Altered expression pattern of circular RNAs in primary and metastatic sites of epithelial ovarian carcinoma

Oncotarget

Volumn 7, Issue 24, 2016, Pages 36366-36381

  Ahmed, Ikhlak ^a   Karedath, Thasni ^a   Andrews, Simeon S ^a   Al Azwani, Iman K ^a   Mohamoud, Yasmin Ali ^a   Querleu, Denis ^b   Rafii, Arash ^a   Malek, Joel A ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (Qatar)

^b UNIV MONTPELLIER   (France)

Author keywords

Circular RNA; Lymph node metastasis; MiRNA; Ovarian cancer; Peritoneal metastasis

Indexed keywords

CIRCULAR RNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MICRORNA; PHOSPHATIDYLINOSITOL 3 KINASE; RNA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; RNA, CIRCULAR;

ARTICLE; CASE REPORT; CONTROLLED STUDY; EPITHELIAL OVARIAN CARCINOMA; EXON; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; LYMPH NODE METASTASIS; METASTASIS; OVARY CARCINOMA; PERITONEUM METASTASIS; RNA SEQUENCE; SIGNAL TRANSDUCTION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; NEOPLASM; OVARY TUMOR; PATHOLOGY; PROCEDURES; SEQUENCE ANALYSIS;

FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; HUMANS; MICRORNAS; NEOPLASM METASTASIS; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; RNA; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION;

EID: 84978175938     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8917     Document Type: Article

References (66)

1. GLOBOCAN 2012 [http://globocan.iarc.fr/Default.aspx.]
2. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ: Cancer statistics, 2009. CA: a cancer journal for clinicians, 59:225-49
3. Morice P, Joulie F, Camatte S, Atallah D, Rouzier R, Pautier P, Pomel C, Lhommé C, Duvillard P, Castaigne D: Lymph node involvement in epithelial ovarian cancer: analysis of 276 pelvic and paraaortic lymphadenectomies and surgical implications. Journal of the American College of Surgeons 2003, 197:198-205
4. Rafii A, Stoeckle E, Jean-Laurent M, Ferron G, Morice P, Houvenaeghel G, Lecuru F, Leblanc E, Querleu D: Multicenter evaluation of post-operative morbidity and mortality after optimal cytoreductive surgery for advanced ovarian cancer. PloS one 2012, 7:e39415
5. Cannistra SA: Cancer of the ovary. The New England journal of medicine 2004, 351:2519-29
6. Aparicio S, Mardis E: Tumor heterogeneity: next-generation sequencing enhances the view from the pathologist's microscope. Genome biology 2014, 15:463
7. Malek JA, Martinez A, Mery E, Ferron G, Huang R, Raynaud C, Jouve E, Thiery J-P, Querleu D, Rafii A: Gene expression analysis of matched ovarian primary tumors and peritoneal metastasis. Journal of translational medicine 2012, 10:121
8. Malek JA, Mery E, Mahmoud YA, Al-Azwani EK, Roger L, Huang R, Jouve E, Lis R, Thiery J-P, Querleu D, Rafii A: Copy number variation analysis of matched ovarian primary tumors and peritoneal metastasis. PloS one 2011, 6:e28561
9. Berchuck A, Iversen ES, Lancaster JM, Dressman HK, West M, Nevins JR, Marks JR: Prediction of optimal versus suboptimal cytoreduction of advanced-stage serous ovarian cancer with the use of microarrays. American journal of obstetrics and gynecology 2004, 190:910-25
10. Berchuck A, Iversen ES, Lancaster JM, Pittman J, Luo J, Lee P, Murphy S, Dressman HK, Febbo PG, West M, Nevins JR, Marks JR: Patterns of gene expression that characterize long-term survival in advanced stage serous ovarian cancers. Clinical cancer research. 2005, 11:3686-96
11. Spentzos D, Levine DA, Ramoni MF, Joseph M, Gu X, Boyd J, Libermann TA, Cannistra SA: Gene expression signature with independent prognostic significance in epithelial ovarian cancer. Journal of clinical oncology. 2004, 22:4700-10
12. Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO: Cell-type specific features of circular RNA expression. PLoS genetics 2013, 9:e1003777
13. Salzman J, Gawad C, Wang PL, Lacayo N, Brown PO: Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PloS one 2012, 7:e30733
14. Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, MarzluffWF, Sharpless NE: Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA (New York, NY) 2013, 19:141-57
15. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N: Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 2013, 495:333-8
16. Danan M, Schwartz S, Edelheit S, Sorek R: Transcriptomewide discovery of circular RNAs in Archaea. Nucleic acids research 2012, 40:3131-42
17. Wang PL, Bao Y, Yee M-C, Barrett SP, Hogan GJ, Olsen MN, Dinneny JR, Brown PO, Salzman J: Circular RNA Is Expressed across the Eukaryotic Tree of Life. PloS one 2014, 9:e90859
18. Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N, Kadener S: circRNA Biogenesis Competes with Pre-mRNA Splicing. Molecular Cell 2014, 56:55-66
19. Zhang X-O, Wang H-B, Zhang Y, Lu X, Chen L-L, Yang L: Complementary Sequence-Mediated Exon Circularization. Cell 2014, 159:134-147
20. Liang D, Wilusz JE: Short intronic repeat sequences facilitate circular RNA production. Genes & development 2014:gad.251926.114-
21. Jeck WR, Sharpless NE: Detecting and characterizing circular RNAs. Nature Biotechnology 2014, 32:453-461
22. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J: Natural RNA circles function as efficient microRNA sponges. Nature 2013, 495:384-8
23. Hansen TB, Kjems J, Damgaard CK: Circular RNA and miR-7 in cancer. Cancer research 2013, 73:5609-12
24. Liu Y, Cui H, Wang W, Li L, Wang Z, Yang S, Zhang X: Construction of circular miRNA sponges targeting miR-21 or miR-221 and demonstration of their excellent anticancer effects on malignant melanoma cells. The international journal of biochemistry & cell biology 2013, 45:2643-50
25. Langmead B, Salzberg SL: Fast gapped-read alignment with Bowtie 2. Nature methods 2012, 9:357-9
26. Holtgrewe M, Emde A-K, Weese D, Reinert K: A novel and well-defined benchmarking method for second generation read mapping. BMC bioinformatics 2011, 12:210
27. Chen I, Chen C-Y, Chuang T-J: Biogenesis, identification, and function of exonic circular RNAs. Wiley interdisciplinary reviews RNA 2015
28. Cocquet J, Chong A, Zhang G, Veitia RA: Reverse transcriptase template switching and false alternative transcripts. Genomics 2006, 88:127-31
29. Gilboa E, Mitra SW, GoffS, Baltimore D: A detailed model of reverse transcription and tests of crucial aspects. Cell 1979, 18:93-100
30. Roy SW, Irimia M: When good transcripts go bad: artifactual RT-PCR "splicing" and genome analysis. BioEssays: news and reviews in molecular, cellular and developmental biology 2008, 30:601-5
31. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward D V, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methé B, DeSantis TZ, Petrosino JF, Knight R, Birren BW: Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome research 2011, 21:494-504
32. McManus CJ, DuffMO, Eipper-Mains J, Graveley BR: Global analysis of trans-splicing in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:12975-9
33. Edgren H, Murumagi A, Kangaspeska S, Nicorici D, Hongisto V, Kleivi K, Rye IH, Nyberg S, Wolf M, Borresen-Dale A-L, Kallioniemi O: Identification of fusion genes in breast cancer by paired-end RNA-sequencing. Genome biology 2011, 12:R6
34. Berger MF, Levin JZ, Vijayendran K, Sivachenko A, Adiconis X, Maguire J, Johnson LA, Robinson J, Verhaak RG, Sougnez C, Onofrio RC, Ziaugra L, Cibulskis K, Laine E, Barretina J, Winckler W, Fisher DE, Getz G, Meyerson M, Jaffe DB, Gabriel SB, Lander ES, Dummer R, Gnirke A, Nusbaum C, Garraway LA: Integrative analysis of the melanoma transcriptome. Genome research 2010, 20:413-27
35. Vincent HA, Deutscher MP: Substrate recognition and catalysis by the exoribonuclease RNase R. The Journal of biological chemistry 2006, 281:29769-75
36. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB: Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456:470-6
37. Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics (Oxford, England) 2009, 25:1105-11
38. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature biotechnology 2010, 28:511-5
39. Kui Wong N, Easton RL, Panico M, Sutton-Smith M, Morrison JC, Lattanzio FA, Morris HR, Clark GF, Dell A, Patankar MS: Characterization of the oligosaccharides associated with the human ovarian tumor marker CA125. The Journal of biological chemistry 2003, 278:28619-34
40. McLemore MR, Aouizerat B: Introducing the MUC16 gene: implications for prevention and early detection in epithelial ovarian cancer. Biological research for nursing 2005, 6:262-7
41. Yin BW, Lloyd KO: Molecular cloning of the CA125 ovarian cancer antigen: identification as a new mucin, MUC16. The Journal of biological chemistry 2001, 276:27371-5
42. Guo H, Ingolia NT, Weissman JS, Bartel DP: Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-40
43. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N: Widespread changes in protein synthesis induced by microRNAs. Nature 2008, 455:58-63
44. Baek D, Villén J, Shin C, Camargo FD, Gygi SP, Bartel DP: The impact of microRNAs on protein output. Nature 2008, 455:64-71
45. Volinia S, Calin GA, Liu C-G, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM: A microRNA expression signature of human solid tumors defines cancer gene targets. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:2257-61
46. Bandyopadhyay S, Mitra R, Maulik U, Zhang MQ: Development of the human cancer microRNA network. Silence 2010, 1:6
47. Grimson A, Farh KK-H, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP: MicroRNA targeting specificity in mammals: Determinants beyond seed pairing. Molecular cell 2007, 27:91-105
48. Lewis BP, Burge CB, Bartel DP: Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20
49. Kozomara A, Griffiths-Jones S: miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic acids research 2014, 42(Database issue):D68-73
50. Bernhart SH, Tafer H, Mückstein U, Flamm C, Stadler PF, Hofacker IL: Partition function and base pairing probabilities of RNA heterodimers. Algorithms for molecular biology: AMB 2006, 1:3
51. Saetrom P, Heale BSE, Snøve O, Aagaard L, Alluin J, Rossi JJ: Distance constraints between microRNA target sites dictate efficacy and cooperativity. Nucleic acids research 2007, 35:2333-42
52. Liao Y, Smyth GK, Shi W: featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics (Oxford, England) 2014, 30:923-30
53. Robinson MD, McCarthy DJ, Smyth GK: edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics (Oxford, England) 2010, 26:139-40
54. Capel B, Swain A, Nicolis S, Hacker A, Walter M, Koopman P, Goodfellow P, Lovell-Badge R: Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 1993, 73:1019-30
55. Bywater MJ, Pearson RB, McArthur GA, Hannan RD: Dysregulation of the basal RNA polymerase transcription apparatus in cancer. Nature reviews Cancer 2013, 13:299-314
56. Villicaña C, Cruz G, Zurita M: The basal transcription machinery as a target for cancer therapy. Cancer cell international 2014, 14:18
57. Hahn William C., Weinberg Robert A.: A subway map of cancer pathways. Nature reviews Cancer 2002
58. Li C-W, Xia W, Huo L, Lim S-O, Wu Y, Hsu JL, Chao C-H, Yamaguchi H, Yang N-K, Ding Q, Wang Y, Lai Y-J, LaBaffAM, Wu T-J, Lin B-R, Yang M-H, Hortobagyi GN, Hung M-C: Epithelial-mesenchymal transition induced by TNF-a requires NF-κB-mediated transcriptional upregulation of Twist1. Cancer research 2012, 72:1290-300
59. Lamouille S, Xu J, Derynck R: Molecular mechanisms of epithelial-mesenchymal transition. Nature reviews Molecular cell biology 2014, 15:178-96
60. Chou C-H, Wei L-H, Kuo M-L, Huang Y-J, Lai K-P, Chen C-A, Hsieh C-Y: Up-regulation of interleukin-6 in human ovarian cancer cell via a Gi/PI3K-Akt/NF-kappaB pathway by lysophosphatidic acid, an ovarian cancer-activating factor. Carcinogenesis 2005, 26:45-52
61. Farazi TA, Hoell JI, Morozov P, Tuschl T: MicroRNAs in human cancer. Advances in experimental medicine and biology 2013, 774:1-20
62. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, Labourier E, Reinert KL, Brown D, Slack FJ: RAS is regulated by the let-7 microRNA family. Cell 2005, 120:635-47
63. Lynam-Lennon N, Maher SG, Reynolds J V: The roles of microRNA in cancer and apoptosis. Biological reviews of the Cambridge Philosophical Society 2009, 84:55-71
64. Liu Q, Lv G-D, Qin X, Gen Y-H, Zheng S-T, Liu T, Lu X-M: Role of microRNA let-7 and effect to HMGA2 in esophageal squamous cell carcinoma. Molecular biology reports 2012, 39:1239-46
65. Du WW, Fang L, Li M, Yang X, Liang Y, Peng C, Qian W, O'Malley YQ, Askeland RW, Sugg SL, Qian J, Lin J, Jiang Z, Yee AJ, Sefton M, Deng Z, Shan SW, Wang C-H, Yang BB: MicroRNA miR-24 enhances tumor invasion and metastasis by targeting PTPN9 and PTPRF to promote EGF signaling. Journal of cell science 2013, 126(Pt 6):1440-53
66. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The Sequence Alignment/Map format and SAMtools. Bioinformatics (Oxford, England) 2009, 25:2078-9