Binding of piperine to mycobacterial RNA polymerase improves the efficacy of rifampicin activity against Mycobacterium leprae and nontuberculous mycobacteria

References

• Brooks, B. R., Brooks, C. L., Mackerell, A. D., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., … Karplus, M. (2009). CHARMM: The biomolecular simulation program. Journal of Computational Chemistry, 30(10), 1545–1614. https://doi.org/10.1002/jcc.21287
   PubMed Web of Science ®Google Scholar
• Brueckner, F., Ortiz, J., & Cramer, P. (2009). A movie of the RNA polymerase nucleotide addition cycle. Current Opinion in Structural Biology, 19(3), 294–299. https://doi.org/10.1016/j.sbi.2009.04.005
   PubMed Web of Science ®Google Scholar
• Caleffi-Ferracioli, K. R., Maltempe, F. G., Siqueira, V. L. D., & Cardoso, R. F. (2013). Fast detection of drug interaction in Mycobacterium tuberculosis by a checkerboard resazurin method. Tuberculosis (Edinburgh, Scotland), 93(6), 660–663. https://doi.org/10.1016/j.tube.2013.09.001
   PubMed Web of Science ®Google Scholar
• Campbell, E. A., Korzheva, N., Mustaev, A., Murakami, K., Nair, S., Goldfarb, A., & Darst, S. A. (2001). Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell, 104(6), 901–912.
   PubMed Web of Science ®Google Scholar
• Castilho, A. L., Caleffi-Ferracioli, K. R., Canezin, P. H., Dias Siqueira, V. L., de Lima Scodro, R. B., & Cardoso, R. F. (2015). Detection of drug susceptibility in rapidly growing mycobacteria by resazurin broth microdilution assay. Journal of Microbiological Methods, 111, 119–121. https://doi.org/10.1016/j.mimet.2015.02.007
   PubMed Web of Science ®Google Scholar
• Coelho, T., Machado, D., Couto, I., Maschmann, R., Ramos, D., von Groll, A., Rossetti, M. L., Silva, P. A., & Viveiros, M. (2015). Enhancement of antibiotic activity by efflux inhibitors against multidrug resistant Mycobacterium tuberculosis clinical isolates from Brazil. Frontiers in Microbiology, 6(APR), 1–12. https://doi.org/10.3389/fmicb.2015.00330
   PubMedGoogle Scholar
• Daley, C. L. (2017). Mycobacterium avium Complex Disease. Microbiology Spectrum, 5(2), U1–U9. https://doi.org/10.1128/microbiolspec.TNMI7-0045-2017
   Google Scholar
• Daley, C. L., Iaccarino, J. M., Lange, C., Cambau, E., Wallace, R. J., Andrejak, C., Böttger, E. C., Brozek, J., Griffith, D. E., Guglielmetti, L., Huitt, G. A., Knight, S. L., Leitman, P., Marras, T. K., Olivier, K. N., Santin, M., Stout, J. E., Tortoli, E., van Ingen, J., Wagner, D., & Winthrop, K. L. (2020). Treatment of nontuberculous mycobacterial pulmonary disease: An official ATS/ERS/ESCMID/IDSA clinical practice guideline. Clinical Infectious Diseases, 71(4), 905–913. https://doi.org/10.1093/cid/ciaa1125
   PubMed Web of Science ®Google Scholar
• Emsley, P., & Cowtan, K. (2004). Coot: Model-building tools for molecular graphics. Acta Crystallographica. Section D, Biological Crystallography, 60(Pt 12 Pt 1), 2126–2132. https://doi.org/10.1107/S0907444904019158
   PubMedGoogle Scholar
• Esther, C. R., Esserman, D. A., Gilligan, P., Kerr, A., & Noone, P. G. (2010). Chronic Mycobacterium abscessus infection and lung function decline in cystic fibrosis. Journal of Cystic Fibrosis, 9(2), 117–123. https://doi.org/10.1016/j.jcf.2009.12.001
   PubMed Web of Science ®Google Scholar
• Feng, Y., Degen, D., Wang, X., Gigliotti, M., Liu, S., Zhang, Y., Das, D., Michalchuk, T., Ebright, Y. W., Talaue, M., Connell, N., & Ebright, R. H. (2015). Structural basis of transcription inhibition by CBR hydroxamidines and CBR pyrazoles. Structure, 23(8), 1470–1481. https://doi.org/10.1016/j.str.2015.06.009
   PubMed Web of Science ®Google Scholar
• Forbes, B. A. (2017). Mycobacterial taxonomy. Journal of Clinical Microbiology, 55(2), 380–383. https://doi.org/10.1128/JCM.01287-16
   PubMed Web of Science ®Google Scholar
• Forno, C., Häusermann, P., Hatz, C., Itin, P., & Blum, J. (2010). The difficulty in diagnosis and treatment of leprosy. Journal of Travel Medicine, 17(4), 281–283. https://doi.org/10.1111/j.1708-8305.2010.00419.x
   PubMed Web of Science ®Google Scholar
• Grant, B. J., Rodrigues, A. P. C., ElSawy, K. M., McCammon, J. A., & Caves, L. S. D. (2006). Bio3d: An R package for the comparative analysis of protein structures. Bioinformatics, 22(21), 2695–2696. https://doi.org/10.1093/bioinformatics/btl461
   PubMed Web of Science ®Google Scholar
• Griffith, D. E., Aksamit, T., Brown-Elliott, B. A., Catanzaro, A., Daley, C., Gordin, F., Holland, S. M., Horsburgh, R., Huitt, G., Iademarco, M. F., Iseman, M., Olivier, K., Ruoss, S., Von Reyn, C. F., Wallace, R. J., & Winthrop, K. (2007). An official ATS/IDSA statement: Diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. American Journal of Respiratory and Critical Care Medicine, 175(4), 367–416. https://doi.org/10.1164/rccm.200604-571ST
   PubMed Web of Science ®Google Scholar
• Haq, I. U., Imran, M., Nadeem, M., Tufail, T., Gondal, T. A., & Mubarak, M. S. (2020). Piperine: A review of its biological effects. Phytotherapy Research, 35(2), 680–700. https://doi.org/10.1002/ptr.6855
   PubMed Web of Science ®Google Scholar
• Hegeto, L. A., Caleffi-Ferracioli, K. R., Nakamura-Vasconcelos, S. S., Almeida, A. L., de, Baldin, V. P., Nakamura, C. V., Siqueira, V. L. D., Scodro, R. B. L., & Cardoso, R. F. (2018). In vitro combinatory activity of piperine and anti-tuberculosis drugs in Mycobacterium tuberculosis. Tuberculosis (Edinburgh, Scotland), 111, 35–40. https://doi.org/10.1016/j.tube.2018.05.006
   PubMed Web of Science ®Google Scholar
• Henkle, E., & Winthrop, K. L. (2015). Nontuberculous mycobacteria infections in immunosuppressed hosts. Clinics in Chest Medicine, 36(1), 91–99. https://doi.org/10.1016/j.ccm.2014.11.002
   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. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Khameneh, B., Iranshahy, M., Ghandadi, M., Ghoochi Atashbeyk, D., Fazly Bazzaz, B. S., & Iranshahi, M. (2015). Investigation of the antibacterial activity and efflux pump inhibitory effect of co-loaded piperine and gentamicin nanoliposomes in methicillin-resistant Staphylococcus aureus. Drug Development and Industrial Pharmacy, 41(6), 989–994. https://doi.org/10.3109/03639045.2014.920025
   PubMed Web of Science ®Google Scholar
• Klein, J. L., Brown, T. J., & French, G. L. (2001). Rifampin resistance in Mycobacterium kansasii is associated with rpoB mutations. Antimicrobial Agents and Chemotherapy, 45(11), 3056–3058. https://doi.org/10.1128/AAC.45.11.3056-3058.2001
   PubMed Web of Science ®Google Scholar
• Lin, W., Mandal, S., Degen, D., Liu, Y., Ebright, Y. W., Li, S., Feng, Y., Zhang, Y., Mandal, S., Jiang, Y., Liu, S., Gigliotti, M., Talaue, M., Connell, N., Das, K., Arnold, E., & Ebright, R. H. (2017). Structural Basis of Mycobacterium tuberculosis transcription and transcription inhibition. Molecular Cell, 66(2), 169–179.e8. https://doi.org/10.1016/j.molcel.2017.03.001
   PubMed Web of Science ®Google Scholar
• Misch, E. A., Saddler, C., & Davis, J. M. (2018). Skin and soft tissue infections due to nontuberculous mycobacteria. Current Infectious Disease Reports, 20(4), 6. https://doi.org/10.1007/s11908-018-0611-3 [PMC][29556857
   PubMed 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. https://doi.org/10.1002/jcc.21256
   PubMed Web of Science ®Google Scholar
• Murase, L. S., Perez de Souza, J. V., Meneguello, J. E., Seixas, F., A. V., Hegeto, L. A., Scodro, R. B. d L., Siqueira, V. L. D., Caleffi Ferracioli, K. R., & Cardoso, R. F. (2019). Possible binding of Piperine in Mycobacterium tuberculosis RNA polymerase and Rifampin Synergism. Antimicrobial Agents and Chemotherapy, 63(11), 1–7. https://doi.org/10.1128/AAC.02520-18
   Web of Science ®Google Scholar
• Neese, F. (2012). The ORCA program system. WIREs Computational Molecular Science, 2(1), 73–78. https://doi.org/10.1002/wcms.81
   Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera–a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Phillips, J. C., Hardy, D. J., Maia, J. D. C., Stone, J. E., Ribeiro, J. V., Bernardi, R. C., Buch, R., Fiorin, G., Hénin, J., Jiang, W., McGreevy, R., Melo, M. C. R., Radak, B. K., Skeel, R. D., Singharoy, A., Wang, Y., Roux, B., Aksimentiev, A., Luthey-Schulten, Z., … Tajkhorshid, E. (2020). Scalable molecular dynamics on CPU and GPU architectures with NAMD. The Journal of Chemical Physics, 153(4), 044130. https://doi.org/10.1063/5.0014475
   PubMed Web of Science ®Google Scholar
• Quan, S., Venter, H., & Dabbs, E. R. (1997). Ribosylative inactivation of rifampin by Mycobacterium smegmatis is a principal contributor to its low susceptibility to this antibiotic. Antimicrobial Agents and Chemotherapy, 41(11), 2456–2460. https://doi.org/10.1128/AAC.41.11.2456
   PubMed Web of Science ®Google Scholar
• Rominski, A., Roditscheff, A., Selchow, P., Böttger, E. C., & Sander, P. (2017). Intrinsic rifamycin resistance of Mycobacterium abscessus is mediated by ADP-ribosyltransferase MAB_0591. The Journal of Antimicrobial Chemotherapy, 72(2), 376–384. https://doi.org/10.1093/jac/dkw466
   PubMed Web of Science ®Google Scholar
• Schöning-Stierand, K., Diedrich, K., Fährrolfes, R., Flachsenberg, F., Meyder, A., Nittinger, E., Steinegger, R., & Rarey, M. (2020). ProteinsPlus: Interactive analysis of protein–ligand binding interfaces. Nucleic Acids Research, 48(W1), W48–W53. https://doi.org/10.1093/nar/gkaa235
   PubMed Web of Science ®Google Scholar
• Sharma, S., Kalia, N. P., Suden, P., Chauhan, P. S., Kumar, M., Ram, A. B., Khajuria, A., Bani, S., & Khan, I. A. (2014). Protective efficacy of piperine against Mycobacterium tuberculosis. Tuberculosis, 94(4), 389–396. https://doi.org/10.1016/j.tube.2014.04.007
   PubMed Web of Science ®Google Scholar
• Sharma, S., Kumar, M., Sharma, S., Nargotra, A., Koul, S., & Khan, I. A. (2010). Piperine as an inhibitor of Rv1258c, a putative multidrug efflux pump of Mycobacterium tuberculosis. The Journal of Antimicrobial Chemotherapy, 65(8), 1694–1701. https://doi.org/10.1093/jac/dkq186
   PubMed Web of Science ®Google Scholar
• Sievers, F., & Higgins, D. G. (2014). Clustal omega, accurate alignment of very large numbers of sequences. Methods in Molecular Biology, 1079, 105–116. https://doi.org/10.1007/978-1-62703-646-7_6 [PMC][24170397
   PubMedGoogle Scholar
• Tharmalingam, N., Kim, S.-H., Park, M., Woo, H., Kim, H., Yang, J., Rhee, K.-J., & Kim, J. (2014). Inhibitory effect of piperine on Helicobacter pylori growth and adhesion to gastric adenocarcinoma cells. Infectious Agents and Cancer, 9(1), 43. https://doi.org/10.1186/1750-9378-9-43 [PMC][25584066
   PubMedGoogle Scholar
• Thomsen, R., & Christensen, M. H. (2006). MolDock: A new technique for high-accuracy molecular docking. Journal of Medicinal Chemistry, 49(11), 3315–3321. https://doi.org/10.1021/jm051197e
   PubMed Web of Science ®Google Scholar
• Vassylyev, D. G., Vassylyeva, M. N., Zhang, J., Palangat, M., Artsimovitch, I., & Landick, R. (2007). Structural basis for substrate loading in bacterial RNA polymerase. Nature, 448(7150), 163–168. https://doi.org/10.1038/nature05931
   PubMed Web of Science ®Google Scholar
• Vedithi, S. C., Malhotra, S., Das, M., Daniel, S., Kishore, N., George, A., Arumugam, S., Rajan, L., Ebenezer, M., Ascher, D. B., Arnold, E., & Blundell, T. L. (2018). Structural implications of mutations conferring rifampin resistance in Mycobacterium leprae. Scientific Reports, 8(1), 1–12. https://doi.org/10.1038/s41598-018-23423-1
   PubMedGoogle Scholar
• Webb, B., & Sali, A. (2014). Protein structure modeling with MODELLER. Methods in Molecular Biology (Clifton, N.J.), 1137, 1–15. https://doi.org/10.1007/978-1-4939-0366-5_1
   PubMedGoogle Scholar
• Woods, G. L., Brown-Elliott, B. A., Conville, P. S., Desmond, E. P., Hall, G. S., Lin, G., Pfyffer, G. E., Ridderhof, J. C., Siddiqi, S. H., Wallace, R. J. J., Nancy, G. W., Frank, G., & Witebsky, M. (2011). Susceptibility testing of mycobacteria, nocardiae, and other aerobic actinomycetes. Approved Standard—Second Edition (Issue March).
   Google Scholar
• World Health Organization. (2019). Situation de la lèpre dans le monde, 2018: parvenir à un monde exempt de lèpre [Global leprosy update, 2018: Moving towards a leprosy-free world]. Relevé Épidémiologique Hebdomadaire [Weekly Epidemiological Record], 94(35/36), 389–411.
   Google Scholar
• World Health Organization. (2020). Global Tuberculosis Report 2020. https://www.who.int/teams/global-tuberculosis-programme/tb-reports
   Google Scholar
• Zaw, M. T., Emran, N. A., & Lin, Z. (2018). Mutations inside rifampicin-resistance determining region of rpoB gene associated with rifampicin-resistance in Mycobacterium tuberculosis. Journal of Infection and Public Health, 11(5), 605–610. https://doi.org/10.1016/j.jiph.2018.04.005
   PubMed Web of Science ®Google Scholar
• Zoete, V., Cuendet, M. A., Grosdidier, A., & Michielin, O. (2011). SwissParam: A fast force field generation tool for small organic molecules. Journal of Computational Chemistry, 32(11), 2359–2368. https://doi.org/10.1002/jcc.21816
   PubMed Web of Science ®Google Scholar