MicroRNA-21 in Pancreatic Ductal Adenocarcinoma Tumor-Associated Fibroblasts Promotes Metastasis

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Kadera, Brian E ^a   Li, Luyi ^a   Toste, Paul A ^a   Wu, Nanping ^a   Adams, Curtis ^a   Dawson, David W ^a   Donahue, Timothy R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; GREEN FLUORESCENT PROTEIN; MICRORNA 21;

ANALYTICAL EQUIPMENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BOYDEN CHAMBER; CARCINOGENESIS; CELL ISOLATION; COCULTURE; CONTROLLED STUDY; DRUG TARGETING; EPITHELIAL MESENCHYMAL TRANSITION; FIBROBLAST; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; METASTASIS; MOUSE; NONHUMAN; OVERALL SURVIVAL; PANCREAS ADENOCARCINOMA; PROTEIN EXPRESSION; STROMA; TISSUE MICROARRAY; TUMOR ASSOCIATED FIBROBLAST; TUMOR INVASION; UPREGULATION;

ADENOCARCINOMA; AGED; ANIMALS; BASE SEQUENCE; CARCINOMA, PANCREATIC DUCTAL; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IN SITU HYBRIDIZATION; KAPLAN-MEIER ESTIMATE; LYMPHATIC METASTASIS; MALE; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MICRORNAS; MIDDLE AGED; PANCREATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR CELLS, CULTURED;

EID: 84882749158     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071978     Document Type: Article

References (48)

1. American Cancer Society (2013) Cancer facts & figures 2013. Atlanta, GA: 1-64. Available: http://www.cancer.org/research/cancerfactsfigures/cancerfactsfigures/cancer-facts-figures-2013. Accessed 2013 Jul 29.
2. Martisian LM, Aizenberg R, Rosenzweig A (2012) The Alarming Rise of Pancreatic Cancer Deaths in the United States: Why We Need to Stem the Tide Today. Pancreatic Cancer Action Network: 1-12. Available: http://www.pancan.org/section_research/reports/pdf/incidence_report_2012.pdf. Accessed 2013 Jul 29.
3. Iacobuzio-Donahue CA, Fu B, Yachida S, Luo M, Abe H, et al. (2009) DPC4 Gene Status of the Primary Carcinoma Correlates With Patterns of Failure in Patients With Pancreatic Cancer. Journal of Clinical Oncology 27: 1806-1813 doi:10.1200/JCO.2008.17.7188.
4. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, et al. (2008) Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Research 68: 918-926 doi:10.1158/0008-5472.CAN-07-5714.
5. Esquela-Kerscher A, Slack FJ, (2006) Oncomirs- microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269 doi:10.1038/nrc1840.
6. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, et al. (2005) MicroRNA expression profiles classify human cancers. Nature 435: 834-838 doi:10.1038/nature03702.
7. Donahue TR, Tran LM, Hill R, Li Y, Kovochich A, et al. (2012) Integrative survival-based molecular profiling of human pancreatic cancer. Clin Cancer Res 18: 1352-1363 doi:10.1158/1078-0432.CCR-11-1539.
8. Meng F, Henson R, Wehbe Janek H, Ghoshal K, Jacob ST, et al. (2007) MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. YGAST 133: 647-658 doi:10.1053/j.gastro.2007.05.022.
9. Asangani IA, Rasheed SAK, Nikolova DA, Leupold JH, Colburn NH, et al. (2008) MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27: 2128-2136 doi:10.1038/sj.onc.1210856.
10. Bloomston M, Frankel WL, Petrocca F, Volinia S, Alder H, et al. (2007) MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA 297: 1901-1908 doi:10.1001/jama.297.17.1901.
11. Dillhoff M, Liu J, Frankel W, Croce C, Bloomston M, (2008) MicroRNA-21 is overexpressed in pancreatic cancer and a potential predictor of survival. J Gastrointest Surg 12: 2171-2176 doi:10.1007/s11605-008-0584-x.
12. Moriyama T, Ohuchida K, Mizumoto K, Yu J, Sato N, et al. (2009) MicroRNA-21 modulates biological functions of pancreatic cancer cells including their proliferation, invasion, and chemoresistance. Molecular Cancer Therapeutics 8: 1067-1074 doi:10.1158/1535-7163.MCT-08-0592.
13. Giovannetti E, Funel N, Peters GJ, Del Chiaro M, Erozenci LA, et al. (2010) MicroRNA-21 in pancreatic cancer: correlation with clinical outcome and pharmacologic aspects underlying its role in the modulation of gemcitabine activity. Cancer Research 70: 4528-4538 doi:10.1158/0008-5472.CAN-09-4467.
14. Hwang JH, Voortman J, Giovannetti E, Steinberg SM, Leon LG, et al. (2010) Identification of microRNA-21 as a biomarker for chemoresistance and clinical outcome following adjuvant therapy in resectable pancreatic cancer. PLoS ONE 5: e10630 doi:10.1371/journal.pone.0010630.t009.
15. Rieu du MC, Torrisani J, Selves J, Saati Al T, Souque A, et al. (2010) MicroRNA-21 is induced early in pancreatic ductal adenocarcinoma precursor lesions. Clin Chem 56: 603-612 doi:10.1373/clinchem.2009.137364.
16. Kjaer-Frifeldt S, Hansen TF, Nielsen BS, Joergensen S, Lindebjerg J, et al. (2012) The prognostic importance of miR-21 in stage II colon cancer: a population-based study. Br J Cancer 107: 1169-1174 doi:10.1038/bjc.2012.365.
17. Nielsen BS, Jørgensen S, Fog JU, Søkilde R, Christensen IJ, et al. (2011) High levels of microRNA-21 in the stroma of colorectal cancers predict short disease-free survival in stage II colon cancer patients. Clin Exp Metastasis 28: 27-38 doi:-10.1007/s10585-010-9355-7.
18. Manuyakorn A, Paulus R, Farrell JJ, Dawson NA, Tze S, et al. (2010) Cellular histone modification patterns predict prognosis and treatment response in resectable pancreatic adenocarcinoma: results from RTOG 9704. Journal of Clinical Oncology 28: 1358-1365 doi:10.1200/JCO.2009.24.5639.
19. Bachem MG, Schünemann M, Ramadani M, Siech M, Beger H, et al. (2005) Pancreatic carcinoma cells induce fibrosis by stimulating proliferation and matrix synthesis of stellate cells. YGAST 128: 907-921 doi:10.1053/j.gastro.2004.12.036.
20. Huang M, Sharma S, Zhu LX, Keane MP, Luo J, et al. (2002) IL-7 inhibits fibroblast TGF-beta production and signaling in pulmonary fibrosis. J Clin Invest 109: 931-937 doi:10.1172/JCI14685.
21. Liu N, Furukawa T, Kobari M, Tsao MS, (1998) Comparative phenotypic studies of duct epithelial cell lines derived from normal human pancreas and pancreatic carcinoma. The American Journal of Pathology 153: 263-269 doi:10.1016/S0002-9440(10)65567-8.
22. Laghi L, Orbetegli O, Bianchi P, Zerbi A, Di Carlo V, et al. (2002) Common occurrence of multiple K-RAS mutations in pancreatic cancers with associated precursor lesions and in biliary cancers. Oncogene 21: 4301-4306 doi:10.1038/sj.onc.1205533.
23. Nguyen Kovochich A, Arensman M, Lay AR, Rao NP, Donahue TR, et al. (2013) HOXB7 promotes invasion and predicts survival in pancreatic adenocarcinoma. Cancer 119: 529-539 doi:10.1002/cncr.27725.
24. Neesse A, Michl P, Frese KK, Feig C, Cook N, et al. (2011) Stromal biology and therapy in pancreatic cancer. Gut 60: 861-868 doi:10.1136/gut.2010.226092.
25. Cameron JL, Riall TS, Coleman J, Belcher KA, (2006) One thousand consecutive pancreaticoduodenectomies. Annals of Surgery 244: 10-15 doi:10.1097/01.sla.0000217673.04165.ea.
26. Omary MB, Lugea A, Lowe AW, Pandol SJ, (2007) The pancreatic stellate cell: a star on the rise in pancreatic diseases. J Clin Invest 117: 50-59 doi:10.1172/JCI30082.
27. Vonlaufen A, Joshi S, Qu C, Phillips PA, Xu Z, et al. (2008) Pancreatic stellate cells: partners in crime with pancreatic cancer cells. Cancer Research 68: 2085-2093 doi:10.1158/0008-5472.CAN-07-2477.
28. Campbell I, Qiu W, Haviv I, (2011) Genetic changes in tumour microenvironments. J Pathol 223: 450-458 doi:10.1002/path.2842.
29. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, et al. (2009) Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324: 1457-1461 doi:10.1126/science.1171362.
30. Hoff Von DD, Ramanathan RK, Borad MJ, Laheru DA, Smith LS, et al. (2011) Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: a phase I/II trial. Journal of Clinical Oncology 29: 4548-4554 doi:10.1200/JCO.2011.36.5742.
31. Nelson PT, Baldwin DA, Scearce LM, Oberholtzer JC, Tobias JW, et al. (2004) Microarray-based, high-throughput gene expression profiling of microRNAs. Nat Methods 1: 155-161 doi:10.1038/nmeth717.
32. Liu G, Friggeri A, Yang Y, Milosevic J, Ding Q, et al. (2010) miR-21 mediates fibrogenic activation of pulmonary fibroblasts and lung fibrosis. J Exp Med 207: 1589-1597 doi:10.1084/jem.20100035.
33. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, et al. (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456: 980-984 doi:10.1038/nature07511.
34. Chau BN, Xin C, Hartner J, Ren S, Castano AP, et al. (2012) MicroRNA-21 promotes fibrosis of the kidney by silencing metabolic pathways. Sci Transl Med 4: 121ra18 doi:10.1126/scitranslmed.3003205.
35. Sabatel C, Malvaux L, Bovy N, Deroanne C, Lambert V, et al. (2011) MicroRNA-21 exhibits antiangiogenic function by targeting RhoB expression in endothelial cells. PLoS ONE 6: e16979 doi:10.1371/journal.pone.0016979.g006.
36. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, et al. (2008) Stromal gene expression predicts clinical outcome in breast cancer. Nature Medicine 14: 518-527 doi:10.1038/nm1764.
37. Navab R, Strumpf D, Bandarchi B, Zhu C-Q, Pintilie M, et al. (2011) Prognostic gene-expression signature of carcinoma-associated fibroblasts in non-small cell lung cancer. P Natl Acad Sci Usa 108: 7160-7165 doi:-10.1073/pnas.1014506108/-/DCSupplemental/st01.doc.
38. Bachem MG, Schneider E, Gross H, Weidenbach H, Schmid RM, et al. (1998) Identification, culture, and characterization of pancreatic stellate cells in rats and humans. YGAST 115: 421-432.
39. Apte MV, Haber PS, Darby SJ, Rodgers SC, McCaughan GW, et al. (1999) Pancreatic stellate cells are activated by proinflammatory cytokines: implications for pancreatic fibrogenesis. Gut 44: 534-541.
40. Brentnall TA, Lai LA, Coleman J, Bronner MP, Pan S, et al. (2012) Arousal of Cancer-Associated Stroma: Overexpression of Palladin Activates Fibroblasts to Promote Tumor Invasion. PLoS ONE 7: e30219 doi:10.1371/journal.pone.0030219.s004.
41. Brønnum H, Andersen DC, Schneider M, Sandberg MB, Eskildsen T, et al. (2013) miR-21 Promotes Fibrogenic Epithelial-to-Mesenchymal Transition of Epicardial Mesothelial Cells Involving Programmed Cell Death 4 and Sprouty-1. PLoS ONE 8: e56280 doi:10.1371/journal.pone.0056280.s011.
42. Guo H, Ingolia NT, Weissman JS, Bartel DP, (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-840 doi:10.1038/nature09267.
43. Chi SW, Zang JB, Mele A, Darnell RB, (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486 doi:10.1038/nature08170.
44. Thomson DW, Bracken CP, Goodall GJ, (2011) Experimental strategies for microRNA target identification. Nucleic Acids Res 39: 6845-6853 doi:10.1093/nar/gkr330.
45. Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, et al. (2005) Silencing of microRNAs in vivo with 'antagomirs'. Nature 438: 685-689 doi:10.1038/nature04303.
46. van Rooij E, Purcell AL, Levin AA, (2012) Developing microRNA therapeutics. Circ Res 110: 496-507 doi:10.1161/CIRCRESAHA.111.247916.
47. Elmén J, Lindow M, Schütz S, Lawrence M, Petri A, et al. (2008) LNA-mediated microRNA silencing in non-human primates. Nature 452: 896-899 doi:10.1038/nature06783.
48. Lanford RE, Hildebrandt-Eriksen ES, Petri A, Persson R, Lindow M, et al. (2010) Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327: 198-201 doi:10.1126/science.1178178.