Proteomic profile of Mycobacterium tuberculosis after eupomatenoid-5 induction reveals potential drug targets

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References

• 1 WHO. Global tuberculosis report 2016. CDC 2016 (2016). www.who.int/tb/publications/global_report/en/.
  Google Scholar
• 2 Hassan HM, Guo HL, Yousef BA, Luyong Z, Zhenzhou J. Hepatotoxicity mechanisms of isoniazid: a mini-review. J. Appl. Toxicol. 35(12), 1427–1432 (2015).
  Medline CASGoogle Scholar
• 3 Hoagland DT, Liu J, Lee RB, Lee RE. New agents for the treatment of drug-resistant Mycobacterium tuberculosis. Adv. Drug Deliv. Rev. 102, 55–72 (2016).
  Medline CASGoogle Scholar
• 4 Kakkar AK, Dahiya N. Bedaquiline for the treatment of resistant tuberculosis: promises and pitfalls. Tuberculosis 94(4), 357–362 (2014).
  Medline CASGoogle Scholar
• 5 Gautam R, Saklani A, Jachak SM. Indian medicinal plants as a source of antimycobacterial agents. J. Ethnopharmacol. 110(2), 200–234 (2007).
  Medline CASGoogle Scholar
• 6 Bunalema L, Kirimuhuzya C, Tabuti JRS et al. The efficacy of the crude root bark extracts of Erythrina abyssinica on rifampicin resistant Mycobacterium tuberculosis. Afr. Health Sci. 11(4), 587–593 (2012).
  Google Scholar
• 7 Carpenter CD, O'Neill T, Picot N et al. Anti-mycobacterial natural products from the Canadian medicinal plant Juniperus communis. J. Ethnopharmacol. 143(2), 695–700 (2012).
  Medline CASGoogle Scholar
• 8 Diaz LE, Munoz DR, Prieto RE et al. Antioxidant, antitubercular and cytotoxic activities of Piper imperiale. Molecules 17(4), 4142–4157 (2012).
  Medline CASGoogle Scholar
• 9 Ymele-Leki P, Cao S, Sharp J et al. A high-throughput screen identifies a new natural product with broad-spectrum antibacterial activity. PLoS ONE 7(2), e31307 (2012).
  Medline CASGoogle Scholar
• 10 Jouda JB, Mawabo IK, Notedji A et al. Anti-mycobacterial activity of polyketides from Penicillium sp. endophyte isolated from Garcinia nobilis against Mycobacterium smegmatis. Int. J. Mycobacteriol. 5(2), 7–11 (2016).
  MedlineGoogle Scholar
• 11 Copp BR, Pearce AN. Natural product growth inhibitors of Mycobacterium tuberculosis. Nat. Prod. Rep. 24(2), 278–297 (2007).
  Medline CASGoogle Scholar
• 12 Gupta R, Thakur B, Singh P et al. Anti-tuberculosis activity of selected medicinal plants against multi-drug resistant Mycobacterium tuberculosis isolates. Indian J. Med. Res. 131, 809–813 (2010).
  MedlineGoogle Scholar
• 13 Zhao BQ, Peng S, He WJ, Liu YH, Wang JF, Zhou XJ. Antitubercular and cytotoxic tigliane-type diterpenoids from Croton tiglium. Bioorg. Med. Chem. Lett. 26(20), 4996–4999 (2016).
  Medline CASGoogle Scholar
• 14 Chinsembu KC. Tuberculosis and nature's pharmacy of putative anti-tuberculosis agents. Acta Trop. 153, 46–56 (2016).
  Medline CASGoogle Scholar
• 15 Bell C, Smith GT, Sweredoski MJ, Hess S. Characterization of the mycobacterium tuberculosis proteome by liquid chromatography mass spectrometry-based proteomics techniques: a comprehensive resource for tuberculosis research. J. Proteome Res. 11(1), 119–130 (2012).
  Medline CASGoogle Scholar
• 16 Li H, Doucet B, Flewelling AJ et al. Antimycobacterial natural products from Endophytes of the medicinal plant Aralia nudicaulis. Nat. Prod. Commun. 10(10), 1641–1642 (2015).
  MedlineGoogle Scholar
• 17 Pires CTA, Brenzan MA, de Lima Scodro RB et al. Anti-Mycobacterium tuberculosis activity and cytotoxicity of Calophyllum brasiliense Cambess (Clusiaceae). Mem. Inst. Oswaldo Cruz. 109(3), 324–329 (2014).
  MedlineGoogle Scholar
• 18 Scodro RBL, Pires CTA, Carrara VS et al. Anti-tuberculosis neolignans from Piper regnellii. Phytomedicine 20(7), 600–604 (2013). • Determined the anti-Mycobacterium tuberculosis (M. tb) activities of supercritical CO2 extracts, neolignans eupomatenoid-5.
  Medline CASGoogle Scholar
• 19 Garcia FP, Lazarin-Bidóia D, Ueda-Nakamura T, Silva SDO, Nakamura CV. Eupomatenoid-5 isolated from leaves of Piper regnellii induces apoptosis in Leishmania amazonensis. Evid. Based Complement. Alternat. Med. 2013, 940531 (2013).
  MedlineGoogle Scholar
• 20 Koroishi AM, Foss SR, Cortez DAG, Ueda-Nakamura T, Nakamura CV, Dias Filho BP. In vitro antifungal activity of extracts and neolignans from Piper regnellii against dermatophytes. J. Ethnopharmacol. 117(2), 270–277 (2008).
  Medline CASGoogle Scholar
• 21 Longato GB, Fiorito GF, Vendramini-Costa DB et al. Different cell death responses induced by eupomatenoid-5 in MCF-7 and 786–0 tumor cell lines. Toxicol. Vitr. 29(5), 1026–1033 (2015).
  Medline CASGoogle Scholar
• 22 Lopes MA, Ferracioli KRC, Siqueira VLD et al. In vitro interaction of eupomatenoid-5 from Piper solmsianum C. DC. var. solmsianum and anti-tuberculosis drugs. Int. J. Tuberc. Lung Dis. 18(12), 1513–1515 (2014). • Evaluated the in vitro interaction between eupomatenoid-5, extracted from Piper solmsianum C. DC. var. solmsianum, and first-line antituberculosis drugs against M. tb.
  Medline CASGoogle Scholar
• 23 Marçal FJB, Cortez DAG, Ueda-Nakamura T, Nakamura CV, Filho BPD. Activity of the extracts and neolignans from Piper regnellii against methicillin-resistant Staphylococcus aureus (MRSA). Molecules 15(4), 2060–2069 (2010).
  Medline CASGoogle Scholar
• 24 Pelizzaro-Rocha KJ, Veiga-Santos P, Lazarin-Bidóia D et al. Trypanocidal action of eupomatenoid-5 is related to mitochondrion dysfunction and oxidative damage in Trypanosoma cruzi. Microbes Infect. 13(12–13), 1018–1024 (2011).
  Medline CASGoogle Scholar
• 25 Luize PS, Ueda-Nakamura T, Filho BPD et al. Ultrastructural alterations induced by the neolignan dihydrobenzofuranic eupomatenoid-5 on epimastigote and amastigote forms of Trypanosoma cruzi. Parasitol. Res. 100(1), 31–37 (2006).
  MedlineGoogle Scholar
• 26 Vendrametto MC, Santos AO dos, Nakamura CV, Filho BPD, Cortez DAG, Ueda-Nakamura T. Evaluation of antileishmanial activity of eupomatenoid-5, a compound isolated from leaves of Piper regnellii var. pallescens. Parasitol. Int. 59(2), 154–158 (2010).
  Medline CASGoogle Scholar
• 27 Lazarin-Bidóia D, Desoti VC, Ueda-Nakamura T, Dias Filho BP, Nakamura CV, Silva SO. Further evidence of the trypanocidal action of eupomatenoid-5: confirmation of involvement of reactive oxygen species and mitochondria owing to a reduction in trypanothione reductase activity. Free Radic. Biol. Med. 60, 17–28 (2013).
  Medline CASGoogle Scholar
• 28 Hughes MA, Silva JC, Geromanos SJ, Townsend CA. Quantitative proteomic analysis of drug-induced changes in mycobacteria. J. Proteome Res. 5(1), 54–63 (2006).
  Medline CASGoogle Scholar
• 29 Sharma P, Kumar B, Singhal N et al. Streptomycin induced protein expression analysis in Mycobacterium tuberculosis by two-dimensional gel electrophoresis & mass spectrometry. Indian J. Med. Res. 132, 400–408 (2010). • Uses the 2D electrophoresis and MS/MS to evaluate drug action in M. tb.
  Medline CASGoogle Scholar
• 30 Sharma D, Kumar B, Lata M et al. Comparative proteomic analysis of aminoglycosides resistant and susceptible Mycobacterium tuberculosis clinical isolates for exploring potential drug targets. PLoS ONE 10(10), e0139414 (2015). • Analyzed the membranes and membrane-associated proteins of Amikacin- and Kanamycin-resistant M. tb by proteomic and bioinformatic approach.
  MedlineGoogle Scholar
• 31 Lata M, Sharma D, Deo N, Tiwari PK, Bisht D, Venkatesan K. Proteomic analysis of ofloxacin-mono resistant Mycobacterium tuberculosis isolates. J. Proteomics 127(Pt A), 114–121 (2015).
  Medline CASGoogle Scholar
• 32 Campanerut-Sá PA, Ghiraldi-Lopes LD, Meneguello JE et al. Proteomic and morphological changes produced by subinhibitory concentration of isoniazid in Mycobacterium tuberculosis. Future Microbiol. 11, 1123–1132 (2016). • Evaluates the proteomic and mophological changes in M. tb after isoniazid induction.
  CASGoogle Scholar
• 33 Sharma D, Bisht D. M. tuberculosis hypothetical proteins and proteins of unknown function: hope for exploring novel resistance mechanisms as well as future target of drug resistance. Front. Microbiol. 8, 465 (2017).
  MedlineGoogle Scholar
• 34 Palomino J, Martin A, Camacho M, Guerra H, Swings J, Portaels F. Resazurin microtiter assay plate: simple and inexpensive method for detection of drug resistance in Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 46(8), 2720–2722 (2002).
  Medline CASGoogle Scholar
• 35 de Steenwinkel JEM, de Knegt GJ, ten Kate MT et al. Time-kill kinetics of anti-tuberculosis drugs, and emergence of resistance, in relation to metabolic activity of Mycobacterium tuberculosis. J. Antimicrob. Chemother. 65(12), 2582–2589 (2010).
  Medline CASGoogle Scholar
• 36 Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).
  Medline CASGoogle Scholar
• 37 Neuhoff V, Arold N, Taube D, Ehrhardt W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using coomassie brilliant blue G-250 and R-250. Electrophoresis 9(6), 255–262 (1988).
  Medline CASGoogle Scholar
• 38 Shevchenko A, Wilm M, Vorm O, Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68(5), 850–858 (1996).
  Medline CASGoogle Scholar
• 39 Aragão AZB, Belloni M, Simabuco FM et al. Novel processed form of syndecan-1 shed from SCC-9 cells plays a role in cell migration. PLoS ONE 7(8), e43521 (2012).
  Medline CASGoogle Scholar
• 40 STRING. http://string.embl.de/.
  Google Scholar
• 41 Mawuenyega KG, Fosrt CV, Dobos KM et al. Mycobacterium tuberculosis functional network analysis by global subcellular protein profiling. Mol. Biol. Cell 16(1), 396–404 (2005).
  Medline CASGoogle Scholar
• 42 Tuberculist. http://genolist.pasteur.fr/Tuberculist.
  Google Scholar
• 43 Campos MP, Cechinel Filho V, Silva RZ, Yunes RA, Monache FD, Cruz AB. Antibacterial activity of extract, fractions and four compounds extracted from Piper solmsianum C. DC. VAR. solmsianum (Piperaceae). Z. Naturforsch. C. 62(3–4), 173–178 (2007).
  Medline CASGoogle Scholar
• 44 Demitto FdeO, Do Amaral RC, Maltempe FG et al. In vitro activity of rifampicin and verapamil combination in multidrug-resistant Mycobacterium tuberculosis. PLoS ONE 10(7), e0133343 (2015).
  MedlineGoogle Scholar
• 45 Pagliotto ADF, Caleffi-Ferracioli KR, Lopes MA et al. Anti-Mycobacterium tuberculosis activity of antituberculosis drugs and amoxicillin/clavulanate combination. J. Microbiol. Immunol. Infect. 49, 980–983 (2016).
  Medline CASGoogle Scholar
• 46 Caleffi-Ferracioli KR, Amaral RCR, Demitto FO et al. Morphological changes and differentially expressed efflux pump genes in Mycobacterium tuberculosis exposed to a rifampicin and verapamil combination. Tuberculosis 97, 65–72 (2016).
  Medline CASGoogle Scholar
• 47 Kang C, Abbott DW, Park ST, Dascher CC, Cantley LC, Husson RN. The Mycobacterium tuberculosis serine/treonine kinase PknA and PknB: substrate identification and regulation of cell shape regulation cell shape. Genes Dev. 19(14), 1692–1704 (2005).
  Medline CASGoogle Scholar
• 48 Nguyen L, Scherr N, Gatfield J, Walburger A, Pieters J, Thompson CJ. Antigen 84, an effector of pleiomorphism in Mycobactenum smegmatis. J. Bacteriol. 189(21), 7896–7910 (2007).
  Medline CASGoogle Scholar
• 49 Mukherjee P, Sureka K, Datta P et al. Novel role of Wag31 in protection of mycobacteria under oxidative stress. Mol. Microbiol. 73(1), 103–119 (2009).
  Medline CASGoogle Scholar
• 50 Cao W, Tang S, Yuan H, Wang H, Zhao X, Lu H. Mycobacterium tuberculosis antigen Wag31 induces expression of C-chemokine XCL2 in macrophages. Curr. Microbiol. 57(3), 189–194 (2008).
  Medline CASGoogle Scholar
• 51 Maurya VK, Singh K, Sinha S. Suppression of Eis and expression of Wag31 and GroES in Mycobacterium tuberculosis cytosol under anaerobic culture conditions. Indian J. Exp. Biol. 52(8), 773–780 (2014).
  MedlineGoogle Scholar
• 52 Shen H, Yang E, Wang F et al. Altered protein expression patterns of Mycobacterium tuberculosis induced by ATB107. J. Microbiol. 48(3), 337–346 (2010).
  Medline CASGoogle Scholar
• 53 Starck J, Kallenius G, Marklund BI, Andersson DI, Akerlund T. Comparative proteome analysis of Mycobacterium tuberculosis grown under aerobic and anaerobic conditions. Microbiology 150, 3821–3829 (2004).
  Medline CASGoogle Scholar
• 54 Oh TJ, Daniel J, Kim HJ, Sirakova TD, Kolattukudy PE. Identification and characterization of Rv3281 as a novel subunit of a biotin-dependent Acyl-CoA carboxylase in Mycobacterium tuberculosis H₃₇Rv. J. Biol. Chem. 281(7), 3899–3908 (2006).
  Medline CASGoogle Scholar
• 55 Gago G, Kurth D, Diacovich L, Tsai S, Gramajo H. Biochemical and structural characterization of an essential acyl coenzyme-A carboxylase from Mycobacterium tuberculosis. Society 188(2), 477–486 (2006).
  CASGoogle Scholar
• 56 Nataraj V, Varela C, Javid A, Singh A, Besra GS, Bhatt A. Mycolic acids: deciphering and targeting the Achilles’ heel of the tubercle bacillus. Mol. Microbiol. 98(1), 7–16 (2015).
  Medline CASGoogle Scholar
• 57 Nicholls C, Li H, Liu JP. GAPDH: a common enzyme with uncommon functions. Clin. Exp. Pharmacol. Physiol. 39(8), 674–679 (2012).
  Medline CASGoogle Scholar
• 58 Wolfson-Stofko B, Hadi T, Blanchard JS. Kinetic and mechanistic characterization of the glyceraldehyde 3-phosphate dehydrogenase from Mycobacterium tuberculosis. Arch. Biochem. Biophys. 540(1–2), 53–61 (2013).
  Medline CASGoogle Scholar
• 59 Singh A, Gopinath K, Sharma P et al. Comparative proteomic analysis of sequential isolates of Mycobacterium tuberculosis from a patient with pulmonary tuberculosis turning from drug sensitive to multidrug resistant. Indian J. Med. Res. 141(1), 27–45 (2015).
  Medline CASGoogle Scholar
• 60 Singh A, Kumar Gupta A, Gopinath K, Sharma P, Singh S. Evaluation of 5 novel protein biomarkers for the rapid diagnosis of pulmonary and extra-pulmonary tuberculosis : preliminary results. Sci. Rep. 7, 44121 (2017).
  Medline CASGoogle Scholar
• 61 Kumar B, Sharma D, Sharma P, Katoch VM, Venkatesan K, Bisht D. Proteomic analysis of Mycobacterium tuberculosis isolates resistant to Kanamycin and Amikacin. J. Proteomics 94, 68–77 (2013).
  Medline CASGoogle Scholar
• 62 Ferraris DM, Spallek R, Oehlmann W, Singh M, Rizzi M. Structures of citrate synthase and malate dehydrogenase of Mycobacterium tuberculosis. Proteins Struct. Funct. Bioinform. 83(2), 389–394 (2015).
  Medline CASGoogle Scholar
• 63 Lv Y, Kandale A, Tadrowski S et al. Crystal structure of Mycobacterium tuberculosis ketol-acid reductoisomerase at 1.00 Å resolution: a possible target for anti-tuberculosis drug discovery. FEBS J. 283(4), 1184–1196 (2016).
  Medline CASGoogle Scholar
• 64 Grandoni JA, Marta PT, Schloss JV. Inhibitors of branched-chain amino acid biosynthesis as potential antituberculosis agents. J. Antimicrob. Chemother. 42(4), 475–482 (1998).
  Medline CASGoogle Scholar
• 65 Sajid A, Arora G, Gupta M et al. Interaction of Mycobacterium tuberculosis elongation factor Tu with GTP is regulated by phosphorylation. J. Bacteriol. 193(19), 5347–5358 (2011).
  Medline CASGoogle Scholar
• 66 Tripathi D, Chandra H, Bhatnagar R et al. Poly-L-glutamate/glutamine synthesis in the cell wall of Mycobacterium bovis is regulated in response to nitrogen availability. BMC Microbiol. 13(1), 226 (2013).
  MedlineGoogle Scholar
• 67 Kumar A, Toledo JC, Patel RP, Lancaster JR, Steyn AJC. Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc. Natl Acad. Sci. USA 104(28), 11568–11573 (2007).
  Medline CASGoogle Scholar
• 68 Shiloh MU, Manzanillo P, Cox JS. Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe 3(5), 323–330 (2008).
  Medline CASGoogle Scholar
• 69 Voskuil MI, Schnappinger D, Visconti KC et al. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J. Exp. Med. 198(5), 705–713 (2003).
  Medline CASGoogle Scholar
• 70 Hozumi H, Tsujimura K, Yamamura Y et al. Immunogenicity of dormancy-related antigens in individuals infected with Mycobacterium tuberculosis in Japan. Int. J. Tuberc. Lung Dis. 17(6), 818–824 (2013).
  Medline CASGoogle Scholar
• 71 Schertzer JW, Whiteley M. Bacterial outer membrane vesicles in trafficking, communication and the host-pathogen interaction. J. Mol. Microbiol. Biotechnol. 23(1–2), 118–130 (2013).
  Medline CASGoogle Scholar
• 72 Prados-Rosales R, Baena A, Martinez LR et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J. Clin. Invest. 121(4), 1471–1483 (2011).
  MedlineGoogle Scholar
• 73 Lopes RL, Borges TJ, Zanin RF, Bonorino C. IL-10 is required for polarization of macrophages to M2-like phenotype by mycobacterial DnaK (heat shock protein 70). Cytokine 85, 123–129 (2016).
  Medline CASGoogle Scholar
• 74 Lopes RL, Borges TJ, Araújo JF et al. Extracellular mycobacterial DnaK polarizes macrophages to the M2-like phenotype. PLoS ONE 9(11), e113441 (2014).
  MedlineGoogle Scholar
• 75 Sharma P, Kumar B, Gupta Y et al. Proteomic analysis of streptomycin resistant and sensitive clinical isolates of Mycobacterium tuberculosis. Proteome Sci. 8(1), 59 (2010).
  Medline CASGoogle Scholar
• 76 Sharma P, Kumar B, Singhal N. Streptomycin induced protein expression analysis in Mycobacterium tuberculosis by two-dimensional gel electrophoresis & mass spectrometry. Indian J. Med. Res. 132, 400–408 (2010).
  Medline CASGoogle Scholar
• 77 Puniya BL, Kulshreshtha D, Verma SP, Kumar S, Ramachandran S. Integrated gene co-expression network analysis in the growth phase of Mycobacterium tuberculosis reveals new potential drug targets. Mol. Biosyst. 9(11), 2798–2815 (2013).
  Medline CASGoogle Scholar
• 78 He X, Zhang J. Why do hubs tend to be essential in protein networks? PLoS Genet. 2(6), e88 (2006).
  MedlineGoogle Scholar
• 79 Burton RL, Chen S, Xu XL, Grant GA. A novel mechanism for substrate inhibition in Mycobacterium. J. Biol Chem. 282(43), 31517–31524 (2007).
  Medline CASGoogle Scholar
• 80 Grant GA. Contrasting catalytic and allosteric mechanisms for phosphoglycerate dehydrogenases. Arch. Biochem. Biophys. 519(2), 175–185 (2012).
  Medline CASGoogle Scholar
• 81 Dey S, Burton RL, Grant GA, Sacchettini JC. Structural analysis of substrate and effector binding in mycobacterium tuberculosis d-3-phosphoglycerate dehydrogenase. Biochemistry 47(32), 8271–8282 (2009).
  Google Scholar
• 82 Dey S, Grant GA, Sacchettini JC. Crystal structure of Mycobacterium tuberculosis D-3-phosphoglycerate dehydrogenase. J. Biol. Chem. 280(15), 14892–14899 (2005).
  Medline CASGoogle Scholar
• 83 Babu R, Krishnamoorthy P, Gayathri G. Identification of drug target site on citrate synthase of food pathogen – Campylobacter jejuni. Res. J. Pharm. Biol. Chem. Sci. 4(1), 618–623 (2013).
  Google Scholar
• 84 Tilton F, Priya L, Nair A. In silico metabolic pathway analysis for potential drug target in Campylobacter jejuni. Int. J. Healthcare Pharm. Res. 3(3), 29–32 (2014).
  Google Scholar
• 85 Timson DJ. Metabolic enzymes of helminth parasites: potential as drug targets. Curr. Protein Pept. Sci. 17(3), 280–295 (2016).
  Medline CASGoogle Scholar
• 86 Mir SA, Sharma S. Immunotherapeutic potential of N-formylated peptides of ESAT-6 and glutamine synthetase in experimental tuberculosis. Int. Immunopharmacol. 18(2), 298–303 (2014).
  Medline CASGoogle Scholar
• 87 Lu P, Lill H, Bald D. ATP synthase in mycobacteria: special features and implications for a function as drug target. Biochim. Biophys. Acta 1837(7), 1208–1218 (2014).
  Medline CASGoogle Scholar