miR-182 and miR-10a Are Key Regulators of Treg Specialisation and Stability during Schistosome and Leishmania-associated Inflammation

PLoS Pathogens

Volumn 9, Issue 6, 2013, Pages

  Kelada, Samir ^a   Sethupathy, Praveen ^a   Okoye, Isobel S ^b   Kistasis, Eleni ^b   Czieso, Stephanie ^b   White, Sandra D ^c   Chou, David ^c   Martens, Craig ^d   Ricklefs, Stacy M ^d   Virtaneva, Kimmo ^d   Sturdevant, Dan E ^d   Porcella, Stephen F ^d   Belkaid, Yasmine ^c   Wynn, Thomas A ^c   Wilson, Mark S ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 4; MICRORNA; MICRORNA 10A; MICRORNA 182; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENVIRONMENTAL FACTOR; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; INFLAMMATION; LEISHMANIA MAJOR; LEISHMANIASIS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA SEQUENCE; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS;

ANIMALS; CYTOKINES; INFLAMMATION; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MICE, KNOCKOUT; MICRORNAS; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TH2 CELLS;

LEISHMANIA MAJOR; SCHISTOSOMA; SCHISTOSOMA MANSONI;

EID: 84879545797     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003451     Document Type: Article

References (89)

1. Bennett CL, Brunkow ME, Ramsdell F, O'Briant KC, Zhu Q, et al. (2001) A rare polyadenylation signal mutation of the FOXP3 gene (AAUAAA→AAUGAA) leads to the IPEX syndrome. Immunogenetics 53: 435-439.
2. Rubtsov YP, Rasmussen JP, Chi EY, Fontenot J, Castelli L, et al. (2008) Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28: 546-558.
3. Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T, Miyara M, et al. (2008) CTLA-4 control over Foxp3+ regulatory T cell function. Science 322: 271-275.
4. Chatila TA, (2005) Role of regulatory T cells in human diseases. J Allergy Clin Immunol 116: 949-959; quiz 960.
5. Lin W, Truong N, Grossman WJ, Haribhai D, Williams CB, et al. (2005) Allergic dysregulation and hyperimmunoglobulinemia E in Foxp3 mutant mice. J Allergy Clin Immunol 116: 1106-1115.
6. Kim JM, Rasmussen JP, Rudensky AY, (2007) Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol 8: 191-197.
7. Wright GP, Stauss HJ, Ehrenstein MR, (2011) Therapeutic potential of Tregs to treat rheumatoid arthritis. Semin Immunol 23: 195-201.
8. Belkaid Y, Tarbell K, (2009) Regulatory T cells in the control of host-microorganism interactions (*). Annu Rev Immunol 27: 551-589.
9. Marson A, Kretschmer K, Frampton GM, Jacobsen ES, Polansky JK, et al. (2007) Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 445: 931-935.
10. Chaudhry A, Rudra D, Treuting P, Samstein RM, Liang Y, et al. (2009) CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 326: 986-991.
11. Chung Y, Tanaka S, Chu F, Nurieva RI, Martinez GJ, et al. (2011) Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat Med 17: 983-988.
12. Koch MA, Tucker-Heard G, Perdue NR, Killebrew JR, Urdahl KB, et al. (2009) The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol 10: 595-602.
13. Linterman MA, Pierson W, Lee SK, Kallies A, Kawamoto S, et al. (2011) Foxp3+ follicular regulatory T cells control the germinal center response. Nat Med 17: 975-982.
14. Zheng Y, Chaudhry A, Kas A, deRoos P, Kim JM, et al. (2009) Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature 458: 351-356.
15. Lal G, Bromberg JS, (2009) Epigenetic mechanisms of regulation of Foxp3 expression. Blood 114: 3727-3735.
16. Ha TY, (2011) The Role of MicroRNAs in Regulatory T Cells and in the Immune Response. Immune Netw 11: 11-41.
17. O'Connell RM, Rao DS, Chaudhuri AA, Baltimore D, (2010) Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 10: 111-122.
18. Leung AK, Sharp PA, (2010) MicroRNA functions in stress responses. Mol Cell 40: 205-215.
19. Chong MM, Rasmussen JP, Rudensky AY, Littman DR, (2008) The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J Exp Med 205: 2005-2017.
20. Cobb BS, Nesterova TB, Thompson E, Hertweck A, O'Connor E, et al. (2005) T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J Exp Med 201: 1367-1373.
21. Muljo SA, Ansel KM, Kanellopoulou C, Livingston DM, Rao A, et al. (2005) Aberrant T cell differentiation in the absence of Dicer. J Exp Med 202: 261-269.
22. Liston A, Lu LF, O'Carroll D, Tarakhovsky A, Rudensky AY, (2008) Dicer-dependent microRNA pathway safeguards regulatory T cell function. J Exp Med 205: 1993-2004.
23. Zhou X, Jeker LT, Fife BT, Zhu S, Anderson MS, et al. (2008) Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J Exp Med 205: 1983-1991.
24. Fayyad-Kazan H, Rouas R, Fayyad-Kazan M, Badran R, El Zein N, et al. (2012) MicroRNA profile of circulating CD4-positive regulatory T cells in human adults and the impact of differentially expressed microRNAs on the expression of two genes essential to their function. The Journal of biological chemistry 287: 9910-22.
25. Beyer M, Thabet Y, Muller RU, Sadlon T, Classen S, et al. (2011) Repression of the genome organizer SATB1 in regulatory T cells is required for suppressive function and inhibition of effector differentiation. Nature immunology 12: 898-907.
26. Lu LF, Thai TH, Calado DP, Chaudhry A, Kubo M, et al. (2009) Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 30: 80-91.
27. Lu LF, Boldin MP, Chaudhry A, Lin LL, Taganov KD, et al. (2010) Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 142: 914-929.
28. Friedman RC, Farh KK, Burge CB, Bartel DP, (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
29. Vickers KC, Shoucri B, Levin MG, Wu H, Pearson DS, et al. (2012) MicroRNA-27b is a regulatory hub in lipid metabolism and is altered in dyslipidemia. Hepatology 57: 533-42.
30. Lesniewski ML, Haviernik P, Weitzel RP, Kadereit S, Kozik MM, et al. (2008) Regulation of IL-2 expression by transcription factor BACH2 in umbilical cord blood CD4+ T cells. Leukemia 22: 2201-2207.
31. Hutchings NJ, Clarkson N, Chalkley R, Barclay AN, Brown MH, (2003) Linking the T cell surface protein CD2 to the actin-capping protein CAPZ via CMS and CIN85. J Biol Chem 278: 22396-22403.
32. Sacks D, Anderson C, (2004) Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice. Immunol Rev 201: 225-238.
33. Wilson MS, Mentink-Kane MM, Pesce JT, Ramalingam TR, Thompson R, et al. (2007) Immunopathology of schistosomiasis. Immunol Cell Biol 85: 148-154.
34. Baumgart M, Tompkins F, Leng J, Hesse M, (2006) Naturally occurring CD4+Foxp3+ regulatory T cells are an essential, IL-10-independent part of the immunoregulatory network in Schistosoma mansoni egg-induced inflammation. J Immunol 176: 5374-5387.
35. Lages CS, Suffia I, Velilla PA, Huang B, Warshaw G, et al. (2008) Functional regulatory T cells accumulate in aged hosts and promote chronic infectious disease reactivation. J Immunol 181: 1835-1848.
36. Layland LE, Mages J, Loddenkemper C, Hoerauf A, Wagner H, et al. (2010) Pronounced phenotype in activated regulatory T cells during a chronic helminth infection. J Immunol 184: 713-724.
37. Singh KP, Gerard HC, Hudson AP, Reddy TR, Boros DL, (2005) Retroviral Foxp3 gene transfer ameliorates liver granuloma pathology in Schistosoma mansoni infected mice. Immunology 114: 410-417.
38. Suffia IJ, Reckling SK, Piccirillo CA, Goldszmid RS, Belkaid Y, (2006) Infected site-restricted Foxp3+ natural regulatory T cells are specific for microbial antigens. J Exp Med 203: 777-788.
39. Turner JD, Jenkins GR, Hogg KG, Aynsley SA, Paveley RA, et al. (2011) CD4CD25 Regulatory Cells Contribute to the Regulation of Colonic Th2 Granulomatous Pathology Caused by Schistosome Infection. PLoS Negl Trop Dis 5: e1269.
40. Takahashi H, Kanno T, Nakayamada S, Hirahara K, Sciume G, et al. (2012) TGF-beta and retinoic acid induce the microRNA miR-10a, which targets Bcl-6 and constrains the plasticity of helper T cells. Nat Immunol 13: 587-95.
41. Lagos D, Pollara G, Henderson S, Gratrix F, Fabani M, et al. (2010) miR-132 regulates antiviral innate immunity through suppression of the p300 transcriptional co-activator. Nat Cell Biol 12: 513-519.
42. Stittrich AB, Haftmann C, Sgouroudis E, Kuhl AA, Hegazy AN, et al. (2010) The microRNA miR-182 is induced by IL-2 and promotes clonal expansion of activated helper T lymphocytes. Nat Immunol 11: 1057-1062.
43. Fang Y, Shi C, Manduchi E, Civelek M, Davies PF, (2010) MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc Natl Acad Sci U S A 107: 13450-13455.
44. Bettini ML, Pan F, Bettini M, Finkelstein D, Rehg JE, et al. (2012) Loss of epigenetic modification driven by the Foxp3 transcription factor leads to regulatory T cell insufficiency. Immunity 36: 717-730.
45. Darce J, Rudra D, Li L, Nishio J, Cipolletta D, et al. (2012) An N-terminal mutation of the Foxp3 transcription factor alleviates arthritis but exacerbates diabetes. Immunity 36: 731-741.
46. Sekiya T, Kashiwagi I, Inoue N, Morita R, Hori S, et al. (2011) The nuclear orphan receptor Nr4a2 induces Foxp3 and regulates differentiation of CD4+ T cells. Nature communications 2: 269.
47. Dominguez-Villar M, Baecher-Allan CM, Hafler DA, (2011) Identification of T helper type 1-like, Foxp3+ regulatory T cells in human autoimmune disease. Nat Med 17: 673-675.
48. Feng T, Cao AT, Weaver CT, Elson CO, Cong Y, (2011) Interleukin-12 converts Foxp3+ regulatory T cells to interferon-gamma-producing Foxp3+ T cells that inhibit colitis. Gastroenterology 140: 2031-2043.
49. Feuerer M, Hill JA, Kretschmer K, von Boehmer H, Mathis D, et al. (2010) Genomic definition of multiple ex vivo regulatory T cell subphenotypes. Proc Natl Acad Sci U S A 107: 5919-5924.
50. Lohoff M, Mittrucker HW, Prechtl S, Bischof S, Sommer F, et al. (2002) Dysregulated T helper cell differentiation in the absence of interferon regulatory factor 4. Proc Natl Acad Sci U S A 99: 11808-11812.
51. Staudt V, Bothur E, Klein M, Lingnau K, Reuter S, et al. (2010) Interferon-regulatory factor 4 is essential for the developmental program of T helper 9 cells. Immunity 33: 192-202.
52. Gao Y, Lin F, Su J, Gao Z, Li Y, et al. (2012) Molecular mechanisms underlying the regulation and functional plasticity of FOXP3(+) regulatory T cells. Genes Immun 13: 1-13.
53. Kuwahara M, Yamashita M, Shinoda K, Tofukuji S, Onodera A, et al. (2012) The transcription factor Sox4 is a downstream target of signaling by the cytokine TGF-beta and suppresses T(H)2 differentiation. Nat Immunol 13: 778-786.
54. Kerdiles YM, Stone EL, Beisner DR, McGargill MA, Ch'en IL, et al. (2010) Foxo transcription factors control regulatory T cell development and function. Immunity 33: 890-904.
55. Ouyang W, Beckett O, Ma Q, Paik JH, DePinho RA, et al. (2010) Foxo proteins cooperatively control the differentiation of Foxp3+ regulatory T cells. Nat Immunol 11: 618-627.
56. Cao S, Liu J, Song L, Ma X, (2005) The protooncogene c-Maf is an essential transcription factor for IL-10 gene expression in macrophages. J Immunol 174: 3484-3492.
57. Ho IC, Hodge MR, Rooney JW, Glimcher LH, (1996) The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 85: 973-983.
58. Verma ND, Plain KM, Nomura M, Tran GT, Robinson C, et al. (2009) CD4+CD25+ T cells alloactivated ex vivo by IL-2 or IL-4 become potent alloantigen-specific inhibitors of rejection with different phenotypes, suggesting separate pathways of activation by Th1 and Th2 responses. Blood 113: 479-487.
59. Yates J, Rovis F, Mitchell P, Afzali B, Tsang JY, et al. (2007) The maintenance of human CD4+ CD25+ regulatory T cell function: IL-2, IL-4, IL-7 and IL-15 preserve optimal suppressive potency in vitro. Int Immunol 19: 785-799.
60. Skapenko A, Kalden JR, Lipsky PE, Schulze-Koops H, (2005) The IL-4 receptor alpha-chain-binding cytokines, IL-4 and IL-13, induce forkhead box P3-expressing CD25+CD4+ regulatory T cells from CD25-CD4+ precursors. J Immunol 175: 6107-6116.
61. Li W, Whaley CD, Mondino A, Mueller DL, (1996) Blocked signal transduction to the ERK and JNK protein kinases in anergic CD4+ T cells. Science 271: 1272-1276.
62. Su L, Creusot RJ, Gallo EM, Chan SM, Utz PJ, et al. (2004) Murine CD4+CD25+ regulatory T cells fail to undergo chromatin remodeling across the proximal promoter region of the IL-2 gene. J Immunol 173: 4994-5001.
63. Wang L, de Zoeten EF, Greene MI, Hancock WW, (2009) Immunomodulatory effects of deacetylase inhibitors: therapeutic targeting of FOXP3+ regulatory T cells. Nat Rev Drug Discov 8: 969-981.
64. Saouaf SJ, Li B, Zhang G, Shen Y, Furuuchi N, et al. (2009) Deacetylase inhibition increases regulatory T cell function and decreases incidence and severity of collagen-induced arthritis. Exp Mol Pathol 87: 99-104.
65. Tao R, de Zoeten EF, Ozkaynak E, Chen C, Wang L, et al. (2007) Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med 13: 1299-1307.
66. de Zoeten EF, Wang L, Sai H, Dillmann WH, Hancock WW, (2009) Inhibition of HDAC9 increases T regulatory cell function and prevents colitis in mice. Gastroenterology 138: 583-594.
67. Jeker LT, Zhou X, Gershberg K, de Kouchkovsky D, Morar MM, et al. (2012) MicroRNA 10a marks regulatory T cells. PLoS One 7: e36684.
68. Jang YS, Kim JH, Seo GY, Kim PH, (2011) TGF-beta1 stimulates mouse macrophages to express APRIL through Smad and p38MAPK/CREB pathways. Mol Cells 32: 251-255.
69. Herblot S, Chastagner P, Samady L, Moreau JL, Demaison C, et al. (1999) IL-2-dependent expression of genes involved in cytoskeleton organization, oncogene regulation, and transcriptional control. J Immunol 162: 3280-3288.
70. Yano S, Ghosh P, Kusaba H, Buchholz M, Longo DL, (2003) Effect of promoter methylation on the regulation of IFN-gamma gene during in vitro differentiation of human peripheral blood T cells into a Th2 population. J Immunol 171: 2510-2516.
71. Hu X, Paik PK, Chen J, Yarilina A, Kockeritz L, et al. (2006) IFN-gamma suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/AP-1 proteins. Immunity 24: 563-574.
72. Kim HP, Leonard WJ, (2007) CREB/ATF-dependent T cell receptor-induced FoxP3 gene expression: a role for DNA methylation. J Exp Med 204: 1543-1551.
73. Grimes CA, Jope RS, (2001) CREB DNA binding activity is inhibited by glycogen synthase kinase-3 beta and facilitated by lithium. J Neurochem 78: 1219-1232.
74. Wen AY, Sakamoto KM, Miller LS, (2010) The role of the transcription factor CREB in immune function. J Immunol 185: 6413-6419.
75. Draheim KM, Chen HB, Tao Q, Moore N, Roche M, et al. (2010) ARRDC3 suppresses breast cancer progression by negatively regulating integrin beta4. Oncogene 29: 5032-5047.
76. Nabhan JF, Pan H, Lu Q, (2010) Arrestin domain-containing protein 3 recruits the NEDD4 E3 ligase to mediate ubiquitination of the beta2-adrenergic receptor. EMBO Rep 11: 605-611.
77. Hansen W, Loser K, Westendorf AM, Bruder D, Pfoertner S, et al. (2006) G protein-coupled receptor 83 overexpression in naive CD4+CD25- T cells leads to the induction of Foxp3+ regulatory T cells in vivo. J Immunol 177: 209-215.
78. Shi Y, Feng Y, Kang J, Liu C, Li Z, et al. (2007) Critical regulation of CD4+ T cell survival and autoimmunity by beta-arrestin 1. Nat Immunol 8: 817-824.
79. Barrios-Rodiles M, Brown KR, Ozdamar B, Bose R, Liu Z, et al. (2005) High-throughput mapping of a dynamic signaling network in mammalian cells. Science 307: 1621-1625.
80. Bluteau D, Gilles L, Hilpert M, Antony-Debre I, James C, et al. (2005) Down-regulation of the RUNX1-target gene NR4A3 contributes to hematopoiesis deregulation in familial platelet disorder/acute myelogenous leukemia (FPD/AML). Blood 118: 6310-20.
81. Onoyama I, Tsunematsu R, Matsumoto A, Kimura T, de Alboran IM, et al. (2007) Conditional inactivation of Fbxw7 impairs cell-cycle exit during T cell differentiation and results in lymphomatogenesis. J Exp Med 204: 2875-2888.
82. Mullican SE, Zhang S, Konopleva M, Ruvolo V, Andreeff M, et al. (2007) Abrogation of nuclear receptors Nr4a3 and Nr4a1 leads to development of acute myeloid leukemia. Nat Med 13: 730-735.
83. Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, et al. (2005) Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22: 329-341.
84. Wan YY, Flavell RA, (2005) Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc Natl Acad Sci U S A 102: 5126-5131.
85. Wilson MS, Elnekave E, Mentink-Kane MM, Hodges MG, Pesce JT, et al. (2007) IL-13Ralpha2 and IL-10 coordinately suppress airway inflammation, airway-hyperreactivity, and fibrosis in mice. J Clin Invest 117: 2941-2951.
86. Kozomara A, Griffiths-Jones S, (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic acids research 39: D152-157.
87. Corcoran DL, Pandit KV, Gordon B, Bhattacharjee A, Kaminski N, et al. (2009) Features of mammalian microRNA promoters emerge from polymerase II chromatin immunoprecipitation data. PloS one 4: e5279.
88. Stitzel ML, Sethupathy P, Pearson DS, Chines PS, Song L, et al. (2010) Global epigenomic analysis of primary human pancreatic islets provides insights into type 2 diabetes susceptibility loci. Cell metabolism 12: 443-455.
89. Levy S, Hannenhalli S, (2002) Identification of transcription factor binding sites in the human genome sequence. Mammalian genome: official journal of the International Mammalian Genome Society 13: 510-514.