Role of regulatory T-cells in the systemic inflammatory response syndrome
https://doi.org/10.17802/2306-1278-2020-9-2-82-90
Abstract
Systemic inflammatory response syndrome is a complex multisyndromic, phase-specific pathological process that develops with systemic damage. Outcomes largely depend on the balance of multidirectional sequential stages: hyperinflammatory reaction and compensatory anti-inflammatory response syndrome (CARS). Regulatory T-cells (Tregs) are able to regulate adaptive and innate immune responses and contribute to the various stages ofthe systemic inflammatory response syndrome. At the initial hyperinflammatory stage, Tregs are able to limit self-inflicted damage. At the same time, Tregs contribute to CARS and the formation of induced immunosuppression, predisposing to a high susceptibility to nosocomial and opportunistic infections, with subsequent transition to multiple organ dysfunction syndrome. Regulatory T-cells and their functional changes are considered as predictors and prognostic markers of critical illness.
About the Authors
M. Yu. Khanova
Federal State Budgetary Institution Research Institute for Complex Issues of Cardiovascular Diseases
Russian Federation
Competing Interests: not
Russian Federation
Khanova Mariam Yu. - research assistant at the Laboratory of Cell Technologies.
6, Sosonoviy Blvd., Kemerovo, 650002
Competing Interests: not
V. G. Matveeva
Federal State Budgetary Institution Research Institute for Complex Issues of Cardiovascular Diseases
Russian Federation
Competing Interests: not
Russian Federation
Matveeva Vera G. - PhD, senior researcher at the Laboratory of Cell Technologies.
6, Sosonoviy Blvd., Kemerovo, 650002
Competing Interests: not
L. V. Antonova
Federal State Budgetary Institution Research Institute for Complex Issues of Cardiovascular Diseases
Russian Federation
Competing Interests: not
Russian Federation
Antonova Larisa V. - PhD, Head of the Laboratory of Cell Technologies.
6, Sosonoviy Blvd., Kemerovo, 650002
Competing Interests: not
E. V. Grigoriev
Federal State Budgetary Institution Research Institute for Complex Issues of Cardiovascular Diseases
Russian Federation
Competing Interests: not
Russian Federation
Grigoriev Evgeny V. - PhD, Professor of the Russian Academy of Sciences, Deputy Director for Scientific and Medical Issues.
6, Sosonoviy Blvd., Kemerovo, 650002
Competing Interests: not
References
1. Bone R.C. Immunologic dissonance: a continuing evolution in our understanding of the systemic inflammatory response syndrome (SIRS) and the multiple organ dysfunction syndrome (MODS). Ann Intern Med. 1996; 125 (8): 680-687. doi: 10.7326/0003-4819-125-8-199610150-00009
2. Sakaguchi S., Sakaguchi N., Shimizu J., Yamazaki S., Sakihama T., Itoh M., Kuniyasu Y, Nomura T., Toda M., Takahashi T. Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev. 2001; 182 (1): 18-32. doi:10.1034/j.1600-065X.2001.1820102.x
3. Abbas A.K., Benoist C., Bluestone J.A., Campbell D.J., Ghosh S., Hori S., Jiang S., Kuchroo V.K., Mathis D., Roncarolo M.G., Rudensky A., Sakaguchi S., Shevach E.M., Vignali D.A., Ziegler S.F. Regulatory T cells: recommendations to simplify the nomenclature. Nat Immunol. 2013; 14 (4): 307308. doi:10.1038/ni.2554. DOI: 10.1038/ni.2554
4. Fehervari Z., Sakaguchi S. CD4(+) Tregs and immune control. Clin. Invest. 2004; 114 (9): 1209-1217. doi:10.1172/JCI200423395
5. Sakaguchi S. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control immune responses. Annu Rev Immunol. 2004; 22: 531-562. doi:10.1146/annurev.immunol.21.120601.141122
6. Gershon R.K., Kondo K. Infectious immunological tolerance. Immunology. 1971; 21 (6): 903-914.
7. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alfa-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 1995; 155: 1151-1164.
8. Baecher-Allan C., Brown J.A., Freeman G.J., Hafler D.A. CD4+CD25high regulatory cells in human peripheral blood. J Immunol. 2001; 167 (3): 1245-1253. doi:10.4049/jimmunol.167.3.1245
9. Yagi H., Nomura T., Nakamura K., Yamazaki S., Kitawaki T., Hori S., Maeda M., Onodera M., Uchiyama T., Fujii S., Sakaguchi S. Crucial role of FOXP3 in the development and function of human CD4+CD25+regulatory T cells. Int. Immunol. 2004; 16 (11): 1643-1656. doi:10.1093/intimm/dxh165
10. Jiang S., Lechler R.I., He X.S., Huang J.F. Regulatory T cells and transplantation tolerance. Hum. Immunol. 2006; 67 (10): 765-776. doi:10.1016/j.humimm.2006.07.013
11. Liu W., Putnam A.L., Xu,Yu Z., Szot G.L., Lee M.R., Zhu S., Gottlieb P.A., Kapranov P., Gingeras T.R., Fazekas de St Groth B., Clayberger C., Soper D.M., Ziegler S.F., Bluestone J.A. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J Exp Med. 2006; 203 (7): 1701-1711. doi:10.1084/jem.20060772
12. Shen L.S., Wang J., Shen D.F. Yuan X.L., Dong P., Li M.X., Xue J., Zhang F.M., Ge H.L., Xu D. CD4+CD25+CD127low/- regulatory T cells express Foxp3 and suppress effector T cell proliferation and contribute to gastric cancers progression. Clin Immunol. 2009; 131 (1): 109-118. doi:10.1016/j.clim.2008.11.010
13. Banham A.H. Cell-surface IL-7 receptor expression facilitates the purification of FOXP3(+) regulatory T cells. Trends Immunol. 2006; 27 (12): 541-544. doi:10.1016/j.it.2006.10.002
14. Taams L.S., Van Amelsfort J.M., Tiemessen M.M., Jacobs K.M., de Jong E.C., Akbar A.N., Bijlsma J.W., Lafeber F.P. Modulation of monocyte/macrophage function by human CD4+CD25+ regulatory T cells. Hum Imunol. 2005; 66 (3): 222-230. doi:10.1016/j.humimm.2004.12.006
15. Piccirillo C.A., Shevach E.M. Cutting edge: control of CD8+ T cell activation by CD4+CD25+ immunoregulatory cells. J Imunol. 2001; 167 (3): 1137-1140. doi:10.4049/jimmunol.167.3.1137
16. Collison L.W., Workman C.J., Kuo T.T., Boyd K., Wang Y., Vignali K.M., Cross R., Sehy D., Blumberg R.S. Vignali D.A. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature. 2007; 450 (7169): 566-569. doi:10.1038/nature06306
17. Shull M.M., Ormsby I., Kier A.B., Pawlowski S., Diebold R.J., Yin M., Allen R., Sidman C., Proetzel G., Calvin D., Annunziata N., Doetschman T. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature. 1992; 359 (6397): 693-699. doi:10.1038/359693a0
18. Brabletz T., Pfeuffer I., Schorr E., Siebelt F., Wirth T., Serfling E. Transforming growth factor beta and cyclosporin A inhibit the inducible activity of the interleukin-2 gene in T cells through a noncanonical octamer-binding site. Mol Cell Biol. 1993; 13 (2): 1155-1162. doi:10.1128/MCB.13.2.1155
19. Moore K.W., de Waal Malefyt R., Coffman R.L., O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol. 2001; 19: 683-765. doi:10.1146/annurev.immunol.19.1.683
20. Kuhn R., Lohler J., Rennick D., Rajewsky K., Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993; 75 (2): 263-274. doi:10.1016/0092-8674(93)80068-P
21. Misra N., Bayry J., Lacroix-Desmazes S., Kazatchkine M.D., Kaveri S.V. Cutting edge: human CD4+CD25+ T cells restrain the maturation and antigen-presenting function of dendritic cells. J Immunol. 2004; 172 (8): 4676-4680. doi:10.4049/jimmunol.172.8.4676
22. Grohmann U., Orabona C., Fallarino F., Vacca C., Calcinaro F., Falorni A., Candeloro P., Belladonna M.L., Bianchi R., Fioretti M.C., Puccetti P. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nature Immunology. 2002; 3 (11), 1097-1101. doi:10.1038/ni846
23. Liang B., Workman C., Lee J., Chew C., Dale B.M., Colonna L., Flores M., Li N., Schweighoffer E., Greenberg S., Tybulewicz V, Vignali D., Clynes R. Regulatory T cells inhibit dendritic cells by lymphocyte activation gene-3 engagement of MHC class II. J Immunol. 2008; 180 (9): 5916-5926. doi:10.4049/jimmunol.180.9.5916
24. Walker L.S. K., Sansom D.M. The emerging role of CTLA4 as a cell-extrinsic regulator of T cell responses. Nature Reviews Immunology. 2011; 11: 852-863. doi:10.1038/nri3108
25. Qureshi O.S., Zheng Y., Nakamura K., Attridge K., Manzotti C., Schmidt E.M., Baker J., Jeffery L.E., Kaur S., Briggs Z., Hou T.Z., Futter C.E., Anderson G., Walker L.S.K., Sansom D.M. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell extrinsic function of CTLA-4. Science. 2011; 332 (6029): 600-603. doi:10.1126/science.1202947
26. Gondek D.C., Lu L.F., Quezada S.A., Sakaguchi S., Noelle R.J.. Cutting Edge: contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J Immunol. 2005; 174 (4): 1783-1786. doi:10.4049/jimmunol.174.4.1783
27. Grossman W.J., Verbsky J.W., Barchet W., Collona M., Atkinson J.P., Ley T.J. Human T regulatory cells can use the perforin pathway to cause autologous target cell death. Immunity. 2004; 21 (4): 589-601. doi:10.1016/j.immuni.2004.09.002
28. Trzonkowski P, Szmit E., Mysliwska J., Dobyszuk A., Myśliwski A. CD4+CD25+ T regulatory cells inhibit cytotoxic activity of T CD8+ and NK lymphocytes in the direct cell-to-cell interaction. Clin Immunol. 2004; 112 (3): 258-267. doi:10.1016/j.clim.2004.04.003
29. Rueda C.M., Jackson C.M., Chougnet C.A. Regulatory T-cell-mediated suppression of conventional T-cells and dendritic cells by different cAMP intracellular pathways. Front Immunol. 2016; 7: 216. doi:10.3389/fimmu.2016.00216
30. Kobie J.J., Shah PR., Yang L., Rebhahn J.A., Fowell D.J., Mosmann T.R. T regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 5'-adenosine monophosphate to adenosine. J Immunol. 2006; 177 (10): 6780-6786. doi:10.4049/jimmunol.177.10.6780
31. Takenaka M.C., Robson S., Quintana F.J. Regulation of the T cell response by CD39. Trends Immunol. 2016; 37 (7): 427-439. doi:10.1016/j.it.2016.04.009
32. Chen G.Y, Nunez G. Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol. 2010; 10 (12): 826-837. doi:10.1038/nri2873
33. Cauwels A., Rogge E., Vandendriessche B., Shiva S., Brouckaert P Extracellular ATP drives systemic inflammation, tissue damage and mortality. Cell Death Dis. 2014; 5: e1102. doi:10.1038/cddis.2014.70
34. Trabanelli S., Ocadhkova D., Gulinelli S., Curti A., Salvestrini V., Vieira R.P., Idzko M., Di Virgilio F., Ferrari D., Lemoli R.M. Extracellular ATP exerts opposite effects on activated and regulatory CD4+ T cells via purinergic P2 receptor activation. J Immunol. 2012; 189 (3): 1303-1310. doi:10.4049/jimmunol.1103800
35. Pandiyan P, Zheng L., Ishihara S., Reed J., Lenardo M.J. CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells. Nature Immunology. 2007; 8, 1353-1362. doi:10.1038/ni1536
36. Kearley J., Barker J.E., Robinson D.S., Lloyd C.M. Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD4+ CD25+ regulatory T cells is interleukin 10 dependent. J Exp Med. 2005; 202 (11): 1539-1547. doi:10.1084/jem.20051166
37. Francisco L.M., Salinas V.H., Brown K.E., Vanguri V.K., Freeman G.J., Kuchroo V.K., Sharpe A.H. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med. 2009; 206 (13): 3015-3029. doi:10.1084/jem.20090847
38. Chen X., Fosco D., Kline D.E., Meng L., Nishi S., Savage P.A., Kline J. PD-1 regulates extrathymic regulatory T-cell differentiation. Eur J Immunol. 2014; 44 (9): 2603-2616. doi:10.1002/eji.201344423
39. Sakaguchi S. Control of immune responses by naturally arising CD4+regulatory T cells that express toll-like receptors. J. Exp. Med. 2003; 197 (4): 397-401. doi:10.1084/jem.20030012
40. Caramalho I., Lopes-Carvalho T., Ostler D., Zelenay S., Haury M., Demengeot J. Regulatory T cells selectively express toll-like receptors and are activated by lipopolysaccharide. J Exp Med. 2003; 197 (4): 403-411. doi:10.1084/jem.20021633
41. Murphy T.J., Ni Choileain N., Zang Y., Mannick J.A., Lederer J.A. CD4+CD25+ regulatory T cells control innate immune reactivity after injury. Immunol. 2005; 174 (5): 29572963. doi:10.4049/jimmunol.174.5.2957
42. Hanschen M., Tajima G., O'Leary F., Ikeda K., Lederer J.A. Injury induces early activation of T-cell receptor signaling pathways in CD4+ regulatory T cells. Shock 2011; 35 (3): 252257. doi:10.1097/SHK.0b013e3181f489c5
43. Choileain N.N., MacConmara M., Zang Y, Murphy T.J., Mannick J.A., Lederer J.A. Enhanced regulatory T cell activity is an element of the host response to injury. J Immunol. 2006; 176 (1): 225-236. doi:10.4049/jimmunol.176.1.225
44. MacConmara M.P., Tajima G., O'Leary F., Delisle A.J., McKenna A.M., Stallwood C.G., Mannick J.A., Lederer J. A. Regulatory T cells suppress antigen-driven CD4 T cell reactivity following injury. J Leukoc Biol. 2011; 89 (1): 137147. doi:10.1189/jlb.0210082
45. Heuer J.G., Zhang T., Zhao J., Ding C., Cramer M., Justen K. L., Vonderfecht S.L., Na S. Adoptive transfer ofin vitro-stimulated CD4+CD25+ regulatory T cells increases bacterial clearance and improves survival in polymicrobial sepsis. J Immunol. 2005; 174 (11): 7141-7146. doi: 10.4049/jimmunol.174.11.714
46. Hein F., Massin F., Cravoisy-Popovic A., Barraud D., Levy B., Bollaert P.E., Gibot S. The relationship between CD4+CD25+CD127- regulatory T cells and inflammatory response and outcome during shock states. Crit Care. 2010; 14 (1): R19. doi:10.1186/cc8876
47. Monneret G., Debard A.L., Venet F., Bohe J., Hequet O., Bienvenu J., Lepape A. Marked elevation of human circulating CD4+CD25+ regulatory T cells in sepsis-induced immunoparalysis. Crit Care Med. 2003; 31 (7): 2068-2071. doi:10.1097/01.CCM.0000069345.78884.0F
48. Venet F., Pachot A., Debard A.L., Bohe J., Bienvenu J., Lepape A., Monneret G. Increased percentage of CD4+CD25+ regulatory T cells during septic shock is due to the decrease of CD4+CD25- lymphocytes. Crit Care Med. 2004; 32 (11): 2329-2331. doi:10.1097/01.CCM.0000145999.42971.4B
49. Huang H., Xu R., Lin F., Bao C., Wang S., Ji C., Li K., Jin L., Mu J., Wang Y, Li L., Sun L., Xu B., Zhang Z., Wang F.S. High circulating CD39+ regulatory T cells predict poor survival for sepsis patients. Int J Infect Dis. 2015; 30: 57-63. doi:10.1016/j.ijid.2014.11.006
50. Leng F. Y, Liu J.L., Liu Z.J., Yin J.Y, Qu H.P. Increased proportion of CD4+CD25+Foxp3+ regulatory T cells during early-stage sepsis in ICU patients. Journal of Microbiology, Immunology and Infection. 2013; 46 (5): 338-344. doi:10.1016/j.jmii.2012.06.012
51. MacConmara M.P., Maung A.A., Fujimi S., MacConmara M.P., Maung A.A., Fujimi S., McKenna A.M., Delisle A., Lapchak P.H., Rogers S., Lederer J.A., Mannick J.A. Increased CD4+ CD25+ T regulatory cell activity in trauma patients depresses protective Th1 immunity. Ann Surg. 2006; 244 (4): 514-523. doi:10.1097/01.sla.0000239031.06906.1f
52. Kuhlhorn F., Rath M., Schmoeckel K., Cziupka K., Nguyen H.H., Hildebrandt P., Hunig T., Sparwasser T., Huehn J., Potschke C., Broker B.M. Foxp3+ regulatory T cells are required for recovery from severe sepsis. PLoS One. 2013; 8 (5): e65109. doi:10.1371/journal.pone.0065109
53. Deaglio S., Dwyer K.M., Gao W., Friedman D., Usheva A., Erat A., Chen J.F., Enjyoji K., Linden J., Oukka M., Kuchroo V.K., Strom T.B., Robson S.C. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med. 2007; 204 (6): 1257-1265. doi:10.1084/jem.20062512
54. Chen K., Zhou Q.X., Shan H.W., Li W.F., Lin Z.F. Prognostic value of CD4+ CD25+ Tregs as a valuable biomarker for patients with sepsis in ICU. World J Emerg Med. 2015; 6 (1): 40-43. doi:10.5847/wjem.j.1920-8642.2015.01.007
Review
For citations:
Khanova M.Yu., Matveeva V.G., Antonova L.V., Grigoriev E.V. Role of regulatory T-cells in the systemic inflammatory response syndrome. Complex Issues of Cardiovascular Diseases. 2020;9(2):82-90. (In Russ.) https://doi.org/10.17802/2306-1278-2020-9-2-82-90
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