Association of the interferon-β gene with pericentromeric heterochromatin is dynamically regulated during virus infection through a YY1-dependent mechanism

Nucleic Acids Research

Volumn 40, Issue 10, 2012, Pages 4396-4411

  Josse, T ^a   Mokrani Benhelli, H ^a   Benferhat, R ^b   Shestakova, E ^a,c   Mansuroglu, Z ^a   Kakanakou, H ^a   Billecocq, A ^b   Bouloy, M ^b   Bonnefoy, Eliette ^a  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

^c MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; TRANSCRIPTION FACTOR YY1;

ALLELE; ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE COURSE; DNA BINDING; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCATION; GENE LOCUS; GENE REPRESSION; GENE STRUCTURE; GENE TARGETING; GENETIC ASSOCIATION; GENETIC REGULATION; GENETIC TRANSFECTION; HETEROCHROMATIN; INTERFERON BETA GENE; NONHUMAN; PERICENTROMERIC HETEROCHROMATIN; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION INITIATION; VIRUS INFECTION; WILD TYPE;

ANIMALS; BINDING SITES; CELL LINE; DNA, SATELLITE; HETEROCHROMATIN; INTERFERON-BETA; MICE; NEWCASTLE DISEASE VIRUS; PROMOTER REGIONS, GENETIC; RIFT VALLEY FEVER VIRUS; TRANSCRIPTIONAL ACTIVATION; YY1 TRANSCRIPTION FACTOR;

EID: 84861541407     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks050     Document Type: Article

References (57)

1. Fraser, P. and Bickmore, W. (2007) Nuclear organization of the genome and the potential for gene regulation. Nature, 447, 413-417.
2. Schneider, R. and Grosschedl, R. (2007) Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev., 21, 3027-3043.
3. Zhao, R., Bodnar, M.S. and Spector, D.L. (2009) Nuclear neighborhoods and gene expression. Curr. Opin. Genet. Dev., 19, 172-179.
4. Francastel, C., Magis, W. and Groudine, M. (2001) Nuclear relocation of a transactivator subunit precedes target gene activation. Proc. Natl Acad. Sci. USA, 98, 12120-12125.
5. Brown, K.E., Guest, S.S., Smale, S.T., Hahm, K., Merkenschlager, M. and Fisher, A.G. (1997) Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell, 91, 845-854.
6. Grogan, J.L., Mohrs, M., Harmon, B., Lacy, D.A., Sedat, J.W. and Locksley, M.R. (2001) Early transcription and silencing of cytokine genes underlie polarization of T helper cell subsets. Immunity, 14, 205-215.
7. Guasconi, V., Pritchard, L.L., Fritsch, L., Mesner, L.D., Francastel, C., Harel-Bellan, A. and Ait-Si-Ali, S. (2010) Preferential association of irreversibly silenced E2F-target genes with pericentromeric heterochromatin in differentiated muscle cells. Epigenetics, 5, 704-709.
8. Fitzsimmons, S.P., Bernstein, R.M., Max, E.E., Skok, J.A. and Shapiro, M.A. (2007) Dynamic changes in accessibility, nuclear positioning, recombination, and transcription at the Igk locus. J. Immunol., 179, 5264-5273.
9. Stark, G.R., Kerr, I.M., Williams, B.R., Silverman, R.H. and Schreiber, R.D. (1998) How cells respond to interferons. Annu. Rev. Biochem., 67, 227-264.
10. Stetson, D.B. and Medzhitov, R. (2006) Type I interferons in host defense. Immunity, 25, 373-381.
11. Dafny, N. and Yang, P.B. (2005) Interferon and the central nervous system. Eur. J. Pharrmacol., 523, 1-15.
12. Axtell, R.C. and Steinman, L. (2008) Type 1 interferons cool the inflamed brain. Immunity, 28, 600-602.
13. Higashi, Y. (1985) Changes of chromatin conformation around mouse interferon-b gene associated with induction of interferon synthesis. Nucleic Acids Res., 13, 5157-5172.
14. Maniatis, T., Falvo, J.V., Kim, T.H., Kim, T.K., Lin, C.H., Parekh, B.S. and Wathelet, M.G. (1998) Structure and function of the Interferon-b enhanceosome. Cold Spring Harb. Symp. Quant. Biol., 63, 609-620.
15. Agalioti, T., Lomvardas, S., Parekh, B., Yie, J., Maniatis, T. and Thanos, D. (2000) Ordered recruitment of chromatin modifying and general transcription factors to the IFN-b promoter. Cell, 103, 667-678.
16. Sato, M., Taniguchi, T. and Tanaka, T. (2001) The interferon system and interferon regulatory factor transcription factors-studies from gene knockout mice. Cytokine Growth Factor Rev., 12, 133-142.
17. Agalioti, T., Chen, G. and Thanos, D. (2002) Deciphering the transcriptional histone acetylation code for a human gene. Cell, 111, 381-392.
18. Weill, L., Shestakova, E. and Bonnefoy, E. (2003) Transcription factor YY1 binds to the murine interferon-beta promoter and regulates its transcriptional capacity with a dual activator/repressor role. J. Virol., 77, 2903-2914.
19. Mokrani, H., Sharaf el Dein, O., Mansuroglu, Z. and Bonnefoy, E. (2006) Binding of YY1 to the proximal region of the murine beta interferon promoter is essential to allow CBP recruitment and K8H4/K14H3 acetylation on the promoter region after virus infection. Mol. Cell. Biol., 26, 8551-8561.
20. Parekh, B.S. and Maniatis, T. (1999) Virus infection leads to localized hyperacetylation of histone H3 and H4 at the IFN-b promoter. Mol. Cell, 3, 125-129.
21. Shestakova, E., Bandu, M.T., Doly, J. and Bonnefoy, E. (2001) Inhibition of histone deacetylation induces constitutive derepression of the beta interferon promoter and confers antiviral activity. J. Virol., 75, 3444-3452.
22. Le May, N., Mansuroglu, Z., Léger, P., Josse, T., Blot, G., Billecocq, A., Flick, R., Jacob, Y., Bonnefoy, E. and Bouloy, M. (2008) A SAP30 complex inhibits IFN-beta expression in Rift Valley Fever Virus infected cells. PloS Pathog., 4, e13.
23. Billecocq, A., Spiegel, M., Vialat, P., Kohl, A., Weber, F., Bouloy, M. and Haller, O. (2004) NSs protein of Rift Valley fever virus blocks interferon production by inhibiting host gene transcription. J. Virol., 78, 9798-9806.
24. Bonnefoy, E., Bandu, M.T. and Doly, J. (1999) Specific binding of High-Mobility-Group I (HMGI) protein and histone H1 to the upstream AT-rich region of the murine beta interferon promoter: HMGI protein acts as a potential antirepressor of the promoter. Mol. Cell. Biol., 19, 2803-2816.
25. Mansuroglu, Z., Josse, T., Gilleron, J., Billecocq, A., Leger, P., Bouloy, M. and Bonnefoy, E. (2010) Nonstructural NSs protein of Rift Valley Fever Virus interacts with pericentromeric DNA sequences of the host cell, inducing chromosme cohesion and segregation defects. J. Virol., 84, 928-939.
26. Lundgren, M., Chow, C.M., Sabbattini, P., Georgiou, A., Minaee, S. and Dillon, N. (2000) Transcription factor dosage affects changes in higher order chromatin structure associated with activation of a heterochromatic gene. Cell, 103, 733-743.
27. Vodjdani, G., Coulombel, C. and Doly, J. (1988) Structure and characterization of a murine chromosomal fragment containing the interferon-b gene. J. Mol. Biol., 204, 221-231.
28. Guenatri, M., Bailly, D., Maison, C. and Almouzni, G. (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell. Biol., 166, 493-505.
29. Eymery, A., Callanan, M. and Vourc'h, C. (2009) The secret message of heterochromatin: new insights into the mechanisms and function of centromeric and pericentric repeat sequence transcription. Int. J. Dev. Biol., 53, 259-268.
30. Hewitt, S.L., Yin, B., Ji, Y., Chaumeil, J., Marszalek, K., Tenthorey, J., Salvagiotto, G., Steinel, N., Ramsey, L.B., Ghysdael, J. et al. (2009) RAG-1 and ATM coordinate monoallelic recombination and nuclear positioning of immunoglobulin loci. Nat. Immunol., 10, 655-664.
31. Brandt, V.L., Hewitt, S.L. and Skok, J.A. (2010) It takes two: communication between homologous alleles preserves genomic stability during V(D)J recombination. Nucleus, 1, 23-29.
32. Lomonte, P. and Merency, E. (2007) Centromeric protein CENP-B proteosomal degradation induced by the viral protein ICP0. FEBS Lett., 581, 658-662.
33. Richards, E.J. and Elgin, S.C.R. (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell, 108, 489-500.
34. Peters, A.H., Kubicek, S., Mechtler, K., O'Sullivan, R.J., Derijck, A.A., Perez-Burgos, L., Kohlmaier, A., Opravil, S., Tachibana, M., Shinkai, Y. et al. (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell, 12, 1577-1589.
35. Barski, A., Cuddapah, S., Cui, K., Roh, T.Y., Schones, D.E., Wang, Z., Wei, G., Chepelev, I. and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell, 129, 823-837.
36. Whittemore, L.A. and Maniatis, T. (1990) Postinduction turnoff of beta-interferon gene expression. Mol. Cell. Biol., 10, 1329-1337.
37. Klar, M. and Bode, J. (2005) Enhanceosome formation over the beta interferon promoter underlies a remote-control mechanism mediated by YY1 and YY2. Mol. Cell. Biol., 25, 10159-10170.
38. Hu, J., Sealfon, S.C., Hayot, F., Jayaprakash, C., Kumar, M., Pendleton, A.C., Ganee, A., Fernandez-Sesma, A., Moran, T.M. and Wetmur, J.G. (2007) Chromosome-specific and noisy IFNB1 transcription in individual virus-infected human primary dendritic cells. Nucleic Acids Res., 35, 5232-5241.
39. Apostolou, E. and Thanos, D. (2008) Virus infection induces NF-kB dependent interchromosomal associations mediating monoallelic IFN-b gene expression. Cell, 134, 85-96.
40. Mighell, A.J., Markham, A.F. and Robinson, P.A. (1997) Alu sequences. FEBS Lett., 417, 1-5.
41. Liang, R., Igarashi, H., Tsuzuki, T., Nakabeppu, Y., Sekiguchi, M., Kasprzak, K.S. and Shiao, Y.H. (2001) Presence of potential nickel-responsive element(s) in the mouse MTH1 promoter. Ann. Clin. Lab. Sci., 31, 91-98.
42. Xu, N., Tsai, C.L. and Lee, J.T. (2006) Transient homologous chromosome pairing marks the onset of X inactivation. Science, 311, 1149-1152.
43. Bacher, C.P., Guggiari, M., Brors, B., Augui, S., Clerc, P., Avner, P., Eils, R. and Heard, E. (2006) Transient colocalization of X-inactivation centres accompanies the initiation of X inactivation. Nat. Cell Biol., 8, 293-299.
44. Magklara, A., Yen, A., Colquitt, B.M., Clowney, E.J., Allen, W., Markenscoff-Papadimitriou, E., Evans, Z.A., Kheradpour, P., Mountoufaris, G., Carey, C. et al. (2011) An epigenetic signature for monoallelic olfactory receptor expression. Cell, 145, 555-570.
45. Affar, el.B., Gay, F., Shi, Y., Liu, H., Huarte, M., Wu, S., Collins, T., Li, E. and Shi, Y. (2006) Essential dosage-dependent functions of the transcription factor Yin Yang 1 in late embryonic development and cell cycle progression. Mol. Cell. Biol., 26, 3565-3581.
46. Huang, S., Li, X., Yusufzai, T.M., Qiu, Y. and Felsenfeld, G. (2007) USF1 recruits histone modification complexes and is critical for maintenance of a chromatin barrier. Mol. Cell. Biol., 27, 7991-8002.
47. Shestakova, E., Mansuroglu, Z., Mokrani, H., Ghinea, N. and Bonnefoy, E. (2004) Transcription factor YY1 associates with pericentromeric g-satellite DNA in cycling but not in quiescent (G0) cells. Nucleic Acids Res., 32, 4390-4399.
48. Underhill, C., Qutob, M.S., Yee, S.P. and Torchia, J. (2000) A novel nuclear receptor corepressor complex, N-CoR, contains components of the mammalian SWI/SNF complex and the corepressor KAP-1. J. Biol. Chem., 275, 40463-40470.
49. David, G., Turner, G.M., Yao, Y., Protopopov, A. and DePinho, R.A. (2003) mSin3-associated protein, mSds3, is essential for pericentric heterochromatin formation and chromosome segregation in mammalian cells. Genes Dev., 17, 2396-2405.
50. Vaute, O., Nicolas, E., Vandel, L. and Trouche, D. (2002) Functional and physical interaction between the histone methyl transferase Suv39H1 and histone deacetylases. Nucleic Acids Res., 30, 475-481.
51. Gyory, I., Wu, J., Fejér, G., Seto, E. and Wright, K.I. (2004) PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat. Immunol., 5, 299-308.
52. Keller, A.D. and Maniatis, T. (1991) Identification and characterization of a novel repressor of b-interferon gene expression. Genes Dev., 5, 868-879.
53. Siednienko, J., Maratha, A., Yang, S., Mitkiewicz, M., Miggin, S.M. and Moynagh, P.N. (2011) The NF-kB subunits RelB and cRel negatively regulate TLR3-mediated IFN-b production via induction of the transcriptional repressor protein YY1. J. Biol. Chem., 286, 44750-44763.
54. de la Cruz, C., Kirmizis, A., Simon, M.D., Isono, K., Koseki, H. and Panning, B. (2007) The Polycomb Group Protein SUZ12 regulates histone H3 lysine 9 methylation and HP1a distribution. Chromosome Res., 15, 299-314.
55. Faulk, C.D. and Kim, J. (2009) YY1's DNA-binding motifs in mammalian olfactory receptor genes. BMC Genomics, 10, 576.
56. Liu, H., Schmidt-Supprian, M., Shi, Y., Hobeika, E., Barteneva, N., Jumaa, H., Pelanda, R., Reth, M., Skok, J., Rajewsky, K. et al. (2007) Yin Yang 1 is a critical regulator of B-cell development. Genes Dev., 21, 1179-1189.
57. Bolte, S. and Cordelières, F.P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc., 224, 213-232.