Mutations in the heme b-binding residue of SDHC inhibit assembly of respiratory chain complex II in mammalian cells

Mitochondrion

Volumn 9, Issue 4, 2009, Pages 254-260

  Lemarie, Anthony ^a   Grimm, Stefan ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Heme b; Mitochondria; Protein assembly; Respiratory chain; Succinate coenzyme Q oxidoreductase; Succinate dehydrogenase

Indexed keywords

HEME; SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE C; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME STRUCTURE; GENE MUTATION; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CRICETINAE; ELECTRON TRANSPORT COMPLEX II; HEME; HUMANS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN SUBUNITS; SEQUENCE ALIGNMENT; SUCCINATE DEHYDROGENASE;

MAMMALIA;

EID: 67349267341     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mito.2009.03.004     Document Type: Article

References (30)

1. Albayrak T., Scherhammer V., Schoenfeld N., Braziulis E., Mund T., Bauer M.K., Scheffler I.E., and Grimm S. The tumor suppressor cybL, a component of the respiratory chain, mediates apoptosis induction. Mol. Biol. Cell 14 (2003) 3082-3096
2. Anderson R.F., Hille R., Shinde S.S., and Cecchini G. Electron transfer within complex II. Succinate:ubiquinone oxidoreductase of Escherichia coli. J. Biol. Chem. 280 (2005) 33331-33337 (Epub 2005 Aug 5)
3. Bayley J.P., Devilee P., and Taschner P.E. The SDH mutation database: an online resource for succinate dehydrogenase sequence variants involved in pheochromocytoma, paraganglioma and mitochondrial complex II deficiency. BMC Med. Genet. 6 (2005) 39
4. 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 C.W.r., Cornelisse C.J., Devilee P., and Devlin B. Mutations in SDHD a mitochondrial complex II gene in hereditary paraganglioma. Science 287 (2000) 848-851
5. Brummelkamp T.R., Bernards R., and Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 296 (2002) 550-553
6. Dibrov E., Fu S., and Lemire B.D. The Saccharomyces cerevisiae TCM62 gene encodes a chaperone necessary for the assembly of the mitochondrial succinate dehydrogenase (complex II). J. Biol. Chem. 273 (1998) 32042-32048
7. Douwes Dekker P.B., Hogendoorn P.C., Kuipers-Dijkshoorn N., Prins F.A., van Duinen S.G., Taschner P.E., van der Mey A.G., and Cornelisse C.J. SDHD mutations in head and neck paragangliomas result in destabilization of complex II in the mitochondrial respiratory chain with loss of enzymatic activity and abnormal mitochondrial morphology. J. Pathol. 201 (2003) 480-486
8. Friden H., and Hederstedt L. Role of His residues in Bacillus subtilis cytochrome b558 for heme binding and assembly of succinate:quinone oxidoreductase (complex II). Mol. Microbiol. 4 (1990) 1045-1056
9. Gewies A., and Grimm S. UBP41 is a proapoptotic ubiquitin-specific protease. Cancer Res. 63 (2003) 682-688
10. Gimenez-Roqueplo A.P., Favier J., Rustin P., Mourad J.J., Plouin P.F., Corvol P., Rotig A., and Jeunemaitre X. 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 (2001) 1186-1197 (Epub 2001 Oct 16)
11. Gimenez-Roqueplo A.P., Favier J., Rustin P., Rieubland C., Kerlan V., Plouin P.F., Rotig A., and Jeunemaitre X. Functional consequences of a SDHB gene mutation in an apparently sporadic pheochromocytoma. J. Clin. Endocrinol. Metab. 87 (2002) 4771-4774
12. Gogvadze, V., Orrenius, S., Zhivotovsky, B., 2004. Analysis of mitochondrial dysfunction during cell death. Current Protocols in Toxicology.
13. Gottlieb E., and Tomlinson I.P. Mitochondrial tumour suppressors: a genetic and biochemical update. Nat. Rev. Cancer 5 (2005) 857-866
14. Ishii T., Yasuda K., Akatsuka A., Hino O., Hartman P.S., and Ishii N. A mutation in the SDHC gene of complex II increases oxidative stress, resulting in apoptosis and tumorigenesis. Cancer Res. 65 (2005) 203-209
15. Kita K., Vibat C.R., Meinhardt S., Guest J.R., and Gennis R.B. One-step purification from Escherichia coli of complex II (succinate:ubiquinone oxidoreductase) associated with succinate-reducible cytochrome b556. J. Biol. Chem. 264 (1989) 2672-2677
16. Lemarie A., Morzadec C., Merino D., Micheau O., Fardel O., and Vernhet L. Arsenic trioxide induces apoptosis of human monocytes during macrophagic differentiation through nuclear factor-kappaB-related survival pathway down-regulation. J. Pharmacol. Exp. Ther. 316 (2006) 304-314 (Epub 2005 Sep 20)
17. Lemire B.D., and Oyedotun K.S. The Saccharomyces cerevisiae mitochondrial succinate:ubiquinone oxidoreductase. Biochim. Biophys. Acta 1553 (2002) 102-116
18. Lombardo A., and Scheffler I.E. Isolation and characterization of a Saccharomyces cerevisiae mutant with a disrupted gene for the IP subunit of succinate dehydrogenase. J. Biol. Chem. 264 (1989) 18874-18877
19. Nakamura K., Yamaki M., Sarada M., Nakayama S., Vibat C.R., Gennis R.B., Nakayashiki T., Inokuchi H., Kojima S., and Kita K. Two hydrophobic subunits are essential for the heme b ligation and functional assembly of complex II (succinate-ubiquinone oxidoreductase) from Escherichia coli. J. Biol. Chem. 271 (1996) 521-527
20. Neuzil J., Dyason J.C., Freeman R., Dong L.F., Prochazka L., Wang X.F., Scheffler I., and Ralph S.J. Mitocans as anti-cancer agents targeting mitochondria: lessons from studies with vitamin E analogues, inhibitors of complex II. J. Bioenerg. Biomembr. 39 (2007) 65-72
21. Niemann S., and Muller U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat. Genet. 26 (2000) 268-270
22. Oostveen F.G., Au H.C., Meijer P.J., and Scheffler I.E. A Chinese hamster mutant cell line with a defect in the integral membrane protein CII-3 of complex II of the mitochondrial electron transport chain. J. Biol. Chem. 270 (1995) 26104-26108
23. Oyedotun K.S., Sit C.S., and Lemire B.D. The Saccharomyces cerevisiae succinate dehydrogenase does not require heme for ubiquinone reduction. Biochim. Biophys. Acta 1767 (2007) 1436-1445 (Epub 2007 Sep 29)
24. Schubert A., and Grimm S. Cyclophilin D, a component of the permeability transition (pt)-pore, is an apoptosis repressor. Cancer Res. 64 (2004) 85-93
25. 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
26. 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
27. Tran Q.M., Rothery R.A., Maklashina E., Cecchini G., and Weiner J.H. Escherichia coli succinate dehydrogenase variant lacking the heme b. Proc. Natl. Acad. Sci. USA 104 (2007) 18007-18012 (Epub 2007 Nov 7)
28. 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
29. Ye W., and Zhang L. Heme deficiency causes apoptosis but does not increase ROS generation in HeLa cells. Biochem. Biophys. Res. Commun. 319 (2004) 1065-1071
30. Yu L., Xu J.X., Haley P.E., and Yu C.A. Properties of bovine heart mitochondrial cytochrome b560. J. Biol. Chem. 262 (1987) 1137-1143