Molecular investigation against the resistant mechanism of PncA mutated pyrazinamide resistance and insight into the role of pH environment for pyrazinamide activation

References

• African, E., & Councils, B. M. R. (1974). Controlled clinical trial of four short-course (6-month) regimens of chemotherapy for treatment of pulmonary tuberculosis: Third report. The Lancet, 304(7875), 237–240.
   Google Scholar
• Aggarwal, M., Singh, A., Grover, S., Pandey, B., Kumari, A., & Grover, A. (2018). Role of pncA gene mutations W68R and W68G in pyrazinamide resistance. Journal of Cellular Biochemistry, 119(3), 2567–2578. doi: 10.1002/jcb.26420
   PubMed Web of Science ®Google Scholar
• Ahmad, S., & Mokaddas, E. (2009). Recent advances in the diagnosis and treatment of multidrug-resistant tuberculosis. Respiratory Medicine, 103(12), 1777–1790. doi: 10.1016/j.rmed.2009.07.010
   PubMed Web of Science ®Google Scholar
• Amadei, A., Linssen, A. B., & Berendsen, H. J. (1993). Essential dynamics of proteins. Proteins: Structure, Function, & Genetics, 17(4), 412–425. doi: 10.1002/prot.340170408
   PubMed Web of Science ®Google Scholar
• Amadei, A., Linssen, A. B. M., De Groot, B. L., Van Aalten, D. M. F., & Berendsen, H. J. C. (1996). An efficient method for sampling the essential subspace of proteins. Journal of Biomolecular Structure & Dynamics, 13(4), 615–625. doi: 10.1080/07391102.1996.10508874
   PubMed Web of Science ®Google Scholar
• Asthana, S., Shukla, S., Ruggerone, P., & Vargiu, A. V. (2014). Molecular mechanism of viral resistance to a potent non-nucleoside inhibitor unveiled by molecular simulations. Biochemistry, 53(44), 6941–6953. doi: 10.1021/bi500490z
   PubMed Web of Science ®Google Scholar
• Chan, R. C. Y., Hui, M., Chan, E. W. C., Au, T. K., Chin, M. L., Yip, C. K., … Cheng, A. F. B. (2007). Genetic and phenotypic characterization of drug-resistant Mycobacterium tuberculosis isolates in Hong Kong. Journal of Antimicrobial Chemotherapy, 59(5), 866–873. doi: 10.1093/jac/dkm054
   PubMed Web of Science ®Google Scholar
• Christie, D., & Tansey, E. (2005). Short-course chemotherapy for tuberculosis. Wellcome Witnesses to Twentieth Century Medicine (vol. 24). London, UK: Wellcome Trust Centre for the History of Medicine at UCL.
   Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅ log (N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. doi: 10.1063/1.464397
   Web of Science ®Google Scholar
• De Lano, W. L. (2002). Pymol: An open-source molecular graphics tool. CCP4 Newsletter on protein crystallography, 40(1), 82-92..
   Google Scholar
• Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. G. (1995). A smooth particle mesh Ewald method. The Journal of Chemical Physics, 103(19), 8577–8593. doi: 10.1063/1.470117
   Web of Science ®Google Scholar
• Frauenfelder, H., Sligar, S. G., & Wolynes, P. G. (1991). The energy landscapes and motions of proteins. Science (New York, NY), 254(5038), 1598–1603. doi: 10.1126/science.1749933
   Google Scholar
• Goodsell, D. S., Morris, G. M., & Olson, A. J. (1996). Automated docking of flexible ligands: Applications of AutoDock. Journal of Molecular Recognition, 9(1), 1–5. doi: 10.1002/(SICI)1099-1352(199601)9:1<1::AID-JMR241>3.0.CO;2-6
   PubMed Web of Science ®Google Scholar
• Gordon, J. C., Myers, J. B., Folta, T., Shoja, V., Heath, L. S., & Onufriev, A. (2005). H++: A server for estimating p K as and adding missing hydrogens to macromolecules. Nucleic Acids Research, 33(Web Server), W368–W371. doi: 10.1093/nar/gki464
   PubMed Web of Science ®Google Scholar
• Hanwell, M. D., Curtis, D. E., Lonie, D. C., Vandermeersch, T., Zurek, E., & Hutchison, G. R. (2012). Avogadro: An advanced semantic chemical editor, visualization, and analysis platform. Journal of Cheminformatics, 4(1), 17. doi: 10.1186/1758-2946-4-17
   PubMed Web of Science ®Google Scholar
• Heifets, L., & Lindholm-Levy, P. (1992). Pyrazinamide sterilizing activity in vitro against semidormant Mycobacterium tuberculosis bacterial populations. American Review of Respiratory Disease, 145(5), 1223–1225. doi: 10.1164/ajrccm/145.5.1223
   PubMedGoogle Scholar
• Hess, B., Bekker, H., Berendsen, H. J., & Fraaije, J. G. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. doi: 10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.3.CO;2-L
   Web of Science ®Google Scholar
• Hess, B., Kutzner, C., Van Der Spoel, D., & Lindahl, E. (2008). GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory & Computation, 4(3), 435–447. doi: 10.1021/ct700301q
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. doi: 10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Jagadeb, M., Rath, S. N., & Sonawane, A. (2018). Computational discovery of potent drugs to improve the treatment of pyrazinamide resistant Mycobacterium tuberculosis mutants. Journal of Cellular Biochemistry, 119(9), 7328–7338. doi: 10.1002/jcb.27033
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79(2), 926–935. doi: 10.1063/1.445869
   Web of Science ®Google Scholar
• Karmakar, M., Globan, M., Fyfe, J. A. M., Stinear, T. P., Johnson, P. D. R., Holmes, N. E., … Ascher, D. B. (2018). Analysis of a novel pncA mutation for susceptibility to pyrazinamide therapy. American Journal of Respiratory & Critical Care Medicine, 198(4), 541–544. doi: 10.1164/rccm.201712-2572LE
   PubMed Web of Science ®Google Scholar
• Kempker, R. R., Heinrichs, M. T., Nikolaishvili, K., Sabulua, I., Bablishvili, N., Gogishvili, S., … Vashakidze, S. (2017). Lung tissue concentrations of pyrazinamide among patients with drug-resistant pulmonary tuberculosis. Antimicrobial Agents & Chemotherapy, 61(6), e00226–17. doi: 10.1128/AAC.00226-17
   PubMed Web of Science ®Google Scholar
• Kumar, A., Srivastava, G., Srivastava, S., Verma, S., Negi, A. S., & Sharma, A. (2017). Investigation of naphthofuran moiety as potential dual inhibitor against BACE-1 and GSK-3β: Molecular dynamics simulations, binding energy, and network analysis to identify first-in-class dual inhibitors against Alzheimer’s disease. Journal of Molecular Modeling, 23(8), 239. doi: 10.1007/s00894-017-3396-7
   PubMed Web of Science ®Google Scholar
• Kumari, R., Kumar, R., & Lynn, A, Open Source Drug Discovery Consortium, & Lynn, A. (2014). g_mmpbsa A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information & Modeling, 54(7), 1951–1962. doi: 10.1021/ci500020m
   PubMed Web of Science ®Google Scholar
• Kumari, R., & Lynn, A. (2011). Application of MM/PBSA in the prediction of relative binding free energy: Re-scoring of docking hit-list. Journal of Natural Science, Biology & Medicine, 2(3), 92–92.
   Google Scholar
• Lee, K. W., Lee, J. M., & Jung, K. S. (2001). Characterization of pncA mutations of pyrazinamide-resistant Mycobacterium tuberculosis in Korea. Journal of Korean Medical Science, 16(5), 537. doi: 10.3346/jkms.2001.16.5.537
   PubMed Web of Science ®Google Scholar
• Leung, C. C., Rieder, H. L., Lange, C., & Yew, W. W. (2011). Treatment of latent infection with Mycobacterium tuberculosis: Update 2010.
   Google Scholar
• Lindorff‐Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J. L., Dror, R. O., … Shaw, D. E. (2010). Improved side‐chain torsion potentials for the Amber ff99SB protein force field. Proteins: Structure, Function, & Bioinformatics, 78(8), 1950–1958. doi: 10.1002/prot.22711
   PubMed Web of Science ®Google Scholar
• Louw, G. E., Warren, R. M., Donald, P. R., Murray, M. B., Bosman, M., Van Helden, P. D., … Victor, T. C. (2006). Frequency and implications of pyrazinamide resistance in managing previously treated tuberculosis patients. The International Journal of Tuberculosis & Lung Disease, 10(7), 802–807.
   PubMed Web of Science ®Google Scholar
• Malik, S. I., Ali, S., Masood, N., Nadeem, T., Khan, A. S., & Afzal, M. T. (2019). Pyrazinamide resistance and mutations in pncA among isolates of Mycobacterium tuberculosis from Khyber Pakhtunkhwa, Pakistan. BMC Infectious Diseases, 19(1), 116. doi: 10.1186/s12879-019-3764-2
   PubMedGoogle Scholar
• Marttila, H. J., Marjamäki, M., Vyshnevskaya, E., Vyshnevskiy, B. I., Otten, T. F., Vasilyef, A. V., & Viljanen, M. K. (1999). pncA mutations in pyrazinamide-resistant Mycobacterium tuberculosis isolates from Northwestern Russia. Antimicrobial Agents & Chemotherapy, 43(7), 1764–1766. doi: 10.1128/AAC.43.7.1764
   PubMed Web of Science ®Google Scholar
• Morlock, G. P., Plikaytis, B. B., & Crawford, J. T. (2000). Characterization of spontaneous, in vitro-selected, rifampin-resistant mutants of Mycobacterium tuberculosis strain H37Rv. Antimicrobial Agents & Chemotherapy, 44(12), 3298–3301. doi: 10.1128/AAC.44.12.3298-3301.2000
   PubMed Web of Science ®Google Scholar
• Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., & Olson, A. J. (1998). Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. Journal of Computational Chemistry, 19(14), 1639–1662. doi: 10.1002/(SICI)1096-987X(19981115)19:14<1639::AID-JCC10>3.0.CO;2-BAQ5
   Web of Science ®Google Scholar
• Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. doi: 10.1002/jcc.21256
   PubMed Web of Science ®Google Scholar
• Pazhang, M., Mardi, N., Mehrnejad, F., & Chaparzadeh, N. (2018). The combinatorial effects of osmolytes and alcohols on the stability of pyrazinamidase: Methanol affects the enzyme stability through hydrophobic interactions and hydrogen bonds. International Journal of Biological Macromolecules, 108, 1339–1347. doi: 10.1016/j.ijbiomac.2017.11.039
   PubMed Web of Science ®Google Scholar
• Peterson, N. D., Rosen, B. C., Dillon, N. A., & Baughn, A. D. (2015). Uncoupling environmental pH and intrabacterial acidification from pyrazinamide susceptibility in Mycobacterium tuberculosis. Antimicrobial Agents & Chemotherapy, 59(12), 7320–7326. doi: 10.1128/AAC.00967-15
   PubMed Web of Science ®Google Scholar
• Petrella, S., Gelus-Ziental, N., Maudry, A., Laurans, C., Boudjelloul, R., & Sougakoff, W. (2011). Crystal structure of the pyrazinamidase of Mycobacterium tuberculosis: Insights into natural and acquired resistance to pyrazinamide. PLoS One, 6(1), e15785. doi: 10.1371/journal.pone.0015785
   PubMed Web of Science ®Google Scholar
• Rajendran, V., & Sethumadhavan, R. (2014). Drug resistance mechanism of PncA in Mycobacterium tuberculosis. Journal of Biomolecular Structure & Dynamics, 32(2), 209–221. doi: 10.1080/07391102.2012.759885
   PubMed Web of Science ®Google Scholar
• Salfinger, M., & Heifets, L. B. (1988). Determination of pyrazinamide MICs for Mycobacterium tuberculosis at different pHs by the radiometric method. Antimicrobial Agents & Chemotherapy, 32(7), 1002–1004. doi: 10.1128/AAC.32.7.1002
   PubMed Web of Science ®Google Scholar
• Sayahi, H., Pugliese, K. M., Zimhony, O., Jacobs, W. R., Jr, Shekhtman, A., & Welch, J. T. (2012). Analogs of the antituberculous agent pyrazinamide are competitive inhibitors of NADPH binding to M. tuberculosis fatty acid synthase I. Chemistry & Biodiversity, 9(11), 2582–2596. doi: 10.1002/cbdv.201200291
   PubMed Web of Science ®Google Scholar
• Scorpio, A., & Zhang, Y. (1996). Mutations in pncA, a gene encoding pyrazinamidase/nicotinamidase, cause resistance to the antituberculous drug pyrazinamide in tubercle bacillus. Nature Medicine, 2(6), 662. doi: 10.1038/nm0696-662
   PubMed Web of Science ®Google Scholar
• Shi, W., Chen, J., Feng, J., Cui, P., Zhang, S., Weng, X., … Zhang, Y. (2014). Aspartate decarboxylase (PanD) as a new target of pyrazinamide in Mycobacterium tuberculosis. Emerging Microbes & Infections, 3(1), 1–8. doi: 10.1038/emi.2014.61
   PubMed Web of Science ®Google Scholar
• Singh, B., Bulusu, G., & Mitra, A. (2015). Understanding the thermostability and activity of Bacillus subtilis lipase mutants: Insights from molecular dynamics simulations. The Journal of Physical Chemistry B, 119(2), 392–409. doi: 10.1021/jp5079554
   PubMed Web of Science ®Google Scholar
• da Silva, A. W. S., & Vranken, W. F. (2012). ACPYPE—Antechamber python parser interface. BMC Research Notes, 5(1), 367. doi: 10.1186/1756-0500-5-367
   PubMedGoogle Scholar
• Sreevatsan, S., Pan, X., Zhang, Y., Kreiswirth, B. N., & Musser, J. M. (1997). Mutations associated with pyrazinamide resistance in pncA of Mycobacterium tuberculosis complex organisms. Antimicrobial Agents & Chemotherapy, 41(3), 636–640. doi: 10.1128/AAC.41.3.636
   PubMed Web of Science ®Google Scholar
• Srivastava, S., Pasipanodya, J. G., & Gumbo, T. (2017). pH conditions under which pyrazinamide works in humans. Antimicrobial Agents & Chemotherapy, 61(9), e00854–17. doi: 10.1128/AAC.00854-17
   PubMed Web of Science ®Google Scholar
• Srivastava, G., Tripathi, S., Kumar, A., & Sharma, A. (2017). Molecular investigation of active binding site of isoniazid (INH) and insight into resistance mechanism of S315T-MtKatG in Mycobacterium tuberculosis. Tuberculosis, 105, 18–27. doi: 10.1016/j.tube.2017.04.002
   PubMed Web of Science ®Google Scholar
• Srivastava, G., Tripathi, S., Kumar, A., & Sharma, A. (2018). Molecular insight into multiple RpoB clinical mutants of Mycobacterium tuberculosis: An attempt to probe structural variations in rifampicin binding site underlying drug resistance. International Journal of Biological Macromolecules, 120, 2200–2214. doi: 10.1016/j.ijbiomac.2018.06.184
   PubMed Web of Science ®Google Scholar
• Tiwari, A., Kumar, A., Srivastava, G., & Sharma, A. (2019). Screening of anti-mycobacterial phytochemical compounds for potential inhibitors against Mycobacterium tuberculosis isocitrate lyase. Current Topics in Medicinal Chemistry, 19(8), 600–608. doi: 10.2174/1568026619666190304125603
   PubMed Web of Science ®Google Scholar
• Tripathi, S., Srivastava, G., & Sharma, A. (2016). Molecular dynamics simulation and free energy landscape methods in probing L215H, L217R and L225M βI-tubulin mutations causing paclitaxel resistance in cancer cells. Biochemical & Biophysical Research Communications, 476(4), 273–279. doi: 10.1016/j.bbrc.2016.05.112
   PubMed Web of Science ®Google Scholar
• Turner, P. J. (2005). XMGRACE, Version 5.1. 19. Beaverton: Center for Coastal and Land-Margin Research, Oregon Graduate Institute of Science and Technology.
   Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. doi: 10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Whitfield, M. G., Soeters, H. M., Warren, R. M., York, T., Sampson, S. L., Streicher, E. M., … van Rie, A. (2015). A global perspective on pyrazinamide resistance: Systematic review and meta-analysis. PLoS One, 10(7), e0133869. doi: 10.1371/journal.pone.0133869
   PubMed Web of Science ®Google Scholar
• World Health Organization. (2016). Global tuberculosis report 2016. Switzerland: World Health Organization Press.
   Google Scholar
• Wright, A., Zignol, M., Van Deun, A., Falzon, D., Gerdes, S. R., Feldman, K., … Raviglione, M. (2009). Epidemiology of antituberculosis drug resistance 2002–07: An updated analysis of the Global Project on Anti-Tuberculosis Drug Resistance Surveillance. The Lancet, 373(9678), 1861–1873. doi: 10.1016/S0140-6736(09)60331-7
   PubMed Web of Science ®Google Scholar
• Zhang, Y., & Mitchison, D. (2003). The curious characteristics of pyrazinamide: A review. The International Journal of Tuberculosis & Lung Disease, 7(1), 6–21.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., Permar, S., & Sun, Z. (2002). Conditions that may affect the results of susceptibility testing of Mycobacterium tuberculosis to pyrazinamide. Journal of Medical Microbiology, 51(1), 42–49. doi: 10.1099/0022-1317-51-1-42
   PubMed Web of Science ®Google Scholar
• Zhang, Y., Scorpio, A., Nikaido, H., & Sun, Z. (1999). Role of acid pH and deficient efflux of pyrazinoic acid in unique susceptibility of Mycobacterium tuberculosis to pyrazinamide. Journal of Bacteriology, 181(7), 2044–2049.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., Zhang, J., Cui, P., Zhang, Y., & Zhang, W. (2017). Identification of novel efflux proteins Rv0191, Rv3756c, Rv3008, and Rv1667c involved in pyrazinamide resistance in Mycobacterium tuberculosis. Antimicrobial Agents & Chemotherapy, 61(8), e00940–17. doi: 10.1128/AAC.00940-17
   PubMed Web of Science ®Google Scholar