New insights into type II NAD(P)H:quinone oxidoreductases

Microbiology and Molecular Biology Reviews

Volumn 68, Issue 4, 2004, Pages 603-616

  Melo, Ana M P ^a,b   Bandeiras, Tiago M ^a   Teixeira, Miguel ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b UNIVERSIDADE LUSÓFONA DE HUMANIDADES E TECNOLOGIAS   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 BENZOQUINONE; CAPSAICIN; CYTOCHROME C OXIDASE; ENZYME INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PIERICIDIN A; POLYPEPTIDE; QUERCETIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; ROTENONE; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BIOCHEMISTRY; CATALYSIS; COMPLEX I DEFICIENCY; ELECTRON; ELECTRON TRANSPORT; ENERGY TRANSFER; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME STRUCTURE; EUKARYOTE; GENE SEQUENCE; GENETIC ANALYSIS; GENOME; GENOME ANALYSIS; HUMAN; MEMBRANE POTENTIAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROKARYOTE; PROTEIN INTERACTION; RESPIRATORY CHAIN; REVIEW; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURAL HOMOLOGY; YEAST;

AMINO ACID SEQUENCE; ANIMALS; BACTERIA; HUMANS; MAMMALS; MOLECULAR SEQUENCE DATA; PROKARYOTIC CELLS; QUINONE REDUCTASES; SEQUENCE ALIGNMENT;

EUKARYOTA; PROKARYOTA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 10344231976     PISSN: 10922172     EISSN: None     Source Type: Journal    
DOI: 10.1128/MMBR.68.4.603-616.2004     Document Type: Review

References (96)

1. Bai, Y., P. Hajek, A. Chomyn, E. Chan, B. B. Seo, A. Matsuno-Yagi, T. Yagi, and G. Attardi. 2001. Lack of complex I activity in human cells carrying a mutation in MtDNA-encoded ND4 subunit is corrected by the Saccharomyces cerevisiae NADH-quinone oxidoreductase (NDH) gene. J. Biol. Chem. 276:38808-38813.
2. Bandeiras, T. M., C. Salgueiro, A. Kletzin, C. M. Gomes, and M. Teixeira. 2002. Acidianus ambivalens type-II NADH dehydrogenase: genetic characterisation and identification of the flavin moiety as FMN. FEBS Lett. 531:273-277.
3. Bandeiras, T. M., C. A. Salgueiro, H. Huber, C. M. Gomes, and M. Teixeira. 2003. The respiratory chain of the thermophilic archaeon Sulfolobus metallicus: studies on the type-II NADH dehydrogenase. Biochim. Biophys. Acta 1557:13-19.
4. +-pumping NADH-quinone oxidoreductase from Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99:10322-10324.
5. Bernardi, P., and G. F. Azzone. 1981. Cytochrome c as an electron shuttle between the outer and inner mitochondrial membranes. J. Biol. Chem. 256:7187-7192.
6. Bertsova, Y. V., A. V. Bogachev, and V. P. Skulachev. 2001. Noncoupled NADH:ubiquinone oxidoreductase of Azotobacter vinelandii is required for diazotrophic growth at high oxygen concentrations. J. Bacteriol. 183:6869-6874.
7. Bertsova, Y. V., A. V. Bogachev, and V. P. Skulachev. 1998. Two NADH:ubiquinone oxidoreductases of Azotobacter vinelandii and their role in the respiratory protection. Biochim. Biophys. Acta 1363:125-133.
8. Bjorklof, K., V. Zickermann, and M. Finel. 2000. Purification of the 45 kDa, membrane bound NADH dehydrogenase of Escherichia coli (NDH-2) and analysis of its interaction with ubiquinone analogues. FEBS Lett. 467:105-110.
9. Bracey, M. H., B. F. Cravatt, and R. C. Stevens. 2004. Structural commonalities among integral membrane enzymes. FEBS Lett. 567:159-165.
10. Bragg, P. D., and C. Hou. 1967. Reduced nicotinamide adenine dinucleotide oxidation in Escherichia coli particles. II. NADH dehydrogenases. Arch. Biochem. Biophys. 119:202-208.
11. Carneiro, P., M. Duarte, and A. Videira. 2004. The main external NAD(P)H dehydrogenase of Neurospora crassa mitochondria. Biochim. Biophys. Acta 1608:45-52.
12. Chrzanowska-Lightowlers, Z. M., R. N. Lightowlers, and D. M. Turnbull. 1995. Gene therapy for mitochondrial DNA defects: is it possible? Gene Ther. 2:311-316.
13. Cypionka, H. 2000. Oxygen respiration by Desulfovibrio species. Annu. Rev. Microbiol. 54:827-848.
14. Dawson, A. G. 1979. Oxidation of cytosolic NADH formed during aerobic metabolism in mammalian cells. Trends Biochem. Sci. 4:171-176.
15. Deckert, G., P. V. Warren, T. Gaasterland, W. G. Young, A. L. Lenox, D. E. Graham, R. Overbeek, M. A. Snead, M. Keller, M. Aujay, R. Huber, R. A. Feldman, J. M. Short, G. J. Olsen, and R. V. Swanson. 1998. The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392:353-358.
16. de Vries, S., and L. A. Grivell. 1988. Purification and characterization of a rotenone-insensitive NADH:Q6 oxidoreductase from mitochondria of Saccharomyces cerevisiae. Eur. J. Biochem. 176:377-384.
17. Duarte, M., M. Peters, U. Schulte, and A. Videira. 2003. The internal alternative NADH dehydrogenase of Neurospora crassa mitochondria. Biochem. J. 371:1005-1011.
18. Fang, J., and D. S. Beattie. 2003. External alternative NADH dehydrogenase of Saccharomyces cerevisiae: a potential source of superoxide. Free Radic. Biol. Med. 34:478-488.
19. Fang, J., and D. S. Beattie. 2002. Novel FMN-containing rotenone-insensitive NADH dehydrogenase from Tiypanosoma brucei mitochondria: isolation and characterization. Biochemistry 41:3065-3072.
20. Finel, M. 1998. Does NADH play a central role in energy metabolism in Helicobacter pylori? Trends Biochem. Sci. 23:412-413.
21. Fisher, N., and P. R. Rich. 2000. A motif for quinone binding sites in respiratory and photosynthetic systems. J. Mol. Biol. 296:1153-1162.
22. Galagan, J. E., S. E. Calvo, K. A. Borkovich, E. U. Selker, N. D. Read, D. Jaffe, W. FitzHugh, L. J. Ma, S. Smirnov, S. Purcell, B. Rehman, T. Elkins, R. Engels, S. Wang, C. B. Nielsen, J. Butler, M. Endrizzi, D. Qui, P. Ianakiev, D. Bell-Pedersen, M. A. Nelson, M. Werner-Washburne, C. P. Selitrennikoff, J. A. Kinsey, E. L. Braun, A. Zelter, U. Schulte, G. O. Kothe, G. Jedd, W. Mewes, C. Staben, E. Marcotte, D. Greenberg, A. Roy, K. Foley, J. Naylor, N. Stange-Thomann, R. Barrett, S. Gnerre, M. Kamal, M. Kamvysselis, E. Mauceli, C. Bielke, S. Rudd, D. Frishman, S. Krystofova, C. Rasmussen, R. L. Metzenberg, D. D. Perkins, S. Kroken, C. Cogoni, G. Macino, D. Catcheside, W. Li, R. J. Pratt, S. A. Osmani, C. P. DeSouza, L. Glass, M. J. Orbach, J. A. Berglund, R. Voelker, O. Yarden, M. Plamann, S. Seiler, J. Dunlap, A. Radford, R. Aramayo, D. O. Natvig, L. A. Alex, G. Mannhaupt, D. J. Ebbole, M. Freitag, I. Paulsen, M. S. Sachs, E. S. Lander, C. Nusbaum, and B. Birren. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859-868.
23. Gomes, C. M., T. M. Bandeiras, and M. Teixeira. 2001. A new type-II NADH dehydrogenase from the archaeon Acidianus ambivalens: characterization and in vitro reconstitution of the respiratory chain. J. Bioenerg. Biomembr. 33:1-8.
24. Green, J., M. F. Anjum, and J. R. Guest. 1997. Regulation of the ndh gene of Escherichia coli by integration host factor and a novel regulator, Arr. Microbiology 143:2865-2875.
25. Hatefi, Y. 1985. The mitochondrial electron transport and oxidative phosphorylation system. Annu. Rev. Biochem. 54:1015-1069.
26. +-translocating NADH-quinone reductase of marine and moderately halophilic bacteria, p. 155- 175. In D. Zannoni (ed.), Respiration in Archaea and Bacteria, vol. 1. Kluwer Publishing, Dordrecht, The Netherlands.
27. Hirokawa, T., S. Boon-Chieng, and S. Mitaku. 1998. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378-379.
28. Howitt, C. A., P. K. Udall, and W. F. Vermaas. 1999. Type 2 NADH dehydrogenases in the cyanobacterium Synechocystis sp. strain PCC 6803 are involved in regulation rather than respiration. J. Bacteriol. 181:3994-4003.
29. Jackson, L., T. Blake, and J. Green. 2004. Regulation of ndh expression in Escherichia coli by Fis. Microbiology 150:407-413.
30. Jaworowski, A., G. Mayo, D. C. Shaw, H. D. Campbell, and I. G. Young. 1981. Characterization of the respiratory NADH dehydrogenase of Escherichia coli and reconstitution of NADH oxidase in ndh mutant membrane vesicles. Biochemistry 20:3621-3268.
31. Kawarabayasi, Y., Y. Hino, H. Horikawa, K. Jin-no, M. Takahashi, M. Sekine, S. Baba, A. Ankai, H. Kosugi, A. Hosoyama, S. Fukui, Y. Nagai, K. Nishijima, R. Otsuka, H. Nakazawa, M. Takamiya, Y. Kato, T. Yoshizawa, T. Tanaka, Y. Kudoh, J. Yamazaki, N. Kushida, A. Oguchi, K. Aoki, S. Masuda, M. Yanagii, M. Nishimura, A. Yamagishi, T. Oshima, and H. Kikuchi. 2001. Complete genome sequence of an aerobic thermoacidophilic crenarchaeon, Sulfolobus tokodai strain7. DNA Res. 8:123-140.
32. Kawarabayasi, Y., Y. Hino, H. Horikawa, S. Yamazaki, Y. Haikawa, K. Jin-no, M. Takahashi, M. Sekine, S. Baba, A. Ankai, H. Kosugi, A. Hosoyama, S. Fukui, Y. Nagai, K. Nishijima, H. Nakazawa, M. Takamiya, S. Masuda, T. Funahashi, T. Tanaka, Y. Kudoh, J. Yamazaki, N. Kushida, A. Oguchi, H. Kikuchi, et al. 1999. Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res 6:83-101, 145-152.
33. Kawashima, T., N. Amano, H. Koike, S. Makino, S. Higuchi, Y. Kawashima-Ohya, K. Watanabe, M. Yamazaki, K. Kanehori, T. Kawamoto, T. Nunoshiba, Y. Yamamoto, H. Aramaki, K. Makino, and M. Suzuki. 2000. Archaeal adaptation to higher temperatures revealed by genomic sequence of Thermoplasma volcanium. Proc. Natl. Acad. Sci. USA 97:14257-14262.
34. Kerscher, S. J., A. Eschemann, P. M. Okun, and U. Brandt. 2001. External alternative NADH:ubiquinone oxidoreductase redirected to the internal face of the mitochondrial inner membrane rescues complex I deficiency in Yarrowia lipolytica. J. Cell Sci. 114:3915-3921.
35. Kerscher, S. J., J. G. Okun, and U. Brandt. 1999. A single external enzyme confers alternative NADH:ubiquinone oxidoreductase activity in Yarrowia lipolytica. J. Cell Sci. 112:2347-2354.
36. Kitajima-Ihara, T., and T. Yagi. 1998. Rotenone-insensitive internal NADH-quinone oxidoreductase of Saccharomyces cerevisiae mitochondria: the enzyme expressed in Escherichia coli acts as a member of the respiratory chain in the host cells. FEBS Lett. 421:37-40.
37. Lemos, R. S., C. M. Gomes, and M. Teixeira. 2001. Acidianus ambivalens complex II typifies a novel family of succinate dehydrogenases. Biochem. Biophys. Res. Commun. 281:141-150.
38. Lemos, R. S., A. S. Fernandes, M. M. Pereira, C. M. Gomes, and M. Teixeira, 2002. Quinol:fumarate oxidoreductases and succinate:quinone oxidoreductases: phylogenetic relationships, metal centres and membrane attachment. Biochim. Biophys. Acta 1553:158-170.
39. Li, Q., R. G. Ritzel, L. L. McLean, L. McIntosh, T. Ko, H. Bertrand, and F. E. Nargang. 1996. Cloning and analysis of the alternative oxidase gene of Neurospora crassa. Genetics 142:129-140.
40. Luethy, M. H., M. K. Hayes, and T. E. Elthon. 1991. Partial purification of three NAD(P)H dehydrogenases from Beta vulgaris mitochondria. Plant Physiol. 97:1317-1322.
41. Luethy, M. H., J. J. Thelen, A. F. Knudten, and T. E. Elthon. 1995. Purification, characterization, and submitochondrial localization of a 58-kilodalton NAD(P)H dehydrogenase. Plant Physiol. 107:443-450.
42. Luttik, M. A., K. M. Overkamp, P. Kotter, S. de Vries, J. P. van Dijken, and J. T. Pronk. 1998. The Saccharomyces cerevisiae NDE1 and NDE2 genes encode separate mitochondrial NADH dehydrogenases catalyzing the oxidation of cytosolic NADH. J. Biol. Chem. 273:24529-24534.
43. Marres, C. A., S. de Vries, and L. A. Grivell. 1991. Isolation and inactivation of the nuclear gene encoding the rotenone-insensitive internal NADH:ubiquinone oxidoreductase of mitochondria from Saccharomyces cerevisiae. Eur. J. Biochem. 195:857-862.
44. Matsushita, K., T. Ohnishi, and H. R. Kaback. 1987. NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain. Biochemistry 26:7732-7737.
45. McGuffin, L. J., K. Bryson, and D. T. Jones. 2000. The PSIPRED protein structure prediction server. Bioinformatics 16:404-405.
46. McIntosh, L. 1994. Molecular biology of the alternative oxidase. Plant Physiol. 105:781-786.
47. Melo, A. M. P. 2001. Characterisation of NAD(P)H dehydrogenases from Neurospora mitochondria. Ph.D. thesis. Universidade de Porto, Porto, Portugal.
48. Melo, A. M. P., M. Duarte, I. M. Moller, H. Prokisch, P. L. Dolan, L. Pinto, M. A. Nelson, and A. Videira. 2001. The external calcium-dependent NADPH dehydrogenase from Neurospora crassa mitochondria. J. Biol. Chem. 276:3947-3951.
49. Melo, A. M. P., M. Duarte, and A. Videira. 1999. Primary structure and characterisation of a 64 kDa NADH dehydrogenase from the inner membrane of Neurospora crassa mitochondria. Biochim. Biophys. Acta 1412:282-287.
50. Melo, A. M. P., T. H. Roberts, and I. M. Moller. 1996. Evidence for the presence of two rotenone-insensitive NAD(P)H dehydrogenases on the inner surface of the inner membrane of potato tuber mitochondria. Biochim. Biophys. Acta 1276:133-139.
51. Menz, R. I., and D. A. Day. 1996. Purification and characterization of a 43-kDa rotenone-insensitive NADH dehydrogenase from plant mitochondria. J. Biol Chem. 271:23117-23120.
52. Michalecka, A. M., A. S. Svensson, F. I. Johansson, S. C. Agius, U. Johanson, A. Brennicke, S. Binder, and A. G. Rasmusson. 2003. Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiol. 133:642-652.
53. Miramar, M. D., P. Costantini, L. Ravagnan, L. M. Saraiva, D. Haouzi, G. Brothers, J. M. Penninger, M. L. Peleato, G. Kroemer, and S. A. Susin. 2001. NADH oxidase activity of mitochondrial apoptosis-inducing factor. J. Biol. Chem. 276:16391-16398.
54. Moller, I. M. 2001. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52:561-591.
55. 2+ in the oxidation of exogenous NADH by Jerusalem-artichoke (Helianthus tuberosus) mitochondria. Biochem. J. 194:487-495.
56. Moller, I. M., and W. Lin. 1986. Membrane-bound NAD(P)H dehydrogenases in higher plant cells. Annu. Rev. Plant Physiol. 37:309-334.
57. Moller, I. M., and J. M. Palmer. 1982. Direct evidence for the presence of a rotenone-resistant NADH dehydrogenase on the inner surface of the inner membrane of plant mitochondria. Physiol. Plant. 54:267-274.
58. Moller, I. M., J.-P. Schwitzguébel, and J. M. Palmer. 1982. Binding and screening by cations and the effect on exogenous NAD(P)H oxidation in Neurospora crassa mitochondria. Eur. J. Biochem. 123:81-88.
59. Nakamura, Y., T. Kaneko, S. Sato, M. Ikeuchi, H. Katoh, S. Sasamoto, A. Watanabe, M. Iriguchi, K. Kawashima, T. Kimura, Y. Kishida, C. Kiyokawa, M. Kohara, M. Matsumoto, A. Matsuno, N. Nakazaki, S. Shimpo, M. Sugimoto, C. Takeuchi, M. Yamada, and S. Tabata. 2002. Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res. 9:123-130.
60. Ng, W. V., S. P. Kennedy, G. G. Mahairas, B. Berquist, M. Pan, H. D. Shukla, S. R. Lasky, N. S. Baliga, V. Thorsson, J. Sbrogna, S. Swartzell, D. Weir, J. Hall, T. A. Dahl, R. Welti, Y. A. Goo, B. Leithauser, K. Keller, R. Cruz, M. J. Danson, D. W. Hough, D. G. Maddocks, P. E. Jablonski, M. P. Krebs, C. M. Angevine, H. Dale, T. A. Isenbarger, R. F. Peck, M. Pohlschroder, J. L. Spudich, K. W. Jung, M. Alam, T. Freitas, S. Hou, C. J. Daniels, P. P. Dennis, A. D. Omer, H. Ebhardt, T. M. Lowe, P. Liang, M. Riley, L. Hood, and S. DasSarma. 2000. Genome sequence of Halobacterium species NRC-1. Proc. Natl. Acad. Sci. USA 97:12176-12181.
61. Nohl, H., L. Gille, and K. Staniek. 1998. The exogenous NADH dehydrogenase of heart mitochondria is the key-enzyme responsible for selective cardiotoxicity of anthracyclines. Z. Naturforsch. Ser. C 53:279-285.
62. Oliveira, P. J., D. J. Santos, and A. J. Moreno. 2000. Carvedilol inhibits the exogenous NADH dehydrogenase in rat heart mitochondria. Arch. Biochem. Biophys. 374:279-285.
63. Owen, P. H., R. Kaback, and H. Doherty. 1979. Immunochemical analysis of membrane vesicles from Escherichia coli. Biochemistry 18:1413-1422.
64. Pereira, M. M., T. M. Bandeiras, A. S. Fernandes, R. S. Lemos, A. M. P. Melo, and M. Teixeira. 2004. Respiratory chains from aerobic thermophilic prokaryotes. J. Bioenerg. Biomembr. 36:93-105.
65. Pereira, M. M., M. Santana, and M. Teixeira. 2001. A novel scenario for the evolution of haem-copper oxygen reductases. Biochim. Biophys. Acta 1505:185-208.
66. Rasmusson, A. G., and I. M. Moller. 1991. NAD(P)H dehydrogenases on the inner surface of the inner mitochondrial membrane studied using inside-out submitochondrial particles. Physiol. Plant. 83:357-365.
67. Rasmusson, A. G., and I. M. Moller. 1993. Purification of a rotenone-insensitive NAD(P)H dehydrogenase from the inner surface of the inner mitochondrial membrane of red beetroot mitochondria. Biochim. Biophys. Acta 1141:107-110.
68. Rasmusson, A. G., A. S. Svensson, V. Knoop, L. Grohmann, and A. Brennicke. 1999. Homologues of yeast and bacterial rotenone-insensitive NADH dehydrogenases in higher eukaryotes: two enzymes are present in potato mitochondria. Plant J. 20:79-87.
69. Roberts, T. H., K. M. Fredlund, and I. M. Moller. 1995. Direct evidence for the presence of two external NAD(P)H dehydrogenases coupled to the electron transport chain in plant mitochondria. FEBS Lett. 373:307-309.
70. Saraste, M. 1999. Oxidative phosphorylation at the fin de siecle. Science 283:1488-1493.
71. Seo, B. B., T. Kitajima-Ihara, E. K. Chan, I. E. Scheffler, A. Matsuno-Yagi, and T. Yagi. 1998. Molecular remedy of complex I defects: rotenone-insensitive internal NADH-quinone oxidoreductase of Saccharomyces cerevisiae mitochondria restores the NADH oxidase activity of complex I-deficient mammalian cells. Proc. Natl. Acad. Sci. USA 95:9167-9171.
72. Seo, B. B., A. Matsuno-Yagi, and T. Yagi. 1999. Modulation of oxidative phosphorylation of human kidney 293 cells by transfection with the internal rotenone-insensitive NADH-quinone oxidoreductase (ND11) gene of Saccharomyces cerevisiae. Biochim. Biophys. Acta 1412:56-65.
73. Seo, B. B., J. Wang, T. R. Flotte, T. Yagi, and A. Matsuno-Yagi. 2000. Use of the NADH-quinone oxidoreductase (NDI1) gene of Saccharomyces cerevisiae as a possible cure for complex 1 defects in human cells. J. Biol. Chem. 275:37774-37778.
74. Small, W. C., and L. McAlister-Henn. 1998. Identification of a cytosolically directed NADH dehydrogenase in mitochondria of Saccharomyces cerevisiae. J. Bacteriol. 180:4051-4055.
75. Spencer, A. G., E. Thuresson, J. C. Otto, I. Song, T. Smith, D. L. DeWitt, R. M. Garavito, and W. L. Smith. 1999. The membrane binding domains of prostaglandin endoperoxide H synthases 1 and 2. Peptide mapping and mutational analysis. J. Biol. Chem. 274:32936-32942.
76. Spiro, S., and J. R. Guest. 1990. FNR and its role in oxygen-regulated gene expression in Escherichia coli. FEMS Microbiol. Rev. 6:399-428.
77. Spiro, S., R. E. Roberts, and J. R. Guest. 1989. FNR-dependent repression of the ndh gene of Escherichia coli and metal ion requirement for FNR-regulated gene expression. Mol. Microbiol. 3:601-608.
78. Sreeramulu, K., C. L. Schmidt, G. Schafer, and S. Anemuller. 1998. Studies of the electron transport chain of the euryarcheon Halobacterium salinarum: indications for a type II NADH dehydrogenase and a complex III analog. J. Bioenerg. Biomembr. 30:443-453.
79. Stenmark, P., and P. Nordlund. 2003. A prokaryotic alternative oxidase present in the bacterium Novosphingobium aromaticivorans. FEBS Lett. 552:189-192.
80. Stryer, L. 1995. Biochemistry. Freeman, New York, N.Y.
81. Susin, S. A., H. K. Lorenzo, N. Zamzami, I. Marzo, B. E. Snow, G. M. Brothers, J. Mangion, E. Jacotot, P. Costantini, M. Loeffler, N. Larochette, D. R. Goodlett, R. Aebersold, D. P. Siderovski, J. M. Penninger, and G. Kroemer. 1999. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441-446.
82. Svensson, A. S., F. I. Johansson, I. M. Moller, and A. G. Rasmusson. 2002. Cold stress decreases the capacity for respiratory NADH oxidation in potato leaves. FEBS Lett. 517:79-82.
83. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
84. Tran, Q. H., J. Bongaerts, D. Vlad, and G. Unden. 1997. Requirement for the proton-pumping NADH dehydrogenase I of Escherichia coli in respiration of NADH to fumarate and its bioenergetic implications. Eur. J. Biochem. 244:155-160.
85. van den Heuvel, L., W. Ruitenbeek, R. Smeets, Z. Gelman-Kohan, O. Elpeleg, J. Loeffen, F. Trijbels, E. Mariman, D. de Bruijn, and J. Smeitink. 1998. Demonstration of a new pathogenic mutation in human complex 1 deficiency: a 5-bp duplication in the nuclear gene encoding the 18-kD (AQDQ) subunit. Am. J. Hum. Genet. 62:262-268.
86. Vanlerberghe, G. C., A. E. Vanlerberghe, and L. McIntosh. 1997. Molecular genetic evidence of the ability of alternative oxidase to support respiratory carbon metabolism. Plant Physiol. 113:657-661.
87. Velazquez, I., and J. P. Pardo. 2001. Kinetic characterization of the rotenone-insensitive internal NADH:ubiquinone oxidoreductase of mitochondria from Saccharomyces cerevisiae. Arch. Biochem. Biophys. 389:7-14.
88. Wackwitz, B., J. Bongaerts, S. D. Goodman, and G. Unden. 1999. Growth phase-dependent regulation of nuoA-N expression in Escherichia coli K-12 by the Fis protein: upstream binding sites and bioenergetic significance. Mol. Gen. Genet. 262:876-883.
89. Wallace, D. C. 1992. Diseases of the mitochondrial DNA. Annu. Rev. Biochem. 61:1175-1212.
90. Weiss, H., G. von Jagow, M. Klingenberg, and T. Bucher. 1970. Characterization of Neurospora crassa mitochondria prepared with a grind-mill. Eur. J. Biochem. 14:75-82.
91. Wierenga, R. K., P. Terpstra, and W. G. Hol. 1986. Prediction of the occurrence of the ADP-binding beta alpha beta-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187:101-107.
92. Wu, M., L. G. Xu, X. Li, Z. Zhai, and H. B. Shu. 2002. AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis. J. Biol. Chem. 277:25617-25623.
93. Yagi, T. 1991. Bacterial NADH-quinone oxidoreductases. J. Bioenerg. Biomembr. 23:211-225.
94. Yagi, T., S. Di Bernardo, E. Nakamuro-Ogise, M. C. Kao, B. B. Seo, and A. Matsuno-Yagi. 2004. NADH dehydrogenases (NADH:quinone oxidoreductase), p. 15-40. In D. Zannoni (ed.), Respiration in Archaea and Bacteria, vol. 1. Kluwer Publishing, Dordrecht, The Netherlands.
95. Yagi, T., T. Yano, and A. Matsuno-Yagi. 1993. Characteristics of the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans as revealed by biochemical, biophysical, and molecular biological approaches. J. Bioenerg. Biomembr. 25:339-345.
96. Young, I. G., B. L. Rogers, H. D. Campbell, A. Jaworowski, and D. C. Shaw. 1981. Nucleotide sequence coding for the respiratory NADH dehydrogenase of Escherichia coli. UUG initiation codon. Eur. J. Biochem. 116:165-170.