Critical role of Bcl11b in suppressor function of T regulatory cells and prevention of inflammatory bowel disease

Journal of Experimental Medicine

Volumn 208, Issue 10, 2011, Pages 2069-2081

  VanValkenburgh, Jeffrey ^a   Albu, Diana I ^a   Bapanpally, Chandra ^a   Casanova, Sarah ^a   Califano, Danielle ^a   Jones, David M ^a   Ignatowicz, Leszek ^b   Kawamoto, Shimpei ^c   Fagarasan, Sidonia ^c   Jenkins, Nancy A ^d   Copeland, Neal G ^d   Liu, Pentao ^e   Avram, Dorina ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c RIKEN Center for Integrative Medical Sciences   (Japan)

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; INTERLEUKIN 17; LUCIFERASE; MESSENGER RNA; PROTEIN BCL11B; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE DISEASE; BINDING SITE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLON MUCOSA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENTERITIS; FOXP3 GENE; GENE EXPRESSION PROFILING; GENE LOCUS; IL 10 GENE; IMMUNE RESPONSE; IMMUNOREGULATION; LAMINA PROPRIA; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INDUCTION; REGULATORY T LYMPHOCYTE; REPORTER GENE; TH1 CELL; TH17 CELL; UPREGULATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; COLON; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATORY BOWEL DISEASES; INTEGRINS; INTERLEUKIN-10; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, CCR; REPRESSOR PROTEINS; T-LYMPHOCYTES, REGULATORY; TUMOR SUPPRESSOR PROTEINS;

EID: 80555139651     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20102683     Document Type: Article

References (51)

1. Ahyi, A.N., H.C. Chang, A.L. Dent, S.L. Nutt, and M.H. Kaplan. 2009. IFN regulatory factor 4 regulates the expression of a subset of Th2 cytokines. J. Immunol. 183:1598-1606.
2. Albu, D.I., D. Feng, D. Bhattacharya, N.A. Jenkins, N.G. Copeland, P. Liu, and D. Avram. 2007. BCL11B is required for positive selection and survival of double-positive thymocytes. J. Exp. Med. 204:3003-3015.
3. Avram, D., A. Fields, K. Pretty On Top, D.J. Nevrivy, J.E. Ishmael, and M. Leid. 2000. Isolation of a novel family of C(2)H(2) zinc finger proteins implicated in transcriptional repression mediated by chicken ovalbumin upstream promoter transcription factor (COUP-TF) orphan nuclear receptors. J. Biol. Chem. 275:10315-10322.
4. Avram, D., A. Fields, T. Senawong, A. Topark-Ngarm, and M. Leid. 2002. COUP-TF (chicken ovalbumin upstream promoter transcription factor)-interacting protein 1 (CTIP1) is a sequence-specific DNA binding protein. Biochem. J. 368:555-563.
5. Bennett, C.L., J. Christie, F. Ramsdell, M.E. Brunkow, P.J. Ferguson, L. Whitesell, T.E. Kelly, F.T. Saulsbury, P.F. Chance, and H.D. Ochs. 2001. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat. Genet. 27:20- 21.
6. Brunkow, M.E., E.W. Jeffery, K.A. Hjerrild, B. Paeper, L.B. Clark, S.A. Yasayko, J.E. Wilkinson, D. Galas, S.F. Ziegler, and F. Ramsdell. 2001. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27:68-73.
7. Chaudhry, A., D. Rudra, P. Treuting, R.M. Samstein, Y. Liang, A. Kas, and A.Y. Rudensky. 2009. CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science. 326:986-991.
8. Cismasiu, V.B., K. Adamo, J. Gecewicz, J. Duque, Q. Lin, and D. Avram. 2005. BCL11B functionally associates with the NuRD complex in T lymphocytes to repress targeted promoter. Oncogene. 24:6753-6764.
9. Cismasiu, V.B., S. Ghanta, J. Duque, D.I. Albu, H.M. Chen, R. Kasturi, and D. Avram. 2006. BCL11B participates in the activation of IL2 gene expression in CD4+ T lymphocytes. Blood. 108:2695-2702.
10. Cismasiu, V.B., E. Paskaleva, S. Suman Daya, M. Canki, K. Duus, and D. Avram. 2008. BCL11B is a general transcriptional repressor of the HIV-1 long terminal repeat in T lymphocytes through recruitment of the NuRD complex. Virology. 380:173-181.
11. Cismasiu, V.B., J. Duque, E. Paskaleva, D. Califano, S. Ghanta, H.A. Young, and D. Avram. 2009. BCL11B enhances TCR/CD28-triggered NF-kappaB activation through up-regulation of Cot kinase gene expression in T-lymphocytes. Biochem. J. 417:457-466.
12. Das, G., M.M. Augustine, J. Das, K. Bottomly, P. Ray, and A. Ray. 2003. An important regulatory role for CD4+CD8 alpha alpha T cells in the intestinal epithelial layer in the prevention of inflammatory bowel disease. Proc. Natl. Acad. Sci. USA. 100:5324-5329.
13. Fontenot, J.D., M.A. Gavin, and A.Y. Rudensky. 2003. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4:330-336.
14. Fontenot, J.D., J.P. Rasmussen, L.M. Williams, J.L. Dooley, A.G. Farr, and A.Y. Rudensky. 2005. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity. 22:329-341.
15. Hill, J.A., M. Feuerer, K. Tash, S. Haxhinasto, J. Perez, R. Melamed, D. Mathis, and C. Benoist. 2007. Foxp3 transcription-factor-dependent and -independent regulation of the regulatory T cell transcriptional signature. Immunity. 27:786-800.
16. Huang, D.W., B.T. Sherman, and R.A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44-57.
17. Ikawa, T., S. Hirose, K. Masuda, K. Kakugawa, R. Satoh, A. Shibano-Satoh, R. Kominami, Y. Katsura, and H. Kawamoto. 2010. An essential developmental checkpoint for production of the T cell lineage. Science. 329:93- 96.
18. Ito, R., M. Shin-Ya, T. Kishida, A. Urano, R. Takada, J. Sakagami, J. Imanishi, M. Kita, Y. Ueda, Y. Iwakura, et al. 2006. Interferon-gamma is causatively involved in experimental inflammatory bowel disease in mice. Clin. Exp. Immunol. 146:330-338.
19. Izcue, A., J.L. Coombes, and F. Powrie. 2006. Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation. Immunol. Rev. 212:256-271.
20. Jones, E.A., and R.A. Flavell. 2005. Distal enhancer elements transcribe intergenic RNA in the IL-10 family gene cluster. J. Immunol. 175:7437-7446.
21. Kim, H.P., and W.J. Leonard. 2007. CREB/ATF-dependent T cell receptor-in 1543-1551.
22. Kitoh, A., M. Ono, Y. Naoe, N. Ohkura, T. Yamaguchi, H. Yaguchi, I. Kitabayashi, T. Tsukada, T. Nomura, Y. Miyachi, et al. 2009. Indispensable role of the Runx1-Cbfbeta transcription complex for in vivo-suppressive function of FoxP3+ regulatory T cells. Immunity. 31:609-620.
23. Koch, M.A., G. Tucker-Heard, N.R. Perdue, J.R. Killebrew, K.B. Urdahl, and D.J. Campbell. 2009. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10:595-602.
24. Koller, B.H., P. Marrack, J.W. Kappler, and O. Smithies. 1990. Normal development of mice deficient in beta 2M, MHC class I proteins, and CD8+ T cells. Science. 248:1227-1230.
25. Kühn, R., J. Löhler, D. Rennick, K. Rajewsky, and W. Müller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 75: 263-274.
26. Lee, C.G., K.H. Kang, J.S. So, H.K. Kwon, J.S. Son, M.K. Song, A. Sahoo, H.J. Yi, K.C. Hwang, T. Matsuyama, et al. 2009. A distal cis-regulatory element, CNS-9, controls NFAT1 and IRF4-mediated IL-10 gene activation in T helper cells. Mol. Immunol. 46:613-621.
27. Li, L., M. Leid, and E.V. Rothenberg. 2010a. An early T cell lineage commitment checkpoint dependent on the transcription factor Bcl11b. Science. 329:89-93.
28. Li, P., S. Burke, J. Wang, X. Chen, M. Ortiz, S.C. Lee, D. Lu, L. Campos, D. Goulding, B.L. Ng, et al. 2010b. Reprogramming of T cells to natural killer-like cells upon Bcl11b deletion. Science. 329:85-89.
29. Mantel, P.Y., N. Ouaked, B. Rückert, C. Karagiannidis, R. Welz, K. Blaser, and C.B. Schmidt-Weber. 2006. Molecular mechanisms underlying FOXP3 induction in human T cells. J. Immunol. 176:3593-3602.
30. Maruyama, T., J. Li, J.P. Vaque, J.E. Konkel, W. Wang, B. Zhang, P. Zhang, B.F. Zamarron, D. Yu, Y. Wu, et al. 2011. Control of the differentiation of regulatory T cells and T(H)17 cells by the DNA-binding inhibitor Id3. Nat. Immunol. 12:86-95.
31. Miyara, M., and S. Sakaguchi. 2007. Natural regulatory T cells: mechanisms of suppression. Trends Mol. Med. 13:108-116.
32. Mottet, C., H.H. Uhlig, and F. Powrie. 2003. Cutting edge: cure of colitis by CD4+CD25+ regulatory T cells. J. Immunol. 170:3939-3943.
33. Ouyang, W., O. Beckett, Q. Ma, J.H. Paik, R.A. DePinho, and M.O. Li. 2010. Foxo proteins cooperatively control the differentiation of Foxp3+ regulatory T cells. Nat. Immunol. 11:618-627.
34. Pan, F., H. Yu, E.V. Dang, J. Barbi, X. Pan, J.F. Grosso, D. Jinasena, S.M. Sharma, E.M. McCadden, D. Getnet, et al. 2009. Eos mediates Foxp3-dependent gene silencing in CD4+ regulatory T cells. Science. 325: 1142-1146.
35. Roers, A., L. Siewe, E. Strittmatter, M. Deckert, D. Schlüter, W. Stenzel, A.D. Gruber, T. Krieg, K. Rajewsky, and W. Müller. 2004. T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J. Exp. Med. 200:1289-1297.
36. Rubtsov, Y.P., J.P. Rasmussen, E.Y. Chi, J. Fontenot, L. Castelli, X. Ye, P. Treuting, L. Siewe, A. Roers, W.R. Henderson Jr., et al. 2008. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity. 28:546-558.
37. Rudra, D., T. Egawa, M.M. Chong, P. Treuting, D.R. Littman, and A.Y. Rudensky. 2009. Runx-CBFbeta complexes control expression of the transcription factor Foxp3 in regulatory T cells. Nat. Immunol. 10:1170- 1177.
38. Tone, Y., K. Furuuchi, Y. Kojima, M.L. Tykocinski, M.I. Greene, and M. Tone. 2008. Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat. Immunol. 9:194-202.
39. Vignali, D.A., L.W. Collison, and C.J. Workman. 2008. How regulatory T cells work. Nat. Rev. Immunol. 8:523-532.
40. Wakabayashi, Y., H. Watanabe, J. Inoue, N. Takeda, J. Sakata, Y. Mishima, J. Hitomi, T. Yamamoto, M. Utsuyama, O. Niwa, et al. 2003. Bcl11b is required for differentiation and survival of alphabeta T lymphocytes. Nat. Immunol. 4:533-539.
41. Wan, Y.Y., and R.A. Flavell. 2007. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature. 445:766- 770.
42. Wang, Z.Y., H. Sato, S. Kusam, S. Sehra, L.M. Toney, and A.L. Dent. 2005. Regulation of IL-10 gene expression in Th2 cells by Jun proteins. J. Immunol. 174:2098-2105.
43. Wing, K., and S. Sakaguchi. 2010. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat. Immunol. 11:7-13.
44. Wu, Y., M. Borde, V. Heissmeyer, M. Feuerer, A.D. Lapan, J.C. Stroud, D.L. Bates, L. Guo, A. Han, S.F. Ziegler, et al. 2006. FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell. 126:375-387.
45. Xu, L., A. Kitani, I. Fuss, and W. Strober. 2007. Cutting edge: regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J. Immunol. 178:6725-6729.
46. Zenewicz, L.A., A. Antov, and R.A. Flavell. 2009. CD4 T-cell differentiation and inflammatory bowel disease. Trends Mol. Med. 15:199-207.
47. + T lymphocytes depend on the transcription factor Bcl11b. J. Exp. Med. 207:1687-1699.
48. Zheng, Y., A. Chaudhry, A. Kas, P. deRoos, J.M. Kim, T.T. Chu, L. Corcoran, P. Treuting, U. Klein, and A.Y. Rudensky. 2009. Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature. 458:351-356.
49. Zheng, Y., S. Josefowicz, A. Chaudhry, X.P. Peng, K. Forbush, and A.Y. Rudensky. 2010. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature. 463:808-812.
50. Zhou, L., M.M. Chong, and D.R. Littman. 2009. Plasticity of CD4+ T cell lineage differentiation. Immunity. 30:646-655.
51. Zorn, E., E.A. Nelson, M. Mohseni, F. Porcheray, H. Kim, D. Litsa, R. Bellucci, E. Raderschall, C. Canning, R.J. Soiffer, et al. 2006. IL-2 regulates FOXP3 expression in human CD4+CD25+ regulatory T cells through a STATdependent mechanism and induces the expansion of these cells in vivo. Blood. 108:1571-1579.