MicroRNA-323-3p inhibits cell invasion and metastasis in pancreatic ductal adenocarcinoma via direct suppression of SMAD2 and SMAD3

Oncotarget

Volumn 7, Issue 12, 2016, Pages 14912-14924

  Wang, Chunyou ^a   Liu, Pian ^a   Wu, Heshui ^a   Cui, Pengfei ^a   Li, Yongfeng ^a   Liu, Yao ^a   Liu, Zhiqiang ^a   Gou, Shanmiao ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

miR 323 3p; Pancreatic ductal adenocarcinoma; SMAD2; SMAD3

Indexed keywords

MICRORNA; MICRORNA 323 3P; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; MIRN323 MICRORNA, HUMAN; SMAD2 PROTEIN, HUMAN; SMAD3 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG METASTASIS; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; OVERALL SURVIVAL; PANCREAS ADENOCARCINOMA; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SURVIVAL TIME; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; CANCER STAGING; CELL MOTION; CELL PROLIFERATION; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; METABOLISM; NUDE MOUSE; PANCREAS CARCINOMA; PANCREAS TUMOR; PATHOLOGY; PROGNOSIS; SECONDARY; SURVIVAL RATE; TUMOR CELL CULTURE;

ANIMALS; APOPTOSIS; CARCINOMA, PANCREATIC DUCTAL; CELL MOVEMENT; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; NEOPLASM STAGING; PANCREATIC NEOPLASMS; PROGNOSIS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; SURVIVAL RATE; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84962821750     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7482     Document Type: Article

References (46)

1. Siegel R, Ma J, Zou Z and Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014; 64:9-29.
2. Muniraj T, Jamidar PA and Aslanian HR. Pancreatic cancer: a comprehensive review and update. Disease-a-month. 2013; 59:368-402.
3. Maitra A and Hruban RH. Pancreatic cancer. Annual review of pathology. 2008; 3:157-188.
4. Stathis A and Moore MJ. Advanced pancreatic carcinoma: current treatment and future challenges. Nature reviews Clinical oncology. 2010; 7:163-172.
5. Wrana JL, Attisano L, Wieser R, Ventura F and Massague J. Mechanism of activation of the TGF-beta receptor. Nature. 1994; 370:341-347.
6. Drabsch Y and ten Dijke P. TGF-beta signalling and its role in cancer progression and metastasis. Cancer metastasis reviews. 2012; 31:553-568.
7. Levy L and Hill CS. Alterations in components of the TGF-beta superfamily signaling pathways in human cancer. Cytokine & growth factor reviews. 2006; 17:41-58.
8. Wrighton KH, Lin X and Feng XH. Phospho-control of TGF-beta superfamily signaling. Cell research. 2009; 19:8-20.
9. Massague J and Gomis RR. The logic of TGFbeta signaling. FEBS letters. 2006; 580:2811-2820.
10. Miyazono K, Suzuki H and Imamura T. Regulation of TGF-beta signaling and its roles in progression of tumors. Cancer science. 2003; 94:230-234.
11. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F and Nieto MA. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nature cell biology. 2000; 2:76-83.
12. Savagner P, Yamada KM and Thiery JP. The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition. The Journal of cell biology. 1997; 137:1403-1419.
13. Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, Mareel M, Huylebroeck D and van Roy F. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Molecular cell. 2001; 7:1267-1278.
14. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A and Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004; 117:927-939.
15. Mani SA, Yang J, Brooks M, Schwaninger G, Zhou A, Miura N, Kutok JL, Hartwell K, Richardson AL and Weinberg RA. Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104:10069-10074.
16. Stankic M, Pavlovic S, Chin Y, Brogi E, Padua D, Norton L, Massague J and Benezra R. TGF-beta-Id1 signaling opposes Twist1 and promotes metastatic colonization via a mesenchymal-to-epithelial transition. Cell reports. 2013; 5:1228-1242.
17. Yuan JH, Yang F, Wang F, Ma JZ, Guo YJ, Tao QF, Liu F, Pan W, Wang TT, Zhou CC, Wang SB, Wang YZ, Yang Y, Yang N, Zhou WP, Yang GS, et al. A long noncoding RNA activated by TGF-beta promotes the invasion-metastasis cascade in hepatocellular carcinoma. Cancer cell. 2014; 25:666-681.
18. Papageorgis P, Lambert AW, Ozturk S, Gao F, Pan H, Manne U, Alekseyev YO, Thiagalingam A, Abdolmaleky HM, Lenburg M and Thiagalingam S. Smad signaling is required to maintain epigenetic silencing during breast cancer progression. Cancer research. 2010; 70:968-978.
19. Culhaci N, Sagol O, Karademir S, Astarcioglu H, Astarcioglu I, Soyturk M, Oztop I and Obuz F. Expression of transforming growth factor-beta-1 and p27Kip1 in pancreatic adenocarcinomas: relation with cell-cycle-associated proteins and clinicopathologic characteristics. BMC cancer. 2005; 5:98.
20. Teraoka H, Sawada T, Yamashita Y, Nakata B, Ohira M, Ishikawa T, Nishino H and Hirakawa K. TGF-beta1 promotes liver metastasis of pancreatic cancer by modulating the capacity of cellular invasion. International journal of oncology. 2001; 19:709-715.
21. Friess H, Yamanaka Y, Buchler M, Ebert M, Beger HG, Gold LI and Korc M. Enhanced expression of transforming growth factor beta isoforms in pancreatic cancer correlates with decreased survival. Gastroenterology. 1993; 105:1846-1856.
22. Melisi D, Ishiyama S, Sclabas GM, Fleming JB, Xia Q, Tortora G, Abbruzzese JL and Chiao PJ. LY2109761, a novel transforming growth factor beta receptor type I and type II dual inhibitor, as a therapeutic approach to suppressing pancreatic cancer metastasis. Molecular cancer therapeutics. 2008; 7:829-840.
23. Gaspar NJ, Li L, Kapoun AM, Medicherla S, Reddy M, Li G, O'Young G, Quon D, Henson M, Damm DL, Muiru GT, Murphy A, Higgins LS, Chakravarty S and Wong DH. Inhibition of transforming growth factor beta signaling reduces pancreatic adenocarcinoma growth and invasiveness. Molecular pharmacology. 2007; 72:152-161.
24. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136:215-233.
25. Nana-Sinkam SP, Fabbri M and Croce CM. MicroRNAs in cancer: personalizing diagnosis and therapy. Annals of the New York Academy of Sciences. 2010; 1210:25-33.
26. Chow JY, Quach KT, Cabrera BL, Cabral JA, Beck SE and Carethers JM. RAS/ERK modulates TGFbeta-regulated PTEN expression in human pancreatic adenocarcinoma cells. Carcinogenesis. 2007; 28:2321-2327.
27. Fernandez-Zapico ME and Ellenrieder V. NFAT transcription factors, the potion mediating "Dr. Jekill-Mr. Hyde" transformation of the TGFbeta pathway in cancer cells. Cell Cycle. 2010; 9:3838-3839.
28. Ungefroren H, Sebens S, Giehl K, Helm O, Groth S, Fandrich F, Rocken C, Sipos B, Lehnert H and Gieseler F. Rac1b negatively regulates TGF-beta1-induced cell motility in pancreatic ductal epithelial cells by suppressing Smad signalling. Oncotarget. 2014; 5:277-290. doi: 10.18632/oncotarget.1696.
29. Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nature reviews Genetics. 2009; 10:704-714.
30. Dalmay T and Edwards DR. MicroRNAs and the hallmarks of cancer. Oncogene. 2006; 25:6170-6175.
31. Salek C, Benesova L, Zavoral M, Nosek V, Kasperova L, Ryska M, Strnad R, Traboulsi E and Minarik M. Evaluation of clinical relevance of examining K-ras, p16 and p53 mutations along with allelic losses at 9p and 18q in EUS-guided fine needle aspiration samples of patients with chronic pancreatitis and pancreatic cancer. World journal of gastroenterology. 2007; 13:3714-3720.
32. Lee EJ, Gusev Y, Jiang J, Nuovo GJ, Lerner MR, Frankel WL, Morgan DL, Postier RG, Brackett DJ and Schmittgen TD. Expression profiling identifies microRNA signature in pancreatic cancer. International journal of cancer. 2007; 120:1046-1054.
33. Dillhoff M, Liu J, Frankel W, Croce C and Bloomston M. MicroRNA-21 is overexpressed in pancreatic cancer and a potential predictor of survival. Journal of gastrointestinal surgery. 2008; 12:2171-2176.
34. Bloomston M, Frankel WL, Petrocca F, Volinia S, Alder H, Hagan JP, Liu CG, Bhatt D, Taccioli C and Croce CM. MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. Jama. 2007; 297:1901-1908.
35. Yu S, Lu Z, Liu C, Meng Y, Ma Y, Zhao W, Liu J, Yu J and Chen J. miRNA-96 suppresses KRAS and functions as a tumor suppressor gene in pancreatic cancer. Cancer research. 2010; 70:6015-6025.
36. Li Y, Vandenboom TG, 2nd, Wang Z, Kong D, Ali S, Philip PA and Sarkar FH. miR-146a suppresses invasion of pancreatic cancer cells. Cancer research. 2010; 70:1486-1495.
37. Weiss FU, Marques IJ, Woltering JM, Vlecken DH, Aghdassi A, Partecke LI, Heidecke CD, Lerch MM and Bagowski CP. Retinoic acid receptor antagonists inhibit miR-10a expression and block metastatic behavior of pancreatic cancer. Gastroenterology. 2009; 137:2136-2145 e2131-2137.
38. Tang B, Vu M, Booker T, Santner SJ, Miller FR, Anver MR and Wakefield LM. TGF-beta switches from tumor suppressor to prometastatic factor in a model of breast cancer progression. The Journal of clinical investigation. 2003; 112:1116-1124.
39. Wakefield LM and Roberts AB. TGF-beta signaling: positive and negative effects on tumorigenesis. Current opinion in genetics & development. 2002; 12:22-29.
40. Siegel PM, Shu W, Cardiff RD, Muller WJ and Massague J. Transforming growth factor beta signaling impairs Neu-induced mammary tumorigenesis while promoting pulmonary metastasis. Proceedings of the National Academy of Sciences of the United States of America. 2003; 100:8430-8435.
41. Hahn SA, Hoque AT, Moskaluk CA, da Costa LT, Schutte M, Rozenblum E, Seymour AB, Weinstein CL, Yeo CJ, Hruban RH and Kern SE. Homozygous deletion map at 18q21.1 in pancreatic cancer. Cancer research. 1996; 56:490-494.
42. Levy L and Hill CS. 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. Molecular and cellular biology. 2005; 25:8108-8125.
43. Fink SP, Mikkola D, Willson JK and Markowitz S. TGF-beta-induced nuclear localization of Smad2 and Smad3 in Smad4 null cancer cell lines. Oncogene. 2003; 22:1317-1323.
44. Oda D, Savard CE, Nguyen TD, Swenson ER and Lee SP. Culture of human main pancreatic duct epithelial cells. In vitro cellular & developmental biology Animal. 1998; 34:211-216.
45. Trautmann B, Schlitt HJ, Hahn EG and Lohr M. Isolation, culture, and characterization of human pancreatic duct cells. Pancreas. 1993; 8:248-254.
46. Cui YM, Jiao HL, Ye YP, Chen CM, Wang JX, Tang N, Li TT, Lin J, Qi L, Wu P, Wang SY, He MR, Liang L, Bian XW, Liao WT and Ding YQ. FOXC2 promotes colorectal cancer metastasis by directly targeting MET. Oncogene. 2015; 34:4379-4390.