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Research Articles

Lysine succinylation of Mycobacterium tuberculosis isocitrate lyase (ICL) fine-tunes the microbial resistance to antibiotics

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Pages 1030-1041 | Received 11 Jan 2016, Accepted 18 Mar 2016, Published online: 19 Apr 2016

References

  • Adams, P. D. , Grosse-Kunstleve, R. W. , Hung, L. W. , Ioerger, T. R. , McCoy, A. J. , Moriarty, N. W. , … Terwilliger, T. C. (2002). PHENIX: Building new software for automated crystallographic structure determination. Acta Crystallographica Section D Biological Crystallography , 58 , 1948–1954. doi:S0907444902016657
  • Baek, S. H. , Li, A. H. , & Sassetti, C. M. (2011). Metabolic regulation of mycobacterial growth and antibiotic sensitivity. PLoS Biology , 9 , e1001065. doi:10.1371/journal.pbio.1001065PBIOLOGY-D-10-01281
  • Boshoff, H. I. , & Barry, C. E. (2005). Tuberculosis – Metabolism and respiration in the absence of growth. Nature Reviews Microbiology , 3 , 70–80. doi:10.1038/nrmicro1065
  • Boshoff, H. I. , Myers, T. G. , Copp, B. R. , McNeil, M. R. , Wilson, M. A. , & Barry, C. E. (2004). The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: Novel insights into drug mechanisms of action. Journal of Biological Chemistry , 279 , 40174–40184. doi:10.1074/jbc.M406796200M406796200
  • Canova, M. J. , Baronian, G. , Brelle, S. , Cohen-Gonsaud, M. , Bischoff, M. , & Molle, V. (2014). A novel mode of regulation of the Staphylococcus aureus Vancomycin-resistance-associated response regulator VraR mediated by Stk1 protein phosphorylation. Biochemical and Biophysical Research Communications , 447 , 165–171. doi:10.1016/j.bbrc.2014.03.128S0006-291X(14)00588-9
  • Emsley, P. , & Cowtan, K. (2004). Coot: Model-building tools for molecular graphics. Acta Crystallographica Section D Biological Crystallography , 60 , 2126–2132. doi:10.1107/S0907444904019158
  • Engström, A. , Morcillo, N. , Imperiale, B. , Hoffner, S. E. , & Juréen, P. (2012). Detection of first- and second-line drug resistance in Mycobacterium tuberculosis clinical isolates by pyrosequencing. Journal of Clinical Microbiology , 50 , 2026–2033. doi:10.1128/JCM.06664-11JCM.06664-11
  • Fenhalls, G. , Stevens, L. , Moses, L. , Bezuidenhout, J. , Betts, J. C. , Helden, P. , … Duncan, K. (2002). In situ detection of Mycobacterium tuberculosis transcripts in human lung granulomas reveals differential gene expression in necrotic lesions. Infection and Immunity , 70 , 6330–6338.10.1128/IAI.70.11.6330-6338.2002
  • Graham, J. E. , & Clark-Curtiss, J. E. (1999). Identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS). Proceedings of the National Academy of Sciences , 96 , 11554–11559.10.1073/pnas.96.20.11554
  • Honer Zu Bentrup, K Miczak, A. , Swenson, D. L Russell, D. G. (1999). Characterization of activity and expression of isocitrate lyase in Mycobacterium avium and Mycobacterium tuberculosis . Journal of Bacteriology , 181 , 7161–7167.
  • Li, J. M. , Li, N. , Zhu, D. Y. , Wan, L. G. , He, Y. L. , & Yang, C. (2008). Isocitrate lyase from Mycobacterium tuberculosis promotes survival of Mycobacterium smegmatis within macrophage by suppressing cell apoptosis. Chinese Medical Journal (English) , 121 , 1114–1119.
  • McCoy, A. J. , Grosse-Kunstleve, R. W. , Adams, P. D. , Winn, M. D. , Storoni, L. C. , & Read, R. J. (2007). Phaser crystallographic software. Journal of Applied Crystallography , 40 , 658–674. doi:10.1107/S0021889807021206
  • McKinney, J. D. , zu Bentrup, K. , Muñoz-Elías, E. J. , Miczak, A. , Chen, B. , Chan, W. T. , … Russell, D. G. (2000). Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature , 406 , 735–738. doi:10.1038/35021074
  • Muñoz-Elías, E. J. , & McKinney, J. D. (2005). Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nature Medicine , 11 , 638–644. doi:10.1038/nm1252
  • Nandakumar, M. , Nathan, C. , & Rhee, K. Y. (2014). Isocitrate lyase mediates broad antibiotic tolerance in Mycobacterium tuberculosis . Nature Communications , 5 , 4306. doi:10.1038/ncomms5306
  • Otwinowski, Z. , Minor, W. , & W Jr, C. C. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol , 276 , 307–326. doi:10.1016/S0076-6879(97)76066-X
  • Pandey, A. K. , Raman, S. , Proff, R. , Joshi, S. , Kang, C. M. , Rubin, E. J. , … Sassetti, C. M. (2009). Nitrile-inducible gene expression in mycobacteria. Tuberculosis , 89 , 12–16. doi:10.1016/j.tube.2008.07.007S1472-9792(08)00073-5
  • Parrish, N. M. , Dick, J. D. , & Bishai, W. R. (1998). Mechanisms of latency in Mycobacterium tuberculosis . Trends in Microbiology , 6 , 107–112. doi:S0966-842X(98)01216-5
  • Reyrat, J. M. , & Kahn, D. (2001). Mycobacterium smegmatis: An absurd model for tuberculosis? Trends in Microbiology , 9 , 472–473. doi:S0966-842X(01)02168-0
  • Schnappinger, D. , Ehrt, S. , Voskuil, M. I. , Liu, Y. , Mangan, J. A. , Monahan, I. M. , … Schoolnik, G. K. (2003). Transcriptional adaptation of Mycobacterium tuberculosis within macrophages. The Journal of Experimental Medicine , 198 , 693–704. doi:10.1084/jem.20030846
  • Sharma, V. , Sharma, S. , zu Bentrup, K. , McKinney, J. D. , Russell, D. G. , Jacobs, W. R., Jr ., & Sacchettini, J. C. (2000). Structure of isocitrate lyase, a persistence factor of Mycobacterium tuberculosis . Nature Structural Biology , 7 , 663–668. doi:10.1038/77964
  • Shukla, H. , Kumar, V. , Singh, A. K. , Singh, N. , Kashif, M. , Siddiqi, M. I. , … Sohail Akhtar, M. (2015). Insight into the structural flexibility and function of Mycobacterium tuberculosis isocitrate lyase. Biochimie , 110 , 73–80. doi:10.1016/j.biochi.2014.12.016S0300-9084(14)00400-3
  • Smith, C. V. , Sharma, V. , & Sacchettini, J. C. (2004). TB drug discovery: Addressing issues of persistence and resistance. Tuberculosis , 84 , 45–55. doi:S1472979203000878
  • Srivastava, V. , Jain, A. , Srivastava, B. S. , & Srivastava, R. (2008). Selection of genes of Mycobacterium tuberculosis upregulated during residence in lungs of infected mice. Tuberculosis , 88 , 171–177. doi:S1472-9792(07)00130-8 10.1016/j.tube.2007.10.002
  • Sun, F. , Ding, Y. , Ji, Q. , Liang, Z. , Deng, X. , Wong, C. C. , … He, C. (2012). Protein cysteine phosphorylation of SarA/MgrA family transcriptional regulators mediates bacterial virulence and antibiotic resistance. Proceedings of the National Academy of Sciences , 109 , 15461–15466. doi:10.1073/pnas.1205952109
  • Timm, J. , Post, F. A. , Bekker, L. G. , Walther, G. B. , Wainwright, H. C. , Manganelli, R. , … McKinney, J. D. (2003). Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronically infected mice and tuberculosis patients. Proceedings of the National Academy of Sciences , 100 , 14321–14326. doi:10.1073/pnas.2436197100
  • Walsh, C. T. , Garneau-Tsodikova, S. , & Gatto, G. J., Jr (2005). Protein posttranslational modifications: The chemistry of proteome diversifications. Angewandte Chemie International Edition , 44 , 7342–7372. doi:10.1002/anie.200501023
  • Wheeler, P. R. , & Ratledge, C. (1988). Use of carbon sources for lipid biosynthesis in Mycobacterium leprae: A comparison with other pathogenic mycobacteria. Journal of general microbiology , 134 , 2111–2121.
  • Witze, E. S. , Old, W. M. , Resing, K. A. , & Ahn, N. G. (2007). Mapping protein post-translational modifications with mass spectrometry. Nature Methods , 4 , 798–806. doi:10.1038/nmeth1100
  • Xie, L. , Liu, W. , Li, Q. , Chen, S. , Xu, M. , Huang, Q. , … Xie, J. (2015). First succinyl-proteome profiling of extensively drug-resistant Mycobacterium tuberculosis revealed involvement of succinylation in cellular physiology. Journal of Proteome Research , 14 , 107–119. doi:10.1021/pr500859a
  • Xie, L. , Wang, X. , Zeng, J. , Zhou, M. , Duan, X. , Li, Q. , … Xie, J. (2015). Proteome-wide lysine acetylation profiling of the human pathogen Mycobacterium tuberculosis. The International Journal of Biochemistry & Cell Biology , 59 , 193–202. doi:10.1016/j.biocel.2014.11.010S1357-2725(14)00375-6
  • Yang, M. , Wang, Y. , Chen, Y. , Cheng, Z. , Gu, J. , Deng, J. , & Bi, Lijun (2015). Succinylome analysis reveals the involvement of lysine succinylation in metabolism in pathogenic Mycobacterium tuberculosis . Molecular & Cellular Proteomics , 14 , 796–811. doi:10.1074/mcp.M114.045922
  • Zhang, Z. , Tan, M. , Xie, Z. , Dai, L. , Chen, Y. , & Zhao, Y. (2011). Identification of lysine succinylation as a new post-translational modification. Nature Chemical Biology , 7 , 58–63. doi:10.1038/nchembio.495
  • Zhang, H. , Li, D. , Zhao, L. , Fleming, J. , Lin, N. , Wang, T. , … Bi, L. (2013). Genome sequencing of 161 Mycobacterium tuberculosis isolates from China identifies genes and intergenic regions associated with drug resistance. Nature Genetics , 45 , 1255–1260. doi:10.1038/ng.2735
  • Zumla, A. , George, A. , Sharma, V. , Herbert, R. H. N. , Oxley, A. , & Oliver, M. (2015). The WHO 2014 Global tuberculosis report – Further to go. The Lancet Global Health , 3 , e10–e12. doi:10.1016/s2214-109x(14)70361-4

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