Chromatin loop organization of the junb locus in mouse dendritic cells

Nucleic Acids Research

Volumn 41, Issue 19, 2013, Pages 8908-8925

  Salem, Tamara ^a,b   Gomard, Tiphanie ^a,b   Court, Franck ^a,b   Moquet Torcy, Gabriel ^a,b   Brockly, Frédérique ^a,b   Forné, Thierry ^a,b   Piechaczyk, Marc ^a,b  

^a INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^b UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; RNA POLYMERASE II;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DENDRITIC CELL; GENE; GENE ACTIVITY; GENE FUNCTION; GENE LOCUS; HISTONE MODIFICATION; JUNB GENE; MOUSE; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINE; CHROMATIN; DENDRITIC CELLS; ENHANCER ELEMENTS, GENETIC; GENETIC LOCI; HISTONES; HUMANS; LIPOPOLYSACCHARIDES; MICE; NUCLEIC ACID CONFORMATION; RNA POLYMERASE II; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTIONAL ACTIVATION;

EID: 84885965887     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt669     Document Type: Article

References (84)

1. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y.J., Pulendran, B. and Palucka, K. (2000) Immunobiology of dendritic cells. Annu. Rev. Immunol., 18, 767-811.
2. Heath, W.R. and Carbone, F.R. (2009) Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat. Immunol., 10, 1237-1244.
3. Reis e Sousa, C. (2006) Dendritic cells in a mature age. Nat. Rev. Immunol., 6, 476-483.
4. Steinman, R.M. and Banchereau, J. (2007) Taking dendritic cells into medicine. Nature, 449, 419-426.
5. Rabani, M., Levin, Z., Fan, L., Adiconis, X., Raychowdhury, R., Garber, M., Gnirke, A., Nusbaum, C., Hacohen, N., Friedman, N. et al. (2011) Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat. Biotechnol., 29, 436-445.
6. Amit, I., Garber, M., Chevrier, N., Leite, A.P., Donner, Y., Eisenhaure, T., Guttman, M., Grenier, J.K., Li, W., Zuk, O. et al. (2009) Unbiased reconstruction of a mammalian transcriptional network mediating pathogen responses. Science, 9, 257-263.
7. Hashimoto, D., Miller, J. and Merad, M. (2011) Dendritic cell and macrophage heterogeneity in vivo. Immunity, 35, 323-335.
8. Kim, H.P., Lee, Y.S., Park, J.H. and Kim, Y.J. (2013) Transcriptional and epigenetic networks in the development and maturation of dendritic cells. Epigenomics, 5, 195-204.
9. Kawai, T. and Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol., 11, 373-384.
10. Takeda, K., Kaisho, T. and Akira, S. (2003) Toll-like receptors. Annu. Rev. Immunol., 21, 335-376.
11. Gomard, T., Michaud, H.A., Tempe, D., Thiolon, K., Pelegrin, M. and Piechaczyk, M. (2010) An NF-kappaB-dependent role for JunB in the induction of proinflammatory cytokines in LPSactivated bone marrow-derived dendritic cells. PLoS One, 5, e9585.
12. Eferl, R. and Wagner, E.F. (2003) AP-1: a double-edged sword in tumorigenesis. Nat. Rev. Cancer, 3, 859-868.
13. Lopez-Bergami, P., Lau, E. and Ronai, Z. (2010) Emerging roles of ATF2 and the dynamic AP1 network in cancer. Nat. Rev. Cancer, 10, 65-76.
14. Shaulian, E. (2010) AP-1-The Jun proteins: oncogenes or tumor suppressors in disguise? Cell Signal., 22, 894-899.
15. Wagner, E.F. and Eferl, R. (2005) Fos/AP-1 proteins in bone and the immune system. Immunol. Rev., 208, 126-140.
16. Fujioka, S., Niu, J., Schmidt, C., Sclabas, G.M., Peng, B., Uwagawa, T., Li, Z., Evans, D.B., Abbruzzese, J.L. and Chiao, P.J. (2004) NF-kappaB and AP-1 connection: mechanism of NF-kappaB-dependent regulation of AP-1 activity. Mol. Cell. Biol., 24, 7806-7819.
17. Krappmann, D., Wegener, E., Sunami, Y., Esen, M., Thiel, A., Mordmuller, B. and Scheidereit, C. (2004) The IkappaB kinase complex and NF-kappaB act as master regulators of lipopolysaccharide-induced gene expression and control subordinate activation of AP-1. Mol. Cell. Biol., 24, 6488-6500.
18. Farras, R., Baldin, V., Gallach, S., Acquaviva, C., Bossis, G., Jariel-Encontre, I. and Piechaczyk, M. (2008) JunB breakdown in mid-/late G2 is required for down-regulation of cyclin A2 levels and proper mitosis. Mol. Cell. Biol., 28, 4173-4187.
19. Baccam, M., Woo, S.Y., Vinson, C. and Bishop, G.A. (2003) CD40- mediated transcriptional regulation of the IL-6 gene in B lymphocytes: involvement of NF-kappa B, AP-1, and C/EBP. J. Immunol., 170, 3099-3108.
20. Mann, J., Oakley, F., Johnson, P.W. and Mann, D.A. (2002) CD40 induces interleukin-6 gene transcription in dendritic cells: regulation by TRAF2, AP-1, NF-kappa B, AND CBF1. J. Biol. Chem., 277, 17125-17138.
21. Yao, J., Mackman, N., Edgington, T.S. and Fan, S.T. (1997) Lipopolysaccharide induction of the tumor necrosis factor-alpha promoter in human monocytic cells. Regulation by Egr-1, c-Jun, and NF-kappaB transcription factors. J. Biol. Chem., 272, 17795-17801.
22. Zagariya, A., Mungre, S., Lovis, R., Birrer, M., Ness, S., Thimmapaya, B. and Pope, R. (1998) Tumor necrosis factor alpha gene regulation: enhancement of C/EBPbeta-induced activation by c-Jun. Mol. Cell. Biol., 18, 2815-2824.
23. Zhu, C., Gagnidze, K., Gemberling, J.H. and Plevy, S.E. (2001) Characterization of an activation protein-1-binding site in the murine interleukin-12 p40 promoter. Demonstration of novel functional elements by a reductionist approach. J. Biol. Chem., 276, 18519-18528.
24. Fujihara, M., Ikebuchi, K., Maekawa, T.L., Wakamoto, S., Ogiso, C., Ito, T., Takahashi, T.A., Suzuki, T. and Sekiguchi, S. (1998) Lipopolysaccharide- induced desensitization of junB gene expression in a mouse macrophage-like cell line, P388D1. J. Immunol., 161, 3659-3665.
25. Jenner, R.G. and Young, R.A. (2005) Insights into host responses against pathogens from transcriptional profiling. Nat. Rev. Microbiol., 3, 281-294.
26. Aida, M., Chen, Y., Nakajima, K., Yamaguchi, Y., Wada, T. and Handa, H. (2006) Transcriptional pausing caused by NELF plays a dual role in regulating immediate-early expression of the junB gene. Mol. Cell. Biol., 26, 6094-6104.
27. Fujita, T., Piuz, I. and Schlegel, W. (2009) Negative elongation factor NELF controls transcription of immediate early genes in a stimulus-specific manner. Exp. Cell. Res., 315, 274-284.
28. Fujita, T., Ryser, S., Piuz, I. and Schlegel, W. (2008) Up-regulation of P-TEFb by the MEK1-extracellular signal-regulated kinase signaling pathway contributes to stimulated transcription elongation of immediate early genes in neuroendocrine cells. Mol. Cell. Biol., 28, 1630-1643.
29. Nechaev, S. and Adelman, K. (2011) Pol II waiting in the starting gates: Regulating the transition from transcription initiation into productive elongation. Biochim. Biophys. Acta., 1809, 34-45.
30. Li, J. and Gilmour, D.S. (2011) Promoter proximal pausing and the control of gene expression. Curr. Opin. Genet. Dev., 21, 231-235.
31. Amato, S.F., Nakajima, K., Hirano, T. and Chiles, T.C. (1996) Transcriptional regulation of the junB promoter in mature B lymphocytes. Activation through a cyclic adenosine 3′, 5′- monophosphate-like binding site. J. Immunol., 157, 146-155.
32. de Groot, R.P., Auwerx, J., Karperien, M., Staels, B. and Kruijer, W. (1991) Activation of junB by PKC and PKA signal transduction through a novel cis-acting element. Nucleic Acids Res., 19, 775-781.
33. Eggen, B.J., Benus, G.F., Folkertsma, S., Jonk, L.J. and Kruijer, W. (2001) TAK1 activation of the mouse JunB promoter is mediated through a CCAAT box and NF-Y. FEBS Lett., 506, 267-271.
34. Finch, J.S., Rosenberger, S.F., Martinez, J.D. and Bowden, G.T. (2001) Okadaic acid induces transcription of junB through a CCA AT box and NF-Y. Gene, 267, 135-144.
35. Jonk, L.J., Itoh, S., Heldin, C.H., ten Dijke, P. and Kruijer, W. (1998) Identification and functional characterization of a Smad binding element (SBE) in the JunB promoter that acts as a transforming growth factor-beta, activin, and bone morphogenetic protein-inducible enhancer. J. Biol. Chem., 273, 21145-21152.
36. Kitabayashi, I., Kawakami, Z., Matsuoka, T., Chiu, R., Gachelin, G. and Yokoyama, K. (1993) Two cis-regulatory elements that mediate different signaling pathways for serum-dependent activation of the junB gene. J. Biol. Chem., 268, 14482-14489.
37. Nakajima, K., Kusafuka, T., Takeda, T., Fujitani, Y., Nakae, K. and Hirano, T. (1993) Identification of a novel interleukin-6 response element containing an Ets-binding site and a CRE-like site in the junB promoter. Mol. Cell. Biol., 13, 3027-3041.
38. Sjin, R.M., Lord, K.A., Abdollahi, A., Hoffman, B. and Liebermann, D.A. (1999) Interleukin-6 and leukemia inhibitory factor induction of JunB is regulated by distinct cell type-specific cis-acting elements. J. Biol. Chem., 274, 28697-28707.
39. Brown, R.T., Ades, I.Z. and Nordan, R.P. (1995) An acute phase response factor/NF-kappa B site downstream of the junB gene that mediates responsiveness to interleukin-6 in a murine plasmacytoma. J. Biol. Chem., 270, 31129-31135.
40. Frazier-Jessen, M.R., Thompson, C.D., Brown, R., Rawat, R., Nordan, R.P. and Feldman, G.M. (2002) NF-kappaB elements contribute to junB inducibility by lipopolysaccharide in the murine macrophage cell line RAW264.7. FEBS Lett., 513, 203-207.
41. Lopez-Rovira, T., Chalaux, E., Rosa, J.L., Bartrons, R. and Ventura, F. (2000) Interaction and functional cooperation of NF-kappa B with Smads. Transcriptional regulation of the junB promoter. J. Biol. Chem., 275, 28937-28946.
42. Perez-Albuerne, E.D., Schatteman, G., Sanders, L.K. and Nathans, D. (1993) Transcriptional regulatory elements downstream of the JunB gene. Proc. Natl Acad. Sci. USA, 90, 11960-11964.
43. Schmidt, D., Textor, B., Pein, O.T., Licht, A.H., Andrecht, S., Sator-Schmitt, M., Fusenig, N.E., Angel, P. and Schorpp-Kistner, M. (2007) Critical role for NF-kappaB-induced JunB in VEGF regulation and tumor angiogenesis. EMBO J., 26, 710-719.
44. Shen, Z., Reznikoff, G., Dranoff, G. and Rock, K.L. (1997) Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol., 158, 2723-2730.
45. Milligan, L., Forne, T., Antoine, E., Weber, M., Hemonnot, B., Dandolo, L., Brunel, C. and Cathala, G. (2002) Turnover of primary transcripts is a major step in the regulation of mouse H19 gene expression. EMBO Rep., 3, 774-779.
46. Braem, C., Recolin, B., Rancourt, R.C., Angiolini, C., Barthes, P., Branchu, P., Court, F., Cathala, G., Ferguson-Smith, A.C. and Forne, T. (2008) Genomic matrix attachment region and chromosome conformation capture quantitative real time PCR assays identify novel putative regulatory elements at the imprinted Dlk1/Gtl2 locus. J. Biol. Chem., 283, 18612-18620.
47. Weber, M., Hagege, H., Murrell, A., Brunel, C., Reik, W., Cathala, G. and Forne, T. (2003) Genomic imprinting controls matrix attachment regions in the Igf2 gene. Mol. Cell. Biol., 23, 8953-8959.
48. Weber, M., Hagege, H., Lutfalla, G., Dandolo, L., Brunel, C., Cathala, G. and Forne, T. (2003) A real-time polymerase chain reaction assay for quantification of allele ratios and correction of amplification bias. Anal. Biochem., 320, 252-258.
49. Dekker, J., Rippe, K., Dekker, M. and Kleckner, N. (2002) Capturing chromosome conformation. Science, 295, 1306-1311.
50. Hagege, H., Klous, P., Braem, C., Splinter, E., Dekker, J., Cathala, G., de Laat, W. and Forne, T. (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat. Protoc., 2, 1722-1733.
51. Court, F., Baniol, M., Hagege, H., Petit, J.S., Lelay-Taha, M.N., Carbonell, F., Weber, M., Cathala, G. and Forne, T. (2011) Longrange chromatin interactions at the mouse Igf2/H19 locus reveal a novel paternally expressed long non-coding RNA. Nucleic Acids Res., 39, 5893-5906.
52. Okada, N., Tsujino, M., Hagiwara, Y., Tada, A., Tamura, Y., Mori, K., Saito, T., Nakagawa, S., Mayumi, T., Fujita, T. et al. (2001) Administration route-dependent vaccine efficiency of murine dendritic cells pulsed with antigens. Br. J. Cancer, 84, 1564-1570.
53. Hayden, M.S. and Ghosh, S. (2008) Shared principles in NF-kappaB signaling. Cell, 132, 344-362.
54. Hu, X., Janssen, W.E., Moscinski, L.C., Bryington, M., Dangsupa, A., Rezai-Zadeh, N., Babbin, B.A. and Zuckerman, K.S. (2001) An IkappaBalpha inhibitor causes leukemia cell death through a p38 MAP kinase-dependent, NF-kappaB-independent mechanism. Cancer Res., 61, 6290-6296.
55. Heintzman, N.D., Stuart, R.K., Hon, G., Fu, Y., Ching, C.W., Hawkins, R.D., Barrera, L.O., Van Calcar, S., Qu, C., Ching, K.A. et al. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet., 39, 311-318.
56. Nishida, H., Suzuki, T., Kondo, S., Miura, H., Fujimura, Y. and Hayashizaki, Y. (2006) Histone H3 acetylated at lysine 9 in promoter is associated with low nucleosome density in the vicinity of transcription start site in human cell. Chromosome Res., 14, 203-211.
57. Ozsolak, F., Song, J.S., Liu, X.S. and Fisher, D.E. (2007) Highthroughput mapping of the chromatin structure of human promoters. Nat. Biotechnol., 25, 244-248.
58. Allis, C.D., Berger, S.L., Cote, J., Dent, S., Jenuwien, T., Kouzarides, T., Pillus, L., Reinberg, D., Shi, Y., Shiekhattar, R. et al. (2007) New nomenclature for chromatin-modifying enzymes. Cell, 131, 633-636.
59. Kouzarides, T. (2007) SnapShot: histone-modifying enzymes. Cell, 131, 822.
60. Bartkowiak, B. and Greenleaf, A.L. (2011) Phosphorylation of RNAPII: To P-TEFb or not to P-TEFb? Transcription, 2, 115-119.
61. Buratowski, S. (2009) Progression through the RNA polymerase II CTD cycle. Mol. Cell, 36, 541-546.
62. Phatnani, H.P. and Greenleaf, A.L. (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev, 20, 2922-2936.
63. Kornberg, R.D. (2007) The molecular basis of eucaryotic transcription. Cell Death Differ., 14, 1989-1997.
64. Ethier, S.D., Miura, H. and Dostie, J. (2011) Discovering genome regulation with 3C and 3C-related technologies. Biochim. Biophys. Acta., 1819, 401-410.
65. Deng, W. and Blobel, G.A. (2010) Do chromatin loops provide epigenetic gene expression states? Curr. Opin. Genet. Dev., 20, 548-554.
66. Schoenfelder, S., Clay, I. and Fraser, P. (2010) The transcriptional interactome: gene expression in 3D. Curr. Opin. Genet. Dev., 20, 127-133.
67. Sexton, T., Bantignies, F. and Cavalli, G. (2009) Genomic interactions: chromatin loops and gene meeting points in transcriptional regulation. Semin. Cell. Dev. Biol., 20, 849-855.
68. Tan-Wong, S.M., French, J.D., Proudfoot, N.J. and Brown, M.A. (2008) Dynamic interactions between the promoter and terminator regions of the mammalian BRCA1 gene. Proc. Natl Acad. Sci. USA, 105, 5160-5165.
69. O'Reilly, D. and Greaves, D.R. (2007) Cell-type-specific expression of the human CD68 gene is associated with changes in Pol II phosphorylation and short-range intrachromosomal gene looping. Genomics, 90, 407-415.
70. Perkins, K.J., Lusic, M., Mitar, I., Giacca, M. and Proudfoot, N.J. (2008) Transcription-dependent gene looping of the HIV-1 provirus is dictated by recognition of pre-mRNA processing signals. Mol. Cell, 29, 56-68.
71. Anamika, K., Gyenis, A., Poidevin, L., Poch, O. and Tora, L. (2012) RNA polymerase II pausing downstream of core histone genes is different from genes producing polyadenylated transcripts. PLoS One, 7, e38769.
72. Lian, Z., Karpikov, A., Lian, J., Mahajan, M.C., Hartman, S., Gerstein, M., Snyder, M. and Weissman, S.M. (2008) A genomic analysis of RNA polymerase II modification and chromatin architecture related to 3′ end RNA polyadenylation. Genome Res., 18, 1224-1237.
73. Richard, P. and Manley, J.L. (2009) Transcription termination by nuclear RNA polymerases. Genes Dev., 23, 1247-1269.
74. Tan-Wong, S.M., Zaugg, J.B., Camblong, J., Xu, Z., Zhang, D.W., Mischo, H.E., Ansari, A.Z., Luscombe, N.M., Steinmetz, L.M. and Proudfoot, N.J. (2012) Gene loops enhance transcriptional directionality. Science, 338, 671-675.
75. Orekhova, A.S. and Rubtsov, P.M. (2013) Bidirectional promoters in the transcription of Mammalian genomes. Biochemistry (Mosc.), 78, 335-341.
76. Jash, A., Yun, K., Sahoo, A., So, J.S. and Im, S.H. (2012) Looping mediated interaction between the promoter and 3′ UTR regulates type II collagen expression in chondrocytes. PLoS One, 7, e40828.
77. Zhao, W., Wang, L., Zhang, M., Wang, P., Zhang, L., Yuan, C., Qi, J., Qiao, Y., Kuo, P.C. and Gao, C. (2011) NF-kappaB- and AP-1-mediated DNA looping regulates osteopontin transcription in endotoxin-stimulated murine macrophages. J. Immunol., 186, 3173-3179.
78. Guo, H., Mi, Z. and Kuo, P.C. (2008) Characterization of short range DNA looping in endotoxin-mediated transcription of the murine inducible nitric-oxide synthase (iNOS) gene. J. Biol. Chem., 283, 25209-25217.
79. Liu, Z., Ma, Z., Terada, L.S. and Garrard, W.T. (2009) Divergent roles of RelA and c-Rel in establishing chromosomal loops upon activation of the Igkappa gene. J. Immunol., 183, 3819-3830.
80. Ying, S., Kojima, T., Kawada, A., Nachat, R., Serre, G., Simon, M. and Takahara, H. (2010) An intronic enhancer driven by NFkappaB contributes to transcriptional regulation of peptidylarginine deiminase type I gene in human keratinocytes. J. Invest. Dermatol., 130, 2543-2552.
81. Carretero, M., Remeseiro, S. and Losada, A. (2010) Cohesin ties up the genome. Curr. Opin. Cell Biol., 22, 781-787.
82. Galande, S., Purbey, P.K., Notani, D. and Kumar, P.P. (2007) The third dimension of gene regulation: organization of dynamic chromatin loopscape by SATB1. Curr. Opin. Genet. Dev., 17, 408-414.
83. Guo, Y., Monahan, K., Wu, H., Gertz, J., Varley, K.E., Li, W., Myers, R.M., Maniatis, T. and Wu, Q. (2012) CTCF/cohesinmediated DNA looping is required for protocadherin alpha promoter choice. Proc. Natl Acad. Sci. USA, 109, 21081-21086.
84. Phillips, J.E. and Corces, V.G. (2009) CTCF: master weaver of the genome. Cell, 137, 1194-1211.