The Korean Journal of Medicine

The Korean Association of Internal Medicine (대한내과학회)
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Immunopathogenesis of Non-Tuberculous Mycobacteria Lung Disease

비결핵항산균 폐질환의 면역 발병 기전

  • Jiwon Lyu (Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Soonchunhyang University Cheonan Hospital, Soonchunhyang University College of Medicine)
  • 류지원 (순천향대학교 의과대학 순천향대학교 천안병원 호흡기내과)
  • Received : 2024.07.11
  • Accepted : 2024.07.30
  • Published : 2024.08.01
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Abstract

In recent years, the incidence and prevalence of non-tuberculous mycobacteria lung disease (NTM-LD) has been increasing worldwide. In Korea, Mycobacterium avium complex (MAC) and Mycobacterium abscessus complex account for most common cause of NTM-LD. It is essential to elucidate the pathophysiology of NTM-LD. The pathophysiology of NTM-LD has not been fully understood, however, it can be divided into bacterial and host-side factor. Among the host factor, innate immunity plays an essential role in the initial host immune response against intracellular non-tuberculous mycobacteria (NTM), and adaptive immunity also has a role. However, the role of these immunity in mycobacterial disease has been mainly studied in tuberculosis, but studies on its role in NTM are limited. In this review, I focus on NTM innate and adaptive immunity, the role of macrophages and neutrophils, and host interaction in NTM infection.

Keywords

References

  1. Lee H, Myung W, Koh WJ, Moon SM, Jhun BW. Epidemiology of nontuberculous mycobacterial infection, South Korea, 2007-2016. Emerg Infect Dis 2019;25:569-572.
  2. Kwon YS, Koh WJ. Diagnosis and treatment of nontuberculous mycobacterial lung disease. J Korean Med Sci 2016;31:649-659.
  3. Matsuyama M, Matsumura S, Nonaka M, et al. Pathophysiology of pulmonary nontuberculous mycobacterial (NTM) disease. Respir Investig 2023;61:135-148.
  4. Abe Y, Fukushima K, Hosono Y, et al. Host immune response and novel diagnostic approach to NTM infections. Int J Mol Sci 2020;21:4351.
  5. Honda JR, Virdi R, Chan ED. Global environmental nontuberculous mycobacteria and their contemporaneous manmade and natural niches. Front Microbiol 2018;9:2029.
  6. Munoz-Egea MC, Akir A, Esteban J. Mycobacterium biofilms. Biofilm 2023;5:100107.
  7. DE Griffith. Pathogenesis of nontuberculous mycobacterial infections [Internet]. Waltham (MA): UpToDate, c2023 [cited 2024 Jul 10]. Available from: https://medilib.ir/uptodate/show/5345.
  8. Sousa S, Bandeira M, Carvalho PA, Duarte A, Jordao L. Nontuberculous mycobacteria pathogenesis and biofilm assembly. Int J Mycobacteriol 2015;4:36-43.
  9. Zamora N, Esteban J, Kinnari TJ, Celdran A, Granizo JJ, Zafra C. In-vitro evaluation of the adhesion to polypropylene sutures of non-pigmented, rapidly growing mycobacteria. Clin Microbiol Infect 2007;13:902-907.
  10. Schorey JS, Sweet L. The mycobacterial glycopeptidolipids: structure, function, and their role in pathogenesis. Glycobiology 2008;18:832-841.
  11. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2004;2:95-108.
  12. Rhoades ER, Archambault AS, Greendyke R, Hsu FF, Streeter C, Byrd TF. Mycobacterium abscessus glycopeptidolipids mask underlying cell wall phosphatidyl-myo-inositol mannosides blocking induction of human macrophage TNF-alpha by preventing interaction with TLR2. J Immunol 2009;183:1997-2007.
  13. Rodriguez-Sevilla G, Garcia-Coca M, Romera-Garcia D, et al. Non-tuberculous Mycobacteria multispecies biofilms in cystic fibrosis: development of an in vitro Mycobacterium abscessus and Pseudomonas aeruginosa dual species biofilm model. Int J Med Microbiol 2018;308:413-423.
  14. Rodriguez-Sevilla G, Crabbe A, Garcia-Coca M, AguileraCorrea JJ, Esteban J, Perez-Jorge C. Antimicrobial treatment provides a competitive advantage to Mycobacterium abscessus in a dual-species biofilm with Pseudomonas aeruginosa. Antimicrob Agents Chemother 2019;63:e01547-19.
  15. Honda JR, Knight V, Chan ED. Pathogenesis and risk factors for nontuberculous mycobacterial lung disease. Clin Chest Med 2015;36:1-11.
  16. Puzo G. The carbohydrate- and lipid-containing cell wall of mycobacteria, phenolic glycolipids: structure and immunological properties. Crit Rev Microbiol 1990;17:305-327.
  17. Tran T, Bonham AJ, Chan ED, Honda JR. A paucity of knowledge regarding nontuberculous mycobacterial lipids compared to the tubercle bacillus. Tuberculosis (Edinb) 2019;115:96-107.
  18. Maeda N, Nigou J, Herrmann JL, et al. The cell surface receptor DC-SIGN discriminates between Mycobacterium species through selective recognition of the mannose caps on lipoarabinomannan. J Biol Chem 2003;278:5513-5516.
  19. Vignal C, Guerardel Y, Kremer L, et al. Lipomannans, but not lipoarabinomannans, purified from Mycobacterium chelonae and Mycobacterium kansasii induce TNF-alpha and IL-8 secretion by a CD14-toll-like receptor 2-dependent mechanism. J Immunol 2003;171:2014-2023.
  20. Wieland CW, Knapp S, Florquin S, et al. Non-mannose-capped lipoarabinomannan induces lung inflammation via toll-like receptor 2. Am J Respir Crit Care Med 2004;170:1367-1374.
  21. Freeman R, Geier H, Weigel KM, Do J, Ford TE, Cangelosi GA. Roles for cell wall glycopeptidolipid in surface adherence and planktonic dispersal of Mycobacterium avium. Appl Environ Microbiol 2006;72:7554-7558.
  22. Byrd TF, Lyons CR. Preliminary characterization of a Mycobacterium abscessus mutant in human and murine models of infection. Infect Immun 1999;67:4700-4707.
  23. Sanguinetti M, Ardito F, Fiscarelli E, et al. Fatal pulmonary infection due to multidrug-resistant Mycobacterium abscessus in a patient with cystic fibrosis. J Clin Microbiol 2001;39:816-819.
  24. Torrelles JB, Ellis D, Osborne T, et al. Characterization of virulence, colony morphotype and the glycopeptidolipid of Mycobacterium avium strain 104. Tuberculosis (Edinb) 2002;82:293-300.
  25. Pedrosa J, Florido M, Kunze ZM, et al. Characterization of the virulence of Mycobacterium avium complex (MAC) isolates in mice. Clin Exp Immunol 1994;98:210-216.
  26. Schaefer WB, Davis CL, Cohn ML. Pathogenicity of transparent, opaque, and rough variants of Mycobacterium avium in chickens and mice. Am Rev Respir Dis 1970;102:499-506.
  27. Nishimura T, Shimoda M, Tamizu E, et al. The rough colony morphotype of Mycobacterium avium exhibits high virulence in human macrophages and mice. J Med Microbiol 2020;69:1020-1033.
  28. Sweet L, Schorey JS. Glycopeptidolipids from Mycobacterium avium promote macrophage activation in a TLR2- and MyD88-dependent manner. J Leukoc Biol 2006;80:415-423.
  29. Takegaki Y. Effect of serotype specific glycopeptidolipid (GPL) isolated from Mycobacterium avium complex (MAC) on phagocytosis and phagosome-lysosome fusion of human peripheral blood monocytes. Kekkaku 2000;75:9-18.
  30. Cebula BR, Rocco JM, Maslow JN, Irani VR. Mycobacterium avium serovars 2 and 8 infections elicit unique activation of the host macrophage immune responses. Eur J Clin Microbiol Infect Dis 2012;31:3407-3412.
  31. McGarvey J, Bermudez LE. Pathogenesis of nontuberculous mycobacteria infections. Clin Chest Med 2002;23:569-583.
  32. Bermudez LE, Goodman J. Mycobacterium tuberculosis invades and replicates within type II alveolar cells. Infect Immun 1996;64:1400-1406.
  33. Lin Y, Zhang M, Barnes PF. Chemokine production by a human alveolar epithelial cell line in response to Mycobacterium tuberculosis. Infect Immun 1998;66:1121-1126.
  34. Abbas AK, Lichtman AH, Pillai S. 김평형, 박석래, 유제욱, 윤지희, 이기종, 장용석 역. 핵심면역학. 6판. 서울: 법문에듀케이션, 2020.
  35. Awuh JA, Flo TH. Molecular basis of mycobacterial survival in macrophages. Cell Mol Life Sci 2017;74:1625-1648.
  36. Gordon S. Phagocytosis: an immunobiologic process. Immunity 2016;44:463-475.
  37. Shamaei M, Mirsaeidi M. Nontuberculous Mycobacteria, macrophages, and host innate immune response. Infect Immun 2021;89:e0081220.
  38. Shin DM, Yang CS, Yuk JM, et al. Mycobacterium abscessus activates the macrophage innate immune response via a physical and functional interaction between TLR2 and dectin-1. Cell Microbiol 2008;10:1608-1621.
  39. Kerscher B, Willment JA, Brown GD. The dectin-2 family of C-type lectin-like receptors: an update. Int Immunol 2013;25:271-277.
  40. Yonekawa A, Saijo S, Hoshino Y, et al. Dectin-2 is a direct receptor for mannose-capped lipoarabinomannan of mycobacteria. Immunity 2014;41:402-413.
  41. Kleinnijenhuis J, Oosting M, Joosten LA, Netea MG, Van Crevel R. Innate immune recognition of Mycobacterium tuberculosis. Clin Dev Immunol 2011;2011:405310.
  42. Yu X, Zeng J, Xie J. Navigating through the maze of TLR2 mediated signaling network for better mycobacterium infection control. Biochimie 2014;102:1-8.
  43. Sampaio EP, Elloumi HZ, Zelazny A, et al. Mycobacterium abscessus and M. avium trigger Toll-like receptor 2 and distinct cytokine response in human cells. Am J Respir Cell Mol Biol 2008;39:431-439.
  44. Lee SJ, Noh KT, Kang TH, et al. The Mycobacterium avium subsp. Paratuberculosis protein MAP1305 modulates dendritic cell-mediated T cell proliferation through Toll-like receptor-4. BMB Rep 2014;47:115-120.
  45. Lee SJ, Shin SJ, Lee SJ, et al. Mycobacterium abscessus MAB2560 induces maturation of dendritic cells via Toll-like receptor 4 and drives Th1 immune response. BMB Rep 2014;47:512-517.
  46. Shimada K, Takimoto H, Yano I, Kumazawa Y. Involvement of mannose receptor in glycopeptidolipid-mediated inhibition of phagosome-lysosome fusion. Microbiol Immunol 2006;50:243-251.
  47. Kano H, Doi T, Fujita Y, Takimoto H, Yano I, Kumazawa Y. Serotype-specific modulation of human monocyte functions by glycopeptidolipid (GPL) isolated from Mycobacterium avium complex. Biol Pharm Bull 2005;28:335-339.
  48. Roux AL, Viljoen A, Bah A, et al. The distinct fate of smooth and rough Mycobacterium abscessus variants inside macrophages. Open Biol 2016;6:160185.
  49. Sia JK, Rengarajan J. Immunology of Mycobacterium tuberculosis Infections. Microbiol Spectr 2019;7:10.1128/microbiolspec.gpp3-0022-2018.
  50. Martin CJ, Booty MG, Rosebrock TR, et al. Efferocytosis is an innate antibacterial mechanism. Cell Host Microbe 2012;12:289-300.
  51. Chen M, Gan H, Remold HG. A mechanism of virulence: virulent Mycobacterium tuberculosis strain H37Rv, but not attenuated H37Ra, causes significant mitochondrial inner membrane disruption in macrophages leading to necrosis. J Immunol 2006;176:3707-3716.
  52. Behar SM, Divangahi M, Remold HG. Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat Rev Microbiol 2010;8:668-674.
  53. Early J, Fischer K, Bermudez LE. Mycobacterium avium uses apoptotic macrophages as tools for spreading. Microb Pathog 2011;50:132-139.
  54. Helguera-Repetto AC, Chacon-Salinas R, Cerna-Cortes JF, et al. Differential macrophage response to slow- and fast-growing pathogenic mycobacteria. Biomed Res Int 2014;2014:916521.
  55. Appelberg R, Pedrosa JM, Silva MT. Host and bacterial factors control the Mycobacterium avium-induced chronic peritoneal granulocytosis in mice. Clin Exp Immunol 1991;83:231-236. 
  56. Petrofsky M, Bermudez LE. Neutrophils from Mycobacterium avium-infected mice produce TNF-alpha, IL-12, and IL-1 beta and have a putative role in early host response. Clin Immunol 1999;91:354-358.
  57. Bermudez LE, Petrofsky M, Stevens P. Treatment with recombinant granulocyte colony-stimulating factor (filgrastin) stimulates neutrophils and tissue macrophages and induces an effective non-specific response against Mycobacterium avium in mice. Immunology 1998;94:297-303.
  58. Appelberg R, Castro AG, Pedrosa J, Silva RA, Orme IM, Minoprio P. Role of gamma interferon and tumor necrosis factor alpha during T-cell-independent and -dependent phases of Mycobacterium avium infection. Infect Immun 1994;62:3962-3971.
  59. Kato T, Hakamada R, Yamane H, Nariuchi H. Induction of IL-12 p40 messenger RNA expression and IL-12 production of macrophages via CD40-CD40 ligand interaction. J Immunol 1996;156:3932-3938.
  60. Altare F, Durandy A, Lammas D, et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 1998;280:1432-1435.
  61. Dorman SE, Holland SM. Mutation in the signal-transducing chain of the interferon-gamma receptor and susceptibility to mycobacterial infection. J Clin Invest 1998;101:2364-2369.
  62. Florido M, Appelberg R. Characterization of the deregulated immune activation occurring at late stages of mycobacterial infection in TNF-deficient mice. J Immunol 2007; 179:7702-7708.
  63. Winthrop KL, Baxter R, Liu L, et al. Mycobacterial diseases and antitumour necrosis factor therapy in USA. Ann Rheum Dis 2013;72:37-42.
  64. Lim A, Allison C, Price P, Waterer G. Susceptibility to pulmonary disease due to Mycobacterium avium-intracellulare complex may reflect low IL-17 and high IL-10 responses rather than Th1 deficiency. Clin Immunol 2010;137:296-302.
  65. Kim SY, Koh WJ, Kim YH, et al. Importance of reciprocal balance of T cell immunity in Mycobacterium abscessus complex lung disease. PLoS One 2014;9:e109941.
  66. Wu UI, Olivier KN, Kuhns DB, et al. Patients with idiopathic pulmonary nontuberculous mycobacterial disease have normal Th1/Th2 cytokine responses but diminished Th17 cytokine and enhanced granulocyte-macrophage colony-stimulating factor production. Open Forum Infect Dis 2019;6:ofz484.
  67. Ratnatunga CN, Lutzky VP, Kupz A, et al. The rise of non-tuberculosis mycobacterial lung disease. Front Immunol 2020;11:303.
  68. Greinert U, Schlaak M, Rusch-Gerdes S, Flad HD, Ernst M. Low in vitro production of interferon-gamma and tumor necrosis factor-alpha in HIV-seronegative patients with pulmonary disease caused by nontuberculous mycobacteria. J Clin Immunol 2000;20:445-452.
  69. Tsuyuguchi I, Kawasumi H, Takashima T, Tsuyuguchi T, Kishimoto S. Mycobacterium avium-Mycobacterium intracellular complex-induced suppression of T-cell proliferation in vitro by regulation of monocyte accessory cell activity. Infect Immun 1990;58:1369-1378.
  70. Bermudez LE, Petrofsky M. Host defense against Mycobacterium avium does not have an absolute requirement for major histocompatibility complex class I-restricted T cells. Infect Immun 1999;67:3108-3111.
  71. Gilbertson B, Zhong J, Cheers C. Anergy, IFN-gamma production, and apoptosis in terminal infection of mice with Mycobacterium avium. J Immunol 1999;163:2073-2080.