Biochemical and biophysical characterization of succinate: Quinone reductase from Thermus thermophilus

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1807, Issue 1, 2011, Pages 68-79

  Kolaj Robin, Olga ^a   O'Kane, Sarah R ^a   Nitschke, Wolfgang ^b   Léger, Christophe ^b   Baymann, Frauke ^b   Soulimane, Tewfik ^a  

^a UNIVERSITY OF LIMERICK   (Ireland)

^b CNRS and Aix Marseille University   (France)

Author keywords

Complex II; Cooperativity; Succinate dehydrogenase; Succinate:quinone oxidoreductase; Thermus thermophilus

Indexed keywords

3 NITROPROPIONIC ACID; ENZYME INHIBITOR; FLAVOPROTEIN; FUMARATE REDUCTASE; HEME; IRON SULFUR PROTEIN; MEMBRANE ANCHOR PROTEIN; MEMBRANE PROTEIN; NONYL 4 HYDROXYQUINOLINE N OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SEMIQUINONE; SODIUM DIETHYL OXALOACETIC ACID; SODIUM MALONIC ACID; SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; CRYSTALLIZATION; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ISOLATION; ENZYME KINETICS; ENZYME PURIFICATION; ENZYME STRUCTURE; MOLECULAR WEIGHT; NONHUMAN; OLIGOMERIZATION; OXIDATION REDUCTION REACTION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN STABILITY; STEADY STATE; STRUCTURE ACTIVITY RELATION; TEMPERATURE; THERMUS THERMOPHILUS;

AMINO ACID SEQUENCE; ANIMALS; BACTERIA; BACTERIAL PROTEINS; CATTLE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CIRCULAR DICHROISM; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME STABILITY; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NAD(P)H DEHYDROGENASE (QUINONE); OXIDATION-REDUCTION; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; THERMUS THERMOPHILUS;

THERMUS THERMOPHILUS;

EID: 78249254576     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.10.009     Document Type: Article

References (77)

1. Hägerhäll C. Succinate: quinone oxidoreductases. Variations on a conserved theme. Biochim Biophys Acta 1997, 1320:107-141.
2. Saraste M. Oxidative phosphorylation at the fin de siecle. Science 1999, 283:1488-1493.
3. Kröger A., Geisler V., Lemma E., Theis F., Lenger R. Bacterial fumarate respiration. Arch Microbiol 1992, 158:311-314.
4. Guest J.R. Partial replacement of succinate dehydrogenase function by phage- and plasmid-specified fumarate reductase in Escherichia coli. J Gen Microbiol 1981, 122:171-179.
5. Maklashina E., Berthold D.A., Cecchini G. Anaerobic expression of Escherichia coli succinate dehydrogenase: functional replacement of fumarate reductase in the respiratory chain during anaerobic growth. J Bacteriol 1998, 180:5989-5996.
6. Lancaster C.R. Succinate:quinone oxidoreductases: an overview. Biochim Biophys Acta 2002, 1553:1-6.
7. Ohnishi T., Moser C.C., Page C.C., Dutton P.L., Yano T. Simple redox-linked proton-transfer design: new insights from structures of quinol-fumarate reductase. Structure 2000, 8:R23-R32.
8. Schirawski J., Unden G. Menaquinone-dependent succinate dehydrogenase of bacteria catalyzes reversed electron transport driven by the proton potential. Eur J Biochem 1998, 257:210-215.
9. 2. Science 1999, 284:1941-1942.
10. Lancaster C.R., Kroger A. Succinate: quinone oxidoreductases: new insights from X-ray crystal structures. Biochim Biophys Acta 2000, 1459:422-431.
11. Lemos R.S., Fernandes A.S., Pereira M.M., Gomes C.M., Teixeira M. Quinol:fumarate oxidoreductases and succinate:quinone oxidoreductases: phylogenetic relationships, metal centres and membrane attachment. Biochim Biophys Acta 2002, 1553:158-170.
12. Juhnke H.D., Hiltscher H., Nasiri H.R., Schwalbe H., Lancaster C.R. Production, characterization and determination of the real catalytic properties of the putative 'succinate dehydrogenase' from Wolinella succinogenes. Mol Microbiol 2009, 71:1088-1101.
13. Iverson T.M., Luna-Chavez C., Cecchini G., Rees D.C. Structure of the Escherichia coli fumarate reductase respiratory complex. Science 1999, 284:1961-1966.
14. Lancaster C.R., Kroger A., Auer M., Michel H. Structure of fumarate reductase from Wolinella succinogenes at 2.2Å resolution. Nature 1999, 402:377-385.
15. Yankovskaya V., Horsefield R., Tornroth S., Luna-Chavez C., Miyoshi H., Leger C., Byrne B., Cecchini G., Iwata S. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 2003, 299:700-704.
16. 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, 281:5965-5972.
17. 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, 121:1043-1057.
18. Nakamura K., Yamaki M., Sarada M., Nakayama S., Vibat C.R., Gennis R.B., Nakayashiki T., Inokuchi H., Kojima S., 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 1996, 271:521-527.
19. Tran Q.M., Rothery R.A., Maklashina E., Cecchini G., Weiner J.H. Escherichia coli succinate dehydrogenase variant lacking the heme b. Proc Natl Acad Sci USA 2007, 104:18007-18012.
20. Xin Y., Lu Y.K., Fromme R., Fromme P., Blankenship R.E. Purification, characterization and crystallization of menaquinol:fumarate oxidoreductase from the green filamentous photosynthetic bacterium Chloroflexus aurantiacus. Biochim Biophys Acta 2009, 1787:86-96.
21. Efremov R.G., Baradaran R., Sazanov L.A. The architecture of respiratory complex I. Nature 2010, 465:441-445.
22. 3-cytochrome c oxidase from Thermus thermophilus. EMBO J 2000, 19:1766-1776.
23. 3-cytochrome c oxidase from Thermus thermophilus: purification, crystallisation and crystal transformation. A Practical Guide to Membrane Protein Purification and Crystallization 2002, 229-251. Academic Press.
24. Berry E.A., Trumpower B.L. Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra. Anal Biochem 1987, 161:1-15.
25. Edman P., Begg G. A protein sequenator. Eur J Biochem 1967, 1:80-91.
26. Reisinger V., Eichacker L.A. Analysis of membrane protein complexes by blue native PAGE. Proteomics 2006, 6(Suppl. 2):6-15.
27. Bohm G., Muhr R., Jaenicke R. Quantitative analysis of protein far UV circular dichroism spectra by neural networks. Protein Eng 1992, 5:191-195.
28. Dutton P.L. Oxidation-reduction potential dependence of the interaction of cytochromes, bacteriochlorophyll and carotenoids at 77 degrees K in chromatophores of Chromatium D and Rhodopseudomonas gelatinosa. Biochim Biophys Acta 1971, 226:63-80.
29. Léger C., Bertrand P. Direct electrochemistry of redox enzymes as a tool for mechanistic studies. Chem Rev 2008, 108:2379-2438.
30. Liebgott P.P., Leroux F., Burlat B., Dementin S., Baffert C., Lautier T., Fourmond V., Ceccaldi P., Cavazza C., Meynial-Salles I., Soucaille P., Fontecilla-Camps J.C., Guigliarelli B., Bertrand P., Rousset M., Léger C. Relating diffusion along the substrate tunnel and oxygen sensitivity in hydrogenase. Nat Chem Biol 2010, 6:63-70.
31. Hägerhäll C., Aasa R., von Wachenfeldt C., Hederstedt L. Two hemes in Bacillus subtilis succinate:menaquinone oxidoreductase. Biochemistry 1992, 31:7411-7421.
32. T. Soulimane, S.R. O'Kane, O. Kolaj, Isolation and purification of Thermus thermophilus HpaB by a crystallization approach, Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66 352-6.
33. Wei Y., Li H., Fu D. Oligomeric state of the Escherichia coli metal transporter YiiP. J Biol Chem 2004, 279:39251-39259.
34. Heuberger E.H., Veenhoff L.M., Duurkens R.H., Friesen R.H., Poolman B. Oligomeric state of membrane transport proteins analyzed with blue native electrophoresis and analytical ultracentrifugation. J Mol Biol 2002, 317:591-600.
35. Mileni M., MacMillan F., Tziatzios C., Zwicker K., Haas A.H., Mantele W., Simon J., Lancaster C.R. Heterologous production in Wolinella succinogenes and characterization of the quinol:fumarate reductase enzymes from Helicobacter pylori and Campylobacter jejuni. Biochem J 2006, 395:191-201.
36. Kurokawa T., Sakamoto J. Purification and characterization of succinate:menaquinone oxidoreductase from Corynebacterium glutamicum. Arch Microbiol 2005, 183:317-324.
37. Madej M.G., Nasiri H.R., Hilgendorff N.S., Schwalbe H., Unden G., Lancaster C.R. Experimental evidence for proton motive force-dependent catalysis by the diheme-containing succinate:menaquinone oxidoreductase from the Gram-positive bacterium Bacillus licheniformis. Biochemistry 2006, 45:15049-15055.
38. Moll R., Schafer G. Purification and characterisation of an archaebacterial succinate dehydrogenase complex from the plasma membrane of the thermoacidophile Sulfolobus acidocaldarius. Eur J Biochem 1991, 201:593-600.
39. Wallace B.A., Janes R.W. Synchrotron radiation circular dichroism spectroscopy of proteins: secondary structure, fold recognition and structural genomics. Curr Opin Chem Biol 2001, 5:567-571.
40. Wallace B.A., Lees J.G., Orry A.J., Lobley A., Janes R.W. Analyses of circular dichroism spectra of membrane proteins. Protein Sci 2003, 12:875-884.
41. Hägerhäll C., Hederstedt L. A structural model for the membrane-integral domain of succinate: quinone oxidoreductases. FEBS Lett 1996, 389:25-31.
42. 558 of the Bacillus subtilis succinate: quinone oxidoreductase indicate bis-histidine coordination of the heme iron. Biochim Biophys Acta 1990, 1041:207-215.
43. 556 in succinate: ubiquinone oxidoreductase from Escherichia coli. FEBS Lett 1994, 355:155-156.
44. 560 in bovine heart succinate-ubiquinone reductase. FEBS Lett 1995, 367:1-4.
45. Madej M.G., Nasiri H.R., Hilgendorff N.S., Schwalbe H., Lancaster C.R. Evidence for transmembrane proton transfer in a dihaem-containing membrane protein complex. EMBO J 2006, 25:4963-4970.
46. Madej M.G., Muller F.G., Ploch J., Lancaster C.R. Limited reversibility of transmembrane proton transfer assisting transmembrane electron transfer in a dihaem-containing succinate:quinone oxidoreductase. Biochim Biophys Acta 2009, 1787:593-600.
47. Collins M.D., Jones D. Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. Microbiol Rev 1981, 45:316-354.
48. Redfarn E.R., Powls R. The quinones of green photosynthetic bacteria. Biochem J 1968, 106.
49. Smirnova I.A., Hagerhall C., Konstantinov A.A., Hederstedt L. HOQNO interaction with cytochrome b in succinate:menaquinone oxidoreductase from Bacillus subtilis. FEBS Lett 1995, 359:23-26.
50. Christenson A., Gustavsson T., Gorton L., Hagerhall C. Direct and mediated electron transfer between intact succinate:quinone oxidoreductase from Bacillus subtilis and a surface modified gold electrode reveals redox state-dependent conformational changes. Biochim Biophys Acta 2008, 1777:1203-1210.
51. Teschner T., Yatsunyk L., Schunemann V., Paulsen H., Winkler H., Hu C., Scheidt W.R., Walker F.A., Trautwein A.X. Models of the membrane-bound cytochromes: Mössbauer spectra of crystalline low-spin ferriheme complexes having axial ligand plane dihedral angles ranging from 0 degree to 90 degrees. J Am Chem Soc 2006, 128:1379-1389.
52. Ohnishi T., King T.E., Salerno J.C., Blum H., Bowyer J.R., Maida T. Thermodynamic and electron paramagnetic resonance characterization of flavin in succinate dehydrogenase. J Biol Chem 1981, 256:5577-5582.
53. Beinert H., Ackrell B.A., Vinogradov A.D., Kearney E.B., Singer T.P. Interrelations of reconstitution activity, reactions with electron acceptors, and iron-sulfur centers in succinate dehydrogenase. Arch Biochem Biophys 1977, 182:95-106.
54. Léger C., Heffron K., Pershad H.R., Maklashina E., Luna-Chavez C., Cecchini G., Ackrell B.A., Armstrong F.A. Enzyme electrokinetics: energetics of succinate oxidation by fumarate reductase and succinate dehydrogenase. Biochemistry 2001, 40:11234-11245.
55. Cheng V.W., Ma E., Zhao Z., Rothery R.A., Weiner J.H. The iron-sulfur clusters in Escherichia coli succinate dehydrogenase direct electron flow. J Biol Chem 2006, 281:27662-27668.
56. Sucheta A., Ackrell B.A., Cochran B., Armstrong F.A. Diode-like behaviour of a mitochondrial electron-transport enzyme. Nature 1992, 356:361-362.
57. Pershad H.R., Hirst J., Cochran B., Ackrell B.A., Armstrong F.A. Voltammetric studies of bidirectional catalytic electron transport in Escherichia coli succinate dehydrogenase: comparison with the enzyme from beef heart mitochondria. Biochim Biophys Acta 1999, 1412:262-272.
58. Hirst J., Sucheta A., Ackrell B.A.C., Armstrong F.A. Electrocatalytic voltammetry of succinate dehydrogenase: direct quantification of the catalytic properties of a complex electron-transport enzyme. J Am Chem Soc 1996, 118:5031-5038.
59. Fourmond V., Burlat B., Dementin S., Sabaty M., Arnoux P., Etienne E., Guigliarelli B., Bertrand P., Pignol D., Léger C. Dependence of catalytic activity on driving force in solution assays and protein film voltammetry: insights from the comparison of nitrate reductase mutants. Biochemistry 2010, 49:2424-2432.
60. Giordano A., Febbraio F., Russo C., Rossi M., Raia C.A. Evidence for co-operativity in coenzyme binding to tetrameric Sulfolobus solfataricus alcohol dehydrogenase and its structural basis: fluorescence, kinetic and structural studies of the wild-type enzyme and non-co-operative N249Y mutant. Biochem J 2005, 388:657-667.
61. Hagerhall C., Friden H., Aasa R., Hederstedt L. Transmembrane topology and axial ligands to hemes in the cytochrome b subunit of Bacillus subtilis succinate:menaquinone reductase. Biochemistry 1995, 34:11080-11089.
62. L. J Bioenerg Biomembr 2001, 33:343-352.
63. Anemuller S., Hettmann T., Moll R., Teixeira M., Schafer G. EPR characterization of an archaeal succinate dehydrogenase in the membrane-bound state. Eur J Biochem 1995, 232:563-568.
64. Qureshi M.H., Fujiwara T., Fukumori Y. Succinate:quinone oxidoreductase (complex II) containing a single heme b in facultative alkaliphilic Bacillus sp. strain YN-2000. J Bacteriol 1996, 178:3031-3036.
65. Gilmour R., Krulwich T.A. Purification and characterization of the succinate dehydrogenase complex and CO-reactive b-type cytochromes from the facultative alkaliphile Bacillus firmus OF4. Biochim Biophys Acta 1996, 1276:57-63.
66. 556. J Biol Chem 1989, 264:2672-2677.
67. Maklashina E., Iverson T.M., Sher Y., Kotlyar V., Andrell J., Mirza O., Hudson J.M., Armstrong F.A., Rothery R.A., Weiner J.H., Cecchini G. Fumarate reductase and succinate oxidase activity of Escherichia coli complex II homologs are perturbed differently by mutation of the flavin binding domain. J Biol Chem 2006, 281:11357-11365.
68. Tushurashvili P.R., Gavrikova E.V., Ledenev A.N., Vinogradov A.D. Studies on the succinate dehydrogenating system. Isolation and properties of the mitochondrial succinate-ubiquinone reductase. Biochim Biophys Acta 1985, 809:145-159.
69. Gomes C.M., Lemos R.S., Teixeira M., Kletzin A., Huber H., Stetter K.O., Schafer G., Anemuller S. The unusual iron sulfur composition of the Acidianus ambivalens succinate dehydrogenase complex. Biochim Biophys Acta 1999, 1411:134-141.
70. Iwasaki T., Wakagi T., Oshima T. Resolution of the aerobic respiratory system of the thermoacidophilic archaeon, Sulfolobus sp. strain 7. III. The archaeal novel respiratory complex II (succinate:caldariellaquinone oxidoreductase complex) inherently lacks heme group. J Biol Chem 1995, 270:30902-30908.
71. Gradin C.H., Hederstedt L., Baltscheffsky H. Soluble succinate dehydrogenase from the halophilic archaebacterium, Halobacterium halobium. Arch Biochem Biophys 1985, 239:200-205.
72. Kawahara K., Mogi T., Tanaka T.Q., Hata M., Miyoshi H., Kita K. Mitochondrial dehydrogenases in the aerobic respiratory chain of the rodent malaria parasite Plasmodium yoelii yoelii. J Biochem 2009, 145:229-237.
73. Munujos P., Coll-Canti J., Gonzalez-Sastre F., Gella F.J. Assay of succinate dehydrogenase activity by a colorimetric-continuous method using iodonitrotetrazolium chloride as electron acceptor. Anal Biochem 1993, 212:506-509.
74. Ingledew W.J., Poole R.K. The respiratory chains of Escherichia coli. Microbiol Rev 1984, 48:222-271.
75. Unden G., Hackenberg H., Kroger A. Isolation and functional aspects of the fumarate reductase involved in the phosphorylative electron transport of Vibrio succinogenes. Biochim Biophys Acta 1980, 591:275-288.
76. Lemos R.S., Gomes C.M., LeGall J., Xavier A.V., Teixeira M. The quinol:fumarate oxidoreductase from the sulphate reducing bacterium Desulfovibrio gigas: spectroscopic and redox studies. J Bioenerg Biomembr 2002, 34:21-30.
77. 3 from Shewanella frigidimarina NCIMB400. Biochemistry 1999, 38:3302-3309.