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Research Article

Extracellular vesicles derived from cancer-associated fibroblasts induce the migration and invasion of oral squamous cell carcinoma

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Article: 1578525 | Received 27 Feb 2018, Accepted 18 Jan 2019, Published online: 13 Feb 2019

References

  • Warnakulasuriya S. Global epidemiology of oral and oropharyngeal cancer. Oral Oncol. 2009;45(4–5):309–12.
  • Wu JS, Sheng SR, Liang XH, et al. The role of tumor microenvironment in collective tumor cell invasion. Future Oncol. 2017 May;13(11):991–1002.
  • Sobral LM, Zecchin KG, Nascimento de Aquino S, et al. Isolation and characterization of myofibroblast cell lines from oral squamous cell carcinoma. Oncol Rep. 2011a Apr;25(4):1013–1020.
  • Prime SS, Cirillo N, Hassona Y, et al. Fibroblast activation and senescence in oral cancer. J Oral Pathol Med. 2017 Feb;46(2):82–88.
  • Sobral LM, Bufalino A, Lopes MA, et al. Myofibroblasts in the stroma of oral cancer promote tumorigenesis via secretion of activin A. Oral Oncol. 2011b Sep;47(9):840–846.
  • Kellermann MG, Sobral LM, Da Silva SD, et al. Mutual paracrine effects of oral squamous cell carcinoma cells and normal oral fibroblasts: induction of fibroblast to myofibroblast transdifferentiation and modulation of tumor cell proliferation. Oral Oncol. 2008 May;44(5):509–517.
  • Cirillo N, Hassona Y, Celentano A, et al. Cancer-associated fibroblasts regulate keratinocyte cell-cell adhesion via TGF-β-dependent pathways in genotype-specific oral cancer. Carcinogenesis. 2017 Jan;38(1):76–85.
  • Takahashi H, Sakakura K, Kudo T, et al. Cancer-associated fibroblasts promote an immunosuppressive microenvironment through the induction and accumulation of protumoral macrophages. Oncotarget. 2017 Jan 31;8(5):8633–8647.
  • Kayamori K, Katsube K, Sakamoto K, et al. NOTCH3 is induced in cancer-associated fibroblasts and promotes angiogenesis in oral squamous cell carcinoma. PLoS One. 2016 Apr 28;11(4):e0154112.
  • Dourado MR, Guerra ENS, Salo T, et al. Prognostic value of the immunohistochemical detection of cancer-associated fibroblasts in oral cancer: A systematic review and meta-analysis. J Oral Pathol Med. 2018 May;47(5):443–453.
  • Webber J, Yeung V, Clayton A. Extracellular vesicles as modulators of the cancer microenvironment. Semin Cell Dev Biol. 2015 Apr;40:27–34.
  • Tkach M, Théry C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016 Mar 10;164(6):1226–1232.
  • Verma M, Lam TK, Hebert E, et al. Extracellular vesicles: potential applications in cancer diagnosis, prognosis, and epidemiology. BMC Clin Pathol. 2015;15:6.
  • Kalra H, Drummen GP, Mathivanan S. Focus on extracellular vesicles: introducing the next small big thing. Int J Mol Sci. 2016 Feb 6;17(2):170.
  • Lo Cicero A, Stahl PD, Raposo G. Extracellular vesicles shuffling intercellular messages: for good or for bad. Curr Opin Cell Biol. 2015 Aug;35:69–77.
  • Becker A, Thakur BK, Weiss JM, et al. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell. 2016 Dec 12;30(6):836–848.
  • Han L, Xu J, Xu Q, et al. Extracellular vesicles in the tumor microenvironment: therapeutic resistance, clinical biomarkers, and targeting strategies. Med Res Rev. 2017 Nov;37(6):1318–1349.
  • Théry C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006 Apr;Chapter 3: Unit 3.22. (3):3–22.
  • Al-Samadi A, Awad SA, Tuomainen K, et al. Crosstalk between tongue carcinoma cells, extracellular vesicles, and immune cells in vitro and in vivo models. Oncotarget. 2017 May 10;8(36):60123–60134.
  • Salo T, Sutinen M, Hoque Apu E, et al. A novel human leiomyoma tissue derived matrix for cell culture studies. BMC Cancer. 2015 Dec;16(15):981.
  • Bufalino A, Cervigne NK, de Oliveira CE, et al. Low miR-143/miR-145 cluster levels induce activin a overexpression in oral squamous cell carcinomas, which contributes to poor prognosis. PLoS ONE. 2015;10(8):e0136599.
  • Nurmenniemi S, Sinikumpu T, Alahuhta I, et al. A novel organotypic model mimics the tumor microenvironment. Am J Pathol. 2009 Sep;175(3):1281–1291.
  • Winck FV, Prado Ribeiro AC, Ramos Domingues R, et al. Insights into immune responses in oral cancer through proteomic analysis of saliva and salivary extracellular vesicles. Sci Rep. 2015 Nov;5(5):16305.
  • Kawahara R, Meirelles GV, Heberle H, et al. Integrative analysis to select cancer candidate biomarkers to targeted validation. Oncotarget. 2015 Dec 22;6(41):43635–43652.
  • Li C, Wong WH. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A. 2001 Jan 2;98(1):31–36.
  • Kuleshov MV, Jones MR, Rouillard AD, et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 2016 Jul 8;44(W1):W90–7.
  • Szklarczyk D, Morris JH, Cook H, et al. The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res. 2017;45:D362–68.
  • Xu Y, Zhou X, Mei M, et al. Reprograming carcinoma-associated fibroblasts by microRNAs. Curr Mol Med. 2017;17(5):341–349.
  • Zheng X, Xu M, Yao B, et al. IL-6/STAT3 axis initiated CAFs via up-regulating TIMP-1 which was attenuated by acetylation of STAT3 induced by PCAF in HCC microenvironment. Cell Signal. 2016 Sep;28(9):1314–1324.
  • Gong Y, Scott E, Lu R, et al. TIMP-1 promotes accumulation of cancer associated fibroblasts and cancer progression. PLoS One. 2013 Oct 15;8(10):e77366.
  • Kabir TD, Leigh RJ, Tasena H, et al. A miR-335/COX-2/PTEN axis regulates the secretory phenotype of senescent cancer-associated fibroblasts. Aging (Albany NY). 2016 Aug;8(8):1608–1635.
  • Leca J, Martinez S, Lac S, et al. Cancer-associated fibroblast-derived annexin A6+ extracellular vesicles support pancreatic cancer aggressiveness. J Clin Invest. 2016 Nov 1;126(11):4140–4156.
  • Luga V, Zhang L, Viloria-Petit AM, et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell. 2012 Dec 21;151(7):1542–1556.
  • Almangush A, Pirinen M, Heikkinen L, et al. Tumor budding in oral squamous cell carcinoma: a meta-analysis. Br J Cancer. 2018 Feb 20;118(4):577–586.
  • Almangush A, Leivo I, Siponen M, et al. Evaluation of the budding and depth of invasion (BD) model in oral tongue cancer biopsies. Virchows Arch. 2018 Feb;472(2):231–236.
  • Almangush A, Bello IO, Keski-Säntti H, et al. Depth of invasion, tumor budding, and worst pattern of invasion: prognostic indicators in early-stage oral tongue cancer. Head Neck. 2014 Jun;36(6):811–818.
  • Angadi PV, Patil PV, Hallikeri K, et al. Tumor budding is an independent prognostic factor for prediction of lymph node metastasis in oral squamous cell carcinoma. Int J Surg Pathol. 2015 Apr;23(2):102–110.
  • Seki M, Sano T, Yokoo S, et al. Tumor budding evaluated in biopsy specimens is a useful predictor of prognosis in patients with cN0 early stage oral squamous cell carcinoma. Histopathology. 2017 May;70(6):869–879.
  • Itoh G, Chida S, Yanagihara K, et al. Cancer-associated fibroblasts induce cancer cell apoptosis that regulates invasion mode of tumours. Oncogene. 2017 Aug;36(31):4434–4444.
  • Yingzi L, Naveed H, Liang J, et al. Effects of mechanical properties on tumor invasion: insights from a cellular model. Conf Proc IEEE Eng Med Biol Soc. 2014;2014:6818–6821.
  • Mitchell MI, Engelbrecht AM. Metabolic hijacking: A survival strategy cancer cells exploit? Crit Rev Oncol Hematol. 2017 Jan;109:1–8.
  • Wang K, Wu F, Seo BR, et al. Breast cancer cells alter the dynamics of stromal fibronectin-collagen interactions. Matrix Biol. 2017;60–61:86–95.
  • Egan K, Crowley D, Smyth P, et al. Platelet adhesion and degranulation induce pro-survival and pro-angiogenic signalling in ovarian cancer cells. PLoS One. 2011;6(10):e26125.
  • Serhan K, Gartung A, Panigrahy D. Drawing a link between the thromboxane A(2) pathway and the role of platelets and tumor cells in ovarian cancer. Prostaglandins Other Lipid Mediat. 2018 Jul;137:40–45.
  • Iraci N, Gaude E, Leonardi T, et al. Extracellular vesicles are independent metabolic units with asparaginase activity. Nat Chem Biol. 2017 Sep;13(9):951–955.
  • Zhao H, Yang L, Baddour J, et al. Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism. Elife. 2016 Feb;27(5):e10250.
  • Principe S, Mejia-Guerrero S, Ignatchenko V, et al. Proteomic analysis of cancer-associated fibroblasts reveals a paracrine role for MFAP5 in human oral tongue squamous cell carcinoma. J Proteome Res. 2018 Jun 1;17(6):2045–2059.
  • Dourado MR, de Oliveira CE, Sawazaki-Calone I, et al. Clinicopathologic significance of ROCK2 expression in oral squamous cell carcinomas. J Oral Pathol Med. 2018 Feb;47(2):121–127.
  • Jiang L, Liu X, Kolokythas A, et al. Downregulation of the Rho GTPase signaling pathway is involved in the microRNA-138-mediated inhibition of cell migration and invasion in tongue squamous cell carcinoma. Int J Cancer. 2010 Aug 1;127(3):505–512.
  • Bae E, Sato M, Kim RJ, et al. Definition of smad3 phosphorylation events that affect malignant and metastatic behaviors in breast cancer cells. Cancer Res. 2014 Nov 1;74(21):6139–6149.
  • Fu Q, Zhang Q, Lou Y, et al. Primary tumor-derived exosomes facilitate metastasis by regulating adhesion of circulating tumor cells via SMAD3 in liver cancer. Oncogene. 2018; 37:6105–6118.
  • Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015 Jul 9;523(7559):177–182.
  • Lu H, Niu F, Liu F, et al. Elevated glypican-1 expression is associated with an unfavorable prognosis in pancreatic ductal adenocarcinoma. Cancer Med. 2017 Jun;6(6):1181–1191.
  • Zhang H, Duan J, Qu Y, et al. Onco-miR-24 regulates cell growth and apoptosis by targeting BCL2L11 in gastric cancer. Protein Cell. 2016 Feb;7(2):141–151.
  • Ji H, Lee JH, Wang Y, et al. EGFR phosphorylates FAM129B to promote Ras activation. Proc Natl Acad Sci U S A. 2016 Jan 19;113(3):644–649.
  • Li H, Zhang Y, Chen SW, et al. Prognostic significance of Flotillin1 expression in clinically N0 tongue squamous cell cancer. Int J Clin Exp Pathol. 2014 Feb 15;7(3):996–1003.