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Current Molecular Pharmacology

Editor-in-Chief

ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

Review Article

Cytochrome bc1-aa3 Oxidase Supercomplex As Emerging and Potential Drug Target Against Tuberculosis

Author(s): Thangaraj Sindhu and Pal Debnath*

Volume 15, Issue 2, 2022

Published on: 21 December, 2021

Article ID: e280921196875 Pages: 13

DOI: 10.2174/1874467214666210928152512

Price: $65

Abstract

The cytochrome bc1-aa3 supercomplex plays an essential role in the cellular respiratory system of Mycobacterium Tuberculosis. It transfers electrons from menaquinol to cytochrome aa3 (Complex IV) via cytochrome bc1 (Complex III), which reduces the oxygen. The electron transfer from a variety of donors into oxygen through the respiratory electron transport chain is essential to pump protons across the membrane creating an electrochemical transmembrane gradient (proton motive force, PMF) that regulates the synthesis of ATP via the oxidative phosphorylation process. Cytochrome bc1-aa3 supercomplex in M. tuberculosis is, therefore, a major drug target for antibiotic action. In recent years, several respiratory chain components have been targeted for developing new candidate drugs, illustrating the therapeutic potential of obstructing energy conversion of M. tuberculosis. The recently available cryo-EM structure of mycobacterial cytochrome bc1-aa3 supercomplex with open and closed conformations has opened new avenues for understanding its structure and function for developing more effective, new therapeutics against pulmonary tuberculosis. In this review, we discuss the role and function of several components, subunits, and drug targeting elements of the supercomplex cytochrome bc1-aa3 and its potential inhibitors in detail.

Keywords: Mycobacterium tuberculosis, electron transport chain, oxidative phosphorylation, anti-TB agents, QcrB, bc1-aa3 oxidase supercomplex.

Graphical Abstract

[1]
Nodieva, A.; Jansone, I.; Broka, L.; Pole, I.; Skenders, G.; Baumanis, V. Recent nosocomial transmission and genotypes of multidrug-resistant Mycobacterium tuberculosis. Int. J. Tuberc. Lung Dis., 2010, 14(4), 427-433.
[PMID: 20202300]
[2]
Tomioka, H.; Namba, K. [Development of antituberculous drugs: Current status and future prospects]. Kekkaku, 2006, 81(12), 753-774.
[PMID: 17240921]
[3]
World Health Organization (WHO), Global tuberculosis report 2020. Available from: https://www.who.int/
[4]
India TB report 2020. Available from: http://www.tbcindia.gov.in
[5]
Mabhula, A.; Singh, V. Drug-resistance in Mycobacterium tuberculosis: Where we stand. MedChemComm, 2019, 10(8), 1342-1360.
[http://dx.doi.org/10.1039/C9MD00057G] [PMID: 31534654]
[6]
Phillips, L. Infectious disease: TB’s revenge. Nature, 2013, 493(7430), 14-16.
[http://dx.doi.org/10.1038/493014a] [PMID: 23282346]
[7]
Dartois, V. The path of anti-tuberculosis drugs: from blood to lesions to mycobacterial cells. Nat. Rev. Microbiol., 2014, 12(3), 159-167.
[http://dx.doi.org/10.1038/nrmicro3200] [PMID: 24487820]
[8]
Bass, J.B., Jr; Farer, L.S.; Hopewell, P.C.; O’Brien, R.; Jacobs, R.F.; Ruben, F.; Snider, D.E., Jr; Thornton, G. Treatment of tuberculosis and tuberculosis infection in adults and children. Am. J. Respir. Crit. Care Med., 1994, 149(5), 1359-1374.
[http://dx.doi.org/10.1164/ajrccm.149.5.8173779] [PMID: 8173779]
[9]
Bates, J.H.; Nardell, E. Institutional control measures for tuberculosis in the era of multiple drug resistance. Chest, 1995, 108(6), 1690-1710.
[http://dx.doi.org/10.1378/chest.108.6.1690] [PMID: 7497783]
[10]
Caminero, J.A.; Sotgiu, G.; Zumla, A.; Migliori, G.B. Best drug treatment for multidrug-resistant and extensively drug-resistant tuberculosis. Lancet Infect. Dis., 2010, 10(9), 621-629.
[http://dx.doi.org/10.1016/S1473-3099(10)70139-0] [PMID: 20797644]
[11]
Villarino, M.E.; Geiter, L.J.; Simone, P.M. The multidrug-resistant tuberculosis challenge to public health efforts to control tuberculosis. Public Health Rep., 1992, 107(6), 616-625.
[PMID: 1454973]
[12]
Coninx, R.; Mathieu, C.; Debacker, M.; Mirzoev, F.; Ismaelov, A.; de Haller, R.; Meddings, D.R. First-line tuberculosis therapy and drug-resistant Mycobacterium tuberculosis in prisons. Lancet, 1999, 353(9157), 969-973.
[http://dx.doi.org/10.1016/S0140-6736(98)08341-X] [PMID: 10459906]
[13]
Espinal, M.A.; Kim, S.J.; Suarez, P.G.; Kam, K.M.; Khomenko, A.G.; Migliori, G.B.; Baéz, J.; Kochi, A.; Dye, C.; Raviglione, M.C. Standard short-course chemotherapy for drug-resistant tuberculosis: treatment outcomes in 6 countries. JAMA, 2000, 283(19), 2537-2545.
[http://dx.doi.org/10.1001/jama.283.19.2537] [PMID: 10815117]
[14]
Extensively drug-resistant tuberculosis (XDR-TB): recommendations for prevention and control. Wkly. Epidemiol. Rec., 2006, 81(45), 430-432.
[PMID: 17096498]
[15]
Andries, K.; Villellas, C.; Coeck, N.; Thys, K.; Gevers, T.; Vranckx, L.; Lounis, N.; de Jong, B.C.; Koul, A. Acquired resistance of Mycobacterium tuberculosis to bedaquiline. PLoS One, 2014, 9(7), e102135.
[http://dx.doi.org/10.1371/journal.pone.0102135] [PMID: 25010492]
[16]
Bloemberg, G.V.; Keller, P.M.; Stucki, D.; Trauner, A.; Borrell, S.; Latshang, T.; Coscolla, M.; Rothe, T.; Hömke, R.; Ritter, C.; Feldmann, J.; Schulthess, B.; Gagneux, S.; Böttger, E.C. Acquired Resistance to Bedaquiline and Delamanid in Therapy for Tuberculosis. N. Engl. J. Med., 2015, 373(20), 1986-1988.
[http://dx.doi.org/10.1056/NEJMc1505196] [PMID: 26559594]
[17]
Munita, J.M.; Arias, C.A. Mechanisms of Antibiotic Resistance. Microbiol. Spectr., 2016, 4(2), 4.2.15.
[http://dx.doi.org/10.1128/microbiolspec.VMBF-0016-2015] [PMID: 27227291]
[18]
Cook, G.M.; Hards, K.; Dunn, E.; Heikal, A.; Nakatani, Y.; Greening, C.; Crick, D.C.; Fontes, F.L.; Pethe, K.; Hasenoehrl, E.; Berney, M. Oxidative Phosphorylation as a Target Space for Tuberculosis: Success, Caution, and Future Directions. Microbiol. Spectr., 2017, 5(3), 1-22.
[http://dx.doi.org/10.1128/microbiolspec.TBTB2-0014-2016] [PMID: 28597820]
[19]
Bald, D.; Villellas, C.; Lu, P.; Koul, A. Targeting energy metabolism in Mycobacterium tuberculosis, a new paradigm in antimycobacterial drug discovery. MBio, 2017, 8(2), e00272-e17.
[http://dx.doi.org/10.1128/mBio.00272-17] [PMID: 28400527]
[20]
Tran, S.L.; Cook, G.M. The F1Fo-ATP synthase of Mycobacterium smegmatis is essential for growth. J. Bacteriol., 2005, 187(14), 5023-5028.
[http://dx.doi.org/10.1128/JB.187.14.5023-5028.2005] [PMID: 15995221]
[21]
Cook, G.M.; Hards, K.; Vilchèze, C.; Hartman, T.; Berney, M. Energetics of respiration and oxidative phosphorylation in mycobacteria. Microbiol. Spectr., 2014, 2(3)
[http://dx.doi.org/10.1128/microbiolspec.MGM2-0015-2013] [PMID: 25346874]
[22]
Rao, S.P.S.; Alonso, S.; Rand, L.; Dick, T.; Pethe, K. The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA, 2008, 105(33), 11945-11950.
[http://dx.doi.org/10.1073/pnas.0711697105] [PMID: 18697942]
[23]
Feng, X.; Zhu, W.; Schurig-Briccio, L.A.; Lindert, S.; Shoen, C.; Hitchings, R.; Li, J.; Wang, Y.; Baig, N.; Zhou, T.; Kim, B.K.; Crick, D.C.; Cynamon, M.; McCammon, J.A.; Gennis, R.B.; Oldfield, E. Antiinfectives targeting enzymes and the proton motive force. Proc. Natl. Acad. Sci. USA, 2015, 112(51), E7073-E7082.
[http://dx.doi.org/10.1073/pnas.1521988112] [PMID: 26644565]
[24]
Kana, B.D.; Weinstein, E.A.; Avarbock, D.; Dawes, S.S.; Rubin, H.; Mizrahi, V. Characterization of the cydAB-encoded cytochrome bd oxidase from Mycobacterium smegmatis. J. Bacteriol., 2001, 183(24), 7076-7086.
[http://dx.doi.org/10.1128/JB.183.24.7076-7086.2001] [PMID: 11717265]
[25]
Kalia, N.P.; Lee, S. B.; Ab Rahman, N. B.; Moraski, G. C.; Miller, M. J.; Pethe, K. Carbon metabolism modulates the efficacy of drugs targeting the cytochrome bc1 :aa3 in Mycobacterium tuberculosis. Sci. Rep., 2019, 9(1), 1-9.
[http://dx.doi.org/10.1038/s41598-019-44887-9] [PMID: 30626917]
[26]
Weinstein, E.A.; Yano, T.; Li, L-S.; Avarbock, D.; Avarbock, A.; Helm, D.; McColm, A.A.; Duncan, K.; Lonsdale, J.T.; Rubin, H. Inhibitors of type II NADH:menaquinone oxidoreductase represent a class of antitubercular drugs. Proc. Natl. Acad. Sci. USA, 2005, 102(12), 4548-4553.
[http://dx.doi.org/10.1073/pnas.0500469102] [PMID: 15767566]
[27]
Sassetti, C.M.; Boyd, D.H.; Rubin, E.J. Genes required for mycobacterial growth defined by high density mutagenesis. Mol. Microbiol., 2003, 48(1), 77-84.
[http://dx.doi.org/10.1046/j.1365-2958.2003.03425.x] [PMID: 12657046]
[28]
Yano, T.; Li, L.S.; Weinstein, E.; Teh, J.S.; Rubin, H. Steady-state kinetics and inhibitory action of antitubercular phenothiazines on mycobacterium tuberculosis type-II NADH-menaquinone oxidoreductase (NDH-2). J. Biol. Chem., 2006, 281(17), 11456-11463.
[http://dx.doi.org/10.1074/jbc.M508844200] [PMID: 16469750]
[29]
Gadre, D.V.; Talwar, V.; Gupta, H.C.; Murthy, P.S. Effect of trifluoperazine, a potential drug for tuberculosis with psychotic disorders, on the growth of clinical isolates of drug resistant Mycobacterium tuberculosis. Int. Clin. Psychopharmacol., 1998, 13(3), 129-131.
[http://dx.doi.org/10.1097/00004850-199805000-00006] [PMID: 9690980]
[30]
Reddy, V.M.; Nadadhur, G.; Daneluzzi, D.; O’Sullivan, J.F.; Gangadharam, P.R. Antituberculosis activities of clofazimine and its new analogs B4154 and B4157. Antimicrob. Agents Chemother., 1996, 40(3), 633-636.
[http://dx.doi.org/10.1128/AAC.40.3.633] [PMID: 8851584]
[31]
Hartman, T.; Weinrick, B.; Vilchèze, C.; Berney, M.; Tufariello, J.; Cook, G.M.; Jacobs, W.R., Jr Succinate dehydrogenase is the regulator of respiration in Mycobacterium tuberculosis. PLoS Pathog., 2014, 10(11), e1004510.
[http://dx.doi.org/10.1371/journal.ppat.1004510] [PMID: 25412183]
[32]
Eoh, H.; Rhee, K.Y. Multifunctional essentiality of succinate metabolism in adaptation to hypoxia in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA, 2013, 110(16), 6554-6559.
[http://dx.doi.org/10.1073/pnas.1219375110] [PMID: 23576728]
[33]
Watanabe, S.; Zimmermann, M.; Goodwin, M.B.; Sauer, U.; Barry, C.E., III; Boshoff, H.I. Fumarate reductase activity maintains an energized membrane in anaerobic Mycobacterium tuberculosis. PLoS Pathog., 2011, 7(10), e1002287.
[http://dx.doi.org/10.1371/journal.ppat.1002287] [PMID: 21998585]
[34]
Niebisch, A.; Bott, M. Molecular analysis of the cytochrome bc1-aa3 branch of the Corynebacterium glutamicum respiratory chain containing an unusual diheme cytochrome c1. Arch. Microbiol., 2001, 175(4), 282-294.
[http://dx.doi.org/10.1007/s002030100262] [PMID: 11382224]
[35]
Sone, N.; Fukuda, M.; Katayama, S.; Jyoudai, A.; Syugyou, M.; Noguchi, S.; Sakamoto, J. QcrCAB operon of a nocardia-form actinomycete Rhodococcus rhodochrous encodes cytochrome reductase complex with diheme cytochrome cc subunit. Biochim. Biophys. Acta, 2003, 1557(1-3), 125-131.
[http://dx.doi.org/10.1016/S0005-2728(02)00394-8] [PMID: 12615356]
[36]
Schägger, H.; Pfeiffer, K. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J., 2000, 19(8), 1777-1783.
[http://dx.doi.org/10.1093/emboj/19.8.1777] [PMID: 10775262]
[37]
Eubel, H.; Jänsch, L.; Braun, H.P. New insights into the respiratory chain of plant mitochondria. Supercomplexes and a unique composition of complex II. Plant Physiol., 2003, 133(1), 274-286.
[http://dx.doi.org/10.1104/pp.103.024620] [PMID: 12970493]
[38]
Acín-Pérez, R.; Fernández-Silva, P.; Peleato, M.L.; Pérez-Martos, A.; Enriquez, J.A. Respiratory active mitochondrial supercomplexes. Mol. Cell, 2008, 32(4), 529-539.
[http://dx.doi.org/10.1016/j.molcel.2008.10.021] [PMID: 19026783]
[39]
Lynch, M.; Marinov, G.K. Membranes, energetics, and evolution across the prokaryote-eukaryote divide. eLife, 2017, 6, e20437.
[http://dx.doi.org/10.7554/eLife.20437] [PMID: 28300533]
[40]
Kühlbrandt, W. Structure and function of mitochondrial membrane protein complexes. BMC Biol., 2015, 13(1), 89.
[http://dx.doi.org/10.1186/s12915-015-0201-x] [PMID: 26515107]
[41]
Medina, M.A.; del Castillo-Olivares, A.; Núñez de Castro, I. Multifunctional plasma membrane redox systems. BioEssays, 1997, 19(11), 977-984.
[http://dx.doi.org/10.1002/bies.950191107] [PMID: 9394620]
[42]
Milenkovic, D.; Blaza, J.N.; Larsson, N.G.; Hirst, J. The enigma of the respiratory chain supercomplex. Cell Metab., 2017, 25(4), 765-776.
[http://dx.doi.org/10.1016/j.cmet.2017.03.009] [PMID: 28380371]
[43]
Clason, T.; Ruiz, T.; Schägger, H.; Peng, G.; Zickermann, V.; Brandt, U.; Michel, H.; Radermacher, M. The structure of eukaryotic and prokaryotic complex I. J. Struct. Biol., 2010, 169(1), 81-88.
[http://dx.doi.org/10.1016/j.jsb.2009.08.017] [PMID: 19732833]
[44]
Ackrell, B.A.C. Progress in understanding structure-function relationships in respiratory chain complex II. FEBS Lett., 2000, 466(1), 1-5.
[http://dx.doi.org/10.1016/S0014-5793(99)01749-4] [PMID: 10648801]
[45]
Xia, D.; Yu, C.A.; Kim, H.; Xia, J.Z.; Kachurin, A.M.; Zhang, L.; Yu, L.; Deisenhofer, J. Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria. Science, 1997, 277(5322), 60-66.
[http://dx.doi.org/10.1126/science.277.5322.60] [PMID: 9204897]
[46]
Iwata, S.; Lee, J.W.; Okada, K.; Lee, J.K.; Iwata, M.; Rasmussen, B.; Link, T.A.; Ramaswamy, S.; Jap, B.K. Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science, 1998, 281(5373), 64-71.
[http://dx.doi.org/10.1126/science.281.5373.64] [PMID: 9651245]
[47]
Iwata, S.; Ostermeier, C.; Ludwig, B.; Michel, H. Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature, 1995, 376(6542), 660-669.
[http://dx.doi.org/10.1038/376660a0] [PMID: 7651515]
[48]
Tomizaki, T.; Yamashita, E.; Yamaguchi, H.; Aoyama, H.; Tsukihara, T.; Shinzawa-Itoh, K.; Nakashima, R.; Yaono, R.; Yoshikawa, S. Structure analysis of bovine heart cytochrome c oxidase at 2.8 A resolution. Acta Crystallogr. D Biol. Crystallogr., 1999, 55(Pt 1), 31-45.
[http://dx.doi.org/10.1107/S0907444998006362] [PMID: 10089392]
[49]
Kim, M.S.; Jang, J.; Ab Rahman, N.B.; Pethe, K.; Berry, E.A.; Huang, L.S. Isolation and characterization of a hybrid respiratory supercomplex consisting of Mycobacterium tuberculosis cytochrome bcc and Mycobacterium smegmatis cytochrome aa3. J. Biol. Chem., 2015, 290(23), 14350-14360.
[http://dx.doi.org/10.1074/jbc.M114.624312] [PMID: 25861988]
[50]
Megehee, J.A.; Hosler, J.P.; Lundrigan, M.D. Evidence for a cytochrome bcc-aa3 interaction in the respiratory chain of Mycobacterium smegmatis. Microbiology, 2006, 152(Pt 3), 823-829.
[http://dx.doi.org/10.1099/mic.0.28723-0] [PMID: 16514162]
[51]
Matsoso, L.G.; Kana, B.D.; Crellin, P.K.; Lea-Smith, D.J.; Pelosi, A.; Powell, D.; Dawes, S.S.; Rubin, H.; Coppel, R.L.; Mizrahi, V. Function of the cytochrome bc1-aa3 branch of the respiratory network in mycobacteria and network adaptation occurring in response to its disruption. J. Bacteriol., 2005, 187(18), 6300-6308.
[http://dx.doi.org/10.1128/JB.187.18.6300-6308.2005] [PMID: 16159762]
[52]
Trumpower, B.L. Cytochrome bc1 complexes of microorganisms. Microbiol. Rev., 1990, 54(2), 101-129.
[http://dx.doi.org/10.1128/mr.54.2.101-129.1990] [PMID: 2163487]
[53]
Hinkle, P.C.; Kumar, M.A.; Resetar, A.; Harris, D.L. Mechanistic stoichiometry of mitochondrial oxidative phosphorylation. Biochemistry, 1991, 30(14), 3576-3582.
[http://dx.doi.org/10.1021/bi00228a031] [PMID: 2012815]
[54]
Zhang, Z.; Huang, L.; Shulmeister, V.M.; Chi, Y.I.; Kim, K.K.; Hung, L.W.; Crofts, A.R.; Berry, E.A.; Kim, S.H. Electron transfer by domain movement in cytochrome bc1. Nature, 1998, 392(6677), 677-684.
[http://dx.doi.org/10.1038/33612] [PMID: 9565029]
[55]
Hunte, C.; Koepke, J.; Lange, C.; Rossmanith, T.; Michel, H. Structure at 2.3 A resolution of the cytochrome bc(1) complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Structure, 2000, 8(6), 669-684.
[http://dx.doi.org/10.1016/S0969-2126(00)00152-0] [PMID: 10873857]
[56]
Berry, E.A.; Huang, L.S.; Saechao, L.K.; Pon, N.G.; Valkova- Valchanova, M.; Daldal, F. X-Ray Structure of Rhodobacter Capsulatus cytochrome bc (1): Comparison with its mitochondrial and chloroplast counterparts. Photosynth. Res., 2004, 81(3), 251-275.
[http://dx.doi.org/10.1023/B:PRES.0000036888.18223.0e] [PMID: 16034531]
[57]
Yu, C.A.; Xia, D.; Kim, H.; Deisenhofer, J.; Zhang, L.; Kachurin, A.M.; Yu, L. Structural basis of functions of the mitochondrial cytochrome bc1 complex. Biochim. Biophys. Acta, 1998, 1365(1-2), 151-158.
[http://dx.doi.org/10.1016/S0005-2728(98)00055-3] [PMID: 9693733]
[58]
Hopkins, A.; Buchanan, G.; Palmer, T. Role of the twin arginine protein transport pathway in the assembly of the Streptomyces coelicolor cytochrome bc1 complex. J. Bacteriol., 2014, 196(1), 50-59.
[http://dx.doi.org/10.1128/JB.00776-13] [PMID: 24142258]
[59]
Sone, N.; Tsuchiya, N.; Inoue, M.; Noguchi, S. Bacillus stearothermophilus qcr operon encoding rieske FeS protein, cytochrome b6, and a novel-type cytochrome c1 of quinol-cytochrome c reductase. J. Biol. Chem., 1996, 271(21), 12457-12462.
[http://dx.doi.org/10.1074/jbc.271.21.12457] [PMID: 8647852]
[60]
Darrouzet, E.; Daldal, F. Movement of the iron-sulfur subunit beyond the ef loop of cytochrome b is required for multiple turnovers of the bc1 complex but not for single turnover Qo site catalysis. J. Biol. Chem., 2002, 277(5), 3471-3476.
[http://dx.doi.org/10.1074/jbc.M107974200] [PMID: 11707449]
[61]
Tian, H.; Yu, L.; Mather, M.W.; Yu, C.A. Flexibility of the neck region of the rieske iron-sulfur protein is functionally important in the cytochrome bc1 complex. J. Biol. Chem., 1998, 273(43), 27953-27959.
[http://dx.doi.org/10.1074/jbc.273.43.27953] [PMID: 9774409]
[62]
Darrouzet, E.; Valkova-Valchanova, M.; Moser, C.C.; Dutton, P.L.; Daldal, F. Uncovering the [2Fe2S] domain movement in cytochrome bc1 and its implications for energy conversion. Proc. Natl. Acad. Sci. USA, 2000, 97(9), 4567-4572.
[http://dx.doi.org/10.1073/pnas.97.9.4567] [PMID: 10781061]
[63]
Esposti, M.D.; De Vries, S.; Crimi, M.; Ghelli, A.; Patarnello, T.; Meyer, A. Mitochondrial cytochrome b: evolution and structure of the protein. Biochim. Biophys. Acta, 1993, 1143(3), 243-271.
[http://dx.doi.org/10.1016/0005-2728(93)90197-N] [PMID: 8329437]
[64]
Widger, W. R.; Cramer, W. A.; Herrmann, R. G. Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b6-f complex : Position of the cytochrome b hemes in the membrane. 1984, 81(3), 674-78.
[http://dx.doi.org/10.1073/pnas.81.3.674]
[65]
Alric, J.; Pierre, Y.; Picot, D.; Lavergne, J.; Rappaport, F. Spectral and redox characterization of the heme ci of the cytochrome b6f complex. Proc. Natl. Acad. Sci. USA, 2005, 102(44), 15860-15865.
[http://dx.doi.org/10.1073/pnas.0508102102] [PMID: 16247018]
[66]
Kramer, D.M.; Roberts, A.G.; Muller, F.; Cape, J.; Bowman, M.K. Q-cycle bypass reactions at the Qo site of the cytochrome bc1 (and related) complexes. Methods Enzymol., 2004, 382, 21-45.
[http://dx.doi.org/10.1016/S0076-6879(04)82002-0] [PMID: 15047094]
[67]
Wikström, M.K.; Berden, J.A. Oxidoreduction of cytochrome b in the presence of antimycin. Biochim. Biophys. Acta, 1972, 283(3), 403-420.
[http://dx.doi.org/10.1016/0005-2728(72)90258-7] [PMID: 4346389]
[68]
Mitchell, P. The protonmotive Q cycle: a general formulation. FEBS Lett., 1975, 59(2), 137-139.
[http://dx.doi.org/10.1016/0014-5793(75)80359-0] [PMID: 1227927]
[69]
Mitchell, P. Protonmotive redox mechanism of the cytochrome b-c1 complex in the respiratory chain: protonmotive ubiquinone cycle. FEBS Lett., 1975, 56(1), 1-6.
[http://dx.doi.org/10.1016/0014-5793(75)80098-6] [PMID: 239860]
[70]
Mitchell, P. Possible molecular mechanisms of the protonmotive function of cytochrome systems. J. Theor. Biol., 1976, 62(2), 327-367.
[http://dx.doi.org/10.1016/0022-5193(76)90124-7] [PMID: 186667]
[71]
Birth, D.; Kao, W.C.; Hunte, C. Structural analysis of atovaquone-inhibited cytochrome bc1 complex reveals the molecular basis of antimalarial drug action. Nat. Commun., 2014, 5, 4029.
[http://dx.doi.org/10.1038/ncomms5029] [PMID: 24893593]
[72]
Gong, H.; Li, J.; Xu, A.; Tang, Y.; Ji, W.; Gao, R.; Wang, S.; Yu, L.; Tian, C.; Li, J.; Yen, H.Y.; Man Lam, S.; Shui, G.; Yang, X.; Sun, Y.; Li, X.; Jia, M.; Yang, C.; Jiang, B.; Lou, Z.; Robinson, C.V.; Wong, L.L.; Guddat, L.W.; Sun, F.; Wang, Q.; Rao, Z. An electron transfer path connects subunits of a mycobacterial respiratory supercomplex. Science, 2018, 362(6418), eaat8923.
[http://dx.doi.org/10.1126/science.aat8923] [PMID: 30361386]
[73]
Esser, L.; Quinn, B.; Li, Y.F.; Zhang, M.; Elberry, M.; Yu, L.; Yu, C.A.; Xia, D. Crystallographic studies of quinol oxidation site inhibitors: a modified classification of inhibitors for the cytochrome bc(1) complex. J. Mol. Biol., 2004, 341(1), 281-302.
[http://dx.doi.org/10.1016/j.jmb.2004.05.065] [PMID: 15312779]
[74]
Pethe, K.; Bifani, P.; Jang, J.; Kang, S.; Park, S.; Ahn, S.; Jiricek, J.; Jung, J.; Jeon, H.K.; Cechetto, J.; Christophe, T.; Lee, H.; Kempf, M.; Jackson, M.; Lenaerts, A.J.; Pham, H.; Jones, V.; Seo, M.J.; Kim, Y.M.; Seo, M.; Seo, J.J.; Park, D.; Ko, Y.; Choi, I.; Kim, R.; Kim, S.Y.; Lim, S.; Yim, S.A.; Nam, J.; Kang, H.; Kwon, H.; Oh, C.T.; Cho, Y.; Jang, Y.; Kim, J.; Chua, A.; Tan, B.H.; Nanjundappa, M.B.; Rao, S.P.S.; Barnes, W.S.; Wintjens, R.; Walker, J.R.; Alonso, S.; Lee, S.; Kim, J.; Oh, S.; Oh, T.; Nehrbass, U.; Han, S.J.; No, Z.; Lee, J.; Brodin, P.; Cho, S.N.; Nam, K.; Kim, J. Discovery of Q203, a potent clinical candidate for the treatment of tuberculosis. Nat. Med., 2013, 19(9), 1157-1160.
[http://dx.doi.org/10.1038/nm.3262] [PMID: 23913123]
[75]
Rybniker, J.; Vocat, A.; Sala, C.; Busso, P.; Pojer, F.; Benjak, A.; Cole, S.T. Lansoprazole is an antituberculous prodrug targeting cytochrome bc1. Nat. Commun., 2015, 6, 7659.
[http://dx.doi.org/10.1038/ncomms8659] [PMID: 26158909]
[76]
Chandrasekera, N.S.; Berube, B.J.; Shetye, G.; Chettiar, S.; O’Malley, T.; Manning, A.; Flint, L.; Awasthi, D.; Ioerger, T.R.; Sacchettini, J.; Masquelin, T.; Hipskind, P.A.; Odingo, J.; Parish, T. Improved phenoxyalkylbenzimidazoles with activity against Mycobacterium tuberculosis appear to target QcrB. ACS Infect. Dis., 2017, 3(12), 898-916.
[http://dx.doi.org/10.1021/acsinfecdis.7b00112] [PMID: 29035551]
[77]
Abrahams, K.A.; Cox, J.A.G.; Spivey, V.L.; Loman, N.J.; Pallen, M.J.; Constantinidou, C.; Fernández, R.; Alemparte, C.; Remuiñán, M.J.; Barros, D.; Ballell, L.; Besra, G.S. Identification of novel imidazo[1,2-a]pyridine inhibitors targeting M. tuberculosis QcrB. PLoS One, 2012, 7(12), e52951.
[http://dx.doi.org/10.1371/journal.pone.0052951] [PMID: 23300833]
[78]
Moraski, G.C.; Seeger, N.; Miller, P.A.; Oliver, A.G.; Boshoff, H.I.; Cho, S.; Mulugeta, S.; Anderson, J.R.; Franzblau, S.G.; Miller, M.J. Arrival of imidazo[2,1-b]thiazole-5-carboxamides: Potent anti-tuberculosis agents that target QcrB. ACS Infect. Dis., 2016, 2(6), 393-398.
[http://dx.doi.org/10.1021/acsinfecdis.5b00154] [PMID: 27627627]
[79]
Hunte, C.; Palsdottir, H.; Trumpower, B. L. Protonmotive pathways and mechanisms in the cytochrome bc1 complex. 2003, 545(1), 39-46.
[80]
Joliot, P.; Joliot, A. Mechanism of electron transfer in the cytochrome b/f complex of algae: evidence for a semiquinone cycle. Proc. Natl. Acad. Sci. USA, 1994, 91(3), 1034-1038.
[http://dx.doi.org/10.1073/pnas.91.3.1034] [PMID: 11607457]
[81]
Shapleigh, J. P.; Hosler, J. P.; Tecklenburg, M. M.; Kim, Y.; Babcock, G. T.; Gennis, R. B.; Ferguson-miller, S. Definition of the catalytic site of cytochrome c oxidase : Specific ligands of heme a and the heme a3-CuB center. 1992, 89(11), 4786-4790.
[http://dx.doi.org/10.1073/pnas.89.11.4786]
[82]
Morales-Rios, E.; Montgomery, M.G.; Leslie, A.G.; Walker, J.E. Structure of ATP synthase from Paracoccus denitrificans determined by X-ray crystallography at 4.0 Å resolution. Proc. Natl. Acad. Sci. USA, 2015, 112(43), 13231-13236.
[http://dx.doi.org/10.1073/pnas.1517542112] [PMID: 26460036]
[83]
Falke, D.; Fischer, M.; Biefel, B.; Ihling, C.; Hammerschmidt, C.; Reinefeld, K.; Haase, A.; Sinz, A.; Sawers, R.G. Cytochrome bcc-aa3 Oxidase Supercomplexes in the Aerobic Respiratory Chain of Streptomyces coelicolor A3(2). J. Mol. Microbiol. Biotechnol., 2018, 28(6), 255-268.
[http://dx.doi.org/10.1159/000496390] [PMID: 30861513]
[84]
Wiseman, B.; Nitharwal, R.G.; Fedotovskaya, O.; Schäfer, J.; Guo, H.; Kuang, Q.; Benlekbir, S.; Sjöstrand, D.; Ädelroth, P.; Rubinstein, J.L.; Brzezinski, P.; Högbom, M. Structure of a functional obligate complex III2IV2 respiratory supercomplex from Mycobacterium smegmatis. Nat. Struct. Mol. Biol., 2018, 25(12), 1128-1136.
[http://dx.doi.org/10.1038/s41594-018-0160-3] [PMID: 30518849]
[85]
Bengtsson, J.; Tjalsma, H.; Rivolta, C.; Hederstedt, L. Subunit II of Bacillus subtilis cytochrome c oxidase is a lipoprotein. J. Bacteriol., 1999, 181(2), 685-688.
[http://dx.doi.org/10.1128/JB.181.2.685-688.1999] [PMID: 9882689]
[86]
Wikström, M.; Jasaitis, A.; Backgren, C.; Puustinen, A.; Verkhovsky, M.I. The role of the D-and K-pathways of proton transfer in the function of the haem–copper oxidases. Biochim. Biophys. Acta (BBA)-. Bioenergetics, 2000, 1459(2–3), 514-520.
[http://dx.doi.org/10.1016/S0005-2728(00)00191-2] [PMID: 11004470]
[87]
Daum, G. Lipids of mitochondria. Biochim. Biophys. Acta (BBA)-. Reviews Biomembr., 1985, 822(1), 1-42.
[88]
Hoch, F.L. Cardiolipins and biomembrane function. Biochim. Biophys. Acta (BBA)-. Reviews Biomembr., 1992, 1113(1), 71-133.
[89]
Kagawa, Y.; Kandrach, A.; Racker, E. Partial resolution of the enzymes catalyzing oxidative phosphorylation. XXVI. Specificity of phospholipids required for energy transfer reactions. J. Biol. Chem., 1973, 248(2), 676-684.
[http://dx.doi.org/10.1016/S0021-9258(19)44427-X] [PMID: 4734332]
[90]
Dale, M.P.; Robinson, N.C. Synthesis of cardiolipin derivatives with protection of the free hydroxyl: its application to the study of cardiolipin stimulation of cytochrome c oxidase. Biochemistry, 1988, 27(21), 8270-8275.
[http://dx.doi.org/10.1021/bi00421a042] [PMID: 2852959]
[91]
Lange, C.; Nett, J.H.; Trumpower, B.L.; Hunte, C. Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J., 2001, 20(23), 6591-6600.
[http://dx.doi.org/10.1093/emboj/20.23.6591] [PMID: 11726495]
[92]
Wenz, T.; Covian, R.; Hellwig, P.; Macmillan, F.; Meunier, B.; Trumpower, B.L.; Hunte, C. Mutational analysis of cytochrome b at the ubiquinol oxidation site of yeast complex III. J. Biol. Chem., 2007, 282(6), 3977-3988.
[http://dx.doi.org/10.1074/jbc.M606482200] [PMID: 17145759]
[93]
Brasseur, G.; Levican, G.; Bonnefoy, V.; Holmes, D.; Jedlicki, E.; Lemesle-Meunier, D. Apparent redundancy of electron transfer pathways via bc(1) complexes and terminal oxidases in the extremophilic chemolithoautotrophic Acidithiobacillus ferrooxidans. Biochim. Biophys. Acta, 2004, 1656(2-3), 114-126.
[http://dx.doi.org/10.1016/j.bbabio.2004.02.008] [PMID: 15178473]
[94]
Lee, D.W.; Selamoglu, N.; Lanciano, P.; Cooley, J.W.; Forquer, I.; Kramer, D.M.; Daldal, F. Loss of a conserved tyrosine residue of cytochrome b induces reactive oxygen species production by cytochrome bc1. J. Biol. Chem., 2011, 286(20), 18139-18148.
[http://dx.doi.org/10.1074/jbc.M110.214460] [PMID: 21454570]
[95]
Crofts, A.R.; Guergova-Kuras, M.; Kuras, R.; Ugulava, N.; Li, J.; Hong, S. Proton-coupled electron transfer at the Q(o) site: what type of mechanism can account for the high activation barrier? Biochim. Biophys. Acta, 2000, 1459(2-3), 456-466.
[http://dx.doi.org/10.1016/S0005-2728(00)00184-5] [PMID: 11004463]
[96]
Kao, W.C.; Hunte, C. The molecular evolution of the Qo motif. Genome Biol. Evol., 2014, 6(7), 1894-1910.
[http://dx.doi.org/10.1093/gbe/evu147] [PMID: 25115012]
[97]
Gao, X.; Wen, X.; Yu, C.; Esser, L.; Tsao, S.; Quinn, B.; Zhang, L.; Yu, L.; Xia, D. The crystal structure of mitochondrial cytochrome bc1 in complex with famoxadone: the role of aromatic-aromatic interaction in inhibition. Biochemistry, 2002, 41(39), 11692-11702.
[http://dx.doi.org/10.1021/bi026252p] [PMID: 12269811]
[98]
Zheng, Y.J. Molecular basis for the enantioselective binding of a novel class of cytochrome bc1 complex inhibitors. J. Mol. Graph. Model., 2006, 25(1), 71-76.
[http://dx.doi.org/10.1016/j.jmgm.2005.11.003] [PMID: 16368254]
[99]
Vallières, C.; Fisher, N.; Antoine, T.; Al-Helal, M.; Stocks, P.; Berry, N.G.; Lawrenson, A.S.; Ward, S.A.; O’Neill, P.M.; Biagini, G.A.; Meunier, B. HDQ, a potent inhibitor of Plasmodium falciparum proliferation, binds to the quinone reduction site of the cytochrome bc1 complex. Antimicrob. Agents Chemother., 2012, 56(7), 3739-3747.
[http://dx.doi.org/10.1128/AAC.00486-12] [PMID: 22547613]
[100]
Wall, R.J.; Carvalho, S.; Milne, R.; Bueren-Calabuig, J.A.; Moniz, S.; Cantizani-Perez, J.; MacLean, L.; Kessler, A.; Cotillo, I.; Sastry, L.; Manthri, S.; Patterson, S.; Zuccotto, F.; Thompson, S.; Martin, J.; Marco, M.; Miles, T.J.; De Rycker, M.; Thomas, M.G.; Fairlamb, A.H.; Gilbert, I.H.; Wyllie, S. The Qi site of cytochrome b is a promiscuous drug target in Trypanosoma cruzi and Leishmania donovani. ACS Infect. Dis., 2020, 6(3), 515-528.
[http://dx.doi.org/10.1021/acsinfecdis.9b00426] [PMID: 31967783]
[101]
Cowley, R.; Leung, S.; Fisher, N.; Al-Helal, M.; Berry, N.G.; Lawrenson, A.S.; Sharma, R.; Shone, A.E.; Ward, S.A.; Biagini, G.A.; O’Neill, P.M. The development of quinolone esters as novel antimalarial agents targeting the Plasmodium falciparum bc1 protein complex. MedChemComm, 2012, 3(1), 39-44.
[http://dx.doi.org/10.1039/C1MD00183C]
[102]
Kim, H.; Xia, D.; Yu, C.A.; Xia, J.Z.; Kachurin, A.M.; Zhang, L.; Yu, L.; Deisenhofer, J. Inhibitor binding changes domain mobility in the iron-sulfur protein of the mitochondrial bc1 complex from bovine heart. Proc. Natl. Acad. Sci. USA, 1998, 95(14), 8026-8033.
[http://dx.doi.org/10.1073/pnas.95.14.8026] [PMID: 9653134]
[103]
Lamprecht, D.A.; Finin, P.M.; Rahman, M.A.; Cumming, B.M.; Russell, S.L.; Jonnala, S.R.; Adamson, J.H.; Steyn, A.J.C. Turning the respiratory flexibility of Mycobacterium tuberculosis against itself. Nat. Commun., 2016, 7, 12393.
[http://dx.doi.org/10.1038/ncomms12393] [PMID: 27506290]
[104]
Jang, J.; Kim, R.; Woo, M.; Jeong, J.; Park, D.E.; Kim, G.; Delorme, V. Efflux Attenuates the Antibacterial Activity of Q203 in Mycobacterium tuberculosis. Antimicrob. Agents Chemother., 2017, 61(7), e02637-e16.
[http://dx.doi.org/10.1128/AAC.02637-16] [PMID: 28416541]
[105]
O’Malley, T.; Alling, T.; Early, J.V.; Wescott, H.A.; Kumar, A.; Moraski, G.C.; Miller, M.J.; Masquelin, T.; Hipskind, P.A.; Parish, T. Imidazopyridine Compounds Inhibit Mycobacterial Growth by Depleting ATP Levels. Antimicrob. Agents Chemother., 2018, 62(6), e02439-e17.
[http://dx.doi.org/10.1128/AAC.02439-17] [PMID: 29632008]
[106]
Moraski, G.C.; Markley, L.D.; Hipskind, P.A.; Boshoff, H.; Cho, S.; Franzblau, S.G.; Miller, M.J. Advent of Imidazo[1,2-a]pyridine-3-carboxamides with Potent Multi- and Extended Drug Resistant Antituberculosis Activity. ACS Med. Chem. Lett., 2011, 2(6), 466-470.
[http://dx.doi.org/10.1021/ml200036r] [PMID: 21691438]
[107]
Moraski, G.C.; Markley, L.D.; Cramer, J.; Hipskind, P.A.; Boshoff, H.; Bailey, M.; Alling, T.; Ollinger, J.; Parish, T.; Miller, M.J. Advancement of Imidazo[1,2-a]pyridines with Improved Pharmacokinetics and Nanomolar Activity Against Mycobacterium tuberculosis. ACS Med. Chem. Lett., 2013, 4(7), 675-679.
[http://dx.doi.org/10.1021/ml400088y] [PMID: 23930153]
[108]
Cleghorn, L.A.T.; Ray, P.C.; Odingo, J.; Kumar, A.; Wescott, H.; Korkegian, A.; Masquelin, T.; Lopez Moure, A.; Wilson, C.; Davis, S.; Huggett, M.; Turner, P.; Smith, A.; Epemolu, O.; Zuccotto, F.; Riley, J.; Scullion, P.; Shishikura, Y.; Ferguson, L.; Rullas, J.; Guijarro, L.; Read, K.D.; Green, S.R.; Hipskind, P.; Parish, T.; Wyatt, P.G. Identification of morpholino thiophenes as novel Mycobacterium tuberculosis inhibitors, targeting QcrB. J. Med. Chem., 2018, 61(15), 6592-6608.
[http://dx.doi.org/10.1021/acs.jmedchem.8b00172] [PMID: 29944372]
[109]
van der Westhuyzen, R.; Winks, S.; Wilson, C.R.; Boyle, G.A.; Gessner, R.K.; Soares de Melo, C.; Taylor, D.; de Kock, C.; Njoroge, M.; Brunschwig, C.; Lawrence, N.; Rao, S.P.S.; Sirgel, F.; van Helden, P.; Seldon, R.; Moosa, A.; Warner, D.F.; Arista, L.; Manjunatha, U.H.; Smith, P.W.; Street, L.J.; Chibale, K. Pyrrolo[3,4-c]pyridine-1,3(2H)-diones: A novel antimycobacterial class targeting mycobacterial respiration. J. Med. Chem., 2015, 58(23), 9371-9381.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01542] [PMID: 26551248]
[110]
Khoje, A.D.; Charnock, C.; Wan, B.; Franzblau, S.; Gundersen, L.L. Synthesis and antimycobacterial activities of non-purine analogs of 6-aryl-9-benzylpurines: Imidazopyridines, pyrrolopyridines, benzimidazoles, and indoles. Bioorg. Med. Chem., 2011, 19(11), 3483-3491.
[http://dx.doi.org/10.1016/j.bmc.2011.04.023] [PMID: 21546254]
[111]
Florent, C.; Audigier, J.C.; Boyer, J.; Camatte, R.; Corallo, J.; Delmont, J.; Doffoel, M.; Escourrou, J.; Evreux, M.; Gipoulou, V.; Laugier, R.; Paris, J.C.; Pascal, J.P.; Pienkowski, P.; Rampal, P.; Joubert-Collin, M. Efficacy and safety of lansoprazole in the treatment of gastric ulcer: a multicentre study. Eur. J. Gastroenterol. Hepatol., 1994, 6(12), 1135-1140.
[http://dx.doi.org/10.1097/00042737-199412000-00012]
[112]
Mee, A.S.; Rowley, J.L. Rapid symptom relief in reflux oesophagitis: a comparison of lansoprazole and omeprazole. Aliment. Pharmacol. Ther., 1996, 10(5), 757-763.
[http://dx.doi.org/10.1046/j.1365-2036.1996.56198000.x] [PMID: 8899084]
[113]
Mdanda, S.; Baijnath, S.; Shobo, A.; Singh, S.D.; Maguire, G.E.M.; Kruger, H.G.; Arvidsson, P.I.; Naicker, T.; Govender, T. Lansoprazole-sulfide, pharmacokinetics of this promising anti-tuberculous agent. Biomed. Chromatogr., 2017, 31(12)
[http://dx.doi.org/10.1002/bmc.4035] [PMID: 28623874]
[114]
Yates, T.A.; Tomlinson, L.A.; Bhaskaran, K.; Langan, S.; Thomas, S.; Smeeth, L.; Douglas, I.J. Lansoprazole use and tuberculosis incidence in the United Kingdom Clinical Practice Research Datalink: A population based cohort. PLoS Med., 2017, 14(11), e1002457.
[http://dx.doi.org/10.1371/journal.pmed.1002457] [PMID: 29161254]
[115]
Welage, L.S. Pharmacologic properties of proton pump inhibitors. Pharmacotherapy, 2003, 23(10 Pt 2), 74S-80S.
[http://dx.doi.org/10.1592/phco.23.13.74S.31929] [PMID: 14587961]
[116]
Delhotal-Landes, B.; Flouvat, B.; Duchier, J.; Molinie, P.; Dellatolas, F.; Lemaire, M. Pharmacokinetics of lansoprazole in patients with renal or liver disease of varying severity. Eur. J. Clin. Pharmacol., 1993, 45(4), 367-371.
[http://dx.doi.org/10.1007/BF00265957] [PMID: 8299672]
[117]
Song, M.; Gao, X.; Hang, T.J.; Wen, A.D. Pharmacokinetic properties of lansoprazole (30-mg enteric-coated capsules) and its metabolites: A single-dose, open-label study in healthy Chinese male subjects. Curr. Ther. Res. Clin. Exp., 2009, 70(3), 228-239.
[http://dx.doi.org/10.1016/j.curtheres.2009.05.002] [PMID: 24683233]

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