Diminished synthesis of subunit a (ATP6) and altered function of ATP synthase and cytochrome c oxidase due to the mtDNA 2 bp microdeletion of TA at positions 9205 and 9206

Biochemical Journal

Volumn 383, Issue 3, 2004, Pages 561-571

  Ješina, Pavel ^a   Tesařová, Markéta ^b   Fornůsková, Daniela ^b   Vojtíšková, Alena ^a   Pecina, Petr ^a   Kaplanová, Vilma ^a   Hansíková, Hana ^b   Zeman, Jiří ^b   Houštěk, Josef ^a  

^a INSTITUTE OF MATHEMATICS   (Czech Republic)

^b Charles University in Prague and General University Hospital in Prague   (Czech Republic)

Author keywords

ATP synthase; ATP6; COX3; Cytochrome c oxidase; Mitochondrial disease; Mitochondrial DNA (mtDNA)

Indexed keywords

BIOSYNTHESIS; BLOOD; CELLS; ELECTROPHORESIS; HYDROLYSIS; MUSCLE; MUTAGENESIS;

FIBROBLASTS; MITOCHONDRIAL ENCEPHALOMYOPATHIES; MITOCHONDRIAL MEMBRANE; MUTATION;

DNA;

ADENOSINE TRIPHOSPHATASE; CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE 3; MITOCHONDRIAL DNA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; BLOOD; CASE REPORT; COMPLEX FORMATION; ENZYME ACTIVITY; ENZYME SYNTHESIS; FIBROBLAST; GENE DELETION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROLYSIS; HYPERLACTATEMIA; MALE; MEMBRANE POTENTIAL; MISSENSE MUTATION; MITOCHONDRIAL ENCEPHALOMYOPATHY; MITOCHONDRIAL MEMBRANE; MUSCLE; NORTHERN BLOTTING; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

ADENINE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; CELLS, CULTURED; CHILD, PRESCHOOL; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FIBROBLASTS; HUMANS; INTRACELLULAR MEMBRANES; MALE; MEMBRANE POTENTIALS; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MUTATION; OXYGEN CONSUMPTION; RNA, MESSENGER; SEQUENCE DELETION; SKIN; THYMIDINE;

EID: 9144272333     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040407     Document Type: Article

References (49)

1. 0-ATPaSeS. FEBS Lett. 346, 39-43
2. Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F. et al. (1981) Sequence and organization of the human mitochondrial genome. Nature (London) 280, 457-465
3. Nijtmans, L. G., Klement, P., Houstek, J. and van den Bogert, C. (1995) Assembly of mitochondrial ATP synthase in cultured human cells: implications for mitochondrial diseases. Biochim. Biophys. Acta 1272, 190-198
4. DiMauro, S. and Schon, E. A. (2001) Mitochondrial DNA mutations in human disease. Am. J. Med. Genet. 106, 18-26
5. Holt, I. J., Harding, A. E., Petty, R. K. H. and Morgan-Hughes, J. A. (1990) A new mitochondrial disease associated with mitochondrial DNA heteroplasmy. Am. J. Hum. Genet. 46, 428-433
6. de Vries, D. D., van Engelen, B. G., Gabreels, F. J., Ruitenbeek, W. and van Oost, B. A. (1993) A second missense mutation in the mitochondrial ATPase 6 gene in Leigh's syndrome. Ann. Neurol. 34, 410-412
7. Tatuch, Y., Christodoulou, J., Feigenbaum, A., Clarke, J. T., Wherret, J., Smith, C., Rudd, N., Petrova Benedict, R. and Robinson, B. H. (1992) Heteroplasmic mtDNA mutation (T → G) at 8993 can cause Leigh disease when the percentage of abnormal mtDNA is high. Am. J. Hum. Genet. 50, 852-858
8. Schon, E. A., Santra, S., Pallotti, F. and Girvin, M. E. (2001) Pathogenesis of primary defects in mitochondrial ATP synthesis. Semin. Cell Dev. Biol. 12, 441-448
9. Tatuch, Y. and Robinson, B. H. (1993) The mitochondrial DNA mutation at 8993 associated with NARP slows the rate of ATP synthesis in isolated lymphoblast mitochondria. Biochem. Biophys. Res. Commun. 192, 124-128
10. Houstek, J., Klement, P., Hermanska, J., Houstkova, H., Hansikova, H., van den Bogert, C. and Zeman, J. (1995) Altered properties of mitochondrial ATP-synthase in patients with a T → G mutation in the ATPase 6 (subunit a) gene at position 8993 of mtDNA. Biochim. Biophys. Acta 1271, 349-357
11. 0 cells completely lacking mtDNA. J. Biol. Chem. 275, 11075-11081
12. Nijtmans, L. G., Henderson, N. S., Attardi, G. and Holt, I. J. (2001) Impaired ATP synthase assembly associated with a mutation in the human ATP synthase subunit 6 gene. J. Biol. Chem. 276, 6755-6762
13. Seneca, S., Abramowicz, M., Lissens, W., Muller, M. F., Vamos, E. and de Meirleir, L. (1996) A mitochondrial DNA microdeletion in a newborn girl with transient lactic acidosis. J. Inherit. Metab. Dis. 19, 115-118
14. Fornuskova, D., Tesarova, M., Hansikova, H. and Zeman, J. (2003) New mtDNA mutation 9204delTA in a family with mitochondrial encephalopathy and ATP synthase defect. Cas. Lek. Cesk. 142, 313
15. Bentlage, H. A., Wendel, U., Schagger, H., ter Laak, H. J., Janssen, A. J. and Trijbels, J. M. (1996) Lethal infantile mitochondrial disease with isolated complex I deficiency in fibroblasts but with combined complex I and IV deficiencies in muscle. Neurology 47, 243-248
16. Klement, P., Nijtmans, L. G., Van den Bogert, C. and Houstek, J. (1995) Analysis of oxidative phosphorylation complexes in cultured human fibroblasts and amniocytes by blue-native-electrophoresis using mitoplasts isolated with the help of digitonin. Anal. Biochem. 231, 218-224
17. Makinen, M. and Lee, C. P. (1968) Biochemical studies of skeletal muscle mitochondria: I. Microanalysis of cytochrome content, oxidative and phosphorylative activities of mammalian skeletal muscle mitochondria. Arch. Biochem. Biophys. 126, 75-82
18. Chrzanowska-Lightowlers, Z. M., Temperley, R. J., Smith, P. M., Seneca, S. H. and Lightowlers, R. N. (2004) Functional polypeptides can be synthesized from human mitochondrial transcripts lacking termination codons. Biochem. J. 377, 725-731
19. Sambrook, J. and Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
20. Schagger, H. and von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199, 223-231
21. Schagger, H. and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379
22. 1-ATPase in brown adipose tissue. J. Biol. Chem. 270, 7689-7694
23. Dubot, A., Godinot, C., Dumur, V., Sablonniere, B., Stojkovic, T., Cuisset, J. M., Vojtiskova, A., Pecina, P., Jesina, P. and Houstek, J. (2004) GUG is an efficient initiation codon to translate the human mitochondrial ATP6 gene. Biochem. Biophys. Res. Commun. 313, 687-693
24. 1-ATPase. Proc. Natl. Acad. Sci. U.S.A. 80, 6167-6171
25. Wharton, D. C. and Tzagoloff, A. (1967) Cytochrome oxidase from beef heart mitochondria. Methods Enzymol. 10, 245-253
26. Rustin, P., Chretien, D., Bourgeron, T., Gerard, B., Rotig, A., Saudubray, J. M. and Munnich, A. (1994) Biochemical and molecular investigations in respiratory chain deficiencies. Clin. Chim. Acta 228, 35-51
27. Fischer, J. C., Ruitenbeek, W., Trijbels, J. M. F., Veerkamp, J. H., Stadhouders, A. M., Sengers, R. C. A. and Janssen, A. J. M. (1985) Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin. Chim. Acta 153, 37-42
28. Fischer, J. C., Ruitenbeek, W., Trijbels, J. M. F., Veerkamp, J. H., Stadhouders, A. M., Sengers, R. C. A. and Janssen, A. J. M. (1986) Estimation of NADH oxidation in human skeletal muscle mitochondria. Clin. Chim. Acta 155, 263-274
29. Chowdhury, S. K., Drahota, Z., Floryk, D., Calda, P. and Houstek, J. (2000) Activities of mitochondrial oxidative phosphorylation enzymes in cultured amniocytes. Clin. Chim. Acta 298, 157-173
30. 1-ATPase affect catalysis, enzyme conformation and high-affinity nucleotide binding sites. Biochim. Biophys. Acta 976, 77-84
31. Pecina, P., Capkova, M., Chowdhury, S. K., Drahota, Z., Dubot, A., Vojtiskova, A., Hansikova, H., Houst'kova, H., Zeman, J., Godinot, C. and Houstek, J. (2003) Functional alteration of cytochrome c oxidase by SURF1 mutations in Leigh syndrome. Biochim. Biophys. Acta 1639, 53-63
32. Floryk, D. and Houstek, J. (1999) Tetramethyl rhodamine methyl ester (TMRM) is suitable for cytofluorometric measurements of mitochondrial membrane potential in cells treated with digitonin. Biosci. Rep. 19, 27-34
33. Wanders, R. J. A., Ruiter, J. P. N., Wijburg, F. A., Zeman, J., Klement, P. and Houstek, J. (1996) Prenatal diagnosis of systemic disorders of the respiratory chain in cultured chorionic villus fibrolasts by study of ATP synthesis in digitonin-permeabilized cells. J. Inherit. Metab. Dis. 19, 133-136
34. Ouhabi, R., Boue-Grabot, M. and Mazat, J. P. (1998) Mitochondrial ATP synthesis in permeabilized cells: assessment of the ATP/O values in situ. Anal. Biochem. 263, 169-175
35. Chomyn, A. (1996) In vivo labeling and analysis of human mitochondrial translation products. Methods Enzymol. 264, 197-211
36. Plasek, J. and Sigler, K. (1996) Slow fluorescent indicators of membrane potential: a survey of different approaches to probe response analysis. J. Photochem. Photobiol. B 33, 101-124
37. Hoffbuhr, K. C., Davidson, E., Filiano, B. A., Davidson, M., Kennaway, N. G. and King, M. P. (2000) A pathogenic 15-base pair deletion in mitochondrial DNA-encoded cytochrome c oxidase subunit III results in the absence of functional cytochrome c oxidase. J. Biol. Chem. 275, 13994-14003
38. Carrozzo, R., Murray, J., Santorelli, F. M. and Capaldi, R. A. (2000) The T9176G mutation of human mtDNA gives a fully assembled but inactive ATP synthase when modeled in Eschericha coli. FEBS Lett. 486, 297-299
39. Pansini, A., Guerrieri, F. and Papa, S. (1978) Control of proton conduction by the H+-ATPase in the inner mitochondrial membrane. Eur. J. Biochem. 92, 545-551
40. 0 sector of Escherichia coli ATP synthase. Proc. Natl. Acad. Sci. U.S.A. 98, 8519-8524
41. 1-ATPase is essential in maintaining growth and membrane potential of human mitochondrial DNA-depleted rho degrees cells. J. Biol. Chem. 273, 22983-22989
42. Shoubridge, E. A. (2001) Cytochrome c oxidase deficiency. Am. J. Med. Genet. 106, 46-52
43. Rossignol, R., Faustin, B., Rocher, C., Malgat, M., Mazat, J. P. and Letellier, T. (2003) Mitochondrial threshold effects. Biochem. J. 370, 751-762
44. Temperley, R. J., Seneca, S. H., Tonska, K., Bartnik, E., Bindoff, L. A., Lightowlers, R. N. and Chrzanowska-Lightowlers, Z. M. (2003) Investigation of a pathogenic mtDNA microdeletion reveals a translation-dependent deadenylation decay pathway in human mitochondria. Hum. Mol. Genet. 12, 2341-2348
45. El Meziane, A., Lehtinen, S. K., Hance, N., Nijtmans, L. G., Dunbar, D., Holt, I. J. and Jacobs, H. T. (1998) A tRNA suppressor mutation in human mitochondria. Nat. Genet. 18, 350-353
46. Hao, H., Morrison, L. E. and Moraes, C. T. (1999) Suppression of a mitochondrial tRNA gene mutation phenotype associated with changes in the nuclear background. Hum. Mol. Genet. 8, 1117-1124
47. +-translocating ATP synthase of Saccharomyces cerevisiae. J. Biol. Chem. 279, 15728-15733
48. Mili, S. and Pinol-Roma, S. (2003) LRP130, a pentatricopeptide motif protein with a noncanonical RNA-binding domain, is bound in vivo to mitochondrial and nuclear RNAs. Mol. Cell. Biol. 23, 4972-4982
49. Mootha, V. K., Lepage, P., Miller, K., Bunkenborg, J., Reich, M., Hjerrild, M., Delmonte, T., Villeneuve, A., Sladek, R., Xu, F. et al. (2003) Identification of a gene causing human cytochrome c oxidase deficiency by integrate genomics. Proc. Natl. Acad. Sci. U.S.A. 100, 605-610