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Review

ATP-binding cassette (ABC) import systems of Mycobacterium tuberculosis: target for drug and vaccine development

ORCID Icon, &
Pages 207-220 | Received 28 Aug 2019, Accepted 02 Dec 2019, Published online: 27 Jan 2020

References

  • World Health Organization (WHO). Global tuberculosis report. 2018; WHO, Geneva.
  • Migliori GB, De Iaco G, Besozzi G, et al. First tuberculosis cases in Italy resistant to all tested drugs. Euro Surveill. 2007;12(5):E070517. 1.
  • Udwadia ZF, Amale RA, Ajbani KK, et al. Totally drug-resistant tuberculosis in India. Clin Infect Dis. 2012;54(4):579–581.
  • Dockrell HM, Smith SG. What have we learnt about BCG vaccination in the last 20 years? Front Immunol. 2017;8:1134.
  • Cook GM, Berney M, Gebhard S, et al. Physiology of mycobacteria. Adv Microb Physiol. 2009;55:81–182. 318-319.
  • Gouzy A, Larrouy-Maumus G, Bottai D, et al. Mycobacterium tuberculosis exploits asparagine to assimilate nitrogen and resist acid stress during infection. PLoS Pathog. 2014;10(2):e1003928.
  • Rohde KH, Abramovitch RB, Russell DG. Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host Microbe. 2007;2(5):352–364.
  • Tailleux L, Waddell SJ, Pelizzola M, et al. Probing host pathogen cross-talk by transcriptional profiling of both Mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS One. 2008;3(1):e1403.
  • Homolka S, Niemann S, Russell DG, et al. Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: delineation of conserved core and lineage-specific transcriptomes during intracellular survival. PLoS Pathog. 2010;6(7):e1000988.
  • Rohde KH, Veiga DF, Caldwell S, et al. Linking the transcriptional profiles and the physiological states of Mycobacterium tuberculosis during an extended intracellular infection. PLoS Pathog. 2012;8(6):e1002769.
  • Braibant M, Gilot P, Content J. The ATP binding cassette (ABC) transport systems of Mycobacterium tuberculosis. FEMS Microbiol Rev. 2000;24(4):449–467.
  • Youm J, Saier MH Jr. Comparative analyses of transport proteins encoded within the genomes of Mycobacterium tuberculosis and Mycobacterium leprae. Biochim Biophys Acta. 2012;1818(3):776–797.
  • Sassetti CM, Boyd DH, Rubin EJ. Comprehensive identification of conditionally essential genes in mycobacteria. Proc Natl Acad Sci USA. 2001;98(22):12712–12717.
  • Sassetti CM, Rubin EJ. Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA. 2003;100(22):12989–12994.
  • Price CT, Bukka A, Cynamon M, et al. Glycine betaine uptake by the ProXVWZ ABC transporter contributes to the ability of Mycobacterium tuberculosis to initiate growth in human macrophages. J Bacteriol. 2008;190(11):3955–3961.
  • Rodriguez GM, Smith I. Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J Bacteriol. 2006;188(2):424–430.
  • Dasgupta A, Sureka K, Mitra D, et al. An oligopeptide transporter of Mycobacterium tuberculosis regulates cytokine release and apoptosis of infected macrophages. PLoS One. 2010;5(8):e12225.
  • van der Heide T, Poolman B. ABC transporters: one, two or four extracytoplasmic substrate-binding sites? EMBO Rep. 2002;3(10):938–943.
  • Davidson AL, Dassa E, Orelle C, et al. Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev. 2008;72(2):317–364.
  • ter Beek J, Guskov A, Slotboom DJ. Structural diversity of ABC transporters. J Gen Physiol. 2014;143(4):419–435.
  • Rees DC, Johnson E, Lewinson O. ABC transporters: the power to change. Nat Rev Mol Cell Biol. 2009;10(3):218–227.
  • Locher KP. Mechanistic diversity in ATP-binding cassette (ABC) transporters. Nat Struct Mol Biol. 2016;23(6):487–493.
  • Kadaba NS, Kaiser JT, Johnson E, et al. The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science. 2008;321(5886):250–253.
  • Gerber S, Comellas-Bigler M, Goetz BA, et al. Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science. 2008;321:246–250.
  • Chen SS, Oldham ML, Davidson AL, et al. Carbon catabolite repression of the maltose transporter revealed by X-ray crystallography. Nature. 2013;499:364–368.
  • Locher KP, Lee AT, Rees DC. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science. 2002;296:1091–1098.
  • Pinkett HW, Lee AT, Lum P, et al. An inward-facing conformation of a putative metal-chelate-type ABC transporter. Science. 2007;315:373–377.
  • Woo JS, Zeltina A, Goetz BA, et al. X-ray structure of the Yersinia pestis heme transporter HmuUV. Nat Struct Mol Biol. 2012;19:1310–1315.
  • Flores-Valdez MA, Morris RP, Laval F, et al. Mycobacterium tuberculosis modulates its cell surface via an oligopeptide permease (Opp) transport system. FASEB J. 2009;23(12):4091–4104.
  • Green RM, Seth A, Connell ND. A peptide permease mutant of Mycobacterium bovis BCG resistant to the toxic peptides glutathione and S-nitrosoglutathione. Infect Immun. 2000;68(2):429–436.
  • Stewart GR, Patel J, Robertson BD, et al. Mycobacterial mutants with defective control of phagosomal acidification. PLoS Pathog. 2005;1(3):269–278.
  • Zhao JH, Chen JH, Wang Y, et al. The putative compatible solute-binding protein ProX from Mycobacterium tuberculosis H37Rv: biochemical characterization and crystallographic data. Acta Crystallogr F Struct Biol Commun. 2018;74(Pt 4):231–235.
  • McKinney JD, Höner zu Bentrup K, Muñoz-Elías EJ, et al. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature. 2000;406(6797):735–738.
  • Muñoz-Elías EJ, McKinney JD. Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat Med. 2005;11(6):638–644.
  • Titgemeyer F, Amon J, Parche S, et al. A genomic view of sugar transport in Mycobacterium smegmatis and Mycobacterium tuberculosis. J Bacteriol. 2007;189(16):5903–5915.
  • Fullam E, Prokes I, Fütterer K, et al. Structural and functional analysis of the solute-binding protein UspC from Mycobacterium tuberculosis that is specific for amino sugars. Open Biol. 2016;6(6):1–11. pii:160105.
  • Schneider E. ABC transporters catalyzing carbohydrate uptake. Res Microbiol. 2001;152(3-4):303–310.
  • Wuttge S, Bommer M, Jäger F, et al. Determinants of substrate specificity and biochemical properties of the sn-glycerol-3-phosphate ATP binding cassette transporter (UgpB-AEC2) of Escherichia coli. Mol Microbiol. 2012;86(4):908–920.
  • Jiang D, Zhang Q, Zheng Q, et al. Structural analysis of Mycobacterium tuberculosis ATP-binding cassette transporter subunit UgpB reveals specificity for glycerophosphocholine. FEBS J. 2014;281(1):331–341.
  • Sutcliffe IC, Harrington DJ. Lipoproteins of Mycobacterium tuberculosis: an abundant and functionally diverse class of cell envelope components. FEMS Microbiol Rev. 2004;28(5):645–659.
  • McDonough JA, McCann JR, Tekippe EM, et al. Identification of functional Tat signal sequences in Mycobacterium tuberculosis proteins. J Bacteriol. 2008;190(19):6428–6438.
  • Borich SM, Murray A, Gormley E. Genomic arrangement of a putative operon involved in maltose transport in the Mycobacterium tuberculosis complex and Mycobacterium leprae. Microbios. 2000;102(401):7–15.
  • Kalscheuer R, Weinrick B, Veeraraghavan U, et al. Trehalose-recycling ABC transporter LpqY-SugA-SugB-SugC is essential for virulence of Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 2010;107(50):21761–21766.
  • Rengarajan J, Bloom BR, Rubin EJ. Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci USA. 2005;102(23):8327–8332.
  • Belisle JT, Vissa VD, Sievert T, et al. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science. 1997;276(5317):1420–1422.
  • Backus KM, Boshoff HI, Barry CS, et al. Uptake of unnatural trehalose analogs as a reporter for Mycobacterium tuberculosis. Nat Chem Biol. 2011;7(4):228–235.
  • Wolber JM, Urbanek BL, Meints LM, et al. The trehalose-specific transporter LpqY-SugABC is required for antimicrobial and anti-biofilm activity of trehalose analogues in Mycobacterium smegmatis. Carbohydr Res. 2017;450:60–66.
  • Yang Y, Kulka K, Montelaro RC, et al. A hydrolase of trehalose dimycolate induces nutrient influx and stress sensitivity to balance intracellular growth of Mycobacterium tuberculosis. Cell Host Microbe. 2014;15(2):153–163.
  • Cole ST, Eiglmeier K, Parkhill J, et al. Massive gene decay in the leprosy bacillus. Nature. 2001;409(6823):1007–1011.
  • Griffin JE, Gawronski JD, Dejesus MA, et al. High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog. 2011;7(9):e1002251.
  • Kim SY, Lee BS, Shin SJ, et al. Differentially expressed genes in Mycobacterium tuberculosis H37Rv under mild acidic and hypoxic conditions. J Med Microbiol. 2008;57(Pt 12):1473–1480.
  • Kim SY, Shin AR, Lee BS, et al. Characterization of immune responses to Mycobacterium tuberculosis Rv2041c protein. J Bacteriol Virol. 2009;39(3):183–193.
  • Kim SY, Shin AR, Kim HJ, et al. Identification of Rv2041c, a novel immunogenic antigen from Mycobacterium tuberculosis with serodiagnostic potential. Scand J Immunol. 2009;70(5):457–464.
  • Crosa JH, Walsh CT. Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev. 2002;66(2):223–249.
  • Krithika R, Marathe U, Saxena P, et al. A genetic locus required for iron acquisition in Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 2006;103(7):2069–2074.
  • Rodriguez GM, Voskuil MI, Gold B, et al. Ider, An essential gene in mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect Immun. 2002;70(7):3371–3381.
  • Farhana A, Kumar S, Rathore SS, et al. Mechanistic insights into a novel exporter-importer system of Mycobacterium tuberculosis unravel its role in trafficking of iron. PLoS One. 2008;3(5):e2087.
  • Wagner D, Sangari FJ, Parker A, et al. Fecb, a gene potentially involved in iron transport in Mycobacterium avium, is not induced within macrophages. FEMS Microbiol Lett. 2005;247(2):185–191.
  • Mattle D, Zeltina A, Woo JS, et al. Two stacked heme molecules in the binding pocket of the periplasmic heme-binding protein HmuT from Yersinia pestis. J Mol Biol. 2010;404(2):220–231.
  • Mitra A, Speer A, Lin K, et al. PPE surface proteins are required for heme utilization by Mycobacterium tuberculosis. MBio. 2017;8(1): pii:e01720-16.
  • Wooff E, Michell SL, Gordon SV, et al. Functional genomics reveals the sole sulphate transporter of the Mycobacterium tuberculosis complex and its relevance to the acquisition of sulphur in vivo. Mol Microbiol. 2002;43(3):653–663.
  • Williams SJ, Senaratne RH, Mougous JD, et al. 5'-adenosinephosphosulfate lies at a metabolic branch point in mycobacteria. J Biol Chem. 2002;277(36):32606–32615.
  • Senaratne RH, De Silva AD, Williams SJ, et al. 5'-Adenosinephosphosulphate reductase (CysH) protects Mycobacterium tuberculosis against free radicals during chronic infection phase in mice. Mol Microbiol. 2006;59(6):1744–1753.
  • Betts JC, Lukey PT, Robb LC, et al. Evaluation of a nutrient starvation model of Mycobacterium tuberculosis persistence by gene and protein expression profiling. Mol Microbiol. 2002;43(3):717–731.
  • Hampshire T, Soneji S, Bacon J, et al. Stationary phase gene expression of Mycobacterium tuberculosis following a progressive nutrient depletion: a model for persistent organisms? Tuberculosis (Edinburg). 2004;84(3–4):228–238.
  • Rustad TR, Harrell MI, Liao R, et al. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS One. 2008;3(1):e1502.
  • Boshoff HI, Myers TG, Copp BR, et al. The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J Biol Chem. 2004;279(38):40174–40184.
  • Criddle DN, Gillies S, Baumgartner-Wilson HK, et al. Menadione-induced reactive oxygen species generation via redox cycling promotes apoptosis of murine pancreatic acinar cells. J Biol Chem. 2006;281(52):40485–40492.
  • Camacho LR, Ensergueix D, Perez E, et al. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol. 1999;34(2):257–267.
  • Williams MJ, Kana BD, Mizrahi V. Functional analysis of molybdopterin biosynthesis in mycobacteria identifies a fused molybdopterin synthase in Mycobacterium tuberculosis. J Bacteriol. 2011;193(1):98–106.
  • Andersen AB, Ljungqvist L, Olsen M. Evidence that protein antigen b of Mycobacterium tuberculosis is involved in phosphate metabolism. J Gen Microbiol. 1990;136(3):477–480.
  • Espitia C, Elinos M, Hernández-Pando R, et al. Phosphate starvation enhances expression of the immunodominant 38-kilodalton protein antigen of Mycobacterium tuberculosis: demonstration by immunogold electron microscopy. Infect Immun. 1992;60(7):2998–3001.
  • Lefèvre P, Braibant M, de Wit L, et al. Three different putative phosphate transport receptors are encoded by the Mycobacterium tuberculosis genome and are present at the surface of Mycobacterium bovis BCG. J Bacteriol. 1997;179(9):2900–2906.
  • Peirs P, Lefèvre P, Boarbi S, et al. Mycobacterium tuberculosis with disruption in genes encoding the phosphate binding proteins PstS1 and PstS2 is deficient in phosphate uptake and demonstrates reduced in vivo virulence. Infect Immun. 2005;73(3):1898–1902.
  • Espitia C, Mancilla R. Identification, isolation and partial characterization of Mycobacterium tuberculosis glycoprotein antigens. Clin Exp Immunol. 1989;77(3):378–383.
  • Young DB, Garbe TR. Lipoprotein antigens of Mycobacterium tuberculosis. Res Microbiol. 1991;142(1):55–65.
  • Espitia C, Cervera I, González R, et al. A 38-kD Mycobacterium tuberculosis antigen associated with infection. Its isolation and serologic evaluation. Clin Exp Immunol. 1989;77(3):373–377.
  • Jung SB, Yang CS, Lee JS, et al. The mycobacterial 38-kilodalton glycolipoprotein antigen activates the mitogen-activated protein kinase pathway and release of proinflammatory cytokines through Toll-like receptors 2 and 4 in human monocytes. Infect Immun. 2006;74(5):2686–2696.
  • Clarke TE, Braun V, Winkelmann G, et al. X-ray crystallographic structures of the Escherichia coli periplasmic protein FhuD bound to hydroxamate-type siderophores and the antibiotic albomycin. J Biol Chem. 2002;277(16):13966–13972.
  • Novikova M, Metlitskaya A, Datsenko K, et al. The Escherichia coli Yej transporter is required for the uptake of translation inhibitor microcin C. J Bacteriol. 2007;189(22):8361–8365.
  • Rebuffat S. Microcins in action: amazing defence strategies of Enterobacteria. Biochem Soc Trans. 2012;40(6):1456–1462.
  • Mistry A, Warren MS, Cusick JK, et al. High-level pacidamycin resistance in Pseudomonas aeruginosa is mediated by an opp oligopeptide permease encoded by the opp-fabI operon. Antimicrob Agents Chemother. 2013;57(11):5565–5571.
  • Pletzer D, Braun Y, Dubiley S, et al. The Pseudomonas aeruginosa PA14 ABC transporter NppA1A2BCD is required for uptake of peptidyl nucleoside antibiotics. J Bacteriol. 2015;197(13):2217–2228.
  • Pletzer D, Lafon C, Braun Y, et al. High-throughput screening of dipeptide utilization mediated by the ABC transporter DppBCDF and its substrate-binding proteins DppA1-A5 in Pseudomonas aeruginosa. PLoS One. 2014;9(10):e111311.
  • Shiver AL, Osadnik H, Kritikos G, et al. A chemical-genomic screen of neglected antibiotics reveals illicit transport of kasugamycin and blasticidin S. PLoS Genet. 2016;12(6):e1006124.
  • Ilari A, Pescatori L, Di Santo R, et al. Salmonella enterica serovar typhimurium growth is inhibited by the concomitant binding of Zn(II) and a pyrrolyl-hydroxamate to ZnuA, the soluble component of the ZnuABC transporter. Biochim Biophys Acta. 2016;1860(3):534–541.
  • Tanghe A, Lefèvre P, Denis O, et al. Immunogenicity and protective efficacy of tuberculosis DNA vaccines encoding putative phosphate transport receptors. J Immunol. 1999;162(2):1113–1119.
  • Rosinha GM, Freitas DA, Miyoshi A, et al. Identification and characterization of a Brucella abortus ATP-binding cassette transporter homolog to Rhizobium meliloti ExsA and its role in virulence and protection in mice. Infect Immun. 2002;70:5036–5044.
  • Brown JS, Ogunniyi AD, Woodrow MC, et al. Immunization with components of two iron uptake ABC transporters protects mice against systemic Streptococcus pneumoniae infection. Infect Immun. 2001;69(11):6702–6706.
  • Yang HJ, Zhang JY, Wei C, et al. Immunisation with Iimmunodominant linear B cell epitopes vaccine of manganese transport protein C confers protection against Staphylococcus aureus infection. PLoS One. 2016;11(2):e0149638.
  • Begier E, Seiden DJ, Patton M, et al. SA4Ag, a 4-antigen Staphylococcus aureus vaccine, rapidly induces high levels of bacteria-killing antibodies. Vaccine. 2017;35(8):1132–1139.