Micro-RNAs miR-29a and miR-330-5p function as tumor suppressors by targeting the MUC1 mucin in pancreatic cancer cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 10, 2015, Pages 2392-2403

  Tréhoux, Solange ^a,b,c   Lahdaoui, Fatima ^a,b,c   Delpu, Yannick ^d   Renaud, Florence ^a,b,c,e   Leteurtre, Emmanuelle ^a,b,c,e   Torrisani, JérÔme ^d   Jonckheere, Nicolas ^a,b,c   Van Seuningen, Isabelle ^a,b,c  

^a JEAN PIERRE AUBERT RESEARCH CENTER   (France)

^b UNIV LILLE   (France)

^c LILLE UNIVERSITY HOSPITAL   (France)

^d CANCER RESEARCH CENTER OF TOULOUSE   (France)

^e Centre de Biologie Pathologie   (France)

Author keywords

Cancer; Chemoresistance; MiRNA; MUC1 mucin; Pancreas

Indexed keywords

GEMCITABINE; MICRORNA 183; MICRORNA 200A; MICRORNA 29A; MICRORNA 330-5P; MICRORNA 876-3P; MICRORNA 939; MUCIN 1; UNCLASSIFIED DRUG; 5' UNTRANSLATED REGION; MICRORNA; MIRN29 MICRORNA, HUMAN; MIRN330 MICRORNA, HUMAN; MUC1 PROTEIN, HUMAN; RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CHEMOSENSITIVITY; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RNA BINDING; TUMOR XENOGRAFT; ANIMAL; BIOSYNTHESIS; CANCER TRANSPLANTATION; GENETICS; METABOLISM; PANCREAS TUMOR; PATHOLOGY; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE; XENOGRAFT;

MUS;

5' UNTRANSLATED REGIONS; ANIMALS; CELL LINE, TUMOR; GENES, TUMOR SUPPRESSOR; HETEROGRAFTS; HUMANS; MICE; MICRORNAS; MUCIN-1; NEOPLASM TRANSPLANTATION; PANCREATIC NEOPLASMS; RNA, NEOPLASM;

EID: 84938149957     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.05.033     Document Type: Article

References (53)

1. Jemal A., Bray F., Center M.M., Ferlay J., Ward E., Forman D. Global cancer statistics. CA Cancer J. Clin. 2011, 61:69-90.
2. Vincent A., Herman J., Schulick R., Hruban R.H., Goggins M. Pancreatic cancer. Lancet 2011, 378:607-620.
3. Conroy T., Desseigne F., Ychou M., Bouché O., Guimbaud R., Bécouarn Y., Adenis A., Raoul J.-L., Gourgou-Bourgade S., de la Fouchardière C., et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N. Engl. J. Med. 2011, 364:1817-1825.
4. Jonckheere N., Van Seuningen I. The membrane-bound mucins: how large O-glycoproteins play key roles in epithelial cancers and hold promise as biological tools for gene-based and immunotherapies. Crit. Rev. Oncog. 2008, 14:177-196.
5. Tréhoux S., Duchêne B., Jonckheere N., Van Seuningen I. The MUC1 oncomucin regulates pancreatic cancer cell biological properties and chemoresistance. Implication of p42-44 MAPK, Akt, Bcl-2 and MMP13 pathways. Biochem. Biophys. Res. Commun. 2015, 456:757-762.
6. Hollingsworth M.A., Swanson B.J. Mucins in cancer: protection and control of the cell surface. Nat. Rev. Cancer 2004, 4:45-60.
7. Kufe D.W. Mucins in cancer: function, prognosis and therapy. Nat. Rev. Cancer 2009, 9:874-885.
8. Schroeder J.A., Thompson M.C., Gardner M.M., Gendler S.J. Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland. J. Biol. Chem. 2001, 276:13057-13064.
9. Besmer D.M., Curry J.M., Roy L.D., Tinder T.L., Sahraei M., Schettini J., Hwang S.-I., Lee Y.Y., Gendler S.J., Mukherjee P. Pancreatic ductal adenocarcinoma mice lacking mucin 1 have a profound defect in tumor growth and metastasis. Cancer Res. 2011, 71:4432-4442.
10. Rajabi H., Ahmad R., Jin C., Kosugi M., Alam M., Joshi M.D., Kufe D. MUC1-C oncoprotein induces TCF7L2 transcription factor activation and promotes cyclin D1 expression in human breast cancer cells. J. Biol. Chem. 2012, 287:10703-10713.
11. Ahmad R., Rajabi H., Kosugi M., Joshi M.D., Alam M., Vasir B., Kawano T., Kharbanda S., Kufe D. MUC1-C oncoprotein promotes STAT3 activation in an autoinductive regulatory loop. Sci. Signal. 2011, 4:ra9.
12. Gao J., McConnell M.J., Yu B., Li J., Balko J.M., Black E.P., Johnson J.O., Lloyd M.C., Altiok S., Haura E.B. MUC1 is a downstream target of STAT3 and regulates lung cancer cell survival and invasion. Int. J. Oncol. 2009, 35:337-345.
13. Singh P.K., Wen Y., Swanson B.J., Shanmugam K., Kazlauskas A., Cerny R.L., Gendler S.J., Hollingsworth M.A. Platelet-derived growth factor receptor β-mediated phosphorylation of MUC1 enhances invasiveness in pancreatic adenocarcinoma cells. Cancer Res. 2007, 67:5201-5210.
14. Roy L.D., Sahraei M., Subramani D.B., Besmer D., Nath S., Tinder T.L., Bajaj E., Shanmugam K., Lee Y.Y., Hwang S.I.L., et al. MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene 2011, 30:1449-1459.
15. Nath S., Daneshvar K., Roy L.D., Grover P., Kidiyoor A., Mosley L., Sahraei M., Mukherjee P. MUC1 induces drug resistance in pancreatic cancer cells via upregulation of multidrug resistance genes. Oncogenesis 2013, 2:e51.
16. Winter J.M., Tang L.H., Klimstra D.S., Brennan M.F., Brody J.R., Rocha F.G., Jia X., Qin L.-X., D'Angelica M.I., DeMatteo R.P., et al. A novel survival-based tissue microarray of pancreatic cancer validates MUC1 and mesothelin as biomarkers. PLoS One 2012, 7:e40157.
17. Mohr A.M., Bailey J.M., Lewallen M.E., Liu X., Radhakrishnan P., Yu F., Tapprich W., Hollingsworth M.A. MUC1 regulates expression of multiple microRNAs involved in pancreatic tumor progression, including the miR-200c/141 cluster. PLoS One 2013, 8:e73306.
18. Kasinski A.L., Slack F.J. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat. Rev. Cancer 2011, 11:849-864.
19. Humeau M., Torrisani J., Cordelier P. miRNA in clinical practice: pancreatic cancer. Clin. Biochem. 2013, 46:933-936.
20. Iorio M.V., Croce C.M. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol. Med. 2012, 4:143-159.
21. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
22. Delpu Y., Lulka H., Sicard F., Saint-Laurent N., Lopez F., Hanoun N., Buscail L., Cordelier P., Torrisani J. The rescue of miR-148a expression in pancreatic cancer: an inappropriate therapeutic tool. PLoS One 2013, 8:e55513.
23. Lahdaoui F., Delpu Y., Vincent A., Renaud F., Messager M., Duchêne B., Leteurtre E., Mariette C., Torrisani J., Jonckheere N., Van Seuningen I. miR-219-1-3p is a negative regulator of the mucin MUC4 expression and is a tumor suppressor in pancreatic cancer. Oncogene 2015, 34:780-788.
24. Khan S., Ebeling M.C., Zaman M.S., Sikander M., Yallapu M.M., Chauhan N., Yacoubian A.M., Behrman S.W., Zafar N., Kumar D., et al. MicroRNA-145 targets MUC13 and suppresses growth and invasion of pancreatic cancer. Oncotarget 2014, 5:7599-7609.
25. Jonckheere N., Perrais M., Mariette C., Batra S.K., Aubert J.-P., Pigny P., Van Seuningen I. A role for human MUC4 mucin gene, the ErbB2 ligand, as a target of TGF-beta in pancreatic carcinogenesis. Oncogene 2004, 23:5729-5738.
26. Skrypek N., Duchêne B., Hebbar M., Leteurtre E., van Seuningen I., Jonckheere N. The MUC4 mucin mediates gemcitabine resistance of human pancreatic cancer cells via the Concentrative Nucleoside Transporter family. Oncogene 2013, 32:1714-1723.
27. Lal A., Thomas M.P., Altschuler G., Navarro F., O'Day E., Li X.L., Concepcion C., Han Y.-C., Thiery J., Rajani D.K., et al. Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling. PLoS Genet. 2011, 7:e1002363.
28. Jonckheere N., Skrypek N., Merlin J., Dessein A.F., Dumont P., Leteurtre E., Harris A., Desseyn J.-L., Susini C., Frénois F., et al. The mucin MUC4 and its membrane partner ErbB2 regulate biological properties of human CAPAN-2 pancreatic cancer cells via different signalling pathways. PLoS One 2012, 7:e32232.
29. Piessen G., Jonckheere N., Vincent A., Hémon B., Ducourouble M.-P., Copin M.-C., Mariette C., Van Seuningen I. Regulation of the human mucin MUC4 by taurodeoxycholic and taurochenodeoxycholic bile acids in oesophageal cancer cells is mediated by hepatocyte nuclear factor 1alpha. Biochem. J. 2007, 402:81-91.
30. Van der Sluis M., Melis M.H.M., Jonckheere N., Ducourouble M.-P., Büller H.A., Renes I., et al. The murine Muc2 mucin gene is transcriptionally regulated by the zinc-fingerGATA-4 transcription factor in intestinal cells. Biochem. Biophys. Res. Commun. 2004, 325:952-960.
31. Mariette C., Perrais M., Leteurtre E., Jonckheere N., Hémon B., Pigny P., et al. Transcriptional regulation of human mucin MUC4 by bile acids in oesophageal cancer cells is promoter-dependent and involves activation of the phosphatidylinositol 3-kinase signalling pathway. Biochem. J. 2004, 377:701-708.
32. Radhakrishnan P., Mohr A.M., Grandgenett P.M., Steele M.M., Batra S.K., Hollingsworth M.A. MicroRNA-200c modulates the expression of MUC4 and MUC16 by directly targeting their coding sequences in human pancreatic cancer. PLoS One 2013, 8:e73356.
33. Sachdeva M., Mo Y.-Y. MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1. Cancer Res. 2010, 70:378-387.
34. Jin C., Rajabi H., Kufe D. miR-1226 targets expression of the mucin 1 oncoprotein and induces cell death. Int. J. Oncol. 2010, 37:61-69.
35. Rajabi H., Jin C., Ahmad R., McClary C., Joshi M.D., Kufe D. MUCIN 1 oncoprotein expression is suppressed by the miR-125b oncomirR. Genes Cancer 2010, 1:62-68.
36. Wellner U., Schubert J., Burk U.C., Schmalhofer O., Zhu F., Sonntag A., Waldvogel B., Vannier C., Darling D., zur Hausen A., et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell Biol. 2009, 11:1487-1495.
37. Xia H., Cheung W.K.C., Sze J., Lu G., Jiang S., Yao H., Bian X.-W., Poon W.S., Kung H., Lin M.C. miR-200a regulates epithelial-mesenchymal to stem-like transition via ZEB2 and β-catenin signaling. J. Biol. Chem. 2010, 285:36995-37004.
38. Chen C., Xiang H., Peng Y.-L., Peng J., Jiang S.-W. Mature miR-183, negatively regulated by transcription factor GATA3, promotes 3T3-L1 adipogenesis through inhibition of the canonical Wnt/β-catenin signaling pathway by targeting LRP6. Cell. Signal. 2014, 26:1155-1165.
39. Kufe D.W. MUC1-C oncoprotein as a target in breast cancer: activation of signaling pathways and therapeutic approaches. Oncogene 2013, 32:1073-1081.
40. Tan M., Wu J., Cai Y. Suppression of Wnt signaling by the miR-29 family is mediated by demethylation of WIF-1 in non-small-cell lung cancer. Biochem. Biophys. Res. Commun. 2013, 438:673-679.
41. Li Y., Zhu X., Xu W., Wang D., Yan J. miR-330 regulates the proliferation of colorectal cancer cells by targeting Cdc42. Biochem. Biophys. Res. Commun. 2013, 431:560-565.
42. Zhao J.-J., Lin J., Lwin T., Yang H., Guo J., Kong W., Dessureault S., Moscinski L.C., Rezania D., Dalton W.S., et al. microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood 2010, 115:2630-2639.
43. Xiong Y., Fang J.-H., Yun J.-P., Yang J., Zhang Y., Jia W.-H., Zhuang S.-M. Effects of microRNA-29 on apoptosis, tumorigenicity, and prognosis of hepatocellular carcinoma. Hepatology 2010, 51:836-845.
44. Liu F., Korc M. Cdk4/6 inhibition induces epithelial-mesenchymal transition and enhances invasiveness in pancreatic cancer cells. Mol. Cancer Ther. 2012, 11:2138-2148.
45. Tang W., Zhu Y., Gao J., Fu J., Liu C., Liu Y., Song C., Zhu S., Leng Y., Wang G., et al. MicroRNA-29a promotes colorectal cancer metastasis by regulating matrix metalloproteinase 2 and E-cadherin via KLF4. Br. J. Cancer 2014, 110:450-458.
46. Gong J., Li J., Wang Y., Liu C., Jia H., Jiang C., Wang Y., Luo M., Zhao H., Dong L., et al. Characterization of microRNA-29 family expression and investigation of their mechanistic roles in gastric cancer. Carcinogenesis 2013, bgt337.
47. Muniyappa M.K., Dowling P., Henry M., Meleady P., Doolan P., Gammell P., Clynes M., Barron N. MiRNA-29a regulates the expression of numerous proteins and reduces the invasiveness and proliferation of human carcinoma cell lines. Eur. J. Cancer 2009, 45:3104-3118.
48. Chen J., Li Q., An Y., Lv N., Xue X., Wei J., Jiang K., Wu J., Gao W., Qian Z., et al. CEACAM6 induces epithelial-mesenchymal transition and mediates invasion and metastasis in pancreatic cancer. Int. J. Oncol. 2013, 43:877-885.
49. Nagano H., Tomimaru Y., Eguchi H., Hama N., Wada H., Kawamoto K., Kobayashi S., Mori M., Doki Y. MicroRNA-29a induces resistance to gemcitabine through the Wnt/β-catenin signaling pathway in pancreatic cancer cells. Int. J. Oncol. 2013, 43:1066-1072.
50. Wei W., He H.-B., Zhang W.-Y., Zhang H.-X., Bai J.-B., Liu H.-Z., Cao J.-H., Chang K.-C., Li X.-Y., Zhao S.-H. miR-29 targets Akt3 to reduce proliferation and facilitate differentiation of myoblasts in skeletal muscle development. Cell Death Dis. 2013, 4:e668.
51. Yu P.-N., Yan M.-D., Lai H.-C., Huang R.-L., Chou Y.-C., Lin W.-C., Yeh L.-T., Lin Y.-W. Downregulation of miR-29 contributes to cisplatin resistance of ovarian cancer cells. Int. J. Cancer 2014, 134:542-551.
52. Park J.-K., Lee E.J., Esau C., Schmittgen T.D. Antisense inhibition of microRNA-21 or-221 arrests cell cycle, induces apoptosis, and sensitizes the effects of gemcitabine in pancreatic adenocarcinoma. Pancreas 2009, 38:e190-e199.
53. Wang Y., Zhang X., Li H., Yu J., Ren X. The role of miRNA-29 family in cancer. Eur. J. Cell Biol. 2013, 92:123-128.