Mycobacterium tuberculosis Biofilms: Immune Responses, Role in TB Pathology, and Potential Treatment

References

• Ogodo AC, Tatah VS, Ebuara FU, Ogodo CF. Therapeutic potentials of phytochemicals against Mycobacterium tuberculosis, the causative agent of tuberculosis. In: Neglected Tropical Diseases and Phytochemicals in Drug Discovery. Wiley Online Library; 2021:543–569.
   Google Scholar
• Organisation WH. Tuberculosis deaths and disease increase during the COVID-19 pandemic 2022; 2022. Available from: https://www.who.int/news/item/27-10-2022-tuberculosis-deaths-and-disease-increase-during-The-covid-19-pandemic. Accessed July 1, 2024.
   Google Scholar
• Chakaya J, Khan M, Ntoumi F, et al. Global tuberculosis report 2020–reflections on the global TB burden, treatment and prevention efforts. Int J Infect Dis. 2021;113:S7–S12. doi:10.1016/j.ijid.2021.02.107
   PubMed Web of Science ®Google Scholar
• Malik AA, Khan U, Khan P, et al. Drug-resistant tuberculosis treatment outcomes among children and adolescents in Karachi, Pakistan. Trop Med Infect Dis. 2022;7(12):418. doi:10.3390/tropicalmed7120418
   PubMedGoogle Scholar
• Ben-Kahla I, Sahal A-H. Drug-resistant tuberculosis viewed from bacterial and host genomes. Int J Antimicrob Agents. 2016;48(4):353–360. doi:10.1016/j.ijantimicag.2016.07.010
   PubMed Web of Science ®Google Scholar
• Costerton JW, Geesey GG, Cheng K-J. How bacteria stick. Sci Am. 1978;238(1):86–95. doi:10.1038/scientificamerican0178-86
   PubMed Web of Science ®Google Scholar
• Alberto Flores-Valdez M. Editorial from guest editor (thematic issue: current approaches and models to develop and evaluate new vaccines and drugs against tuberculosis). Curr Respir Med Rev. 2014;10(2):73. doi:10.2174/1573398X1002141114102626
   Google Scholar
• Niño-Padilla EI, Velazquez C, Garibay-Escobar A. Mycobacterial biofilms as players in human infections: a review. Biofouling. 2021;37(4):410–432. doi:10.1080/08927014.2021.1925886
   PubMed Web of Science ®Google Scholar
• Esteban J, García-Coca M. Mycobacterium biofilms. Front Microbiol. 2018;8:2651. doi:10.3389/fmicb.2017.02651
   PubMed Web of Science ®Google Scholar
• Chakraborty P, Kumar A. The extracellular matrix of mycobacterial biofilms: could we shorten the treatment of mycobacterial infections? Microb Cell. 2019;6(2):105. doi:10.15698/mic2019.02.667
   PubMed Web of Science ®Google Scholar
• Chaubey KK, Abdullah M, Gupta S, Navabharath M, Singh SV. Mycobacterium Biofilms Synthesis, Ultrastructure, and Their Perspectives in Drug Tolerance, Environment, and Medicine. Microbial Polymers: Springer; 2021:465–478.
   Google Scholar
• Richards JP, Ojha AK. Mycobacterial biofilms. Microbiol Spectr. 2014;2(5):2.5.16. doi:10.1128/microbiolspec.MGM2-0004-2013
   PubMedGoogle Scholar
• Sambandan D, Dao DN, Weinrick BC, et al. Keto-mycolic acid-dependent pellicle formation confers tolerance to drug-sensitive Mycobacterium tuberculosis. MBio. 2013;4(3):e00222–13. doi:10.1128/mBio.00222-13
   PubMed Web of Science ®Google Scholar
• Ackart DF, Hascall-Dove L, Caceres SM, et al. Expression of antimicrobial drug tolerance by attached communities of Mycobacterium tuberculosis. Pathog Dis. 2014a;70(3):359–369. doi:10.1111/2049-632X.12144
   PubMed Web of Science ®Google Scholar
• Trivedi A, Mavi PS, Bhatt D, Kumar A. Thiol reductive stress induces cellulose-anchored biofilm formation in Mycobacterium tuberculosis. Nat Commun. 2016;7(1):1–15. doi:10.1038/ncomms11392
   Google Scholar
• Richards JP, Cai W, Zill NA, Zhang W, Ojha AK. Adaptation of Mycobacterium tuberculosis to biofilm growth is genetically linked to drug tolerance. Antimicrob Agents Chemother. 2019;63(11):e01213–19. doi:10.1128/AAC.01213-19
   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.06304-11
   PubMed Web of Science ®Google Scholar
• Khawary M, Rakshit R, Bahl A, et al. M. tb-Rv2462c of Mycobacterium tuberculosis shows chaperone-like activity and plays a role in stress adaptation and immunomodulation. Biology. 2023;12(1):69. doi:10.3390/biology12010069
   Google Scholar
• Cholo MC, Rasehlo SS, Venter E, Venter C, Anderson R. Effects of cigarette smoke condensate on growth and biofilm formation by Mycobacterium tuberculosis. Biomed Res Int. 2020;2020:1–7. doi:10.1155/2020/8237402
   Web of Science ®Google Scholar
• Yang S, Sui S, Qin Y, et al. Protein O‐mannosyltransferase Rv1002c contributes to low cell permeability, biofilm formation in vitro, and mycobacterial survival in mice. APMIS. 2022;130(3):181–192. doi:10.1111/apm.13204
   PubMed Web of Science ®Google Scholar
• Chakraborty P, Bajeli S, Kaushal D, Radotra BD, Kumar A. Biofilm formation in the lung contributes to virulence and drug tolerance of Mycobacterium tuberculosis. Nat Commun. 2021;12(1):1606. doi:10.1038/s41467-021-21748-6
   PubMed Web of Science ®Google Scholar
• Hunter RL, Actor JK, Hwang S-A, Karev V, Jagannath C. Pathogenesis of post primary tuberculosis: immunity and hypersensitivity in the development of cavities. Ann Clin Lab Sci. 2014;44(4):365–387.
   PubMed Web of Science ®Google Scholar
• Fennelly KP, Jones-López EC. Quantity and quality of inhaled dose predicts immunopathology in tuberculosis. Front Immunol. 2015;6:313. doi:10.3389/fimmu.2015.00313
   PubMed Web of Science ®Google Scholar
• Orme IM. A new unifying theory of the pathogenesis of tuberculosis. Tuberculosis. 2014;94(1):8–14. doi:10.1016/j.tube.2013.07.004
   PubMed Web of Science ®Google Scholar
• Dalton JP, Uy B, Phummarin N, et al. Effect of common and experimental anti-tuberculosis treatments on Mycobacterium tuberculosis growing as biofilms. PeerJ. 2016;4:e2717. doi:10.7717/peerj.2717
   PubMed Web of Science ®Google Scholar
• Lenaerts AJ, Hoff D, Aly S, et al. Location of persisting mycobacteria in a Guinea pig model of tuberculosis revealed by r207910. Antimicrob Agents Chemother. 2007;51(9):3338–3345. doi:10.1128/AAC.00276-07
   PubMed Web of Science ®Google Scholar
• Hira P. Overview of Immune System. In: An Interplay of Cellular and Molecular Components of Immunology. CRC Press; 2022:1–26.
   Google Scholar
• Sia JK, Rengarajan J. Immunology of Mycobacterium tuberculosis infections. Microbiol Spectr. 2019;7(4):7.4.6.
   PubMed Web of Science ®Google Scholar
• Batoni G, Martinez-Pomares L, Esin S. Immune response to biofilms. Front Immunol. 2021;12:696356. doi:10.3389/fimmu.2021.696356
   PubMed Web of Science ®Google Scholar
• De Martino M, Lodi L, Galli L, Chiappini E. Immune response to Mycobacterium tuberculosis: a narrative review. Front Pediatr. 2019;7:350. doi:10.3389/fped.2019.00350
   PubMed Web of Science ®Google Scholar
• Kaya E, Grassi L, Benedetti A, et al. In vitro interaction of Pseudomonas aeruginosa biofilms with human peripheral blood mononuclear cells. Front Cell Infect Microbiol. 2020;10:187. doi:10.3389/fcimb.2020.00187
   PubMed Web of Science ®Google Scholar
• Gries CM, Rivas Z, Chen J, Lo DD. Intravital multiphoton examination of implant-associated Staphylococcus aureus biofilm infection. Front Cell Infect Microbiol. 2020;10:574092. doi:10.3389/fcimb.2020.574092
   PubMed Web of Science ®Google Scholar
• Weathered C, Pennington K, Escalante P, Pienaar E. The role of biofilms, bacterial phenotypes, and innate immune response in Mycobacterium avium colonization to infection. J Theor Biol. 2022;534:110949. doi:10.1016/j.jtbi.2021.110949
   PubMed Web of Science ®Google Scholar
• Bekier A, Kawka M, Lach J, et al. Imidazole-thiosemicarbazide derivatives as potent Anti-Mycobacterium tuberculosis compounds with antibiofilm activity. Cells. 2021;10(12):3476. doi:10.3390/cells10123476
   PubMed Web of Science ®Google Scholar
• Watters C, Fleming D, Bishop D, Rumbaugh K. Host responses to biofilm. Prog Mol Biol Transl Sci. 2016;142:193–239.
   PubMed Web of Science ®Google Scholar
• Eldholm V, Balloux F. Antimicrobial resistance in Mycobacterium tuberculosis: the odd one out. Trends Microbiol. 2016;24(8):637–648. doi:10.1016/j.tim.2016.03.007
   PubMed Web of Science ®Google Scholar
• Cai Y, Yang Q, Tang Y, et al. Increased complement C1q level marks active disease in human tuberculosis. PLoS One. 2014;9(3):e92340. doi:10.1371/journal.pone.0092340
   PubMed Web of Science ®Google Scholar
• Keating T, Lethbridge S, Allnutt JC, et al. Mycobacterium tuberculosis modifies cell wall carbohydrates during biofilm growth with a concomitant reduction in complement activation. Cell Surface. 2021;7:100065. doi:10.1016/j.tcsw.2021.100065
   PubMedGoogle Scholar
• Netea MG, Schlitzer A, Placek K, Joosten LA, Schultze JL. Innate and adaptive immune memory: an evolutionary continuum in the host’s response to pathogens. Cell Host Microbe. 2019;25(1):13–26. doi:10.1016/j.chom.2018.12.006
   PubMed Web of Science ®Google Scholar
• Moser C, Jensen PØ, Thomsen K, et al. Immune responses to Pseudomonas aeruginosa biofilm infections. Front Immunol. 2021;12:625597. doi:10.3389/fimmu.2021.625597
   PubMed Web of Science ®Google Scholar
• McDaniel MM, Meibers HE, Pasare C. Innate control of adaptive immunity and adaptive instruction of innate immunity: bi-directional flow of information. Curr Opin Immunol. 2021;73:25–33. doi:10.1016/j.coi.2021.07.013
   PubMed Web of Science ®Google Scholar
• Tebruegge M, Ritz N, Donath S, et al. Mycobacteria-specific mono- and polyfunctional CD4+ T cell profiles in children with latent and active tuberculosis: a prospective proof-of-concept study. Front Immunol. 2019;10:431. doi:10.3389/fimmu.2019.00431
   PubMed Web of Science ®Google Scholar
• Prezzemolo T, Guggino G, La Manna MP, Di Liberto D, Dieli F, Caccamo N. Functional signatures of human CD4 and CD8 T cell responses to Mycobacterium tuberculosis. Front Immunol. 2014;5:180. doi:10.3389/fimmu.2014.00180
   PubMed Web of Science ®Google Scholar
• Lu YJ, Barreira-Silva P, Boyce S, Powers J, Cavallo K, Behar SM. CD4 T cell help prevents CD8 T cell exhaustion and promotes control of Mycobacterium tuberculosis infection. Cell Rep. 2021;36(11):109696. doi:10.1016/j.celrep.2021.109696
   PubMed Web of Science ®Google Scholar
• Shang S, Siddiqui S, Bian Y, Zhao J, Wang CR. Nonclassical MHC Ib-restricted CD8+ T Cells recognize Mycobacterium tuberculosis-derived protein antigens and contribute to protection against infection. PLoS Pathog. 2016;12(6):e1005688. doi:10.1371/journal.ppat.1005688
   PubMed Web of Science ®Google Scholar
• Ocaña-Guzmán R, Téllez-Navarrete NA, Ramón-Luing LA, et al. Leukocytes from patients with drug-sensitive and multidrug-resistant tuberculosis exhibit distinctive profiles of chemokine receptor expression and migration capacity. J Immunol Res. 2021;2021:6654220. doi:10.1155/2021/6654220
   PubMed Web of Science ®Google Scholar
• Kudryavtsev I, Zinchenko Y, Serebriakova M, et al. A key role of CD8+ T cells in controlling of tuberculosis infection. Diagnostics. 2023;13(18):2961. doi:10.3390/diagnostics13182961
   Web of Science ®Google Scholar
• Segura-Cerda CA, de Jesús Aceves-Sánchez M, Marquina-Castillo B, et al. Immune response elicited by two rBCG strains devoid of genes involved in c-di-GMP metabolism affect protection versus challenge with M. tuberculosis strains of different virulence. Vaccine. 2018;36(16):2069–2078. doi:10.1016/j.vaccine.2018.03.014
   PubMed Web of Science ®Google Scholar
• Kozakiewicz L, Phuah J, Flynn J, Chan J. The role of B cells and humoral immunity in Mycobacterium tuberculosis infection. In: The New Paradigm of Immunity to Tuberculosis. Springer; 2013:225–250.
   Google Scholar
• Gil C, Solano C, Burgui S, et al. Biofilm matrix exoproteins induce a protective immune response against Staphylococcus aureus biofilm infection. Infect Immun. 2014;82(3):1017–1029. doi:10.1128/IAI.01419-13
   PubMed Web of Science ®Google Scholar
• Kerns PW. Development and Testing of a Five-Subunit Biofilm Vaccine for the Prevention of Pulmonary Tuberculosis. Baltimore: University of Maryland; 2014b.
   Google Scholar
• Mishra R, Hannebelle M, Patil VP, et al. Mechanopathology of biofilm-like Mycobacterium tuberculosis cords. Cell. 2023;186(23):5135–50.e28. doi:10.1016/j.cell.2023.09.016
   PubMed Web of Science ®Google Scholar
• Pedroza-Roldán C, Guapillo C, Barrios-Payán J, et al. The BCGΔBCG1419c strain, which produces more pellicle in vitro, improves control of chronic tuberculosis in vivo. Vaccine. 2016;34(40):4763–4770. doi:10.1016/j.vaccine.2016.08.035
   PubMed Web of Science ®Google Scholar
• Kerns PW, Ackhart DF, Basaraba RJ, Leid JG, Shirtliff ME. Mycobacterium tuberculosis pellicles express unique proteins recognized by the host humoral response. Pathog Dis. 2014a;70(3):347–358. doi:10.1111/2049-632X.12142
   PubMed Web of Science ®Google Scholar
• Oluyori AP, Rode HB. Mycobacterium tuberculosis biofilm inhibitors. Future Med Chem. 2022;14(4):203–205. doi:10.4155/fmc-2021-0281
   PubMed Web of Science ®Google Scholar
• Ramalingam V, Sundaramahalingam S, Rajaram R. Size-dependent antimycobacterial activity of titanium oxide nanoparticles against Mycobacterium tuberculosis. J Mat Chem B. 2019;7(27):4338–4346.
   Web of Science ®Google Scholar
• Kalera K, Liu R, Lim J, et al. Targeting Mycobacterium tuberculosis Persistence through Inhibition of the Trehalose Catalytic Shift. ACS Infect Dis. 2024;10(4):1391–1404. doi:10.1021/acsinfecdis.4c00138
   PubMed Web of Science ®Google Scholar
• Ma F, Zhou H, Yang Z, et al. Gene expression profile analysis and target gene discovery of Mycobacterium tuberculosis biofilm. Appl Microbiol Biotechnol. 2021;105(12):5123–5134. doi:10.1007/s00253-021-11361-4
   PubMed Web of Science ®Google Scholar
• Kumar R, Singh N, Chauhan A, Kumar M, Bhatta RS, Singh SK. Mycobacterium tuberculosis survival and biofilm formation studies: effect of d-amino acids, d-cycloserine and its components. J Antibiot. 2022;75(1):1–8. doi:10.1038/s41429-021-00483-6
   PubMedGoogle Scholar
• Mashele SA, Steel HC, Matjokotja MT, Rasehlo SS, Anderson R, Cholo MC. Assessment of the efficacy of clofazimine alone and in combination with primary agents against Mycobacterium tuberculosis in vitro. J Global Antimicrob Resist. 2022;29:343–352. doi:10.1016/j.jgar.2022.03.008
   PubMed Web of Science ®Google Scholar
• Jiang C-H, Gan M-L, An -T-T, Yang Z-C. Bioassay-guided isolation of a Mycobacterium tuberculosis biofilm inhibitor from Arisaema sinii Krause. Microb Pathog. 2019;126:351–356. doi:10.1016/j.micpath.2018.11.022
   PubMed Web of Science ®Google Scholar
• Kumar A, Alam A, Grover S, et al. Peptidyl-prolyl isomerase-B is involved in Mycobacterium tuberculosis biofilm formation and a generic target for drug repurposing-based intervention. NPJ Biofilms Microbiomes. 2019;5(1):1–11. doi:10.1038/s41522-018-0075-0
   PubMedGoogle Scholar
• Wang C, Zhang Q, Tang X, et al. Effects of CwlM on autolysis and biofilm formation in Mycobacterium tuberculosis and Mycobacterium smegmatis. Int J Med Microbiol. 2019;309(1):73–83. doi:10.1016/j.ijmm.2018.12.002
   PubMed Web of Science ®Google Scholar
• Ackart DF, Lindsey EA, Podell BK, Melander RJ, Basaraba RJ, Melander C. Reversal of Mycobacterium tuberculosis phenotypic drug resistance by 2-aminoimidazole-based small molecules. Pathog Dis. 2014b;70(3):370–378. doi:10.1111/2049-632X.12143
   PubMed Web of Science ®Google Scholar
• Dalton JP, Uy B, Swift S, Wiles S Effect of ascorbic acid on Mycobacterium tuberculosis biofilms. PeerJ PrePrints; 2014.
   Google Scholar
• Wang F, Sambandan D, Halder R, et al. Identification of a small molecule with activity against drug-resistant and persistent tuberculosis. Proc Natl Acad Sci. 2013;110(27):E2510–E7.
   PubMed Web of Science ®Google Scholar
• Srivastava S, Dey S, Mukhopadhyay S. Vaccines against Tuberculosis: where are we now? Vaccines. 2023;11(5):1013. doi:10.3390/vaccines11051013
   Web of Science ®Google Scholar
• Loera-Muro A, Guerrero-Barrera A, Tremblay DNY, Hathroubi S, Angulo C. Bacterial biofilm-derived antigens: a new strategy for vaccine development against infectious diseases. Expert Rev Vaccines. 2021;20(4):385–396. doi:10.1080/14760584.2021.1892492
   PubMed Web of Science ®Google Scholar
• Kiran D, Podell BK, Chambers M, Basaraba RJ, editors. Host-directed therapy targeting the Mycobacterium tuberculosis granuloma: a review. In: Semin Immunopathol. Springer; 2016:167–183.
   Google Scholar
• Flores-Valdez MA. Vaccines directed against microorganisms or their products present during biofilm lifestyle: can we make a translation as a broad biological model to tuberculosis? Front Microbiol. 2016;7:14. doi:10.3389/fmicb.2016.00014
   PubMed Web of Science ®Google Scholar