6,334
Views
87
CrossRef citations to date
0
Altmetric
Research Article

Tumor-secreted extracellular vesicles promote the activation of cancer-associated fibroblasts via the transfer of microRNA-125b

ORCID Icon, ORCID Icon, ORCID Icon, , , , , , , ORCID Icon, , ORCID Icon, & ORCID Icon show all
Article: 1599680 | Received 27 Sep 2018, Accepted 21 Mar 2019, Published online: 14 Apr 2019

References

  • Bray F, Ren J-S, Masuyer E, et al. Global estimates of cancer prevalence for 27 sites in the adult population in 2008. Int J Cancer. 2013;132(5):1133–24.
  • Vanharanta S, Massagué J. Origins of metastatic traits. Cancer Cell. 2013;24(4):410–421.
  • Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013;19(11):1423–1437.
  • Karagiannis GS, Poutahidis T, Erdman SE, et al. Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue. Mol Cancer Res. 2012;10(11):1403–1418.
  • Cirri P, Chiarugi P. Cancer-associated-fibroblasts and tumour cells: a diabolic liaison driving cancer progression. Cancer Metastasis Rev. 2012;31(1–2):195–208.
  • Jung D-W, Yu SX, Borgel S, et al. Tumor-stromal crosstalk in invasion of oral squamous cell carcinoma: a pivotal role of CCL7. Int J Cancer. 2010;127(2):332–344.
  • Erez N, Truitt M, Olson P, et al. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell. 2010;17(2):135–147.
  • Olumi AF, Grossfeld GD, Hayward SW, et al. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res. 1999;59(19):5002–5011.
  • Martins VR, Dias MS, Hainaut P. Tumor-cell-derived microvesicles as carriers of molecular information in cancer. Curr Opin Oncol. 2013;25(1):66–75.
  • Kosaka N, Iguchi H, Hagiwara K, et al. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J Biol Chem. 2013;288(15):10849–10859.
  • Bobrie A, Krumeich S, Reyal F, et al. Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res. 2012;72(19):4920–4930.
  • Pang W, Su J, Wang Y, et al. Pancreatic cancer-secreted miR-155 implicates in the conversion from normal fibroblasts to cancer-associated fibroblasts. Cancer Sci. 2015;106(10):1362–1369.
  • Silva TA, Smuczek B, Valadão IC, et al. AHNAK enables mammary carcinoma cells to produce extracellular vesicles that increase neighboring fibroblast cell motility. Oncotarget. 2016;7(31):49998–50016.
  • Webber J, Jenkins RH, Meran S, et al. Modulation of TGFbeta1-dependent myofibroblast differentiation by hyaluronan. Am J Pathol. 2009;175(1):148–160.
  • Valadi H, Ekström 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(6):654–659.
  • Kosaka N, Iguchi H, Ochiya T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 2010;101(10):2087–2092.
  • Kosaka N, Yoshioka Y, Hagiwara K, et al. Trash or treasure: extracellular microRNAs and cell-to-cell communication. Front Genet. 2013;4. DOI:10.3389/fgene.2013.00173.
  • Le MTN, Hamar P, Guo C, et al. miR-200–containing extracellular vesicles promote breast cancer cell metastasis. J Clin Invest. 2014;124(12):5109–5128.
  • Kobayashi T, Vischer UM, Rosnoblet C, et al. The tetraspanin CD63/lamp3 cycles between endocytic and secretory compartments in human endothelial cells. Mol Biol Cell. 2000;11(5):1829–1843.
  • Santner SJ, Dawson PJ, Tait L, et al. Malignant MCF10CA1 cell lines derived from premalignant human breast epithelial MCF10AT Cells. Breast Cancer Res Treat. 2001;65(2):101–110.
  • Ohshima K, Inoue K, Fujiwara A, et al. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLOS ONE. 2010;5(10):e13247.
  • Yin H, Sun Y, Wang X, et al. Progress on the relationship between miR-125 family and tumorigenesis. Exp Cell Res. 2015;339(2):252–260.
  • Zhou M, Liu Z, Zhao Y, et al. MicroRNA-125b confers the resistance of breast cancer cells to paclitaxel through suppression of pro-apoptotic Bcl-2 antagonist killer 1 (Bak1) expression. J Biol Chem. 2010;285(28):21496–21507.
  • Zheng Y, Li S, Boohaker RJ, et al. A microRNA expression signature in taxane-anthracycline-based neoadjuvant chemotherapy response. J Cancer. 2015;6(7):671–677.
  • Wang H, Tan G, Dong L, et al. Circulating miR-125b as a marker predicting chemoresistance in breast cancer. PloS One. 2012;7(4):e34210.
  • Usman WM, Pham TC, Kwok YY, et al. Efficient RNA drug delivery using red blood cell extracellular vesicles. Nat Commun. 2018;9(1):2359.
  • van der Vlist EJ, Enm N-TH, Stoorvogel W, et al. Fluorescent labeling of nano-sized vesicles released by cells and subsequent quantitative and qualitative analysis by high-resolution flow cytometry. Nat Protoc. 2012;7(7):1311–1326.
  • Le MTN, Teh C, Shyh-Chang N, et al. MicroRNA-125b is a novel negative regulator of p53. Genes Dev. 2009;23(7):862–876.
  • Le MTN, Shyh-Chang N, Khaw SL, et al. Conserved regulation of p53 network dosage by microRNA-125b occurs through evolving miRNA-target gene pairs. PLoS Genet. 2011;7(9):e1002242.
  • Procopio M-G, Shemesh T, Thiagarajan V, et al. Combined CSL and p53 downregulation promotes cancer-associated fibroblast activation. Nat Cell Biol. 2015;17(9):1193–1204.
  • Shi X-B, Xue L, Ma A-H, et al. miR-125b promotes growth of prostate cancer xenograft tumor through targeting pro-apoptotic genes. Prostate. 2011;71(5):538–549.
  • Bousquet M, Nguyen D, Chen C, et al. MicroRNA-125b transforms myeloid cell lines by repressing multiple mRNA. Haematologica. 2012;97(11):1713–1721.
  • Bousquet M, Harris MH, Zhou B, et al. MicroRNA miR-125b causes leukemia. Proc Natl Acad Sci. 2010;107(50):21558–21563.
  • Chaudhuri AA, So AY-L, Mehta A, et al. Oncomir miR-125b regulates hematopoiesis by targeting the gene Lin28A. Proc Natl Acad Sci. 2012;109(11):4233–4238.
  • Haemmig S, Baumgartner U, Glück A, et al. miR-125b controls apoptosis and temozolomide resistance by targeting TNFAIP3 and NKIRAS2 in glioblastomas. Cell Death Dis. 2014;5:e1279.
  • Nagpal V, Rai R, Place AT, et al. MiR-125b is critical for fibroblast-to-myofibroblast transition and cardiac fibrosis. Circulation. 2016;133(3):291–301.
  • Bie Z-D, Sun L-Y, Geng C-L, et al. MiR-125b regulates SFRP5 expression to promote growth and activation of cardiac fibroblasts. Cell Biol Int. 2016;40(11):1224–1234.
  • Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010;141(1):52–67.
  • Cao H, Eppinga RD, Razidlo GL, et al. Stromal fibroblasts facilitate cancer cell invasion by a novel invadopodia-independent matrix degradation process. Oncogene. 2016;35(9):1099–1110.
  • Sharon Y, Alon L, Glanz S, et al. Isolation of normal and cancer-associated fibroblasts from fresh tissues by fluorescence activated cell sorting (FACS). J Vis Exp. 2013;71:e4425.
  • Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011;21(2):193–215.
  • Hoshino A. Tumour exosome integrins determine organotropic metastasis. Nature. 2015. DOI:10.1038/nature15756.
  • Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011;17(1):10–12.
  • Langmead B, Trapnell C, Pop M, et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25.
  • Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinforma Oxf Engl. 2010;26(6):841–842.
  • EV-TRACK Consortium. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat Methods. 2017;14(3):228–232.
  • Khan M, Gasser S. Generating primary fibroblast cultures from mouse ear and tail tissues. J Vis Exp. 2016;107. DOI:10.3791/53565.