Login Register Cart 0
Generic placeholder image

Current Computer-Aided Drug Design

Editor-in-Chief

ISSN (Print): 1573-4099
ISSN (Online): 1875-6697

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Structure-based in silico and in vitro Analysis Reveals Asiatic Acid as Novel Potential Inhibitor of Mycobacterium tuberculosis Maltosyl Transferase

Author(s): Kratika Singh, Akanksha Sharma, Tarun Kumar Upadhyay, Mohammad Hayat-ul-Islam, M. Kalim A. Khan, Upendra N. Dwivedi and Rolee Sharma*

Volume 18, Issue 3, 2022

Published on: 17 August, 2022

Page: [213 - 227] Pages: 15

DOI: 10.2174/1573409918666220623105908

Price: $65

conference banner
Abstract

Aims: The present study aimed to search for novel potent inhibitor(s) against the recently discovered maltosyltransferase (GlgE) target of M.tb.

Background: GlgE belongs to an α-amylase family and catalyzes the elongation of cytosolic branched α-glucan. Inactivation of M.tb. GlgE results in DNA damage and rapid death of M.tb. due to the accumulation of a toxic altosyl donor, maltose-1-phosphate (M1P), suggesting that GlgE is an intriguing target for inhibitor design.

Methods: 1000 natural compounds were compiled from public databases and literature through virtual screening, of which 25 compounds were found to satisfy all drug-likeness properties and ADME/ toxicity criteria, followed by molecular docking with GlgE. Compound(s) showing the lowest binding energy was further subjected to molecular dynamics simulation (MDS) and in vitro analysis.

Results: Molecular docking analysis allowed the selection of 5 compounds withsignificant binding affinity to GlgE targets. Amongst these compounds, asiatic acid exhibited the lowest binding energy (-12.61 kcal/mol). The results of 20-ns MDS showed that asiatic acid formed a stable complex with GlgE. Additionally, asiatic acid exhibited in vitro anti-mycobacterial activity against M.tb. H37Ra, M. bovis BCG, and M. smegmatis strains.

Conclusion: The study reveals asiatic acid as a promising anti-mycobacterial agent that might emerge as a novel natural anti-TB lead molecule in the future.

Keywords: Tuberculosis, maltosyltransferase, molecular docking, molecular dynamic simulation, anti-TB, natural compounds.

« Previous Next »
Graphical Abstract

[1]
Organization, W.H. W.H. Organization, WHO Global tuberculosis report, 2020.
[2]
Mishra, G.P.; Mulani, J.D. First national anti tuberculosis drug resistance survey (ndrs) from India - an eye opener. J. Infect., 2018, 1(2), 26-29.
[http://dx.doi.org/10.29245/2689-9981/2018/2.1117]
[3]
Chatue, K. Isoniazid and adverse events. Res. Pediatr. Neonatol., 2017, 1(2), 20-22.
[4]
Schaaf, H.S.; Thee, S.; van der Laan, L.; Hesseling, A.C.; Garcia-Prats, A.J. Adverse effects of oral second-line antituberculosis drugs in children. Expert Opin. Drug Saf., 2016, 15(10), 1369-1381.
[http://dx.doi.org/10.1080/14740338.2016.1216544] [PMID: 27458876]
[5]
Lahlou, M. The success of natural products in drug discovery. Pharmacol. Pharm., 2013, 4, 17-31.
[http://dx.doi.org/10.4236/pp.2013.43A003]
[6]
Butler, M.S.; Buss, A.D. Natural products--the future scaffolds for novel antibiotics? Biochem. Pharmacol., 2006, 71(7), 919-929.
[http://dx.doi.org/10.1016/j.bcp.2005.10.012] [PMID: 16289393]
[7]
Jachak, S.M.; Saklani, A. Challenges and opportunities in drug discovery from plants. Curr. Sci., 2007, 92, 1251-1257.
[8]
Ekins, S.; Freundlich, J.S.; Choi, I.; Sarker, M.; Talcott, C. Computational databases, pathway and cheminformatics tools for tuberculosis drug discovery. Trends Microbiol., 2011, 19(2), 65-74.
[http://dx.doi.org/10.1016/j.tim.2010.10.005] [PMID: 21129975]
[9]
Kalscheuer, R.; Syson, K.; Veeraraghavan, U.; Weinrick, B.; Biermann, K.E.; Liu, Z.; Sacchettini, J.C.; Besra, G.; Bornemann, S.; Jacobs, W.R. Jr Self-poisoning of Mycobacterium tuberculosis by targeting GlgE in an α-glucan pathway. Nat. Chem. Biol., 2010, 6(5), 376-384.
[http://dx.doi.org/10.1038/nchembio.340] [PMID: 20305657]
[10]
Chandra, G.; Chater, K.F.; Bornemann, S. Unexpected and widespread connections between bacterial glycogen and trehalose metabolism. Microbiology, 2011, 157(Pt 6), 1565-1572.
[http://dx.doi.org/10.1099/mic.0.044263-0] [PMID: 21474533]
[11]
Dinadayala, P.; Sambou, T.; Daffé, M.; Lemassu, A. Comparative structural analyses of the α-glucan and glycogen from Mycobacterium bovis. Glycobiology, 2008, 18(7), 502-508.
[http://dx.doi.org/10.1093/glycob/cwn031] [PMID: 18436565]
[12]
Gagliardi, M.C.; Lemassu, A.; Teloni, R.; Mariotti, S.; Sargentini, V.; Pardini, M.; Daffé, M.; Nisini, R. Cell wall-associated α-glucan is in-strumental for Mycobacterium tuberculosis to block CD1 molecule expression and disable the function of dendritic cell derived from infect-ed monocyte. Cell. Microbiol., 2007, 9(8), 2081-2092.
[http://dx.doi.org/10.1111/j.1462-5822.2007.00940.x] [PMID: 17441985]
[13]
Kaur, D.; Guerin, M.E.; Skovierová, H.; Brennan, P.J.; Jackson, M. Chapter 2: Biogenesis of the cell wall and other glycoconjugates of My-cobacterium tuberculosis. Adv. Appl. Microbiol., 2009, 69, 23-78.
[http://dx.doi.org/10.1016/S0065-2164(09)69002-X] [PMID: 19729090]
[14]
Sambou, T.; Dinadayala, P.; Stadthagen, G.; Barilone, N.; Bordat, Y.; Constant, P.; Levillain, F.; Neyrolles, O.; Gicquel, B.; Lemassu, A.; Daffé, M.; Jackson, M. Capsular glucan and intracellular glycogen of Mycobacterium tuberculosis: Biosynthesis and impact on the persis-tence in mice. Mol. Microbiol., 2008, 70(3), 762-774.
[http://dx.doi.org/10.1111/j.1365-2958.2008.06445.x] [PMID: 18808383]
[15]
Kalscheuer, R.; Jacobs, W.R., Jr The significance of GlgE as a new target for tuberculosis. Drug News Perspect., 2010, 23(10), 619-624.
[http://dx.doi.org/10.1358/dnp.2010.23.10.1534855] [PMID: 21180647]
[16]
Veleti, S.K.; Lindenberger, J.J.; Ronning, D.R.; Sucheck, S.J. Synthesis of a C-phosphonate mimic of maltose-1-phosphate and inhibition studies on Mycobacterium tuberculosis GlgE. Bioorg. Med. Chem., 2014, 22(4), 1404-1411.
[http://dx.doi.org/10.1016/j.bmc.2013.12.058] [PMID: 24461562]
[17]
Veleti, S.K.; Lindenberger, J.J.; Thanna, S.; Ronning, D.R.; Sucheck, S.J. Synthesis of a poly-hydroxypyrolidine-based inhibitor of Myco-bacterium tuberculosis GlgE. J. Org. Chem., 2014, 79(20), 9444-9450.
[http://dx.doi.org/10.1021/jo501481r] [PMID: 25137149]
[18]
Billones, J.B.; Valle, A.M.F. Structure-based design of inhibitors against maltosyltransferase GlgE. Orient. J. Chem., 2014, 30(3), 1137-1145.
[http://dx.doi.org/10.13005/ojc/300326]
[19]
Desoubzdanne, D.; Marcourt, L.; Raux, R.; Chevalley, S.; Dorin, D.; Doerig, C.; Valentin, A.; Ausseil, F.; Debitus, C. Alisiaquinones and alisiaquinol, dual inhibitors of Plasmodium falciparum enzyme targets from a new caledonian deep water sponge. J. Nat. Prod., 2008, 71(7), 1189-1192.
[http://dx.doi.org/10.1021/np8000909] [PMID: 18512987]
[20]
Mangal, M.; Sagar, P.; Singh, H.; Raghava, G.P.; Agarwal, S.M. NPACT: Naturally occurring plant-based anti-cancer compound-activity-target database. Nucleic Acids Res., 2013, 41(Database issue), D1124-D1129.
[http://dx.doi.org/10.1093/nar/gks1047] [PMID: 23203877]
[21]
Yamashita, S.; Furubayashi, T.; Kataoka, M.; Sakane, T.; Sezaki, H.; Tokuda, H. Optimized conditions for prediction of intestinal drug per-meability using Caco-2 cells. Eur. J. Pharm. Sci., 2000, 10(3), 195-204.
[http://dx.doi.org/10.1016/S0928-0987(00)00076-2] [PMID: 10767597]
[22]
Molinspiration Cheminformatics. 2016. Available from: 2016.http://www.molinspiration.com/cgi-bin/properties
[23]
Lipinski, C.A.; Lombardo, F.; Dominy, B.W.; Feeney, P.J. Experimental and computational approaches to estimate solubility and permeabil-ity in drug discovery and development settings. Adv. Drug Deliv. Rev., 2001, 46(1-3), 3-26.
[http://dx.doi.org/10.1016/S0169-409X(00)00129-0] [PMID: 11259830]
[24]
Lindenberger, J.J.; Veleti, S.K.; Wilson, B.N.; Sucheck, S.J.; Ronning, D.R. Crystal structures of Mycobacterium tuberculosis GlgE and com-plexes with non-covalent inhibitors. Sci. Rep., 2015, 5, 12830.
[http://dx.doi.org/10.1038/srep12830] [PMID: 26245983]
[25]
Morris, G.M.; Huey, R.; Lindstrom, W.; Sanner, M.F.; Belew, R.K.; Goodsell, D.S.; Olson, A.J. Autodock4 and autodocktools4: Automated docking with selective receptor flexibility. J. Comput. Chem., 2009, 30(16), 2785-2791.
[http://dx.doi.org/10.1002/jcc.21256] [PMID: 19399780]
[26]
Baig, M.H.; Ahmad, K.; Roy, S.; Ashraf, J.M.; Adil, M.; Siddiqui, M.H.; Khan, S.; Kamal, M.A.; Provazník, I.; Choi, I. Computer aided drug design: Success and limitations. Curr. Pharm. Des., 2016, 22(5), 572-581.
[http://dx.doi.org/10.2174/1381612822666151125000550] [PMID: 26601966]
[27]
Jacob, K.S.; Ganguly, S.; Kumar, P.; Poddar, R.; Kumar, A. Homology model, molecular dynamics simulation and novel pyrazole analogs design of Candida albicans CYP450 lanosterol 14 α-demethylase, a target enzyme for antifungal therapy. J. Biomol. Struct. Dyn., 2017, 35(7), 1446-1463.
[http://dx.doi.org/10.1080/07391102.2016.1185380] [PMID: 27142238]
[28]
Pandey, R.K.; Narula, A.; Naskar, M.; Srivastava, S.; Verma, P.; Malik, R.; Shah, P.; Prajapati, V.K. Exploring dual inhibitory role of febri-fugine analogues against Plasmodium utilizing structure-based virtual screening and molecular dynamic simulation. J. Biomol. Struct. Dyn., 2017, 35(4), 791-804.
[http://dx.doi.org/10.1080/07391102.2016.1161560] [PMID: 26984239]
[29]
Pathak, R.K. MamtaBaunthiyal, M.; Rohit Shukla, R.; Pandey, D.; Taj, G.; Kumar, A. In silico identification of mimicking molecules as defense inducers triggering jasmonic acid mediated immunity against Alternaria blight disease in Brassica species. Front Plant Sci., 2017, 8, 609.
[http://dx.doi.org/10.3389/fpls.2017.00609] [PMID: 28487711]
[30]
Sharma, V.; Wakode, S. Structural insight into selective phosphodiesterase 4B inhibitors: Pharmacophore-based virtual screening, docking, and molecular dynamics simulations. J. Biomol. Struct. Dyn., 2017, 35(6), 1339-1349.
[http://dx.doi.org/10.1080/07391102.2016.1183520] [PMID: 27136969]
[31]
Sun, D.R.; Zheng, Q.C.; Zhang, H.X. Probing the interaction mechanism of small molecule inhibitors with matriptase based on molecular dynamics simulation and free energy calculations. J. Biomol. Struct. Dyn., 2017, 35(4), 755-764.
[http://dx.doi.org/10.1080/07391102.2016.1160259] [PMID: 26942570]
[32]
Pronk, S.; Páll, S.; Schulz, R.; Larsson, P.; Bjelkmar, P.; Apostolov, R.; Shirts, M.R.; Smith, J.C.; Kasson, P.M.; van der Spoel, D.; Hess, B.; Lindahl, E. GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics, 2013, 29(7), 845-854.
[http://dx.doi.org/10.1093/bioinformatics/btt055] [PMID: 23407358]
[33]
Goncalves, A.S.; Franca, T.C.C.; Figueroa-Villar, J.D.; Pascutti, P.G. Molecular dynamics simulations and QM/MM studies of the reactiva-tion by 2-PAM of tabun inhibited human acethylcolinesterase. J. Braz. Chem. Soc., 2011, 22, 155-165.
[http://dx.doi.org/10.1590/S0103-50532011000100021]
[34]
Elshikh, M.; Ahmed, S.; Funston, S.; Dunlop, P.; McGaw, M.; Marchant, R.; Banat, I.M. Resazurin-based 96-well plate microdilution meth-od for the determination of minimum inhibitory concentration of biosurfactants. Biotechnol. Lett., 2016, 38(6), 1015-1019.
[http://dx.doi.org/10.1007/s10529-016-2079-2] [PMID: 26969604]
[35]
Martin, A.; Camacho, M.; Portaels, F.; Palomino, J.C. Resazurin microtiter assay plate testing of Mycobacterium tuberculosis susceptibilities to second-line drugs: Rapid, simple, and inexpensive method. Antimicrob. Agents Chemother., 2003, 47(11), 3616-3619.
[http://dx.doi.org/10.1128/AAC.47.11.3616-3619.2003] [PMID: 14576129]
[36]
Wayne, P.A. NCCLS: National committee for clinical laboratory standards. methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard CLSI Document M7-A5; National Committee for Clinical Laboratory Standards: Wayne, PA, USA, 2002.
[37]
Shleeva, M.O.; Kondratieva, T.K.; Demina, G.R.; Rubakova, E.I.; Goncharenko, A.V.; Apt, A.S.; Kaprelyants, A.S. Overexpression of ade-nylyl cyclase encoded by the mycobacterium tuberculosis rv2212 gene confers improved fitness, accelerated recovery from dormancy and enhanced virulence in mice. Front. Cell. Infect. Microbiol., 2017, 7(7), 370.
[http://dx.doi.org/10.3389/fcimb.2017.00370] [PMID: 28861399]
[38]
Zhao, Y.H.; Le, J.; Abraham, M.H.; Hersey, A.; Eddershaw, P.J.; Luscombe, C.N.; Butina, D.; Beck, G.; Sherborne, B.; Cooper, I.; Platts, J.A. Evaluation of human intestinal absorption data and subsequent derivation of a quantitative structure-activity relationship (QSAR) with the Abraham descriptors. J. Pharm. Sci., 2001, 90(6), 749-784.
[http://dx.doi.org/10.1002/jps.1031] [PMID: 11357178]
[39]
Sharma, A.; Islam, M.H.; Fatima, N.; Upadhyay, T.K.; Khan, M.K.A.; Dwivedi, U.N.; Sharma, R. Deciphering the binding of natural terpe-noids to Mycobacterium tuberculosis type iii polyketide synthase18 (pks18): An in-silico approach. J. Appl. Pharm. Sci., 2018, 8(5), 26-34.
[http://dx.doi.org/10.7324/JAPS.2018.8504]
[40]
Horie, K.; Tang, F.; Borchardt, R.T. Isolation and characterization of Caco-2 subclones expressing high levels of multidrug resistance pro-tein efflux transporter. Pharm. Res., 2003, 20(2), 161-168.
[http://dx.doi.org/10.1023/A:1022359300826] [PMID: 12636153]
[41]
Ma, X.L.; Chen, C.; Yang, J. Predictive model of blood-brain barrier penetration of organic compounds. Acta Pharmacol. Sin., 2005, 26(4), 500-512.
[http://dx.doi.org/10.1111/j.1745-7254.2005.00068.x] [PMID: 15780201]
[42]
Mendes, V.; Blaszczyk, M.; Maranha, A.; Empadinhas, N.; Blundell, T.L. Structure of Mycobacterium thermoresistibile glge defines novel conformational states that contribute to the catalytic mechanism. Sci. Rep., 2015, 5, 17144.
[http://dx.doi.org/10.1038/srep17144] [PMID: 26616850]
[43]
Syson, K.; Stevenson, C.E.M.; Rejzek, M.; Fairhurst, S.A.; Nair, A.; Bruton, C.J.; Field, R.A.; Chater, K.F.; Lawson, D.M.; Bornemann, S. Structure of streptomyces maltosyltransferase glge, a homologue of a genetically validated anti-tuberculosis target. J. Biol. Chem., 2011, 286(44), 38298-38310.
[http://dx.doi.org/10.1074/jbc.M111.279315] [PMID: 21914799]
[44]
Xu, M.F.; Xiong, Y.Y.; Liu, J.K.; Qian, J.J.; Zhu, L.; Gao, J. Asiatic acid, a pentacyclic triterpene in Centella asiatica, attenuates glutamate-induced cognitive deficits in mice and apoptosis in SH-SY5Y cells. Acta Pharmacol. Sin., 2012, 33(5), 578-587.
[http://dx.doi.org/10.1038/aps.2012.3] [PMID: 22447225]
[45]
Gurfinkel, D.M.; Chow, S.; Hurren, R.; Gronda, M.; Henderson, C.; Berube, C.; Hedley, D.W.; Schimmer, A.D. Disruption of the endoplas-mic reticulum and increases in cytoplasmic calcium are early events in cell death induced by the natural triterpenoid Asiatic acid. Apoptosis, 2006, 11(9), 1463-1471.
[http://dx.doi.org/10.1007/s10495-006-9086-z] [PMID: 16820960]
[46]
Tang, L.; Yang, G.; Tan, J. Inhibitory effect of asiatic acid on expression of collagen i protein in hsc-t6 cells. J. Fourth Military Univ., 2007, 28, 1178-1180.
[47]
Zhou, J.; Jing, G.; Chun-Qian, F. Effect of asiatic acid on the proliferation of hepg2 cells. J. Jiangsu Univ., 2009, 19(6), 209-218.
[48]
Lyuet, T.; Liu, F.; Chen, Y. Effect of asiatic acid on proliferation of multiple myeloma cells and its mechanism. Chin. Tradit. Herbal Drugs, 2010, 41, 1484-1488.
[49]
Wu, Q.; Lv, T.; Chen, Y.; Wen, L.; Zhang, J.; Jiang, X.; Liu, F. Apoptosis of HL-60 human leukemia cells induced by Asiatic acid through modulation of B-cell lymphoma 2 family proteins and the mitogen-activated protein kinase signaling pathway. Mol. Med. Rep., 2015, 12(1), 1429-1434.
[http://dx.doi.org/10.3892/mmr.2015.3534] [PMID: 25815462]
[50]
Kavitha, C.V.; Jain, A.K.; Agarwal, C.; Pierce, A.; Keating, A.; Huber, K.M.; Serkova, N.J.; Wempe, M.F.; Agarwal, R.; Deep, G. Asiatic acid induces endoplasmic reticulum stress and apoptotic death in glioblastoma multiforme cells both in vitro and in vivo. Mol. Carcinog., 2015, 54(11), 1417-1429.
[http://dx.doi.org/10.1002/mc.22220] [PMID: 25252179]
[51]
Gonçalves, B.; Salvador, J.; Marín, S. Synthesis and biological evaluation of novel asiatic acid derivatives with anticancer activity. RSC Advances, 2016, 2016(6), 1-21.
[http://dx.doi.org/10.1039/C5RA19120C]
[52]
Lee, J.W.; Park, H.A.; Kwon, O.K.; Jang, Y.G.; Kim, J.Y.; Choi, B.K.; Lee, H.J.; Lee, S.; Paik, J.H.; Oh, S.R.; Ahn, K.S.; Lee, H.J. Asiatic acid inhibits pulmonary inflammation induced by cigarette smoke. Int. Immunopharmacol., 2016, 39, 208-217.
[http://dx.doi.org/10.1016/j.intimp.2016.07.010] [PMID: 27494684]
[53]
Alfrd Mavondo, G.A.; Tagumirwa, M.C. Asiatic acid-pectin hydrogel matrix patch transdermal delivery system influences parasitaemia suppression and inflammation reduction in P. berghei murine malaria infected Sprague-Dawley rats. Asian Pac. J. Trop. Med., 2016, 9(12), 1172-1180.
[http://dx.doi.org/10.1016/j.apjtm.2016.10.008] [PMID: 27955745]
[54]
Dong, S.H.; Liu, Y.W.; Wei, F.; Tan, H.Z.; Han, Z.D. Asiatic acid ameliorates pulmonary fibrosis induced by bleomycin (BLM) via sup-pressing pro-fibrotic and inflammatory signaling pathways. Biomed. Pharmacother., 2017, 89, 1297-1309.
[http://dx.doi.org/10.1016/j.biopha.2017.03.005] [PMID: 28320097]
[55]
Zhang, L.; Chen, J.; Gong, Y.; Liu, J.; Zhang, L.; Hua, W.; Sun, H. Synthesis and biological evaluation of asiatic acid derivatives as inhibi-tors of glycogen phosphorylases. Chem. Biodivers., 2009, 6(6), 864-874.
[http://dx.doi.org/10.1002/cbdv.200800092] [PMID: 19551727]
[56]
Fang, C.; Guo, J.; Zhou, J. Asiatic acid protects hearts and relative mitochondria of streptozotocin-induced diabetic rats. J. Jiangsu Univ., 2010, 2, 285-286.
[57]
Chen, C.Y. TCM Database@Taiwan: The world’s largest traditional Chinese medicine database for drug screening in silico. PLoS One, 2011, 6(1), e15939.
[http://dx.doi.org/10.1371/journal.pone.0015939] [PMID: 21253603]
[58]
Lu, Y.; Liu, S.; Wang, Y.; Wang, D.; Gao, J.; Zhu, L. Asiatic acid uncouples respiration in isolated mouse liver mitochondria and induces HepG2 cells death. Eur. J. Pharmacol., 2016, 786, 212-223.
[http://dx.doi.org/10.1016/j.ejphar.2016.06.010] [PMID: 27288117]
[59]
Qi, Z.; Ci, X.; Huang, J.; Liu, Q.; Yu, Q.; Zhou, J.; Deng, X. Asiatic acid enhances Nrf2 signaling to protect HepG2 cells from oxidative damage through Akt and ERK activation. Biomed. Pharmacother., 2017, 88, 252-259.
[http://dx.doi.org/10.1016/j.biopha.2017.01.067] [PMID: 28110191]
[60]
Gao, Z.; Gao, R.; Dong, X. Selective oxidationreduction and esterification of asiatic acid by pestalotiopsismicrospora and anti-hcv activity. Phytochemistry, 2017, 19, 108-113.
[http://dx.doi.org/10.1016/j.phytol.2016.12.014]
[61]
Jiang, W.; Li, M.; He, F.; Bian, Z.; He, Q.; Wang, X.; Yao, W.; Zhu, L. Neuroprotective effect of asiatic acid against spinal cord injury in rats. Life Sci., 2016, 157, 45-51.
[http://dx.doi.org/10.1016/j.lfs.2016.05.004] [PMID: 27153777]
[62]
Ternchoocheep, K.; Surangkul, D. The recovery and protective effects of asiatic acid on differentiated human neuroblastoma sh-sy5y cells cytotoxic-induced by cholesterol. Asian Pacific J., 2017, 7, 416-420.
[http://dx.doi.org/10.1016/j.apjtb.2017.01.012]
[63]
Liu, W.H.; Liu, T.C.; Mong, M.C. Antibacterial effects and action modes of asiatic acid. Biomedicine (Taipei), 2015, 5(3), 16.
[http://dx.doi.org/10.7603/s40681-015-0016-7] [PMID: 26280399]
[64]
Masoko, P.; Picard, J.; Howard, R.L.; Mampuru, L.J.; Eloff, J.N. in vivo antifungal effect of Combretum and Terminalia species extracts on cutaneous wound healing in immunosuppressed rats. Pharm. Biol., 2010, 48(6), 621-632.
[http://dx.doi.org/10.3109/13880200903229080] [PMID: 20645734]
[65]
Suresh, M.; Rath, P.K.; Panneerselvam, A.; Dhanasekaran, D.; Thajuddin, N. Anti-mycobacterial effect of leaf extract of centellaasiatica (mackinlayaceae). Res. J. Pharm. Technol., 2010, 3(3), 872-876.
[66]
Siddiqi, S.; Takhar, P.; Baldeviano, C.; Glover, W.; Zhang, Y. Isoniazid induces its own resistance in nonreplicating Mycobacterium tubercu-losis. Antimicrob. Agents Chemother., 2007, 51(6), 2100-2104.
[http://dx.doi.org/10.1128/AAC.00086-07] [PMID: 17438054]
[67]
Teng, R.; Dick, T. Isoniazid resistance of exponentially growing Mycobacterium smegmatis biofilm culture. FEMS Microbiol. Lett., 2003, 227(2), 171-174.
[http://dx.doi.org/10.1016/S0378-1097(03)00584-6]

Rights & Permissions Print Cite
Article Metrics
13
© 2024 Bentham Science Publishers | Privacy Policy