MicroRNA-199a and -214 as potential therapeutic targets in pancreatic stellate cells in pancreatic tumor

Oncotarget

Volumn 7, Issue 13, 2016, Pages 16396-16408

  Kuninty, Praneeth R ^a   Bojmar, Linda ^b,c   Tjomsland, Vegard ^b,d   Larsson, Marie ^b   Storm, Gert ^a,e   Östman, Arne ^f   Sandström, Per ^b   Prakash, Jai ^a,f  

^a UNIVERSITY OF TWENTE   (Netherlands)

^b LINKÖPING UNIVERSITY   (Sweden)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d UNIVERSITY OF OSLO   (Norway)

^e UTRECHT UNIVERSITY   (Netherlands)

^f KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Cancer associated fibroblasts; miRNA; Pancreatic cancer; Pancreatic stellate cells; Stroma

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; MICRORNA 199A; MICRORNA 214; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN BAX; PROTEIN P53; SMAD1 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ANTAGOMIR; MIRN199 MICRORNA, HUMAN; MIRN214 MICRORNA, HUMAN; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CANCER ASSOCIATED FIBROBLAST; CELL MIGRATION; CELL PROLIFERATION; CELL SIZE; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; PANCREAS CELL; PANCREAS TUMOR; PANCREATIC SATELLITE CELL; PARACRINE SIGNALING; STROMA; TUMOR GROWTH; APOPTOSIS; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; PANCREATIC STELLATE CELL; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTAGOMIRS; APOPTOSIS; CANCER-ASSOCIATED FIBROBLASTS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IN SITU HYBRIDIZATION; MICRORNAS; PANCREATIC NEOPLASMS; PANCREATIC STELLATE CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84971602028     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7651     Document Type: Article

References (57)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA: a cancer journal for clinicians. 2013; 63:11-30.
2. Mantoni TS, Lunardi S, Al-Assar O, Masamune A, Brunner TB. Pancreatic stellate cells radioprotect pancreatic cancer cells through beta1-integrin signaling. Cancer research. 2011; 71:3453-3458.
3. Cabrera MC, Tilahun E, Nakles R, Diaz-Cruz ES, Charabaty A, Suy S, Jackson P, Ley L, Slack R, Jha R, Collins SP, Haddad N, Kallakury BV, et al. Human Pancreatic Cancer-Associated Stellate Cells Remain Activated after in vivo Chemoradiation. Front Oncol. 2014; 4:102.
4. Neesse A, Algul H, Tuveson DA, Gress TM. Stromal biology and therapy in pancreatic cancer: a changing paradigm. Gut. 2015.
5. Ozdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu CC, Simpson TR, Laklai H, Sugimoto H, Kahlert C, Novitskiy SV, De Jesus-Acosta A, Sharma P, Heidari P, et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer cell. 2014; 25:719-734.
6. Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, Dekleva EN, Saunders T, Becerra CP, Tattersall IW, Westphalen CB, Kitajewski J, Fernandez-Barrena MG, et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer cell. 2014; 25:735-747.
7. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, Madhu B, Goldgraben MA, Caldwell ME, Allard D, Frese KK, Denicola G, Feig C, et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science (New York, NY). 2009; 324:1457-1461.
8. Kim EJ, Sahai V, Abel EV, Griffith KA, Greenson JK, Takebe N, Khan GN, Blau JL, Craig R, Balis UG, Zalupski MM, Simeone DM. Pilot clinical trial of hedgehog pathway inhibitor GDC-0449 (vismodegib) in combination with gemcitabine in patients with metastatic pancreatic adenocarcinoma. Clinical cancer research. 2014; 20:5937-5945.
9. Bijlsma MF, van Laarhoven HW. The conflicting roles of tumor stroma in pancreatic cancer and their contribution to the failure of clinical trials: a systematic review and critical appraisal. Cancer metastasis reviews. 2015; 34:97-114.
10. Augsten M. Cancer-associated fibroblasts as another polarized cell type of the tumor microenvironment. Front Oncol. 2014; 4:62.
11. Apte MV, Wilson JS, Lugea A, Pandol SJ. A starring role for stellate cells in the pancreatic cancer microenvironment. Gastroenterology. 2013; 144:1210-1219.
12. Apte MV, Haber PS, Applegate TL, Norton ID, McCaughan GW, Korsten MA, Pirola RC, Wilson JS. Periacinar stellate shaped cells in rat pancreas: identification, isolation, and culture. Gut. 1998; 43:128-133.
13. Apte MV, Park S, Phillips PA, Santucci N, Goldstein D, Kumar RK, Ramm GA, Buchler M, Friess H, McCarroll JA, Keogh G, Merrett N, Pirola R, et al. Desmoplastic reaction in pancreatic cancer: role of pancreatic stellate cells. Pancreas. 2004; 29:179-187.
14. Apte MV, Pirola RC, Wilson JS. Pancreatic stellate cells: a starring role in normal and diseased pancreas. Frontiers in physiology. 2012; 3:344.
15. Bachem MG, Schneider E, Gross H, Weidenbach H, Schmid RM, Menke A, Siech M, Beger H, Grunert A, Adler G. Identification, culture, and characterization of pancreatic stellate cells in rats and humans. Gastroenterology. 1998; 115:421-432.
16. Apte MV, Wilson JS. Dangerous liaisons: pancreatic stellate cells and pancreatic cancer cells. Journal of gastroenterology and hepatology. 2012; 27:69-74.
17. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, Ji B, Evans DB, Logsdon CD. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer research. 2008; 68:918-926.
18. Coleman SJ, Chioni AM, Ghallab M, Anderson RK, Lemoine NR, Kocher HM, Grose RP. Nuclear translocation of FGFR1 and FGF2 in pancreatic stellate cells facilitates pancreatic cancer cell invasion. EMBO molecular medicine. 2014; 6:467-481.
19. Xu Z, Vonlaufen A, Phillips PA, Fiala-Beer E, Zhang X, Yang L, Biankin AV, Goldstein D, Pirola RC, Wilson JS, Apte MV. Role of pancreatic stellate cells in pancreatic cancer metastasis. The American journal of pathology. 2010; 177:2585-2596.
20. Vonlaufen A, Joshi S, Qu C, Phillips PA, Xu Z, Parker NR, Toi CS, Pirola RC, Wilson JS, Goldstein D, Apte MV. Pancreatic stellate cells: partners in crime with pancreatic cancer cells. Cancer research. 2008; 68:2085-2093.
21. Masamune A, Kikuta K, Watanabe T, Satoh K, Hirota M, Shimosegawa T. Hypoxia stimulates pancreatic stellate cells to induce fibrosis and angiogenesis in pancreatic cancer. Am J Physiol Gastrointest Liver Physiol. 2008; 295:G709-717.
22. Feig C, Gopinathan A, Neesse A, Chan DS, Cook N, Tuveson DA. The pancreas cancer microenvironment. Clinical cancer research. 2012; 18:4266-4276.
23. Omary MB, Lugea A, Lowe AW, Pandol SJ. The pancreatic stellate cell: a star on the rise in pancreatic diseases. The Journal of clinical investigation. 2007; 117:50-59.
24. Kasinski AL, Slack FJ. Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nature reviews Cancer. 2011; 11:849-864.
25. Melo SA, Kalluri R. Molecular pathways: microRNAs as cancer therapeutics. Clinical cancer research. 2012; 18:4234-4239.
26. Kadera BE, Li L, Toste PA, Wu N, Adams C, Dawson DW, Donahue TR. MicroRNA-21 in pancreatic ductal adenocarcinoma tumor-associated fibroblasts promotes metastasis. PloS one. 2013; 8:e71978.
27. Lino Cardenas CL, Henaoui IS, Courcot E, Roderburg C, Cauffiez C, Aubert S, Copin MC, Wallaert B, Glowacki F, Dewaeles E, Milosevic J, Maurizio J, Tedrow J, et al. miR-199a-5p Is upregulated during fibrogenic response to tissue injury and mediates TGFbeta-induced lung fibroblast activation by targeting caveolin-1. PLoS genetics. 2013; 9:e1003291.
28. Mitra AK, Zillhardt M, Hua Y, Tiwari P, Murmann AE, Peter ME, Lengyel E. MicroRNAs reprogram normal fibroblasts into cancer-associated fibroblasts in ovarian cancer. Cancer discovery. 2012; 2:1100-1108.
29. Musumeci M, Coppola V, Addario A, Patrizii M, Maugeri-Sacca M, Memeo L, Colarossi C, Francescangeli F, Biffoni M, Collura D, Giacobbe A, D'Urso L, Falchi M, et al. Control of tumor and microenvironment cross-talk by miR-15a and miR-16 in prostate cancer. Oncogene. 2011; 30:4231-4242.
30. Giovannetti E, Funel N, Peters GJ, Del Chiaro M, Erozenci LA, Vasile E, Leon LG, Pollina LE, Groen A, Falcone A, Danesi R, Campani D, Verheul HM, et al. MicroRNA-21 in pancreatic cancer: correlation with clinical outcome and pharmacologic aspects underlying its role in the modulation of gemcitabine activity. Cancer research. 2010; 70:4528-4538.
31. Takikawa T, Masamune A, Hamada S, Nakano E, Yoshida N, Shimosegawa T. miR-210 regulates the interaction between pancreatic cancer cells and stellate cells. Biochemical and biophysical research communications. 2013; 437:433-439.
32. Tavano F, di Mola FF, Piepoli A, Panza A, Copetti M, Burbaci FP, Latiano T, Pellegrini F, Maiello E, Andriulli A, di Sebastiano P. Changes in miR-143 and miR-21 expression and clinicopathological correlations in pancreatic cancers. Pancreas. 2012; 41:1280-1284.
33. Masamune A, Nakano E, Hamada S, Takikawa T, Yoshida N, Shimosegawa T. Alteration of the microRNA expression profile during the activation of pancreatic stellate cells. Scandinavian journal of gastroenterology. 2014; 49:323-331.
34. Kordes C, Brookmann S, Haussinger D, Klonowski-Stumpe H. Differential and synergistic effects of platelet-derived growth factor-BB and transforming growth factor-beta1 on activated pancreatic stellate cells. Pancreas. 2005; 31:156-167.
35. Gore J, Korc M. Pancreatic cancer stroma: friend or foe? Cancer cell. 2014; 25:711-712.
36. Madsen CD, Pedersen JT, Venning FA, Singh LB, Moeendarbary E, Charras G, Cox TR, Sahai E, Erler JT. Hypoxia and loss of PHD2 inactivate stromal fibroblasts to decrease tumour stiffness and metastasis. EMBO Rep. 2015.
37. Masamune A, Kikuta K, Satoh M, Satoh K, Shimosegawa T. Rho kinase inhibitors block activation of pancreatic stellate cells. Br J Pharmacol. 2003; 140:1292-1302.
38. Kozono S, Ohuchida K, Eguchi D, Ikenaga N, Fujiwara K, Cui L, Mizumoto K, Tanaka M. Pirfenidone inhibits pancreatic cancer desmoplasia by regulating stellate cells. Cancer research. 2013; 73:2345-2356.
39. Kwon JJ, Nabinger SC, Vega Z, Sahu SS, Alluri RK, Abdul-Sater Z, Yu Z, Gore J, Nalepa G, Saxena R, Korc M, Kota J. Pathophysiological role of microRNA-29 in pancreatic cancer stroma. Sci Rep. 2015; 5:11450.
40. Ali S, Suresh R, Banerjee S, Bao B, Xu Z, Wilson J, Philip PA, Apte M, Sarkar FH. Contribution of microRNAs in understanding the pancreatic tumor microenvironment involving cancer associated stellate and fibroblast cells. Am J Cancer Res. 2015; 5:1251-1264.
41. El Azzouzi H, Leptidis S, Dirkx E, Hoeks J, van Bree B, Brand K, McClellan EA, Poels E, Sluimer JC, van den Hoogenhof MM, Armand AS, Yin X, Langley S, et al. The hypoxia-inducible microRNA cluster miR-199a approximately 214 targets myocardial PPARdelta and impairs mitochondrial fatty acid oxidation. Cell metabolism. 2013; 18:341-354.
42. Bassi C, Stambolic V. PTEN, here, there, everywhere. Cell Death Differ. 2013; 20:1595-1596.
43. Kurose K, Gilley K, Matsumoto S, Watson PH, Zhou XP, Eng C. Frequent somatic mutations in PTEN and TP53 are mutually exclusive in the stroma of breast carcinomas. Nat Genet. 2002; 32:355-357.
44. Zheng H, Ying H, Yan H, Kimmelman AC, Hiller DJ, Chen AJ, Perry SR, Tonon G, Chu GC, Ding Z, Stommel JM, Dunn KL, Wiedemeyer R, et al. Pten and p53 converge on c-Myc to control differentiation, self-renewal, and transformation of normal and neoplastic stem cells in glioblastoma. Cold Spring Harb Symp Quant Biol. 2008; 73:427-437.
45. Hill R, Song Y, Cardiff RD, Van Dyke T. Selective evolution of stromal mesenchyme with p53 loss in response to epithelial tumorigenesis. Cell. 2005; 123:1001-1011.
46. Kiaris H, Chatzistamou I, Trimis G, Frangou-Plemmenou M, Pafiti-Kondi A, Kalofoutis A. Evidence for nonautonomous effect of p53 tumor suppressor in carcinogenesis. Cancer research. 2005; 65:1627-1630.
47. Trimboli AJ, Cantemir-Stone CZ, Li F, Wallace JA, Merchant A, Creasap N, Thompson JC, Caserta E, Wang H, Chong JL, Naidu S, Wei G, Sharma SM, et al. Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature. 2009; 461:1084-1091.
48. Gao X, Cao Y, Yang W, Duan C, Aronson JF, Rastellini C, Chao C, Hellmich MR, Ko TC. BMP2 inhibits TGF-beta-induced pancreatic stellate cell activation and extracellular matrix formation. Am J Physiol Gastrointest Liver Physiol. 2013; 304:G804-813.
49. Sartori R, Gregorevic P, Sandri M. TGFbeta and BMP signaling in skeletal muscle: potential significance for muscle-related disease. Trends Endocrinol Metab. 2014; 25:464-471.
50. Que J, Lian Q, El Oakley RM, Lim B, Lim SK. PI3 K/Akt/mTOR-mediated translational control regulates proliferation and differentiation of lineage-restricted RoSH stem cell lines. J Mol Signal. 2007; 2:9.
51. Xiang X, Zhao J, Xu G, Li Y, Zhang W. mTOR and the differentiation of mesenchymal stem cells. Acta Biochim Biophys Sin (Shanghai). 2011; 43:501-510.
52. Alamri A, Semlali A, Jacques E, Alanazi M, Zakrzewski A, Chmielewski W, Rouabhia M. Long-term exposure of human gingival fibroblasts to cigarette smoke condensate reduces cell growth by modulating Bax, caspase-3 and p53 expression. J Periodontal Res. 2015; 50:423-433.
53. Schuler M, Maurer U, Goldstein JC, Breitenbucher F, Hoffarth S, Waterhouse NJ, Green DR. p53 triggers apoptosis in oncogene-expressing fibroblasts by the induction of Noxa and mitochondrial Bax translocation. Cell Death Differ. 2003; 10:451-460.
54. Moreno A, Soleto I, Garcia-Sanz P, Moreno-Bueno G, Palmero I. ING4 regulates a secretory phenotype in primary fibroblasts with dual effects on cell proliferation and tumor growth. Oncogene. 2014; 33:1945-1953.
55. Tjomsland V, Spangeus A, Valila J, Sandstrom P, Borch K, Druid H, Falkmer S, Falkmer U, Messmer D, Larsson M. Interleukin 1alpha sustains the expression of inflammatory factors in human pancreatic cancer microenvironment by targeting cancer-associated fibroblasts. Neoplasia. 2011; 13:664-675.
56. Bansal R, Post E, Proost JH, de Jager-Krikken A, Poelstra K, Prakash J. PEGylation improves pharmacokinetic profile, liver uptake and efficacy of Interferon gamma in liver fibrosis. J Control Release. 2011; 154:233-240.
57. Sicard F, Gayral M, Lulka H, Buscail L, Cordelier P. Targeting miR-21 for the therapy of pancreatic cancer. Mol Ther. 2013; 21:986-994.