2018 / 03

Следующая статья
DOI: 10.24075/vrgmu.2018.036

МНЕНИЕ

Лимфоциты TH1: корреляты протекции или маркеры активности туберкулезной инфекции?

И. В. Лядова, А. В. Пантелеев, И. Ю. Никитина, Т. В. Радаева
Информация об авторах

Лаборатория биотехнологии, Центральный научно-исследовательский институт туберкулеза, Москва

Для корреспонденции: Ирина Владимировна Лядова
Яузская аллея, д. 2, г. Москва, 107564; ur.liam@avodaylvi

Информация о статье

Финансирование: исследование выполнено в рамках темы НИР ФГБНУ «ЦНИИТ» 0515-2015-0010 «Иммунологические методы в диагностике туберкулеза легких».

Статья получена: 29.05.2018 Статья принята к печати: 25.07.2018 Опубликовано online: 21.08.2018
|
  1. Нечаева О. Б. Эпидемическая ситуация по туберкулезу в России в 2016 году. Отчет. М.: Федеральный Центр мониторинга противодействия распространению туберкулеза. 2017. 69 с.
  2. Flynn JL, Chan J. Immunology of tuberculosis. Ann Rev Immunol. 2001; 19: 93–129.
  3. North RJ, Jung YJ. Immunity to tuberculosis. Annu Rev Immunol. 2004; 22: 599–623.
  4. Kaufmann SH, Tuberculosis: back on the immunologists' agenda. Immunity. 2006; 24 (4): 351–7.
  5. Cooper AM, Khader SA. The role of cytokines in the initiation, expansion, and control of cellular immunity to tuberculosis. Immunol. Rev. 2008; 226: 191–204.
  6. Lyadova IV. Inflammation and Immunopathogenesis of Tuberculosis Progression. In: Pere-Joan Cardona, еditor. Understanding Tuberculosis — Analyzing the Origin of Mycobacterium Tuberculosis Pathogenicity. InTech; 2012: 19–42. Available from: http://www.intechopen.com/books/understanding-tuberculosis-analyzing-the-origin-of-mycobacterium-tuberculosis-pathogenicity.
  7. Lyadova IV, Panteleev AV. Th1 and Th17 Cells in Tuberculosis: Protection, Pathology, and Biomarkers. Mediators Inflamm. 2015; ID 854507.
  8. Gallant JE, Ko AH, Joel E. Cavitary pulmonary lesions in patients infected with human immunodeficiency virus. Clin Infect Dis. 1996; 22: 671–82.
  9. Müller I, Cobbold SP, Waldmann H, Kaufmann SH. Impaired resistance to Mycobacterium tuberculosis infection after selective in vivo depletion of L3T4+ and Lyt-2+ T cells. Infect Immun. 1987; 55 (9): 2037–41.
  10. Saunders BM, Cheers C. Inflammatory response following intranasal infection with Mycobacterium avium complex: role of T-cell subsets and gamma interferon. Infect Immun. 1995; 63 (6): 2282–87.
  11. Ladel CH, Daugelat S, Kaufmann SH. Immune response to Mycobacterium bovis bacille Calmette Guérin infection in major histocompatibility complex class I- and II-deficient knock-out mice: contribution of CD4 and CD8 T cells to acquired resistance. Eur J Immunol. 1995; 25 (2): 377–84.
  12. Flory CM, Hubbard RD, Collins FM. Effects of in vivo T lymphocyte subset depletion on mycobacterial infections in mice. J Leukoc Biol. 1992; 51 (3): 225–9.
  13. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med. 1993; 178 (6): 2243–47.
  14. Flynn JL. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med. 1993; 178 (6): 2249–54.
  15. Kamijo R, Le J, Shapiro D, Havell EA, Huang S, Aguet M, et al. Mice that lack the interferon-gamma receptor have profoundly altered responses to infection with Bacillus Calmette-Guérin and subsequent challenge with lipopolysaccharide. J Exp Med. 1993; 178 (4): 1435–40.
  16. Flynn JL, Goldstein MM, Chan J, Triebold KJ, Pfeffer K, Lowenstein CJ, et al. Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity. 1995; 2 (6): 561–72.
  17. MacMicking JD, North RJ, LaCourse R, Mudgett JS, Shah SK, Nathan CF. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc Natl Acad Sci USA. 1997; 94 (10): 5243–8.
  18. Cooper AM, Segal BH, Frank AA, Holland SM, Orme IM. Transient loss of resistance to pulmonary tuberculosis in p47(phox-/-) mice. Infect Immun. 2000; 68 (3): 1231–4.
  19. Jung Y-J, LaCourse R, Ryan L, North RJ. Virulent but not avirulent Mycobacterium tuberculosis can evade the growth inhibitory action of a T helper 1-dependent, nitric oxide Synthase 2-independent defense in mice. J Exp Med. 2002; 196 (7): 991–8.
  20. Scanga CA, Mohan VP, Tanaka K, Alland D, Flynn JL, Chan J. The inducible nitric oxide synthase locus confers protection against aerogenic challenge of both clinical and laboratory strains of Mycobacterium tuberculosis in mice. Infect Immun. 2001; 69 (12): 7711–7.
  21. de Jong R, Altare F, Haagen IA, Elferink DG, Boer T, van Breda Vriesman PJ, et al. Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science. 1998; 280 (5368): 1435–8.
  22. Jouanguy E, Lamhamedi-Cherradi S, Lammas D, Dorman SE, Fondanèche MC, Dupuis S, et al. A human IFNGR1 small deletion hotspot associated with dominant susceptibility to mycobacterial infection. Nat Genet. 1999; 21 (4): 370–8.
  23. Dorman SE, Holland SM. Interferon-gamma and interleukin-12 pathway defects and human disease. Cytokine Growth Factor Rev. 2000; 11 (4): 321–33.
  24. Newport M. The genetics of nontuberculous mycobacterial infection. Expert Rev Mol Med. 2003; 5 (6): 1–13.
  25. Hambleton S, Salem S, Bustamante J, Bigley V, Boisson-Dupuis S, Azevedo J, et al. IRF8 Mutations and Human Dendritic-Cell Immunodeficiency. N Engl J Med. 2011; 365 (2): 127–38.
  26. Lee WI, Huang JL, Yeh KW, Jaing TH, Lin TY, Huang YC, et al. Immune defects in active mycobacterial diseases in patients with primary immunodeficiency diseases (PIDs). J Formos Med Assoc. 2011; 110 (12): 750–8.
  27. Bogunovic D, Byun M, Durfee LA, Abhyankar A, Sanal O, Mansouri D, et al. Mycobacterial disease and impaired IFN-γ immunity in humans with inherited ISG15 deficiency. Science. 2012; 337 (6102): 1684–8.
  28. Khan TA, Schimke LF, Amaral EP, Ishfaq M, Barbosa Bonfim CC, Rahman H, et al. Interferon-gamma reduces the proliferation of M. tuberculosis within macrophages from a patient with a novel hypomorphic NEMO mutation. Pediatr Blood Cancer. 2016; 63 (10): 1863–6.
  29. Bustamante J, Boisson-Dupuis S, Abel L, Casanova J-L. Mendelian susceptibility to mycobacterial disease: Genetic, immunological, and clinical features of inborn errors of IFN-γ immunity. Semin Immunol. 2014; 26 (6): 454–70.
  30. Harris J, Keane J. How tumour necrosis factor blockers interfere with tuberculosis immunity. Clin Exp Immunol. 2010; 161(1): 1–9.
  31. Salgado E, Gómez-Reino JJ. The risk of tuberculosis in patients treated with TNF antagonists. Expert Rev Clin Immunol. 2011; 7 (3): 329–40.
  32. Rose RM, Fuglestad JM, Remington L. Growth Inhibition of Mycobacterium avium Complex in Human Alveolar Macrophages by the Combination of Recombinant Macrophage Colony-stimulating Factor and Interferon-gamma. Am J Respir Cell Mol Biol. 1991; 4 (3): 248–54.
  33. Byrd TF. Multinucleated giant cell formation induced by IFN-gamma/IL-3 is associated with restriction of virulent Mycobacterium tuberculosis cell to cell invasion in human monocyte monolayers. Cell Immunol. 1998; 188 (2): 89–96.
  34. Schaible UE, Sturgill-Koszycki S, Schlesinger PH, Russell DG. Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J Immunol. 1998; 160 (3): 1290–6.
  35. Flesch IE, Kaufmann SH. Attempts to characterize the mechanisms involved in mycobacterial growth inhibition by gamma-interferon-activated bone marrow macrophages. Infect. Immun. 1988; 56 (6): 1464–9.
  36. Chan J, Xing Y, Magliozzo RS, Bloom BR. Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 1992. 175 (4): 1111–22.
  37. Yu K, Mitchell C, Xing Y, Magliozzo RS, Bloom BR, Chan J. Toxicity of nitrogen oxides and related oxidants on mycobacteria: M. tuberculosis is resistant to peroxynitrite anion. Tuber Lung Dis. 1999; 79 (4): 191–8.
  38. Majlessi L, Simsova M, Jarvis Z, Brodin P, Rojas M-J, Bauche C, et al. An increase in antimycobacterial Th1-cell responses by prime-boost protocols of immunization does not enhance protection against tuberculosis. Infect Immun. 2006; 74 (4): 2128–37.
  39. Mittrücker H-W, Steinhoff U, Köhler A, Krause M, Lazar D, Mex P, et al. Poor correlation between BCG vaccination-induced T cell responses and protection against tuberculosis. Proc Natl Acad Sci USA. 2007; 104 (30): 12434–9.
  40. Cowley C, Elkins KL. CD4+ T cells mediate IFN-γ-independent control of Mycobacterium tuberculosis infection both in vitro and in vivo. J Immunol. 2003; 171 (9): 4689–99.
  41. Gallegos AM, van Heijst JW, Samstein M, et al., A gamma interferon independent mechanism of CD4 T cell mediated control of M. tuberculosis infection in vivo. PLoS Pathog, 2011; 7 (5): e1002052.
  42. Nandi B, Behar SM. Regulation of neutrophils by interferon-γ limits lung inflammation during tuberculosis infection. J Exp Med. 2011; 208 (11): 2251–62.
  43. Barber DL, Mayer-Barber KD, Feng CG, Sharpe AH, Sher A. CD4 T Cells Promote Rather than Control Tuberculosis in the Absence of PD-1-Mediated Inhibition. J Immunol. 2011; 186 (3): 1598– 607.
  44. Sakai S, Kauffman KD, Sallin MA, Sharpe AH, Young HA, Ganusov VV, et al. CD4 T Cell-Derived IFN-γ Plays a Minimal Role in Control of Pulmonary Mycobacterium tuberculosis Infection and Must Be Actively Repressed by PD-1 to Prevent Lethal Disease. PLoS Pathog. 2016; 12 (5): e1005667.
  45. Rook GA, Steele J, Ainsworth M, Champion BR. Activation of macrophages to inhibit proliferation of Mycobacterium tuberculosis: comparison of the effects of recombinant gamma-interferon on human monocytes and murine peritoneal macrophages. Immunology. 1986; 59 (3): 333–8.
  46. Bermudez LE. Differential mechanisms of intracellular killing of Mycobacterium avium and Listeria monocytogenes by activated human and murine macrophages. The role of nitric oxide. Clin Exp Immunol. 1993; 91 (2): 277–81.
  47. Meyer CG, Intemann CD, Förster B, Owusu-Dabo E, Franke A, Horstmann RD, Thye T. No significant impact of IFN-γ pathway gene variants on tuberculosis susceptibility in a West African population. Eur J Hum Genet. 2016; 24 (5): 748–55.
  48. Sahiratmadja E, Alisjahbana B, de Boer T, Adnan I, Maya A, Danusantoso H, et al. Dynamic changes in pro- and anti-inflammatory cytokine profiles and gamma interferon receptor signaling integrity correlate with tuberculosis disease activity and response to curative treatment. Infect Immun. 2007; 75 (2): 820–9.
  49. Hirsch CS, Toossi Z, Othieno C, Johnson JL, Schwander SK, Robertson S, et al. Depressed T‐Cell Interferon‐γ Responses in Pulmonary Tuberculosis: Analysis of Underlying Mechanisms and Modulation with Therapy. J Infect Dis. 1999; 180 (6): 2069–73.
  50. Hasan Z, Jamil B, Ashraf M, Islam M, Dojki M, Irfan M, et al. Differential live Mycobacterium tuberculosis-, M. bovis BCG-, recombinant ESAT6-, and culture filtrate protein 10-induced immunity in tuberculosis. Clin Vaccine Immunol. 2009; 16 (7): 991–8.
  51. Martinez V, Carcelain G, Badell E, Jouan M, Mauger I, Sellier P, et al. T-cell and serological responses to Erp, an exported Mycobacterium tuberculosis protein, in tuberculosis patients and healthy individuals. BMC Infect Dis. 2007; 7: 83.
  52. Rueda CM, Marín ND, García LF, Rojas M. Characterization of CD4 and CD8 T cells producing IFN-γ in human latent and active tuberculosis. Tuberculosis (Edinb). 2010; 90 (6): 346–53.
  53. Morosini M, Meloni F, Marone Bianco A, Paschetto E, Uccelli M, Pozzi E, et al. The assessment of IFN-gamma and its regulatory cytokines in the plasma and bronchoalveolar lavage fluid of patients with active pulmonary tuberculosis. Int J Tuberc Lung Dis. 2003; 7 (10): 994–1000.
  54. Verbon A, Juffermans N, Van Deventer SJH, Speelman P, Van Deutekom H, Van Der Poll T. Serum concentrations of cytokines in patients with active tuberculosis (TB) and after treatment. Clin Exp Immunol. 1999; 115 (1): 110–3.
  55. Sahiratmadja E, Alisjahbana B, Buccheri S, Di Liberto D, de Boer T, Adnan I, et al. Plasma granulysin levels and cellular interferon-gamma production correlate with curative host responses in tuberculosis, while plasma interferon-gamma levels correlate with tuberculosis disease activity in adults. Tuberculosis (Edinb). 2007; 87 (4): 312–21.
  56. Nikitina IY, Panteleev A V., Sosunova E V., Karpina NL, Bagdasarian TR, Burmistrova IA, et al. Antigen-Specific IFN-γ Responses Correlate with the Activity of M. tuberculosis Infection but Are Not Associated with the Severity of Tuberculosis Disease. J Immunol Res. 2016; 2016 (Recent Advances in the Host Immunity to Mycobacterium tuberculosis Infection): 1–9.
  57. Panteleev AV, Nikitina IY, Burmistrova IA, Kosmiadi GA, Radaeva TV, Amansahedov RB, et al. Severe Tuberculosis in Humans Correlates Best with Neutrophil Abundance and Lymphocyte Deficiency and Does Not Correlate with Antigen- Specific CD4 T-Cell Response. Front Immunol. 2017; 8: 1–16.
  58. Tan Q, Xie WP, Min R, Dai GQ, Xu CC, Pan HQ, et al. Characterization of Th1- and Th2-type immune response in human multidrug-resistant tuberculosis. Eur J Clin Microbiol Infect Dis. 2012; 31 (6): 1233–42.
  59. Kagina BMN, Abel B, Scriba TJ, Hughes EJ, Keyser A, Soares A, et al. Specific T cell frequency and cytokine expression profile do not correlate with protection against tuberculosis after bacillus Calmette-Guérin vaccination of newborns. Am J Respir Crit Care Med. 2010; 182 (8): 1073–9.
  60. Umemura M, Yahagi A, Hamada S, Begum MD, Watanabe H, Kawakami K, et al. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J Immunol. 2007; 178 (6): 3786–96.
  61. Gopal R, Lin Y, Obermajer N, Slight S, Nuthalapati N, Ahmed M, Kalinski P, Khader SA. IL-23-dependent IL-17 drives Th1-cell responses following Mycobacterium bovis BCG vaccination. Eur J Immunol. 2012; 42 (2): 364–73.
  62. Khader SA, Bell GK, Pearl JE, Fountain JJ, Rangel-Moreno J, Cilley GE, Shen F, Eaton SM, Gaffen SL, Swain SL, Locksley RM, Haynes L, Randall TD, Cooper AM. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol. 2007; 8 (4): 369–77.
  63. Griffiths KL, Pathan AA, Minassian AM, Sander CR, Beveridge NER, Hill AVS, Fletcher HA, McShane H. Th1/Th17 Cell Induction and Corresponding Reduction in ATP Consumption following Vaccination with the Novel Mycobacterium tuberculosis Vaccine MVA85A. PLoS One. 2011; 6 (8): e23463.
  64. Arlehamn CL, Seumois G, Gerasimova A, Huang C, Fu Z, Yue X, et al. Transcriptional profile of tuberculosis antigen-specific T cells reveals novel multifunctional features. J Immunol. 2014; 193 (6): 2931–40.
  65. Strickland N, Müller TL, Berkowitz N, Goliath R, Carrington MN, Wilkinson RJ, et al. Characterization of Mycobacterium tuberculosis-Specific Cells Using MHC Class II Tetramers Reveals Phenotypic Differences Related to HIV Infection and Tuberculosis Disease. J Immunol. 2017; 199 (7): 2440–50.
  66. Nikitina IY, Panteleev AV, Kosmiadi GA, Serdyuk YV, Nenasheva TA, Nikolaev AA, et al. Th1, Th17, and Th1Th17 Lymphocytes during Tuberculosis: Th1 Lymphocytes Predominate and Appear as Low- Differentiated CXCR3 + CCR6 + Cells in the Blood and Highly Differentiated CXCR3 +/− CCR6 − Cells in the Lung. J Immunol. 2018; 200 (6): 2090–103.