Effects of site-directed mutations in Escherichia coli succinate dehydrogenase on the enzyme activity and production of superoxide radicals

Biochemistry and Cell Biology

Volumn 84, Issue 6, 2006, Pages 1013-1021

  Zhao, Zhongwei ^a   Rothery, Richard A ^a   Weiner, Joel H ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Mitochondria related diseases; Paraganglioma; Reactive oxygen species; Succinate dehydrogenase; Ubiquinone

Indexed keywords

BINDING SITES; CELLS; CONCENTRATION (PROCESS); DISEASES; ENZYME KINETICS; ESCHERICHIA COLI; OXIDATION;

MITOCHONDRIA RELATED DISEASES; PARAGANGLIOMA; REACTIVE OXYGEN SPECIES; SUCCINATE DEHYDROGENASE; UBIQUINONE;

MUTAGENESIS;

ESCHERICHIA COLI PROTEIN; FUMARIC ACID; HEME; REACTIVE OXYGEN METABOLITE; SUCCINATE DEHYDROGENASE; SUCCINIC ACID; SUPEROXIDE; UBIQUINONE;

BACTERIAL GENE; BACTERIAL STRAIN; BINDING SITE; CONFERENCE PAPER; ENZYME ACTIVITY; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENE MUTATION; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION; PARAGANGLIOMA; SITE DIRECTED MUTAGENESIS; SPECTROPHOTOMETRY;

BINDING SITES; ESCHERICHIA COLI; MUTAGENESIS, SITE-DIRECTED; MUTATION; PENTACHLOROPHENOL; SUCCINATE DEHYDROGENASE; SUPEROXIDES; UBIQUINONE;

ESCHERICHIA COLI;

EID: 33947358279     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/O06-188     Document Type: Conference Paper

References (51)

1. Ackrell, B.A., Kearney, E.B., and Singer, T.P. 1978. Mammalian succinate dehydrogenase. Methods Enzymol. 53: 466-483.
2. Astuti, D., Latif, F., Dallol, A., Dahia, P.L., Douglas, F., George, E., et al. 2001. Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am. J. Hum. Genet. 69: 49-54. doi:10.1086/321282.
3. Azzi, A., Montecucco, C., and Richter, C 1975. The use of acetylated ferricytochrome c for the detection of superoxide radicals produced in biological membranes. Biochem. Biophys. Res. Commun. 65: 597-603. doi:10.1016/S0006-291X(75)80188-4.
4. Baysal, B.E., Ferrell, R.E., Willett-Brozick, J.E., Lawrence, E.C., Myssiorek, D., Bosch, A., et al. 2000. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science (Washington, D.C.), 287: 848-851. doi:10.1126/science.287.5454.848.
5. Bourgeron, T., Rustin, P., Chretien, D., Birch-Machin, M., Bourgeois, M., Viegas-Pequignot, E., Munnich, A., and Rotig, A. 1995. Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nat. Genet. 11: 144-149. doi:10.1038/ng1095-144.
6. Briere, J.J., Favier, J., El Ghouzzi, V., Djouadi, F., Benit, P., Gimenez, A.P., and Rustin, P. 2005. Succinate dehydrogenase deficiency in human. Cell. Mol. Life Sci. 62: 2317-2324. doi:10.1007/s00018-005-5237-6.
7. Briere, J.J., Favier, J., Gimenez-Roqueplo, A.P., and Rustin, P. 2006. Tricarboxylic acid cycle dysfunction as a cause of human diseases and tumour formation. Am. J. Physiol. Cell Physiol., In press, doi:10.1152/ajpcell.00216. 2006.
8. Cecchini, G. 2003. Function and structure of complex II of the respiratory chain. Annu. Rev. Biochem. 72: 77-109. doi:10.1146/annurev. biochem.72.121801.161700.
9. Condon, C., Cammack, R., Patil, D.S., and Owen, P. 1985. The succinate dehydrogenase of Escherichia coli. Immunochemical resolution and biophysical characterization of a 4-subunit enzyme complex. J. Biol. Chem. 260: 9427-9434.
10. Dahia, P.L., Ross, K.N., Wright, M.E., Hayashida, C.Y., Santagata, S., Barontini, M., et al. 2005. A HIF1 alpha regulatory loop links hypoxia and mitochondrial signals in pheochromocytomas. PLoS Genet. 1: 72-80.
11. Depew, M.C., and Wan, J.K.S. 1988. Quinhydrones and semiquionoes. In The chemistry of quinonoid compounds. Edited by S. Patai and Z. Rappoport. John Wiley & Sons, Ltd, New York, pp. 963-1018.
12. Esposti, M.D. 2001. Assessing functional integrity of mitochondria in vitro and vivo. Methods Cell Biol. 65: 75-96.
13. Genova, M.L., Ventura, B., Giuliano, G., Bovina, C., Formiggini, G., Parenti Castelli, G., and Lenaz, G. 2001. The site of production of superoxide radical in mitochondrial Complex I is not a bound ubisemiquinone but presumably iron-sulfur cluster N2. FEBS Lett. 505: 364-368. doi:10.1016/S0014- 5793(01)02850-2.
14. Genova, M.L., Pich, M.M., Bernacchia, A., Bianchi, C., Biondi, A., Bovina, C., et al. 2004. The mitochondrial production of reactive oxygen species in relation to aging and pathology. Ann. N. Y. Acad. Sci. 1011: 86-100. doi:10.1196/annals.1293.010.
15. Gerald, D., Berra, E., Frapart, Y.M., Chan, D.A., Giaccia, A.J., Mansuy, D., et al. 2004. JunD reduces tumor angiogenesis by protecting cells from oxidative stress. Cell, 118: 781-794. doi:10.1016/j.cell.2004.08.025.
16. Gimenez-Roqueplo, A.P., Favier, J., Rustin, P., Mourad, J.J., Plouin, P.F., Corvol, P., Rotig, A., and Jeunemaitre, X. 2001. The R22X mutation of the SDHD gene in hereditary paraganglioma abolishes the enzymatic activity of complex II in the mitochondrial respiratory chain and activates the hypoxia pathway. Am. J. Hum. Genet. 69: 1186-1197. doi: 10.1086/324413.
17. Guo, J., and Lemire, B.D. 2003. The ubiquinone-binding site of the Saccharomyces cerevisiae succinate-ubiquinone oxidoreductase is a source of superoxide. J. Biol. Chem. 278: 47629-47635. doi:10.1074/jbc. M306312200.
18. Hagerhall, C., Magnitsky, S., Sled, V.D., Schroder, I., Gunsalus, R.P., Cecchini, G., and Ohnishi, T. 1999. An Escherichia coli mutant quinol:fumarate reductase contains an EPR-detectable semiquinone stabilized at the proximal quinone-binding site. J. Biol. Chem. 274: 26157-26164. doi:10.1074/jbc.274.37.26157.
19. Hatefi, Y. 1978. Resolution of complex II and isolation of succinate dehydrogenase (EC 1.3.99.1). Methods Enzymol. 53: 27-35.
20. Imlay, J.A., and Fridovich, I. 1991. Assay of metabolic superoxide production in Escherichia coli. J. Biol. Chem. 266: 6957-6965.
21. Ishii, N., Fujii, M., Hartman, P.S., Tsuda, M., Yasuda, K., Senoo-Matsuda, N., et al. 1998. A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature (London), 394: 694-697. doi: 10.1038/29331.
22. Ishii, T., Yasuda, K., Akatsuka, A., Hino, O., Hartman, P.S., and Ishii, N. 2005. A mutation in the SDHC gene of complex II increases oxidative stress, resulting in apoptosis and tumorigenesis. Cancer Res. 65: 203-209.
23. Ishii, N., Ishii, T., and Hartman, P.S. 2006. The role of the electron transport gene SDHC on lifespan and cancer. Exp. Gerontol., In press.
24. Iverson, T.M., Luna-Chavez, C., Cecchini, G., and Rees, D.C. 1999. Structure of the Escherichia coli fumarate reductase respiratory complex. Science (Washington, D.C.), 284: 1961-1966. doi:10.1126/science.284. 5422.1961.
25. Kinnula, V.L., and Crapo, J.D. 2004. Superoxide dismutases in malignant cells and human tumors. Free Radic. Biol. Med. 36: 718-744. doi:10.1016/j.freeradbiomed.2003.12.010.
26. Kita, K., Vibat, C.R., Meinhardt, S., Guest, J.R., and Gennis, R.B. 1989. One-step purification from Escherichia coli of complex II (succinate: ubiquinone oxidoreductase) associated with succinate-reducible cytochrome b556. J. Biol. Chem. 264: 2672-2677.
27. Lenaz, G., Fato, R., Baracca, A., and Genova, M.L. 2004. Mitochondrial quinone reductases: complex I. Methods Enzymol. 382: 3-20.
28. Maklashina, E., Berthold, D.A., and Cecchini, G. 1998. Anaerobic expression of Escherichia coli succinate dehydrogenase: functional replacement of fumarate reductase in the respiratory chain during anaerobic growth. J. Bacteriol. 180: 5989-5996.
29. Maklashina, E., Rothery, R.A., Weiner, J.H., and Cecchini, G. 2001. Retention of heme in axial ligand mutants of succinate-ubiquinone xxidoreductase (complex II) from Escherichia coli. J. Biol. Chem. 276: 18968-18976. doi:10.1074/jbc.M011270200.
30. Markwell, M.A.D., Haas, S.M., Bieber, L.L., and Tolbert, N.E. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87: 206-210. doi:10.1016/0003-2697(78)90586-9.
31. McCord, J.M., and Fridovich, I. 1969. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244: 6049-6055.
32. Messner, K.R., and Imlay, J.A. 2002a. In vitro quantitation of biological superoxide and hydrogen peroxide generation. Methods Enzymol. 349: 354-361.
33. Messner, K.R., and Imlay, J.A. 2002b. Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. J. Biol. Chem. 277: 42563-42571. doi:10.1074/jbc. M204958200.
34. Niemann, S., and Muller, U. 2000. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat. Genet. 26: 268-270.
35. Ohnishi, T., King, T.E., Salerno, J.C., Blum, H., Bowyer, J.R., and Maida, T. 1981. Thermodynamic and electron paramagnetic resonance characterization of flavin in succinate dehydrogenase. J. Biol. Chem. 256: 5577-5582.
36. Page, C.C., Moser, C.C., Chen, X., and Dutton, P.L. 1999. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature (London), 402: 47-52.
37. Parfait, B., Chretien, D., Rotig, A., Marsac, C., Munnich, A., and Rustin, P. 2000. Compound heterozygous mutations in the flavoprotein gene of the respiratory chain complex II in a patient with Leigh syndrome. Hum. Genet. 106: 236-243. doi:10.1007/s004390051033.
38. Paulsen, K.E., Stankovich, M.T., and Orville, A.M. 1993. Electron paramagnetic resonance spectroelectrochemical titration. Methods Enzymol. 227: 396-411.
39. Pollard, P.J., Briere, J.J., Alam, N.A., Barwell, J., Barclay, E., Wortham, N.C., et al. 2005. Accumulation of Krebs cycle intermediates and over-expression of HIF1 alpha in tumours which result from germline FH and SDH mutations. Hum. Mol. Genet. 14: 2231-2239. doi:10.1093/hmg/ddi227.
40. Rothery, R.A., Seime, A.M., Spiers, A.M., Maklashina, E., Schroder, I., Gunsalus, R.P., Cecchini, G., and Weiner, J.H. 2005. Defining the Q-site of Escherichia coli fumarate reductase by site-directed mutagenesis, fluorescence quench titrations and EPR spectroscopy. FEBS J. 272: 313-326. doi:10.1111/j.1742-4658.2004.04469.x.
41. Rustin, P., and Rotig, A. 2002. Inborn errors of complex II-unusual human mitochondrial diseases. Biochim. Biophys. Acta, 1553: 117-122.
42. Rustin, P., Munnich, A., and Rotig, A. 2002. Succinate dehydrogenase and human diseases: new insights into a well-known enzyme. Eur. J. Hum. Genet. 10: 289-291. doi:10.1038/sj.ejhg.5200793.
43. Ruzicka, F.J., Beinert, H., Schepler, K.L., Dunham, W.R., and Sands, R.H. 1975. Interaction of ubisemiquinone with a paramagnetic component in heart tissue. Proc. Natl. Acad. Sci. U.S.A. 72: 2886-2890. doi:10.1073/pnas.72. 8.2886.
44. Selak, M.A., Armour, S.M., MacKenzie, E.D., Boulahbel, H., Watson, D.G., Mansfield, K.D., et al. 2005. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell, 7: 77-85. doi:10.1016/j.ccr.2004.11.022.
45. Senoo-Matsuda, N., Yasuda, K., Tsuda, M., Ohkubo, T., Yoshimura, S., Nakazawa, H., Hartman, P.S., and Ishii, N. 2001. A defect in the cytochrome b large subunit in complex II causes both superoxide anion overproduction and abnormal energy metabolism in Caenorhabditis elegans. J. Biol. Chem. 276: 41553-41558. doi:10.1074/jbc.M104718200.
46. Tran, Q.M., Rothery, R.A., Maklashina, E., Cecchini, G., and Weiner, J.H. 2006. The quinone binding site in Escherichia coli succinate dehydrogenase is required for electron transfer to the heme b. J. Biol. Chem. In press.
47. Vanharanta, S., Pollard, P.J., Lehtonen, H.J., Laiho, P., Sjoberg, J., Leminen, A., et al. 2006. Distinct expression profile in fumarate-hydratase- deficient uterine fibroids. Hum. Mol. Genet. 15: 97-103.
48. Vibat, C.R., Cecchini, G., Nakamura, K., Kita, K., and Gennis, R.B. 1998. Localization of histidine residues responsible for heme axial ligation in cytochrome b556 of complex II (succinate: ubiquinone oxidoreductase) in Escherichia coli. Biochemistry, 37: 4148-4159. doi:10.1021/bi9716635.
49. Waldeck, A.R., Stowell, M.H., Lee, H.K., Hung, S.C., Matsson, M., Hederstedt, L., Ackrell, B.A., and Chan, S.I. 1997. Electron paramagnetic resonance studies of succinate:ubiquinone oxidoreductase from Paracoccus denitrificans. Evidence for a magnetic interaction between the 3Fe-4S cluster and cytochrome b. J. Biol. Chem. 272: 19373-19382. doi:10.1074/jbc.272. 31.19373.
50. Westenberg, D.J., Gunsalus, R.P., Ackrell, B.A.C., Sices, H., and Cecchini, G. 1993. Escherichia coli fumarate reductase frdC and frdD mutants. Identification of amino acid residues involved in catalytic activity with quinones. J. Biol. Chem. 268: 815-822.
51. Yankovskaya, V., Horsefield, R., Tornroth, S., Luna-Chavez, C., Miyoshi, H., Leger, C., et al. 2003. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science (Washington, D.C.), 299: 700-704. doi:10.1126/science.1079605.