Knockdown of Human Oxa1l Impairs the Biogenesis of F1Fo-ATP Synthase and NADH:Ubiquinone Oxidoreductase

Journal of Molecular Biology

Volumn 374, Issue 2, 2007, Pages 506-516

  Stiburek, Lukas ^a   Fornuskova, Daniela ^a   Wenchich, Laszlo ^a   Pejznochova, Martina ^a   Hansikova, Hana ^a   Zeman, Jiri ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

ATP synthase; biogenesis; mitochondria; NADH:ubiquinone oxidoreductase; Oxa1l

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA TUBULIN; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOCHROME C OXIDASE; MEMBRANE PROTEIN; PORIN; PROTEIN ALB3; PROTEIN OXA1L; PROTEIN YIDC; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SHORT HAIRPIN RNA; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL STRAIN HEK293; CHIMERA; CHLOROPLAST; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL GENE; GENETIC COMPLEMENTATION; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNOBLOTTING; MITOCHONDRION; MUTANT; OXA1 GENE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA STABILITY; STEADY STATE; TWO DIMENSIONAL ELECTROPHORESIS;

EID: 35548996344     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.09.044     Document Type: Article

References (43)

1. Yi L., and Dalbey R.E. Oxa1/Alb3/YidC system for insertion of membrane proteins in mitochondria, chloroplasts and bacteria (review). Mol. Membr. Biol. 22 (2005) 101-111
2. Herrmann J.M., and Neupert W. Protein insertion into the inner membrane of mitochondria. IUBMB Life 55 (2003) 219-225
3. Bonnefoy N., Chalvet F., Hamel P., Slonimski P.P., and Dujardin G. OXA1, a Saccharomyces cerevisiae nuclear gene whose sequence is conserved from prokaryotes to eukaryotes controls cytochrome oxidase biogenesis. J. Mol. Biol. 239 (1994) 201-212
4. Altamura N., Capitanio N., Bonnefoy N., Papa S., and Dujardin G. The Saccharomyces cerevisiae OXA1 gene is required for the correct assembly of cytochrome c oxidase and oligomycin-sensitive ATP synthase. FEBS Letters 382 (1996) 111-115
5. Hell K., Herrmann J., Pratje E., Neupert W., and Stuart R.A. Oxa1p mediates the export of the N- and C-termini of pCoxII from the mitochondrial matrix to the intermembrane space. FEBS Letters 418 (1997) 367-370
6. He S., and Fox T.D. Membrane translocation of mitochondrially coded Cox2p: distinct requirements for export of N and C termini and dependence on the conserved protein Oxa1p. Mol. Biol. Cell 8 (1997) 1449-1460
7. Lemaire C., Guibet-Grandmougin F., Angles D., Dujardin G., and Bonnefoy N. A yeast mitochondrial membrane methyltransferase-like protein can compensate for oxa1 mutations. J. Biol. Chem. 279 (2004) 47464-74742
8. Hell K., Herrmann J.M., Pratje E., Neupert W., and Stuart R.A. Oxa1p, an essential component of the N-tail protein export machinery in mitochondria. Proc. Natl Acad. Sci. USA 95 (1998) 2250-2255
9. Hell K., Neupert W., and Stuart R.A. Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. EMBO J. 20 (2001) 1281-1288
10. Jia L., Dienhart M.K., and Stuart R.A. Oxa1 Directly Interacts with Atp9 and Mediates Its Assembly into the Mitochondrial F1Fo-ATP Synthase Complex. Mol. Biol. Cell 18 (2007) 1897-1908
11. Bonnefoy N., Kermorgant M., Groudinsky O., and Dujardin G. The respiratory gene OXA1 has two fission yeast orthologues which together encode a function essential for cellular viability. Mol. Microbiol. 35 (2000) 1135-1145
12. Nargang F.E., Preuss M., Neupert W., and Herrmann J.M. The Oxa1 protein forms a homooligomeric complex and is an essential part of the mitochondrial export translocase in Neurospora crassa. J. Biol. Chem. 277 (2002) 12846-12853
13. Jia L., Dienhart M., Schramp M., McCauley M., Hell K., and Stuart R.A. Yeast Oxa1 interacts with mitochondrial ribosomes: the importance of the C-terminal region of Oxa1. EMBO J. 22 (2003) 6438-6447
14. Szyrach G., Ott M., Bonnefoy N., Neupert W., and Herrmann J.M. Ribosome binding to the Oxa1 complex facilitates co-translational protein insertion in mitochondria. EMBO J. 22 (2003) 6448-6457
15. Bonnefoy N., Kermorgant M., Groudinsky O., Minet M., Slonimski P.P., and Dujardin G. Cloning of a human gene involved in cytochrome oxidase assembly by functional complementation of an oxa1-mutation in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 91 (1994) 11978-11982
16. Rotig A., Parfait B., Heidet L., Dujardin G., Rustin P., and Munnich A. Sequence and structure of the human OXA1L gene and its upstream elements. Biochim. Biophys. Acta 1361 (1997) 6-10
17. Strausberg R.L., Feingold E.A., Grouse L.H., Derge J.G., Klausner R.D., Collins F.S., et al. Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc. Natl Acad. Sci. USA 99 (2002) 16899-16903
18. Sylvestre J., Margeot A., Jacq C., Dujardin G., and Corral-Debrinski M. The role of the 3' untranslated region in mRNA sorting to the vicinity of mitochondria is conserved from yeast to human cells. Mol. Biol. Cell 14 (2003) 3848-3856
19. Stegmeier F., Hu G., Rickles R.J., Hannon G.J., and Elledge S.J. A lentiviral microRNA-based system for single-copy polymerase II-regulated RNA interference in mammalian cells. Proc. Natl Acad. Sci. USA 102 (2005) 13212-13217
20. Kermorgant M., Bonnefoy N., and Dujardin G. Oxa1p, which is required for cytochrome c oxidase and ATP synthase complex formation, is embedded in the mitochondrial inner membrane. Curr. Genet. 31 (1997) 302-307
21. Herrmann J.M., Neupert W., and Stuart R.A. Insertion into the mitochondrial inner membrane of a polytopic protein, the nuclear-encoded Oxa1p. Embo J. 16 (1997) 2217-2226
22. Reif S., Randelj O., Domanska G., Dian E.A., Krimmer T., Motz C., and Rassow J. Conserved mechanism of Oxa1 insertion into the mitochondrial inner membrane. J. Mol. Biol. 354 (2005) 520-528
23. Stiburek L., Hansikova H., Tesarova M., Cerna L., and Zeman J. Biogenesis of eukaryotic cytochrome c oxidase. Physiol. Res. 55 (2006) S27-S41
24. Stiburek L., Vesela K., Hansikova H., Pecina P., Tesarova M., Cerna L., et al. Tissue-specific cytochrome c oxidase assembly defects due to mutations in SCO2 and SURF1. Biochem. J. 392 (2005) 625-632
25. Preuss M., Ott M., Funes S., Luirink J., and Herrmann J.M. Evolution of mitochondrial oxa proteins from bacterial YidC. Inherited and acquired functions of a conserved protein insertion machinery. J. Biol. Chem. 280 (2005) 13004-13011
26. Villani G., Greco M., Papa S., and Attardi G. Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J. Biol. Chem. 273 (1998) 31829-31836
27. Piccoli C., Scrima R., Boffoli D., and Capitanio N. Control by cytochrome c oxidase of the cellular oxidative phosphorylation system depends on the mitochondrial energy state. Biochem. J. 396 (2006) 573-583
28. Villani G., and Attardi G. In vivo control of respiration by cytochrome c oxidase in human cells. Free Radic. Biol. Med. 29 (2000) 202-210
29. Diaz F., Fukui H., Garcia S., and Moraes C.T. Cytochrome c oxidase is required for the assembly/stability of respiratory complex I in mouse fibroblasts. Mol. Cell. Biol. 26 (2006) 4872-4881
30. Ugalde C., Janssen R.J., van den Heuvel L.P., Smeitink J.A., and Nijtmans L.G. Differences in assembly or stability of complex I and other mitochondrial OXPHOS complexes in inherited complex I deficiency. Hum. Mol. Genet. 13 (2004) 659-667
31. Pecina P., Capkova M., Chowdhury S.K., Drahota Z., Dubot A., Vojtiskova A., et al. Functional alteration of cytochrome c oxidase by SURF1 mutations in Leigh syndrome. Biochim. Biophys. Acta 1639 (2003) 53-63
32. Buchet K., and Godinot C. Functional F1-ATPase essential in maintaining growth and membrane potential of human mitochondrial DNA-depleted rho degrees cells. J. Biol. Chem. 273 (1998) 22983-22989
33. Garcia J.J., Ogilvie I., Robinson B.H., and Capaldi R.A. Structure, functioning, and assembly of the ATP synthase in cells from patients with the T8993G mitochondrial DNA mutation. Comparison with the enzyme in Rho(0) cells completely lacking mtDNA. J. Biol. Chem. 275 (2000) 11075-11081
34. Carrozzo R., Wittig I., Santorelli F.M., Bertini E., Hofmann S., Brandt U., and Schagger H. Subcomplexes of human ATP synthase mark mitochondrial biosynthesis disorders. Ann. Neurol. 59 (2006) 265-275
35. Houstek J., Pickova A., Vojtiskova A., Mracek T., Pecina P., and Jesina P. Mitochondrial diseases and genetic defects of ATP synthase. Biochim. Biophys. Acta 1757 (2006) 1400-1405
36. Houstek J., Andersson U., Tvrdik P., Nedergaard J., and Cannon B. The expression of subunit c correlates with and thus may limit the biosynthesis of the mitochondrial F0F1-ATPase in brown adipose tissue. J. Biol. Chem. 270 (1995) 7689-7694
37. Andersson U., Houstek J., and Cannon B. ATP synthase subunit c expression: physiological regulation of the P1 and P2 genes. Biochem. J. 323 (1997) 379-385
38. Sangawa H., Himeda T., Shibata H., and Higuti T. Gene expression of subunit c(P1), subunit c(P2), and oligomycin sensitivity-conferring protein may play a key role in biogenesis of H+-ATP synthase in various rat tissues. J. Biol. Chem. 272 (1997) 6034-6037
39. Kramarova, T. (2006). Limiting factors in ATP synthesis, PhD thesis. Stockholm University.
40. Olson A., Sheth N., Lee J.S., Hannon G., and Sachidanandam R. RNAi Codex: a portal/database for short-hairpin RNA (shRNA) gene-silencing constructs. Nucl. Acids Res. 34 (2006) D153-D157
41. Rustin P., Chretien D., Bourgeron T., Gerard B., Rotig A., Saudubray J.M., and Munnich A. Biochemical and molecular investigations in respiratory chain deficiencies. Clin. Chim. Acta 228 (1994) 35-51
42. Jesina P., Tesarova M., Fornuskova D., Vojtiskova A., Pecina P., Kaplanova V., et al. 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. Biochem. J. 383 (2004) 561-571
43. Fujiki Y., Hubbard A.L., Fowler S., and Lazarow P.B. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93 (1982) 97-102