The factors of dysregualtion of the immune response (at different stage of its implementation) in patients with pulmonary tuberculosis
https://doi.org/10.20538/1682-0363-2016-5-166-177
Abstract
The article provides an overview of scientific research to explain the mechanisms of inefficient implementation of antigen-specific immune response in patients with tuberculosis infection depending on the clinical form (infiltrative and disseminated pulmonary tuberculosis) and the course (drug-sensitive and drug-resistant pulmonary tuberculosis) of the disease. The mechanisms of immune imbalance in patients with pulmonary tuberculosis are associated with abnormal co-stimulation of a signal required for the activation of T-lymphocytes and immunosuppressive influence of regulatory T-cells both when they interact with dendritic cells at the inductive stage of the immune response, and in the process of differentiation and proliferation of effector cells with formation of suppressive mode of immune-regulation.
About the Authors
E. G. Churina
Siberian State Medical University;
National Research Tomsk State University (NR TSU)
Russian Federation
Russian Federation
MD, Associate Professor of the Department of Pathophysiology, 2, Moscow Trakt, Tomsk, 634050,
Professor of the Department of Organic Chemistry, 36, Lenina Av., Tomsk, 634050
O. I. Urazova
Siberian State Medical University
Russian Federation
Russian Federation
MD, Professor, Corresponding Member of RAS, Department of Pathophysiology,
2, Moscow Trakt, Tomsk, 634050
V. V. Novitskiy
Siberian State Medical University
Russian Federation
Russian Federation
MD, Professor, Academician of RAS, Honored Scientist of Russia, Head of Department of Pathophysiology,
2, Moscow Trakt, Tomsk, 634050
I. Ye. Yesimova
Siberian State Medical University
Russian Federation
Russian Federation
PhD, Associate Professor of the Department of Pathophysiology,
2, Moscow Trakt, Tomsk, 634050
T. Ye. Kononova
Siberian State Medical University
Russian Federation
Russian Federation
PhD, Associate Professor of the Department of Pathophysiology,
2, Moscow Trakt, Tomsk, 634050
O. V. Filinyuk
Siberian State Medical University
Russian Federation
Russian Federation
MD, Associate Professor, Head of the Department of Tuberculosis and Pulmonology,
2, Moscow Trakt, Tomsk, 634050
Yu. V. Kolobovnikova
Siberian State Medical University
Russian Federation
Russian Federation
MD, Professor of the Department of Pathophysiology,
2, Moscow Trakt, Tomsk, 634050
A. I. Dmitrieva
Siberian State Medical University
Russian Federation
Russian Federation
MD, Professor of the Department of Pathophysiology,
2, Moscow Trakt, Tomsk, 634050
References
1. Churina E.G., Urazova O.I., Novitskiy V.V., Esimova I.E. Vtorichnaya immunologicheskaya nedostatochnost’ u bol’nykh tuberkulezom legkikh. Immunodiagnostika i immunoterapiya [Secondary immune deficiency in patients with pulmonary tuberculosis. Immunodiagnostics and immunotherapy]. Tomsk: Pechatnaya manufaktura Publ., 2013: 84 (in Russian).
2. Churina E.G., Urazova O.I., Novitskiy V.V., Kononova T.E. Rol’ Gamma-Del’ta-T-kletok v immunnom otvete na Mycobacterium tuberculosis [Role of gamma delta T cells in the immune response to Mycobacterium tuberculosis] // Tuberkulez i bolezni legkikh – Tuberculosis and Lung Diseases.2014; 3: 59–63 (in Russian).
3. Caramori G., Lasagna L., Casalini A.G. et al. Immune response to Mycobacterium tuberculosis infection in the parietal pleura of patients with tuberculous pleurisy // PLoS One. 2011; 6 (7): e22637.
4. Churina E.G., Urazova O.I., Novitskiy V.V. Regulyatornyye T-kletki. Immunosupressornyye effekty pri tuberkuleze legkikh [Regulatory T-cells. Immunosuppressive effects of pulmonary
5. tuberculosis]. Saarbrucken, LAP LAMBERT Academic Pablishing, 2012: 169 (in Russian).
6. Churina E.G., Urazova O.I., Novitskiy V.V. Regulyatornyye T-kletki i protivotuberkuleznyy immunitet [Regulatory T-cells and anti-TB immunity]. Tomsk: Pechatnaya manufaktura Publ., 2014: 156
7. Churina E.G., Urazova O.I., Novitskiy V.V. The role of foxp3-expressing regulatory T-cells and T-helpers in immunopathogenesis of multidrug resistant pulmonary tuberculosis // Tuberc. Res. Treat. 2012; 2012. Article ID 931291: 9.
8. Yarilin А.А. Transkriptsionnyye regulyatory differentsirovki T-khelperov [Transcriptional regulators of differentiation of T-helper cells] // Immunologiya– Immunology. 2010; 31 (3): 152–166 (in Russian).
9. Yamazaki S., Morita A. Dendritic cells in the periphery control antigen-specific natural and induced regulatory T cells // Front. Immunol. 2013. Article ID 10.3389 / fimmu.2013. 00151: 13.
10. Khaitova Z.K., Urazova O.I., Voronkova O.V. i dr. Osobennosti immunofenotipa i tsitokinsekretornoy aktivnosti dendritnykh kletok u bol’nykh tuberkulezom legkikh [Features tsitokinsekretornoy immunophenotype and activity of dendritic cells in patients with pulmonary tuberculosis] // Fundamental’nyye issledovaniya – Fundamental Research. 2013; 9: 152–155 (in Russian).
11. Khaitova Z.K., Urazova O.I., Khasanova R.R. i dr. Osobennosti immunofenotipa dendritnykh kletok i T-limfotsitov u bol’nykh tuberkulezom legkikh [Features immunophenotype of dendritic cells and T-lymphocytes in patients with pulmonary tuberculosis] // Fundamental’nyye issledovaniya – Fundamental Research. 2012; 12: 386–390 (in Russian).
12. Khaitova Z.K., Khasanova R.R., Voronkova O.V. i dr. Rol’ dendritnykh kletok v protivotuberkuleznom immunitete [The role of dendritic cells in the TB immunity] //Rossiyskiy immunologicheskiy zhurnal – Russian Journal of Immunology. 2012; 6 (2): 119–123 (in Russian).
13. Druszczynska M., Wlodarczyk M., Janiszewska-Drobinska B. et al. Monocyte signal transduction receptors in active and latent tuberculosis // Clin. Dev. Immunol. 2013; 2013. Article ID 851452: 15.
14. Balboa L., Romero M.M., Yokobori N. et al. Mycobacterium tuberculosis impairs dendritic cell response by altering CD1b, DC-SIGN and MR profile // Immunol. Cell Biol. 2010; 88 (7): 716–726.
15. Geurtsen J., Chedammi S., Mesters J. et al. Identification of mycobacterial alpha-glucan as a novel ligand for DC-SIGN: involvement of mycobacterial capsular polysaccharides in host immune modulation // J. Immunol. 2009; 183 (8): 5221–5231.
16. Chaudhry A., Rudensky A.Y. Control of inflammation by integration of environmental cues by regulatory T-cells // J. Clin Invest. 2013; 123 (3): 939–944.
17. Sallusto F., Lanzavecchia A. The instructive role of dendritic cells on T-cell responses // Arthritis Research. 2002; 4 (3): 127–132.
18. Oestreich K.J., Weinmann A.S. Transcriptional mechanisms that regulate T-helper 1 cell differentiation // Curr. Opin. Immunol. 2012; 24 (2): 191–195.
19. Khasanova R.R., Urazova O.I., Voronkova O.V. i dr. Produktsiya IL-12β mononuklearnymi leykotsitami krovi u bol’nykh tuberkulezom legkikh v zavisimosti ot spektra lekarstvennoy ustoychivosti Mycobacterium tuberculosis [Production of IL-12β blood mononuclear leukocytes in patients with pulmonary tuberculosis, depending on the spectrum of drug resistance in Mycobacterium tuberculosis] // Immunologiya – Immunology. 2013; 34 (2): 115–118 (in Russian).
20. Khasanova R.R., Urazova O.I., Khaitova Z.K. i dr. Uroven’ produktsii IL-12β mononuklearnymi leykotsitami perifericheskoy krovi v zavisimosti ot klinicheskoy formy tuberkuleza legkikh [The level of production IL-12β mononuclear leukocytes of peripheral blood, depending on the clinical form of pulmonary tuberculosis] // Byulleten’ sibirskoy meditsiny – Bulletin of Siberian Medicine. 2012; 6: 218–220 (in Russian).
21. Ketlinskiy S.А. Rol’ geterodimernykh tsitokinov semeystva IL-12 v razvitii i regulyatsii vrozhdennogo immuniteta i TH1 immunnogo otveta [Role of heterodimeric IL-12 cytokine family, and in the development and regulation of innate immunity TH1 immune response] // Meditsinskiy akademicheskiy zhur. – Medical Academic Journal. 2005; 5 (3): 13–25 (in Russian).
22. Ketlinskiy S.А., Simbirtsev А.S. Tsitokiny [Cytokines]. Saint Petersburg, Foliant Publ., 2008: 552 (in Russian).
23. Pompei L., Jang S., Zamlynny B. et al. Disparity in IL-12 release in dendritic cells and macrophages in response to Mycobacterium tuberculosis is due to use of distinct TLRs // J. Immunol. 2007; 178 (8): 5192–5199.
24. Pisarenko M.S., Esimova I.E., Novitskiy V.V. i dr. Narusheniya IL-12/IL-27-zavisimoy aktivatsii T-limfotsitov pri disseminirovannom tuberkuleze legkikh [Disorders IL-12 / IL-27-dependent activation of T-lymphocytes with disseminated pulmonary tuberculosis] // Tuberkulez i bolezni legkikh – Tuberculosis and Lung Diseases. 2013; 11: 52–57 (in Russian).
25. Zhao Jingxian, Zhao Jincun, Perlman S. Differential effects of IL-12 on Tregs and non-Treg T-cells: roles of IFN-γ, IL-2 and IL-2R // PLoS One. 2012; 7 (9): e46241. doi: 10.1371/journal.pone.0046241.
26. Villarino A., Hibbert L., Lieberman L. et al. The IL- 27R (WSX-1) is required to suppress T-cell hyperactivity during infection // Immunity. 2003; 19 (5): 645–655.
27. Coskun M., Salem M., Pedersen J., Nielsen O.H. Involvement of JAK/STAT signaling in the pathogenesis of inflammatory bowel disease // Pharmacol. Res. 2013; 76: 1–8. doi: 10.1016/j.phrs.2013.06.007.
28. Sakhno L.V., Tikhonova M.А., Leplina O.YU. i dr. Rol’ PD-1/V7-N1-oposredovannogo puti v narushenii antigenspetsificheskogo otveta u bol’nykh tuberkulezom legkikh [The role of the PD-1 / B7-H1-mediated pathway in violation of an antigen specific response in patients with pulmonary tuberculosis] // Immunologiya – Immunology. 2011; 2: 89–93 (in Russian).
29. Churina E.G., Novitskiy V.V., Urazova O.I. Faktory immunosupressii pri razlichnykh patologiyakh [Factors immunosuppression with different pathologies] // Byulleten’ sibirskoy meditsiny – Bulletin of Siberian Medicine. 2012; 4: 103–111 (in Russian).
30. Pinheiro R.O., de Oliveira E.B., Dos Santos G. et al. Different immunosuppressive mechanisms in multi-drugresistant tuberculosis and non-tuberculous mycobacteria patients // Clin. Exp. Immunol. 2013; 171 (2): 210–219.
31. Dhamne C., Chung Y., Alousi A.M. et al. Peripheral and thymic foxp3(+) regulatory T-сells in search of origin, distinction, and function // Front. Immunol. 2013; 4: 253.
32. Josefowicz S.Z., Lu L.F., Rudensky A.Y. Regulatory T-cells: mechanisms of differentiation and function // Annu Rev. Immunol. 2012; 30: 531–564.
33. Larson R.P., Shafiani S., Urdahl K.B. Foxp3(+) regulatory T-cells in tuberculosis // Adv. Exp. Med. Biol. 2013; 783: 165–180.
34. Sakaguchi S., Miyara M., Costantino C.M., Hafler D.A. Foxp3+ regulatory T-cells in the human immune system // Nat. Rev .Immunol. 2010; 10 (7): 490–500.
35. Semple P.L., Binder A.B., Davids M. et al. Regulatory T-cells attenuate mycobacterial stasis in alveolar and blood-derived macrophages from patients with tuberculosis // Am. J. Respir. Crit. Care Med. 2013; 187 (11): 1249–1258.
36. Vignali D.А., Collison L.W., Workman C.J. How regulatory T-cells work // Nat. Rev. Immunol. 2008; 8 (7): 523–532.
37. Beyer M., Schultze J.L. Plasticity of T(reg)-cells: is reprogramming of T(reg)-cells possible in the presence of FOXP3? // Int. Immunopharmacol. 2011; 11 (5): 555–560.
38. Miyara M., Sakaguchi S. Human FoxP3(+)CD4(+) regulatory T-cells: their knowns and unknowns // Immunol. Cell. Biol. 2011; 89 (3): 346–351.
39. Sakaguchi S., Vignali D.A., Rudensky A.Y. et al. The plasticity and stability of regulatory T-cells // Nat. Rev. Immunol. 2013; 13 (6): 461–467.
40. Rudensky A.Y. Regulatory T-cells and Foxp3 // Immunol. Rev. 2011; 241 (1): 260–268.
41. Churina E.G., Novitskiy V.V., Urazova O.I. i dr. Pokazateli apoptoza i proliferativnoy aktivnosti limfotsitov u bol’nykh tuberkulezom legkikh s mnozhestvennoy lekarstvennoy ustoychivost’yu M. tuberculosis [Indicators of apoptosis and proliferative activity of lymphocytes in patients with pulmonary tuberculosis with multidrug-resistant M. tuberculosis] // Meditsinskaya immunologiya – Medical Immunology. 2012; 14 (1–2): 119–126 (in Russian).
42. Sakhno L.V., Tikhonova M.А., Kurganova E.V. i dr. T-kletochnaya anergiya v patogeneze immunnoy nedostatochnosti pri tuberkuleze legkikh [T-cell anergy in the pathogenesis of immune deficiency in pulmonary tuberculosis] // Problemy tuberkulёza i bolezney lёgkikh. 2004; 5: 23–28 (in Russian).
43. Lee D.C., Harker J.A., Tregoning J.S. et al. CD25+ natural regulatory T-cells are critical in limiting innate and adaptive immunity and resolving disease following respiratory syncytial virus infection // J. Virol. 2010; 84 (17): 8790–8798.
44. Liu Y., Yu S., Li Z. et al. TGF-β enhanced IL-21-induced differentiation of human IL-21-producing CD4+ T-cells via Smad3 // PLoS One. 2013; 8 (5): e64612. doi: 10.1371/journal.pone.0064612.
45. Yadav M., Stephan S., Bluestone J.A. Peripherally induced Tregs – role in immune homeostasis and autoimmunity // Front. Immunol. 2013; 4: 232.
46. Kononova T.E., Urazova O.I., Novitskiy V.V., Churina E.G. Oposredovannaya T-limfotsitami-khelperami tipa 17 regulyatsiya antibakterial’nogo (protivotuberkuleznogo) immuniteta [T-lymphocyte-mediated helper type 17 regulation of antibacterial (TB) immunity] // Molekulyarnaya biologiya – Molecular Biology. 2013; 47 (6): 883–890.
47. Burgler S., Mantel P.Y., Bassin C. et al. RORC2 is involved in T-cell polarization through interaction with the FoxP3 promoter // J. Immunol. 2010; 184: 6161–6169.
48. Eisenstein E.M., Williams C.B. The Treg/Th17 cell balance: a new paradigm for autoimmunity // Pediatr. Res. 2009; 65: 26R–31R.
49. Laurence A., Tato C.M., Davidson T.C. et al. Interleukin-2 signaling via STAT5 constrains T-helper 17 cell generation // Immunity. 2007; 26: 371–381.
50. Xu L., Kitani A., Fuss I., Strober W. Cutting edge: regulatory T cells induce CD4+CD25-Foxp3- T-cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta // J. Immunol. 2007; 178 (11): 6725–6729.
51. Yang X.O., Pappu B.P., Nurieva R. et al. T-helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma // Immunity.2008; 28 (10): 29–39.
52. Zheng S.G. Regulatory T-cells vs Th17: differentiation of Th17 versus Treg, are the mutually exclusive? // Am. J. of Clin. Exp. Immunol. 2013; 2 (1): 94–106.
53. Khader S.A., Gopal R. IL-17 in protective immunity to intracellular pathogens // Virulence. 2010; 1 (5): 423–427.
54. McAleer J.P., Kolls J.K. Directing traffic: IL-17 and IL-22 coordinate pulmonary immune defense // Immunol Rev. 2014; 260 (1): 129–144.
55. Paidipally P., Periasamy S., Barnes P.F. et al. NKG2D-dependent IL-17 production by human T-cells in response to an intracellular pathogen // J. Immunol. 2009; 183 (3): 1940–1945.
56. Scriba T.J., Kalsdorf B., Abrahams D.A. et al. Distinct, specific IL-17- and IL-22-producing CD4+ T-cell subsets contribute to the human anti-mycobacterial immune response // J. Immunol. 2008; 180 (3): 1962–1970.
57. Tesmer L.A., Lundy S.K., Sarkar S., Fox D.A. Th17 cells in human disease // Immunol. Reviews. 2008; 223: 87–113.
58. Kononova T.E., Urazova O.I., Novitskiy V.V. i dr. Funktsional’naya aktivnost’ Th17-limfotsitov pri tuberkuleze legkikh [Functional activity of Th17 lymphocytes in pulmonary tuberculosis] // Byulleten’ eksperimental’noy biologii i meditsiny – Bulletin of Experimental Biology and Medicine. 2013; 156 (12): 701–704 (in Russian).
59. Awasthi A., Kuchroo V. Th17 cells: from precursors to players in inflammation and infection // Int. Immunol. 2009; 21 (5): 489–498.
60. Li L., Qiao D., Fu X. et al. Identification of Mycobacterium tuberculosis – specific Th1, Th17 and Th22 cells using the expression of CD40L in tuberculous pleurisy // PLoS One. 2011; 6 (5): e20165. doi: 10.1371/journal.pone.0020165.
61. Miossec P., Kolls J.K. Targeting IL-17 and TH17-cells in chronic inflammation // Nat. Rev. Drug. Discov. 2012; 11: 763–776.
62. Yang J. Yang X., Zou H. et al. Recovery of the immune balance between Th17 and regulatory T-cells as a treatment for systemic lupus erythematosus // Rheumatology. 2011; 50: 1366–1372.
Review
For citations:
Churina E.G., Urazova O.I., Novitskiy V.V., Yesimova I.Ye., Kononova T.Ye., Filinyuk O.V., Kolobovnikova Yu.V., Dmitrieva A.I. The factors of dysregualtion of the immune response (at different stage of its implementation) in patients with pulmonary tuberculosis. Bulletin of Siberian Medicine. 2016;15(5):166-177. (In Russ.) https://doi.org/10.20538/1682-0363-2016-5-166-177
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