Type-II NADH Dehydrogenase (NDH-2): a promising therapeutic target for antitubercular and antibacterial drug discovery

References

• Chukwuanukwu RC, Onyenekwe CC, Martinez-Pomares L, et al. Modulation of the immune response to Mycobacterium tuberculosis during malaria/M. tuberculosis co-infection. Clin Exp Immunol. 2017;187:259–268.
   PubMed Web of Science ®Google Scholar
• Shiffman J. Four challenges that global health networks face. Int J Health Policy Manag. 2017;6:183–189.
   PubMed Web of Science ®Google Scholar
• Riccardi G, Old IG, Ekins S. Raising awareness of the importance of funding for tuberculosis small-molecule research. Drug Discovery Today. 2017;22:487–491.
   PubMed Web of Science ®Google Scholar
• Organization WH. Global tuberculosis report 2016. 2016.
   Google Scholar
• Knechel NA. Tuberculosis: pathophysiology, clinical features, and diagnosis. Crit Care Nurse. 2009;29:34–43.
   PubMed Web of Science ®Google Scholar
• Lin PL, Flynn JL. Understanding latent tuberculosis: a moving target. J Immunol. 2010;185:15–22.
   PubMed Web of Science ®Google Scholar
• Dai R, Wilson DJ, Geders TW, et al. Inhibition of Mycobacterium tuberculosis transaminase BioA by aryl hydrazines and hydrazides. ChemBioChem. 2014;15:575–586.
   PubMed Web of Science ®Google Scholar
• Blair HA, Scott LJ. Delamanid: a review of its use in patients with multidrug-resistant tuberculosis. Drugs. 2015;75:91–100.
   PubMed Web of Science ®Google Scholar
• Lu X, Smare C, Kambili C, et al. Health outcomes of bedaquiline in the treatment of multidrug-resistant tuberculosis in selected high burden countries. BMC Health Serv Res. 2017;17:87.
   PubMed Web of Science ®Google Scholar
• Somoskovi A, Bruderer V, Hömke R, et al. A mutation associated with clofazimine and bedaquiline cross-resistance in MDR-TB following bedaquiline treatment. Eur Respir J. 2015;45(2):554–557.
   PubMed Web of Science ®Google Scholar
• Andries K, Villellas C, Coeck N, et al. Acquired Resistance of Mycobacterium tuberculosis to Bedaquiline. Plos ONE. 2014;9:e102135.
   PubMed Web of Science ®Google Scholar
• Santana M, Ionescu MS, Vertes A, et al. Bacillus subtilis F0F1 ATPase: DNA sequence of the atp operon and characterization of atp mutants. J Bacteriol. 1994;176:6802–6811.
   PubMed Web of Science ®Google Scholar
• Andries K, Verhasselt P, Guillemont J, et al. A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science. 2005;307:223–227.
   PubMed Web of Science ®Google Scholar
• Koul A, Vranckx L, Dendouga N, et al. Diarylquinolines are bactericidal for dormant mycobacteria as a result of disturbed ATP homeostasis. J Biol Chem. 2008;283:25273–25280.
   PubMed Web of Science ®Google Scholar
• Cook GM, Hards K, Vilchèze C, et al. Energetics of respiration and oxidative phosphorylation in mycobacteria. Microbiol Spectr. 2014;2(3). DOI:10.1128/microbiolspec.MGM2-0015-2013
   Google Scholar
• Cox RA, Cook GM. Growth regulation in the mycobacterial cell. Curr Mol Med. 2007;7:231–245.
   PubMed Web of Science ®Google Scholar
• Rao SP, Alonso S, Rand L, et al. The protonmotive force is required for maintaining ATP homeostasis and viability of hypoxic, nonreplicating Mycobacterium tuberculosis. Proc Natl Acad Sci. 2008;105:11945–11950.
   PubMed Web of Science ®Google Scholar
• Fang J, Beattie DS. Novel FMN-containing rotenone-insensitive NADH dehydrogenase from Trypanosoma brucei mitochondria: isolation and characterization. Biochemistry. 2002;41:3065–3072.
   PubMed Web of Science ®Google Scholar
• Fisher N, Bray PG, Ward SA, et al. The malaria parasite type II NADH: quinone oxidoreductase: an alternative enzyme for an alternative lifestyle. Trends Parasitol. 2007;23:305–310.
   PubMed Web of Science ®Google Scholar
• Teh JS, Yano T, Rubin H. Type II NADH: menaquinone oxidoreductase of Mycobacterium tuberculosis. Infect Disord Drug Targets. 2007;7:169–181.
   PubMedGoogle Scholar
• Cosma CL, Sherman DR, Ramakrishnan L. The secret lives of the pathogenic mycobacteria. Annu Rev Microbiol. 2003;57:641–676.
   PubMed Web of Science ®Google Scholar
• Koul A, Arnoult E, Lounis N, et al. The challenge of new drug discovery for tuberculosis. Nature. 2011;469:483–490.
   PubMed Web of Science ®Google Scholar
• Wayne LG, Sohaskey CD. Nonreplicating persistence of Mycobacterium tuberculosis. Annu Rev Microbiol. 2001;55:139–163.
   PubMed Web of Science ®Google Scholar
• Timm J, Post FA, Bekker L-G, et al. Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronically infected mice and tuberculosis patients. Proc Natl Acad Sci. 2003;100:14321–14326.
   PubMed Web of Science ®Google Scholar
• Bald D, Koul A. Respiratory ATP synthesis: the new generation of mycobacterial drug targets? FEMS Microbiol Lett. 2010;308:1–7.
   PubMed Web of Science ®Google Scholar
• Berney M, Cook GM. Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS One. 2010;5:e8614.
   PubMed Web of Science ®Google Scholar
• Gomez JE, McKinney JD. M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis. 2004;84:29–44.
   PubMed Web of Science ®Google Scholar
• Bald D, Koul A. Advances and strategies in discovery of new antibacterials for combating metabolically resting bacteria. Drug Discovery Today. 2013;18:250–255.
   PubMed Web of Science ®Google Scholar
• Kerscher S, Dröse S, Zickermann V, et al. The three families of respiratory NADH dehydrogenases. Results Probl Cell Differ. 2008;45:185–222.
   PubMedGoogle Scholar
• Heikal A, Nakatani Y, Dunn E, et al. Structure of the bacterial type II NADH dehydrogenase: a monotopic membrane protein with an essential role in energy generation. Mol Microbiol. 2014;91:950–964.
   PubMed Web of Science ®Google Scholar
• Neehaul Y, Juárez O, Barquera B, et al. Infrared spectroscopic evidence of a redox-dependent conformational change involving ion binding residue NqrB-D397 in the Na+-pumping NADH: quinone oxidoreductase from Vibrio cholerae. Biochemistry. 2013;52:3085–3093.
   PubMed Web of Science ®Google Scholar
• Novakovsky GE, Dibrova DV, Mulkidjanian AY. Phylogenomic analysis of type 1 NADH: quinone oxidoreductase. Biochemistry (Moscow). 2016;81:770–784.
   PubMed Web of Science ®Google Scholar
• Heikal A, Hards K, Cheung C-Y, et al. Activation of type II NADH dehydrogenase by quinolinequinones mediates antitubercular cell death. J Antimicrob Chemother. 2016;71(10):2840–2847.
   PubMed Web of Science ®Google Scholar
• Young IG, Rogers BL, Campbell HD, et al. Nucleotide sequence coding for the respiratory NADH dehydrogenase of Escherichia coli. UUG Initiation Codon. Eur J Biochem. 1981;116:165–170.
   PubMed Web of Science ®Google Scholar
• Jaworowski A, Mayo G, Shaw DC, et al. Characterization of the respiratory NADH dehydrogenase of Escherichia coli and reconstitution of NADH oxidase in ndh mutant membrane vesicles. Biochemistry. 1981;20:3621–3628.
   PubMed Web of Science ®Google Scholar
• Sena FV, Batista AP, Catarino T, et al. Type‐II NADH: quinone oxidoreductase from Staphylococcus aureus has two distinct binding sites and is rate limited by quinone reduction. Mol Microbiol. 2015;98:272–288.
   PubMed Web of Science ®Google Scholar
• Yano T, Rahimian M, Aneja KK, et al. Mycobacterium tuberculosis type II NADH-menaquinone oxidoreductase catalyzes electron transfer through a two-site ping-pong mechanism and has two quinone-binding sites. Biochemistry. 2014;53:1179–1190.
   PubMed Web of Science ®Google Scholar
• Yang Y, Yamashita T, Nakamaru-Ogiso E, et al. Reaction mechanism of single subunit NADH-Ubiquinone Oxidoreductase (Ndi1) from Saccharomyces cerevisiae evidence for a ternary complex mechanism. J Biol Chem. 2011;286:9287–9297.
   PubMed Web of Science ®Google Scholar
• Weinstein EA, Yano T, Li L-S, et al. Inhibitors of type II NADH: menaquinone oxidoreductase represent a class of antitubercular drugs. Proc Natl Acad Sci USA. 2005;102:4548–4553.
   PubMed Web of Science ®Google Scholar
• Mogi T, Matsushita K, Murase Y, et al. Identification of new inhibitors for alternative NADH dehydrogenase (NDH-II). FEMS Microbiol Lett. 2009;291:157–161.
   PubMed Web of Science ®Google Scholar
• Kerscher SJ, Okun JG, Brandt U. A single external enzyme confers alternative NADH: ubiquinone oxidoreductase activity in Yarrowia lipolytica. ‎J Cell Sci. 1999;112:2347–2354.
   PubMed Web of Science ®Google Scholar
• Vries S, Grivell LA. Purification and characterization of a rotenone insensitive NADH: Q6 oxidoreductase from mitochondria of Saccharomyces cerevisiae. Eur J Biochem. 1988;176:377–384.
   PubMedGoogle Scholar
• Biagini GA, Viriyavejakul P, O’neill PM, et al. Functional characterization and target validation of alternative complex I of Plasmodium falciparum mitochondria. Antimicrob Agents Chemother. 2006;50:1841–1851.
   PubMed Web of Science ®Google Scholar
• Björklöf K, Zickermann V, Finel M. Purification of the 45 kDa, membrane bound NADH dehydrogenase of Escherichia coli (NDH-2) and analysis of its interaction with ubiquinone analogues. FEBS Letters. 2000;467:105–110.
   PubMed Web of Science ®Google Scholar
• Salewski J, Batista AP, Sena FV, et al. Substrate-Protein Interactions of Type II NADH: quinone Oxidoreductase from Escherichia coli. Biochemistry. 2016;55:2722–2734.
   PubMed Web of Science ®Google Scholar
• Payne DJ, Gwynn MN, Holmes DJ, et al. Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat Rev Drug Discov. 2007;6:29–40.
   PubMed Web of Science ®Google Scholar
• Sharma U. Current possibilities and unresolved issues of drug target validation in Mycobacterium tuberculosis. Expert Opin Drug Discov. 2011;6:1171–1186.
   PubMed Web of Science ®Google Scholar
• Duncan K. Identification and validation of novel drug targets in tuberculosis. Curr Pharm Des. 2004;10:3185–3194.
   PubMed Web of Science ®Google Scholar
• Koul A, Dendouga N, Vergauwen K, et al. Diarylquinolines target subunit c of mycobacterial ATP synthase. Nat Chem Biol. 2007;3:323–324.
   PubMed Web of Science ®Google Scholar
• De Jonge MR, Koymans LH, Guillemont JE, et al. A computational model of the inhibition of Mycobacterium tuberculosis ATPase by a new drug candidate R207910. Proteins. 2007;67:971–980.
   PubMed Web of Science ®Google Scholar
• Vilcheze C, Weisbrod TR, Chen B, et al. Altered NADH/NAD+ ratio mediates coresistance to isoniazid and ethionamide in mycobacteria. Antimicrob Agents Chemother. 2005;49:708–720.
   PubMed Web of Science ®Google Scholar
• Barry CE, Boshoff HI, Dartois V, et al. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nature Rev Microbiol. 2009;7:845–855.
   PubMed Web of Science ®Google Scholar
• Schurig-Briccio LA, Yano T, Rubin H, et al. Characterization of the type 2 NADH: menaquinone oxidoreductases from Staphylococcus aureus and the bactericidal action of phenothiazines. Biochimica Et Biophysica Acta (Bba)-Bioenergetics. 2014;1837:954–963.
   PubMed Web of Science ®Google Scholar
• Young I, Jaworowski A, Poulis M. Amplification of the respiratory NADH dehydrogenase of Escherichia coli by gene cloning. Gene. 1978;4:25–36.
   PubMed Web of Science ®Google Scholar
• Miesel L, Weisbrod TR, Marcinkeviciene JA, et al. NADH dehydrogenase defects confer isoniazid resistance and conditional lethality in Mycobacterium smegmatis. ‎J Bacteriol. 1998;180:2459–2467.
   PubMed Web of Science ®Google Scholar
• Awasthy D, Ambady A, Narayana A, et al. Roles of the two type II NADH dehydrogenases in the survival of Mycobacterium tuberculosis in vitro. Gene. 2014;550:110–116.
   PubMed Web of Science ®Google Scholar
• Shirude PS, Paul B, Roy Choudhury N, et al. Quinolinyl pyrimidines: potent inhibitors of NDH-2 as a novel class of anti-TB agents. ACS Med Chem Lett. 2012;3:736–740.
   PubMed Web of Science ®Google Scholar
• Fisher N, Warman AJ, Ward SA, et al. Type II NADH: quinone oxidoreductases of plasmodium falciparum and mycobacterium tuberculosis: kinetic and high-throughput assays. Methods Enzymol. 2009;456:303–320.
   PubMed Web of Science ®Google Scholar
• He C-X, Meng H, Zhang X, et al. Synthesis and bio-evaluation of phenothiazine derivatives as new anti-tuberculosis agents. Chin Chem Lett. 2015;26:951–954.
   Web of Science ®Google Scholar
• Bourdon J. Contribution to the study of the antibiotic properties of chlorpromazine or 4560 RP. Ann Inst Pasteur (Paris). 1961;101:876–886.
   PubMedGoogle Scholar
• Kamińska M. Role of chlorpromazine in the treatment of pulmonary tuberculosis in psychiatric patients. Folia Medica Cracoviensia. 1966;9:115–143.
   Google Scholar
• Amaral L, Martins A, Molnar J, et al. Phenothiazines, bacterial efflux pumps and targeting the macrophage for enhanced killing of intracellular XDRTB. In Vivo. 2010;24:409–424.
   PubMed Web of Science ®Google Scholar
• Amaral L, Molnar J. Potential therapy of multidrug-resistant and extremely drug-resistant tuberculosis with thioridazine. In Vivo. 2012;26:231–236.
   PubMed Web of Science ®Google Scholar
• Amaral L, Kristiansen JE, Viveiros M, et al. Activity of phenothiazines against antibiotic-resistant Mycobacterium tuberculosis: a review supporting further studies that may elucidate the potential use of thioridazine as anti-tuberculosis therapy. J Antimicrob Chemother. 2001;47:505–511.
   PubMed Web of Science ®Google Scholar
• Gadre D, Talwar V, Gupta H, et al. Effect of trifluoperazine, a potential drug for tuberculosis with psychotic disorders, on the growth of clinical isolates of drug resistant Mycobactehum tuberculosis. Int Clin Psychopharmacol. 1998;13:129–132.
   PubMed Web of Science ®Google Scholar
• Crowle A, Douvas G, May M. Chlorpromazine: a drug potentially useful for treating mycobacterial infections. Chemotherapy. 1992;38:410–419.
   PubMed Web of Science ®Google Scholar
• Reddy MV, Nadadhur G, Gangadharam PRJ. In-vitro and intracellular antimycobacterial activity of trifluoperazine. J Antimicrob Chemother. 1996;37:196–197.
   PubMed Web of Science ®Google Scholar
• Van Soolingen D, Hernandez-Pando R, Orozco H, et al. The antipsychotic thioridazine shows promising therapeutic activity in a mouse model of multidrug-resistant tuberculosis. PLoS One. 2010;5:e12640.
   PubMed Web of Science ®Google Scholar
• Katoch VM, Saxena N, Shivannavar CT, et al. Effect of trifluoperazine on in vitro ATP synthesis by Mycobacterium leprae. FEMS Immunol Med Microbiol. 1998;20:99–102.
   PubMedGoogle Scholar
• Amaral L, Viveiros M. Why thioridazine in combination with antibiotics cures extensively drug-resistant Mycobacterium tuberculosis infections. Int J Antimicrob Agents. 2012;39:376–380.
   PubMed Web of Science ®Google Scholar
• Amaral L, Martins M, Viveiros M, et al. Promising therapy of XDR-TB/MDR-TB with thioridazine an inhibitor of bacterial efflux pumps. Curr Drug Targets. 2008;9:816–819.
   PubMed Web of Science ®Google Scholar
• Bate AB, Kalin JH, Fooksman EM, et al. Synthesis and antitubercular activity of quaternized promazine and promethazine derivatives. Bioorg Med Chem Lett. 2007;17:1346–1348.
   PubMed Web of Science ®Google Scholar
• Dunn EA, Roxburgh M, Larsen L, et al. Incorporation of triphenylphosphonium functionality improves the inhibitory properties of phenothiazine derivatives in Mycobacterium tuberculosis. Bioorg Med Chem. 2014;22:5320–5328.
   PubMed Web of Science ®Google Scholar
• Warman AJ, Rito T, Fisher N, et al. The type II NADH: quinone oxidoreductase of Mycobacterium tuberculosis: a novel drug target for an age-old problem. Biochimica Et Biophysica Acta (Bba)-Bioenergetics. 2010;1797(Supplement):117–118.
   Web of Science ®Google Scholar
• Mulchin BJ, Newton CG, Baty JW, et al. The anti-cancer, anti-inflammatory and tuberculostatic activities of a series of 6, 7-substituted-5, 8-quinolinequinones. Bioorg Med Chem. 2010;18:3238–3251.
   PubMed Web of Science ®Google Scholar
• Lipinski CA, Lombardo F, Dominy BW, et al. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev. 2012;64:4–17.
   Web of Science ®Google Scholar
• Dunn EA, Cook GM, Heikal A. Comparison of lipid and detergent enzyme environments for identifying inhibitors of membrane-bound energy-transducing proteins. J Microbiol Methods. 2016;120:41–43.
   PubMed Web of Science ®Google Scholar
• Dunn EA, Cook GM, Heikal A. Annotated compound data for modulators of detergent-solubilised or lipid-reconstituted respiratory type II NADH dehydrogenase activity obtained by compound library screening. Data in Brief. 2016;6:275–278.
   PubMedGoogle Scholar
• Jünemann S. Cytochrome bd terminal oxidase. Biochimica Et Biophysica Acta (Bba)-Bioenergetics. 1997;1321:107–127.
   PubMed Web of Science ®Google Scholar
• Mogi T. Two terminal quinol oxidase families in Escherichia coli: variations on molecular machinery for dioxygen reduction. J Biochem Mol Biol Biophys. 1998;2:79–110.
   Google Scholar
• Ui H, Ishiyama A, Sekiguchi H, et al. Selective and potent in vitro antimalarial activities found in four microbial metabolites. J Antibiot. 2007;60:220.
   PubMed Web of Science ®Google Scholar
• Mogi T, Ui H, Shiomi K, et al. Gramicidin S identified as a potent inhibitor for cytochrome bd-type quinol oxidase. FEBS Letters. 2008;582:2299–2302.
   PubMed Web of Science ®Google Scholar
• Yano T, Li L-S, Weinstein E, et al. Steady-state kinetics and inhibitory action of antitubercular phenothiazines on Mycobacterium tuberculosis type-II NADH-menaquinone oxidoreductase (NDH-2). J Biol Chem. 2006;281:11456–11463.
   PubMed Web of Science ®Google Scholar
• Yano T, Kassovska-Bratinova S, Teh JS, et al. Reduction of clofazimine by mycobacterial type 2 NADH: quinone oxidoreductase: a pathway for the generation of bactericidal levels of reactive oxygen species. J Biol Chem. 2011;286:10276–10287.
   PubMed Web of Science ®Google Scholar
• Zumla AI, Gillespie SH, Hoelscher M, et al. New antituberculosis drugs, regimens, and adjunct therapies: needs, advances, and future prospects. Lancet Infect Dis. 2014;14:327–340.
   PubMed Web of Science ®Google Scholar
• Melo AMP, Bandeiras TM, Teixeira M. New insights into type II NAD(P)H: quinone oxidoreductases. Microbiol Mol Biol Rev. 2004;68:603–616.
   PubMed Web of Science ®Google Scholar
• Vesenbeckh S, Krieger D, Bettermann G, et al. Neuroleptic drugs in the treatment of tuberculosis: minimal inhibitory concentrations of different phenothiazines against Mycobacterium tuberculosis. Tuberculosis. 2016;98:27–29.
   PubMed Web of Science ®Google Scholar