Reduction of miR-29c enhances pancreatic cancer cell migration and stem cell-like phenotype

Oncotarget

Volumn 6, Issue 5, 2015, Pages 2767-2778

  Jiang, Jianxin ^a   Yu, Chao ^a   Chen, Meiyuan ^a   Zhang, Hao ^a   Tian, Se ^a   Sun, Chengyi ^a  

^a GUIZHOU MEDICAL UNIVERSITY   (China)

Author keywords

FRAT2; FZD4; FZD5; LRP6; miR 29c; Pancreatic cancer; Smad3; TGF ; Wnt

Indexed keywords

FREQUENTLY REARRANGED IN ADVANCED T CELL LYMPHOMAS 2 PROTEIN; FRIZZLED 4 PROTEIN; FRIZZLED 5 PROTEIN; FRIZZLED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; MICRORNA; MICRORNA 29C; REGULATOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN; MIRN29 MICRORNA, HUMAN; SMAD3 PROTEIN; SMAD3 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER STEM CELL; CARCINOGENESIS; CELL MIGRATION; CELL RENEWAL; CONTROLLED STUDY; DOWN REGULATION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC SCREENING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PANCREAS CANCER; PHENOTYPE; PROTEIN RNA BINDING; TISSUE SECTION; ANIMAL; CELL MOTION; GENETIC EPIGENESIS; GENETIC TRANSFECTION; GENETICS; METABOLISM; MORTALITY; NUDE MOUSE; PANCREAS TUMOR; PATHOLOGY; PROGNOSIS; TIME; TUMOR CELL LINE; TUMOR INVASION; WNT SIGNALING PATHWAY;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PANCREATIC NEOPLASMS; PHENOTYPE; PROGNOSIS; SMAD3 PROTEIN; TIME FACTORS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA; WNT SIGNALING PATHWAY;

EID: 84923267461     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3089     Document Type: Article

References (52)

1. Stewart BW and Wild C. (2014). World cancer report 2014: World Health Organization).
2. Demols A, Peeters M, Polus M, Marechal R, Gay F, Monsaert E, Hendlisz A and Van Laethem JL. Gemcitabine and oxaliplatin (GEMOX) in gemcitabine refractory advanced pancreatic adenocarcinoma: a phase II study. Br J Cancer. 2006; 94(4):481-485.
3. Hernandez BY, Green MD, Cassel KD, Pobutsky AM, Vu V and Wilkens LR. Preview of Hawaii Cancer Facts and Figures 2010. Hawaii Med J. 2010; 69(9):223-224.
4. Bussom S and Saif MW. Methods and rationale for the early detection of pancreatic cancer. Highlights from the "2010 ASCO Gastrointestinal Cancers Symposium". Orlando, FL, USA. January 22-24, 2010. JOP. 2010; 11(2):128-130.
5. Shahrokni A and Saif MW. Metastatic pancreatic cancer: the dilemma of quality vs. quantity of life. JOP. 2013; 14(4):391-394.
6. Bardou M and Le Ray I. Treatment of pancreatic cancer: A narrative review of cost-effectiveness studies. Best Pract Res Clin Gastroenterol. 2013; 27(6):881-892.
7. Kummermehr JC. Tumour stem cells--the evidence and the ambiguity. Acta Oncol. 2001; 40(8):981-988.
8. Reya T, Morrison SJ, Clarke MF and Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001; 414(6859):105-111.
9. Kuhn NZ and Tuan RS. Regulation of stemness and stem cell niche of mesenchymal stem cells: implications in tumorigenesis and metastasis. J Cell Physiol. 2010; 222(2):268-277.
10. Brabletz T, Jung A, Spaderna S, Hlubek F and Kirchner T. Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat Rev Cancer. 2005; 5(9):744-749.
11. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF and Simeone DM. Identification of pancreatic cancer stem cells. Cancer Res. 2007; 67(3):1030-1037.
12. Lee CJ, Dosch J and Simeone DM. Pancreatic cancer stem cells. J Clin Oncol. 2008; 26(17):2806-2812.
13. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ and Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007; 1(3):313-323.
14. Visvader JE and Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008; 8(10):755-768.
15. Mueller MT, Hermann PC, Witthauer J, Rubio-Viqueira B, Leicht SF, Huber S, Ellwart JW, Mustafa M, Bartenstein P, D'Haese JG, Schoenberg MH, Berger F, Jauch KW, Hidalgo M and Heeschen C. Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology. 2009; 137(3):1102-1113.
16. Hammond SM. MicroRNAs as oncogenes. Curr Opin Genet Dev. 2006; 16(1):4-9.
17. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, Diehn M, Liu H, Panula SP, Chiao E, Dirbas FM, Somlo G, Pera RA, Lao K and Clarke MF. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell. 2009; 138(3):592-603.
18. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D and Tang DG. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med. 2011; 17(2):211-215.
19. Ji J, Yamashita T, Budhu A, Forgues M, Jia HL, Li C, Deng C, Wauthier E, Reid LM, Ye QH, Qin LX, Yang W, Wang HY, Tang ZY, Croce CM and Wang XW. Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology. 2009; 50(2):472-480.
20. Croce CM and Calin GA. miRNAs, cancer, and stem cell division. Cell. 2005; 122(1):6-7.
21. Reya T and Clevers H. Wnt signalling in stem cells and cancer. Nature. 2005; 434(7035):843-850.
22. Zeng G, Germinaro M, Micsenyi A, Monga NK, Bell A, Sood A, Malhotra V, Sood N, Midda V, Monga DK, Kokkinakis DM and Monga SP. Aberrant Wnt/beta-catenin signaling in pancreatic adenocarcinoma. Neoplasia. 2006; 8(4):279-289.
23. Bauer AS, Keller A, Costello E, Greenhalf W, Bier M, Borries A, Beier M, Neoptolemos J, Buchler M, Werner J, Giese N and Hoheisel JD. Diagnosis of pancreatic ductal adenocarcinoma and chronic pancreatitis by measurement of microRNA abundance in blood and tissue. PLoS One. 2012; 7(4):e34151.
24. Wicha MS, Liu S and Dontu G. Cancer stem cells: an old idea--a paradigm shift. Cancer Res. 2006; 66(4):1883-1890; discussion 1895-1886.
25. DiMeo TA, Anderson K, Phadke P, Fan C, Perou CM, Naber S and Kuperwasser C. A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. Cancer Res. 2009; 69(13):5364-5373.
26. Chen G, Shukeir N, Potti A, Sircar K, Aprikian A, Goltzman D and Rabbani SA. Up-regulation of Wnt-1 and beta-catenin production in patients with advanced metastatic prostate carcinoma: potential pathogenetic and prognostic implications. Cancer. 2004; 101(6):1345-1356.
27. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES and Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005; 102(43):15545-15550.
28. Mermel CH, Schumacher SE, Hill B, Meyerson ML, Beroukhim R and Getz G. GISTIC2.0 facilitates sensitive and confident localization of the targets of focal somatic copy-number alteration in human cancers. Genome Biol. 2011; 12(4):R41.
29. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, Mc Henry KT, Pinchback RM, Ligon AH, Cho YJ, Haery L, Greulich H, et al. The landscape of somatic copynumber alteration across human cancers. Nature. 2010; 463(7283):899-905.
30. Qin W, Chung AC, Huang XR, Meng XM, Hui DS, Yu CM, Sung JJ and Lan HY. TGF-beta/Smad3 signaling promotes renal fibrosis by inhibiting miR-29. J Am Soc Nephrol. 2011; 22(8):1462-1474.
31. Jung A, Schrauder M, Oswald U, Knoll C, Sellberg P, Palmqvist R, Niedobitek G, Brabletz T and Kirchner T. The invasion front of human colorectal adenocarcinomas shows co-localization of nuclear beta-catenin, cyclin D1, and p16INK4A and is a region of low proliferation. Am J Pathol. 2001; 159(5):1613-1617.
32. Rasola A, Fassetta M, De Bacco F, D'Alessandro L, Gramaglia D, Di Renzo MF and Comoglio PM. A positive feedback loop between hepatocyte growth factor receptor and beta-catenin sustains colorectal cancer cell invasive growth. Oncogene. 2007; 26(7):1078-1087.
33. Lin SY, Xia W, Wang JC, Kwong KY, Spohn B, Wen Y, Pestell RG and Hung MC. Beta-catenin, a novel prognostic marker for breast cancer: its roles in cyclin D1 expression and cancer progression. Proc Natl Acad Sci U S A. 2000; 97(8):4262-4266.
34. Yook JI, Li XY, Ota I, Hu C, Kim HS, Kim NH, Cha SY, Ryu JK, Choi YJ, Kim J, Fearon ER and Weiss SJ. A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol. 2006; 8(12):1398-1406.
35. Lowry WE, Blanpain C, Nowak JA, Guasch G, Lewis L and Fuchs E. Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes Dev. 2005; 19(13):1596-1611.
36. Woodward WA, Chen MS, Behbod F and Rosen JM. On mammary stem cells. J Cell Sci. 2005; 118(Pt 16):3585-3594.
37. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R and Weissman IL. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature. 2003; 423(6938):409-414.
38. de La Coste A, Romagnolo B, Billuart P, Renard CA, Buendia MA, Soubrane O, Fabre M, Chelly J, Beldjord C, Kahn A and Perret C. Somatic mutations of the beta-catenin gene are frequent in mouse and human hepatocellular carcinomas. Proc Natl Acad Sci U S A. 1998; 95(15):8847-8851.
39. Hugh TJ, Dillon SA, O'Dowd G, Getty B, Pignatelli M, Poston GJ and Kinsella AR. beta-catenin expression in primary and metastatic colorectal carcinoma. Int J Cancer. 1999; 82(4):504-511.
40. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B and Kinzler KW. Identification of c-MYC as a target of the APC pathway. Science. 1998; 281(5382):1509-1512.
41. Morin PJ. beta-catenin signaling and cancer. Bioessays. 1999; 21(12):1021-1030.
42. Rimm DL, Caca K, Hu G, Harrison FB and Fearon ER. Frequent nuclear/cytoplasmic localization of beta-catenin without exon 3 mutations in malignant melanoma. Am J Pathol. 1999; 154(2):325-329.
43. Hsieh JC, Kodjabachian L, Rebbert ML, Rattner A, Smallwood PM, Samos CH, Nusse R, Dawid IB and Nathans J. A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature. 1999; 398(6726):431-436.
44. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ and Hammond SM. A microRNA polycistron as a potential human oncogene. Nature. 2005; 435(7043):828-833.
45. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio MV, Visone R, Sever NI, Fabbri M, Iuliano R, Palumbo T, Pichiorri F, Roldo C, Garzon R, Sevignani C, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005; 353(17):1793-1801.
46. Cummins JM, He Y, Leary RJ, Pagliarini R, Diaz LA, Jr., Sjoblom T, Barad O, Bentwich Z, Szafranska AE, Labourier E, Raymond CK, Roberts BS, Juhl H, Kinzler KW, Vogelstein B and Velculescu VE. The colorectal microRNAome. Proc Natl Acad Sci U S A. 2006; 103(10):3687-3692.
47. Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, Liu S, Alder H, Costinean S, Fernandez-Cymering C, Volinia S, Guler G, Morrison CD, Chan KK, Marcucci G, Calin GA, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A. 2007; 104(40):15805-15810.
48. Sengupta S, den Boon JA, Chen IH, Newton MA, Stanhope SA, Cheng YJ, Chen CJ, Hildesheim A, Sugden B and Ahlquist P. MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins. Proc Natl Acad Sci U S A. 2008; 105(15):5874-5878.
49. Esquela-Kerscher A and Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer. 2006; 6(4):259-269.
50. Nagano H, Tomimaru Y, Eguchi H, Hama N, Wada H, Kawamoto K, Kobayashi S, Mori M and Doki Y. MicroRNA-29a induces resistance to gemcitabine through the Wnt/beta-catenin signaling pathway in pancreatic cancer cells. Int J Oncol. 2013; 43(4):1066-1072.
51. Singh P, Wig JD and Srinivasan R. The Smad family and its role in pancreatic cancer. Indian J Cancer. 2011; 48(3):351-360.
52. Li J, Zhang N, Song LB, Liao WT, Jiang LL, Gong LY, Wu J, Yuan J, Zhang HZ, Zeng MS and Li M. Astrocyte elevated gene-1 is a novel prognostic marker for breast cancer progression and overall patient survival. Clin Cancer Res. 2008; 14(11):3319-3326.