Long non-coding RNAs in cancer and development: Where do we go from here?

International Journal of Molecular Sciences

Volumn 16, Issue 1, 2015, Pages 1395-1405

  Haemmerle, Monika ^a,b   Gutschner, Tony ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Functional genomics; Genetically engineered mouse models (GEMM); HOX transcript antisense RNA (HOTAIR); Long intergenic RNA (lincRNA); Metastasis; Metastasis associated lung adenocarcinoma transcript 1 (MALAT1)

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; HOX PROTEIN; LONG UNTRANSLATED RNA; POLYADENYLIC ACID; TUMOR MARKER;

APOPTOSIS; CELL CYCLE PROGRESSION; CELL MIGRATION; CELL PROLIFERATION; FRAMESHIFT MUTATION; GENE DELETION; GENE EXPRESSION; GENE REPLACEMENT THERAPY; GENE SEQUENCE; GENE SILENCING; GENETIC ANALYSIS; HUMAN; LOSS OF FUNCTION MUTATION; LUNG ADENOCARCINOMA; NEOPLASM; NONHUMAN; PROTEIN EXPRESSION; REVIEW; RNA TRANSCRIPTION; SPECIES COMPARISON; TUMOR GENE; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DEGENERATIVE DISEASE; GENETICS; METABOLISM; PATHOLOGY;

ANIMALIA;

ANIMALS; BIOMARKERS, TUMOR; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; HUMANS; NEOPLASMS; NEURODEGENERATIVE DISEASES; OLIGONUCLEOTIDES, ANTISENSE; RNA, LONG NONCODING;

EID: 84920911903     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms16011395     Document Type: Review

References (64)

1. Mattick, J.S. Introns: Evolution and function. Curr. Opin. Genet. Dev. 1994, 4, 823–831.
2. Liu, G.; Mattick, J.S.; Taft, R.J. A meta-analysis of the genomic and transcriptomic composition of complex life. Cell Cycle 2013, 12, 2061–2072.
3. Lynch, M.; Walsh, B. The Origins of Genome Architecture; Sinauer Associates, Inc.: Sunderland, MA, USA, 2007.
4. Carninci, P.; Kasukawa, T.; Katayama, S.; Gough, J.; Frith, M.C.; Maeda, N.; Oyama, R.; Ravasi, T.; Lenhard, B.; Wells, C.; et al. The transcriptional landscape of the mammalian genome. Science 2005, 309, 1559–1563.
5. Cheng, J.; Kapranov, P.; Drenkow, J.; Dike, S.; Brubaker, S.; Patel, S.; Long, J.; Stern, D.; Tammana, H.; Helt, G.; et al. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 2005, 308, 1149–1154.
6. Consorium, E.P, Birney, E, Stamatoyannopoulos, J.A, Dutta, A, Guigo, R, Gingeras, T.R, Margulies, E.H, Weng, Z, Snyder, M, Dermitzakis, E.T, et al. Identification and analysis of functional elements in 1% of the human genome by the encode pilot project. Nature 2007, 447, 799–816.
7. Cabili, M.N.; Trapnell, C.; Goff, L.; Koziol, M.; Tazon-Vega, B.; Regev, A.; Rinn, J.L. Integrative annotation of human large intergenic non-coding RNAs reveals global properties and specific subclasses. Genes Dev. 2011, 25, 1915–1927.
8. Derrien, T.; Johnson, R.; Bussotti, G.; Tanzer, A.; Djebali, S.; Tilgner, H.; Guernec, G.; Martin, D, Merkel, A.; Knowles, D.G, et al. The GENCODE v7 catalog of human long non-coding RNAs: Analysis of their gene structure, evolution, and expression. Genome Res. 2012, 22, 1775–1789.
9. Dinger, M.E.; Amaral, P.P.; Mercer, T.R.; Pang, K.C.; Bruce, S.J.; Gardiner, B.B.; Askarian-Amiri, M.E.; Ru, K.; Solda, G.; Simons, C, et al. Long non-coding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 2008, 18, 1433–1445.
10. Gutschner, T.; Diederichs, S. The hallmarks of cancer: A long non-coding RNA point of view. RNA Biol. 2012, 9, 703–719.
11. Faghihi, M.A.; Modarresi, F.; Khalil, A.M.; Wood, D.E.; Sahagan, B.G.; Morgan, T.E.; Finch, C.E.; St-Laurent, G., III; Kenny, P.J.; Wahlestedt, C. Expression of a non-coding RNA is elevated in Alzheimer’s Disease and drives rapid feed-forward regulation of β-secretase. Nat. Med. 2008, 14, 723–730.
12. Pastori, C.; Wahlestedt, C. Involvement of long non-coding RNAs in diseases affecting the central nervous system. RNA Biol. 2012, 9, 860–870.
13. Cheetham, S.W.; Gruhl, F.; Mattick, J.S.; Dinger, M.E. Long non-coding RNAs and the genetics of cancer. Br. J. Cancer 2013, 108, 2419–2425.
14. Freedman, M.L.; Monteiro, A.N.; Gayther, S.A.; Coetzee, G.A.; Risch, A.; Plass, C.; Casey, G.; de Biasi, M.; Carlson, C.; Duggan, D, et al. Principles for the post-GWAS functional characterization of cancer risk loci. Nat. Genet. 2011, 43, 513–518.
15. Eissmann, M.; Gutschner, T.; Hammerle, M.; Gunther, S.; Caudron-Herger, M.; Gross, M.; Schirmacher, P.; Rippe, K.; Braun, T.; Zornig, M, et al. Loss of the abundant nuclear non-coding RNA Malat1 is compatible with life and development. RNA Biol. 2012, 9, 1076–1087.
16. Sauvageau, M.; Goff, L.A.; Lodato, S.; Bonev, B.; Groff, A.F.; Gerhardinger, C.; Sanchez-Gomez, D.B.; Hacisuleyman, E.; Li, E.; Spence, M, et al. Multiple knockout mouse models reveal lincRNAs are required for life and brain development. eLIFE 2013, 2, e01749.
17. Hung, T.; Wang, Y.; Lin, M.F.; Koegel, A.K.; Kotake, Y.; Grant, G.D.; Horlings, H.M.; Shah, N.; Umbricht, C.; Wang, P, et al. Extensive and coordinated transcription of non-coding RNAs within cell-cycle promoters. Nat. Genet. 2011, 43, 621–629.
18. Ponjavic, J.; Oliver, P.L.; Lunter, G.; Ponting, C.P. Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain. PLoS Genet. 2009, 5, e1000617.
19. Sigova, A.A.; Mullen, A.C.; Molinie, B.; Gupta, S.; Orlando, D.A.; Guenther, M.G.; Almada, A.E.; Lin, C.; Sharp, P.A.; Giallourakis, C.C, et al. Divergent transcription of long non-coding RNA/mRNA gene pairs in embryonic stem cells. Proc. Natl. Acad. Sci. USA 2013, 110, 2876–2881.
20. Nakagawa, S.; Naganuma, T.; Shioi, G.; Hirose, T. Paraspeckles are subpopulation-specific nuclear bodies that are not essential in mice. J. Cell Biol. 2011, 193, 31–39.
21. Zhang, B.; Arun, G.; Mao, Y.S.; Lazar, Z.; Hung, G.; Bhattacharjee, G.; Xiao, X.; Booth, C.J.; Wu, J.; Zhang, C, et al. The lncRNA Malat1 is dispensable for mouse development but its transcription plays a cis-regulatory role in the adult. Cell Rep. 2012, 2, 111–123.
22. Gutschner, T.; Baas, M.; Diederichs, S. Non-coding RNA gene silencing through genomic integration of RNA destabilizing elements using zinc finger nucleases. Genome Res. 2011, 21, 1944–1954.
23. Gutschner, T. Silencing long noncoding RNAs with genome-editing tools. Methods Mol. Biol. 2015, 1239, 241–250.
24. Bond, A.M.; Vangompel, M.J.; Sametsky, E.A.; Clark, M.F.; Savage, J.C.; Disterhoft, J.F.; Kohtz, J.D. Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal gaba circuitry. Nat. Neurosci. 2009, 12, 1020–1027.
25. Nakagawa, S.; Ip, J.Y.; Shioi, G.; Tripathi, V.; Zong, X.; Hirose, T.; Prasanth, K.V. Malat1 is not an essential component of nuclear speckles in mice. RNA 2012, 18, 1487–1499.
26. Sleutels, F.; Zwart, R.; Barlow, D.P. The non-coding air RNA is required for silencing autosomal imprinted genes. Nature 2002, 415, 810–813.
27. Brown, J.A.; Bulkley, D.; Wang, J.; Valenstein, M.L.; Yario, T.A.; Steitz, T.A.; Steitz, J.A. Structural insights into the stabilization of malat1 noncoding RNA by a bipartite triple helix. Nat. Struct. Mol. Biol. 2014, 21, 633–640.
28. Peart, N.; Sataluri, A.; Baillat, D.; Wagner, E.J. Non-mRNA 3' end formation: How the other half lives. Wiley Interdiscip. Rev. RNA 2013, 4, 491–506.
29. Wilusz, J.E.; Freier, S.M.; Spector, D.L. 3' End processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell 2008, 135, 919–932.
30. Wilusz, J.E.; JnBaptiste, C.K.; Lu, L.Y.; Kuhn, C.D.; Joshua-Tor, L.; Sharp, P.A. A triple helix stabilizes the 3' ends of long noncoding RNAs that lack poly (A) tails. Genes Dev. 2012, 26, 2392–2407.
31. Bassett, A.R.; Akhtar, A.; Barlow, D.P.; Bird, A.P.; Brockdorff, N.; Duboule, D.; Ephrussi, A.; Ferguson-Smith, A.C.; Gingeras, T.R.; Haerty, W, et al. Considerations when investigating lncRNA function in vivo. eLife 2014, 3, e03058.
32. Gutschner, T.; Hammerle, M.; Diederichs, S. MALAT1—A paradigm for long noncoding RNA function in cancer. J. Mol. Med. 2013, 91, 791–801.
33. Gutschner, T.; Hammerle, M.; Eissmann, M.; Hsu, J.; Kim, Y.; Hung, G.; Revenko, A.; Arun, G.; Stentrup, M.; Gross, M, et al. The non-coding RNA malat1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res. 2013, 73, 1180–1189.
34. Engreitz, J.M.; Sirokman, K.; McDonel, P.; Shishkin, A.A.; Surka, C.; Russell, P.; Grossman, S.R.; Chow, A.Y.; Guttman, M.; Lander, E.S. RNA–RNA interactions enable specific targeting of non-coding RNAs to nascent pre-mRNAs and chromatin sites. Cell 2014, 159, 188–199.
35. Tripathi, V.; Ellis, J.D.; Shen, Z.; Song, D.Y.; Pan, Q.; Watt, A.T.; Freier, S.M.; Bennett, C.F.; Sharma, A.; Bubulya, P.A, et al. The nuclear-retained non-coding RNA Malat1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol. Cell 2010, 39, 925–938.
36. West, J.A.; Davis, C.P.; Sunwoo, H.; Simon, M.D.; Sadreyev, R.I.; Wang, P.I.; Tolstorukov, M.Y.; Kingston, R.E. The long noncoding RNAs Neat1 and Malat1 bind active chromatin sites. Mol. Cell 2014, 55, 791–802.
37. Yang, L.; Lin, C.; Liu, W.; Zhang, J.; Ohgi, K.A.; Grinstein, J.D.; Dorrestein, P.C.; Rosenfeld, M.G. ncRNAand Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 2011, 147, 773–788.
38. Michalik, K.M.; You, X.; Manavski, Y.; Doddaballapur, A.; Zornig, M.; Braun, T.; John, D.; Ponomareva, Y.; Chen, W.; Uchida, S, et al. Long non-coding RNA Malat1 regulates endothelial cell function and vessel growth. Circ. Res. 2014, 114, 1389–1397.
39. Ahituv, N.; Zhu, Y.; Visel, A.; Holt, A.; Afzal, V.; Pennacchio, L.A.; Rubin, E.M. Deletion of ultraconserved elements yields viable mice. PLoS Biol. 2007, 5, e234.
40. Mercer, T.R.; Dinger, M.E.; Sunkin, S.M.; Mehler, M.F.; Mattick, J.S. Specific expression of long non-coding RNAs in the mouse brain. Proc. Natl. Acad. Sci. USA 2008, 105, 716–721.
41. Ji, P.; Diederichs, S.; Wang, W.; Boing, S.; Metzger, R.; Schneider, P.M.; Tidow, N.; Brandt, B.; Buerger, H.; Bulk, E, et al. Malat-1, a novel noncoding RNA, and thymosin β4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 2003, 22, 8031–8041.
42. Paez-Ribes, M.; Allen, E.; Hudock, J.; Takeda, T.; Okuyama, H.; Vinals, F.; Inoue, M.; Bergers, G.; Hanahan, D.; Casanovas, O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009, 15, 220–231.
43. Kim, I.S.; Baek, S.H. Mouse models for breast cancer metastasis. Biochem. Biophys. Res. Commun. 2010, 394, 443–447.
44. Kwon, M.C.; Berns, A. Mouse models for lung cancer. Mol. Oncol. 2013, 7, 165–177.
45. Heyer, J.; Kwong, L.N.; Lowe, S.W.; Chin, L. Non-germline genetically engineered mouse models for translational cancer research. Nat. Rev. Cancer 2010, 10, 470–480.
46. Gupta, R.A.; Shah, N.; Wang, K.C.; Kim, J.; Horlings, H.M.; Wong, D.J.; Tsai, M.C.; Hung, T.; Argani, P.; Rinn, J.L, et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 2010, 464, 1071–1076.
47. Li, L.; Liu, B.; Wapinski, O.L.; Tsai, M.C.; Qu, K.; Zhang, J.; Carlson, J.C.; Lin, M.; Fang, F.; Gupta, R.A, et al. Targeted disruption of HOTAIR leads to homeotic transformation and gene derepression. Cell Rep. 2013, 5, 3–12.
48. Guttman, M.; Amit, I.; Garber, M.; French, C.; Lin, M.F.; Feldser, D.; Huarte, M.; Zuk, O.; Carey, B.W.; Cassady, J.P, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458, 223–227.
49. Ponjavic, J.; Ponting, C.P.; Lunter, G. Functionality or transcriptional noise? Evidence for selection within long non-coding RNAs. Genome Res. 2007, 17, 556–565.
50. Ulitsky, I.; Shkumatava, A.; Jan, C.H.; Sive, H.; Bartel, D.P. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 2011, 147, 1537–1550.
51. Diederichs, S. The four dimensions of noncoding RNA conservation. Trends Genet. 2014, 30, 121–123.
52. Kim, M.; Gans, J.D.; Nogueira, C.; Wang, A.; Paik, J.H.; Feng, B.; Brennan, C.; Hahn, W.C.; Cordon-Cardo, C.; Wagner, S.N, et al. Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene. Cell 2006, 125, 1269–1281.
53. Zender, L.; Spector, M.S.; Xue, W.; Flemming, P.; Cordon-Cardo, C.; Silke, J.; Fan, S.T.; Luk, J.M.; Wigler, M.; Hannon, G.J, et al. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 2006, 125, 1253–1267.
54. Xing, Z.; Lin, A.; Li, C.; Liang, K.; Wang, S.; Liu, Y.; Park, P.K.; Qin, L.; Wei, Y.; Hawke, D.H, et al. lncRNA directs cooperative epigenetic regulation downstream of chemokine signals. Cell 2014, 159, 1110–1125.
55. Engreitz, J.M.; Pandya-Jones, A.; McDonel, P.; Shishkin, A.; Sirokman, K.; Surka, C.; Kadri, S.; Xing, J.; Goren, A.; Lander, E.S, et al. The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 2013, 341, 6147.
56. Buenrostro, J.D.; Araya, C.L.; Chircus, L.M.; Layton, C.J.; Chang, H.Y.; Snyder, M.P.; Greenleaf, W. J. Quantitative analysis of RNA-protein interactions on a massively parallel array reveals biophysical and evolutionary landscapes. Nat. Biotechnol. 2014, 32, 562–568.
57. Quinn, J.J.; Ilik, I.A.; Qu, K.; Georgiev, P.; Chu, C.; Akhtar, A.; Chang, H.Y. Revealing long non-coding RNA architecture and functions using domain-specific chromatin isolation by RNA purification. Nat. Biotechnol. 2014, 32, 933–940.
58. Ding, Y.; Tang, Y.; Kwok, C.K.; Zhang, Y.; Bevilacqua, P.C.; Assmann, S.M. In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature 2014, 505, 696–700.
59. Mortimer, S.A.; Kidwell, M.A.; Doudna, J.A. Insights into RNA structure and function from genome-wide studies. Nat. Rev. Genet. 2014, 15, 469–479.
60. Rouskin, S.; Zubradt, M.; Washietl, S.; Kellis, M.; Weissman, J.S. Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature 2014, 505, 701–705.
61. Wan, Y.; Qu, K.; Zhang, Q.C.; Flynn, R.A.; Manor, O.; Ouyang, Z.; Zhang, J.; Spitale, R.C.; Snyder, M.P.; Segal, E, et al. Landscape and variation of RNA secondary structure across the human transcriptome. Nature 2014, 505, 706–709.
62. Doudna, J.A.; Charpentier, E. Genome editing: The new frontier of genome engineering with CRISPR-Cas9. Science 2014, doi:10.1126/science.1258096.
63. Cheng, C.J.; Bahal, R.; Babar, I.A.; Pincus, Z.; Barrera, F.; Liu, C.; Svoronos, A.; Braddock, D.T.; Glazer, P.M.; Engelman, D.M, et al. MicroRNA silencing for cancer therapy targeted to the tumour microenvironment. Nature 2014, doi:10.1038/nature13905.
64. Meade, B.R.; Gogoi, K.; Hamil, A.S.; Palm-Apergi, C.; Berg, A.; Hagopian, J.C.; Springer, A.D.; Eguchi, A.; Kacsinta, A.D.; Dowdy, C.F, et al. Efficient delivery of RNAi prodrugs containing reversible charge-neutralizing phosphotriester backbone modifications. Nat. Biotechnol. 2014, 32, 1256–1261.