LSD1 cooperates with CTIP2 to promote HIV-1 transcriptional silencing.

Cell Line; Cell Nucleus/chemistry/virology; Epigenesis, Genetic; Gene Silencing; HIV Long Terminal Repeat; HIV-1/genetics/physiology; Histone Demethylases/analysis/metabolism; Histone-Lysine N-Methyltransferase/metabolism; Histones/metabolism; Humans; Methylation; Microglia/virology; Promoter Regions, Genetic; Repressor Proteins/analysis/metabolism; Transcription, Genetic; Tumor Suppressor Proteins/analysis/metabolism; Virus Replication; tat Gene Products, Human Immunodeficiency Virus/analysis

Abstract :

[en] Microglial cells are the main HIV-1 targets in the central nervous system (CNS) and constitute an important reservoir of latently infected cells. Establishment and persistence of these reservoirs rely on the chromatin structure of the integrated proviruses. We have previously demonstrated that the cellular cofactor CTIP2 forces heterochromatin formation and HIV-1 gene silencing by recruiting HDAC and HMT activities at the integrated viral promoter. In the present work, we report that the histone demethylase LSD1 represses HIV-1 transcription and viral expression in a synergistic manner with CTIP2. We show that recruitment of LSD1 at the HIV-1 proximal promoter is associated with both H3K4me3 and H3K9me3 epigenetic marks. Finally, our data suggest that LSD1-induced H3K4 trimethylation is linked to hSET1 recruitment at the integrated provirus.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Le Douce, Valentin

Colin, Laurence

Redel, Laetitia

Cherrier, Thomas ; Université de Liège - ULiège > Chimie et bio-industries > Biologie cell. et moléc.

Herbein, Georges

Aunis, Dominique

Rohr, Olivier

Van Lint, Carine

Schwartz, Christian

Language :

English

Title :

LSD1 cooperates with CTIP2 to promote HIV-1 transcriptional silencing.

Publication date :

2012

Journal title :

Nucleic Acids Research

ISSN :

0305-1048

eISSN :

1362-4962

Publisher :

Oxford University Press, United Kingdom

Volume :

Issue :

Pages :

1904-15

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 25 January 2013

Statistics

Number of views

79 (1 by ULiège)

Number of downloads

80 (2 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Kornberg, R. D. and Thomas, J. O. (1974) Chromatin structure; oligomers of the histones. Science, 184, 865-868.
Fischle, W., Wang, Y. and Allis, C. D. (2003) Histone and chromatin cross-talk. Curr. Opin. Cell. Biol., 15, 172-183.
Imhof, A. and Becker, P. B. (2001) Modifications of the histone N-terminal domains Evidence for an "epigenetic code"?. Mol. Biotechnol., 17, 1-13.
Jenuwein, T. and Allis, C. D. (2001) Translating the histone code. Science, 293, 1074-1080.
Pinskaya, M. and Morillon, A. (2009) Histone H3 lysine 4 di-methylation: a novel mark for transcriptional fidelity? Epigenetics, 4, 302-306.
Kouzarides, T. (2007) Chromatin modifications and their function. Cell, 128, 693-705.
Shilatifard, A. (2006) Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem., 75, 243-269.
Sims, R. J. 3rd and Reinberg, D. (2006) Histone H3 Lys 4 methylation: caught in a bind? Genes Dev., 20, 2779-2786.
Kim, T. and Buratowski, S. (2009) Dimethylation of H3K4 by Set1 recruits the Set3 histone deacetylase complex to 5' transcribed regions. Cell, 137, 259-272.
Vakoc, C. R., Mandat, S. A., Olenchock, B. A. and Blobel, G. A. (2005) Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol. Cell., 19, 381-391.
Pinskaya, M., Gourvennec, S. and Morillon, A. (2009) H3 lysine 4 di-and trimethylation deposited by cryptic transcription attenuates promoter activation. EMBO J., 28, 1697-1707.
du Chene, I., Basyuk, E., Lin, Y. L., Triboulet, R., Knezevich, A., Chable-Bessia, C., Mettling, C., Baillat, V., Reynes, J., Corbeau, P. et al. (2007) Suv39H1 and HP1gamma are responsible for chromatin-mediated HIV-1 transcriptional silencing and post-integration latency. EMBO J., 26, 424-435.
Marban, C., Suzanne, S., Dequiedt, F., de Walque, S., Redel, L., Van Lint, C., Aunis, D. and Rohr, O. (2007) Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. EMBO J., 26, 412-423.
Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., Casero, R. A. and Shi, Y. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell, 119, 941-953.
Ballas, N., Grunseich, C., Lu, D. D., Speh, J. C. and Mandel, G. (2005) REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell, 121, 645-657.
Battaglioli, E., Andres, M. E., Rose, D. W., Chenoweth, J. G., Rosenfeld, M. G., Anderson, M. E. and Mandel, G. (2002) REST repression of neuronal genes requires components of the hSWI. SNF complex. J. Biol. Chem., 277, 41038-41045.
Forneris, F., Binda, C., Battaglioli, E. and Mattevi, A. (2008) LSD1: oxidative chemistry for multifaceted functions in chromatin regulation. Trends Biochem Sci, 33, 181-189.
Metzger, E., Wissmann, M., Yin, N., Muller, J. M., Schneider, R., Peters, A. H., Gunther, T., Buettner, R. and Schule, R. (2005) LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature, 437, 436-439.
Wissmann, M., Yin, N., Muller, J. M., Greschik, H., Fodor, B. D., Jenuwein, T., Vogler, C., Schneider, R., Gunther, T., Buettner, R. et al. (2007) Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression. Nat. Cell. Biol., 9, 347-353.
Huang, J., Kent, J. R., Placek, B., Whelan, K. A., Hollow, C. M., Zeng, P. Y., Fraser, N. W. and Berger, S. L. (2006) Trimethylation of histone H3 lysine 4 by Set1 in the lytic infection of human herpes simplex virus 1. J. Virol., 80, 5740-5746.
Liang, Y., Vogel, J. L., Narayanan, A., Peng, H. and Kristie, T. M. (2009) Inhibition of the histone demethylase LSD1 blocks alpha-herpesvirus lytic replication and reactivation from latency. Nat. Med., 15, 1312-1317.
Narayanan, A., Ruyechan, W. T. and Kristie, T. M. (2007) The coactivator host cell factor-1 mediates Set1 and MLL1 H3K4 trimethylation at herpesvirus immediate early promoters for initiation of infection. Proc. Natl Acad. Sci. USA, 104, 10835-10840.
Peng, H., Nogueira, M. L., Vogel, J. L. and Kristie, T. M. (2010) Transcriptional coactivator HCF-1 couples the histone chaperone Asf1b to HSV-1 DNA replication components. Proc. Natl Acad. Sci. USA, 107, 2461-2466.
Garcia-Bassets, I., Kwon, Y. S., Telese, F., Prefontaine, G. G., Hutt, K. R., Cheng, C. S., Ju, B. G., Ohgi, K. A., Wang, J., Escoubet-Lozach, L. et al. (2007) Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell, 128, 505-518.
Le Douce, V., Herbein, G., Rohr, O. and Schwartz, C. (2010) Molecular mechanisms of HIV1 persistence in the monocyte-macrophage lineage. Retrovirology, 7, 32.
Colin, L. and Van Lint, C. (2009) Molecular control of HIV-1 postintegration latency: implications for the development of new therapeutic strategies. Retrovirology, 6, 111.
Reuse, S., Calao, M., Kabeya, K., Guiguen, A., Gatot, J. S., Quivy, V., Vanhulle, C., Lamine, A., Vaira, D., Demonte, D. et al. (2009) Synergistic activation of HIV-1 expression by deacetylase inhibitors and prostratin: implications for treatment of latent infection. PLoS One, 4, e6093.
Avram, D., Fields, A., Pretty On Top, K., Nevrivy, D. J., Ishmael, J. E. and Leid, M. (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.
Marban, C., Redel, L., Suzanne, S., Van Lint, C., Lecestre, D., Chasserot-Golaz, S., Leid, M., Aunis, D., Schaeffer, E. and Rohr, O. (2005) COUP-TF interacting protein 2 represses the initial phase of HIV-1 gene transcription in human microglial cells. Nucleic Acids Res., 33, 2318-2331.
Rohr, O., Lecestre, D., Chasserot-Golaz, S., Marban, C., Avram, D., Aunis, D., Leid, M. and Schaeffer, E. (2003) Recruitment of Tat to heterochromatin protein HP1 via interaction with CTIP2 inhibits human immunodeficiency virus type 1 replication in microglial cells. J. Virol., 77, 5415-5427.
Trono, D., Van Lint, C., Rouzioux, C., Verdin, E., Barre-Sinoussi, F., Chun, T. W. and Chomont, N. (2010) HIV persistence and the prospect of long-term drug-free remissions for HIV-infected individuals. Science, 329, 174-180.
Cherrier, T., Suzanne, S., Redel, L., Calao, M., Marban, C., Samah, B., Mukerjee, R., Schwartz, C., Gras, G., Sawaya, B. E. et al. (2009) p21(WAF1) gene promoter is epigenetically silenced by CTIP2 and SUV39H1. Oncogene, 28, 3380-3389.
Vazquez, N., Greenwell-Wild, T., Marinos, N. J., Swaim, W. D., Nares, S., Ott, D. E., Schubert, U., Henklein, P., Orenstein, J. M., Sporn, M. B. et al. (2005) Human immunodeficiency virus type 1-induced macrophage gene expression includes the p21 gene, a target for viral regulation. J. Virol., 79, 4479-4491.
Janabi, N., Peudenier, S., Heron, B., Ng, K. H. and Tardieu, M. (1995) Establishment of human microglial cell lines after transfection of primary cultures of embryonic microglial cells with the SV40 large T antigen. Neurosci. Lett., 195, 105-108.
Musri, M. M., Carmona, M. C., Hanzu, F. A., Kaliman, P., Gomis, R. and Parrizas, M. Histone demethylase LSD1 regulates adipogenesis. J. Biol. Chem, 285, 30034-30041.
Ouyang, J., Shi, Y., Valin, A., Xuan, Y. and Gill, G. (2009) Direct binding of CoREST1 to SUMO-2/3 contributes to gene-specific repression by the LSD1/CoREST1/HDAC complex. Mol. Cell., 34, 145-154.
Jiang, G., Espeseth, A., Hazuda, D. J. and Margolis, D. M. (2007) c-Myc and Sp1 contribute to proviral latency by recruiting histone deacetylase 1 to the human immunodeficiency virus type 1 promoter. J. Virol., 81, 10914-10923.
Redel, L., Le Douce, V., Cherrier, T., Marban, C., Janossy, A., Aunis, D., Van Lint, C., Rohr, O. and Schwartz, C. (2010) HIV-1 regulation of latency in the monocyte-macrophage lineage and in CD4+T lymphocytes. J. Leukoc. Biol., 87, 575-588.
Barber, S. A., Gama, L., Dudaronek, J. M., Voelker, T., Tarwater, P. M. and Clements, J. E. (2006) Mechanism for the establishment of transcriptional HIV latency in the brain in a simian immunodeficiency virus-macaque model. J. Infect. Dis., 193, 963-970.
Blazkova, J., Trejbalova, K., Gondois-Rey, F., Halfon, P., Philibert, P., Guiguen, A., Verdin, E., Olive, D., Van Lint, C., Hejnar, J. et al. (2009) CpG methylation controls reactivation of HIV from latency. PLoS Pathog., 5, e1000554.
Kauder, S. E., Bosque, A., Lindqvist, A., Planelles, V. and Verdin, E. (2009) Epigenetic regulation of HIV-1 latency by cytosine methylation. PLoS Pathog., 5, e1000495.
Shi, Y. J., Matson, C., Lan, F., Iwase, S., Baba, T. and Shi, Y. (2005) Regulation of LSD1 histone demethylase activity by its associated factors. Mol. Cell., 19, 857-864.
Krogan, N. J., Dover, J., Khorrami, S., Greenblatt, J. F., Schneider, J., Johnston, M. and Shilatifard, A. (2002) COMPASS, a histone H3 (Lysine 4) methyltransferase required for telomeric silencing of gene expression. J. Biol. Chem., 277, 10753-10755.
Miller, T., Krogan, N. J., Dover, J., Erdjument-Bromage, H., Tempst, P., Johnston, M., Greenblatt, J. F. and Shilatifard, A. (2001) COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc. Natl Acad. Sci. USA, 98, 12902-12907.
Schneider, J., Wood, A., Lee, J. S., Schuster, R., Dueker, J., Maguire, C., Swanson, S. K., Florens, L., Washburn, M. P. and Shilatifard, A. (2005) Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol. Cell., 19, 849-856.
Wood, A., Shukla, A., Schneider, J., Lee, J. S., Stanton, J. D., Dzuiba, T., Swanson, S. K., Florens, L., Washburn, M. P., Wyrick, J. et al. (2007) Ctk complex-mediated regulation of histone methylation by COMPASS. Mol. Cell. Biol., 27, 709-720.
Eszterhas, S. K., Bouhassira, E. E., Martin, D. I. and Fiering, S. (2002) Transcriptional interference by independently regulated genes occurs in any relative arrangement of the genes and is influenced by chromosomal integration position. Mol. Cell. Biol., 22, 469-479.
Wang, G. P., Ciuffi, A., Leipzig, J., Berry, C. C. and Bushman, F. D. (2007) HIV integration site selection: analysis by massively parallel pyrosequencing reveals association with epigenetic modifications. Genome Res., 17, 1186-1194.