085-6093.
38. GIORDANO, C., M. SEBASTIANI, G. PLAZZI, C. TRAVAGLINI, P. SALE et al., 2006 Mitochondrial neurogastrointestinal encephalomyopathy: evidence of mitochondrial DNA depletion in the small intestine. Gastroenterology 130: 893-901.
39. GNERER, J. P., R. A. KREBER and B. GANETZKY, 2006 wasted away, a Drosophila mutation in triosephosphate isomerase, causes paralysis, neurodegeneration, and early death. Proc. Natl. Acad. Sci. USA 103: 14987-14993.
40. GROPMAN, A. L., 2004 The neurological presentations of childhood and adult mitochondrial disease: established syndromes and phenotypic variations. Mitochondrion 4: 503-520.
41. GU, G. G., and S. SINGH, 1997 Modulation of the dihydropyridinesensitive calcium channels in Drosophila by a phospholipase C-mediated pathway. J. Neurobiol. 33: 265-275.
42. + channels in Drosophila. J. Biol. Chem. 274: 22109-22113.
43. KEENEY, P. M., J. XIE, R. A. CAPALDI and J. P. BENNETT, JR., 2006 Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J. Neurosci. 26: 5256-5264.
44. ts, a mutation affecting sodium channel activity in Drosophila, is an allele of mle, a regulator of X chromosome transcription. Cell 66: 949-959.
45. KRALIZ, D., and S. SINGH, 1997 Selective blockade of the delayed rectifier potassium current by tacrine in Drosophila. J. Neurobiol. 32: 1-10.
46. KRALIZ, D., A. BHATTACHARYA and S. SINGH, 1998 Blockade of the delayed rectifier potassium current in Drosophila by quinidine and related compounds. J. Neurogenet. 12: 25-39.
47. LEIGH, D., 1951 Subacute necrotizing encephalomyelopathy in an infant. J. Neurochem. 14: 216-221.
48. LEWIS, E. B., and F. BACHER, 1968 Method of feeding ethylmethanesulfonate (EMS) to Drosophila males. Drosoph. Inf. Serv. 43: 193.
49. LIAO, T. S., G. B. CALL, P. GUPTAN, A. CESPEDES, J. MARSHALL et al., 2006 An efficient genetic screen in Drosophila to identify nuclear-encoded genes with mitochondrial function. Genetics 174: 525-533.
50. LISS, B., O. HAECKEL, J. WILDMANN, T. MIKI, S. SEINO et al., 2005 K-ATP channels promote the differential degeneration of dopaminergic midbrain neurons. Nat. Neurosci. 8: 1742-1751.
51. LOUGHNEY, K., R. KREBER and B. GANETZKY, 1989 Molecular analysis of the para locus, a sodium channel gene in Drosophila. Cell 58: 1143-1154.
52. LUDWIG, B., E. BENDER, S. ARNOLD, M. HUTTEMANN, I. LEE et al., 2001 Cytochrome C oxidase and the regulation of oxidative phosphorylation. Chembiochem 2: 392-403.
53. MATTSON, M. P., and G. KROEMER, 2003 Mitochondria in cell death: novel targets for neuroprotection and cardioprotection. Trends Mol. Med. 9: 196-205.
54. MCFARLAND, R., R. W. TAYLOR and D. M. TURNBULL, 2002 The neurology of mitochondrial DNA disease. Lancet Neurol. 1: 343-351.
55. MCKAY, R. R., D. M. CHEN, K. MILLER, S. KIM, W. S. STARK et al., 1995 Phospholipase C rescues visual defect in norpA mutant of Drosophila melanogaster. J. Biol. Chem. 270: 13271-13276.
56. PALLADINO, M. J., T. J. HADLEY and B. GANETZKY, 2002 Temperature-sensitive paralytic mutants are enriched for those causing neurodegeneration in Drosophila. Genetics 161: 1197-1208.
57. PALLANCK, L., and J. T. GREENAMYRE, 2006 Neurodegenerative disease: pink, parkin and the brain. Nature 441: 1058.
58. PAVLIDIS, P., M. RAMASWAMI and M. A. TANOUYE, 1994 The Drosophila easily shocked gene: a mutation in a phospholipid synthetic pathway causes seizure, neuronal failure, and paralysis. Cell 79: 23-33.
59. PEQUIGNOT, M. O., R. DEY, M. ZEVIANI, V. TIRANTI, C. GODINOT et al., 2001 Mutations in the SURF1 gene associated with Leigh syndrome and cytochrome C oxidase deficiency. Hum. Mutat. 17: 374-381.
60. RAHMAN, S., R. B. BLOK, H. H. DAHL, D. M. DANKS, D. M. KIRBY et al., 1996 Leigh syndrome: clinical features and biochemical and DNA abnormalities. Ann. Neurol. 39: 343-351.
61. SCHAPIRA, A. H., 2006 Mitochondrial disease. Lancet 368: 70-82.
62. SCHON, E. A., 2004 Complements of the house. J. Clin. Invest. 114: 760-762.
63. SHOUBRIDGE, E. A., 2001 Cytochrome c oxidase deficiency. Am. J. Med. Genet. 106: 46-52.
64. SINGH, S., 1983 A mutagenesis scheme for obtaining autosomal mutations in Drosophila. Indian J. Exp. Biol. 21: 635-636.
65. SINGH, A., and S. SINGH, 1999 Unmasking of a novel potassium current in Drosophila by a mutation and drugs. J. Neurosci. 19: 6838-6843.
66. SINGH, S., P. BHANDARI, M. J. S. CHOPRA and D. GUHA, 1987 Isolation of autosomal mutations in Drosophila melanogaster without setting up lines. Mol. Gen. Genet. 208: 226-229.
67. SMITH, T. S., and J. P. BENNETT, JR., 1997 Mitochondrial toxins in models of neurodegenerative diseases. I: In vivo brain hydroxyl radical production during systemic MPTP treatment or following microdialysis infusion of methylpyridinium or azide ions. Brain Res. 765: 183-188.
68. SZUPLEWSKI, S., and R. TERRACOL, 2001 The cyclope gene of Drosophila encodes a cytochrome c oxidase subunit VIc homolog. Genetics 158: 1629-1643.
69. TAANMAN, J. W., and R. A. CAPALDI, 1993 Subunit VIa of yeast cytochrome c oxidase is not necessary for assembly of the enzyme complex but modulates the enzyme activity. Isolation and characterization of the nuclear-coded gene. J. Biol. Chem. 268: 18754-18761.
70. TAANMAN, J. W., P. TURINA and R. A. CAPALDI, 1994 Regulation of cytochrome c oxidase by interaction of ATP at two binding sites, one on subunit VIa. Biochemistry 33: 11833-11841.
71. K potassium channels revealed by Drosophila Shaker and Shab mutations. J. Neurosci. 26: 6238-6248.
72. 2+ channels: a possible involvement of free radicals. J. Neurochem. 68: 265-271.
73. YAGER, J. Y., E. A. ARMSTRONG, H. MIYASHITA and E. C. WIRRELL, 2002 Prolonged neonatal seizures exacerbate hypoxic-ischemic brain damage: correlation with cerebral energy metabolism and excitatory amino acid release. Dev. Neurosci. 24: 367-381.
74. ZORDAN, M. A., P. CISOTTO, C. BENNA, A. AGOSTINO, G. RIZZO et al., 2006 Post-transcriptional silencing and functional characterization of the Drosophila melanogaster homolog of human Surf1. Genetics 172: 229-241.