Comprehensive analysis of lncRNA expression profiles reveals a novel lncRNA signature to discriminate nonequivalent outcomes in patients with ovarian cancer

Oncotarget

Volumn 7, Issue 22, 2016, Pages 32433-32448

  Zhou, Meng ^a   Sun, Yanying ^a   Sun, Yifan ^a   Xu, Wanying ^a   Zhang, Zhaoyue ^a   Zhao, Hengqiang ^a   Zhong, Zhaohua ^a   Sun, Jie ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

BRCA1 2; Long non coding RNAs; Outcome; Ovarian cancer

Indexed keywords

ANTINEOPLASTIC AGENT; BRCA1 PROTEIN; BRCA2 PROTEIN; LONG UNTRANSLATED RNA;

ADULT; ARTICLE; BRCA2 GENE; CANCER PROGNOSIS; CANCER STAGING; COHORT ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE MUTATION; GENETIC ANALYSIS; HIGH RISK POPULATION; HUMAN; LOW RISK POPULATION; MAJOR CLINICAL STUDY; OVARY CANCER; PATHOGENESIS; TREATMENT RESPONSE; TUMOR SUPPRESSOR GENE; BIOSYNTHESIS; GENETICS; METABOLISM; MIDDLE AGED; OVARY TUMOR; PATHOLOGY; PROGNOSIS; TREATMENT OUTCOME;

FEMALE; HUMANS; MIDDLE AGED; OVARIAN NEOPLASMS; PROGNOSIS; RNA, LONG NONCODING; TREATMENT OUTCOME;

EID: 84973570902     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8653     Document Type: Article

References (86)

1. Siegel R, Ma J, Zou Z and Jemal A. Cancer statistics, 2014. CA: a cancer journal for clinicians. 2014; 64:9-29.
2. Wang B, Liu S-Z, Zheng R-S, Zhang F, Chen W-Q and Sun X-B. Time trends of ovarian cancer incidence in China. Asian Pacific journal of cancer prevention. 2013; 15:191-193.
3. Du Bois A, Quinn M, Thigpen T, Vermorken J, Avall-Lundqvist E, Bookman M, Bowtell D, Brady M, Casado A and Cervantes A. 2004 consensus statements on the management of ovarian cancer: final document of the 3rd International Gynecologic Cancer Intergroup Ovarian Cancer Consensus Conference (GCIG OCCC 2004). Annals of oncology. 2005; 16:viii7.
4. Kim A, Ueda Y, Naka T and Enomoto T. Therapeutic strategies in epithelial ovarian cancer. J Exp Clin Cancer Res. 2012; 31:14.
5. Coleman M, Forman D, Bryant H, Butler J, Rachet B, Maringe C, Nur U, Tracey E, Coory M and Hatcher J. Cancer survival in Australia, Canada, Denmark, Norway, Sweden, and the UK, 1995-2007 (the International Cancer Benchmarking Partnership): an analysis of population-based cancer registry data. The Lancet. 2011; 377:127-138.
6. Rinn JL and Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem. 2012; 81:145-166.
7. Kornienko AE, Guenzl PM, Barlow DP and Pauler FM. Gene regulation by the act of long non-coding RNA transcription. BMC biology. 2013; 11:59.
8. Cao J. The functional role of long non-coding RNAs and epigenetics. Biol Proced Online. 2014; 16:11.
9. Mercer TR, Dinger ME and Mattick JS. Long non-coding RNAs: insights into functions. Nature Reviews Genetics. 2009; 10:155-159.
10. Fatica A and Bozzoni I. Long non-coding RNAs: new players in cell differentiation and development. Nature Reviews Genetics. 2014; 15:7-21.
11. Moran VA, Perera RJ and Khalil AM. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic acids research. 2012; 40:6391-6400.
12. Gibb EA, Brown CJ and Lam WL. The functional role of long non-coding RNA in human carcinomas. Mol Cancer. 2011; 10:38-55.
13. Cheetham S, Gruhl F, Mattick J and Dinger M. Long noncoding RNAs and the genetics of cancer. British journal of cancer. 2013; 108:2419-2425.
14. Yang G, Lu X and Yuan L. LncRNA: a link between RNA and cancer. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms. 2014; 1839:1097-1109.
15. Wu D, Huang Y, Kang J, Li K, Bi X, Zhang T, Jin N, Hu Y, Tan P and Zhang L. ncRDeathDB: A comprehensive bioinformatics resource for deciphering network organization of the ncRNA-mediated cell death system. Autophagy. 2015; 11:1917-1926.
16. Li Y, Zhuang L, Wang Y, Hu Y, Wu Y, Wang D and Xu J. Connect the dots: a systems level approach for analyzing the miRNA-mediated cell death network. Autophagy. 2013; 9:436-439.
17. Wang Y, Chen L, Chen B, Li X, Kang J, Fan K, Hu Y, Xu J, Yi L and Yang J. Mammalian ncRNA-disease repository: a global view of ncRNA-mediated disease network. Cell Death Dis. 2013; 4:e765.
18. Spizzo R, Almeida MI, Colombatti A and Calin GA. Long non-coding RNAs and cancer: a new frontier of translational research&quest. Oncogene. 2012; 31:4577-4587.
19. Gibb EA, Vucic EA, Enfield K, Stewart GL, Lonergan KM, Kennett JY, Becker-Santos DD, MacAulay CE, Lam S and Brown CJ. Human cancer long non-coding RNA transcriptomes. PloS one. 2011; 6:e25915.
20. White NM, Cabanski CR, Silva-Fisher JM, Dang HX, Govindan R and Maher CA. Transcriptome sequencing reveals altered long intergenic non-coding RNAs in lung cancer. Genome Biol. 2014; 415:429.
21. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A and Rinn JL. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes & development. 2011; 25:1915-1927.
22. Tørring PM, Larsen MJ, Kjeldsen AD, Ousager LB, Tan Q and Brusgaard K. Long non-coding RNA expression profiles in hereditary haemorrhagic telangiectasia. PloS one. 2014; 9:e90272.
23. Luo M, Li Z, Wang W, Zeng Y, Liu Z and Qiu J. Long non-coding RNA H19 increases bladder cancer metastasis by associating with EZH2 and inhibiting E-cadherin expression. Cancer letters. 2013; 333:213-221.
24. Duret L, Chureau C, Samain S, Weissenbach J and Avner P. The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science. 2006; 312:1653-1655.
25. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai M-C, Hung T, Argani P and Rinn JL. Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature. 2010; 464:1071-1076.
26. Braconi C, Kogure T, Valeri N, Huang N, Nuovo G, Costinean S, Negrini M, Miotto E, Croce C and Patel T. microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene. 2011; 30:4750-4756.
27. Wu Y, Liu H, Shi X, Yao Y, Yang W and Song Y. The long non-coding RNA HNF1A-AS1 regulates proliferation and metastasis in lung adenocarcinoma. Oncotarget. 2015; 6:9160. doi: 10.18632/oncotarget.3247
28. Colombo T, Farina L, Macino G and Paci P. PVT1: a rising star among oncogenic long noncoding RNAs. Biomed Res Int. 2015; 2015:304208.
29. Hauptman N and Glavac D. Long non-coding RNA in cancer. International journal of molecular sciences. 2013; 14:4655-4669.
30. Zhang X-Q, Sun S, Lam K-F, Kiang KM-Y, Pu JK-S, Ho AS-W, Lui W-M, Fung C-F, Wong T-S and Leung GK-K. A long non-coding RNA signature in glioblastoma multiforme predicts survival. Neurobiology of disease. 2013; 58:123-131.
31. Li J, Chen Z, Tian L, Zhou C, He MY, Gao Y, Wang S, Zhou F, Shi S and Feng X. LncRNA profile study reveals a three-lncRNA signature associated with the survival of patients with oesophageal squamous cell carcinoma. Gut. 2014; 63:1700-1710.
32. Hu Y, Chen H-Y, Yu C-Y, Xu J, Wang J-L, Qian J, Zhang X and Fang J-Y. A long non-coding RNA signature to improve prognosis prediction of colorectal cancer. Oncotarget. 2014; 5:2230. doi: 10.18632/oncotarget.1895.
33. Meng J, Li P, Zhang Q, Yang Z and Fu S. A four-long noncoding RNA signature in predicting breast cancer survival. J Exp Clin Cancer Res. 2014; 33:84.
34. Sun J, Chen X, Wang Z, Guo M, Shi H, Wang X, Cheng L and Zhou M. A potential prognostic long non-coding RNA signature to predict metastasis-free survival of breast cancer patients. Sci Rep. 2015; 5:16553.
35. Liu H, Li J, Koirala P, Ding X, Chen B, Wang Y, Wang Z, Wang C, Zhang X and Mo YY. Long non-coding RNAs as prognostic markers in human breast cancer. Oncotarget.
36. Zhou M, Guo M, He D, Wang X, Cui Y, Yang H, Hao D and Sun J. A potential signature of eight long non-coding RNAs predicts survival in patients with non-small cell lung cancer. Journal of translational medicine. 2015; 13:1-13.
37. Zhou M, Zhao H, Wang Z, Cheng L, Yang L, Shi H, Yang H and Sun J. Identification and validation of potential prognostic lncRNA biomarkers for predicting survival in patients with multiple myeloma. Journal of Experimental & Clinical Cancer Research. 2015; 34:1.
38. Lawrenson K, Spindler T and Gayther SA. A novel long non-coding RNA associated with poor prognosis in epithelial ovarian cancer. Cancer Research. 2014; 74:1497-1497.
39. Qiu J-j, Lin Y-y, Ye L-c, Ding J-x, Feng W-w, Jin H-y, Zhang Y, Li Q and Hua K-q. Overexpression of long noncoding RNA HOTAIR predicts poor patient prognosis and promotes tumor metastasis in epithelial ovarian cancer. Gynecologic oncology. 2014; 134:121-128.
40. Qiu J-J, Ye L-C, Ding J-X, Feng W-W, Jin HY, Zhang Y, Li Q and Hua K-Q. Expression and clinical significance of estrogen-regulated long non-coding RNAs in estrogen receptor a-positive ovarian cancer progression. Oncology reports. 2014; 31:1613-1622.
41. Liu SP, Yang JX, Cao DY and Shen K. Identification of differentially expressed long non-coding RNAs in human ovarian cancer cells with different metastatic potentials. Cancer Biol Med. 2013; 10:138-141.
42. Cheng Z, Guo J, Chen L, Luo N, Yang W and Qu X. A long noncoding RNA AB073614 promotes tumorigenesis and predicts poor prognosis in ovarian cancer. Oncotarget. 2015; 6:25381. doi: 10.18632/oncotarget.4541.
43. Lossos IS, Czerwinski DK, Alizadeh AA, Wechser MA, Tibshirani R, Botstein D and Levy R. Prediction of survival in diffuse large-B-cell lymphoma based on the expression of six genes. New England Journal of Medicine. 2004; 350:1828-1837.
44. Alizadeh AA, Gentles AJ, Alencar AJ, Liu CL, Kohrt HE, Houot R, Goldstein MJ, Zhao S, Natkunam Y and Advani RH. Prediction of survival in diffuse large B-cell lymphoma based on the expression of 2 genes reflecting tumor and microenvironment. Blood. 2011; 118:1350-1358.
45. Yang D, Khan S, Sun Y, Hess K, Shmulevich I, Sood AK and Zhang W. Association of BRCA1 and BRCA2 mutations with survival, chemotherapy sensitivity, and gene mutator phenotype in patients with ovarian cancer. Jama. 2011; 306:1557-1565.
46. Pignata S, Cannella L, Leopardo D, Pisano C, Bruni GS and Facchini G. Chemotherapy in epithelial ovarian cancer. Cancer letters. 2011; 303:73-83.
47. Kang J, D'Andrea AD and Kozono D. A DNA repair pathway-focused score for prediction of outcomes in ovarian cancer treated with platinum-based chemotherapy. Journal of the National Cancer Institute. 2012; 104:670-681.
48. Du Z, Fei T, Verhaak RG, Su Z, Zhang Y, Brown M, Chen Y and Liu XS. Integrative genomic analyses reveal clinically relevant long noncoding RNAs in human cancer. Nature structural & molecular biology. 2013; 20:908-913.
49. Liao Q, Liu C, Yuan X, Kang S, Miao R, Xiao H, Zhao G, Luo H, Bu D and Zhao H. Large-scale prediction of long non-coding RNA functions in a coding-non-coding gene co-expression network. Nucleic acids research. 2011; 39:3864-3878.
50. Paci P, Colombo T and Farina L. Computational analysis identifies a sponge interaction network between long noncoding RNAs and messenger RNAs in human breast cancer. BMC systems biology. 2014; 8:83.
51. Network CGAR. Integrated genomic analyses of ovarian carcinoma. Nature. 2011; 474:609-615.
52. Bonome T, Levine DA, Shih J, Randonovich M, Pise-Masison CA, Bogomolniy F, Ozbun L, Brady J, Barrett JC and Boyd J. A gene signature predicting for survival in suboptimally debulked patients with ovarian cancer. Cancer research. 2008; 68:5478-5486.
53. Spentzos D, Levine DA, Ramoni MF, Joseph M, Gu X, Boyd J, Libermann TA and Cannistra SA. Gene expression signature with independent prognostic significance in epithelial ovarian cancer. Journal of Clinical Oncology. 2004; 22:4700-4710.
54. Yoshihara K, Tajima A, Yahata T, Kodama S, Fujiwara H, Suzuki M, Onishi Y, Hatae M, Sueyoshi K and Fujiwara H. Gene expression profile for predicting survival in advancedstage serous ovarian cancer across two independent datasets. PloS one. 2010; 5:e9615.
55. Verhaak RG, Tamayo P, Yang J-Y, Hubbard D, Zhang H, Creighton CJ, Fereday S, Lawrence M, Carter SL and Mermel CH. Prognostically relevant gene signatures of high-grade serous ovarian carcinoma. The Journal of clinical investigation. 2013; 123:517.
56. Gu Y, Zhang M, Peng F, Fang L, Zhang Y, Liang H, Zhou W, Ao L and Guo Z. The BRCA1/2-directed miRNA signature predicts a good prognosis in ovarian cancer patients with wild-type BRCA1/2. Oncotarget. 2015; 6:2397. doi: 10.18632/oncotarget.2963.
57. Jin N, Wu H, Miao Z, Huang Y, Hu Y, Bi X, Wu D, Qian K, Wang L and Wang C. Network-based survival-associated module biomarker and its crosstalk with cell death genes in ovarian cancer. Sci Rep. 2015; 5:11566.
58. Zhou M, Wang X, Shi H, Cheng L, Wang Z, Zhao H, Yang L and Sun J. Characterization of long non-coding RNAassociated ceRNA network to reveal potential prognostic lncRNA biomarkers in human ovarian cancer. Oncotarget.doi: 10.18632/oncotarget.7181.
59. Liu B, Fang L, Long R, Lan X and Chou K-C. iEnhancer-2L: a two-layer predictor for identifying enhancers and their strength by pseudo k-tuple nucleotide composition. Bioinformatics. 2016; 32:362-369.
60. Liu B, Fang L, Liu F, Wang X, Chen J and Chou K-C. Identification of real microRNA precursors with a pseudo structure status composition approach. PloS one. 2015; 10:e0121501.
61. Ries LAG. Ovarian cancer: survival and treatment differences by age. Cancer. 1993; 71:524-529.
62. Vollebergh MA, Jonkers J and Linn SC. Genomic instability in breast and ovarian cancers: translation into clinical predictive biomarkers. Cellular and Molecular Life Sciences. 2012; 69:223-245.
63. Fong PC, Yap TA, Boss DS, Carden CP, Mergui-Roelvink M, Gourley C, De Greve J, Lubinski J, Shanley S and Messiou C. Poly (ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. Journal of Clinical Oncology. 2010; 28:2512-2519.
64. Lu J, Wu D, Li C, Zhou M and Hao D. Correlation between gene expression and mutator phenotype predicts homologous recombination deficiency and outcome in ovarian cancer. Journal of Molecular Medicine. 2014; 92:1159-1168.
65. Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, Aken BL, Barrell D, Zadissa A and Searle S. GENCODE: the reference human genome annotation for The ENCODE Project. Genome research. 2012; 22:1760-1774.
66. Xie C, Yuan J, Li H, Li M, Zhao G, Bu D, Zhu W, Wu W, Chen R and Zhao Y. NONCODEv4: exploring the world of long non-coding RNA genes. Nucleic acids research. 2014; 42:D98-D103.
67. Volders P-J, Verheggen K, Menschaert G, Vandepoele K, Martens L, Vandesompele J and Mestdagh P. An update on LNCipedia: a database for annotated human lncRNA sequences. Nucleic acids research. 2015; 43:D174-D180.
68. Chen S, Li P, Xiao B and Guo J. Long noncoding RNA HMlincRNA717 and AC130710 have been officially named as gastric cancer associated transcript 2 (GACAT2) and GACAT3, respectively. Tumor Biology. 2014; 35:8351-8352.
69. Guo X, Gao L, Liao Q, Xiao H, Ma X, Yang X, Luo H, Zhao G, Bu D and Jiao F. Long non-coding RNAs function annotation: a global prediction method based on bi-colored networks. Nucleic acids research. 2013; 41:e35-e35.
70. Ma H, Hao Y, Dong X, Gong Q, Chen J, Zhang J and Tian W. Molecular mechanisms and function prediction of long noncoding RNA. The ScientificWorldJournal. 2012; 2012:541786.
71. Sodek KL, Evangelou AI, Ignatchenko A, Agochiya M, Brown TJ, Ringuette MJ, Jurisica I and Kislinger T. Identification of pathways associated with invasive behavior by ovarian cancer cells using multidimensional protein identification technology (MudPIT). Molecular BioSystems. 2008; 4:762-773.
72. Dhillon A, Hagan S, Rath O and Kolch W. MAP kinase signalling pathways in cancer. Oncogene. 2007; 26:3279-3290.
73. Seidman R, Gitelman I, Sagi O, Horwitz SB and Wolfson M. The role of ERK 1/2 and p38 MAP-kinase pathways in taxol-induced apoptosis in human ovarian carcinoma cells. Experimental cell research. 2001; 268:84-92.
74. Dolezal S, Hester S, Kirby PS, Nairn A, Pierce M and Abbott KL. Elevated levels of glycosylphosphatidylinositol (GPI) anchored proteins in plasma from human cancers detected by C. septicum alpha toxin. Cancer biomarkers: section A of Disease markers. 2014; 14:55.
75. Samuel P, Pink RC, Caley DP, Currie J, Brooks SA and Carter D. Over-expression of miR-31 or loss of KCNMA1 leads to increased cisplatin resistance in ovarian cancer cells. Tumour biology. 2015.
76. Guo S-H, Deng E-Z, Xu L-Q, Ding H, Lin H, Chen W and Chou K-C. iNuc-PseKNC: a sequence-based predictor for predicting nucleosome positioning in genomes with pseudo k-tuple nucleotide composition. Bioinformatics. 2014; 30:1522-1529.
77. Chou K-C. Impacts of bioinformatics to medicinal chemistry. Medicinal Chemistry. 2015; 11:218-234.
78. Guo Q, Cheng Y, Liang T, He Y, Ren C, Sun L and Zhang G. Comprehensive analysis of lncRNA-mRNA co-expression patterns identifies immune-associated lncRNA biomarkers in ovarian cancer malignant progression. Sci Rep. 2015; 5:17683.
79. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R and Larsson E. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Science signaling. 2013; 6:pl1.
80. Johnson WE, Li C and Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics. 2007; 8:118-127.
81. Therneau T. A package for survival analysis in S. R package version 2.37-4. URL http://CRANR-projectorg/package=survivalBox. 2013; 980032:23298-20032.
82. Heagerty PJ, Lumley T and Pepe MS. Time -dependent ROC curves for censored survival data and a diagnostic marker. Biometrics. 2000; 56:337-344.
83. Heagerty PJ and Zheng Y. Survival model predictive accuracy and ROC curves. Biometrics. 2005; 61:92-105.
84. Huang DW, Sherman BT and Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols. 2008; 4:44-57.
85. Huang DW, Sherman BT and Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic acids research. 2009; 37:1-13.
86. Merico D, Isserlin R, Stueker O, Emili A and Bader GD. Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PloS one. 2010; 5:e13984.