Carcinoma-associated fibroblasts release microRNA-331-3p containing extracellular vesicles to exacerbate the development of pancreatic cancer via the SCARA5-FAK axis

References

• Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64(1):9–29. PMID: 24399786. doi:10.3322/caac.21208.
   PubMed Web of Science ®Google Scholar
• Ilic M, Ilic I. Epidemiology of pancreatic cancer. World J Gastroenterol. 2016;22(44):9694–9705. PMID: 27956793. doi:10.3748/wjg.v22.i44.9694.
   PubMed Web of Science ®Google Scholar
• Lai E, Puzzoni M, Ziranu P, Pretta A, Impera V, Mariani S, Liscia N, Soro P, Musio F, Persano M, et al. New therapeutic targets in pancreatic cancer. Cancer Treat Rev. 2019;81:101926. PMID: 31739115. doi:10.1016/j.ctrv.2019.101926.
   PubMed Web of Science ®Google Scholar
• Kleeff J, Korc M, Apte M, La Vecchia C, Johnson CD, Biankin AV, Neale RE, Tempero M, Tuveson DA, Hruban RH, et al. Pancreatic cancer. Nat Rev Dis Primers. 2016;2:16022. PMID: 27158978. doi:10.1038/nrdp.2016.22.
   PubMed Web of Science ®Google Scholar
• Thery C. Cancer: diagnosis by extracellular vesicles. Nat. 2015;523(7559):161–162. PMID: 26106856.doi:10.1038/nature14626.
   Google Scholar
• Qiu J, Yang G, Feng M, Zheng S, Cao Z, You L, Zheng L, Zhang T, Zhao Y. Extracellular vesicles as mediators of the progression and chemoresistance of pancreatic cancer and their potential clinical applications. Mol Cancer. 2018;17(1):2. PMID: 29304816. doi:10.1186/s12943-017-0755-z.
   PubMedGoogle Scholar
• Richards KE, Zeleniak AE, Fishel ML, Wu J, Littlepage LE, Hill R. Cancer-associated fibroblast exosomes regulate survival and proliferation of pancreatic cancer cells. Oncogene. 2017;36(13):1770–1778. PMID: 27669441.doi:10.1038/onc.2016.353.
   PubMed Web of Science ®Google Scholar
• Santi A, Caselli A, Ranaldi F, Paoli P, Mugnaioni C, Michelucci E, Cirri P. Cancer associated fibroblasts transfer lipids and proteins to cancer cells through cargo vesicles supporting tumor growth. Biochim Biophys Acta. 2015;1853(12):3211–3223. PMID: 26384873.doi:10.1016/j.bbamcr.2015.09.013.
   PubMed Web of Science ®Google Scholar
• Santi A, Kugeratski FG, Zanivan S. Cancer associated fibroblasts: the architects of stroma remodeling. Proteomics. 2018;18(5–6):e1700167. PMID: 29280568. doi:10.1002/pmic.201700167.
   PubMed Web of Science ®Google Scholar
• Raposo G, Stahl PD. Extracellular vesicles: a new communication paradigm? Nat Rev Mol Cell Biol. 2019;20(9):509–510. PMID: 31324871. doi:10.1038/s41580-019-0158-7.
   PubMed Web of Science ®Google Scholar
• Maacha S, Bhat AA, Jimenez L, Raza A, Haris M, Uddin S, Grivel JC. Extracellular vesicles-mediated intercellular communication: roles in the tumor microenvironment and anti-cancer drug resistance. Mol Cancer. 2019;18(1):55. PMID: 30925923. doi:10.1186/s12943-019-0965-7.
   PubMedGoogle Scholar
• Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373–383. PMID: 23420871.doi:10.1083/jcb.201211138.
   PubMed Web of Science ®Google Scholar
• Vlassov AV, Magdaleno S, Setterquist R, Conrad R. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim Biophys Acta. 2012;1820(7):940–948. PMID: 22503788.doi:10.1016/j.bbagen.2012.03.017.
   PubMed Web of Science ®Google Scholar
• Raimondo S, Giavaresi G, Lorico A, Alessandro R. Extracellular vesicles as biological shuttles for targeted therapies. Int J Mol Sci. 2019;20(8):1848. PMID: 30991632.doi:10.3390/ijms20081848.
   PubMed Web of Science ®Google Scholar
• Tafrihi M, Hasheminasab E. MiRNAs: biology, biogenesis, their web-based tools, and databases. Microrna. 2019;8(1):4–27. PMID: 30147022.doi:10.2174/2211536607666180827111633.
   PubMedGoogle Scholar
• Hutvagner G. Small RNA asymmetry in RNAi: function in RISC assembly and gene regulation. FEBS Lett. 2005;579(26):5850–5857. PMID: 16199039.doi:10.1016/j.febslet.2005.08.071.
   PubMed Web of Science ®Google Scholar
• Croce CM, Calin GA. MiRNAs, cancer, and stem cell division. Cell. 2005;122(1):6–7. PMID: 16009126.doi:10.1016/j.cell.2005.06.036.
   PubMed Web of Science ®Google Scholar
• Pandima Devi K, Rajavel T, Daglia M, Nabavi SF, Bishayee A, Nabavi SM. Targeting miRNAs by polyphenols: novel therapeutic strategy for cancer. Semin Cancer Biol. 2017;46:146–157. PMID: 28185862. doi:10.1016/j.semcancer.2017.02.001.
   PubMed Web of Science ®Google Scholar
• Thind A, Wilson C. Exosomal miRNAs as cancer biomarkers and therapeutic targets. J Extracell Vesicles. 2016;5(1):31292. PMID: 27440105.doi:10.3402/jev.v5.31292.
   PubMed Web of Science ®Google Scholar
• Jafri MA, Al-Qahtani MH, Shay JW. Role of miRNAs in human cancer metastasis: implications for therapeutic intervention. Semin Cancer Biol. 2017;44:117–131. PMID: 28188828. doi:10.1016/j.semcancer.2017.02.004.
   PubMed Web of Science ®Google Scholar
• Lu K, Wang J, Song Y, Zhao S, Liu H, Tang D, Pan B, Zhao H, Zhang Q. MiRNA-24-3p promotes cell proliferation and inhibits apoptosis in human breast cancer by targeting p27Kip1. Oncol Rep. 2015;34(2):995–1002. PMID: 26044523.doi:10.3892/or.2015.4025.
   PubMed Web of Science ®Google Scholar
• Chang RM, Yang H, Fang F, Xu JF, Yang LY. MicroRNA-331-3p promotes proliferation and metastasis of hepatocellular carcinoma by targeting PH domain and leucine-rich repeat protein phosphatase. Hepatology. 2014;60(4):1251–1263. PMID: 24825302doi:10.1002/hep.27221.
   PubMed Web of Science ®Google Scholar
• Buranjiang G, Kuerban R, Abuduwanke A, Li X, Kuerban G. MicroRNA-331-3p inhibits proliferation and metastasis of ovarian cancer by targeting RCC2. Arch Med Sci. 2019;15(6):1520–1529. PMID: 31749881. doi:10.5114/aoms.2018.77858.
   PubMed Web of Science ®Google Scholar
• Wu D, Pan H, Zhou Y, Zhou J, Fan Y, Qu P. MicroRNA-133b downregulation and inhibition of cell proliferation, migration and invasion by targeting matrix metallopeptidase-9 in renal cell carcinoma. Mol Med Rep. 2014;9(6):2491–2498. doi:10.3892/mmr.2014.2116.
   PubMed Web of Science ®Google Scholar
• Chen X, Luo H, Li X, Tian X, Peng B, Liu S, Zhan T, Wan Y, Chen W, Li Y, et al. MiR-331-3p functions as an oncogene by targeting ST7L in pancreatic cancer. Carcinogenesis. 2018;39(8):1006–1015. 10.1093/carcin/bgy074. PMID: 29850766.
   PubMed Web of Science ®Google Scholar
• Liu H, Hu J, Wei R, Zhou L, Pan H, Zhu H, Huang M, Luo J, Xu W. SPAG5 promotes hepatocellular carcinoma progression by downregulating SCARA5 through modifying β-catenin degradation. J Exp Clin Cancer Res. 2018;37(1):229. doi:10.1186/s13046-018-0891-3. PMID: 30249289.
   PubMedGoogle Scholar
• Ulker D, Ersoy YE, Gucin Z, Muslumanoglu M, Buyru N. Downregulation of SCARA5 may contribute to breast cancer via promoter hypermethylation. Gene. 2018;673:102–106. PMID: 29908284. doi:10.1016/j.gene.2018.06.036.
   PubMed Web of Science ®Google Scholar
• Zhan T, Chen X, Tian X, Han Z, Liu M, Zou Y, Huang S, Chen A, Cheng X, Deng J, et al. MiR-331-3p links to drug resistance of pancreatic cancer cells by activating wnt/beta-catenin signal via ST7L. Technol Cancer Res Treat. 2020;19:1533033820945801. doi:10.1177/1533033820945801. PMID: 32924881.
   Web of Science ®Google Scholar
• Huang J, Zheng D-L, Qin F-S, Cheng N, Chen H, Wan -B-B, Wang Y-P, Xiao H-S, Han Z-G. Genetic and epigenetic silencing of SCARA5 may contribute to human hepatocellular carcinoma by activating FAK signaling. J Clin Invest. 2010;120(1):223–241. doi:10.1172/JCI38012. PMID: 20038795.
   PubMed Web of Science ®Google Scholar
• Kang Y, Yoon SW, Park B. Allergen removed rhus verniciflua stokes suppresses invasion and migration of pancreatic cancer cells through downregulation of the jak/stat and src/FAK signaling pathways. Oncol Rep. 2018;40(5):3060–3068. doi:10.3892/or.2018.6699. PMID: 30226611.
   PubMed Web of Science ®Google Scholar
• Rawla P, Sunkara T, Gaduputi V. Epidemiology of pancreatic cancer: global trends, etiology and risk factors. World J Oncol. 2019;10(1):10–27. doi:10.14740/wjon1166. PMID: 30834048.
   PubMedGoogle Scholar
• Pitt JM, Kroemer G, Zitvogel L. Extracellular vesicles: masters of intercellular communication and potential clinical interventions. J Clin Invest. 2016;126(4):1139–1143. doi:10.1172/JCI87316. PMID: 27035805.
   PubMed Web of Science ®Google Scholar
• Gebert LFR, MacRae IJ. Regulation of microRNA function in animals. Nat Rev Mol Cell Biol. 2019;20(1):21–37. doi:10.1038/s41580-018-0045-7. PMID: 30108335.
   PubMed Web of Science ®Google Scholar
• Kozomara A, Birgaoanu M, Griffiths-Jones S. MiRBase: from microRNA sequences to function. Nucleic Acids Res. 2019;47(D1):D155–D162. doi:10.1093/nar/gky1141. PMID: 30423142.
   PubMed Web of Science ®Google Scholar
• Mohr AM, Mott JL. Overview of microRNA biology. Semin Liver Dis. 2015;35(1):3–11. doi:10.1055/s-0034-1397344. PMID: 25632930.
   PubMed Web of Science ®Google Scholar
• Bushati N, Cohen SM. MicroRNA functions. Annu Rev Cell Dev Biol. 2007;23(1):175–205. doi:10.1146/annurev.cellbio.23.090506.123406. PMID: 17506695.
   PubMed Web of Science ®Google Scholar
• Calin GA, Croce CM. MicroRNA-cancer connection: the beginning of a new tale. Cancer Res. 2006;66(15):7390–7394. doi:10.1146/annurev.cellbio.23.090506.123406. PMID: 16885332.
   PubMed Web of Science ®Google Scholar
• Rupaimoole R, Slack FJ. MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat Rev Drug Discov. 2017;16(3):203–222. doi:10.1038/nrd.2016.246. PMID: 28209991.
   PubMed Web of Science ®Google Scholar
• Yonemori K, Kurahara H, Maemura K, Natsugoe S. MicroRNA in pancreatic cancer. J Hum Genet. 2017;62(1):33–40. doi:10.1038/jhg.2016.59. PMID: 27251005.
   PubMed Web of Science ®Google Scholar
• Pearson AM. Scavenger receptors in innate immunity. Curr Opin Immunol. 1996;8(1):20–28. doi:10.1016/s0952-7915(96)80100-2. PMID: 8729442.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Oliver P, Davies KE, Platt N. Identification and characterization of murine SCARA5, a novel class A scavenger receptor that is expressed by populations of epithelial cells. J Biol Chem. 2006;281(17):11834–11845. doi:10.1074/jbc.M507599200. PMID: 16407294.
   PubMed Web of Science ®Google Scholar
• Yan N, Zhang S, Yang Y, Cheng L, Li C, Dai L, Dai L, Zhang X, Fan P, Tian H, et al. Therapeutic upregulation of class a scavenger receptor member 5 inhibits tumor growth and metastasis. Cancer Sci. 2012;103(9):1631–1639. 10.1111/j.1349-7006.2012.02350.x. PMID: 22642751.
   PubMed Web of Science ®Google Scholar
• Wen X, Wang N, Zhang F, Dong C. Overexpression of SCARA5 inhibits tumor proliferation and invasion in osteosarcoma via suppression of the FAK signaling pathway. Mol Med Rep. 2016;13(3):2885–2891. doi:10.3892/mmr.2016.4857. PMID: 26847210.
   PubMed Web of Science ®Google Scholar
• Gilmore AP, Romer LH. Inhibition of focal adhesion kinase (FAK) signaling in focal adhesions decreases cell motility and proliferation. Mol Biol Cell. 1996;7(8):1209–1224. doi:10.1091/mbc.7.8.1209. PMID: 8856665.
   PubMed Web of Science ®Google Scholar
• Zhao X, Guan JL. Focal adhesion kinase and its signaling pathways in cell migration and angiogenesis. Adv Drug Deliv Rev. 2011;63(8):610–615. doi:10.1016/j.addr.2010.11.001. PMID: 21118706.
   PubMed Web of Science ®Google Scholar
• Hochwald SN, Nyberg C, Zheng M, Zheng D, Wood C, Massoll NA, Magis A, Ostrov D, Cance WG, Golubovskaya VM. A novel small molecule inhibitor of FAK decreases growth of human pancreatic cancer. Cell Cycle. 2009;8(15):2435–2443. doi:10.4161/cc.8.15.9145. PMID: 19571674.
   PubMed Web of Science ®Google Scholar
• Kanteti R, Batra SK, Lennon FE, Salgia R. FAK and paxillin, two potential targets in pancreatic cancer. Oncotarget. 2016;7(21):31586–31601. doi:10.18632/oncotarget.8040. PMID: 26980710.
   PubMedGoogle Scholar
• Symeonides SN, Anderton SM, Serrels A. FAK-inhibition opens the door to checkpoint immunotherapy in pancreatic cancer. J Immunother Cancer. 2017;5(1):17. doi:10.1186/s40425-017-0217-6. PMID: 28239470.
   PubMedGoogle Scholar