Type II Fp of human mitochondrial respiratory complex II and its role in adaptation to hypoxia and nutrition-deprived conditions

Mitochondrion

Volumn 13, Issue 6, 2013, Pages 602-609

  Sakai, Chika ^a,d   Tomitsuka, Eriko ^a   Miyagishi, Makoto ^b   Harada, Shigeharu ^c   Kita, Kiyoshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c KYOTO INSTITUTE OF TECHNOLOGY   (Japan)

^d NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

Complex II; Flavoprotein; Fumarate respiration; Human mitochondria; Succinate ubiquinone reductase

Indexed keywords

FLAVOPROTEIN; ISOPROTEIN; MESSENGER RNA; SUCCINATE DEHYDROGENASE (UBIQUINONE); TYPE I FLAVOPROTEIN; TYPE II FLAVOPROTEIN; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; CANCER TISSUE; CELL FUNCTION; CELL HYPOXIA; CELL PH; CELLULAR ADAPTATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBUNIT; FETUS (ANATOMY); GENE EXPRESSION; HUMAN; HUMAN CELL; ISCHEMIA; NUTRITION; NUTRITION DEPRIVATION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

0.1MM 5,5′-DITHIOBIS-(2-NITROBENZOIC ACID); 2,6-DICHLOROPHENOLINDOPHENOL; 3-NITROPROPIONIC ACID; 3-NP; 50% INHIBITORY CONCENTRATION; COMPLEX II; DCIP; DTNB; FLAVOPROTEIN; FP; FUMARATE RESPIRATION; HIF-1Α; HUMAN MITOCHONDRIA; HYPOXIA-INDUCIBLE FACTOR-1Α; IC(50); QFR; QUINOL-FUMARATE REDUCTASE; SDHAF1; SDHAF2; SML; SQR; SUCCINATE-DEHYDROGENASE ASSEMBLY FACTOR 1; SUCCINATE-DEHYDROGENASE ASSEMBLY FACTOR 2; SUCCINATE-UBIQUINONE REDUCTASE; SUCROSE MONOLAURATE;

ADAPTATION, PHYSIOLOGICAL; ANOXIA; BASE SEQUENCE; DNA PRIMERS; ELECTRON TRANSPORT COMPLEX II; HUMANS; HYDROGEN-ION CONCENTRATION; MALNUTRITION; MITOCHONDRIA; POLYMERASE CHAIN REACTION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, MESSENGER;

EID: 84884390578     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2013.08.009     Document Type: Article

References (55)

1. Ackrell B.A., Kearney E.B., Mayr M. Role of oxalacetate in the regulation of mammalian succinate dehydrogenase. J. Biol. Chem. 1974, 249:2021-2027.
2. Amino H., Wang H., Hirawake H., Saruta F., Mizuchi D., Mineki R., Shindo N., Murayama K., Takamiya S., Aoki T., Kojima S., Kita K. Stage-specific isoforms of Ascaris suum complex II: the fuma rate reductase of the parasitic adult and the succinate dehydrogenase of free-living larvae share a common iron-sulfur subunit. Mol. Biochem. Parasitol. 2000, 106:63-76.
3. Balut C., vandeVen M., Despa S., Lambrichts I., Ameloot M., Steels P., Smets I. Measurement of cytosolic and mitochondrial pH in living cells during reversible metabolic inhibition. Kidney Int. 2008, 73:226-232.
4. + concentration, measured by CoroNa Red, in the protection of metabolically inhibited MDCK cells. J. Am. Soc. Nephrol. 2005, 16:3490-3497.
5. Bayley J.P., Devilee P., Taschner E.M.P. The SDH mutation database: an online resource for succinate dehydrogenase sequence variants involved in pheochromocytoma, paraganglioma and mitochondrial complex II deficiency. BMC Med. Genet. 2005, 6:391.
6. Baysal B.E. On the association of succinate dehydrogenase mutations with hereditary paraganglioma. Trends Endocrinol. Metab. 2003, 14:453-459.
7. Baysal B.E., Lawrence E.C., Ferrell R.E. Sequence variation in human succinate dehydrogenase genes: evidence for long-term balancing selection on SDHA. BMC Biol. 2007, 5:12.
8. Bourgeron T., Rustin P., Chretien D., Birch-Machin M., Bourgeois M., Viegas-Pequignot E., Munnich A., Rotig A. Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nat. Genet. 1995, 11:144-149.
9. Briere J.J., Favier J., Benit P., Ghouzzi V., Lorenzato A., Rabier D., Flavia M., Gimenez-Roqueplo A.P., Rustin P. Mitochondrial succinate is instrumental for HIF1a nuclear translocation in SDHA-mutant fibroblasts under normoxic conditions. Hum. Mol. Genet. 2005, 14:3263-3269.
10. Brockmann K., Bjornstad A., Dechent P., Korenke C.G., Smeitink J., Frans Trijbels J.M., Athanassopoulos S., Villagran R., Skjeldal O.H., Wilichowski E., Frahm J., Hanefeld F. Succinate in dystrophic white matter: a proton magnetic resonance spectroscopy finding characteristic for complex II deficiency. Ann. Neurol. 2002, 52:38-46.
11. Burnichon N., Brière J.J., Libe R., Vescovo L., Riviere J., Tissier F., Jouanno E., Jeunemaitre X., Benit P., Tzagoloff A., Rustin P., Bertherat J., Favier J., Gimenez-Roqueplo A.P. SDHA is a tumor suppressor gene causing paraganglioma. Hum. Mol. Genet. 2010, 19:3011-3020.
12. Busch H., Potter V.R. Succinate accumulation in vivo following injection of malonate. J. Biol. Chem. 1952, 198:71-77.
13. 2+ increase depends on mitochondria in a human proximal renal cell line. Am. J. Physiol. Renal Physiol. 2007, 293:533-540.
14. Eng C., Kiuru M., Fernandez M.J., Aaltonen L.A. A role for hypoxic mitochondrial enzymes in inherited neoplasia and beyond. Nat. Rev. Cancer 2003, 3:193-202.
15. Ghezzi D., Goffrini P., Uziel G., Horvath R., Klopstock T., Lochmüller H., D'Adamo P., Gasparini P., Strom T.M., Prokisch H., Invernizzi F., Ferrero I., Zeviani M. SDHAF1, encoding a LYR complex-II specific assembly factor, is mutated in SDH-defective infantile leukoencephalopathy. Nat. Genet. 2009, 41:654-656.
16. Hao H.X., Khalimonchuk O., Schraders M., Dephoure N., Bayley J.P., Kunst H., Devilee P., Cremers C.W., Schiffman J.D., Bentz B.G., Gygi S.P., Winge D.R., Kremer H., Rutter J. SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 2009, 325:1139-1142.
17. Harada S., Inaoka D.K., Ohmori J., Kita K. Diversity of parasite complex II. Biochim. Biophys. Acta 2013, 1827:658-667.
18. Huang L.S., Sun G., Cobessi D., Wang A.C., Shen J.T., Tung E.Y., Anderson V.E., Berry E.A. 3-nitropropionic acid is a suicide inhibitor of mitochondrial respiration that, upon oxidation by complex II, forms a covalent adduct with a catalytic base arginine in the active site of the enzyme. J. Biol. Chem. 2006, 281(9):5965-5972.
19. Ishii N., Ishii T., Hartman P.S. The role of the electron transport SDHC gene on lifespan and cancer. Mitochondrion 2007, 7:24-38.
20. Iverson T.M., Maklashina E., Cecchini G. Structural basis for malfunction in complex II. J. Biol. Chem. 2012, 287:35430-35438.
21. Izuishi K., Kato K., Ogura T., Kinoshita T., Esumi H. Remarkable tolerance of tumor cells to nutrient deprivation: possible new biochemical target for cancer therapy. Cancer Res. 2000, 60:6201-6207.
22. Killian J.K., Kim S.Y., Miettinen M., et al. Succinate dehydrogenase mutation underlies global epigenomic divergence in gastrointestinal stromal tumor. Cancer Discov. 2013, 10:2159-8290.
23. Kingdom J.C., Kaufmann P. Oxygen and placental vascular development. Adv. Exp. Med. Biol. 1999, 474:259-275.
24. Kita K., Hirawake H., Miyadera H., Amino H., Takeo S. Role of complex II in anaerobic respiration of the parasite mitochondria from Ascaris suum and Plasmodium falciparum. Biochem. Biophys. Acta 2002, 1553:123-139.
25. Kita K., Shiomi K., Õmura S. Parasitology in Japan: advances in drug discovery and biochemical studies. Trends Parasitol. 2007, 23:223-229.
26. Kler R.S., Jackson S., Bartkett K., Bindoff L.A., Eaton S., Pourfarzan M., Frerman F.E., Gooldman S.I., Watmough N.J., Turnbull D.M. Quantitation of Acyl-CoA and Acylcarnitine esters accumulated during abnormal mitochondria fatty acid oxidation. J. Biol. Chem. 1991, 266:22932-22938.
27. Kroger A., Geisler V., Lemma E., Theis F., Lenger R. Bacterial fumarate respiration. Arch. Microbiol. 1992, 158:311-314.
28. Kuramochi T., Hirawake H., Kojima S., Takamiya S., Furushima R., Aoki T., Komuniecki R., 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 theaerobic, free-living nematode, Caenorhabditis elegans. Mol. Biochem. Parasitol. 1994, 68:177-187.
29. Llopis J., McCaffery J.M., Miyawaki A., Farquhar M.G., Tsien R.Y. Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. \Proc. Natl. Acad. Sci. U. S. A. 1998, 95:6803-6808.
30. McGovern S., Pan J., Oliver G., Cutz E., Yeger H. The role of hypoxia and neurogenic genes (Mash-1 and Prox-1) in the developmental programming and maturation of pulmonary neuroendocrine cells in fetal mouse lung. Lab. Invest. 2010, 90:180-195.
31. Miyadera H., Shiomi K., Ui H., Yamaguchi Y., Masuma R., Tomoda H., Miyoshi H., Osanai A., Kita K., Ōmura S. Atpenins, potent and specific inhibitors of mitochondrial complex II (succinate-ubiquinone oxidoreductase). Proc. Natl. Acad. Sci. U. S. A. 2003, 100:473-477.
32. Miyagishi M., Taira K. U6 promoter-driven siRNAs with four uridine 3' overhangs efficiently suppress targeted gene expression in mammalian cells. Nat. Biotechnol. 2002, 20:497-500.
33. Parfait B., Chretien D., Rötig A., Marsac C., Munnich A., Rustin P. Compound heterozygous mutations in the flavoprotein gene of the respiratory chain complex II in a patient with Leigh syndrome. Hum. Genet. 2000, 106:236-243.
34. Pollard P.J., Wortham N.C., Tomlinson I.P. The TCA cycle and tumorigenesis: the examples of fumarate hydratase and succinate dehydrogenase. Ann. Med. 2003, 35:632-639.
35. Quinlan C.L., Orr A.L., Perevoshchikova I.V., Treberg J.R., Ackrell B.A., Brand M.D. Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J. Biol. Chem. 2012, 27255-27264.
36. Ramshesh V.K., Lemasters J.J. Imaging of mitochondrial pH using SNARF-1. Methods Mol. Biol. 2012, 810:243-248.
37. Rustin P., Rotig A. Inborn errors of complex II-unusual human mitochondrial diseases. Biochim. Biophys. Acta 2002, 1553:117-122.
38. Rutter J., Winge D.R., Schiffman J.D. Succinate dehydrogenase - assembly, regulation and role in human disease. Mitochondrion 2010, 10:393-401.
39. Sakai C., Tomitsuka E., Esumi H., Harada S., Kita K. Mitochondrial fumarate reductase as a target of chemotherapy: from parasites to cancer cells. Biochim. Biophys. Acta 2012, 820:643-651.
40. Salvi M., Morrice N., Brunati A., Toninello A. Identification of the flavoprotein of succinate dehydrogenase and aconitase as in vitro mitochondrial substrates of Fgr tyrosine kinase. FEBS Lett. 2007, 581:5579-5585.
41. Saruta F., Hirawake H., Takamiya S., Ma Y.C., Aoki T., Sekimizu K., Kojima S., 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 1996, 1276:1-5.
42. Schwarz D.S., Ding H., Kennington L., Moore J.T., Schelter J., Burchard J., Linsley P.S., Aronin N., Xu Z., Zamore P.D. Designing siRNA that distinguish between genes that differ by a single nucleotide. PLoS Genet. 2006, 2:e140.
43. 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., Gottlieb E. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 2005, 7:77-85.
44. Shimizu H., Osanai A., Sakamoto K., Inaoka D.K., Shiba T., Harada S., Kita K. Crystal structure of mitochondrial quinol-fumarate reductase from the parasitic nematode Ascaris suum. J. Biochem. 2012, 151:589-592.
45. Sun F., Huo X., Zhai Y., Wang A., Xu J., Su D., Bartlam M., Rao Z. Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 2005, 121(7):1043-1057.
46. Takahashi M., Watanabe S., Murata M., Furuya H., Kanazawa I., Wada K., Hohjoh H. Tailor-made RNAi knockdown against triplet repeat disease-causing alleles. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:21731-21736.
47. Toma I., Kang J.J., Sipos A., Vargas S., Bansal E., Hanner F., Meer E., Peti-Peterdi J. Succinate receptor GPR91 provides a direct link between high glucose levels and renin release in murine and rabbit kidney. J. Clin. Invest. 2008, 118:2526-2534.
48. Tomitsuka E., Hirawake H., Goto Y., Taniwaki M., Harada S., Kita K. Direct evidence for two distinct forms of the flavoprotein subunit of human mitochondrial complex II (succinate-ubiquinone reductase). J. Biochem. 2003, 134:191-195.
49. Tomitsuka E., Goto Y., Taniwaki M., Kita K. Direct evidence for expression of type II flavoprotein subunit in human complex II (succinate-ubiquinone reductase). Biochem. Biophys. Res. Commun. 2003, 311:74-79.
50. Tomitsuka E., Kita K., Esumi H. Regulation of succinate-ubiquinone reductase and fumarate reductase activities in human complex II by phosphorylation of its flavoprotein subunit. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 2009, 85:258-265.
51. Tomitsuka E., Kita K., Esumi H. The NADH-fumarate reductase system, a novel mitochondrial energy metabolism, is a new target for anticancer therapy in tumor microenvironments. Ann. N. Y. Acad. Sci. 2011, 201:44-49.
52. Tomitsuka E., Kita K., Esumi H. An anticancer agent, pyrvinium pamonate inhibits the NADH-fumarate system-a unique mitochondrial energy metabolism in tumor microenvironments. J. Biochem. 2012, 52:171-183.
53. Van Coster R., Seneca S., Smet J., Van Hecke R., Gerlo E., Devreese B., Van Beeumen J., Leroy J.G., De Meirleir L., Lissens W. Homozygous Gly555Glu mutation in the nuclear-encoded 70kDa flavoprotein gene causes instability of the respiratory chain complex II. Am. J. Med. Genet. A 2003, 120:13-18.
54. Wojtovich A.P., Smith C.O., Haynes C.M., Nehrke K.W., Brookes P.S. Physiological consequences of complex II inhibition for aging, disease, and the mKATP channel. Biochim. Biophys. Acta 2013, 1827:598-611.
55. Yu D., Pendergraff H., Liu J., Kordasiewicz H.B., Cleveland D.W., Swayze E.E., Lima W.F., Crooke S.T., Prakash T.P., Corey D.R. Single-stranded RNAs use RNAi to potently and allele-selectively inhibit mutant huntingtin expression. Cell 2012, 150:895-908.