Phage therapy as a renewed therapeutic approach to mycobacterial infections: a comprehensive review

References

• Gondil V, Chhibber S. Exploring potential of phage therapy for tuberculosis using model organism. Biomed Biotechnol Res J. 2018;2(1):9–15. doi:10.4103/bbrj.bbrj_93_17
   Google Scholar
• Azimi T, Shariati A, Fallah F, et al. Mycobacterium tuberculosis genotyping using MIRU-VNTR typing. J Mazandaran Univ Med Sci. 2017;27(149):40–48.
   Google Scholar
• Azimi T, Nasiri MJ, Zamani S, et al. High genetic diversity among Mycobacterium tuberculosis strains in Tehran, Iran. J Clin Tuberc Other Mycobact Dis. 2018;11:1–6. doi:10.1016/j.jctube.2018.01.001
   Google Scholar
• Taghipour A, Azimi T, Javanmard E, et al. Immunocompromised patients with pulmonary tuberculosis; a susceptible group to intestinal parasites. Gastroenterol Hepatol Bed Bench. 2018;11(Suppl 1):S134–S139.30774820
   PubMedGoogle Scholar
• WHO. Global Tuberculosis Report 2018. World Health Organization; 2018.
   Google Scholar
• Hatfull GF. Mycobacteriophages: windows into tuberculosis. PLoS Pathog. 2014;10(3):e1003953. doi:10.1371/journal.ppat.100395324651299
   PubMed Web of Science ®Google Scholar
• Wei L, Wu J, Liu H, et al. A mycobacteriophage-derived trehalose-6, 6′-dimycolate-binding peptide containing both antimycobacterial and anti-inflammatory abilities. Faseb J. 2013;27(8):3067–3077. doi:10.1096/fj.13-22745423603838
   PubMed Web of Science ®Google Scholar
• Sharahi JY, Azimi T, Shariati A, Safari H, Tehrani MK, Hashemi A. Advanced strategies for combating bacterial biofilms. J Cell Physiol. 2019;234(9):14689–14708. doi:10.1002/jcp.v234.9
   Web of Science ®Google Scholar
• Lu TK, Collins JJ. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc National Acad Sci. 2009;106(12):4629–4634. doi:10.1073/pnas.0800442106
   PubMed Web of Science ®Google Scholar
• Ergene C, Yasuhara K, Palermo EF. Biomimetic antimicrobial polymers: recent advances in molecular design. Polym Chem. 2018;9(18):2407–2427. doi:10.1039/C8PY00012C
   Web of Science ®Google Scholar
• Li W, Tailhades J, O’Brien-Simpson NM, et al. Proline-rich antimicrobial peptides: potential therapeutics against antibiotic-resistant bacteria. Amino Acids. 2014;46(10):2287–2294. doi:10.1007/s00726-014-1820-125141976
   PubMed Web of Science ®Google Scholar
• Bajpai U, Mehta AK, Eniyan K, et al. Isolation and characterization of bacteriophages from India, with lytic activity against Mycobacterium tuberculosis. Can J Microbiol. 2018;64(7):483–491. doi:10.1139/cjm-2017-038729544082
   PubMed Web of Science ®Google Scholar
• Guo S, Ao Z. Phage in the diagnosis and treatment of tuberculosis. Front Biosci. 2012;17:2691–2697. doi:10.2741/4080
   Web of Science ®Google Scholar
• Nasser A, Azizian R, Tabasi M, et al. Specification of bacteriophage isolated against clinical methicillin-resistant staphylococcus aureus. Osong Public Health Res Perspect. 2019;10(1):20–24. doi:10.24171/j.phrp.2019.10.1.0530847267
   PubMedGoogle Scholar
• Azizian R, Nasser A, Askari H, et al. Sewage as a rich source of phage study against Pseudomonas aeruginosa PAO. Biologicals. 2015;43(4):238–241. doi:10.1016/j.biologicals.2015.05.00426049814
   PubMed Web of Science ®Google Scholar
• Reza A, Farid AJ, Zamberi S, et al. Dynamics of bacteriophages as a promising antibiofilm agents. J Pure Appl Microbiol. 2014;8(2):1015–1019.
   Google Scholar
• Nasser A, azizi J, azizian R, askari H, pakzad I. The use of mrsa phage as a super specialized antibiotic against lethal methicillin-resistant staphylococcus aureus. J Ilam Univ Med Sci. 2014;22:171–179.
   Google Scholar
• Suttle CA. Marine viruses—major players in the global ecosystem. Nat Rev Microbiol. 2007;5(10):801–812. doi:10.1038/nrmicro175017853907
   PubMed Web of Science ®Google Scholar
• Summers WC. The strange history of phage therapy. Bacteriophage. 2012;2(2):130–133. doi:10.4161/bact.2075723050223
   PubMedGoogle Scholar
• Sulakvelidze A, Alavidze Z, Morris JG. Bacteriophage therapy. Antimicrob Agents Chemother. 2001;45(3):649–659. doi:10.1128/AAC.45.3.649-659.200111181338
   PubMed Web of Science ®Google Scholar
• Principi N, Silvestri E, Esposito S. Advantages and limitations of bacteriophages for the treatment of bacterial infections. Front Pharmacol. 2019;10:513. doi:10.3389/fphar.2019.0084831139086
   PubMed Web of Science ®Google Scholar
• Dublanchet A, Patey O, Mazure H, Liddle M, Smithyman AM. Indications and Limitations of Phage Therapy in Human Medicine: Personal Experience and Literature Review. Reprints 2018.
   Google Scholar
• Torres-Barceló C. Phage therapy faces evolutionary challenges. Viruses. 2018;10(6):323–330. doi:10.3390/v10060323
   PubMed Web of Science ®Google Scholar
• Kakasis A, Panitsa G. Bacteriophage therapy as an alternative treatment for human infections. A comprehensive review. Int J Antimicrob Agents. 2018;53(1):16–21. doi:10.1016/j.ijantimicag.2018.09.00430236954
   PubMed Web of Science ®Google Scholar
• Bogovazova G, Voroshilova N, Bondarenko V. The efficacy of Klebsiella pneumoniae bacteriophage in the therapy of experimental Klebsiella infection. Zh Mikrobiol Epidemiol Immunobiol. 1991;68(4):5–8.
   PubMed Web of Science ®Google Scholar
• Del Pozo J, Alonso M, Arciola C, et al. Biotechnological war against biofilms. Could phages mean the end of device-related infections? Int J Artif Organs. 2007;30(9):805–812.17918126
   PubMed Web of Science ®Google Scholar
• Vitiello CL, Merril CR, Adhya S. An amino acid substitution in a capsid protein enhances phage survival in mouse circulatory system more than a 1000-fold. Virus Res. 2005;114(1–2):101–103. doi:10.1016/j.virusres.2005.05.01416055223
   PubMed Web of Science ®Google Scholar
• Mattila S, Ruotsalainen P, Jalasvuori M. On-demand isolation of bacteriophages against drug-resistant bacteria for personalized phage therapy. Front Microbiol. 2015;6:1271. doi:10.3389/fmicb.2015.0127126617601
   PubMed Web of Science ®Google Scholar
• Seed KD. Battling phages: how bacteria defend against viral attack. PLoS Pathog. 2015;11(6):e1004847. doi:10.1371/journal.ppat.100484726066799
   PubMed Web of Science ®Google Scholar
• Vandenheuvel D, Lavigne R, Brüssow H. Bacteriophage therapy: advances in formulation strategies and human clinical trials. Annu Rev Virol. 2015;2:599–618. doi:10.1146/annurev-virology-100114-05491526958930
   PubMed Web of Science ®Google Scholar
• Brabban A, Hite E, Callaway T. Evolution of foodborne pathogens via temperate bacteriophage-mediated gene transfer. Foodborne Pathog Dis. 2005;2(4):287–303. doi:10.1089/fpd.2005.2.28716366852
   PubMed Web of Science ®Google Scholar
• Maiques E, Úbeda C, Tormo MÁ, et al. Role of staphylococcal phage and SaPI integrase in intra-and interspecies SaPI transfer. J Bacteriol. 2007;189(15):5608–5616. doi:10.1128/JB.00619-0717545290
   PubMed Web of Science ®Google Scholar
• Kaźmierczak Z, Piotrowicz A, Owczarek B, et al. Molecular imaging of T4 phage in mammalian tissues and cells. Bacteriophage. 2014;4(2):e28364. doi:10.4161/bact.2836424653943
   PubMedGoogle Scholar
• Dąbrowska K, Miernikiewicz P, Piotrowicz A, et al. Immunogenicity studies of proteins forming the T4 phage head surface. J Virol. 2014;88(21):12551–12557. doi:10.1128/JVI.02043-1425142581
   PubMed Web of Science ®Google Scholar
• Rhoads D, Wolcott R, Kuskowski M, Wolcott B, Ward L, Sulakvelidze A. Bacteriophage therapy of venous leg ulcers in humans: results of a phase I safety trial. J Wound Care. 2009;18(6):237–243. doi:10.12968/jowc.2009.18.6.4280119661847
   PubMedGoogle Scholar
• Biswas B, Adhya S, Washart P, et al. Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faecium. Infect Immun. 2002;70(1):204–210. doi:10.1128/iai.70.1.204-210.200211748184
   PubMed Web of Science ®Google Scholar
• Kaur S, Harjai K, Chhibber S. Bacteriophage-aided intracellular killing of engulfed methicillin-resistant Staphylococcus aureus (MRSA) by murine macrophages. Appl Microbiol Biotechnol. 2014;98(10):4653–4661. doi:10.1007/s00253-014-5643-524633444
   PubMed Web of Science ®Google Scholar
• Gondil VS, Chhibber S. Evading antibody mediated inactivation of bacteriophages using delivery systems. J Virol Curr Res. 2017;1:555–574.
   Google Scholar
• Grover N, Paskaleva EE, Mehta KK, Dordick JS, Kane RS. Growth inhibition of Mycobacterium smegmatis by mycobacteriophage-derived enzymes. Enzyme Microb Technol. 2014;63:1–6. doi:10.1016/j.enzmictec.2014.04.01825039052
   PubMed Web of Science ®Google Scholar
• Morello E, Saussereau E, Maura D, Huerre M, Touqui L, Debarbieux L. Pulmonary bacteriophage therapy on Pseudomonas aeruginosa cystic fibrosis strains: first steps towards treatment and prevention. PLoS One. 2011;6(2):e16963. doi:10.1371/journal.pone.001696321347240
   PubMed Web of Science ®Google Scholar
• Li Q, Zhou M, Fan X, Yan J, Li W, Xie J. Mycobacteriophage SWU1 gp39 can potentiate multiple antibiotics against Mycobacterium via altering the cell wall permeability. Sci Rep. 2016;6:28701. doi:10.1038/srep2870127350398
   PubMed Web of Science ®Google Scholar
• Nieth A, Verseux C, Barnert S, Süss R, Römer W. A first step toward liposome-mediated intracellular bacteriophage therapy. Expert Opin Drug Deliv. 2015;12(9):1411–1424. doi:10.1517/17425247.2015.104312525937143
   PubMed Web of Science ®Google Scholar
• Catalão MJ, Gil F, Moniz‐Pereira J, Pimentel M. The mycobacteriophage Ms6 encodes a chaperone‐like protein involved in the endolysin delivery to the peptidoglycan. Mol Microbiol. 2010;77(3):672–686. doi:10.1111/j.1365-2958.2010.07239.x20545844
   PubMed Web of Science ®Google Scholar
• McNerney R, Traore H. Mycobacteriophage and their application to disease control. J Appl Microbiol. 2005;99(2):223–233. doi:10.1111/jam.2005.99.issue-216033452
   PubMed Web of Science ®Google Scholar
• Mayer O, Jain P, Weisbrod TR, et al. Fluorescent reporter DS6A mycobacteriophages reveal unique variations in infectibility and phage production in mycobacteria. J Bacteriol. 2016;198(23):3220–3232. doi:10.1128/JB.00592-1627672191
   PubMed Web of Science ®Google Scholar
• Sula L, Sulova J, Stolcpartova M. Therapy of experimental tuberculosis in guinea pigs with mycobacterial phages DS-6A, GR-21 T, My-327. Czech Med. 1981;4(4):209–214.7327068
   PubMedGoogle Scholar
• Ford M, Stenstrom C, Hendrix R, Hatfull G. Mycobacteriophage TM4: genome structure and gene expression. Tuber Lung Dis. 1998;79(2):63–73. doi:10.1054/tuld.1998.000710645443
   PubMedGoogle Scholar
• Broxmeyer L, Sosnowska D, Miltner E, et al. Killing of Mycobacterium avium and Mycobacterium tuberculosis by a mycobacteriophage delivered by a nonvirulent mycobacterium: a model for phage therapy of intracellular bacterial pathogens. J Infect Dis. 2002;186(8):1155–1160. doi:10.1086/34381212355367
   PubMed Web of Science ®Google Scholar
• Ranjan A, Vidyarthi AS, Poddar R. Evaluation of codon bias perspectives in phage therapy of Mycobacterium tuberculosis by multivariate analysis. In Silico Biol. 2007;7(4,5):423–431.18391235
   PubMedGoogle Scholar
• Allen TM, Cullis PR. Liposomal drug delivery systems: from concept to clinical applications. Adv Drug Deliv Rev. 2013;65(1):36–48. doi:10.1016/j.addr.2012.09.03723036225
   PubMed Web of Science ®Google Scholar
• Un K, Sakai-Kato K, Oshima Y, Kawanishi T, Okuda H. Intracellular trafficking mechanism, from intracellular uptake to extracellular efflux, for phospholipid/cholesterol liposomes. Biomaterials. 2012;33(32):8131–8141. doi:10.1016/j.biomaterials.2012.07.03022858002
   PubMed Web of Science ®Google Scholar
• Rybniker J, Kramme S, Small PL. Host range of 14 mycobacteriophages in Mycobacterium ulcerans and seven other mycobacteria including Mycobacterium tuberculosis–application for identification and susceptibility testing. J Med Microbiol. 2006;55(1):37–42. doi:10.1099/jmm.0.46238-016388028
   PubMed Web of Science ®Google Scholar
• Joshi H, Seniya SP, Suryanarayanan V, Patidar ND, Singh SK, Jain V. Dissecting the structure–function relationship in lysozyme domain of mycobacteriophage D29‐encoded peptidoglycan hydrolase. FEBS Lett. 2017;591(20):3276–3287. doi:10.1002/1873-3468.1284828901529
   PubMed Web of Science ®Google Scholar
• Peng L, Luo Y, Chen B, et al. Therapeutic effect of bacteriophage D29 in the treatment for guinea pigs infected with sensitive strain of Mycobacterium tuberculosis. Chin J Zoonoses. 2009;25(8):733–736.
   Google Scholar
• Pohane AA, Joshi H, Jain V. Molecular dissection of phage endolysin: an interdomain interaction confers host specificity in Lysin A of Mycobacterium phage D29. J Biol Chem. 2014;289(17):12085–12095. doi:10.1074/jbc.M113.52959424627486
   PubMed Web of Science ®Google Scholar
• Hassan S, Dusthackeer A, Subramanyam B, Ponnuraja C, Sivaramakrishnan GN, Kumar V. Lytic efficiency of mycobacteriophages. Open Syst Biol J. 2010;3(1):21–28. doi:10.2174/1876392801003010021
   Google Scholar
• Kamilla S, Jain V. Mycobacteriophage D29 holin C‐terminal region functionally assists in holin aggregation and bacterial cell death. Febs J. 2016;283(1):173–190. doi:10.1111/febs.1356526471254
   PubMed Web of Science ®Google Scholar
• Payne K, Sun Q, Sacchettini J, Hatfull GF. Mycobacteriophage Lysin B is a novel mycolylarabinogalactan esterase. Mol Microbiol. 2009;73(3):367–381. doi:10.1111/j.1365-2958.2009.06775.x19555454
   PubMed Web of Science ®Google Scholar
• Catalao MJ, Gil F, Moniz-Pereira J, Sao-Jose C, Pimentel M. Diversity in bacterial lysis systems: bacteriophages show the way. FEMS Microbiol Rev. 2013;37(4):554–571. doi:10.1111/1574-6976.1200623043507
   PubMed Web of Science ®Google Scholar
• Deng X, Wang L, You X, Dai P, Zeng Y. Advances in the T7 phage display system (Review). Mol Med Rep. 2018;17(1):714–720. doi:10.3892/mmr.2017.799429115536
   PubMed Web of Science ®Google Scholar
• Wisuthiphaet N, Yang X, Young GM, Nitin N. Rapid detection of Escherichia coli in beverages using genetically engineered bacteriophage T7. AMB Express. 2019;9(1):55. doi:10.1186/s13568-019-0776-731004244
   PubMed Web of Science ®Google Scholar
• Chan LY, Kosuri S, Endy D. Refactoring bacteriophage T7. Mol Syst Biol. 2005;1:2005.0018. doi:10.1038/msb4100025
   Web of Science ®Google Scholar
• Sipley J, Stassi D, Dunn J, Goldman E. Analysis of bacteriophage T7 gene 10A and frameshifted 10B proteins. Gene Expression J Liver Res. 1991;1(2):127–136.
   Web of Science ®Google Scholar
• Du Plessis J, Cloete R, Burchell L, et al. Exploring the potential of T7 bacteriophage protein Gp2 as a novel inhibitor of mycobacterial RNA polymerase. Tuberculosis. 2017;106:82–90. doi:10.1016/j.tube.2017.07.00428802409
   PubMed Web of Science ®Google Scholar
• Sheppard C, Cámara B, Shadrin A, et al. Inhibition of Escherichia coli RNAp by T7 Gp2 protein: role of negatively charged strip of amino acid residues in Gp2. J Mol Biol. 2011;407(5):623–632. doi:10.1016/j.jmb.2011.02.01321316373
   PubMed Web of Science ®Google Scholar
• Mekler V, Minakhin L, Sheppard C, Wigneshweraraj S, Severinov K. Molecular mechanism of transcription inhibition by phage T7 gp2 protein. J Mol Biol. 2011;413(5):1016–1027. doi:10.1016/j.jmb.2011.09.02921963987
   PubMed Web of Science ®Google Scholar
• Shadrin A, Sheppard C, Severinov K, Matthews S, Wigneshweraraj S. Substitutions in the Escherichia coli RNA polymerase inhibitor T7 Gp2 that allow inhibition of transcription when the primary interaction interface between Gp2 and RNA polymerase becomes compromised. Microbiology. 2012;158(Pt 11):2753–2764. doi:10.1099/mic.0.062547-022977089
   PubMed Web of Science ®Google Scholar
• Shadrin A, Sheppard C, Savalia D, Severinov K, Wigneshweraraj S. Overexpression of Escherichia coli udk mimics the absence of T7 Gp2 function and thereby abrogates successful infection by T7 phage. Microbiology. 2013;159(Pt 2):269–274. doi:10.1099/mic.0.064527-023242801
   PubMed Web of Science ®Google Scholar
• McClure WR, Cech CL. On the mechanism of rifampicin inhibition of RNA synthesis. J Bio Chem. 1978;253(24):8949–8956.363713
   PubMed Web of Science ®Google Scholar
• Boudvillain M, Nollmann M, Margeat E. Keeping up to speed with the transcription termination factor Rho motor. Transcription. 2010;1(2):70–75. doi:10.4161/trns.1.2.1223221326894
   PubMedGoogle Scholar
• Banerjee S, Chalissery J, Bandey I, Sen R. Rho-dependent transcription termination: more questions than answers. J Microbiol. 2006;44(1):11–22.16554712
   PubMed Web of Science ®Google Scholar
• Peters JM, Vangeloff AD, Landick R. Bacterial transcription terminators: the RNA 3′-end chronicles. J Mol Biol. 2011;412(5):793–813. doi:10.1016/j.jmb.2011.03.03621439297
   PubMed Web of Science ®Google Scholar
• Ray-Soni A, Bellecourt MJ, Landick R. Mechanisms of bacterial transcription termination: all good things must end. Annu Rev Biochem. 2016;85:319–347. doi:10.1146/annurev-biochem-060815-01484427023849
   PubMed Web of Science ®Google Scholar
• Kalyani BS, Muteeb G, Qayyum MZ, Sen R. Interaction with the nascent RNA is a prerequisite for the recruitment of Rho to the transcription elongation complex in vitro. J Mol Biol. 2011;413(3):548–560. doi:10.1016/j.jmb.2011.08.05321920369
   PubMed Web of Science ®Google Scholar
• Grylak-Mielnicka A, Bidnenko V, Bardowski JK, Bidnenko E. Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria. Microbiology. 2016;162(3):433–447. doi:10.1099/mic.0.00024426796109
   PubMed Web of Science ®Google Scholar
• Ghosh G, Reddy J, Sambhare S, Sen R. A bacteriophage capsid protein is an inhibitor of a conserved transcription terminator of various bacterial pathogens. J Bacteriol. 2018;200(1):e00380–e00317. doi:10.1128/JB.00380-17
   PubMed Web of Science ®Google Scholar
• Botella L, Vaubourgeix J, Livny J, Schnappinger D. Depleting Mycobacterium tuberculosis of the transcription termination factor Rho causes pervasive transcription and rapid death. Nat Commun. 2017;8:14731. doi:10.1038/ncomms1473128348398
   PubMed Web of Science ®Google Scholar
• Pani B, Banerjee S, Chalissery J, et al. Mechanism of inhibition of Rho-dependent transcription termination by bacteriophage P4 protein Psu. J Biol Chem. 2006;281(36):26491–26500. doi:10.1074/jbc.M60398220016829521
   PubMed Web of Science ®Google Scholar
• Smith KC, Castro-Nallar E, Fisher JN, Breakwell DP, Grose JH, Burnett SH. Phage cluster relationships identified through single gene analysis. BMC Genomics. 2013;14(1):410. doi:10.1186/1471-2164-14-18123777341
   PubMed Web of Science ®Google Scholar
• Li L, Lee E, Shaw N. Expression, purification and crystallization of phosphoribosyl transferase from a mycobacteriophage. Acta Crystallogr F Struct Biol Commun. 2018;74(3):161–165.29497020
   PubMed Web of Science ®Google Scholar
• Lai M-J, Liu -C-C, Jiang S-J, et al. Antimycobacterial activities of endolysins derived from a mycobacteriophage, BTCU-1. Molecules. 2015;20(10):19277–19290. doi:10.3390/molecules20101927726506338
   PubMed Web of Science ®Google Scholar
• Berman HM, Westbrook J, Feng Z, et al. The protein data bank. Nucleic Acids Res. 2000;28(1):235–242. doi:10.1093/nar/28.1.23510592235
   PubMed Web of Science ®Google Scholar
• Daniel A, Euler C, Collin M, Chahales P, Gorelick KJ, Fischetti VA. Synergism between a novel chimeric lysin and oxacillin protects against infection by methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2010;54(4):1603–1612. doi:10.1128/AAC.01625-0920086153
   PubMed Web of Science ®Google Scholar
• Hermoso JA, García JL, García P. Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Curr Opin Microbiol. 2007;10(5):461–472. doi:10.1016/j.mib.2007.08.00217904412
   PubMed Web of Science ®Google Scholar
• Borysowski J, Weber-Dąbrowska B, Górski A. Bacteriophage endolysins as a novel class of antibacterial agents. Exp Biol Med. 2006;231(4):366–377. doi:10.1177/153537020623100402
   PubMed Web of Science ®Google Scholar
• Payne KM, Hatfull GF. Mycobacteriophage endolysins: diverse and modular enzymes with multiple catalytic activities. PLoS One. 2012;7(3):e34052.22470512
   PubMed Web of Science ®Google Scholar
• Gan Y, Wu T, Liu P, Guo S. Characterization and classification of Bo4 as a cluster G mycobacteriophage that can infect and lyse M. tuberculosis. Arch Microbiol. 2014;196(3):209–218. doi:10.1007/s00203-014-0954-624504137
   PubMed Web of Science ®Google Scholar
• W T. Preliminary Research about Mycobacteriophage Cocktail Therapy against Drug-resistance Tuberculosis. Chongqing, China: Chongqing Medical University; 2012.
   Google Scholar
• Jr WD J, Good RC, Thompson NJ, Kelly GD. Bacteriophage types of Mycobacterium tuberculosis in the United States. Am Rev Respir Dis. 1982;125(6):740–745. doi:10.1164/arrd.1982.125.6.7407091881
   PubMedGoogle Scholar
• Fan X, Teng T, Wang H, Xie J. Biology of a novel mycobacteriophage, SWU1, isolated from Chinese soil as revealed by genomic characteristics. Am Soc Microbiol. 2012;86(18):10230–10231.
   Google Scholar
• Hatfull GF, Jacobs-Sera D, Lawrence JG, et al. Comparative genomic analysis of 60 mycobacteriophage genomes: genome clustering, gene acquisition, and gene size. J Mol Biol. 2010;397(1):119–143. doi:10.1016/j.jmb.2010.01.01120064525
   PubMed Web of Science ®Google Scholar
• Molshanski-Mor S, Yosef I, Kiro R, et al. Revealing bacterial targets of growth inhibitors encoded by bacteriophage T7. Proc National Acad Sci. 2014;111(52):18715–18720. doi:10.1073/pnas.1413271112
   PubMed Web of Science ®Google Scholar
• Banerjee A, Dubnau E, Quemard A, et al. inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science. 1994;263(5144):227–230. doi:10.1126/science.82846738284673
   PubMed Web of Science ®Google Scholar
• Yan S, Xu M, Duan X, et al. Mycobacteriophage putative GTPase-activating protein can potentiate antibiotics. Appl Microbiol Biotechnol. 2016;100(18):8169–8177. doi:10.1007/s00253-016-7681-727345061
   PubMed Web of Science ®Google Scholar
• Johnson DS, Chen YH. Ras family of small GTPases in immunity and inflammation. Curr Opin Pharmacol. 2012;12(4):458–463.22401931
   PubMed Web of Science ®Google Scholar
• Bourne HR, Sanders DA, McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. nature. 1991;349(6305):117–127. doi:10.1038/349117a01898771
   PubMed Web of Science ®Google Scholar
• Merril CR, Scholl D, Adhya SL. The prospect for bacteriophage therapy in Western medicine. Nat Rev Drug Discov. 2003;2(6):489–497. doi:10.1038/nrd111112776223
   PubMed Web of Science ®Google Scholar
• Pang JM, Layre E, Sweet L, et al. The polyketide Pks1 contributes to biofilm formation in Mycobacterium tuberculosis. J Bacteriol. 2012;194(3):715–721. doi:10.1128/JB.06304-1122123254
   PubMed Web of Science ®Google Scholar
• Catalão MJ, Milho C, Gil F, Moniz-Pereira J, Pimentel M. A second endolysin gene is fully embedded in-frame with the lysA gene of mycobacteriophage Ms6. PLoS One. 2011;6(6):e20515. doi:10.1371/journal.pone.002051521694774
   PubMed Web of Science ®Google Scholar
• Catalão MJ, Gil F, Moniz-Pereira J, Pimentel M. Functional analysis of the holin-like proteins of mycobacteriophage Ms6. J Bacteriol. 2011;193(11):2793–2803. doi:10.1128/JB.01519-1021441511
   PubMed Web of Science ®Google Scholar
• Gil F, Grzegorzewicz AE, Catalao MJ, Vital J, McNeil MR, Pimentel M. Mycobacteriophage Ms6 LysB specifically targets the outer membrane of Mycobacterium smegmatis. Microbiology. 2010;156(Pt 5):1497–1504. doi:10.1099/mic.0.032821-020093291
   PubMed Web of Science ®Google Scholar
• Gil F, Catalao MJ, Moniz-Pereira J, Leandro P, McNeil M, Pimentel M. The lytic cassette of mycobacteriophage Ms6 encodes an enzyme with lipolytic activity. Microbiology. 2008;154(5):1364–1371. doi:10.1099/mic.0.2007/014621-018451045
   PubMed Web of Science ®Google Scholar
• Waldor MK, Friedman DI, Adhya SL. Phages: their role in bacterial pathogenesis and biotechnology. ASM Press. 2005;59(9):1003–1004.
   Google Scholar
• Timms VJ, Gehringer MM, Mitchell HM, Daskalopoulos G, Neilan BA. How accurately can we detect Mycobacterium avium subsp. paratuberculosis infection? J Microbiol Methods. 2011;85(1):1–8. doi:10.1016/j.mimet.2011.01.02621281678
   PubMed Web of Science ®Google Scholar
• Basra S, Anany H, Brovko L, Kropinski AM, Griffiths MW. Isolation and characterization of a novel bacteriophage against Mycobacteriumavium subspecies paratuberculosis. Arch Virol. 2014;159(10):2659–2674. doi:10.1007/s00705-014-2122-324903601
   PubMed Web of Science ®Google Scholar
• Busatto C, Vianna JS, Da Silva LVJ, Ramis IB, Da Silva PEA. Mycobacterium avium: an overview. Tuberculosis (Edinb). 2019;114:127–134. doi:10.1016/j.tube.2018.12.00430711152
   PubMed Web of Science ®Google Scholar
• Jr FJ P, Delaney KM, Moorman AC, et al. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. N Engl J Med. 1998;338(13):853–860. doi:10.1056/NEJM1998032633813019516219
   PubMed Web of Science ®Google Scholar
• Kaplan JE, Hanson D, Dworkin MS, et al. Epidemiology of human immunodeficiency virus-associated opportunistic infections in the United States in the era of highly active antiretroviral therapy. Clin Infect Dis. 2000;30(Supplement_1):S5–S14. doi:10.1086/31384310770911
   PubMed Web of Science ®Google Scholar
• Danelishvili L, Young LS, Bermudez LE. In vivo efficacy of phage therapy for Mycobacterium avium infection as delivered by a nonvirulent mycobacterium. Microb Drug Resist. 2006;12(1):1–6. doi:10.1089/mdr.2006.12.116584300
   PubMed Web of Science ®Google Scholar
• van der Paardt A-F, Wilffert B, Akkerman OW, et al. Evaluation of macrolides for possible use against multidrug-resistant Mycobacterium tuberculosis. Eur Respir J. 2015;46(2):444–455. doi:10.1183/09031936.0014701426022960
   PubMed Web of Science ®Google Scholar
• Foley-Thomas EM, Whipple DL, Bermudez LE, Barletta RG. Phage infection, transfection and transformation of Mycobacterium avium complex and Mycobacterium paratuberculosis. Microbiology. 1995;141(5):1173–1181. doi:10.1099/13500872-141-5-11737773411
   PubMed Web of Science ®Google Scholar
• Pradhan G, Shrivastva R, Mukhopadhyay S. Mycobacterial PknG Targets the Rab7l1 signaling pathway to inhibit phagosome–lysosome fusion. J Immunol. 2018;201(5):1421–1433. doi:10.4049/jimmunol.180053030037848
   PubMed Web of Science ®Google Scholar
• Gomes MS, Paul S, Moreira AL, Appelberg R, Rabinovitch M, Kaplan G. Survival of Mycobacterium avium andMycobacterium tuberculosis in acidified vacuoles of murine macrophages. Infect Immun. 1999;67(7):3199–3206.10377091
   PubMed Web of Science ®Google Scholar
• Trigo G, Martins TG, Fraga AG, et al. Phage therapy is effective against infection by Mycobacterium ulcerans in a murine footpad model. PLoS Negl Trop Dis. 2013;7(4):e2183. doi:10.1371/journal.pntd.000218323638204
   PubMed Web of Science ®Google Scholar
• Sarfo FS, Phillips R, Wansbrough‐Jones M, Simmonds RE. Recent advances: role of mycolactone in the pathogenesis and monitoring of Mycobacterium ulcerans infection/Buruli ulcer disease. Cell Microbiol. 2016;18(1):17–29. doi:10.1111/cmi.1254726572803
   PubMed Web of Science ®Google Scholar
• Bolz M, Kerber S, Zimmer G, Pluschke G. Use of recombinant virus replicon particles for vaccination against Mycobacterium ulcerans disease. PLoS Negl Trop Dis. 2015;9(8):e0004011. doi:10.1371/journal.pntd.000401126275222
   PubMed Web of Science ®Google Scholar
• Torrado E, Fraga AG, Logarinho E, et al. IFN-γ–dependent activation of macrophages during experimental infections by Mycobacterium ulcerans is impaired by the toxin mycolactone. J Immunol. 2010;184(2):947–955. doi:10.4049/jimmunol.090271720008288
   PubMed Web of Science ®Google Scholar
• Torrado E, Adusumilli S, Fraga AG, Small PL, Castro AG, Pedrosa J. Mycolactone-mediated inhibition of tumor necrosis factor production by macrophages infected with Mycobacterium ulcerans has implications for the control of infection. Infect Immun. 2007;75(8):3979–3988. doi:10.1128/IAI.00290-0717517872
   PubMed Web of Science ®Google Scholar
• George KM, Chatterjee D, Gunawardana G, et al. Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science. 1999;283(5403):854–857. doi:10.1126/science.283.5403.8549933171
   PubMed Web of Science ®Google Scholar
• Einarsdottir T, Huygen K. Buruli ulcer. Hum Vaccin. 2011;7(11):1198–1203. doi:10.4161/hv.7.11.1775122048117
   PubMed Web of Science ®Google Scholar
• Yeboah‐Manu D, Peduzzi E, Mensah‐Quainoo E, et al. Systemic suppression of interferon‐γ responses in Buruli ulcer patients resolves after surgical excision of the lesions caused by the extracellular pathogen Mycobacterium ulcerans. J Leukoc Biol. 2006;79(6):1150–1156. doi:10.1189/jlb.100558116531561
   PubMed Web of Science ®Google Scholar
• WHO, Initiative GBU. Provisional Guidance on the Role of Specific Antibiotics in the Management of Mycobacterium Ulcerans Disease (buruli Ulcer). Geneva: World Health Organization; 2004.
   Google Scholar
• Kibadi K, Boelaert M, Fraga AG, et al. Response to treatment in a prospective cohort of patients with large ulcerated lesions suspected to be Buruli Ulcer (Mycobacterium ulcerans disease). PLoS Negl Trop Dis. 2010;4(7):e736. doi:10.1371/journal.pntd.000073620625556
   PubMed Web of Science ®Google Scholar
• Nienhuis WA, Stienstra Y, Thompson WA, et al. Antimicrobial treatment for early, limited Mycobacterium ulcerans infection: a randomised controlled trial. Lancet. 2010;375(9715):664–672. doi:10.1016/S0140-6736(09)61962-020137805
   PubMed Web of Science ®Google Scholar
• Sarfo FS, Phillips R, Asiedu K, et al. Clinical efficacy of combination of rifampin and streptomycin for treatment of Mycobacterium ulcerans disease. Antimicrob Agents Chemother. 2010;54(9):3678–3685. doi:10.1128/AAC.00299-1020566765
   PubMed Web of Science ®Google Scholar
• Ruf M-T, Chauty A, Adeye A, et al. Secondary Buruli ulcer skin lesions emerging several months after completion of chemotherapy: paradoxical reaction or evidence for immune protection? PLoS Negl Trop Dis. 2011;5(8):e1252. doi:10.1371/journal.pntd.000137021829740
   PubMed Web of Science ®Google Scholar
• Sopoh GE, Dossou AD, Brun LV, et al. Severe multifocal form of Buruli ulcer after streptomycin and rifampin treatment: comments on possible dissemination mechanisms. Am J Trop Med Hyg. 2010;83(2):307–313. doi:10.4269/ajtmh.2010.09-061720682873
   PubMed Web of Science ®Google Scholar
• Gordon CL, Buntine JA, Hayman JA, et al. All-oral antibiotic treatment for buruli ulcer: a report of four patients. PLoS Negl Trop Dis. 2010;4(11):e770. doi:10.1371/journal.pntd.000077021152060
   PubMed Web of Science ®Google Scholar
• Jikia D, Chkhaidze N, Imedashvili E, et al. The use of a novel biodegradable preparation capable of the sustained release of bacteriophages and ciprofloxacin, in the complex treatment of multidrug‐resistant Staphylococcus aureus‐infected local radiation injuries caused by exposure to Sr90. Clin Exp Dermatol. 2005;30(1):23–26. doi:10.1111/j.1365-2230.2004.01600.x15663496
   PubMed Web of Science ®Google Scholar
• Gorski A. Bacteriophage penetration in vertebrates. J Appl Microbiol. 2005;98(1):7–13. doi:10.1111/j.1365-2672.2004.02422.x15610412
   PubMed Web of Science ®Google Scholar
• Mve-Obiang A, Lee RE, Portaels F, Small P. Heterogeneity of mycolactones produced by clinical isolates of Mycobacterium ulcerans: implications for virulence. Infect Immun. 2003;71(2):774–783. doi:10.1128/iai.71.2.774-783.200312540557
   PubMed Web of Science ®Google Scholar