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01-10-2014 | Review

The lncRNA-MYC regulatory network in cancer

Authors: Kaiyuan Deng, Xiaoqiang Guo, Hao Wang, Jiazeng Xia

Published in: Tumor Biology | Issue 10/2014

Abstract

Long non-coding RNAs (lncRNAs) have been widely studied in recent years, and accumulating evidence identified lncRNAs as crucial regulators of various biological processes, including cell cycle progression, chromatin remodeling, gene transcription, and posttranscriptional processing. In addition, the fact that lncRNAs interact with the MYC gene family in human carcinomas has been discovered. This review summarizes the latest progress on the investigation of lncRNAs and MYC, particularly focusing on the interplay between lncRNAs and MYC in cancer to reveal the significance of lncRNA-MYC network in regulating initiation, development, and metastasis of tumors. Further research and collection of clinical data would provide a better understanding of lncRNA-MYC network in cancer diagnosis and treatment.

Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, et al. Initial sequencing and analysis of the human genome. Nature. 2001;409(6822):860–921. doi:10.1038/35057062.CrossRefPubMed

Consortium EP, Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, et al. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489(7414):57–74. doi:10.1038/nature11247.CrossRef

Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, et al. The transcriptional landscape of the mammalian genome. Science. 2005;309(5740):1559–63. doi:10.1126/science.1112014.CrossRefPubMed

Liu C, Bai B, Skogerbo G, Cai L, Deng W, Zhang Y, et al. NONCODE: an integrated knowledge database of non-coding RNAs. Nucleic Acids Res. 2005;33(Database issue):D112–5. doi:10.1093/nar/gki041.PubMedCentralCrossRefPubMed

Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, et al. Characterization of the piRNA complex from rat testes. Science. 2006;313(5785):363–7. doi:10.1126/science.1130164.CrossRefPubMed

Farazi TA, Hoell JI, Morozov P, Tuschl T. MicroRNAs in human cancer. Adv Exp Med Biol. 2013;774:1–20. doi:10.1007/978-94-007-5590-1_1.PubMedCentralCrossRefPubMed

Fabbri M, Calin GA. Epigenetics and miRNAs in human cancer. Adv Genet. 2010;70:87–99. doi:10.1016/B978-0-12-380866-0.60004-6.CrossRefPubMed

Iorio MV, Croce CM. MicroRNAs in cancer: small molecules with a huge impact. J Clin Oncol. 2009;27(34):5848–56. doi:10.1200/JCO.2009.24.0317.PubMedCentralCrossRefPubMed

Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009;136(4):629–41. doi:10.1016/j.cell.2009.02.006.CrossRefPubMed

10.

Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet. 2009;10(3):155–9. doi:10.1038/nrg2521.CrossRefPubMed

11.

Pauli A, Rinn JL, Schier AF. Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet. 2011;12(2):136–49. doi:10.1038/nrg2904.PubMedCentralCrossRefPubMed

12.

Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, et al. LincRNAs act in the circuitry controlling pluripotency and differentiation. Nature. 2011;477(7364):295–300. doi:10.1038/nature10398.PubMedCentralCrossRefPubMed

13.

Wapinski O, Chang HY. Long noncoding RNAs and human disease. Trends Cell Biol. 2011;21(6):354–61. doi:10.1016/j.tcb.2011.04.001.CrossRefPubMed

14.

Huarte M, Rinn JL. Large non-coding RNAs: missing links in cancer? Hum Mol Genet. 2010;19(R2):R152–61. doi:10.1093/hmg/ddq353.PubMedCentralCrossRefPubMed

15.

Gibb EA, Brown CJ, Lam WL. The functional role of long non-coding RNA in human carcinomas. Mol Cancer. 2011;10:38. doi:10.1186/1476-4598-10-38.PubMedCentralCrossRefPubMed

16.

Kung JT, Colognori D, Lee JT. Long noncoding RNAs: past, present, and future. Genetics. 2013;193(3):651–69. doi:10.1534/genetics.112.146704.PubMedCentralCrossRefPubMed

17.

Xie C, Yuan J, Li H, Li M, Zhao G, Bu D, et al. NONCODEv4: exploring the world of long non-coding RNA genes. Nucleic Acids Res. 2014;42(Database issue):D98–103. doi:10.1093/nar/gkt1222.PubMedCentralCrossRefPubMed

18.

Ma L, Bajic VB, Zhang Z. On the classification of long non-coding RNAs. RNA Biol. 2013;10(6):925–33. doi:10.4161/rna.24604.CrossRefPubMed

19.

Novikova IV, Hennelly SP, Sanbonmatsu KY. Sizing up long non-coding RNAs: do lncRNAs have secondary and tertiary structure? Bioarchitecture. 2012;2(6):189–99. doi:10.4161/bioa.22592.PubMedCentralCrossRefPubMed

20.

Jeon Y, Sarma K, Lee JT. New and Xisting regulatory mechanisms of X chromosome inactivation. Curr Opin Genet Dev. 2012;22(2):62–71. doi:10.1016/j.gde.2012.02.007.PubMedCentralCrossRefPubMed

21.

Mattick JS, Amaral PP, Dinger ME, Mercer TR, Mehler MF. RNA regulation of epigenetic processes. BioEssays : News Rev Mol Cell Dev Biol. 2009;31(1):51–9. doi:10.1002/bies.080099.CrossRef

22.

Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, et al. Long noncoding RNAs with enhancer-like function in human cells. Cell. 2010;143(1):46–58. doi:10.1016/j.cell.2010.09.001.PubMedCentralCrossRefPubMed

23.

Clark MB, Mattick JS. Long noncoding RNAs in cell biology. Semin Cell Dev Biol. 2011;22(4):366–76. doi:10.1016/j.semcdb.2011.01.001.CrossRefPubMed

24.

Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell. 2011;43(6):904–14. doi:10.1016/j.molcel.2011.08.018.PubMedCentralCrossRefPubMed

25.

Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, et al. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell. 2011;147(2):358–69. doi:10.1016/j.cell.2011.09.028.PubMedCentralCrossRefPubMed

26.

Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, et al. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell. 2010;39(6):925–38. doi:10.1016/j.molcel.2010.08.011.PubMedCentralCrossRefPubMed

27.

Hung T, Chang HY. Long noncoding RNA in genome regulation: prospects and mechanisms. RNA Biol. 2010;7(5):582–5.PubMedCentralCrossRefPubMed

28.

Lee JT. Lessons from X-chromosome inactivation: long ncRNA as guides and tethers to the epigenome. Genes Dev. 2009;23(16):1831–42. doi:10.1101/gad.1811209.PubMedCentralCrossRefPubMed

29.

Spitale RC, Tsai MC, Chang HY. RNA templating the epigenome: long noncoding RNAs as molecular scaffolds. Epigenetics. 2011;6(5):539–43.PubMedCentralCrossRefPubMed

30.

Lu L, Zhu G, Zhang C, Deng Q, Katsaros D, Mayne ST, et al. Association of large noncoding RNA HOTAIR expression and its downstream intergenic CpG island methylation with survival in breast cancer. Breast Cancer Res Treat. 2012;136(3):875–83. doi:10.1007/s10549-012-2314-z.CrossRefPubMed

31.

Niinuma T, Suzuki H, Nojima M, Nosho K, Yamamoto H, Takamaru H, et al. Upregulation of miR-196a and HOTAIR drive malignant character in gastrointestinal stromal tumors. Cancer Res. 2012;72(5):1126–36. doi:10.1158/0008-5472.CAN-11-1803.CrossRefPubMed

32.

Ishibashi M, Kogo R, Shibata K, Sawada G, Takahashi Y, Kurashige J, et al. Clinical significance of the expression of long non-coding RNA HOTAIR in primary hepatocellular carcinoma. Oncol Rep. 2013;29(3):946–50. doi:10.3892/or.2012.2219.PubMed

33.

Kogo R, Shimamura T, Mimori K, Kawahara K, Imoto S, Sudo T, et al. Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res. 2011;71(20):6320–6. doi:10.1158/0008-5472.CAN-11-1021.CrossRefPubMed

34.

Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature. 2010;464(7291):1071–6. doi:10.1038/nature08975.PubMedCentralCrossRefPubMed

35.

Ji P, Diederichs S, Wang W, Boing S, Metzger R, Schneider PM, et al. MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene. 2003;22(39):8031–41. doi:10.1038/sj.onc.1206928.CrossRefPubMed

36.

Schmidt LH, Spieker T, Koschmieder S, Schaffers S, Humberg J, Jungen D, et al. The long noncoding MALAT-1 RNA indicates a poor prognosis in non-small cell lung cancer and induces migration and tumor growth. J Thoracic Oncol : Off Publ Int Assoc Study Lung Cancer. 2011;6(12):1984–92. doi:10.1097/JTO.0b013e3182307eac.CrossRef

37.

Lin R, Maeda S, Liu C, Karin M, Edgington TS. A large noncoding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomas. Oncogene. 2007;26(6):851–8. doi:10.1038/sj.onc.1209846.CrossRefPubMed

38.

Li L, Feng T, Lian Y, Zhang G, Garen A, Song X. Role of human noncoding RNAs in the control of tumorigenesis. Proc Natl Acad Sci U S A. 2009;106(31):12956–61. doi:10.1073/pnas.0906005106.PubMedCentralCrossRefPubMed

39.

Zhang X, Zhou Y, Mehta KR, Danila DC, Scolavino S, Johnson SR, et al. A pituitary-derived MEG3 isoform functions as a growth suppressor in tumor cells. J Clin Endocrinol Metab. 2003;88(11):5119–26. doi:10.1210/jc.2003-030222.CrossRefPubMed

40.

Zhou Y, Zhong Y, Wang Y, Zhang X, Batista DL, Gejman R, et al. Activation of p53 by MEG3 non-coding RNA. J Biol Chem. 2007;282(34):24731–42. doi:10.1074/jbc.M702029200.CrossRefPubMed

41.

Wu H, Zheng J, Deng J, Hu M, You Y, Li N, et al. A genetic polymorphism in lincRNA-uc003opf.1 is associated with susceptibility to esophageal squamous cell carcinoma in Chinese populations. Carcinogenesis. 2013;34(12):2908–17.CrossRefPubMed

42.

Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458(7235):223–7. doi:10.1038/nature07672.PubMedCentralCrossRefPubMed

43.

Wheeler TM, Leger AJ, Pandey SK, MacLeod AR, Nakamori M, Cheng SH, et al. Targeting nuclear RNA for in vivo correction of myotonic dystrophy. Nature. 2012;488(7409):111–5. doi:10.1038/nature11362.PubMedCentralCrossRefPubMed

44.

Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A. 2009;106(28):11667–72. doi:10.1073/pnas.0904715106.PubMedCentralCrossRefPubMed

45.

Du Y, Kong G, You X, Zhang S, Zhang T, Gao Y, et al. Elevation of highly up-regulated in liver cancer (HULC) by hepatitis B virus X protein promotes hepatoma cell proliferation via down-regulating p18. J Biol Chem. 2012;287(31):26302–11. doi:10.1074/jbc.M112.342113.PubMedCentralCrossRefPubMed

46.

Gutschner T, Hammerle M, Eissmann M, Hsu J, Kim Y, Hung G, et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res. 2013;73(3):1180–9. doi:10.1158/0008-5472.CAN-12-2850.PubMedCentralCrossRefPubMed

47.

Li CH, Chen Y. Targeting long non-coding RNAs in cancers: progress and prospects. Int J Biochem Cell Biol. 2013;45(8):1895–910. doi:10.1016/j.biocel.2013.05.030.CrossRefPubMed

48.

Ling H, Fabbri M, Calin GA. MicroRNAs and other non-coding RNAs as targets for anticancer drug development. Nat Rev Drug Discov. 2013;12(11):847–65. doi:10.1038/nrd4140.CrossRefPubMed

49.

Taub R, Kirsch I, Morton C, Lenoir G, Swan D, Tronick S, et al. Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proc Natl Acad Sci U S A. 1982;79(24):7837–41.PubMedCentralCrossRefPubMed

50.

Shou Y, Martelli ML, Gabrea A, Qi Y, Brents LA, Roschke A, et al. Diverse karyotypic abnormalities of the c-myc locus associated with c-myc dysregulation and tumor progression in multiple myeloma. Proc Natl Acad Sci U S A. 2000;97(1):228–33.PubMedCentralCrossRefPubMed

51.

Nesbit CE, Tersak JM, Prochownik EV. MYC oncogenes and human neoplastic disease. Oncogene. 1999;18(19):3004–16. doi:10.1038/sj.onc.1202746.CrossRefPubMed

52.

Schwab M. MYCN in neuronal tumours. Cancer Lett. 2004;204(2):179–87. doi:10.1016/S0304-3835(03)00454-3.CrossRefPubMed

53.

Wu R, Lin L, Beer DG, Ellenson LH, Lamb BJ, Rouillard JM, et al. Amplification and overexpression of the L-MYC proto-oncogene in ovarian carcinomas. Am J Pathol. 2003;162(5):1603–10. doi:10.1016/S0002-9440(10)64294-0.PubMedCentralCrossRefPubMed

54.

Luscher B. Function and regulation of the transcription factors of the Myc/Max/Mad network. Gene. 2001;277(1–2):1–14.CrossRefPubMed

55.

Blackwood EM, Eisenman RN. Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc. Science. 1991;251(4998):1211–7.CrossRefPubMed

56.

Blackwood EM, Kretzner L, Eisenman RN. Myc and Max function as a nucleoprotein complex. Current Opin Genet Dev. 1992;2(2):227–35.CrossRef

57.

Torres R, Schreiber-Agus N, Morgenbesser SD, DePinho RA. Myc and Max: a putative transcriptional complex in search of a cellular target. Curr Opin Cell Biol. 1992;4(3):468–74.CrossRefPubMed

58.

Park J, Kunjibettu S, McMahon SB, Cole MD. The ATM-related domain of TRRAP is required for histone acetyltransferase recruitment and Myc-dependent oncogenesis. Genes Dev. 2001;15(13):1619–24. doi:10.1101/gad.900101.PubMedCentralCrossRefPubMed

59.

McMahon SB, Van Buskirk HA, Dugan KA, Copeland TD, Cole MD. The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell. 1998;94(3):363–74.CrossRefPubMed

60.

Nilsson JA, Cleveland JL. Myc pathways provoking cell suicide and cancer. Oncogene. 2003;22(56):9007–21. doi:10.1038/sj.onc.1207261.CrossRefPubMed

61.

Mai S, Mushinski JF. c-Myc-induced genomic instability. J Environ Pathol Toxicol Oncol. 2003;22(3):179–99.CrossRefPubMed

62.

Secombe J, Pierce SB, Eisenman RN. Myc: a weapon of mass destruction. Cell. 2004;117(2):153–6.CrossRefPubMed

63.

Ponzielli R, Katz S, Barsyte-Lovejoy D, Penn LZ. Cancer therapeutics: targeting the dark side of Myc. Eur J Cancer. 2005;41(16):2485–501. doi:10.1016/j.ejca.2005.08.017.CrossRefPubMed

64.

Dominguez-Sola D, Ying CY, Grandori C, Ruggiero L, Chen B, Li M, et al. Non-transcriptional control of DNA replication by c-Myc. Nature. 2007;448(7152):445–51. doi:10.1038/nature05953.CrossRefPubMed

65.

Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, West KM, et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet. 2008;40(1):43–50. doi:10.1038/ng.2007.30.PubMedCentralCrossRefPubMed

66.

O’Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 2005;435(7043):839–43. doi:10.1038/nature03677.CrossRefPubMed

67.

Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet. 2001;2(1):21–32. doi:10.1038/35047554.CrossRefPubMed

68.

Hao Y, Crenshaw T, Moulton T, Newcomb E, Tycko B. Tumour-suppressor activity of H19 RNA. Nature. 1993;365(6448):764–7. doi:10.1038/365764a0.CrossRefPubMed

69.

Matouk IJ, DeGroot N, Mezan S, Ayesh S, Abu-lail R, Hochberg A, et al. The H19 non-coding RNA is essential for human tumor growth. PLoS One. 2007;2(9):e845. doi:10.1371/journal.pone.0000845.PubMedCentralCrossRefPubMed

70.

Ariel I, Lustig O, Schneider T, Pizov G, Sappir M, De-Groot N, et al. The imprinted H19 gene as a tumor marker in bladder carcinoma. Urology. 1995;45(2):335–8.CrossRefPubMed

71.

Barsyte-Lovejoy D, Lau SK, Boutros PC, Khosravi F, Jurisica I, Andrulis IL, et al. The c-Myc oncogene directly induces the H19 noncoding RNA by allele-specific binding to potentiate tumorigenesis. Cancer Res. 2006;66(10):5330–7. doi:10.1158/0008-5472.CAN-06-0037.CrossRefPubMed

72.

Nissan A, Stojadinovic A, Mitrani-Rosenbaum S, Halle D, Grinbaum R, Roistacher M, et al. Colon cancer associated transcript-1: a novel RNA expressed in malignant and pre-malignant human tissues. Int J Cancer J Int du Cancer. 2012;130(7):1598–606. doi:10.1002/ijc.26170.CrossRef

73.

Yang F, Xue X, Bi J, Zheng L, Zhi K, Gu Y, et al. Long noncoding RNA CCAT1, which could be activated by c-Myc, promotes the progression of gastric carcinoma. J Cancer Res Clin Oncol. 2013;139(3):437–45. doi:10.1007/s00432-012-1324-x.CrossRefPubMed

74.

Xiang JF, Yin QF, Chen T, Zhang Y, Zhang XO, Wu Z, et al. Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res. 2014. doi:10.1038/cr.2014.35.

75.

Ling H, Spizzo R, Atlasi Y, Nicoloso M, Shimizu M, Redis RS, et al. CCAT2, a novel noncoding RNA mapping to 8q24, underlies metastatic progression and chromosomal instability in colon cancer. Genome Res. 2013;23(9):1446–61. doi:10.1101/gr.152942.112.PubMedCentralCrossRefPubMed

76.

Yang F, Xue X, Zheng L, Bi J, Zhou Y, Zhi K, et al. Long non-coding RNA GHET1 promotes gastric carcinoma cell proliferation by increasing c-Myc mRNA stability. FEBS J. 2014;281(3):802–13. doi:10.1111/febs.12625.CrossRefPubMed

77.

Liao LM, Sun XY, Liu AW, Wu JB, Cheng XL, Lin JX, et al. Low expression of long noncoding XLOC_010588 indicates a poor prognosis and promotes proliferation through upregulation of c-Myc in cervical cancer. Gynecol Oncol. 2014. doi:10.1016/j.ygyno.2014.03.555.

78.

Buechner J, Einvik C. N-myc and noncoding RNAs in neuroblastoma. Mol Cancer Res. 2012;10(10):1243–53. doi:10.1158/1541-7786.MCR-12-0244.CrossRefPubMed

79.

Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, Mattick JS, et al. Ultraconserved elements in the human genome. Science. 2004;304(5675):1321–5. doi:10.1126/science.1098119.CrossRefPubMed

80.

Mestdagh P, Fredlund E, Pattyn F, Rihani A, Van Maerken T, Vermeulen J, et al. An integrative genomics screen uncovers ncRNA T-UCR functions in neuroblastoma tumours. Oncogene. 2010;29(24):3583–92. doi:10.1038/onc.2010.106.CrossRefPubMed

81.

Atmadibrata B, Liu PY, Sokolowski N, Zhang L, Wong M, Tee AE, et al. The novel long noncoding RNA linc00467 promotes cell survival but is down-regulated by N-Myc. PLoS ONE. 2014;9(2):e88112. doi:10.1371/journal.pone.0088112.PubMedCentralCrossRefPubMed

82.

Tee AE, Ling D, Nelson C, Atmadibrata B, Dinger ME, Xu N et al. The histone demethylase JMJD1A induces cell migration and invasion by up-regulating the expression of the long noncoding RNA MALAT1. Oncotarget. 2014;5(7):1793–804.

Title: The lncRNA-MYC regulatory network in cancer
Authors: Kaiyuan Deng
Xiaoqiang Guo
Hao Wang
Jiazeng Xia
Publication date: 01-10-2014
Publisher: Springer Netherlands
Published in: Tumor Biology / Issue 10/2014
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI: https://doi.org/10.1007/s13277-014-2511-y

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