Long non-coding RNAs as key regulators of cancer metastasis

Pratirodh Koirala , De-Hong Zou , Yin-Yuan Mo

Journal of Cancer Metastasis and Treatment ›› 2016, Vol. 2 : 1 -10.

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Journal of Cancer Metastasis and Treatment ›› 2016, Vol. 2:1 -10. DOI: 10.4103/2394-4722.171829
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Long non-coding RNAs as key regulators of cancer metastasis

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Abstract

The recent advances in functional genomics have discovered that a large number of long non-coding RNAs (lncRNAs) are pervasively transcribed from the human genome. Increasing evidence further indicates that lncRNAs are important for gene expression during cell differentiation and development through various mechanisms such as nuclear organization, post-transcription regulation, alternative splicing, and epigenetic regulation. Thus, aberrant expression of lncRNAs can cause abnormality in those cellular functions and lead to various pathological conditions. One of such fatal consequences is cancer metastasis which is responsible for more than 90% of cancer-related deaths. A good understanding of how lncRNAs regulate different genetic and epigenetic changes during different stages of cancer metastasis is important not only for general cancer biology but also for identifi cation of novel biomarkers and therapeutic targets for treatment of metastatic cancer. A significant progress has been made regarding the role of lncRNAs in cancer for past several years. In this study, we first discuss general functions of lncRNAs and then highlight recent fi ndings of how lncRNAs impact cancer metastasis, and finally we provide our perspectives on clinical implications of lncRNAs.

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Cancer metastasis / epigenetics / gene regulation / long non-coding RNA

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Pratirodh Koirala, De-Hong Zou, Yin-Yuan Mo. Long non-coding RNAs as key regulators of cancer metastasis. Journal of Cancer Metastasis and Treatment, 2016, 2: 1-10 DOI:10.4103/2394-4722.171829

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References

[1]

Lander ES,Birren B,Zody MC,Devon K,Doyle M,Funke R,Harris K,Howland J,Lehoczky J,McEwan P,Meldrim J,Miranda C,Naylor J,Rosetti M,Sheridan A,Stange-Thomann N,Subramanian A,Rogers J,Ainscough R,Bentley D,Clee C,Coulson A,Deloukas P,Dunham I,French L,Gregory S,Humphray S,Jones M,McMurray A,Mercer S,Mullikin JC,Plumb R,Shownkeen R,Waterston RH,Hillier LW,Marra MA,Fulton LA,Pepin KH,Chissoe SL,Delehaunty KD,Delehaunty A,Cook LL,Johnson DL,Clifton SW,Branscomb E,Richardson P,Slezak T,Cheng JF,Lucas S,Uberbacher E,Gibbs RA,Scherer SE,Sodergren EJ,Rives CM,Metzker ML,Kucherlapati RS,Weinstock GM,Fujiyama A,Yada T,Itoh T,Watanabe H,Taylor T,Heilig R,Artiguenave F,Bruls T,Robert C,Smith DR,Rubenfield M,Lee HM,Rosenthal A,Nyakatura G,Rump A,Yu J,Huang G,Hood L,Madan A,Davis RW,Abola AP,Myers RM,Dickson M,Cox DR,Kaul R,Shimizu N,Minoshima S,Athanasiou M,Roe BA,Pan H,Lehrach H,McCombie WR,Dedhia N,Hornischer K,Agarwala R,Bailey JA,Batzoglou S,Bork P,Burge CB,Chen HC,Clamp M,Doerks T,Eichler EE,Galagan J,Harmon C,Haussler D,Hokamp K,Johnson LS,Kasif S,Kennedy S,Kitts P,Korf I,Lancet D,McLysaght A,Moran JV,Pollara VJ,Schuler G,Slater G,Stupka E,Thierry-Mieg D,Wagner L,Wheeler R,Wolf YI,Yang SP,Collins F,Peterson J,Wetterstrand KA,Morgan MJ,Catanese JJ,Shizuya H,Chen YJ.Initial sequencing and analysis of the human genome..Nature2001;409:860-921

[2]

Bertone P,Royce TE,Urban AE,Rinn JL,Samanta M,Gerstein M.Global identification of human transcribed sequences with genome tiling arrays..Science2004;306:2242-6

[3]

Mattick JS.Challenging the dogma: the hidden layer of non-protein-coding RNAs in complex organisms..Bioessays2003;25:930-9

[4]

Ponting CP,Reik W.Evolution and functions of long noncoding RNAs..Cell2009;136:629-41

[5]

Carthew RW.Origins and mechanisms of miRNAs and siRNAs..Cell2009;136:642-55 PMCID:PMC2675692

[6]

Carninci P,Katayama S,Frith MC,Oyama R,Lenhard B,Kodzius R,Bajic VB,Batalov S,Zavolan M,Wilming LG,Allen JE,Apweiler R,Bailey TL,Baxter L,Bersano T,Chalk AM,Choudhary V,Clutterbuck DR,Dalla E,de Bono B,di Bernardo D,Engstrom P,Faulkner G,Fukushima T,Futaki S,Georgii-Hemming P,Gojobori T,Gustincich S,Hayashi Y,Hirokawa N,Huminiecki L,Ikeo K,Ishikawa T,Kanapin A,Kawasawa Y,Kitamura H,Kollias G,Kruger A,Kurochkin IV,Lazarevic D,Liu J,McWilliam S,Madera M,Matsuda H,Miki H,Miyake S,Mottagui-Tabar S,Nakano N,Ng P,Nishiguchi S,Nori F,Okazaki Y,Pang KC,Pavesi G,Petrovsky N,Reed J,Ring BZ,Rost B,Salzberg SL,Schneider C,Sekiguchi K,Seno S,Sheng Y,Shimada H,Silva D,Sperling S,Sugiura K,Takenaka Y,Tammoja K,Tang S,Tegner J,Ueda HR,Verardo R,Yagi K,Zabarovsky E,Zimmer A,Bult C,Teasdale RD,Brusic V,Wahlestedt C,Hume DA,Sasaki D,Fukuda S,Suzuki M,Arakawa T,Imamura K,Kato T,Kawagashira N,Kojima M,Konno H,Ninomiya N,Okada M,Shibata K,Suzuki S,Waki K,Okamura-Oho Y,Kawai J.The transcriptional landscape of the mammalian genome..Science2005;309:1559-63

[7]

Harrow J,Gonzalez JM,Diekhans M,Aken BL,Zadissa A,Barnes I,Boychenko V,Kay M,Rajan J,Saunders G,Harte R,Howald C,Derrien T,Walters N,Pei B,Rodriguez JM,van Baren J,Haussler D,Valencia A,Gerstein M,Hubbard TJ.GENCODE: the reference human genome annotation for the ENCODE project..Genome Res2012;22:1760-74

[8]

Sparmann A.Polycomb silencers control cell fate, development and cancer..Nat Rev Cancer2006;6:846-56

[9]

Pasmant E,Heron D,Vidaud D.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 Res2007;67:3963-9

[10]

Yap KL,Munoz-Cabello AM,Zeng L,Gil J,Zhou MM.Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a..Mol Cell2010;38:662-74 PMCID:PMC2886305

[11]

Plath K,Mlynarczyk-Evans SK,Worringer KA,de la Cruz CC,Panning B.Role of histone H3 lysine 27 methylation in X inactivation..Science2003;300:131-5

[12]

Kim K,Heo K,Levens D,Johnson EM,An W.Isolation and characterization of a novel H1.2 complex that acts as a repressor of p53-mediated transcription..J Biol Chem2008;283:9113-26 PMCID:PMC2431041

[13]

Yoon JH,Srikantan S,Martindale JL,Huarte M,Becker KG.LincRNA-p21 suppresses target mRNA translation..Mol Cell2012;47:648-55 PMCID:PMC3509343

[14]

Derrien T,Bussotti G,Djebali S,Guernec G,Merkel A,Lagarde J,Ruan X,Lassmann T,Brown JB,Gonzalez JM,Davis CA,Gingeras TR,Notredame C,Guigo R.The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression..Genome Res2012;22:1775-89 PMCID:PMC3431493

[15]

Rodriguez A,Ashurst JL.Identification of mammalian microRNA host genes and transcription units..Genome Res2004;14:1902-10 PMCID:PMC524413

[16]

Cai X.The imprinted H19 noncoding RNA is a primary microRNA precursor..RNA2007;13:313-6 PMCID:PMC1800509

[17]

Liu Q,Zhou N,Zhang A,Wu F.LncRNA loc285194 is a p53-regulated tumor suppressor..Nucleic Acids Res2013;41:4976-87 PMCID:PMC3643595

[18]

Zhang Z,Watabe K,Bai C,Wu F.Negative regulation of lncRNA GAS5 by miR-21..Cell Death Differ2013;20:1558-68 PMCID:PMC3792431

[19]

Poliseno L,Zhang J,Haveman WJ.A coding-independent function of gene and pseudogene mRNAs regulates tumour biology..Nature2010;465:1033-8 PMCID:PMC3206313

[20]

Schneider C,Philipson L.Genes specifically expressed at growth arrest of mammalian cells..Cell1988;54:787-93

[21]

Kino T,Ichijo T,Chrousos GP.Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor..Sci Signal2010;3:ra8

[22]

Good MC,Lim WA.Scaffold proteins: hubs for controlling the flow of cellular information..Science2011;332:680-6 PMCID:PMC3117218

[23]

Loewer S,Guttman M,Thomas K,Garber M,Onder T,Manos PD,Lander ES,Daley GQ.Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells..Nat Genet2010;42:1113-7 PMCID:PMC3040650

[24]

Zhang A,Huang J,Fukuda K,Lu Z,Watabe K.The human long non-coding RNA-RoR is a p53 repressor in response to DNA damage..Cell Res2013;23:340-50 PMCID:PMC3587705

[25]

Fox AH,Leung AK,Andersen J,Lamond AI.Paraspeckles: a novel nuclear domain..Curr Biol2002;12:13-25

[26]

Emili A,McCracken S,Tucker PW,Blencowe BJ.Splicing and transcription-associated proteins PSF and p54nrb/nonO bind to the RNA polymerase II CTD..RNA2002;8:1102-11 PMCID:PMC1370324

[27]

Auboeuf D,Li X,Ko L,O'Malley BW.CoAA, a nuclear receptor coactivator protein at the interface of transcriptional coactivation and RNA splicing..Mol Cell Biol2004;24:442-53 PMCID:PMC303353

[28]

Fox AH,Lamond AI.P54nrb forms a heterodimer with PSP1 that localizes to paraspeckles in an RNA-dependent manner..Mol Biol Cell2005;16:5304-15 PMCID:PMC1266428

[29]

Clemson CM,Sara SA,Fox AH,Lawrence JB.An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles..Mol Cell2009;33:717-26 PMCID:PMC2696186

[30]

Morin GB.The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats..Cell1989;59:521-9

[31]

Greider CW.A telomeric sequence in the RNA of tetrahymena telomerase required for telomere repeat synthesis..Nature1989;337:331-7

[32]

Ly H,Parslow TG.Comprehensive structure-function analysis of the core domain of human telomerase RNA..Mol Cell Biol2003;23:6849-56 PMCID:PMC193926

[33]

Vulliamy T,Dokal I.Association between aplastic anaemia and mutations in telomerase RNA..Lancet2002;359:2168-70

[34]

Chaffer CL.A perspective on cancer cell metastasis..Science2011;331:1559-64

[35]

Oka H,Kobayashi K,Tahara H,Takatsuka Y,Hirano S,Mori T.Expression of E-cadherin cell adhesion molecules in human breast cancer tissues and its relationship to metastasis..Cancer Res1993;53:1696-701

[36]

Schipper JH,Behrens J,Jahnke K.E-cadherin expression in squamous cell carcinomas of head and neck: inverse correlation with tumor dedifferentiation and lymph node metastasis..Cancer Res1991;51:6328-37

[37]

Werb Z.ECM and cell surface proteolysis: regulating cellular ecology..Cell1997;91:439-42

[38]

Cheng GZ,Wang Q,Sun CD.Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel..Cancer Res2007;67:1979-87

[39]

Chambers AF,MacDonald IC.Dissemination and growth of cancer cells in metastatic sites..Nat Rev Cancer2002;2:563-72

[40]

Nash GF,Scully MF.Platelets and cancer..Lancet Oncol2002;3:425-30

[41]

Wang H,Im JH,Santoro SA,DiPersio CM,Quaranta V,Muschel RJ.Tumor cell alpha3beta1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis..J Cell Biol2004;164:935-41 PMCID:PMC2172296

[42]

Gupta GP.Cancer metastasis: building a framework..Cell2006;127:679-95

[43]

Aguirre-Ghiso JA.Models, mechanisms and clinical evidence for cancer dormancy..Nat Rev Cancer2007;7:834-46 PMCID:PMC2519109

[44]

Ji P,Wang W,Metzger R,Tidow N,Buerger H,Thomas M,Serve H.MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer..Oncogene2003;22:8031-41

[45]

Tripathi V,Shen Z,Pan Q,Freier SM,Sharma A,Blencowe BJ,Prasanth KV.The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation..Mol Cell2010;39:925-38 PMCID:PMC4158944

[46]

Gutschner T,Eissmann M,Kim Y,Revenko A,Stentrup M,Zornig M,Spector DL.The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells..Cancer Res2013;73:1180-9 PMCID:PMC3589741

[47]

Tano K,Okada T,Shibato J,Ijiri K.MALAT-1 enhances cell motility of lung adenocarcinoma cells by influencing the expression of motility-related genes..FEBS Lett2010;584:4575-80

[48]

Jiang Y,Fang S,Qin C,Zhou G.The role of MALAT1 correlates with HPV in cervical cancer..Oncol Lett2014;7:2135-41 PMCID:PMC4049771

[49]

Jiao F,Han T,Wang L,Guo Z.Long noncoding RNA MALAT-1 enhances stem cell-like phenotypes in pancreatic cancer cells..Int J Mol Sci2015;16:6677-93 PMCID:PMC4424983

[50]

Gupta RA,Wang KC,Horlings HM,Tsai MC,Argani P,Wang Y,Kong B,West RB,Sukumar S.Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis..Nature2010;464:1071-6 PMCID:PMC3049919

[51]

Tsai MC,Wan Y,Wang JK,Shi Y,Chang HY.Long noncoding RNA as modular scaffold of histone modification complexes..Science2010;329:689-93 PMCID:PMC2967777

[52]

Wu Y,Zhang L,Li H,Wei F,Liu T,Zhou X,Hao X.Long non-coding RNA HOTAIR promotes tumor cell invasion and metastasis by recruiting EZH2 and repressing E-cadherin in oral squamous cell carcinoma..Int J Oncol2015;46:2586-94

[53]

Niinuma T,Nojima M,Yamamoto H,Yamamoto E,Nobuoka T,Nishida T,Kanda T,Taguchi T,Takahashi H,Hosokawa M,Tokino T,Imai K,Shinomura Y.Upregulation of miR-196a and HOTAIR drive malignant character in gastrointestinal stromal tumors..Cancer Res2012;72:1126-36

[54]

Pachnis V,Tilghman SM.Locus unlinked to alpha-fetoprotein under the control of the murine raf and rif genes..Proc Natl Acad Sci U S A1984;81:5523-7 PMCID:PMC391738

[55]

Brannan CI,Ingram RS.The product of the H19 gene may function as an RNA..Mol Cell Biol1990;10:28-36 PMCID:PMC360709

[56]

Hao Y,Moulton T,Tycko B.Tumour-suppressor activity of H19 RNA..Nature1993;365:764-7

[57]

Hibi K,Hirai A,Kasai Y,Ito K.Loss of H19 imprinting in esophageal cancer..Cancer Res1996;56:480-2

[58]

Ariel I,Ji XR,Roll D,Hochberg A.Imprinted H19 oncofetal RNA is a candidate tumour marker for hepatocellular carcinoma..Mol Pathol1998;51:21-5 PMCID:PMC395603

[59]

Ayesh S,Schneider T,Laster M,De-Groot N.Possible physiological role of H19 RNA..Mol Carcinog2002;35:63-74

[60]

Luo M,Wang W,Liu Z.Long non-coding RNA H19 increases bladder cancer metastasis by associating with EZH2 and inhibiting E-cadherin expression..Cancer Lett2013;333:213-21

[61]

Adriaenssens E,Berteaux N,Fauquette W,Peyrat JP,Hondermarck H,Dugimont T.Cross-talk between mesenchyme and epithelium increases H19 gene expression during scattering and morphogenesis of epithelial cells..Exp Cell Res2002;275:215-29

[62]

Liang WC,Wong CW,Wang WM,Zhang L,Wan DC,Waye MM.The lncRNA H19 promotes epithelial to mesenchymal transition by functioning as miRNA sponges in colorectal cancer..Oncotarget2015;6:22513-25

[63]

Liu B,Liu Q,Yao Y,Lin L,Su F,Zeng M.A cytoplasmic NF-kappaB interacting long noncoding RNA blocks IkappaB phosphorylation and suppresses breast cancer metastasis..Cancer Cell2015;27:370-81

[64]

Chaturvedi MM,Yadav VR,Aggarwal BB.NF-kappaB addiction and its role in cancer: 'one size does not fit all'..Oncogene2011;30:1615-30 PMCID:PMC3141287

[65]

Ghosh S.Missing pieces in the NF-kappaB puzzle..Cell2002;109 Suppl:S81-96

[66]

Thiery JP,Huang RY.Epithelial-mesenchymal transitions in development and disease..Cell2009;139:871-90

[67]

Akhurst RJ.Targeting the TGFbeta signalling pathway in disease..Nat Rev Drug Discov2012;11:790-811 PMCID:PMC3520610

[68]

Pardali K.Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer..Biochim Biophys Acta2007;1775:21-62

[69]

Yuan JH,Wang F,Guo YJ,Liu F,Wang TT,Wang SB,Yang Y,Zhou WP,Sun SH.A long noncoding RNA activated by TGF-beta promotes the invasion-metastasis cascade in hepatocellular carcinoma..Cancer Cell2014;25:666-81

[70]

Burk U,Wellner U,Vincan E,Brabletz T.A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells..EMBO Rep2008;9:582-9 PMCID:PMC2396950

[71]

Yang F,Huo XS,Xu D,Zhu N,Yang GS,Shang JL,Zhang FR,Sun SH.Long noncoding RNA high expression in hepatocellular carcinoma facilitates tumor growth through enhancer of zeste homolog 2 in humans..Hepatology2011;54:1679-89

[72]

Yang F,Yuan SX,Zhou WP,Sun SH.Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis..Mol Cell2013;49:1083-96

[73]

Peinado H,Cano A.Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?.Nat Rev Cancer2007;7:415-28

[74]

Nissan A,Mitrani-Rosenbaum S,Grinbaum R,Bochem A,Ritter G,Bostanci EB,Chen YT,Gure AO.Colon cancer associated transcript-1: a novel RNA expressed in malignant and pre-malignant human tissues..Int J Cancer2012;130:1598-606

[75]

Yang F,Bi J,Zhi K,Fang G.Long noncoding RNA CCAT1, which could be activated by c-Myc, promotes the progression of gastric carcinoma..J Cancer Res Clin Oncol2013;139:437-45

[76]

Deng L,Xu FF.Long noncoding RNA CCAT1 promotes hepatocellular carcinoma progression by functioning as let-7 sponge..J Exp Clin Cancer Res2015;34:18 PMCID:PMC4339002

[77]

Prensner JR.The emergence of lncRNAs in cancer biology..Cancer Discov2011;1:391-407 PMCID:PMC3215093

[78]

Winkle M,Tayari M,Terpstra M,de Jong D,Diepstra A,Kluiver J.Long noncoding RNAs as a novel component of the Myc transcriptional network..FASEB J2015;29:2338-46

[79]

Jinek M,Fonfara I,Doudna JA.A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity..Science2012;337:816-21

[80]

Sanchez-Rivera FJ.Applications of the CRISPR-Cas9 system in cancer biology..Nat Rev Cancer2015;15:387-95 PMCID:PMC4530801

[81]

Ho TT,Huang J,Xu M,Wu F.Targeting non-coding RNAs with the CRISPR/Cas9 system in human cell lines..Nucleic Acids Res2015;43:e17

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