Extracellular vesicles swarm the cancer microenvironment: from tumor–stroma communication to drug intervention

F Wendler; R Favicchio; T Simon; C Alifrangis; J Stebbing; G Giamas

doi:10.1038/onc.2016.253

journal article Aug 22, 2016

Extracellular vesicles swarm the cancer microenvironment: from tumor–stroma communication to drug intervention

F Wendler R Favicchio T Simon C Alifrangis J Stebbing G Giamas

Oncogene Vol. 36 No. 7 pp. 877-884 · Springer Science and Business Media LLC

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References

86

[1]

Abels ER, Breakefield XO . Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell Mol Neurobiol 2016; 36: 301–312. 10.1007/s10571-016-0366-z

[2]

Biogenesis, Secretion, and Intercellular Interactions of Exosomes and Other Extracellular Vesicles

Marina Colombo, Graça Raposo, Clotilde Théry

Annual Review of Cell and Developmental Biology 2014 10.1146/annurev-cellbio-101512-122326

[3]

Khan S, Jutzy JM, Valenzuela MM, Turay D, Aspe JR, Ashok A et al. Plasma-derived exosomal survivin, a plausible biomarker for early detection of prostate cancer. PLoS One 2012; 7: e46737. 10.1371/journal.pone.0046737

[4]

Glypican-1 identifies cancer exosomes and detects early pancreatic cancer

Sonia A. Melo, Linda B. Luecke, Christoph Kahlert et al.

Nature 2015 10.1038/nature14581

[5]

Ogata-Kawata H, Izumiya M, Kurioka D, Honma Y, Yamada Y, Furuta K et al. Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS One 2014; 9: e92921. 10.1371/journal.pone.0092921

[6]

microRNAs Derived from Circulating Exosomes as Noninvasive Biomarkers for Screening and Diagnosing Lung Cancer

Riccardo Cazzoli, Fiamma Buttitta, Marta Di Nicola et al.

Journal of Thoracic Oncology 2013 10.1097/jto.0b013e318299ac32

[7]

Wang T, Gilkes DM, Takano N, Xiang L, Luo W, Bishop CJ et al. Hypoxia-inducible factors and RAB22A mediate formation of microvesicles that stimulate breast cancer invasion and metastasis. Proc Natl Acad Sci USA 2014; 111: E3234–E3242.

[8]

Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 2009; 284: 34211–34222. 10.1074/jbc.m109.041152

[9]

Yu X, Harris SL, Levine AJ . The regulation of exosome secretion: a novel function of the p53 protein. Cancer Res 2006; 66: 4795–4801. 10.1158/0008-5472.can-05-4579

[10]

Amorim M, Fernandes G, Oliveira P, Martins-de-Souza D, Dias-Neto E, Nunes D . The overexpression of a single oncogene (ERBB2/HER2) alters the proteomic landscape of extracellular vesicles. Proteomics 2014; 14: 1472–1479. 10.1002/pmic.201300485

[11]

Ji H, Erfani N, Tauro BJ, Kapp EA, Zhu HJ, Moritz RL et al. Difference gel electrophoresis analysis of Ras-transformed fibroblast cell-derived exosomes. Electrophoresis 2008; 29: 2660–2671. 10.1002/elps.200800015

[12]

Clark DJ, Fondrie WE, Yang A, Mao L . Triple SILAC quantitative proteomic analysis reveals differential abundance of cell signaling proteins between normal and lung cancer-derived exosomes. J Proteomics 2016; 133: 161–169. 10.1016/j.jprot.2015.12.023

[13]

Ekstrom EJ, Bergenfelz C, von Bulow V, Serifler F, Carlemalm E, Jonsson G et al. WNT5A induces release of exosomes containing pro-angiogenic and immunosuppressive factors from malignant melanoma cells. Mol Cancer 2014; 13: 88. 10.1186/1476-4598-13-88

[14]

Meckes Jr DG, Gunawardena HP, Dekroon RM, Heaton PR, Edwards RH, Ozgur S et al. Modulation of B-cell exosome proteins by gamma herpesvirus infection. Proc Natl Acad Sci USA 2013; 110: E2925–E2933.

[15]

Halestrap AP . The monocarboxylate transporter family—structure and functional characterization. IUBMB Life 2012; 64: 1–9. 10.1002/iub.573

[16]

Halestrap AP, Wilson MC . The monocarboxylate transporter family—role and regulation. IUBMB Life 2012; 64: 109–119. 10.1002/iub.572

[17]

Le Floch R, Chiche J, Marchiq I, Naiken T, Ilc K, Murray CM et al. CD147 subunit of lactate/H+ symporters MCT1 and hypoxia-inducible MCT4 is critical for energetics and growth of glycolytic tumors. Proc Natl Acad Sci USA 2011; 108: 16663–16668. 10.1073/pnas.1106123108

[18]

Webb BA, Chimenti M, Jacobson MP, Barber DL . Dysregulated pH: a perfect storm for cancer progression. Nat Rev Cancer 2011; 11: 671–677. 10.1038/nrc3110

[19]

Porporato PE, Payen VL, Baselet B, Sonveaux P . Metabolic changes associated with tumor metastasis, part 2: mitochondria, lipid and amino acid metabolism. Cell Mol Life Sci 2016; 73: 1349–1363. 10.1007/s00018-015-2100-2

[20]

Ronquist KG, Sanchez C, Dubois L, Chioureas D, Fonseca P, Larsson A et al. Energy-requiring uptake of prostasomes and PC3 cell-derived exosomes into non-malignant and malignant cells. J Extracell Vesicles 2016; 5: 29877. 10.3402/jev.v5.29877

[21]

Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism

Hongyun Zhao, Lifeng Yang, Joelle Baddour et al.

eLife 10.7554/elife.10250

[22]

Kerr EM, Gaude E, Turrell FK, Frezza C, Martins CP . Mutant Kras copy number defines metabolic reprogramming and therapeutic susceptibilities. Nature 2016; 531: 110–113. 10.1038/nature16967

[23]

Liou GY, Doppler H, DelGiorno KE, Zhang L, Leitges M, Crawford HC et al. Mutant KRas-induced mitochondrial oxidative stress in acinar cells upregulates EGFR signaling to drive formation of pancreatic precancerous lesions. Cell Rep 2016; 14: 2325–2336. 10.1016/j.celrep.2016.02.029

[24]

Belmont PJ, Jiang P, McKee TD, Xie T, Isaacson J, Baryla NE et al. Resistance to dual blockade of the kinases PI3K and mTOR in KRAS-mutant colorectal cancer models results in combined sensitivity to inhibition of the receptor tyrosine kinase EGFR. Sci Signal 2014. 7ra107. 10.1126/scisignal.2005516

[25]

Mazzeo C, Calvo V, Alonso R, Merida I, Izquierdo M . Protein kinase D1/2 is involved in the maturation of multivesicular bodies and secretion of exosomes in T and B lymphocytes. Cell Death Differ 2016; 23: 99–109. 10.1038/cdd.2015.72

[26]

Minciacchi VR, You S, Spinelli C, Morley S, Zandian M, Aspuria PJ et al. Large oncosomes contain distinct protein cargo and represent a separate functional class of tumor-derived extracellular vesicles. Oncotarget 2015; 6: 11327–11341. 10.18632/oncotarget.3598

[27]

Plebanek MP, Mutharasan RK, Volpert O, Matov A, Gatlin JC, Thaxton CS . Nanoparticle targeting and cholesterol flux through scavenger receptor type B-1 inhibits cellular exosome uptake. Sci Rep 2015; 5: 15724. 10.1038/srep15724

[28]

Aga M, Bentz GL, Raffa S, Torrisi MR, Kondo S, Wakisaka N et al. Exosomal HIF1alpha supports invasive potential of nasopharyngeal carcinoma-associated LMP1-positive exosomes. Oncogene 2014; 33: 4613–4622. 10.1038/onc.2014.66

[29]

Fibroblasts in cancer

Raghu Kalluri, Michael Zeisberg

Nature Reviews Cancer 2006 10.1038/nrc1877

[30]

Cho JA, Park H, Lim EH, Lee KW . Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int J Oncol 2012; 40: 130–138. 10.3892/ijo.2011.1280

[31]

Cancer exosomes trigger mesenchymal stem cell differentiation into pro-angiogenic and pro-invasive myofibroblasts

Ridwana Chowdhury, Jason P. Webber, Mark Gurney et al.

Oncotarget 2015 10.18632/oncotarget.2711

[32]

Morello M, Minciacchi VR, de Candia P, Yang J, Posadas E, Kim H et al. Large oncosomes mediate intercellular transfer of functional microRNA. Cell Cycle 2013; 12: 3526–3536. 10.4161/cc.26539

[33]

Franzen CA, Blackwell RH, Todorovic V, Greco KA, Foreman KE, Flanigan RC et al. Urothelial cells undergo epithelial-to-mesenchymal transition after exposure to muscle invasive bladder cancer exosomes. Oncogenesis 2015; 4: e163. 10.1038/oncsis.2015.21

[34]

Paggetti J, Haderk F, Seiffert M, Janji B, Distler U, Ammerlaan W et al. Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts. Blood 2015; 126: 1106–1117. 10.1182/blood-2014-12-618025

[35]

Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, Chiu E et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 2012; 151: 1542–1556. 10.1016/j.cell.2012.11.024

[36]

Au Yeung CL, Co NN, Tsuruga T, Yeung TL, Kwan SY, Leung CS et al. Exosomal transfer of stroma-derived miR21 confers paclitaxel resistance in ovarian cancer cells through targeting APAF1. Nat Commun 2016; 7: 11150. 10.1038/ncomms11150

[37]

Exosomes – Structure, Biogenesis and Biological Role in Non‐Small‐Cell Lung Cancer

M. Frydrychowicz, A. Kolecka‐Bednarczyk, M. Madejczyk et al.

Scandinavian Journal of Immunology 2015 10.1111/sji.12247

[38]

Park JE, Tan HS, Datta A, Lai RC, Zhang H, Meng W et al. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol Cell Proteomics 2010; 9: 1085–1099. 10.1074/mcp.m900381-mcp200

[39]

Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10: 1470–1476. 10.1038/ncb1800

[40]

Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis

Simona Taverna, Anna Flugy, Laura Saieva et al.

International Journal of Cancer 2012 10.1002/ijc.26217

[41]

Paracrine induction of endothelium by tumor exosomes

Joshua L Hood, Hua Pan, Gregory M Lanza et al.

Laboratory Investigation 2009 10.1038/labinvest.2009.94

[42]

Millimaggi D, Mari M, D'Ascenzo S, Carosa E, Jannini EA, Zucker S et al. Tumor vesicle-associated CD147 modulates the angiogenic capability of endothelial cells. Neoplasia 2007; 9: 349–357. 10.1593/neo.07133

[43]

Gopal SK, Greening DW, Hanssen EG, Zhu HJ, Simpson RJ, Mathias RA . Oncogenic epithelial cell-derived exosomes containing Rac1 and PAK2 induce angiogenesis in recipient endothelial cells. Oncotarget 2016, e-pub ahead of print 22 February 2016 doi:10.18632/oncotarget.7573. 10.18632/oncotarget.7573

[44]

Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus MC et al. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 2011; 71: 5346–5356. 10.1158/0008-5472.can-11-0241

[45]

Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringner M et al. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci USA 2013; 110: 7312–7317. 10.1073/pnas.1220998110

[46]

Vader P, Breakefield XO, Wood MJ . Extracellular vesicles: emerging targets for cancer therapy. Trends Mol Med 2014; 20: 385–393. 10.1016/j.molmed.2014.03.002

[47]

Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J . Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci USA 2009; 106: 3794–3799. 10.1073/pnas.0804543106

[48]

Huber V, Fais S, Iero M, Lugini L, Canese P, Squarcina P et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology 2005; 128: 1796–1804. 10.1053/j.gastro.2005.03.045

[49]

MicroRNA-210 Modulates Endothelial Cell Response to Hypoxia and Inhibits the Receptor Tyrosine Kinase Ligand Ephrin-A3

Pasquale Fasanaro, Yuri D'Alessandra, Valeria Di Stefano et al.

Journal of Biological Chemistry 2008 10.1074/jbc.m800731200

[50]

Decoding the Secret of Cancer by Means of Extracellular Vesicles

Nobuyoshi Kosaka

Journal of Clinical Medicine 2016 10.3390/jcm5020022

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Published: Aug 22, 2016
Vol/Issue: 36(7)
Pages: 877-884
License: View

Authors

Cite This Article

F Wendler, R Favicchio, T Simon, et al. (2016). Extracellular vesicles swarm the cancer microenvironment: from tumor–stroma communication to drug intervention. Oncogene, 36(7), 877-884. https://doi.org/10.1038/onc.2016.253

Extracellular vesicles swarm the cancer microenvironment: from tumor–stroma communication to drug intervention

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