Transcriptional regulator Bhlhe40 works as a cofactor of T-bet in the regulation of IFN-γ production in iNKT cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 24, 2016, Pages E3394-E3402

  Kanda, Masatoshi ^a,b,c   Yamanaka, Hiroyuki ^a,d   Kojo, Satoshi ^a   Usui, Yuu ^a   Honda, Hiroaki ^e   Sotomaru, Yusuke ^e   Harada, Michishige ^f   Taniguchi, Masaru ^f   Suzuki, Nao ^d   Atsumi, Tatsuya ^b   Wada, Haruka ^a   Baghdadi, Muhammad ^a   Seino, Ken Ichiro ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^d ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e HIROSHIMA UNIVERSITY   (Japan)

^f RIKEN Center for Integrative Medical Sciences   (Japan)

Author keywords

Basic helix loop helix transcription factors; Bhlhe40; Interferon ; Natural killer T cells; T box transcription factor Tbx21

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR MEMBER E40; CD1D ANTIGEN; CD4 ANTIGEN; GAMMA INTERFERON; HISTONE H3; INTERLEUKIN 12; INTERLEUKIN 17 RECEPTOR; MESSENGER RNA; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG; BHLHE40 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; IFNG PROTEIN, MOUSE; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL MATURATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE LOCUS; IN VIVO STUDY; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; THYMOCYTE; TRANSCRIPTION REGULATION; ANIMAL; CELLULAR IMMUNITY; EXPERIMENTAL NEOPLASM; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PROMOTER REGION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; IMMUNITY, CELLULAR; INTERFERON-GAMMA; MICE; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; NEOPLASMS, EXPERIMENTAL; PROMOTER REGIONS, GENETIC; T-BOX DOMAIN PROTEINS;

EID: 84974707245     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1604178113     Document Type: Article

References (50)

1. Taniguchi M, Harada M, Kojo S, Nakayama T, Wakao H (2003) The regulatory role of Valpha14 NKT cells in innate and acquired immune response. Annu Rev Immunol 21: 483-513.
2. Coquet JM, et al. (2008) Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1- NKT cell population. Proc Natl Acad Sci USA 105(32):11287-11292.
3. Kitamura H, et al. (1999) The natural killer T (NKT) cell ligand alpha-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells. J Exp Med 189(7):1121-1128.
4. Kojo S, et al. (2005) Induction of regulatory properties in dendritic cells by Valpha14 NKT cells. J Immunol 175(6):3648-3655.
5. Terabe M, Berzofsky JA (2008) The role of NKT cells in tumor immunity. Adv Cancer Res 101:277-348.
6. Constantinides MG, Bendelac A (2013) Transcriptional regulation of the NKT cell lineage. Curr Opin Immunol 25(2):161-167.
7. Hu T, et al. (2013) Increased level of E protein activity during invariant NKT development promotes differentiation of invariant NKT2 and invariant NKT17 subsets. J Immunol 191(10):5065-5073.
8. Lee YJ, Holzapfel KL, Zhu J, Jameson SC, Hogquist KA (2013) Steady-state production of IL-4 modulates immunity in mouse strains and is determined by lineage diversity of iNKT cells. Nat Immunol 14(11):1146-1154.
9. Watarai H, et al. (2012) Development and function of invariant natural killer T cells producing T(h)2- and T(h)17-cytokines. PLoS Biol 10(2):e1001255.
10. Honma S, et al. (2002) Dec1 and Dec2 are regulators of the mammalian molecular clock. Nature 419(6909):841-844.
11. Miyazaki K, et al. (2010) The role of the basic helix-loop-helix transcription factor Dec1 in the regulatory T cells. J Immunol 185(12):7330-7339.
12. Seuter S, Pehkonen P, Heikkinen S, Carlberg C (2013) The gene for the transcription factor BHLHE40/DEC1/stra13 is a dynamically regulated primary target of the vitamin D receptor. J Steroid Biochem Mol Biol 136:62-67.
13. Sun H, Lu B, Li RQ, Flavell RA, Taneja R (2001) Defective T cell activation and autoimmune disorder in Stra13-deficient mice. Nat Immunol 2(11):1040-1047.
14. Benlagha K, Kyin T, Beavis A, Teyton L, Bendelac A (2002) A thymic precursor to the NK T cell lineage. Science 296(5567):553-555.
15. Maeda M, Lohwasser S, Yamamura T, Takei F (2001) Regulation of NKT cells by Ly49: Analysis of primary NKT cells and generation of NKT cell line. J Immunol 167(8):4180-4186.
16. Benlagha K, Wei DG, Veiga J, Teyton L, Bendelac A (2005) Characterization of the early stages of thymic NKT cell development. J Exp Med 202(4):485-492.
17. Griewank K, et al. (2007) Homotypic interactions mediated by Slamf1 and Slamf6 receptors control NKT cell lineage development. Immunity 27(5):751-762.
18. Stetson DB, et al. (2003) Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J Exp Med 198(7):1069-1076.
19. Kawano T, et al. (1997) CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science 278(5343):1626-1629.
20. Toura I, et al. (1999) Cutting edge: Inhibition of experimental tumor metastasis by dendritic cells pulsed with alpha-galactosylceramide. J Immunol 163(5):2387-2391.
21. Smyth MJ, et al. (2002) Sequential production of interferon-gamma by NK1.1(+) T cells and natural killer cells is essential for the antimetastatic effect of alpha-galactosylceramide. Blood 99(4):1259-1266.
22. Kojo S, et al. (2009) Mechanisms of NKT cell anergy induction involve Cbl-b-promoted monoubiquitination of CARMA1. Proc Natl Acad Sci USA 106(42):17847-17851.
23. Szabo SJ, Sullivan BM, Peng SL, Glimcher LH (2003) Molecular mechanisms regulating Th1 immune responses. Annu Rev Immunol 21:713-758.
24. Hwang ES, Szabo SJ, Schwartzberg PL, Glimcher LH (2005) T helper cell fate specified by kinase-mediated interaction of T-bet with GATA-3. Science 307(5708):430-433.
25. Morinobu A, et al. (2002) STAT4 serine phosphorylation is critical for IL-12-induced IFN-gamma production but not for cell proliferation. Proc Natl Acad Sci USA 99(19): 12281-12286.
26. Bailis W, et al. (2013) Notch simultaneously orchestrates multiple helper T cell programs independently of cytokine signals. Immunity 39(1):148-159.
27. Fields PE, Kim ST, Flavell RA (2002) Cutting edge: Changes in histone acetylation at the IL-4 and IFN-gamma loci accompany Th1/Th2 differentiation. J Immunol 169(2): 647-650.
28. Grenningloh R, Kang BY, Ho IC (2005) Ets-1, a functional cofactor of T-bet, is essential for Th1 inflammatory responses. J Exp Med 201(4):615-626.
29. Lovett-Racke AE, et al. (2004) Silencing T-bet defines a critical role in the differentiation of autoreactive T lymphocytes. Immunity 21(5):719-731.
30. Szabo SJ, et al. (2000) A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100(6):655-669.
31. Beima KM, et al. (2006) T-bet binding to newly identified target gene promoters is cell type-independent but results in variable context-dependent functional effects. J Biol Chem 281(17):11992-12000.
32. Baguet A, Bix M (2004) Chromatin landscape dynamics of the Il4-Il13 locus during T helper 1 and 2 development. Proc Natl Acad Sci USA 101(31):11410-11415.
33. Nishimura T, et al. (2000) The interface between innate and acquired immunity: Glycolipid antigen presentation by CD1d-expressing dendritic cells to NKT cells induces the differentiation of antigen-specific cytotoxic T lymphocytes. Int Immunol 12(7):987-994.
34. Motohashi S, et al. (2009) A phase I-II study of alpha-galactosylceramide-pulsed IL-2/GM-CSF-cultured peripheral blood mononuclear cells in patients with advanced and recurrent non-small cell lung cancer. J Immunol 182(4):2492-2501.
35. Cohen NR, et al.; ImmGen Project Consortium (2013) Shared and distinct transcriptional programs underlie the hybrid nature of iNKT cells. Nat Immunol 14(1):90-99.
36. Li Y, et al. (2003) DEC1 negatively regulates the expression of DEC2 through binding to the E-box in the proximal promoter. J Biol Chem 278(19):16899-16907.
37. Zawel L, et al. (2002) DEC1 is a downstream target of TGF-beta with sequence-specific transcriptional repressor activities. Proc Natl Acad Sci USA 99(5):2848-2853.
38. Shen M, et al. (2002) Basic helix-loop-helix protein DEC1 promotes chondrocyte differentiation at the early and terminal stages. J Biol Chem 277(51):50112-50120.
39. Li Y, et al. (2006) The expression of antiapoptotic protein survivin is transcriptionally upregulated by DEC1 primarily through multiple sp1 binding sites in the proximal promoter. Oncogene 25(23):3296-3306.
40. Sekimata M, et al. (2009) CCCTC-binding factor and the transcription factor T-bet orchestrate T helper 1 cell-specific structure and function at the interferon-gamma locus. Immunity 31(4):551-564.
41. Chen GY, Osada H, Santamaria-Babi LF, Kannagi R (2006) Interaction of GATA-3/T-bet transcription factors regulates expression of sialyl Lewis X homing receptors on Th1/Th2 lymphocytes. Proc Natl Acad Sci USA 103(45):16894-16899.
42. Miller SA, Huang AC, Miazgowicz MM, Brassil MM, Weinmann AS (2008) Coordinated but physically separable interaction with H3K27-demethylase and H3K4-methyltransferase activities are required for T-box protein-mediated activation of developmental gene expression. Genes Dev 22(21):2980-2993.
43. Lin CC, et al. (2014) Bhlhe40 controls cytokine production by T cells and is essential for pathogenicity in autoimmune neuroinflammation. Nat Commun 5:3551.
44. Hu G, Chen J (2013) A genome-wide regulatory network identifies key transcription factors for memory CD8+ T-cell development. Nat Commun 4:2830.
45. Liu Y, et al. (2013) DEC1 is positively associated with the malignant phenotype of invasive breast cancers and negatively correlated with the expression of claudin-1. Int J Mol Med 31(4):855-860.
46. Cui J, et al. (1997) Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 278(5343):1623-1626.
47. Watarai H, et al. (2010) Generation of functional NKT cells in vitro from embryonic stem cells bearing rearranged invariant Valpha14-Jalpha18 TCRalpha gene. Blood 115(2):230-237.
48. Watarai H, Nakagawa R, Omori-Miyake M, Dashtsoodol N, Taniguchi M (2008) Methods for detection, isolation and culture of mouse and human invariant NKT cells. Nat Protoc 3(1):70-78.
49. Szabo SJ, Gold JS, Murphy TL, Murphy KM (1993) Identification of cis-acting regulatory elements controlling interleukin-4 gene expression in T cells: Roles for NF-Y and NF-ATc. Mol Cell Biol 13(8):4793-4805.
50. Ranganath S, et al. (1998) GATA-3-dependent enhancer activity in IL-4 gene regulation. J Immunol 161(8):3822-3826.