T cell thymic selection and peripheral homeostatic proliferation in infectious diseases

Cover Page


Cite item

Full Text

Abstract

There is no doubt that infectious agents and host undergo multilayered yet not fully understood interactions. This is primarily due to at least mechanisms resulting in chronic course of infectious process. Acute infection proceeds in parallel with primary immune response and its typical phases, each of which manifests as certain stage in clinical picture featured with disease onset and subsequent recovery. A whole process of immune response developing against infectious agent occurs in peripheral lymphoid organs and immune tissues. With regard to the role of immune system in infectious process, process, two main outstanding issues still remain unanswered: 1) what are the mechanisms of host death in the case of acute infectious process? 2) what is a “fault” of immune system in it? In its inferiority or in abruptly suppressed functions induced by infectious agent, when it “does not have time” to mount an immune response of sufficient power? So far, no answer is still found yet. The second question concerns mechanisms of converting to chronic course of infectious process. The obtained available in publications evidence about an intimately involved thymus as the central immune organ in infectious process of, the main function of which is to ensure developing central immune tolerance to self-antigens accomplished via T-cell positive and negative selection. It turned out that in case of some examined infections due to pathogens, which entered the thymus, such intimate events such as partial tolerance to pathogens and autoimmune reactivity are altered. Moreover, these processes are further aggravated by homeostatic proliferation, which is also induced by an infectious agent. In both cases, it accounts for decreased magnitude of immune response against a certain pathogen, burdened by emergence of autoimmune reactions.

About the authors

V. A. Kozlov

Scientific Research Institute of Fundamental and Clinical Immunology; Novosibirsk State Medical University

Author for correspondence.
Email: vakoz40@yandex.ru
ORCID iD: 0000-0002-1756-1782

Vladimir A. Kozlov, RAS Full Member, PhD, MD (Medicine), Professor, Scientific Director,; Head of the Department Clinical Immunology

630099, Novosibirsk, Yadrintsevskaya str., 14.

Phone: +7 (383) 222-66-27. Fax: +7 (383) 222-70-28.

Russian Federation

References

  1. Козлов В.А. Гомеостатическая пролиферация как основа неизбежного формирования тотального иммунодефицита // Медицинская иммунология. 2014. Т. 16, № 5. С. 403–408. doi: 10.15789/1563-0625-2014-5-403-408
  2. Козлов В.А. Директивная фаза иммунного ответа в проблеме регуляции // Методологические аспекты современной иммунологии. Новосибирск: Наука, 1991. C. 45–51.
  3. Козлов В.А. Клетки-супрессоры — основа иммунопатогенеза атеросклероза // Атеросклероз. 2015. Т. 11, № 2. С. 37–42. doi: 10.15789/1563-0625-2016-1-7-14
  4. Козлов В.А. Клетки-супрессоры — основа иммунопатогенеза аутоиммунных заболеваний // Медицинская иммунология. 2016. Т. 18, № 1. С. 7–15. doi: 10.15789/1563-0625-2016-1-7-14
  5. Козлов В.А. Клетки-супрессоры — основа иммунопатогенеза онкозаболеваний // Вопросы онкологии. 2016. № 3. С. 390–396.
  6. Козлов В.А., Демина Д.В. Регуляторные клетки-супрессоры в иммунопатогенгезе аллергических заболеваний // Иммунология. 2017. Т. 38, № 6. С. 327–336. doi: 10.18821/0206-4952-2017-38-6-327-336
  7. Atarashi K., Tanoue T., Oshima K., Suda W., Nagano Y., Nishikawa H., Fukuda S., Saito T., Narushima S., Hase K., Kim S., Fritz J.V., Wilmes P., Ueha S., Matsushima K., Ohno H., Olle B., Sakaguchi S., Taniguchi T., Morita H., Hattori M., Honda K. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature, 2013, vol. 500, no. 7461, pp. 232–236. doi: 10.1038/nature12331
  8. Bomoto A., Kehn P.J., Shevach E.M. Premature escape of double-positive thymocytes to the periphery of young mice. J. Immunol., 1994, vol. 152, pp. 1509–1518.
  9. Bonasio R., Scimone M.L., Schaerli P., Grabie N., Lichtman A.H., von Andrian U.H. Clonal deletion of thymocytes by circulating dendritic cells homing to the thymus. Nat. Immunol., 2006, vol. 7, pp. 1092–1100. doi: 10.1038/ni1385
  10. Cotta-de-Almeida V., Bonomo A., Mendes-da-Cruz D.A., Riederer I., de Meis J., Lima-Quaresma K.R.F., Vieira-de-Abreu A., Villa-Verde D.M.S., Savino W. Trypanosoma cruzi infection modulates intrathymic contents of Extracellular matrix ligand and receptors and alters thymocyte Migration. Eur. J. Immunol., 2003, vol. 33, pp. 2439–2448. doi: 10.1002/eji.200323860
  11. Donskoy E., Goldschneider I. Two developmentally distinct populations of dendritic cells inha-bit mouse thymus: demonstration by differential importation of hematogenous precursors under steady state conditions. J. Immunol., 2003, vol. 170, no. 7, pp. 3514–3521. doi: 10.4049/jimmunol.170.7.3514
  12. Enouz S., Carrie L., Merkler D., Bevan M.J., Zehn D. Autoreactive T cells bypass negative selection and respond to self-antigen stimulation during infection. J. Exp. Med., 2012, vol. 209, no. 10, pp. 1769–1779. doi: 10.1084/jem.20120905
  13. Ernst B., Lee D.S., Chang J.M., Sprent J., Surh C.D. The peptide ligands mediating positive selection in the hymus control T cell survival and homeostatic proliferation in the periphery. Immunity, 1999, vol. 11, no. 2, pp. 173–181.
  14. Fulton R.B., Meyerholz D.K., Varga S.M. Foxp3+ CD4 Regulatory T cells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J. Immunol., 2010, vol. 185, no. 4, pp. 2382–2392. doi: 10.4049/jimmunol.1000423
  15. Gonzalez F.B., Calmon-Hamaty F., Cordeiro S.N.S., Bussy R.F., Spinelli S.V., D’Attilio L., Bottasso O., Savino W., Cotta-de-Almedia V., Villar S.R., Perez A.R. Trypanosoma cruzi experimental infection impacts on the thymic Regulatory N cell compartment. PLoS Negl. Trop. Dis., 2016, vol. 10, no. 1, pp. 1–21. doi: 10.1371/journal.pntd.0004285
  16. Hadeiba H., Butcher E.C. Thymus-homing dendritic cells in central tolerance. Eur. J. Immunol., 2013, vol. 43, no. 6, pp. 1425–1429. doi: 10.1002/eji.201243192
  17. Hadeida H., Lahl K., Edalati A., Oderup C., Habtezion A., Pachynski R., Nguyen L., Ghodsi A., Adler S., Butcher E.C. Plasmacytoid dendritic cells transport peripheral antigens to the Thymus to promote central tolerance. Immunol., 2012, vol. 36, no. 3, pp. 438–450. doi: 10.1016/j.immuni.2012.01.017
  18. Hale J.S., Fink P.J. Back to the thymus: peripheral T cells come home. Immunol. Cell. Biol., 2009, vol. 87, no. 1, pp. 58–64. doi: 10.1038/icb.2008.87
  19. Jaidane H., San é F., Hiar R., Goffard A., Gharbi J., Geenen V., Hober D. Immunology in the clinic review series; focus on type 1 diabetes and viruses: enterovirus, thymus and type 1 diabetes pathogenesis. Clin. Exp. Immunol., 2012, vol. 168, no. 1, pp. 39–46. doi: 10.1111/j.1365-2249.2011.04558.x.
  20. Korostoff J.M., Nakada M.T., Faas S.J., Blank K.J., Gaulton G.N. Neonatal exposure to thymotropic gross murine leukemia virus Induces virus-specific immunological nonresponsiveness. J. Exp. Med., 1990, vol. 172, no. 6, pp. 1765–1775.
  21. Lamontagne L., Jolicoeur P. Low-virulent mouse viruses exhibiting various tropisms in macrophages, T and B cell subpopulations, and thymus stromal cells. Lab. Anim. Sci., 1994, vol. 44, no. 1, pp. 17–24.
  22. Leake I. Gut microbiota: selecting Clostridia strains that induce TREG cells from gut microbiota. Nat. Rev. Gastroenterol. Hepatol., 2013, vol. 10, no. 9, p. 504. doi: 10.1038/nrgastro.2013.139
  23. Mendes-da-Cruz D.A., Silva J.S., Cotta-de-Almeida V., Savino W. Altered thymocyte migration during experimental acute Trypanosoma cruzi infection: combined role of fibronectin and the chemokines CXCL12 and CCL4. Eur. J. Immunol., 2006, vol. 36, no. 6, pp. 1486–1493. doi: 10.1002/eji.200535629
  24. Michaux H., Martens H., Jaidane H., Halouani A., Hober D., Geenen V. How does thymus infection by coxsackievirus contribute to the pathogenesis of type 1 diabetes? Frontiers in Immunol., 2015, vol. 6, pp. 338–343. doi: 10.3389/fimmu.2015.00338
  25. Milich D.R., Jones J.E., Hughes J.L., Price J., Raney A.K., McLachlan A. Is function of the secreted hepatitis B e antigen to induce immunologic tolerance in utero? Proc. Natl. Acad. Sci. USA, 1990, vol. 87, no. 17, pp. 6599–6603.
  26. Morrot A., Terra-Granado E., Perez A.R., Silva-Barbosa S.D., Milicevic N.M., Farias-de-Oliveira D.A., Berbert L.R., De Meis J., Takiya C.M., Beloscar J., Wang X., Kont V., Peterson P., Bottasso O., Savino W. Chagasic thymic atrophy does not affect negative selection but results in the export of activated CD4+CD8+ T cells in severe forms of human disease. PLoS Negl. Trop. Dis., 2011, vol. 5, no. 8: e1268. doi: 10.1371/journal.pntd.0001268
  27. Nascimbeni M., Pol S., Saunier B. Distinct CD4+CD8+ double-positive T cells in the blood and liver of patients during chronic hepatitis B and C. PLoS One, 2011, vol. 6, no. 5: e20145. doi: 10.1371/journal.pone.0020145
  28. Nobrega C., Roque S., Nunes-Alves C., Coelho A., Medeiros I., Castro A.G., Appelberg R., Correira-Neves M. Dissemination of Mycobacteria to the thymus renders newly generated T cells tolerant to the invading pathogen. J. Immunol., 2010, vol. 184, pp. 351–358. doi: 10.4049/jimmunol.0902152
  29. Nunes-Alves C., Nobrega C., Behar S.M., Correia-Neves M. Tolerance has its limits: how the thymus copes with infection. Trends Immunol., 2013, vol. 34, no. 10, pp. 502–510. doi: 10.1016/j.it.2013.06.004
  30. Perez A.R., Berbert L.R., Lepletier A., Revelli S., Bottasso O., Silva-Barbosa S.D., Savino W. TNF-α is involved in the abnormal thymocyte migration during experimental trypanosoma cruzi infection and favor the export of immature cells. PLoS One, 2012, vol. 7, no. 3: e34360. doi: 10.1371/journal.pone.0034360
  31. Richards D.M., Delacher M., Goldfarb Y., Kagebein D., Hofer A.-C., Abramson J., Feuerer M. Treg cell differentiation: from thymus to peripheral tissue. Prog. Mol. Biol. Transl. Sci., 2015, vol. 136, pp. 175–205. doi: 10.1016/bs.pmbts.2015.07.014
  32. Rogers M.C., Lamens K.D., Shafagati N., Johnson M., Oury T.D., Joyce S., Williams J.V. CD4+ regulatory T cells exert differential functions during early and late stages of the immune response to respiratory viruses. J. Immunol., 2018, vol. 201, no. 4, pp. 1253–1266. doi: 10.4049/jimmunol.1800096
  33. Savino W., Leite-de-Moraes M.C., Hontebeyrie-Joskowicz M, Dardenne M. Studies on thymus in Chagas’disease. I. Changes in the thymic microenvironment in mice acutely infected with Trypanosoma cruzi. Eur. J. Immunol., 1989, vol. 19, no. 9, pp. 1727–1733. doi: 10.1002/eji.1830190930
  34. Savino W., Villa-Verde D.M., Mendes-da-Cruz D.A., Silva-Monteiro E., Perez A.R., Aoki Mdel P., Bottasso O., Gui ñ az ú N., Silva-Barbosa S.D., Gea S. Cytokines and cell adhesion receptor in the regulation of immunity to Trypanosoma cruzi. Cytokine Growth Factor Rev., 2007, vol. 18, no. 1–2, pp. 107–124. doi: 10.1016/j.cytogfr.2007.01.010
  35. Silva-Monteiro E., Lorenzato L.R., Nihei O.K., Junqueira M., Rabinovich G.A., Hsu D.K., Liu F.-T., Savino W., Chammas R., Villa-Verde D.M.S. Altered expression of galectin-3 induces cortical thymocyte depletion and premature exit of immature thymocytes during Trypanaosoma cruzi infection. Am. J. Pathol., 2007, vol. 170, no. 2, pp. 546–556. doi: 10.2353/ajpath.2007.060389
  36. Stephen-Victor E., Karnam A., Fontaine T., Beauvais A., Das M., Hegde P., Prakhar P., Holla S., Balaji K.N., Kaveri S.V., Latg é J.P., Aimanianda V., Bayry J. Aspergillus fumigatus cell wall α-(1,3)-glucan stimulates regulatory T-cell polarization by inducing PD-L1 expression on human dendritic cells. J. Infect. Dis., 2017, vol. 216, no. 10, pp. 1281–1294. doi: 10.1093/infdis/jix469
  37. Stevens C.E., Beasley R.P., Tsui J., Lee W.C. Vertical transmission of hepatitis B antigen in Taiwan. N. Engl. J. Med., 1975, vol. 292, no. 15, pp. 771–774. doi: 10.1056/NEJM197504102921503
  38. Takada H., Takayanag H. The mechanisms of T cell selection in the thymus. Trends Immunol., 2017, vol. 38, no. 11, pp. 805–816. doi: 10.1016/j.it.2017.07.010
  39. Thiault N., Darrigues J., Adoue V., Gros M., Binet B., Perals C., Leobon B., Fazilleau N., Joffre O.P., Robey E.A., van Meerwijk J.P., Romagnoli P. Peripheral regulatory T lymphocytes recirculating to the thymus suppress the development of their precursors. Nat. Immunol., 2015, vol. 16, no. 6, pp. 628–634. doi: 10.1038/ni.3150.
  40. Wang J., Cardoso R., Marreros N., M ü ller N., Lundstr ö m-Stadelmann B., Siffert M., Vuitton D.A., Bou é F., Lin R., Wen H., Gottstein B. Foxp3+ Tregs 1 as a potential target for immunotherapy against primary infection with Echinococcus multilocularis eggs. Infect. Immun., 2018, vol. 86, iss. 10: e00542-18. doi: 10.1128/IAI.00542-18
  41. Weiss L., Roux A., Garcia S., Demouchy C., Haeffner-Cavaillon N., Kazatchkine M.D., Gougeon M.L. Persistent expansion, in a Human immunodeficiency virus-infected person, of Vβ-restricted CD4+CD8+ T lymphocytes that express cytotoxicityassociated molecules and are committed to produce interferon-γ and tumor necrosis factor-α. J. Infect. Dis., 1998, vol. 178, iss. 4, pp. 1158–1162. doi: 10.1086/515674

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2020 Kozlov V.A.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies