Contribution of the FAD and quinone binding sites to the production of reactive oxygen species from Ascaris suum mitochondrial complex II

Mitochondrion

Volumn 10, Issue 2, 2010, Pages 158-165

  Paranagama, Madhavi P ^a   Sakamoto, Kimitoshi ^a   Amino, Hisako ^a   Awano, Mutsumi ^a   Miyoshi, Hideto ^b   Kita, Kiyoshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Ascaris suum; Complex II; Reactive oxygen species

Indexed keywords

FLAVINE ADENINE NUCLEOTIDE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUPEROXIDE DISMUTASE;

ARTICLE; ASCARIS SUUM; BINDING SITE; CONTROLLED STUDY; ENERGY YIELD; ENZYME ACTIVITY; ENZYME METABOLISM; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY CHAIN;

ANIMALS; ASCARIS SUUM; BENZOQUINONES; BINDING SITES; ELECTRON TRANSPORT COMPLEX II; FLAVIN-ADENINE DINUCLEOTIDE; LARVA; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

ASCARIS SUUM; ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 76049086567     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mito.2009.12.145     Document Type: Article

References (56)

1. Ackrell B.A. Cytopathies involving mitochondrial complex II. Mol. Aspects. Med. 23 (2002) 369-384
2. Amino H., Osanai A., Miyadera H., Shinjyo N., Tomitsuka E., Taka H., Mineki R., Murayama K., Takamiya S., Aoki T., Miyoshi H., Sakamoto K., Kojima S., and Kita K. Isolation and characterization of the stage-specific cytochrome b small subunit (CybS) of Ascaris suum complex II from the aerobic respiratory chain of larval mitochondria. Mol. Biochem. Parasitol. 128 (2003) 175-186
3. Amino H., Wang H., Hirawake H., Saruta F., Mizuchi D., Mineki R., Shindo N., Murayama K., Takamiya S., Aoki T., Kojima S., and Kita K. Stage-specific isoforms of Ascaris suum complex. II: The fumarate reductase of the parasitic adult and the succinate dehydrogenase of free-living larvae share a common iron-sulfur subunit. Mol. Biochem. Parasitol. 106 (2000) 63-76
4. Astuti D., Latif F., Dallol A., Dahia P.L., Douglas F., George E., Skoldberg F., Husebye E.S., Eng C., and Maher E.R. Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am. J. Hum. Genet. 69 (2001) 49-54
5. Azzi A., Montecucco C., and Richter C. The use of acetylated ferricytochrome c for the detection of superoxide radicals produced in biological membranes. Biochem. Biophys. Res. Commun. 65 (1975) 597-603
6. Bayley J.P., van Minderhout I., Weiss M.M., Jansen J.C., Oomen P.H., Menko F.H., Pasini B., Ferrando B., Wong N., Alpert L.C., Williams R., Blair E., Devilee P., and Taschner P.E. Mutation analysis of SDHB and SDHC: novel germline mutations in sporadic head and neck paraganglioma and familial paraganglioma and/or pheochromocytoma. BMC Med. Genet. (2006) 10-1186/1471-2350-7-1
7. Baysal B.E., Ferrell R.E., Willett-Brozick J.E., Lawrence E.C., Myssiorek D., Bosch A., van der Mey A., Taschner P.E., Rubinstein W.S., Myers E.N., Richard III C.W., Cornelisse C.J., Devilee P., and Devlin B. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287 (2000) 848-851
8. Baysal B.E., Willett-Brozick J.E., Lawrence E.C., Drovdlic C.M., Savul S.A., McLeod D.R., Yee H.A., Brackmann D.E., Slattery III W.H., Myers E.N., Ferrell R.E., and Rubinstein W.S. Prevalence of SDHB, SDHC, and SDHD germline mutations in clinic patients with head and neck paragangliomas. J. Med. Genet. 39 (2002) 178-183
9. Bourgeron T., Rustin P., Chretien D., Birch-Machin M., Bourgeois M., Viegas-Pequignot E., Munnich A., and Rotig A. Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nat. Genet. 11 (1995) 144-149
10. Briere J.J., Favier J., Benit P., El Ghouzzi V., Lorenzato A., Rabier D., Di Renzo M.F., Gimenez-Roqueplo A.P., and Rustin P. Mitochondrial succinate is instrumental for HIF1alpha nuclear translocation in SDHA-mutant fibroblasts under normoxic conditions. Hum. Mol. Genet. 14 (2005) 3263-3269
11. Cecchini G., Schroder I., Gunsalus R.P., and Maklashina E. Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochim. Biophys. Acta. 1553 (2002) 140-157
12. Cervera A.M., Apostolova N., Crespo F.L., Mata M., and McCreath K.J. Cells silenced for SDHB expression display characteristic features of the tumor phenotype. Cancer Res. 68 (2008) 4058-4067
13. Chen Q., Vazquez E.J., Moghaddas S., Hoppel C.L., and Lesnefsky E.J. Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 278 (2003) 36027-36031
14. Eng C., Kiuru M., Fernandez M.J., and Aaltonen L.A. A role for mitochondrial enzymes in inherited neoplasia and beyond. Nat. Rev. Cancer 3 (2003) 193-202
15. Eto Y., Kang D., Hasegawa E., Takeshige K., and Minakami S. Succinate-dependent lipid peroxidation and its prevention by reduced ubiquinone in beef heart submitochondrial particles. Arch. Biochem. Biophys. 295 (1992) 101-106
16. Guo J., and Lemire B.D. The ubiquinone-binding site of the Saccharomyces cerevisiae succinate-ubiquinone oxidoreductase is a source of superoxide. J. Biol. Chem. 278 (2003) 47629-47635
17. Guzy R.D., Sharma B., Bell E., Chandel N.S., and Schumacker P.T. Loss of the SdhB, but Not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol. Cell Biol. 28 (2008) 718-731
18. Hirst J., King M.S., and Pryde K.R. The production of reactive oxygen species by complex I. Biochem. Soc. Trans. 36 (2008) 976-980
19. Horsefield R., Yankovskaya V., Sexton G., Whittingham W., Shiomi K., Omura S., Byrne B., Cecchini G., and Iwata S. Structural and computational analysis of the quinone-binding site of complex II (succinate-ubiquinone oxidoreductase): a mechanism of electron transfer and proton conduction during ubiquinone reduction. J. Biol. Chem. 281 (2006) 7309-7316
20. Huang J., and Lemire B.D. Mutations in the C. elegans succinate dehydrogenase iron-sulfur subunit promote superoxide generation and premature aging. J. Mol. Biol. 387 (2009) 559-569
21. Huang L.S., Shen J.T., Wang A.C., and Berry E.A. Crystallographic studies of the binding of ligands to the dicarboxylate site of Complex II, and the identity of the ligand in the "oxaloacetate-inhibited" state. Biochim. Biophys. Acta 1757 (2006) 1073-1083
22. Imlay J.A., and Fridovich I. Assay of metabolic superoxide production in Escherichia coli. J. Biol. Chem. 266 (1991) 6957-6965
23. Indo H.P., Davidson M., Yen H.C., Suenaga S., Tomita K., Nishii T., Higuchi M., Koga Y., Ozawa T., and Majima H.J. Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion 7 (2007) 106-118
24. Ishii T., Sakurai T., Usami H., and Uchida K. Oxidative modification of proteasome: identification of an oxidation-sensitive subunit in 26S proteasome. Biochemistry 44 (2005) 13893-13901
25. Iwata F., Shinjyo N., Amino H., Sakamoto K., Islam M.K., Tsuji N., and Kita K. Change of subunit composition of mitochondrial complex II (succinate-ubiquinone reductase/quinol-fumarate reductase) in Ascaris suum during the migration in the experimental host. Parasitol. Int. 57 (2008) 54-61
26. Jezek P., and Hlavata L. Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int. J. Biochem. Cell Biol. 37 (2005) 2478-2503
27. Kita K., Hirawake H., Miyadera H., Amino H., and Takeo S. Role of complex II in anaerobic respiration of the parasite mitochondria from Ascaris suum and Plasmodium falciparum. Biochim. Biophys. Acta 1553 (2002) 123-139
28. Kita K., and Takamiya S. Electron-transfer complexes in Ascaris mitochondria. Adv. Parasitol. 51 (2002) 95-131
29. Kita K., Shiomi K., and Õmura S. Parasitology in Japan: advances in drug discovery and biochemical studies. Trends. Parasitol. 23 (2007) 223-229
30. Kuramochi T., Hirawake H., Kojima S., Takamiya S., Furushima R., Aoki T., Komuniecki R., and Kita K. Sequence comparison between the flavoprotein subunit of the fumarate reductase (complex II) of the anaerobic parasitic nematode, Ascaris suum and the succinate dehydrogenase of the aerobic, free-living nematode, Caenorhabditis elegans. Mol. Biochem. Parasitol. 68 (1994) 177-187
31. Lancaster C.R.D. Structure and function of succinate: quinone oxidoreductases and the role of quinol: fumarate reductases in fumarate respiration. In: Zannoni D. (Ed). Respiration in Archaea and Bacteria: Diversity of Prokaryotic Electron Transport Carriers (2004), Kluwer Academic Publishers, The Netherlands 57-85
32. Liu Y., Fiskum G., and Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80 (2002) 780-787
33. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
34. Matsumoto J., Sakamoto K., Shinjyo N., Kido Y., Yamamoto N., Yagi K., Miyoshi H., Nonaka N., Katakura K., Kita K., and Oku Y. Anaerobic NADH-fumarate reductase system is predominant in the respiratory chain of Echinococcus multilocularis, providing a novel target for the chemotherapy of alveolar echinococcosis. Antimicrob. Agents Chemother. 52 (2008) 164-170
35. Matsuno-Yagi A., and Hatefi Y. Studies on the mechanism of oxidative phosphorylation. Catalytic site cooperativity in ATP synthesis. J. Biol. Chem. 260 (1985) 11424-11427
36. Messner K.R., and Imlay J.A. Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. J. Biol. Chem. 277 (2002) 42563-42571
37. Miyadera H., Shiomi K., Ui H., Yamaguchi Y., Masuma R., Tomoda H., Miyoshi H., Osanai A., Kita K., and Omura S. Atpenins, potent and specific inhibitors of mitochondrial complex II (succinate-ubiquinone oxidoreductase). Proc. Natl. Acad. Sci. USA 100 (2003) 473-477
38. Mohanty J.G., Jaffe J.S., Schulman E.S., and Raible D.G. A highly sensitive fluorescent micro-assay of H2O2 release from activated human leukocytes using a dihydroxyphenoxazine derivative. J. Immunol. Methods 202 (1997) 133-141
39. Muller F.L., Liu Y., Abdul-Ghani M.A., Lustgarten M.S., Bhattacharya A., Jang Y.C., and Van Remmen H. High rates of superoxide production in skeletal-muscle mitochondria respiring on both complex I- and complex II-linked substrates. Biochem. J. 409 (2008) 491-499
40. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 417 (2009) 1-13
41. Ni Y., Zbuk K.M., Sadler T., Patocs A., Lobo G., Edelman E., Platzer P., Orloff M.S., Waite K.A., and Eng C. Germline mutations and variants in the succinate dehydrogenase genes in Cowden and Cowden-like syndromes. Am. J. Hum. Genet. 83 (2008) 261-268
42. Paddenberg R., Ishaq B., Goldenberg A., Faulhammer P., Rose F., Weissmann N., Braun-Dullaeus R.C., and Kummer W. Essential role of complex II of the respiratory chain in hypoxia-induced ROS generation in the pulmonary vasculature. Am. J. Physiol. Lung. Cell. Mol. Physiol. 284 (2003) L710-719
43. Saruta F., Hirawake H., Takamiya S., Ma Y.C., Aoki T., Sekimizu K., Kojima S., and Kita K. Cloning of a cDNA encoding the small subunit of cytochrome b558 (cybS) of mitochondrial fumarate reductase (complex II) from adult Ascaris suum. Biochim. Biophys. Acta. 1276 (1996) 1-5
44. Saruta F., Kuramochi T., Nakamura K., Takamiya S., Yu Y., Aoki T., Sekimizu K., Kojima S., and Kita K. Stage-specific isoforms of complex II (succinate-ubiquinone oxidoreductase) in mitochondria from the parasitic nematode, Ascaris suum. J. Biol. Chem. 270 (1995) 928-932
45. Senoo-Matsuda N., Yasuda K., Tsuda M., Ohkubo T., Yoshimura S., Nakazawa H., Hartman P.S., and Ishii N. 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 (2001) 41553-41558
46. Selak M.A., Armour S.M., MacKenzie E.D., Boulahbel H., Watson D.G., Mansfield K.D., Pan Y., Simon M.C., Thompson C.B., and Gottlieb E. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7 (2005) 77-85
47. Shinjyo N., and Kita K. Relationship between reactive oxygen species and heme metabolism during the differentiation of Neuro2a cells. Biochem. Biophys. Res. Commun. 358 (2007) 130-135
48. St-Pierre J., Buckingham J.A., Roebuck S.J., and Brand M.D. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277 (2002) 44784-44790
49. Sun F., Huo X., Zhai Y., Wang A., Xu J., Su D., Bartlam M., and Rao Z. Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121 (2005) 1043-1057
50. Szeto S.S., Reinke S.N., Sykes B.D., and Lemire B.D. Ubiquinone-binding site mutations in the Saccharomyces cerevisiae succinate dehydrogenase generate superoxide and lead to the accumulation of succinate. J. Biol. Chem. 282 (2007) 27518-27526
51. Takamiya S., Furushima R., and Oya H. Electron transfer complexes of Ascaris suum muscle mitochondria. II. Succinate-coenzyme Q reductase (complex II) associated with substrate-reducible cytochrome b558. Biochim. Biophys. Acta 848 (1986) 99-107
52. Van Hellmond J.J., van der Klei A., van Weelden S.W.H., and Tielens A.G.M. Biochemical and evolutionary aspects of anaerobically functioning bacteria. Phil. Trans. R. Soc. B. 358 (2003) 205-215
53. Yamashita T., Ino T., Miyoshi H., Sakamoto K., Osanai A., Nakamaru-Ogiso E., and Kita K. Rhodoquinone reaction site of mitochondrial complex I, in parasitic helminth, Ascaris suum. Biochim. Biophys. Acta 1608 (2004) 97-103
54. Yankovskaya V., Horsefield R., Tornroth S., Luna-Chavez C., Miyoshi H., Leger C., Byrne B., Cecchini G., and Iwata S. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299 (2003) 700-704
55. Zhang L., Yu L., and Yu C.A. Generation of superoxide anion by succinate-cytochrome c reductase from bovine heart mitochondria. J. Biol. Chem. 273 (1998) 33972-33976
56. Zhao Z., Rothery R.A., and Weiner J.H. Effects of site-directed mutations in Escherichia coli succinate dehydrogenase on the enzyme activity and production of superoxide radicals. Biochem. Cell Biol. 84 (2006) 1013-1021