Down-regulation of MicroRNA-31 in CD4+ T cells contributes to immunosuppression in human sepsis by promoting TH2skewing

Anesthesiology

Volumn 124, Issue 4, 2016, Pages 908-922

  Van Der Heide, Verena ^a   Möhnle, Patrick ^a   Rink, Jessica ^a   Briegel, Josef ^a   Kreth, Simone ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD150 ANTIGEN; GAMMA INTERFERON; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 2; INTERLEUKIN 4; MESSENGER RNA; MICRORNA 31; SMALL INTERFERING RNA; MICRORNA; MIRN31 MICRORNA, HUMAN;

ADULT; ARTICLE; BINDING SITE; CD4+ T LYMPHOCYTE; CELL FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; EPIGENETICS; FEMALE; FLOW CYTOMETRY; GENE; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; MALE; MIDDLE AGED; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; RNA BINDING; SEPSIS; SIGNAL TRANSDUCTION; TH2 CELL; WESTERN BLOTTING; CELL CULTURE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY;

ADULT; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DOWN-REGULATION; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNE TOLERANCE; MALE; MICRORNAS; MIDDLE AGED; REAL-TIME POLYMERASE CHAIN REACTION; SEPSIS; TH2 CELLS;

EID: 84955564018     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0000000000001031     Document Type: Article

References (66)

1. Levy MM, Artigas A, Phillips GS, Rhodes A, Beale R, Osborn T, Vincent JL, Townsend S, Lemeshow S, Dellinger RP: Outcomes of the Surviving Sepsis Campaign in intensive care units in the USA and Europe: A prospective cohort study. Lancet Infect Dis 2012; 12:919-24
2. Gaieski DF, Edwards JM, Kallan MJ, Carr BG: Benchmarking the incidence and mortality of severe sepsis in the United States. Crit Care Med 2013; 41:1167-74
3. Hotchkiss RS, Monneret G, Payen D: Sepsis-induced immu-nosuppression: From cellular dysfunctions to immunother-apy. Nat Rev Immunol 2013; 13:862-74
4. 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; 83:523-35
5. Cuenca AG, Delano MJ, Kelly-Scumpia KM, Moreno C, Scumpia PO, Laface DM, Heyworth PG, Efron PA, Moldawer LL: A paradoxical role for myeloid-derived suppressor cells in sepsis and trauma. Mol Med 2011; 17:281-92
6. Brudecki L, Ferguson DA, McCall CE, El Gazzar M: Myeloid-derived suppressor cells evolve during sepsis and can enhance or attenuate the systemic infammatory response. Infect Immun 2012; 80:2026-34
7. Boomer JS, Shuherk-Shaffer J, Hotchkiss RS, Green JM: A prospective analysis of lymphocyte phenotype and function over the course of acute sepsis. Crit Care 2012; 16:R112
8. Boomer JS, To K, Chang KC, Takasu O, Osborne DF, Walton AH, Bricker TL, Jarman SD II, 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; 306:2594-605
9. Hotchkiss RS, Swanson PE, Freeman BD, Tinsley KW, Cobb JP, Matuschak GM, Buchman TG, Karl IE: Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit Care Med 1999; 27:1230-51
10. Le Tulzo Y, Pangault C, Gacouin A, Guilloux V, Tribut O, Amiot L, Tattevin P, Thomas R, Fauchet R, Drénou B: Early circulating lymphocyte apoptosis in human septic shock is associated with poor outcome. Shock 2002; 18:487-94
11. Chang K, Svabek C, Vazquez-Guillamet C, Sato B, Rasche D, Wilson S, Robbins P, Ulbrandt N, Suzich J, Green J, Patera AC, Blair W, Krishnan S, Hotchkiss R: Targeting the programmed cell death 1: Programmed cell death ligand 1 pathway reverses T cell exhaustion in patients with sepsis. Crit Care 2014; 18:R3
12. Guignant C, Lepape A, Huang X, Kherouf H, Denis L, Poitevin F, Malcus C, Chéron A, Allaouchiche B, Gueyffer F, Ayala A, Monneret G, Venet F: Programmed death-1 levels correlate with increased mortality, nosocomial infection and immune dysfunctions in septic shock patients. Crit Care 2011; 15:R99
13. Shubin NJ, Chung CS, Heffernan DS, Irwin LR, Monaghan SF, Ayala A: BTLA expression contributes to septic morbidity and mortality by inducing innate infammatory cell dysfunction. J Leukoc Biol 2012; 92:593-603
14. Shubin NJ, Monaghan SF, Heffernan DS, Chung CS, Ayala A: B and T lymphocyte attenuator expression on CD4+ T-cells associates with sepsis and subsequent infections in ICU patients. Crit Care 2013; 17:R276
15. White M, Mahon V, Grealy R, Doherty DG, Stordeur P, Kelleher D P, McManus R, Ryan T: Post-operative infection and sepsis in humans is associated with defcient gene expression of γc cytokines and their apoptosis mediators. Crit Care 2011; 15:R158
16. Roth G, Moser B, Krenn C, Brunner M, Haisjackl M, Almer G, Gerlitz S, Wolner E, Boltz-Nitulescu G, Ankersmit HJ: Susceptibility to programmed cell death in T-lymphocytes from septic patients: A mechanism for lymphopenia and Th2 predominance. Biochem Biophys Res Commun 2003; 308:840-6
17. Bartel DP: MicroRNAs: Target recognition and regulatory functions. Cell 2009; 136:215-33
18. Montano M: MicroRNAs: miRRORS of health and disease. Transl Res 2011; 157:157-62
19. O'Connell RM, Rao DS, Baltimore D: microRNA regulation of infammatory responses. Annu Rev Immunol 2012; 30:295-312
20. Schetter AJ, Heegaard NH, Harris CC: Infammation and cancer: Interweaving microRNA, free radical, cytokine and p53 pathways. Carcinogenesis 2010; 31:37-49
21. Creighton CJ, Fountain MD, Yu Z, Nagaraja AK, Zhu H, Khan M, Olokpa E, Zariff A, Gunaratne PH, Matzuk MM, Anderson ML: Molecular profling uncovers a p53-associated role for microRNA-31 in inhibiting the proliferation of serous ovarian carcinomas and other cancers. Cancer Res 2010; 70:1906-15
22. Valastyan S, Reinhardt F, Benaich N, Calogrias D, Szász AM, Wang ZC, Brock JE, Richardson AL, Weinberg RA: A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 2009; 137:1032-46
23. Liu CJ, Tsai MM, Hung PS, Kao SY, Liu TY, Wu KJ, Chiou SH, Lin SC, Chang KW: miR-31 ablates expression of the HIF regulatory factor FIH to activate the HIF pathway in head and neck carcinoma. Cancer Res 2010; 70:1635-44
24. Yamagishi M, Nakano K, Miyake A, Yamochi T, Kagami Y, Tsutsumi A, Matsuda Y, Sato-Otsubo A, Muto S, Utsunomiya A, Yamaguchi K, Uchimaru K, Ogawa S, Watanabe T: Polycomb-mediated loss of miR-31 activates NIK-dependent NF-KB pathway in adult T cell leukemia and other cancers. Cancer Cell 2012; 21:121-35
25. Thiel M, Caldwell CC, Kreth S, Kuboki S, Chen P, Smith P, Ohta A, Lentsch AB, Lukashev D, Sitkovsky MV: Targeted deletion of HIF-1alpha gene in T cells prevents their inhibition in hypoxic infamed tissues and improves septic mice survival. PLoS One 2007; 2:e853
26. Lukashev D, Klebanov B, Kojima H, Grinberg A, Ohta A, Berenfeld L, Wenger RH, Ohta A, Sitkovsky M: Cutting edge: Hypoxia-inducible factor 1alpha and its activation-inducible short isoform I.1 negatively regulate functions of CD4+ and CD8+ T lymphocytes. J Immunol 2006; 177:4962-5
27. Eltzschig HK, Carmeliet P: Hypoxia and infammation. N Engl J Med 2011; 364:656-65
28. Taylor CT: Interdependent roles for hypoxia inducible factor and nuclear factor-kappaB in hypoxic infammation. J Physiol 2008; 586(Pt 17):4055-9
29. Gerondakis S, Fulford TS, Messina NL, Grumont RJ: NF-KB control of T cell development. Nat Immunol 2014; 15:15-25
30. Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL, Ramsay G; SCCM/ESICM/ACCP/ATS/SIS: 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Defnitions Conference. Crit Care Med 2003; 31:1250-6
31. Ledderose C, Möhnle P, Limbeck E, Schütz S, Weis F, Rink J, Briegel J, Kreth S: Corticosteroid resistance in sepsis is infuenced by microRNA-124-induced downregulation of glucocorticoid receptor-a. Crit Care Med 2012; 40:2745-53
32. Möhnle P, Schütz SV, van der Heide V, Hübner M, Luchting B, Sedlbauer J, Limbeck E, Hinske LC, Briegel J, Kreth S: MicroRNA-146a controls Th1-cell differentiation of human CD4+ T lymphocytes by targeting PRKCe. Eur J Immunol 2015; 45:260-72
33. Lewis BP, Burge CB, Bartel DP: Conserved seed pairing, often fanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120:15-20
34. Ledderose C, Heyn J, Limbeck E, Kreth S: Selection of reliable reference genes for quantitative real-time PCR in human T cells and neutrophils. BMC Res Notes 2011; 4:427
35. Betel D, Koppal A, Agius P, Sander C, Leslie C: Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol 2010; 11:R90
36. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS: Human MicroRNA targets. PLoS Biol 2004; 2:e363
37. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E: The role of site accessibility in microRNA target recognition. Nat Genet 2007; 39:1278-84
38. Asangani IA, Harms PW, Dodson L, Pandhi M, Kunju LP, Maher CA, Fullen DR, Johnson TM, Giordano TJ, Palanisamy N, Chinnaiyan AM: Genetic and epigenetic loss of microRNA-31 leads to feed-forward expression of EZH2 in melanoma. Oncotarget 2012; 3:1011-25
39. McNamee EN, Korns Johnson D, Homann D, Clambey ET: Hypoxia and hypoxia-inducible factors as regulators of T cell development, differentiation, and function. Immunol Res 2013; 55:58-70
40. Caldwell CC, Kojima H, Lukashev D, Armstrong J, Farber M, Apasov SG, Sitkovsky MV: Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J Immunol 2001; 167:6140-9
41. Cannons JL, Yu LJ, Hill B, Mijares LA, Dombroski D, Nichols KE, Antonellis A, Koretzky GA, Gardner K, Schwartzberg PL: SAP regulates T(H)2 differentiation and PKC-theta-mediated activation of NF-kappaB1. Immunity 2004; 21:693-706
42. Czar MJ, Kersh EN, Mijares LA, Lanier G, Lewis J, Yap G, Chen A, Sher A, Duckett CS, Ahmed R, Schwartzberg PL: Altered lymphocyte responses and cytokine production in mice defcient in the X-linked lymphoproliferative disease gene SH2D1A/DSHP/SAP. Proc Natl Acad Sci USA 2001; 98:7449-54
43. Ferreira FL, Bota DP, Bross A, Mélot C, Vincent JL: Serial evaluation of the SOFA score to predict outcome in critically ill patients. JAMA 2001; 286:1754-8
44. Held TK, Weihua X, Yuan L, Kalvakolanu DV, Cross AS: Gamma interferon augments macrophage activation by lipo-polysaccharide by two distinct mechanisms, at the signal transduction level and via an autocrine mechanism involving tumor necrosis factor alpha and interleukin-1. Infect Immun 1999; 67:206-12
45. Murphey ED, Lin CY, McGuire RW, Toliver-Kinsky T, Herndon DN, Sherwood ER: Diminished bacterial clearance is associated with decreased IL-12 and interferon-gamma production but a sustained proinfammatory response in a murine model of postseptic immunosuppression. Shock 2004; 21:415-25
46. Smeltz RB, Chen J, Ehrhardt R, Shevach EM: Role of IFN-gamma in Th1 differentiation: IFN-gamma regulates IL-18R alpha expression by preventing the negative effects of IL-4 and by inducing/maintaining IL-12 receptor beta 2 expression. J Immunol 2002; 168:6165-72
47. Song GY, Chung CS, Chaudry IH, Ayala A: IL-4-induced activation of the Stat6 pathway contributes to the suppression of cell-mediated immunity and death in sepsis. Surgery 2000; 128:133-8
48. Bogdan C, Vodovotz Y, Paik J, Xie QW, Nathan C: Mechanism of suppression of nitric oxide synthase expression by inter-leukin-4 in primary mouse macrophages. J Leukoc Biol 1994; 55:227-33
49. Williams MA, Tyznik AJ, Bevan MJ: Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature 2006; 441:890-3
50. Liu R, Zhou Q, La Cava A, Campagnolo DI, Van Kaer L, Shi FD: Expansion of regulatory T cells via IL-2/anti-IL-2 mAb complexes suppresses experimental myasthenia. Eur J Immunol 2010; 40:1577-89
51. Tang Q, Adams JY, Penaranda C, Melli K, Piaggio E, Sgouroudis E, Piccirillo CA, Salomon BL, Bluestone JA: Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 2008; 28:687-97
52. Sánchez-Valdepeñas C, Martín AG, Ramakrishnan P, Wallach D, Fresno M: NF-kappaB-inducing kinase is involved in the activation of the CD28 responsive element through phosphorylation of c-Rel and regulation of its transactivating activity. J Immunol 2006; 176:4666-74
53. Matsumoto M, Yamada T, Yoshinaga SK, Boone T, Horan T, Fujita S, Li Y, Mitani T: Essential role of NF-kappa B-inducing kinase in T cell activation through the TCR/CD3 pathway. J Immunol 2002; 169:1151-8
54. Yamada T, Mitani T, Yorita K, Uchida D, Matsushima A, Iwamasa K, Fujita S, Matsumoto M: Abnormal immune function of hemopoietic cells from alymphoplasia (aly) mice, a natural strain with mutant NF-kappa B-inducing kinase. J Immunol 2000; 165:804-12
55. Bartels K, Grenz A, Eltzschig HK: Hypoxia and infammation are two sides of the same coin. Proc Natl Acad Sci USA 2013; 110:18351-2
56. Schwartzberg PL, Mueller KL, Qi H, Cannons JL: SLAM receptors and SAP infuence lymphocyte interactions, development and function. Nat Rev Immunol 2009; 9:39-46
57. Veillette A: SLAM-family receptors: Immune regulators with or without SAP-family adaptors. Cold Spring Harb Perspect Biol 2010; 2:a002469
58. Fan W, Liang D, Tang Y, Qu B, Cui H, Luo X, Huang X, Chen S, Higgs BW, Jallal B, Yao Y, Harley JB, Shen N: Identifcation of microRNA-31 as a novel regulator contributing to impaired interleukin-2 production in T cells from patients with systemic lupus erythematosus. Arthritis Rheum 2012; 64:3715-25
59. Song H, Wang Q, Guo Y, Liu S, Song R, Gao X, Dai L, Li B, Zhang D, Cheng J: Microarray analysis of microRNA expression in peripheral blood mononuclear cells of critically ill patients with infuenza A (H1N1). BMC Infect Dis 2013; 13:257
60. Roger PM, Hyvernat H, Ticchioni M, Kumar G, Dellamonica J, Bernardin G: The early phase of human sepsis is characterized by a combination of apoptosis and proliferation of T cells. J Crit Care 2012; 27:384-93
61. DiPiro JT, Howdieshell TR, Goddard JK, Callaway DB, Hamilton RG, Mansberger AR Jr: Association of interleukin-4 plasma levels with traumatic injury and clinical course. Arch Surg 1995; 130:1159-62; discussion 1162-3
62. Wu HP, Wu CL, Chen CK, Chung K, Tseng JC, Liu YC, Chuang DY: The interleukin-4 expression in patients with severe sepsis. J Crit Care 2008; 23:519-24
63. Cifuentes-Rojas C, Hernandez AJ, Sarma K, Lee JT: Regulatory interactions between RNA and polycomb repressive complex 2. Mol Cell 2014; 55:171-85
64. Margueron R, Reinberg D: The Polycomb complex PRC2 and its mark in life. Nature 2011; 469:343-9
65. Kirmizis A, Bartley SM, Kuzmichev A, Margueron R, Reinberg D, Green R, Farnham PJ: Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev 2004; 18:1592-605
66. Kondo Y: Targeting histone methyltransferase EZH2 as cancer treatment. J Biochem 2014; 156:249-57