The Emerging Function and Mechanism of ceRNAs in Cancer

Trends in Genetics

Volumn 32, Issue 4, 2016, Pages 211-224

  Wang, Yunfei ^a   Hou, Jiakai ^a   He, Dandan ^a   Sun, Ming ^a   Zhang, Peng ^a   Yu, Yonghao ^b   Chen, Yiwen ^a  

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

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPETING ENDOGENOUS RNA; MICRORNA; RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

BREAST CANCER; CARCINOGENESIS; DIGESTIVE SYSTEM CANCER; ENDOMETRIUM CANCER; GENE EXPRESSION; GENE FUNCTION; HUMAN; HUMAN GENOME; KIDNEY CARCINOMA; LEUKEMIA; LUNG CANCER; LYMPHOMA; MALIGNANT NEOPLASTIC DISEASE; MATHEMATICAL ANALYSIS; MOLECULAR BIOLOGY; PRIORITY JOURNAL; REVIEW; RNA STRUCTURE; SOLID TUMOR; THYROID CANCER; TUMOR SUPPRESSOR GENE; GENETICS; NEOPLASM; PHYSIOLOGY;

HUMANS; NEOPLASMS; RNA;

EID: 84959098255     PISSN: 01689525     EISSN: 13624555     Source Type: Journal    
DOI: 10.1016/j.tig.2016.02.001     Document Type: Review

References (130)

1. Rinn J.L., Chang H.Y. Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 2012, 81:145-166.
2. Djebali S., et al. Landscape of transcription in human cells. Nature 2012, 489:101-108.
3. Mattick J.S., Rinn J.L. Discovery and annotation of long noncoding RNAs. Nat. Struct. Mol. Biol. 2015, 22:5-7.
4. Prensner J.R., Chinnaiyan A.M. The emergence of lncRNAs in cancer biology. Cancer Discov. 2011, 1:391-407.
5. Chew G.L., et al. Ribosome profiling reveals resemblance between long non-coding RNAs and 5' leaders of coding RNAs. Development 2013, 140:2828-2834.
6. Magny E.G., et al. Conserved regulation of cardiac calcium uptake by peptides encoded in small open reading frames. Science 2013, 341:1116-1120.
7. Anderson D.M., et al. A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell 2015, 160:595-606.
8. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
9. Rhoades M.W., et al. Prediction of plant microRNA targets. Cell 2002, 110:513-520.
10. Lewis B.P., et al. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
11. Clark P.M., et al. Argonaute CLIP-Seq reveals miRNA targetome diversity across tissue types. Sci. Rep. 2014, 4:5947.
12. Hafner M., et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010, 141:129-141.
13. Hausser J., et al. Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation. Genome Res. 2013, 23:604-615.
14. Helwak A., et al. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 2013, 153:654-665.
15. Yekta S., et al. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004, 304:594-596.
16. Davis E., et al. RNAi-mediated allelic trans-interaction at the imprinted Rtl1/Peg11 locus. Curr. Biol. 2005, 15:743-749.
17. Friedman R.C., et al. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009, 19:92-105.
18. Brown B.D., et al. Endogenous microRNA can be broadly exploited to regulate transgene expression according to tissue, lineage and differentiation state. Nat. Biotechnol. 2007, 25:1457-1467.
19. Care A., et al. MicroRNA-133 controls cardiac hypertrophy. Nat. Med. 2007, 13:613-618.
20. Ebert M.S., et al. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 2007, 4:721-726.
21. Gentner B., et al. Stable knockdown of microRNA in vivo by lentiviral vectors. Nat. Methods 2009, 6:63-66.
22. Valastyan S., et al. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 2009, 137:1032-1046.
23. Luna J.M., et al. Hepatitis C virus RNA functionally sequesters miR-122. Cell 2015, 160:1099-1110.
24. Ebert M.S., Sharp P.A. MicroRNA sponges: progress and possibilities. RNA 2010, 16:2043-2050.
25. Salmena L., et al. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language?. Cell 2011, 146:353-358.
26. Ebert M.S., Sharp P.A. Emerging roles for natural microRNA sponges. Curr. Biol. 2010, 20:R858-R861.
27. Seitz H. Redefining microRNA targets. Curr. Biol. 2009, 19:870-873.
28. Franco-Zorrilla J.M., et al. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 2007, 39:1033-1037.
29. Cazalla D., et al. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 2010, 328:1563-1566.
30. Poliseno L., et al. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 2010, 465:1033-1038.
31. Tay Y., et al. Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell 2011, 147:344-357.
32. Karreth F.A., et al. In vivo identification of tumor-suppressive PTEN ceRNAs in an oncogenic BRAF-induced mouse model of melanoma. Cell 2011, 147:382-395.
33. Cesana M., et al. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 2011, 147:358-369.
34. Levine E., et al. Quantitative characteristics of gene regulation by small RNA. PLoS Biol. 2007, 5:e229.
35. Irnov I., et al. Identification of regulatory RNAs in Bacillus subtilis. Nucleic Acids Res. 2010, 38:6637-6651.
36. Opdyke J.A., et al. GadY, a small-RNA regulator of acid response genes in Escherichia coli. J. Bacteriol. 2004, 186:6698-6705.
37. Jens M., Rajewsky N. Competition between target sites of regulators shapes post-transcriptional gene regulation. Nat. Rev. Genet. 2015, 16:113-126.
38. Osborne R.J., Thornton C.A. RNA-dominant diseases. Hum. Mol. Genet. 2006, 15:R162-R169.
39. Sumazin P., et al. An extensive microRNA-mediated network of RNA-RNA interactions regulates established oncogenic pathways in glioblastoma. Cell 2011, 147:370-381.
40. de Giorgio A., et al. Emerging roles of competing endogenous RNAs in cancer: insights from the regulation of PTEN. Mol. Cell. Biol. 2013, 33:3976-3982.
41. Yoon J.H., et al. LincRNA-p21 suppresses target mRNA translation. Mol. Cell 2012, 47:648-655.
42. Wang J., et al. CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acids Res. 2010, 38:5366-5383.
43. Fan M., et al. A long non-coding RNA, PTCSC3, as a tumor suppressor and a target of miRNAs in thyroid cancer cells. Exp. Ther. Med. 2013, 5:1143-1146.
44. Wang Y., et al. Endogenous miRNA sponge lincRNA-RoR regulates Oct4, Nanog, and Sox2 in human embryonic stem cell self-renewal. Dev. Cell 2013, 25:69-80.
45. Zhou Du, et al. Integrative analyses reveal a long non-coding-RNA mediated sponge regulatory network in prostate cancer. Nat. Commun. 2016, (in press).
46. Guttman M., Rinn J.L. Modular regulatory principles of large non-coding RNAs. Nature 2012, 482:339-346.
47. Liang D.M., Wilusz J.E. Short intronic repeat sequences facilitate circular RNA production. Gene Dev. 2014, 28:2233-2247.
48. Jeck W.R., et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 2013, 19:141-157.
49. Hansen T.B., et al. miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J. 2011, 30:4414-4422.
50. Salzman J., et al. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS ONE 2012, 7:30733.
51. Zhang X.O., et al. Complementary sequence-mediated exon circularization. Cell 2014, 159:134-147.
52. Guo J.U., et al. Expanded identification and characterization of mammalian circular RNAs. Genome Biol. 2014, 15:409.
53. Hansen T.B., et al. Natural RNA circles function as efficient microRNA sponges. Nature 2013, 495:384-388.
54. Memczak S., et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 2013, 495:333-338.
55. Li F., et al. Circular RNA ITCH has inhibitory effect on ESCC by suppressing the Wnt/beta-catenin pathway. Oncotarget 2015, 6:6001-6013.
56. Huang G., et al. cir-ITCH plays an inhibitory role in colorectal cancer by regulating the Wnt/beta-catenin pathway. PLoS ONE 2015, 10:e0131225.
57. Krek A., et al. Combinatorial microRNA target predictions. Nat. Genet. 2005, 37:495-500.
58. John B., et al. Human microRNA targets. PLoS Biol. 2004, 2:1862-1879.
59. Kertesz M., et al. The role of site accessibility in microRNA target recognition. Nat. Genet. 2007, 39:1278-1284.
60. Chi S.W., et al. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 2009, 460:479-486.
61. Loeb G.B., et al. Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol. Cell 2012, 48:760-770.
62. Chiu H.S., et al. Cupid: simultaneous reconstruction of microRNA-target and ceRNA networks. Genome Res. 2015, 25:257-267.
63. Yuan Y., et al. Model-guided quantitative analysis of microRNA-mediated regulation on competing endogenous RNAs using a synthetic gene circuit. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:3158-3163.
64. Ala U., et al. Integrated transcriptional and competitive endogenous RNA networks are cross-regulated in permissive molecular environments. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:7154-7159.
65. Denzler R., et al. Assessing the ceRNA hypothesis with quantitative measurements of miRNA and target abundance. Mol. Cell 2014, 54:766-776.
66. Bosson A.D., et al. Endogenous miRNA and target concentrations determine susceptibility to potential ceRNA competition. Mol. Cell 2014, 56:347-359.
67. Yuan J.H., et al. A long noncoding RNA activated by TGF-beta promotes the invasion-metastasis cascade in hepatocellular carcinoma. Cancer Cell 2014, 25:666-681.
68. Peng H., et al. Pseudogene INTS6P1 regulates its cognate gene INTS6 through competitive binding of miR-17-5p in hepatocellular carcinoma. Oncotarget 2015, 6:5666-5677.
69. Shen K., et al. Post-transcriptional regulation of the tumor suppressor miR-139-5p and a network of miR-139-5p-mediated mRNA interactions in colorectal cancer. FEBS J. 2014, 281:3609-3624.
70. Hu Y., et al. Long noncoding RNA GAPLINC regulates CD44-dependent cell invasiveness and associates with poor prognosis of gastric cancer. Cancer Res. 2014, 74:6890-6902.
71. Rutnam Z.J., et al. The pseudogene TUSC2P promotes TUSC2 function by binding multiple microRNAs. Nat. Commun. 2014, 5:2914.
72. Zhou X., et al. Linc-RNA-RoR acts as a 'sponge' against mediation of the differentiation of endometrial cancer stem cells by microRNA-145. Gynecol. Oncol. 2014, 133:333-339.
73. Yu G., et al. Pseudogene PTENP1 functions as a competing endogenous RNA to suppress clear-cell renal cell carcinoma progression. Mol. Cancer Ther. 2014, 13:3086-3097.
74. Liu K., et al. AEG-1 3'-untranslated region functions as a ceRNA in inducing epithelial-mesenchymal transition of human non-small cell lung cancer by regulating miR-30a activity. Eur. J. Cell Biol. 2015, 94:22-31.
75. Karreth F.A., et al. The BRAF pseudogene functions as a competitive endogenous RNA and induces lymphoma in vivo. Cell 2015, 161:319-332.
76. Guo G., et al. A long noncoding RNA critically regulates Bcr-Abl-mediated cellular transformation by acting as a competitive endogenous RNA. Oncogene 2015, 34:1768-1779.
77. Tay Y., et al. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 2008, 455:1124-1128.
78. Mayr C., Bartel D.P. Widespread shortening of 3' UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 2009, 138:673-684.
79. Xia Z., et al. Dynamic analyses of alternative polyadenylation from RNA-seq reveal a 3'-UTR landscape across seven tumour types. Nat. Commun. 2014, 5:5274.
80. Kawahara Y., et al. Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science 2007, 315:1137-1140.
81. Levanon E.Y., et al. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat. Biotechnol. 2004, 22:1001-1005.
82. Borchert G.M., et al. Adenosine deamination in human transcripts generates novel microRNA binding sites. Hum. Mol. Genet. 2009, 18:4801-4807.
83. Lee J.H., et al. Highly multiplexed subcellular RNA sequencing in situ. Science 2014, 343:1360-1363.
84. Chen K.H., et al. RNA imaging. Spatially resolved, highly multiplexed RNA profiling in single cells. Science 2015, 348:aaa6090.
85. Cabili M.N., et al. Localization and abundance analysis of human lncRNAs at single-cell and single-molecule resolution. Genome Biol. 2015, 16:20.
86. Castello A., et al. System-wide identification of RNA-binding proteins by interactome capture. Nat. Protoc. 2013, 8:491-500.
87. Baltz A.G., et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol. Cell 2012, 46:674-690.
88. Cox J., Mann M. Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 2011, 80:273-299.
89. Gstaiger M., Aebersold R. Applying mass spectrometry-based proteomics to genetics, genomics and network biology. Nat. Rev. Genet. 2009, 10:617-627.
90. Gerlinger M., et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 2012, 366:883-892.
91. Dalerba P., et al. Single-cell dissection of transcriptional heterogeneity in human colon tumors. Nat. Biotechnol. 2011, 29:1120-1127.
92. Ramskold D., et al. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat. Biotechnol. 2012, 30:777-782.
93. Miranda K.C., et al. A pattern-based method for the identification of microRNA binding sites and their corresponding heteroduplexes. Cell 2006, 126:1203-1217.
94. Li J.H., et al. starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data. Nucleic Acids Res. 2013, 42:D92-D97.
95. Licatalosi D.D., et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 2008, 456:464-469.
96. Konig J., et al. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat. Struct. Mol. Biol. 2010, 17:909-915.
97. Flynn R.A., et al. Dissecting noncoding and pathogen RNA-protein interactomes. RNA 2015, 21:135-143.
98. Nonne N., et al. Tandem affinity purification of miRNA target mRNAs (TAP-Tar). Nucleic Acids Res. 2010, 38:e20.
99. Orom U.A., Lund A.H. Isolation of microRNA targets using biotinylated synthetic microRNAs. Methods 2007, 43:162-165.
100. Hsu R.J., et al. Labeled microRNA pull-down assay system: an experimental approach for high-throughput identification of microRNA-target mRNAs. Nucleic Acids Res. 2009, 37:e77.
101. Yoon J.H., et al. MS2-TRAP (MS2-tagged RNA affinity purification): tagging RNA to identify associated miRNAs. Methods 2012, 58:81-87.
102. Braun J., et al. Rapid identification of regulatory microRNAs by miTRAP (miRNA trapping by RNA in vitro affinity purification). Nucleic Acids Res. 2014, 42:e66.
103. Hassan T., et al. Isolation and identification of cell-specific microRNAs targeting a messenger RNA using a biotinylated anti-sense oligonucleotide capture affinity technique. Nucleic Acids Res. 2013, 41:e71.
104. Kudla G., et al. Cross-linking, ligation, and sequencing of hybrids reveals RNA-RNA interactions in yeast. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:10010-10015.
105. Bantscheff M., et al. Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present. Anal. Bioanal. Chem. 2012, 404:939-965.
106. Gygi S.P., et al. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 1999, 17:994-999.
107. Thompson A., et al. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem. 2003, 75:1895-1904.
108. Ross P.L., et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 2004, 3:1154-1169.
109. Ong S.E., et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1:376-386.
110. Castello A., et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 2012, 149:1393-1406.
111. Zheng L., et al. The 3'UTR of the pseudogene CYP4Z2P promotes tumor angiogenesis in breast cancer by acting as a ceRNA for CYP4Z1. Breast Cancer Res. Treat. 2015, 150:105-118.
112. Ferracin M., et al. miR-125b targets erythropoietin and its receptor and their expression correlates with metastatic potential and ERBB2/HER2 expression. Mol. Cancer 2013, 12:130.
113. Yang J., et al. FOXO1 3'UTR functions as a ceRNA in repressing the metastases of breast cancer cells via regulating miRNA activity. FEBS Lett. 2014, 588:3218-3224.
114. Li D., et al. OCT4B modulates OCT4A expression as ceRNA in tumor cells. Oncol. Rep. 2015, 33:2622-2630.
115. Lee D.Y., et al. Expression of versican 3'-untranslated region modulates endogenous microRNA functions. PLoS ONE 2010, 5:e13599.
116. Fang L., et al. Versican 3'-untranslated region (3'-UTR) functions as a ceRNA in inducing the development of hepatocellular carcinoma by regulating miRNA activity. FASEB J. 2013, 27:907-919.
117. Pilyugin M., Irminger-Finger I. Long non-coding RNA and microRNAs might act in regulating the expression of BARD1 mRNAs. Int. J. Biochem. Cell Biol. 2014, 54:356-367.
118. Ma M.Z., et al. Long non-coding RNA CCAT1 promotes gallbladder cancer development via negative modulation of miRNA-218-5p. Cell Death Dis. 2015, 6:e1583.
119. Deng L., et al. Long noncoding RNA CCAT1 promotes hepatocellular carcinoma progression by functioning as let-7 sponge. J. Exp. Clin. Cancer Res. 2015, 34:18.
120. Yuan S.X., et al. Long noncoding RNA DANCR increases stemness features of hepatocellular carcinoma by derepression of CTNNB1. Hepatology 2015, 63:499-511.
121. Zhang Z., et al. Negative regulation of lncRNA GAS5 by miR-21. Cell Death Differ. 2013, 20:1558-1568.
122. Tsang F.H., et al. Long non-coding RNA HOTTIP is frequently up-regulated in hepatocellular carcinoma and is targeted by tumour suppressive miR-125b. Liver Int. 2015, 35:1597-1606.
123. Liu X.H., et al. Lnc RNA HOTAIR functions as a competing endogenous RNA to regulate HER2 expression by sponging miR-331-3p in gastric cancer. Mol. Cancer 2014, 13:92.
124. Tang J., et al. A novel biomarker Linc00974 interacting with KRT19 promotes proliferation and metastasis in hepatocellular carcinoma. Cell Death Dis. 2014, 5:e1549.
125. Xia T., et al. Long noncoding RNA associated-competing endogenous RNAs in gastric cancer. Sci. Rep. 2014, 4:6088.
126. Eades G., et al. lincRNA-RoR and miR-145 regulate invasion in triple-negative breast cancer via targeting ARF6. Mol. Cancer Res. 2015, 13:330-338.
127. Prensner J.R., et al. The long non-coding RNA PCAT-1 promotes prostate cancer cell proliferation through cMyc. Neoplasia 2014, 16:900-908.
128. Wang F., et al. Upregulated lncRNA-UCA1 contributes to progression of hepatocellular carcinoma through inhibition of miR-216b and activation of FGFR1/ERK signaling pathway. Oncotarget 2015, 6:7899-7917.
129. Yao Y., et al. Knockdown of long non-coding RNA XIST exerts tumor-suppressive functions in human glioblastoma stem cells by up-regulating miR-152. Cancer Lett. 2015, 359:75-86.
130. Chen C.L., et al. Suppression of hepatocellular carcinoma by baculovirus-mediated expression of long non-coding RNA PTENP1 and MicroRNA regulation. Biomaterials 2015, 44:71-81.