Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Proteomic and Morphologic Evidence for Taurine-5-Bromosalicylaldehyde Schiff Base as an Efficient Anti-Mycobacterial Drug

  • Ding, Wenyong (Biochemistry and Molecular Biology Department, College of Basic Medical Sciences, Dalian Medical University) ;
  • Zhang, Houli (Institute of Pharmacology, Dalian Medical University) ;
  • Xu, Yuefei (Biochemistry and Molecular Biology Department, College of Basic Medical Sciences, Dalian Medical University) ;
  • Ma, Li (Department of Epidemiology, Dalian Medical University) ;
  • Zhang, Wenli (Biochemistry and Molecular Biology Department, College of Basic Medical Sciences, Dalian Medical University)
  • Received : 2019.01.10
  • Accepted : 2019.07.24
  • Published : 2019.08.28
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Abstract

Mycobacterium tuberculosis, a causative pathogen of tuberculosis (TB), still threatens human health worldwide. To find a novel drug to eradicate this pathogen, we tested taurine-5-bromosalicylaldehyde Schiff base (TBSSB) as an innovative anti-mycobacterial drug using Mycobacterium smegmatis as a surrogate model for M. tuberculosis. We investigated the antimicrobial activity of TBSSB against M. smegmatis by plotting growth curves, examined the effect of TBSSB on biofilm formation, observed morphological changes by scanning electron microscopy and transmission electron microscopy, and detected differentially expressed proteins using two-dimensional gel electrophoresis coupled with mass spectrometry. TBSSB inhibited mycobacterial growth and biofilm formation, altered cell ultrastructure and intracellular content, and inhibited cell division. Furthermore, M. smegmatis adapted itself to TBSSB inhibition by regulating the metabolic pathways and enzymatic activities of the identified proteins. NDMA-dependent methanol dehydrogenase, NAD(P)H nitroreductase, and amidohydrolase AmiB1 appear to be pivotal factors to regulate the M. smegmatis survival under TBSSB. Our dataset reinforced the idea that Schiff base-taurine compounds have the potential to be developed as novel anti-mycobacterial drugs.

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References

  1. Organization WH. 2018. GLOBAL TUBERCULOSIS REPORT 2018. http://www.who.int/tb/publications/global_report/en/.
  2. Rimbu C, Danac R, Pui A. 2014. Antibacterial activity of Pd(II) complexes with salicylaldehyde-amino acids Schiff bases ligands. Chem. Pharm. Bull. (Tokyo) 62: 12-15. https://doi.org/10.1248/cpb.c12-01087
  3. Chaudhary NK, Mishra P. 2017. Metal complexes of a novel schiff base based on penicillin: characterization, molecular modeling, and antibacterial activity study. Bioinorg. Chem. Appl. 2017: 6927675. https://doi.org/10.1155/2017/6927675
  4. Siddappa K, Mayana NS. 2014. Synthesis, spectroscopic characterization, and biological evaluation studies of 5-bromo-3-(((hydroxy-2-methylquinolin-7-yl)methylene)hydrazono) indolin-2-one and its metal (II) complexes. Bioinorg. Chem. Appl. 2014: 483282.
  5. Andiappan K, Sanmugam A, Deivanayagam E, Karuppasamy K, Kim HS, Vikraman D. 2018. In vitro cytotoxicity activity of novel Schiff base ligand-lanthanide complexes. Sci. Rep. 8(1): 3054. https://doi.org/10.1038/s41598-018-21366-1
  6. Zhang X, Bi C, Fan Y, Cui Q, Chen D, Xiao Y, et al. 2008. Induction of tumor cell apoptosis by taurine Schiff base copper complex is associated with the inhibition of proteasomal activity. Int. J. Mol. Med. 22: 677-682.
  7. Li L, Guo Q, Dong J, Xu T, Li J. 2013. DNA binding, DNA cleavage and BSA interaction of a mixed-ligand copper(II) complex with taurine Schiff base and 1,10-phenanthroline. J. Photochem. Photobiol. B. 125: 56-62. https://doi.org/10.1016/j.jphotobiol.2013.05.007
  8. Yuan R, Diao Y, Zhang W, Lin Y, Huang S, Zhang H, et al. 2014. In vitro activity of taurine-5-bromosalicylaldehyde Schiff base against planktonic and biofilm cultures of methicillinresistant Staphylococcus aureus. J. Microbiol. Biotechnol. 24: 1059-1064. https://doi.org/10.4014/jmb.1401.01037
  9. Zhang W, Jones VC, Scherman MS, Mahapatra S, Crick D, Bhamidi S, et al. 2008. Expression, essentiality, and a microtiter plate assay for mycobacterial GlmU, the bifunctional glucosamine-1-phosphate acetyltransferase and N-acetylglucosamine-1-phosphate uridyltransferase. Int. J. Biochem. Cell Biol. 40: 2560-2571. https://doi.org/10.1016/j.biocel.2008.05.003
  10. Chen Y, Xu Y, Yang S, Li S, Ding W, Zhang W. 2019. Deficiency of D-alanyl-D-alanine ligase A attenuated cell division and greatly altered the proteome of Mycobacterium smegmatis. MicrobiologyOpen 3: e819.
  11. Yang S, Xu Y, Wang Y, Ren F, Li S, Ding W, et al. 2018. The biological properties and potential interacting proteins of D-alanyl-D-alanine ligase A from Mycobacterium tuberculosis. Molecules 23: E324. https://doi.org/10.3390/molecules23020324
  12. Marland Z, Beddoe T, Zaker-Tabrizi L, Coppel RL, Crellin PK, Rossjohn J. 2005. Expression, purification, crystallization and preliminary X-ray diffraction analysis of an essential lipoprotein implicated in cell-wall biosynthesis in Mycobacteria. Acta crystallogr. Sec. F, Struct. Biol. Cryst. Commun. 61: 1081-1083. https://doi.org/10.1107/S1744309105037541
  13. Pan F, Jackson M, Ma Y, McNeil M. 2001. Cell wall core galactofuran synthesis is essential for growth of mycobacteria. J. Bacteriol. 183: 3991-3998. https://doi.org/10.1128/JB.183.13.3991-3998.2001
  14. Kieser KJ, Baranowski C, Chao MC, Long JE, Sassetti CM, Waldor MK, et al. 2015. Peptidoglycan synthesis in Mycobacterium tuberculosis is organized into networks with varying drug susceptibility. Proc. Nat. Acad. Sci. USA 112: 13087-13092. https://doi.org/10.1073/pnas.1514135112
  15. Rombouts Y, Brust B, Ojha AK, Maes E, Coddeville B, Elass-Rochard E, et al. 2012. Exposure of mycobacteria to cell wall-inhibitory drugs decreases production of arabinoglycerolipid related to Mycolyl-arabinogalactan-peptidoglycan metabolism. J. Biol. Chem. 287: 11060-11069. https://doi.org/10.1074/jbc.M111.327387
  16. Alderwick LJ, Harrison J, Lloyd GS, Birch HL. 2015. The mycobacterial cell wall--peptidoglycan and arabinogalactan. Cold Spring Harb. Perspect. Med. 5: a021113. https://doi.org/10.1101/cshperspect.a021113
  17. Jankute M, Cox JA, Harrison J, Besra GS. 2015. Assembly of the mycobacterial cell wall. Ann. Rev. Microbiol. 69: 405-423. https://doi.org/10.1146/annurev-micro-091014-104121
  18. Lewis K. 2000. Programmed death in bacteria. Microbiol. Mol. Biol. Rev. 64: 503-514. https://doi.org/10.1128/MMBR.64.3.503-514.2000
  19. Tanouchi Y, Lee AJ, Meredith H, You L. 2013. Programmed cell death in bacteria and implications for antibiotic therapy. Trends Microbiol. 21: 265-270. https://doi.org/10.1016/j.tim.2013.04.001
  20. Peters NT, Dinh T, Bernhardt TG. 2011. A fail-safe mechanism in the septal ring assembly pathway generated by the sequential recruitment of cell separation amidases and their activators. J. Bacteriol. 193: 4973-4983. https://doi.org/10.1128/JB.00316-11
  21. Yang DC, Tan K, Joachimiak A, Bernhardt TG. 2012. A conformational switch controls cell wall-remodelling enzymes required for bacterial cell division. Mol. Microbiol. 85: 768-781. https://doi.org/10.1111/j.1365-2958.2012.08138.x
  22. Chauviac F-X, Bommer M, Yan J, Parkin G, Daviter T, Lowden P, et al. 2012. Crystal structure of reduced MsAcg, a putative nitroreductase from mycobacterium smegmatisand a close homologue of mycobacterium tuberculosis Acg. J. Biol. Chem. 287: 44372-44383. https://doi.org/10.1074/jbc.M112.406264
  23. Pitsawong W, Haynes CA, Koder RL, Jr., Rodgers DW, Miller AF. 2017. Mechanism-informed refinement reveals altered substrate-binding mode for catalytically competent nitroreductase. Structure 25: 978-987. https://doi.org/10.1016/j.str.2017.05.002
  24. Cortial S, Chaignon P, Iorga BI, Aymerich S, Truan G, Gueguen-Chaignon V, et al. 2010. NADH oxidase activity of Bacillus subtilis nitroreductase NfrA1: insight into its biological role. FEBS Lett. 584: 3916-3922. https://doi.org/10.1016/j.febslet.2010.08.019
  25. Hektor HJ, Kloosterman H, Dijkhuizen L. 2002. Identification of a magnesium-dependent NAD(P)(H)-binding domain in the nicotinoprotein methanol dehydrogenase from Bacillus methanolicus. J. Biol. Chem. 277: 46966-46973. https://doi.org/10.1074/jbc.M207547200
  26. Liu H, Yang M, He ZG. 2016. Novel TetR family transcriptional factor regulates expression of multiple transport-related genes and affects rifampicin resistance in Mycobacterium smegmatis. Sci. Rep. 6: 27489. https://doi.org/10.1038/srep27489
  27. Titgemeyer F, Amon J, Parche S, Mahfoud M, Bail J, Schlicht M, et al. 2007. A genomic view of sugar transport in Mycobacterium smegmatis and Mycobacterium tuberculosis. J. Bacteriol. 189: 5903-5915. https://doi.org/10.1128/JB.00257-07
  28. Valente W, Pienaar E, Fast A, Fluitt A, Whitney S, Fenton R, et al. 2009. A Kinetic Study of In vitro lysis of mycobacterium smegmatis. Chem. Eng. Sci. 64: 1944-1952. https://doi.org/10.1016/j.ces.2008.12.015
  29. Agrawal P, Miryala S, Varshney U. 2015. Use of Mycobacterium smegmatis deficient in ADP-ribosyltransferase as surrogate for Mycobacterium tuberculosis in drug testing and mutation analysis. PLoS One 10: e0122076. https://doi.org/10.1371/journal.pone.0122076
  30. Namouchi A, Cimino M, Favre-Rochex S, Charles P, Gicquel B. 2017. Phenotypic and genomic comparison of Mycobacterium aurum and surrogate model species to Mycobacterium tuberculosis: implications for drug discovery. BMC Genomics 18(1): 530. https://doi.org/10.1186/s12864-017-3924-y
  31. Verma A, Sampla AK, Tyagi JS. 1999. Mycobacterium tuberculosis rrn promoters: differential usage and growth rate-dependent control. J. Bacteriol. 181: 4326-4333. https://doi.org/10.1128/JB.181.14.4326-4333.1999
  32. Manca C, Paul S, Barry CEr, Freedman VH, Kaplan G. 1999. Mycobacterium tuberculosis catalase and peroxidase activities and resistance to oxidative killing in human monocytes in vitro. Infect. Immun. 67: 74-79. https://doi.org/10.1128/IAI.67.1.74-79.1999

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