Adenosine promotes Foxp3 expression in treg cells in sepsis model by activating JNK/AP-1 pathway

American Journal of Translational Research

Volumn 8, Issue 5, 2016, Pages 2284-2292

  Bao, Rui ^a   Hou, Jiong ^a   Li, Yan ^a   Bian, Jinjun ^a   Deng, Xiaoming ^a   Zhu, Xiaoyan ^b   Yang, Tao ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Adenosine; Foxp3; JNK AP 1 pathway; Regulatory T cells; Sepsis

Indexed keywords

ADENOSINE; PROTEIN C FOS; PROTEIN C JUN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR FRA 2; TRANSCRIPTION FACTOR JUND;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GENETIC TRANSFECTION; NONHUMAN; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SEPSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 84971659095     PISSN: None     EISSN: 19438141     Source Type: Journal    
DOI: None     Document Type: Article

References (41)

1. Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL, Ramsay G. 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med 2003; 31: 1250-1256.
2. Angus DC, Wax RS. Epidemiology of sepsis: an update. Crit Care Med 2001; 29: S109-116.
3. Hotchkiss RS, Karl IE. The pathophysiology and treatment of sepsis. N Engl J Med 2003; 348: 138-150.
4. Hotchkiss RS, Coopersmith CM, McDunn JE, Ferguson TA. The sepsis seesaw: tilting toward immunosuppression. Nat Med 2009; 15: 496-497.
5. Boomer JS, To K, Chang KC, Takasu O, Osborne DF, Walton AH, Bricker TL, Jarman SD 2nd, Kreisel D, Krupnick AS, Srivastava A, Swanson PE, Green JM, Hotchkiss RS. Immunosuppression in patients who die of sepsis and multiple organ failure. JAMA 2011; 306: 2594-2605.
6. Busse M, Traeger T, Potschke C, Billing A, Dummer A, Friebe E, Kiank C, Grunwald U, Jack RS, Schutt C, Heidecke CD, Maier S, Broker BM. Detrimental role for CD4+ T lymphocytes in murine diffuse peritonitis due to inhibition of local bacterial elimination. Gut 2008; 57: 188-195.
7. Stromberg PE, Woolsey CA, Clark AT, Clark JA, Turnbull IR, McConnell KW, Chang KC, Chung CS, Ayala A, Buchman TG, Hotchkiss RS, Coopersmith CM. CD4+ lymphocytes control gut epithelial apoptosis and mediate survival in sepsis. FASEB J 2009; 23: 1817-1825.
8. Shevach EM, DiPaolo RA, Andersson J, Zhao DM, Stephens GL, Thornton AM. The lifestyle of naturally occurring CD4+ CD25+ Foxp3+ regulatory T cells. Immunol Rev 2006; 212: 60-73.
9. Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, Shimizu J, Takahashi T, Nomura T. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006; 212: 8-27.
10. Venet F, Chung CS, Monneret G, Huang X, Horner B, Garber M, Ayala A. Regulatory T cell populations in sepsis and trauma. J Leukoc Biol 2008; 83: 523-535.
11. Bacchetta R, Gambineri E, Roncarolo MG. Role of regulatory T cells and FOXP3 in human diseases. J Allergy Clin Immunol 2007; 120: 227-235; quiz 236-227.
12. Chatila TA. Role of regulatory T cells in human diseases. J Allergy Clin Immunol 2005; 116: 949-959; quiz 960.
13. Ramsdell F. Foxp3 and natural regulatory T cells: key to a cell lineage? Immunity 2003; 19: 165-168.
14. Leng FY, Liu JL, Liu ZJ, Yin JY, Qu HP. Increased proportion of CD4(+)CD25(+)Foxp3(+) regulatory T cells during early-stage sepsis in ICU patients. J Microbiol Immunol Infect 2013; 46: 338-344.
15. Nascimento DC, Alves-Filho JC, Sonego F, Fukada SY, Pereira MS, Benjamim C, Zamboni DS, Silva JS, Cunha FQ. Role of regulatory T cells in long-term immune dysfunction associated with severe sepsis. Crit Care Med 2010; 38: 1718-1725.
16. Shevach EM. CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002; 2: 389-400.
17. Scumpia PO, Delano MJ, Kelly KM, O’Malley KA, Efron PA, McAuliffe PF, Brusko T, Ungaro R, Barker T, Wynn JL, Atkinson MA, Reeves WH, Salzler MJ, Moldawer LL. Increased natural CD4+CD25+ regulatory T cells and their suppressor activity do not contribute to mortality in murine polymicrobial sepsis. J Immunol 2006; 177: 7943-7949.
18. Wichterman KA, Baue AE, Chaudry IH. Sepsis and septic shock--a review of laboratory models and a proposal. J Surg Res 1980; 29: 189-201.
19. Munford RS, Pugin J. Normal responses to injury prevent systemic inflammation and can be immunosuppressive. Am J Respir Crit Care Med 2001; 163: 316-321.
20. Kessel A, Bamberger E, Masalha M, Toubi E. The role of T regulatory cells in human sepsis. J Autoimmun 2009; 32: 211-215.
21. Cao C, Ma T, Chai YF, Shou ST. The role of regulatory T cells in immune dysfunction during sepsis. World J Emerg Med 2015; 6: 5-9.
22. Venet F, Pachot A, Debard AL, Bohe J, Bienvenu J, Lepape A, Monneret G. Increased percent- age of CD4+CD25+ regulatory T cells during septic shock is due to the decrease of CD4+CD25- lymphocytes. Crit Care Med 2004; 32: 2329-2331.
23. Ziegler SF, Buckner JH. Influence of FOXP3 on CD4+CD25+ regulatory T cells. Expert Rev Clin Immunol 2006; 2: 639-647.
24. Williams LM, Rudensky AY. Maintenance of the Foxp3-dependent developmental program in mature regulatory T cells requires continued expression of Foxp3. Nat Immunol 2007; 8: 277-284.
25. Wan YY, Flavell RA. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 2007; 445: 766-770.
26. Gavin MA, Rasmussen JP, Fontenot JD, Vasta V, Manganiello VC, Beavo JA, Rudensky AY. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 2007; 445: 771-775.
27. Lin W, Haribhai D, Relland LM, Truong N, Carlson MR, Williams CB, Chatila TA. Regulatory T cell development in the absence of functional Foxp3. Nat Immunol 2007; 8: 359-368.
28. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA, Wilkinson JE, Galas D, Ziegler SF, Ramsdell F. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 2001; 27: 68-73.
29. Ziegler SF. FOXP3: of mice and men. Annu. Rev. Immunol 2006; 24: 209-226.
30. Campbell DJ, Ziegler SF. FOXP3 modifies the phenotypic and functional properties of regulatory T cells. Nat Rev Immunol 2007; 7: 305-310.
31. Mandapathil M, Hilldorfer B, Szczepanski MJ, Czystowska M, Szajnik M, Ren J, Lang S, Jackson EK, Gorelik E, Whiteside TL. Generation and accumulation of immunosuppressive adenosine by human CD4+CD25high-FOXP3+ regulatory T cells. J Biol Chem 2010; 285: 7176-7186.
32. Zheng Y, Josefowicz S, Chaudhry A, Peng XP, Forbush K, Rudensky AY. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 2010; 463: 808-812.
33. Tone Y, Furuuchi K, Kojima Y, Tykocinski ML, Greene MI, Tone M. Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat Immunol 2008; 9: 194-202.
34. Yao Z, Kanno Y, Kerenyi M, Stephens G, Durant L, Watford WT, Laurence A, Robinson GW, Shevach EM, Moriggl R, Hennighausen L, Wu C, O’Shea JJ. Nonredundant roles for Stat5a/b in directly regulating Foxp3. Blood 2007; 109: 4368-4375.
35. Wu Y, Borde M, Heissmeyer V, Feuerer M, Lapan AD, Stroud JC, Bates DL, Guo L, Han A, Ziegler SF, Mathis D, Benoist C, Chen L, Rao A. FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell 2006; 126: 375-387.
36. Ono M, Yaguchi H, Ohkura N, Kitabayashi I, Nagamura Y, Nomura T, Miyachi Y, Tsukada T, Sakaguchi S. Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 2007; 446: 685-689.
37. Mantel PY, Ouaked N, Ruckert B, Karagiannidis C, Welz R, Blaser K, Schmidt-Weber CB. Molecular mechanisms underlying FOXP3 induction in human T cells. J Immunol 2006; 176: 3593-3602.
38. Tran DQ, Ramsey H, Shevach EM. Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood 2007; 110: 2983-2990.
39. Zarek PE, Huang CT, Lutz ER, Kowalski J, Horton MR, Linden J, Drake CG, Powell JD. A2A receptor signaling promotes peripheral tolerance by inducing T-cell anergy and the generation of adaptive regulatory T cells. Blood 2008; 111: 251-259.
40. Bynoe MS, Viret C. Foxp3+CD4+ T cell-mediated immunosuppression involves extracellular nucleotide catabolism. Trends Immunol 2008; 29: 99-102.
41. Xu L, Kitani A, Stuelten C, McGrady G, Fuss I, Strober W. Positive and negative transcriptional regulation of the Foxp3 gene is mediated by access and binding of the Smad3 protein to enhancer I. Immunity 2010; 33: 313-325.