MicroRNA-301a-3p promotes pancreatic cancer progression via negative regulation of SMAD4

Oncotarget

Volumn 6, Issue 25, 2015, Pages 21046-21063

  Xia, Xiang ^a   Zhang, Kundong ^a   Cen, Gang ^a   Jiang, Tao ^a   Cao, Jun ^a   Huang, Kejian ^a   Huang, Chen ^a   Zhao, Qian ^b   Qiu, Zhengjun ^a  

^a SHANGHAI FIRST PEOPLE S HOSPITAL   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

miR 301a 3p; Pancreatic ductal adenocarcinoma; Prognosis; SMAD4; Xenograft tumor

Indexed keywords

MICRORNA; MICRORNA 301A-3P; SMAD4 PROTEIN; UNCLASSIFIED DRUG; MIRN301 MICRORNA, HUMAN; SMAD4 PROTEIN, HUMAN;

ADULT; ADVANCED CANCER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CARCINOGENICITY; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; OVERALL SURVIVAL; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PANCREATIC CANCER CELL LINE; PANCREATICODUODENECTOMY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMAD4 GENE; TISSUE MICROARRAY; TUMOR XENOGRAFT; AGED; ANIMAL; CANCER TRANSPLANTATION; CELL MOTION; CELL PROLIFERATION; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; NUDE MOUSE; PANCREAS CARCINOMA; PANCREAS TUMOR; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; TUMOR INVASION;

AGED; ANIMALS; CARCINOMA, PANCREATIC DUCTAL; CELL MOVEMENT; CELL PROLIFERATION; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LYMPHATIC METASTASIS; MALE; MICE; MICE, NUDE; MICRORNAS; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; PANCREATIC NEOPLASMS; PANCREATICODUODENECTOMY; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; SMAD4 PROTEIN; TISSUE ARRAY ANALYSIS;

EID: 84940785951     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4124     Document Type: Article

References (42)

1. R. Siegel, E. Ward, O. Brawley, A. Jemal, Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 61 (2011) 212-236.
2. M. Wagner, C. Redaelli, M. Lietz, C.A. Seiler, H. Friess, M.W. Buchler, Curative resection is the single most important factor determining outcome in patients with pancreatic adenocarcinoma. Br J Surg 91 (2004) 586-594.
3. A. Stathis, M.J. Moore, Advanced pancreatic carcinoma: current treatment and future challenges. Nat Rev Clin Oncol 7 (2010) 163-172.
4. T. Muniraj, P.A. Jamidar, H.R. Aslanian, Pancreatic cancer: a comprehensive review and update. Dis Mon 59 (2013) 368-402.
5. O.P. Jones, J.D. Melling, P. Ghaneh, Adjuvant therapy in pancreatic cancer. World J Gastroenterol 20 (2014) 14733-14746.
6. A. Jemal, R. Siegel, E. Ward, Y. Hao, J. Xu, M.J. Thun, Cancer statistics, 2009. CA Cancer J Clin 59 (2009) 225-249.
7. D. Su, K. Yamaguchi, M. Tanaka, The characteristics of disseminated tumor cells in pancreatic cancer: a black box needs to be explored. Pancreatology 5 (2005) 316-324; discussion 324.
8. N.C. Lau, L.P. Lim, E.G. Weinstein, D.P. Bartel, An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294 (2001) 858-862.
9. M. Lagos-Quintana, R. Rauhut, W. Lendeckel, T. Tuschl, Identification of novel genes coding for small expressed RNAs. Science 294 (2001) 853-858.
10. D.P. Bartel, MicroRNAs: target recognition and regulatory functions. Cell 136 (2009) 215-233.
11. S.K. Shenouda, S.K. Alahari, MicroRNA function in cancer: oncogene or a tumor suppressor? Cancer Metastasis Rev 28 (2009) 369-378.
12. M.M. Tsai, C.S. Wang, C.Y. Tsai, C.Y. Chen, H.C. Chi, Y.H. Tseng, P.J. Chung, Y.H. Lin, I.H. Chung, K.H. Lin, MicroRNA-196a/-196b promote cell metastasis via negative regulation of radixin in human gastric cancer. Cancer Lett 351 (2014) 222-231.
13. W. Shi, K. Gerster, N.M. Alajez, J. Tsang, L. Waldron, M. Pintilie, A.B. Hui, J. Sykes, C. P'ng, N. Miller, D. McCready, A. Fyles, F.F. Liu, MicroRNA-301 mediates proliferation and invasion in human breast cancer. Cancer Res 71 (2011) 2926-2937.
14. M. Wang, C. Li, B. Yu, L. Su, J. Li, J. Ju, Y. Yu, Q. Gu, Z. Zhu, B. Liu, Overexpressed miR-301a promotes cell proliferation and invasion by targeting RUNX3 in gastric cancer. J Gastroenterol 48 (2013) 1023-1033.
15. P. Zhou, W. Jiang, L. Wu, R. Chang, K. Wu, Z. Wang, miR-301a is a candidate oncogene that targets the homeobox gene Gax in human hepatocellular carcinoma. Dig Dis Sci 57 (2012) 1171-1180.
16. H. Yamaguchi, T. Kojima, T. Ito, Y. Kimura, M. Imamura, S. Son, J. Koizumi, M. Murata, M. Nagayama, T. Nobuoka, S. Tanaka, K. Hirata, N. Sawada, Transcriptional control of tight junction proteins via a protein kinase C signal pathway in human telomerase reverse transcriptase-transfected human pancreatic duct epithelial cells. Am J Pathol 177 (2010) 698-712.
17. L. Fang, H. Li, L. Wang, J. Hu, T. Jin, J. Wang, B.B. Yang, MicroRNA-17-5p promotes chemotherapeutic drug resistance and tumour metastasis of colorectal cancer by repressing PTEN expression. Oncotarget 5 (2014) 2974-2987.
18. Z. Hua, Y.C. Zhang, X.M. Hu, Z.G. Jia, Loss of DPC4 expression and its correlation with clinicopathological parameters in pancreatic carcinoma. World J Gastroenterol 9 (2003) 2764-2767.
19. A. Blackford, O.K. Serrano, C.L. Wolfgang, G. Parmigiani, S. Jones, X. Zhang, D.W. Parsons, J.C. Lin, R.J. Leary, J.R. Eshleman, M. Goggins, E.M. Jaffee, C.A. Iacobuzio-Donahue, A. Maitra, J.L. Cameron, K. Olino, R. Schulick, J. Winter, J.M. Herman, D. Laheru, A.P. Klein, B. Vogelstein, K.W. Kinzler, V.E. Velculescu, R.H. Hruban, SMAD4 gene mutations are associated with poor prognosis in pancreatic cancer. Clin Cancer Res 15 (2009) 4674-4679.
20. L. Levy, C.S. Hill, Smad4 dependency defines two classes of transforming growth factor {beta} (TGF-{beta}) target genes and distinguishes TGF-{beta}-induced epithelial-mesenchymal transition from its antiproliferative and migratory responses. Mol Cell Biol 25 (2005) 8108-8125.
21. S.B. Jakowlew, Transforming growth factor-beta in cancer and metastasis. Cancer Metastasis Rev 25 (2006) 435-457.
22. M.S. Ebert, P.A. Sharp, Roles for microRNAs in conferring robustness to biological processes. Cell 149 (2012) 515-524.
23. A.L. Kasinski, F.J. Slack, Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat Rev Cancer 11 (2011) 849-864.
24. C. Stahlhut, F.J. Slack, MicroRNAs and the cancer phenotype: profiling, signatures and clinical implications. Genome Med 5 (2013) 111.
25. G. Cao, B. Huang, Z. Liu, J. Zhang, H. Xu, W. Xia, J. Li, S. Li, L. Chen, H. Ding, Q. Zhao, M. Fan, B. Shen, N. Shao, Intronic miR-301 feedback regulates its host gene, ska2, in A549 cells by targeting MEOX2 to affect ERK/CREB pathways. Biochem Biophys Res Commun 396 (2010) 978-982.
26. X. Ma, L.E. Becker Buscaglia, J.R. Barker, Y. Li, MicroRNAs in NF-kappaB signaling. J Mol Cell Biol 3 (2011) 159-166.
27. E.J. Lee, Y. Gusev, J. Jiang, G.J. Nuovo, M.R. Lerner, W.L. Frankel, D.L. Morgan, R.G. Postier, D.J. Brackett, T.D. Schmittgen, Expression profiling identifies microRNA signature in pancreatic cancer. Int J Cancer 120 (2007) 1046-1054.
28. Z. Lu, Y. Li, A. Takwi, B. Li, J. Zhang, D.J. Conklin, K.H. Young, R. Martin, miR-301a as an NF-kappaB activator in pancreatic cancer cells. EMBO J 30 (2011) 57-67.
29. X.D. Xu, X.J. He, H.Q. Tao, W. Zhang, Y.Y. Wang, Z.Y. Ye, Z.S. Zhao, Abnormal expression of miR-301a in gastric cancer associated with progression and poor prognosis. J Surg Oncol 108 (2013) 197-202.
30. B.P. Lewis, C.B. Burge, D.P. Bartel, Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120 (2005) 15-20.
31. L. Liu, J. Nie, L. Chen, G. Dong, X. Du, X. Wu, Y. Tang, W. Han, The oncogenic role of microRNA-130a/301a/454 in human colorectal cancer via targeting Smad4 expression. PLoS One 8 (2013) e55532.
32. Y. Shi, J. Massague, Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113 (2003) 685-700.
33. S. Zhao, K. Venkatasubbarao, J.W. Lazor, J. Sperry, C. Jin, L. Cao, J.W. Freeman, Inhibition of STAT3 Tyr705 phosphorylation by Smad4 suppresses transforming growth factor beta-mediated invasion and metastasis in pancreatic cancer cells. Cancer Res 68 (2008) 4221-4228.
34. D.G. Duda, M. Sunamura, L.P. Lefter, T. Furukawa, T. Yokoyama, T. Yatsuoka, T. Abe, H. Inoue, F. Motoi, S. Egawa, S. Matsuno, A. Horii, Restoration of SMAD4 by gene therapy reverses the invasive phenotype in pancreatic adenocarcinoma cells. Oncogene 22 (2003) 6857-6864.
35. R.A. Smith, J. Tang, C. Tudur-Smith, J.P. Neoptolemos, P. Ghaneh, Meta-analysis of immunohistochemical prognostic markers in resected pancreatic cancer. Br J Cancer 104 (2011) 1440-1451.
36. P. Singh, R. Srinivasan, J.D. Wig, SMAD4 genetic alterations predict a worse prognosis in patients with pancreatic ductal adenocarcinoma. Pancreas 41 (2012) 541-546.
37. Y. Saiki, A. Horii, Molecular pathology of pancreatic cancer. Pathol Int 64 (2014) 10-19.
38. C.A. Iacobuzio-Donahue, J. Song, G. Parmiagiani, C.J. Yeo, R.H. Hruban, S.E. Kern, Missense mutations of MADH4: characterization of the mutational hot spot and functional consequences in human tumors. Clin Cancer Res 10 (2004) 1597-1604.
39. M.K. Wendt, M. Tian, W.P. Schiemann, Deconstructing the mechanisms and consequences of TGF-beta-induced EMT during cancer progression. Cell Tissue Res 347 (2012) 85-101.
40. G. Genovese, A. Ergun, S.A. Shukla, B. Campos, J. Hanna, P. Ghosh, S.N. Quayle, K. Rai, S. Colla, H. Ying, C.J. Wu, S. Sarkar, Y. Xiao, J. Zhang, H. Zhang, L. Kwong, K. Dunn, W.R. Wiedemeyer, C. Brennan, H. Zheng, D.L. Rimm, J.J. Collins, L. Chin, microRNA regulatory network inference identifies miR-34a as a novel regulator of TGF-beta signaling in glioblastoma. Cancer Discov 2 (2012) 736-749.
41. B. Xiao, E.D. Zhu, N. Li, D.S. Lu, W. Li, B.S. Li, Y.L. Zhao, X.H. Mao, G. Guo, P.W. Yu, Q.M. Zou, Increased miR-146a in gastric cancer directly targets SMAD4 and is involved in modulating cell proliferation and apoptosis. Oncol Rep 27 (2012) 559-566.
42. Y. Zhang, K.J. Fan, Q. Sun, A.Z. Chen, W.L. Shen, Z.H. Zhao, X.F. Zheng, X. Yang, Functional screening for miRNAs targeting Smad4 identified miR-199a as a negative regulator of TGF-beta signalling pathway. Nucleic Acids Res 40 (2012) 9286-9297.