Hypoxia-induced lncRNA-NUTF2P3-001 contributes to tumorigenesis of pancreatic cancer by derepressing the miR-3923/KRAS pathway

Oncotarget

Volumn 7, Issue 5, 2016, Pages 6000-6014

  Li, Xiang ^a   Deng, Shi Jiang ^a   Zhu, Shuai ^a   Jin, Yan ^a   Cui, Shi Peng ^a   Chen, Jing Yuan ^a   Xiang, Cheng ^a   Li, Qun Ying ^a   He, Chi ^a   Zhao, Shu Feng ^a   Chen, Heng Yu ^a   Niu, Yi ^a   Liu, Yang ^a   Deng, Shi Chang ^a   Wang, Chun You ^a   Zhao, Gang ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

HIF 1 ; KRAS; LncRNAs; miRNAs; Pancreatic cancer

Indexed keywords

COBALT CHLORIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LONG UNTRANSLATED RNA; LONG UNTRANSLATED RNA NUTF2P3 001; MICRORNA; MICRORNA 3923; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; KRAS PROTEIN, HUMAN; PROTEIN P21;

3' UNTRANSLATED REGION; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING COMPETITION; CANCER CELL; CANCER PROGNOSIS; CANCER STAGING; CARCINOGENESIS; CELL INVASION; CELL PROLIFERATION; CHRONIC PANCREATITIS; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; LUCIFERASE ASSAY; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; ONCOGENE K RAS; PANCREAS CANCER; PROMOTER REGION; RNA BINDING; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL HYPOXIA; GENETICS; METABOLISM; NUDE MOUSE; PANCREAS TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CARCINOGENESIS; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS P21(RAS); RNA, LONG NONCODING;

EID: 84958092647     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6830     Document Type: Article

References (45)

1. Liu Q, Huang J, Zhou N, Zhang Z, Zhang A, Lu Z, Wu F, Mo YY. LncRNA loc285194 is a p53-regulated tumor suppressor. Nucleic Acids Res. 2013; 41:4976-4987.
2. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermüller J, Hofacker IL, Bell I, Cheung E, Drenkow J, et al. RNA Maps Reveal New RNA Classes and a Possible Function for Pervasive Transcription. Science. 2007; 316:1484-1488.
3. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov GK, Khatun J, et al. Landscape of transcription in human cells. Nature. 2012; 489:101-108.
4. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell. 2011; 43:904-914.
5. Takayama K, Horie-Inoue K, Katayama S, Suzuki T, Tsutsumi S, Ikeda K, Urano T, Fujimura T, Takagi K, Takahashi S, Homma Y, Ouchi Y, Aburatani H, et al. Androgen-responsive long noncoding RNA CTBP1-AS promotes prostate cancer. EMBO J. 2013; 32:1665-1680.
6. Yang X, Song JH, Cheng Y, Wu W, Bhagat T, Yu Y, Abraham JM, Ibrahim S, Ravich W, Roland BC, Khashab M, Singh VK, Shin EJ, et al. Long non-coding RNA HNF1A-AS1 regulates proliferation and migration in oesophageal adenocarcinoma cells. Gut. 2014; 63:881-890.
7. Yang F, Zhang L, Huo XS, Yuan JH, Xu D, Yuan SX, Zhu N, Zhou WP, Yang GS, Wang YZ, Shang JL, Gao CF, Zhang FR, et al. Long noncoding RNA high expression in hepatocellular carcinoma facilitates tumor growth through enhancer of zeste homolog 2 in humans. Hepatology. 2011; 54:1679-1689.
8. Quagliata L, Matter MS, Piscuoglio S, Arabi L, Ruiz C, Procino A, Kovac M, Moretti F, Makowska Z, Boldanova T, Andersen JB, Hämmerle M, Tornillo L, et al. Long noncoding RNA HOTTIP/HOXA13 expression is associated with disease progression and predicts outcome in hepatocellular carcinoma patients. Hepatology. 2014; 59:911-923.
9. Tahira AC, Kubrusly MS, Faria MF, Dazzani B, Fonseca RS, Maracaja-Coutinho V, Verjovski-Almeida S, Machado MC, Reis EM. Long noncoding intronic RNAs are differentially expressed in primary and metastatic pancreatic cancer. Mol Cancer. 2011; 10:141.
10. Peng W, Gao W, Feng J. Long noncoding RNA HULC is a novel biomarker of poor prognosis in patients with pancreatic cancer. Med Oncol. 2014; 31:346.
11. Ding YC, Yu W, Ma C, Wang Q, Huang CS, Huang T. Expression of long non-coding RNA LOC285194 and its prognostic significance in human pancreatic ductal adenocarcinoma. Int J Clin Exp Pathol. 2014; 7:8065-70.
12. Pang EJ, Yang R, Fu XB, Liu YF. Overexpression of long non-coding RNA MALAT1 is correlated with clinical progression and unfavorable prognosis in pancreatic cancer. Tumour Biol. 2015; 36:2403-7.
13. Li Z, Zhao X, Zhou Y, Liu Y, Zhou Q, Ye H, Wang Y, Zeng J, Song Y, Gao W, Zheng S, Zhuang B, Chen H, et al. The long non-coding RNA HOTTIP promotes progression and gemcitabine resistance by regulating HOXA13 in pancreatic cancer. J Transl Med. 2015; 13:84.
14. Sun YW, Chen YF, Li J, Huo YM, Liu DJ, Hua R, Zhang JF, Liu W, Yang JY, Fu XL, Yan T, Hong J, Cao H. A novel long non-coding RNA ENST00000480739 suppresses tumour cell invasion by regulating OS-9 and HIF-1a in pancreatic ductal adenocarcinoma. Br J Cancer. 2014; 111:2131-41.
15. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, Hong SM, Fu B, Lin MT, et al. Core Signaling Pathways in Human Pancreatic Cancers Revealed by Global Genomic Analyses. Science. 2008; 321:1801-1806.
16. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature. 2010; 465:1033-1038.
17. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell. 2011; 147:358-369.
18. Wang Y, Xu Z, Jiang J, Xu C, Kang J, Xiao L, Wu M, Xiong J, Guo X, Liu H. Endogenous miRNA sponge lincRNA-RoR regulates Oct4, Nanog, and Sox2 in human embryonic stem cell self-renewal. Dev Cell. 2013; 25:69-80.
19. Kranenburg O. The KRAS oncogene: past, present, and future. Biochim Biophys Acta. 2005; 1756:81-82.
20. Tam IY, Chung LP, Suen WS, Wang E, Wong MC, Ho KK, Lam WK, Chiu SW, Girard L, Minna JD, Gazdar AF, Wong MP. Distinct epidermal growth factor receptor and KRAS mutation patterns in non-small cell lung cancer patients with different tobacco exposure and clinicopathologic features. Clin Cancer Res. 2006; 12:1647-1653.
21. Kong B, Qia C, Erkan M, Kleeff J, Michalski CW. Overview on how oncogenic Kras promotes pancreatic carcinogenesis by inducing low intracellular ROS levels. Front Physiol. 2013; 4:246.
22. Collins MA, Bednar F, Zhang Y, Brisset JC, Galbán S, Galbán CJ, Rakshit S, Flannagan KS, Adsay NV, Pasca di Magliano M. Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice. J Clin Invest. 2012; 122:639-653.
23. Zorde Khvalevsky E, Gabai R, Rachmut IH, Horwitz E, Brunschwig Z, Orbach A, Shemi A, Golan T, Domb AJ, Yavin E, Giladi H, Rivkin L, Simerzin A, et al. Mutant KRAS is a druggable target for pancreatic cancer. Proc Natl Acad Sci USA. 2013; 110:20723-20728.
24. Yu S, Lu Z, Liu C, Meng Y, Ma Y, Zhao W, Liu J, Yu J, Chen J. miRNA-96 suppresses KRAS and functions as a tumor suppressor gene in pancreatic cancer. Cancer Res. 2010; 70:6015-6025.
25. Zhao WG, Yu SN, Lu ZH, Ma YH, Gu YM, Chen J. The miR-217 microRNA functions as a potential tumor suppressor in pancreatic ductal adenocarcinoma by targeting KRAS. Carcinogenesis. 2010; 31:1726-1733.
26. Gómez-Maldonado L, Tiana M, Roche O, Prado-Cabrero A, Jensen L, Fernandez-Barral A, Guijarro-Muñoz I, Favaro E, Moreno-Bueno G, Sanz L, Aragones J, Harris A, Volpert O, et al. EFNA3 long noncoding RNAs induced by hypoxia promote metastatic dissemination. Oncogene. 2014; 0. doi: 10.1038/onc.2014.200.
27. Xue M, Li X, Li Z, Chen W. Urothelial carcinoma associated 1 is a hypoxia-inducible factor-1alpha-targeted long noncoding RNA that enhances hypoxic bladder cancer cell proliferation, migration, and invasion. Tumour Biol. 2014; 35:6901-6912.
28. Takahashi K, Yan IK, Haga H, Patel T. Modulation of hypoxia-signaling pathways by extracellular linc-RoR. J Cell Sci. 2014; 127:1585-1594.
29. Brown JM, Giaccia AJ, The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res. 1998; 58:1408-1416.
30. Zeng Y, Cullen BR. RNA interference in human cells is restricted to the cytoplasm. RNA. 2002; 8:855-60.
31. Chiu YL, Ali A, Chu CY, Cao H, Rana TM. Visualizing a correlation between siRNA localization, cellular uptake, and RNAi in living cells. Chem Biol. 2004; 11:1165-75.
32. Karreth FA, Tay Y, Perna D, Ala U, Tan SM, Rust AG, DeNicola G, Webster KA, Weiss D, Perez-Mancera PA, Krauthammer M, Halaban R, Provero P, 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. Sumazin P, Yang X, Chiu HS, Chung WJ, Iyer A, Llobet-Navas D, Rajbhandari P, Bansal M, Guarnieri P, Silva J, Califano A. An extensive microRNA-mediated network of RNA-RNA interactions regulates established oncogenic pathways in glioblastoma. Cell. 2011; 147:370-381.
34. Hao J. HIF-1 is a critical target of pancreatic cancer. Oncoimmunology. 2015; 4:e1026535.
35. Gao C, Li S, Zhao T, Chen J, Ren H, Zhang H, Wang X, Lang M, Liu J, Gao S, Zhao X, Sheng J, Yuan Z, et al. SCF, regulated by HIF-1a, promotes pancreatic ductal adenocarcinoma cell progression. PLoS One. 2015; 10:e0121338.
36. Shan T, Ma J, Ma Q, Guo K, Guo J, Li X, Li W, Liu J, Huang C, Wang F, Wu E. β2-AR-HIF-1a: a novel regulatory axis for stress-induced pancreatic tumor growth and angiogenesis. Curr Mol Med. 2013; 13:1023-1034.
37. Koda M, Sulkowska M, Wincewicz A, Kanczuga-Koda L, Musiatowicz B, Szymanska M, Sulkowski S. Expression of leptin, leptin receptor, and hypoxia-inducible factor 1 alpha in human endometrial cancer. Ann N Y Acad Sci. 2007; 1095:90-98.
38. Yang F, Zhang H, Mei Y, Wu M. Reciprocal regulation of HIF-1alpha and lincRNA-p21 modulates the Warburg effect. Mol Cell 2014; 53:88-100.
39. Yang F, Huo XS, Yuan SX, Zhang L, Zhou WP, Wang F, Sun SH. Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis. Mol Cell. 2013; 49:1083-1096.
40. Zhao G, Wang B, Liu Y, Zhang JG, Deng SC, Qin Q, Tian K, Li X, Zhu S, Niu Y, Gong Q, Wang CY. miRNA-141, downregulated in pancreatic cancer, inhibits cell proliferation and invasion by directly targeting MAP4K4. Mol Cancer Ther. 2013; 12:2569-80.
41. Wu D, Yotnda P. Induction and testing of hypoxia in cell culture. J Vis Exp. 2011; pii:2899.
42. Zhao G, Cui J, Zhang JG, Qin Q, Chen Q, Yin T, Deng SC, Liu Y, Liu L, Wang B, Tian K, Wang GB, Wang CY. SIRT1 RNAi knockdown induces apoptosis and senescence, inhibits invasion and enhances chemosensitivity in pancreatic cancer cells. Gene Ther. 2011; 18:920-928.
43. Albini A, Benelli R. The chemoinvasion assay: a method to assess tumor and endothelial cell invasion and its modulation. Nat Protoc. 2007; 2:504-511.
44. Fernandis AZ, Prasad A, Band H, Klösel R, Ganju RK. Regulation of CXCR4-mediated chemotaxis and chemoinvasion of breast cancer cells. Oncogene. 2004; 23:157-167.
45. Zhao G, Zhang JG, Liu Y, Qin Q, Wang B, Tian K, Liu L, Li X, Niu Y, Deng SC, Wang CY. miR-148b functions as a tumor suppressor in pancreatic cancer by targeting AMPKalpha1. Mol Cancer Ther. 2013; 12:83-93.