Exosomal miR-106a derived from gastric cancer promotes peritoneal metastasis via direct regulation of Smad7

References

• Van Cutsem E, Sagaert X, Topal B, et al. Gastric cancer. Lancet. 2016;388:2654–2664.
   PubMed Web of Science ®Google Scholar
• Cristescu R, Lee J, Nebozhyn M, et al. Molecular analysis of gastric cancer identifies subtypes associated with distinct clinical outcomes. Nat Med. 2015;21:449–456.
   PubMed Web of Science ®Google Scholar
• Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66:115–132.
   PubMed Web of Science ®Google Scholar
• Zong L, Abe M, Seto Y, et al. The challenge of screening for early gastric cancer in China. Lancet. 2016;388:2606.
   PubMed Web of Science ®Google Scholar
• Chen JG, Chen HZ, Zhu J, et al. Cancer survival in patients from a hospital-based cancer registry, China. J Cancer. 2018;9:851–860.
   PubMed Web of Science ®Google Scholar
• Cho JM, Jang YJ, Kim JH, et al. Pattern, timing and survival in patients with recurrent gastric cancer. Hepato-gastroenterology. 2014;61:1148–1153.
   PubMedGoogle Scholar
• Yoo CH, Noh SH, Shin DW, et al. Recurrence following curative resection for gastric carcinoma. Br J Surg. 2000;87:236–242.
   PubMed Web of Science ®Google Scholar
• Orditura M, Galizia G, Sforza V, et al. Treatment of gastric cancer. World J Gastroenterol. 2014;20:1635–1649.
   PubMed Web of Science ®Google Scholar
• Hoshino A, Costa-Silva B, Shen TL, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527:329–335.
   PubMed Web of Science ®Google Scholar
• Ruivo CF, Adem B, Silva M, et al. The biology of cancer exosomes: insights and new perspectives. Cancer Res. 2017;77:6480–6488.
   PubMed Web of Science ®Google Scholar
• Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164:1226–1232.
   PubMed Web of Science ®Google Scholar
• Zhu M, Zhang N, He S, et al. MicroRNA-106a targets TIMP2 to regulate invasion and metastasis of gastric cancer. FEBS Lett. 2014;588:600–607.
   PubMed Web of Science ®Google Scholar
• Zhu M, Zhang N, He S, et al. MicroRNA-106a functions as an oncogene in human gastric cancer and contributes to proliferation and metastasis in vitro and in vivo. Clin Exp Metastasis. 2016;33:509–519.
   PubMed Web of Science ®Google Scholar
• Paget S. The distribution of secondary growths in cancer of the breast. Cancer Metastasis Rev. 1989;8:98–101.
   PubMed Web of Science ®Google Scholar
• Mikula-Pietrasik J, Uruski P, Tykarski A, et al. The peritoneal “soil” for a cancerous “seed”: a comprehensive review of the pathogenesis of intraperitoneal cancer metastases. Cell Mol Life Sci. 2018;75:509–525.
   PubMed Web of Science ®Google Scholar
• Li K, Chen Y, Li A, et al. Exosomes play roles in sequential processes of tumor metastasis. Int J Cancer. 2019;144:1486–1495.
   PubMed Web of Science ®Google Scholar
• Yuyama K, Sun H, Mitsutake S, et al. Sphingolipid-modulated exosome secretion promotes clearance of amyloid-beta by microglia. J Biol Chem. 2012;287:10977–10989.
   PubMed Web of Science ®Google Scholar
• Deng G, Qu J, Zhang Y, et al. Gastric cancer-derived exosomes promote peritoneal metastasis by destroying the mesothelial barrier. FEBS Lett. 2017;591:2167–2179.
   PubMed Web of Science ®Google Scholar
• Lopez-Cabrera M. Mesenchymal conversion of mesothelial cells is a key event in the pathophysiology of the peritoneum during peritoneal dialysis. Adv Med. 2014;2014:473134.
   PubMedGoogle Scholar
• Jan AT, Rahman S, Khan S, et al. Biology, pathophysiological role, and clinical implications of exosomes: a critical appraisal. Cells. 2019;8:99.
   Web of Science ®Google Scholar
• Valadi H, Ekstrom K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–659.
   PubMed Web of Science ®Google Scholar
• Yu X, Odenthal M, Fries JW. Exosomes as miRNA carriers: formation-function-future. Int J Mol Sci. 2016;17:2028.
   Google Scholar
• Tai YL, Chen KC, Hsieh JT, et al. Exosomes in cancer development and clinical applications. Cancer Sci. 2018;109:2364–2374.
   PubMed Web of Science ®Google Scholar
• Zhang HG, Grizzle WE. Exosomes: a novel pathway of local and distant intercellular communication that facilitates the growth and metastasis of neoplastic lesions. Am J Pathol. 2014;184:28–41.
   PubMed Web of Science ®Google Scholar
• Fang T, Lv H, Lv G, et al. Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat Commun. 2018;9:191.
   PubMed Web of Science ®Google Scholar
• Li XJ, Ren ZJ, Tang JH, et al. Exosomal microRNA miR-1246 promotes cell proliferation, invasion and drug resistance by targeting CCNG2 in breast cancer. Cell Physiol Biochem. 2017;44:1741–1748.
   PubMed Web of Science ®Google Scholar
• Valcz G, Galamb O, Krenacs T, et al. Exosomes in colorectal carcinoma formation: ALIX under the magnifying glass. Mod Pathol. 2016;29:928–938.
   PubMed Web of Science ®Google Scholar
• Batista IA, Melo SA. Exosomes and the future of immunotherapy in pancreatic cancer. Int J Mol Sci. 2019;20:567.
   Google Scholar
• van Baal JO, Van de Vijver KK, Nieuwland R, et al. The histophysiology and pathophysiology of the peritoneum. Tissue Cell. 2017;49:95–105.
   PubMed Web of Science ®Google Scholar
• Tobioka H, Sawada N, Zhong Y, et al. Enhanced paracellular barrier function of rat mesothelial cells partially protects against cancer cell penetration. Br J Cancer. 1996;74:439–445.
   PubMed Web of Science ®Google Scholar
• Capobianco A, Cottone L, Monno A, et al. The peritoneum: healing, immunity, and diseases. J Pathol. 2017;243:137–147.
   PubMed Web of Science ®Google Scholar
• Ge Q, Zhou Y, Lu J, et al. miRNA in plasma exosome is stable under different storage conditions. Molecules. 2014;19:1568–1575.
   PubMed Web of Science ®Google Scholar
• Wang Z, Liu M, Zhu H, et al. miR-106a is frequently upregulated in gastric cancer and inhibits the extrinsic apoptotic pathway by targeting FAS. Mol Carcinog. 2013;52:634–646.
   PubMed Web of Science ®Google Scholar
• Zhu M, Zhang N, Lu X, et al. Negative regulation of Kruppel-Like Factor 4 on microRNA-106a at upstream transcriptional level and the role in gastric cancer metastasis. Dig Dis Sci. 2018;63:2604–2616.
   PubMed Web of Science ®Google Scholar
• Espinosa-Parrilla Y, Munoz X, Bonet C, et al. Genetic association of gastric cancer with miRNA clusters including the cancer-related genes MIR29, MIR25, MIR93 and MIR106: results from the EPIC-EURGAST study. Int J Cancer. 2014;135:2065–2076.
   PubMed Web of Science ®Google Scholar
• Volinia S, Calin GA, Liu CG, et al. (2006) A microRNA expression signature of human solid tumors defines cancer gene targets, Proc Natl Acad Sci USA. 2006;103,2257–2261.
   Google Scholar
• Concepcion CP, Bonetti C, Ventura A. The microRNA-17-92 family of microRNA clusters in development and disease. Cancer J. 2012;18:262–267.
   PubMed Web of Science ®Google Scholar
• Nakamura M, Ono YJ, Kanemura M, et al. Hepatocyte growth factor secreted by ovarian cancer cells stimulates peritoneal implantation via the mesothelial-mesenchymal transition of the peritoneum. Gynecol Oncol. 2015;139:345–354.
   PubMed Web of Science ®Google Scholar
• Matte I, Lane D, Laplante C, et al. Ovarian cancer ascites enhance the migration of patient-derived peritoneal mesothelial cells via cMet pathway through HGF-dependent and -independent mechanisms. Int J Cancer. 2015;137:289–298.
   PubMed Web of Science ®Google Scholar
• Yokoi A, Yoshioka Y, Yamamoto Y, et al. Malignant extracellular vesicles carrying MMP1 mRNA facilitate peritoneal dissemination in ovarian cancer. Nat Commun. 2017;8:14470.
   PubMed Web of Science ®Google Scholar
• Lamora A, Talbot J, Bougras G, et al. Overexpression of smad7 blocks primary tumor growth and lung metastasis development in osteosarcoma. Clin Cancer Res. 2014;20:5097–5112.
   PubMed Web of Science ®Google Scholar
• Halder SK, Rachakonda G, Deane NG, et al. Smad7 induces hepatic metastasis in colorectal cancer. Br J Cancer. 2008;99:957–965.
   PubMed Web of Science ®Google Scholar
• Rynne-Vidal A, Au-Yeung CL, Jimenez-Heffernan JA, et al. Mesothelial-to-mesenchymal transition as a possible therapeutic target in peritoneal metastasis of ovarian cancer. J Pathol. 2017;242:140–151.
   PubMed Web of Science ®Google Scholar
• Zhang S, Fei T, Zhang L, et al. Smad7 antagonizes transforming growth factor beta signaling in the nucleus by interfering with functional Smad-DNA complex formation. Mol Cell Biol. 2007;27:4488–4499.
   PubMed Web of Science ®Google Scholar
• Yan X, Chen YG. Smad7: not only a regulator, but also a cross-talk mediator of TGF-beta signalling. Biochem J. 2011;434:1–10.
   PubMed Web of Science ®Google Scholar