Plasticity of the quinone-binding site of the complex II homolog quinol: Fumarate reductase

Journal of Biological Chemistry

Volumn 288, Issue 34, 2013, Pages 24293-24301

  Singh, Prashant K ^a   Sarwar, Maruf ^a   Maklashina, Elena ^c,d   Kotlyar, Violetta ^c   Rajagukguk, Sany ^c   Tomasiak, Thomas M ^a,d   Cecchini, Gary ^c,d   Iverson, Tina M ^a,b  

^a Department of Pharmacology ^*  (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; COMPUTATIONAL DOCKINGS; COMPUTATIONAL STUDIES; ENZYME INTERACTION; INTERCONVERSIONS; KINETIC MEASUREMENT; QUINOL:FUMARATE REDUCTASE; TRANSMEMBRANE PROTON GRADIENT;

ARGININE; KETONES; PROTEINS; REDOX REACTIONS; REDUCTION;

BINDING SITES;

ENZYME VARIANT; MENAQUINOL; OXIDOREDUCTASE; QUINOL FUMARATE REDUCTASE; QUINOLINE DERIVATIVE; QUINONE DERIVATIVE; SOLVENT; UBIQUINONE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BIOENERGY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; GENE MUTATION; MOLECULAR DOCKING; MOLECULAR INTERACTION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTON TRANSPORT; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

BIOENERGETICS/ELECTRON TRANSFER COMPLEX; ELECTRON TRANSFER; MENAQUINONE; NAPHTHOQUINONE; REDOX; RESPIRATORY CHAIN; TRICARBOXYLIC ACID (TCA) CYCLE; UBIQUINONE;

CATALYTIC DOMAIN; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MOLECULAR DOCKING SIMULATION; OXIDOREDUCTASES; STRUCTURE-ACTIVITY RELATIONSHIP; UBIQUINONE;

EID: 84883182920     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.487082     Document Type: Article

References (45)

1. Smith, M. W., and Neidhardt, F. C. (1983) Proteins induced by aerobiosis in Escherichia coli. J. Bacteriol. 154, 344-350
2. Smith, M. W., and Neidhardt, F. C. (1983) Proteins induced by anaerobiosis in Escherichia coli. J. Bacteriol. 154, 336-343
3. Arai, H., Roh, J. H., and Kaplan, S. (2008) Transcriptome dynamics during the transition from anaerobic photosynthesis to aerobic respiration in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 190, 286-299
4. Unden, G., and Bongaerts, J. (1997) Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim. Biophys. Acta 1320, 217-234
5. Shestopalov, A. I., Bogachev, A. V., Murtazina, R. A., Viryasov, M. B., and Skulachev, V. P. (1997) Aeration-dependent changes in composition of the quinone pool in Escherichia coli. Evidence of post-transcriptional regulation of the quinone biosynthesis. FEBS Lett. 404, 272-274
6. Holländer, R. (1976) Correlation of the function of demethylmenaquinone in bacterial electron transport with its redox potential. FEBS Lett. 72, 98-100
7. Sharma, P., Teixeira de Mattos, M. J., Hellingwerf, K. J., and Bekker, M. (2012) On the function of the various quinone species in Escherichia coli. FEBS J. 279, 3364-3373
8. Hägerhäll, C. (1997) Succinate:quinone oxidoreductases. Variations on a conserved theme. Biochim. Biophys. Acta 1320, 107-141
9. Cecchini, G. (2003) Function and structure of complex II of the respiratory chain. Annu. Rev. Biochem. 72, 77-109
10. Cecchini, G., Maklashina, E., Yankovskaya, V., Iverson, T. M., and Iwata, S. (2003) Variation in proton donor/acceptor pathways in succinate:quinone oxidoreductases. FEBS Lett. 545, 31-38
11. Guest, J. R. (1981) Partial replacement of succinate dehydrogenase function by phage-and plasmid-specified fumarate reductase in Escherichia coli. J. Gen. Microbiol. 122, 171-179
12. Iverson, T. M., Luna-Chavez, C., Cecchini, G., and Rees, D. C. (1999) Structure of the Escherichia coli fumarate reductase respiratory complex. Science 284, 1961-1966
13. Iverson, T. M., Luna-Chavez, C., Croal, L. R., Cecchini, G., and Rees, D. C. (2002) Crystallographic studies of the Escherichia coli quinol-fumarate reductase with inhibitors bound to the quinol-binding site. J. Biol. Chem. 277, 16124-16130
14. Yankovskaya, V., Horsefield, R., Törnroth, S., Luna-Chavez, C., Miyoshi, H., Léger, C., Byrne, B., Cecchini, G., and Iwata, S. (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299, 700-704
15. Iverson, T. M. (2013) Catalytic mechanisms of complex II enzymes: a structural perspective. Biochim. Biophys. Acta 1827, 648-657
16. Maklashina, E., Hellwig, P., Rothery, R. A., Kotlyar, V., Sher, Y., Weiner, J. H., and Cecchini, G. (2006) Differences in protonation of ubiquinone and menaquinone in fumarate reductase from Escherichia coli. J. Biol. Chem. 281, 26655-26664
17. Westenberg, D. J., Gunsalus, R. P., Ackrell, B. A., 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
18. Maklashina, E., and Cecchini, G. (2010) The quinone-binding and catalytic site of complex II. Biochim. Biophys. Acta 1797, 1877-1882
19. Hägerhäll, C., Magnitsky, S., Sled, V. D., Schröder, 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
20. Luna-Chavez, C., Iverson, T. M., Rees, D. C., and Cecchini, G. (2000) Overexpression, purification, and crystallization of the membrane-bound fumarate reductase from Escherichia coli. Protein Expr. Purif. 19, 188-196
21. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
22. Tomasiak, T. M., Archuleta, T. L., Andréll, J., Luna-Chávez, C., Davis, T. A., Sarwar, M., Ham, A. J., McDonald, W. H., Yankovskaya, V., Stern, H. A., Johnston, J. N., Maklashina, E., Cecchini, G., and Iverson, T. M. (2011) Geometric restraint drives on-and off-pathway catalysis by the Escherichia coli menaquinol:fumarate reductase. J. Biol. Chem. 286, 3047-3056
23. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
24. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921
25. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
26. Painter, J., and Merritt, E. A. (2006) TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallogr. 39, 109-111
27. Friesner, R. A., Murphy, R. B., Repasky, M. P., Frye, L. L., Greenwood, J. R., Halgren, T. A., Sanschagrin, P. C., and Mainz, D. T. (2006) Extra precision glide: docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes. J. Med. Chem. 49, 6177-6196
28. Lomize, M. A., Lomize, A. L., Pogozheva, I. D., and Mosberg, H. I. (2006) OPM: orientations of proteins in membranes database. Bioinformatics 22, 623-625
29. Maklashina, E., and Cecchini, G. (1999) Comparison of catalytic activity and inhibitors of quinone reactions of succinate dehydrogenase (succinate-ubiquinone oxidoreductase) and fumarate reductase (menaquinolfumarate oxidoreductase) from Escherichia coli. Arch. Biochem. Biophys. 369, 223-232
30. Rothery, R. A., and Weiner, J. H. (1998) Interaction of a menaquinol binding site with the [3Fe-4S] cluster of Escherichia coli fumarate reductase. Eur. J. Biochem. 254, 588-595
31. Rothery, R. A., Seime, A. M., Spiers, A. M., Maklashina, E., Schröder, 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
32. Maklashina, E., Iverson, T. M., Sher, Y., Kotlyar, V., Andréll, J., Mirza, O., Hudson, J. M., Armstrong, F. A., Rothery, R. A., Weiner, J. H., and Cecchini, G. (2006) 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. 281, 11357-11365
33. Pokkuluri, P. R., Laible, P. D., Deng, Y. L., Wong, T. N., Hanson, D. K., and Schiffer, M. (2002) The structure of a mutant photosynthetic reaction center shows unexpected changes in main chain orientations and quinone position. Biochemistry 41, 5998-6007
34. -·) in reaction centers from Rhodobacter sphaeroides. Biochemistry 46, 8234-8243
35. 1 complex. Biochim. Biophys. Acta, in press
36. Léger, C., Heffron, K., Pershad, H. R., Maklashina, E., Luna-Chavez, C., Cecchini, G., Ackrell, B. A., and Armstrong, F. A. (2001) Enzyme electrokinetics: energetics of succinate oxidation by fumarate reductase and succinate dehydrogenase. Biochemistry 40, 11234-11245
37. Yang, X., Yu, L., He, D., and Yu, C. A. (1998) The quinone-binding site in succinate-ubiquinone reductase from Escherichia coli. Quinone-binding domain and amino acid residues involved in quinone binding. J. Biol. Chem. 273, 31916-31923
38. Cheng, V. W., Johnson, A., Rothery, R. A., and Weiner, J. H. (2008) Alternative sites for proton entry from the cytoplasm to the quinone binding site in Escherichia coli succinate dehydrogenase. Biochemistry 47, 9107-9116
39. Horsefield, R., Yankovskaya, V., Sexton, G., Whittingham, W., Shiomi, K., Omura, S., Byrne, B., Cecchini, G., and Iwata, S. (2006) 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, 7309-7316
40. Bader, M. W., Xie, T., Yu, C. A., and Bardwell, J. C. (2000) Disulfide bonds are generated by quinone reduction. J. Biol. Chem. 275, 26082-26088
41. Azarkina, N., and Konstantinov, A. A. (2002) Stimulation of menaquinone-dependent electron transfer in the respiratory chain of Bacillus subtilis by membrane energization. J. Bacteriol. 184, 5339-5347
42. Takahashi, Y. H., Inaba, K., and Ito, K. (2004) Characterization of the menaquinone-dependent disulfide bond formation pathway of Escherichia coli. J. Biol. Chem. 279, 47057-47065
43. Inaba, K., Takahashi, Y. H., and Ito, K. (2005) Reactivities of quinone-free DsbB from Escherichia coli. J. Biol. Chem. 280, 33035-33044
44. Mustafa, G., Migita, C. T., Ishikawa, Y., Kobayashi, K., Tagawa, S., and Yamada, M. (2008) Menaquinone as well as ubiquinone as a bound quinone crucial for catalytic activity and intramolecular electron transfer in Escherichia coli membrane-bound glucose dehydrogenase. J. Biol. Chem. 283, 28169-28175
45. 2 is a mitochondrial electron carrier that rescues pink1 deficiency. Science 336, 1306-1310