Non-coding RNAs: Novel players in chromatin-regulation during viral latency

Current Opinion in Virology

Volumn 3, Issue 4, 2013, Pages 387-393

  Eilebrecht, Sebastian ^a   Schwartz, Christian ^b   Rohr, Olivier ^b  

^a INSERM U955   (France)

^b Institut de Parasitologie et de Pathologie Tropicale   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE H1; LONG UNTRANSLATED RNA; MICRORNA; PROTEIN; UNTRANSLATED RNA;

ARTICLE; CELL INTERACTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; COMPETITIVE INHIBITION; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE SILENCING; HEMATOPOIETIC STEM CELL; HERPES SIMPLEX VIRUS 1; HETEROCHROMATIN; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN IMMUNODEFICIENCY VIRUS 1; LATENT PERIOD; MICROPROCESSOR; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROCESSING; PROTEIN SECONDARY STRUCTURE; SYSTEMS BIOLOGY; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; VIRUS GENE;

EID: 84885057631     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2013.04.001     Document Type: Review

References (67)

1. Divito S, Cherpes TL, Hendricks RL: A triple entente: virus, neurons, and CD8+ T cells maintain HSV-1 latency. Immunol Res 2006, 36:119-126. (Pubitemid 46398586)
2. Ballestas ME, Kaye KM: The latency-associated nuclear antigen, a multifunctional protein central to Kaposi's sarcoma-associated herpesvirus latency. Future Microbiol 2011, 6:1399-1413.
3. Takacs M, Banati F, Koroknai A, Segesdi J, Salamon D, Wolf H, Niller HH, Minarovits J: Epigenetic regulation of latent Epstein- Barr virus promoters. Biochim Biophys Acta 2010, 1799: 228-235.
4. Margolis DM: Histone deacetylase inhibitors and HIV latency. Curr Opin HIV AIDS 2011, 6:25-29.
5. Hakre S, Chavez L, Shirakawa K, Verdin E: Epigenetic regulation of HIV latency. Curr Opin HIV AIDS 2011, 6:19-24.
6. Benecke A: Genomic plasticity and information processing by transcription coregulators. ComPlexUs 2003, 1:65-76.
7. Marcello A: Latency: The hidden HIV-1 challenge. Retrovirology 2006, 3:7.
8. Van Wolfswinkel JC, Ketting RF: The role of small non-coding RNAs in genome stability and chromatin organization. J Cell Sci 2010, 123:1825-1839.
9. Olovnikov I, Aravin AA, Fejes Toth K: Small RNA in the nucleus: The RNA-chromatin Ping-Pong. Curr Opin Genet Dev 2012, 22:164-171.
10. Mercer TR, Mattick JS: Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 2013, 20:300-307.
11. Flynn RA, Chang HY: Active chromatin and noncoding RNAs: An intimate relationship. Curr Opin Genet Dev 2012, 22:172-178.
12. Lee JT: Epigenetic regulation by long noncoding RNAs. Science 2012, 338:1435-1439.
13. Magistri M, Faghihi MA, St Laurent G 3rd, Wahlestedt C: Regulation of chromatin structure by long noncoding RNAs:focus on natural antisense transcripts. Trends Genet 2012, 28:389-396.
14. Malecova B, Morris KV: Transcriptional gene silencing through epigenetic changes mediated by non-coding RNAs. Curr Opin Mol Ther 2010, 12:214-222.
15. Knipe DM, Lieberman PM, Jung JU, McBride AA, Morris KV, Ott M, Margolis D, Nieto A, Nevels M, Parks RJ, Kristie TM: Snapshots: chromatin control of viral infection. Virology 2013, 435:141-156.
16. Bloom DC, Giordani NV, Kwiatkowski DL: Epigenetic regulation of latent HSV-1 gene expression. Biochim Biophys Acta 2010, 1799:246-256.
17. Minarovits J: Epigenotypes of latent herpesvirus genomes. Curr Top Microbiol Immunol 2006, 310:61-80. (Pubitemid 47400286)
18. Nevels M, Nitzsche A, Paulus C: How to control an infectious bead string: nucleosome-based regulation and targeting of herpesvirus chromatin. Rev Med Virol 2011, 21:154-180.
19. Huang J, Kent JR, Placek B, Whelan KA, Hollow CM, Zeng PY, Fraser NW, Berger SL: Trimethylation of histone H3 lysine 4 by Set1 in the lytic infection of human herpes simplex virus 1. J Virol 2006, 80:5740-5746. (Pubitemid 43849152)
20. Liang Y, Vogel JL, Narayanan A, Peng H, Kristie TM: Inhibition of the histone demethylase LSD1 blocks alpha-herpesvirus lytic replication and reactivation from latency. Nat Med 2009, 15:1312-1317.
21. Narayanan A, Ruyechan WT, Kristie TM: 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 2007, 104:10835-10840. (Pubitemid 47175187)
22. Donahue DA, Wainberg MA: Cellular and molecular mechanisms involved in the establishment of HIV-1 latency. Retrovirology 2013, 10:11.
23. Le Douce V, Colin L, Redel L, Cherrier T, Herbein G, Aunis D, Rohr O, Van Lint C, Schwartz C: LSD1 cooperates with CTIP2 to promote HIV-1 transcriptional silencing. Nucleic Acids Res 2012, 40:1904-1915.
24. Marban C, Suzanne S, Dequiedt F, de Walque S, Redel L, Van Lint C, Aunis D, Rohr O: Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. EMBO J 2007, 26:412-423. (Pubitemid 46160942)
25. Pinskaya M, Gourvennec S, Morillon A: H3 lysine 4 di- and tri-methylation deposited by cryptic transcription attenuates promoter activation. EMBO J 2009, 28:1697-1707.
26. Pinskaya M, Morillon A: Histone H3 lysine 4 di-methylation: A novel mark for transcriptional fidelity? Epigenetics 2009, 4:302-306.
27. Friedman J, Cho WK, Chu CK, Keedy KS, Archin NM, Margolis DM, Karn J: Epigenetic silencing of HIV-1 by the histone H3 lysine 27 methyltransferase enhancer of zeste 2. J Virol 2011, 85:9078-9089.
28. Guttman M, Rinn JL: Modular regulatory principles of large noncoding RNAs. Nature 2012, 482:339-346.
29. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY: Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129:1311-1323. (Pubitemid 46962090)
30. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y et al.: Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010, 464:1071-1076. This study demonstrated that HOTAIR is overexpressed in breast cancer, which results in genome-wide changes of PRC2-mediated H3K27 methylation. The resulting changes in gene expression lead to an increase of metastatic potential.
31. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, Song JJ, Kingston RE, Borowsky M, Lee JT: Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell 2010, 40:939-953.
32. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY: Long noncoding RNA as modular scaffold of histone modification complexes. Science 2010, 329:689-693.
33. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A et al.: Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci USA 2009, 106:11667-11672.
34. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X et al.: LincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011, 477:295-300. This study functionally characterized lincRNAs expressed in mouse embryonic stem (ES) cells. Guttman et al. identified several lincRNAs associating with multiple chromatin-modifying enzymes and that way affecting gene expression patterns, which are important for ES cell state.
35. Borah S, Darricarrere N, Darnell A, Myoung J, Steitz JA: A viral nuclear noncoding RNA binds re-localized poly(A) binding protein and is required for late KSHV gene expression. PLoS Pathog 2011, 7:e1002300.
36. Rossetto CC, Pari G: KSHV PAN RNA associates with demethylases UTX and JMJD3 to activate lytic replication through a physical interaction with the virus genome. PLoS Pathog 2012, 8:e1002680. This study demonstrated a role of KSHV PAN RNA in activating the repressed KSHV genome by recruiting the HDMs UTX and JMJD3 as well as the HMT MLL2 to the viral promoter, resulting in a decrease of the repressive H3K27 chromatin mark.
37. Cliffe AR, Garber DA, Knipe DM: Transcription of the herpes simplex virus latency-associated transcript promotes the formation of facultative heterochromatin on lytic promoters. J Virol 2009, 83:8182-8190.
38. Li G, Reinberg D: Chromatin higher-order structures and gene regulation. Curr Opin Genet Dev 2011, 21:175-186.
39. Eilebrecht S, Brysbaert G, Wegert T, Urlaub H, Benecke BJ, Benecke A: 7SK small nuclear RNA directly affects HMGA1 function in transcription regulation. Nucleic Acids Res 2011, 39:2057-2072. This study identified 7SK RNA as a negative regulator of the chromatin master regulator and histone H1 antagonist HMGA1.
40. Eilebrecht S, Becavin C, Leger H, Benecke BJ, Benecke A: HMGA1-dependent and independent 7SK RNA gene regulatory activity. RNA Biol 2011, 8:143-157.
41. Zhou Q, Li T, Price DH: RNA polymerase II elongation control. Annu Rev Biochem 2012, 81:119-143.
42. Ott M, Geyer M, Zhou Q: The control of HIV transcription: keeping RNA polymerase II on track. Cell Host Microbe 2011, 10:426-435.
43. Eilebrecht S, Benecke BJ, Benecke A: 7SK snRNA-mediated, gene-specific cooperativity of HMGA1 and P-TEFb. RNA Biol 2011, 8:1084-1093.
44. Kotake Y, Nakagawa T, Kitagawa K, Suzuki S, Liu N, Kitagawa M, Xiong Y: Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4b) tumor suppressor gene. Oncogene 2011, 30:1956-1962.
45. Yu W, Gius D, Onyango P, Muldoon-Jacobs K, Karp J, Feinberg AP, Cui H: Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature 2008, 451:202-206.
46. Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou MM: Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycombCBX7 in transcriptional silencing of INK4a. Mol Cell 2010, 38:662-674. This study identified ANRIL-mediated epigenetic silencing of the tumor suppressor p16/INK4a locus by recruiting chromobox 7 and polycomb repressive complex 1.
47. Landry S, Halin M, Lefort S, Audet B, Vaquero C, Mesnard JM, Barbeau B: Detection, characterization and regulation of antisense transcripts in HIV-1. Retrovirology 2007, 4:71.
48. Kobayashi-Ishihara M, Yamagishi M, Hara T, Matsuda Y, Takahashi R, Miyake A, Nakano K, Yamochi T, Ishida T, Watanabe T: HIV-1-encoded antisense RNA suppresses viral replication for a prolonged period. Retrovirology 2012, 9:38. This study characterized a major occurring antisense transcript arising from HIV provirus and identified this transcript to play a role during viral replication.
49. Eilebrecht S, Wilhelm E, Benecke BJ, Bell B, Benecke AG: HMGA1 directly interacts with TAR to modulate basal and Tatdependent HIV transcription. RNA Biol 2013, 10:1-9.
50. Hammond SM: Dicing and slicing: The core machinery of the RNA interference pathway. FEBS Lett 2005, 579:5822-5829. (Pubitemid 41484128)
51. Lejeune E, Bayne EH, Allshire RC: On the connection between RNAi and heterochromatin at centromeres. Cold Spring Harb Symp Quant Biol 2010, 75:275-283.
52. Noma K, Sugiyama T, Cam H, Verdel A, Zofall M, Jia S, Moazed D, Grewal SI: RITS acts in cis to promote RNA interferencemediated transcriptional and post-transcriptional silencing. Nat Genet 2004, 36:1174-1180. (Pubitemid 41288966)
53. Weinberg MS, Villeneuve LM, Ehsani A, Amarzguioui M, Aagaard L, Chen ZX, Riggs AD, Rossi JJ, Morris KV: The antisense strand of small interfering RNAs directs histone methylation and transcriptional gene silencing in human cells. RNA 2006, 12:256-262. (Pubitemid 43121930)
54. Klase Z, Kale P, Winograd R, Gupta MV, Heydarian M, Berro R, McCaffrey T, Kashanchi F: HIV-1 TAR element is processed by dicer to yield a viral micro-RNA involved in chromatin remodeling of the viral LTR. BMC Mol Biol 2007, 8:63.
55. Cullen BR: Viruses and microRNAs: Riscy interactions with serious consequences. Genes Dev 2011, 25:1881-1894.
56. Wagschal A, Rousset E, Basavarajaiah P, Contreras X, Harwig A, Laurent-Chabalier S, Nakamura M, Chen X, Zhang K, Meziane O, Boyer F et al.: Microprocessor, Setx, Xrn2, and Rrp6 co-operate to induce premature termination of transcription by RNAPII. Cell 2012, 150:1147-1157. Wagschal et al. characterized the cellular factors involved in the premature termination of HIV transcription, the cleavage of HIV-1 TAR and the subsequent processing to viral miRNAs, which are thought to be subsequently involved in chromatin remodeling at the HIV promoter (as shown by Klase et al. [54]).
57. Bouchat S, Gatot JS, Kabeya K, Cardona C, Colin L, Herbein G, De Wit S, Clumeck N, Lambotte O, Rouzioux C, Rohr O et al.: Histone methyltransferase inhibitors induce HIV-1 recovery in resting CD4(+) T cells from HIV-1-infected HAART-treated patients. AIDS 2012, 26:1473-1482.
58. Colin L, Van Lint C: Molecular control of HIV-1 postintegration latency: implications for the development of new therapeutic strategies. Retrovirology 2009, 6:111.
59. Le Douce V, Janossy A, Hallay H, Ali S, Riclet R, Rohr O, Schwartz C: Achieving a cure for HIV infection: do we have reasons to be optimistic? J Antimicrob Chemother 2012, 67:1063-1074.
60. Redel L, Le Douce V, Cherrier T, Marban C, Janossy A, Aunis D, Van Lint C, Rohr O, Schwartz C: HIV-1 regulation of latency in the monocyte-macrophage lineage and in CD4+ T lymphocytes. J Leukoc Biol 2010, 87:575-588.
61. Reeves MB, Lehner PJ, Sissons JG, Sinclair JH: An in vitro model for the regulation of human cytomegalovirus latency and reactivation in dendritic cells by chromatin remodelling. J Gen Virol 2005, 86:2949-2954. (Pubitemid 41555558)
62. Le Douce V, Herbein G, Rohr O, Schwartz C: Molecular mechanisms of HIV-1 persistence in the monocyte- macrophage lineage. Retrovirology 2010, 7:.
63. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL: Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 2011, 25:1915-1927.
64. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, Rinn JL et al.: Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 2010, 28:503-510. In this study a novel technology, based only on RNA-seq reads and the genome sequence, was applied to determine the cellular transcriptome. Different cell types from different tissues were compared and despite differentially expressed protein coding genes, strong differences in the expression of known and novel ncRNAs were detected.
65. Peng X, Gralinski L, Armour CD, Ferris MT, Thomas MJ, Proll S, Bradel-Tretheway BG, Korth MJ, Castle JC, Biery MC, Bouzek HK et al.: Unique signatures of long noncoding RNA expression in response to virus infection and altered innate immune signaling. MBio 2010, 1:5.
66. Chang ST, Sova P, Peng X, Weiss J, Law GL, Palermo RE, Katze MG: Next-generation sequencing reveals HIV-1- mediated suppression of T cell activation and RNA processing and regulation of noncoding RNA expression in a CD4+ T cell line. MBio 2011, 2:5. Chang et al. applied next generation sequencing technology to identify cellular and viral transcriptome changes upon HIV-1 infection in CD4+ T cells. Besides differentially expressed host and viral mRNAs, also the expression of ncRNAs were shown to be affected, including miRNAs, snoRNAs and antisense transcripts.
67. Benecke AG: Critical dynamics in host-pathogen systems. Curr Top Microbiol Immunol 2013, 363:235-259. Non-coding RNAs Eilebrecht, Schwartz and Rohr 393 www.