The lncRNA MIR31HG regulates p16 INK4A expression to modulate senescence

Nature Communications

Volumn 6, Issue , 2015, Pages

  Montes, Marta ^a   Nielsen, Morten M ^b   Maglieri, Giulia ^a   Jacobsen, Anders ^c   Højfeldt, Jonas ^a,d   Agrawal Singh, Shuchi ^a,d   Hansen, Klaus ^a,d   Helin, Kristian ^a,d   Van De Werken, Harmen J G ^e   Pedersen, Jakob S ^b,f   Lund, Anders H ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; LONG UNTRANSLATED RNA; MIR31HG PROTEIN; POLYCOMB GROUP PROTEIN; UNCLASSIFIED DRUG;

CANCER; CYTOPLASM; GENE EXPRESSION; GENOMICS; SENESCENCE;

ARTICLE; CELL AGING; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; ENHANCER REGION; GENE; GENE EXPRESSION REGULATION; GENE LOCUS; GENE REPRESSION; GENOMICS; HUMAN; HUMAN CELL; MELANOMA; ONCOGENE; PHENOTYPE; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; GENE SILENCING; HEK293 CELL LINE; METABOLISM; MOUSE;

ANIMALS; CELL AGING; CYCLIN-DEPENDENT KINASE INHIBITOR P16; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; MELANOMA; MICE; ONCOGENES; PHENOTYPE; POLYCOMB-GROUP PROTEINS; PROTO-ONCOGENE PROTEINS B-RAF; RNA, LONG NONCODING;

EID: 84928820765     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7967     Document Type: Article

References (70)

1. Batista, P. J. & Chang, H. Y. Long noncoding RNAs: cellular address codes in development and disease. Cell 152, 1298-1307 (2013).
2. Qureshi, I. A. & Mehler, M. F. Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nat. Rev. Neurosci. 13, 528-541 (2012).
3. Ghosal, S., Das, S. & Chakrabarti, J. Long Noncoding RNAs: new players in the molecular mechanism for maintenance and differentiation of pluripotent stem cells. Stem Cells Dev. 22, 2240-2253 (2013).
4. Lee, J. T. Epigenetic regulation by long noncoding RNAs. Science 338, 1435-1439 (2012).
5. Bergmann, J. H. & Spector, D. L. Long non-coding RNAs: modulators of nuclear structure and function. Curr. Opin. Cell Biol. 26, 10-18 (2014).
6. Yoon, J. H., Abdelmohsen, K. & Gorospe, M. Posttranscriptional gene regulation by long noncoding RNA. J. Mol. Biol. 425, 3723-3730 (2013).
7. Petruk, S. et al. Transcription of bxd noncoding RNAs promoted by trithorax represses Ubx in cis by transcriptional interference. Cell 127, 1209-1221 (2006).
8. Zhao, J., Sun, B. K., Erwin, J. A., Song, J. J. & Lee, J. T. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322, 750-756 (2008).
9. Melo, C. A. et al. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol. Cell 49, 524-535 (2013).
10. Gupta, R. A. et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464, 1071-1076 (2010).
11. Tsai, M. C. et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science 329, 689-693 (2010).
12. Guttman, M. et al. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477, 295-300 (2011).
13. Huarte, M. et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142, 409-419 (2010).
14. Hayflick, L. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37, 614-636 (1965).
15. Kuilman, T., Michaloglou, C., Mooi, W. J. & Peeper, D. S. The essence of senescence. Genes Dev. 24, 2463-2479 (2010).
16. Storer, M. et al. Senescence is a developmental mechanism that contributes to embryonic growth and patterning. Cell 155, 1119-1130 (2013).
17. Munoz-Espin, D. et al. Programmed cell senescence during mammalian embryonic development. Cell 155, 1104-1118 (2013).
18. Serrano, M., Lin, A. W., McCurrach, M. E., Beach, D. & Lowe, S. W. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88, 593-602 (1997).
19. Michaloglou, C. et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 436, 720-724 (2005).
20. Braig, M. et al. Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 436, 660-665 (2005).
21. Salama, R., Sadaie, M., Hoare, M. & Narita, M. Cellular senescence and its effector programs. Genes Dev. 28, 99-114 (2014).
22. Coppe, J. P., Desprez, P. Y., Krtolica, A. & Campisi, J. The senescenceassociated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol. 5, 99-118 (2010).
23. Collado, M., Blasco, M. A. & Serrano, M. Cellular senescence in cancer and aging. Cell 130, 223-233 (2007).
24. Campisi, J. Cancer and ageing: rival demons? Nat. Rev. Cancer 3, 339-349 (2003).
25. Jacobs, J. J., Kieboom, K., Marino, S., DePinho, R. A. & van Lohuizen, M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397, 164-168 (1999).
26. Bracken, A. P. et al. The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev. 21, 525-530 (2007).
27. Popov, N. & Gil, J. Epigenetic regulation of the INK4b-ARF-INK4a locus: in sickness and in health. Epigenetics 5, 685-690 (2010).
28. Pasmant, E. et al. Characterization of a germ-line deletion, including the entire INK4/ARF locus, in a melanoma-neural system tumor family: identification of ANRIL, an antisense noncoding RNA whose expression coclusters with ARF. Cancer Res. 67, 3963-3969 (2007).
29. Yu, W. et al. Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature 451, 202-206 (2008).
30. Kotake, Y. et al. Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene 30, 1956-1962 (2011).
31. Kumar, P. P. et al. Coordinated control of senescence by lncRNA and a novel T-box3 co-repressor complex. eLife 3, e02805 (2014).
32. Puvvula, P. K. et al. Long noncoding RNA PANDA and scaffold-attachmentfactor SAFA control senescence entry and exit. Nat. Commun. 5, 5323 (2014).
33. Abdelmohsen, K. et al. Senescence-associated lncRNAs: senescence-associated long noncoding RNAs. Aging Cell 12, 890-900 (2013).
34. Augoff, K., McCue, B., Plow, E. F. & Sossey-Alaoui, K. miR-31 and its host gene lncRNA LOC554202 are regulated by promoter hypermethylation in triplenegative breast cancer. Mol. Cancer 11, 5 (2012).
35. Christoffersen, N. R. et al. p53-independent upregulation of miR-34a during oncogene-induced senescence represses MYC. Cell Death Differ. 17, 236-245 (2010).
36. Coppe, J. P. et al. Senescence-associated secretory phenotypes reveal cellnonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 6, 2853-2868 (2008).
37. Coppe, J. P. et al. Tumor suppressor and aging biomarker p16(INK4a) induces cellular senescence without the associated inflammatory secretory phenotype. J. Biol. Chem. 286, 36396-36403 (2011).
38. Beausejour, C. M. et al. Reversal of human cellular senescence: roles of the p53 and p16 pathways. EMBO J. 22, 4212-4222 (2003).
39. Tuck, A. C. & Tollervey, D. A transcriptome-wide atlas of RNP composition reveals diverse classes of mRNAs and lncRNAs. Cell 154, 996-1009 (2013).
40. McCloskey, A., Taniguchi, I., Shinmyozu, K. & Ohno, M. hnRNP C tetramer measures RNA length to classify RNA polymerase II transcripts for export. Science 335, 1643-1646 (2012).
41. Dias, A. P., Dufu, K., Lei, H. & Reed, R. A role for TREX components in the release of spliced mRNA from nuclear speckle domains. Nat. Commun. 1, 97 (2010).
42. Yap, K. L. et al. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 38, 662-674 (2010).
43. Khalil, A. M. et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl Acad. Sci. USA 106, 11667-11672 (2009).
44. Davidovich, C., Zheng, L., Goodrich, K. J. & Cech, T. R. Promiscuous RNA binding by Polycomb repressive complex 2. Nat. Struct. Mol. Biol. 20, 1250-1257 (2013).
45. Chu, C., Quinn, J. & Chang, H. Y. Chromatin isolation by RNA purification (ChIRP). J Vis Exp 61, e3912 (2012).
46. Chu, C., Qu, K., Zhong, F. L., Artandi, S. E. & Chang, H. Y. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol. Cell 44, 667-678 (2011).
47. van de Werken, H. J. et al. Robust 4C-seq data analysis to screen for regulatory DNA interactions. Nat. Methods 9, 969-972 (2012).
48. Rosenbloom, K. R. et al. ENCODE whole-genome data in the UCSC Genome Browser: update 2012. Nucleic Acids Res. 40, D912-D917 (2012).
49. Kim, T. K. et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 465, 182-187 (2010).
50. Shi, Y. et al. Long non-coding RNA Loc554202 regulates proliferation and migration in breast cancer cells. Biochem. Biophys. Res. Commun. 446, 448-453 (2014).
51. Xi, S. et al. Cigarette smoke induces C/EBP-beta-mediated activation of miR-31 in normal human respiratory epithelia and lung cancer cells. PLoS One 5, e13764 (2010).
52. Hung, M. L., Hautbergue, G. M., Snijders, A. P., Dickman, M. J. & Wilson, S. A. Arginine methylation of REF/ALY promotes efficient handover of mRNA to TAP/NXF1. Nucleic Acids Res. 38, 3351-3361 (2010).
53. Kuilman, T. et al. Oncogene-induced senescence relayed by an interleukindependent inflammatory network. Cell 133, 1019-1031 (2008).
54. Negishi, M. et al. A New lncRNA, APTR, Associates with and Represses the CDKN1A/p21 Promoter by Recruiting Polycomb Proteins. PLoS One 9, e95216 (2014).
55. Holdt, L. M. et al. Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLoS Genet. 9, e1003588 (2013).
56. Zhang, H. et al. Long noncoding RNA-mediated intrachromosomal interactions promote imprinting at the Kcnq1 locus. J. Cell Biol. 204, 61-75 (2014).
57. Xiang, J. F. et al. Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res. 24, 513-531 (2014).
58. Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380 (2012).
59. Whyte, W. A. et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153, 307-319 (2013).
60. Li, W. et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498, 516-520 (2013).
61. Liu, Z. et al. Enhancer activation requires trans-recruitment of a mega transcription factor complex. Cell 159, 358-373 (2014).
62. Mousavi, K. et al. eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol. Cell 51, 606-617 (2013).
63. Lai, F. et al. Activating RNAs associate with Mediator to enhance chromatin architecture and transcription. Nature 494, 497-501 (2013).
64. van de Werken, H. J. et al. 4C technology: protocols and data analysis. Methods Enzymol. 513, 89-112 (2012).
65. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
66. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
67. Anders, S. et al. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nat. Protoc. 8, 1765-1786 (2013).
68. Harrow, J. et al. GENCODE: producing a reference annotation for ENCODE. Genome Biol. 7 (Suppl 1), S4.1-9 (2006).
69. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
70. de Wit, E., Braunschweig, U., Greil, F., Bussemaker, H. J. & van Steensel, B. Global chromatin domain organization of the Drosophila genome. PLoS Genet. 4, e1000045 (2008).