2,086
Views
56
CrossRef citations to date
0
Altmetric
Original Research

Tumor-derived exosomes educate dendritic cells to promote tumor metastasis via HSP72/HSP105-TLR2/TLR4 pathway

, , , , , , , & show all
Article: e1362527 | Received 26 Apr 2017, Accepted 26 Jul 2017, Published online: 05 Sep 2017

References

  • Gilboa E. DC-based cancer vaccines. J Clin Invest. 2007;117:1195-203. doi:10.1172/JCI31205. PMID:17476349
  • Hargadon KM. The extent to which melanoma alters tissue-resident dendritic cell function correlates with tumorigenicity. Oncoimmunology. 2016;5:e1069462. doi:10.1080/2162402X.2015.1069462. PMID:26942090
  • Tesone AJ, Rutkowski MR, Brencicova E, Svoronos N, Perales-Puchalt A, Stephen TL, Allegrezza MJ, Payne KK, Nguyen JM, Wickramasinghe J, et al. Satb1 Overexpression Drives Tumor-Promoting Activities in Cancer-Associated Dendritic Cells. Cell Rep. 2016;14:1774-86. doi:10.1016/j.celrep.2016.01.056. PMID:26876172
  • Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol. 2004;5:987-95. doi:10.1038/ni1112. PMID:15454922
  • Tang CH, Chen CF, Chen WM, Fong YC. IL-6 increases MMP-13 expression and motility in human chondrosarcoma cells. J Biol Chem. 2011;286:11056-66. doi:10.1074/jbc.M110.204081. PMID:21278254
  • Dohadwala M, Luo J, Zhu L, Lin Y, Dougherty GJ, Sharma S, Huang M, Pold M, Batra RK, Dubinett SM. Non-small cell lung cancer cyclooxygenase-2-dependent invasion is mediated by CD44. J Biol Chem. 2001;276:20809-12. doi:10.1074/jbc.C100140200. PMID:11320076
  • Sheng KC, Pietersz GA, Wright MD, Apostolopoulos V. Dendritic cells: activation and maturation–applications for cancer immunotherapy. Curr Med Chem. 2005;12:1783-800. doi:10.2174/0929867054367248. PMID:16029147
  • Verhasselt V, Buelens C, Willems F, De Groote D, Haeffner-Cavaillon N, Goldman M. Bacterial lipopolysaccharide stimulates the production of cytokines and the expression of costimulatory molecules by human peripheral blood dendritic cells: evidence for a soluble CD14-dependent pathway. J Immunol. 1997;158:2919-25. PMID:9058830
  • Monrad SU, Kojima F, Kapoor M, Kuan EL, Sarkar S, Randolph GJ, Crofford LJ. Genetic deletion of mPGES-1 abolishes PGE2 production in murine dendritic cells and alters the cytokine profile, but does not affect maturation or migration. Prostaglandins Leukot Essent Fatty Acids.. 2011;84:113-21. doi:10.1016/j.plefa.2010.10.003. PMID:21190819
  • Tkach M, Thery C. Communication by Extracellular Vesicles: Where We Are and Where We Need to Go. Cell. 2016;164:1226-32. doi:10.1016/j.cell.2016.01.043. PMID:26967288
  • Liu Y, Gu Y, Cao X. The exosomes in tumor immunity. Oncoimmunology. 2015;4:e1027472. doi:10.1080/2162402X.2015.1027472. PMID:26405598
  • Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, Flament C, Pouzieux S, Faure F, Tursz T, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med. 2001;7:297-303. doi:10.1038/85438. PMID:11231627
  • Dai S, Wan T, Wang B, Zhou X, Xiu F, Chen T, Wu Y, Cao X. More efficient induction of HLA-A*0201-restricted and carcinoembryonic antigen (CEA)-specific CTL response by immunization with exosomes prepared from heat-stressed CEA-positive tumor cells. Clin Cancer Res. 2005;11:7554-63. doi:10.1158/1078-0432.CCR-05-0810. PMID:16243831
  • Xiang X, Poliakov A, Liu C, Liu Y, Deng ZB, Wang J, Cheng Z, Shah SV, Wang GJ, Zhang L, et al. Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer. 2009;124:2621-33. doi:10.1002/ijc.24249. PMID:19235923
  • Lewis AM, Varghese S, Xu H, Alexander HR. Interleukin-1 and cancer progression: the emerging role of interleukin-1 receptor antagonist as a novel therapeutic agent in cancer treatment. J Transl Med. 2006;4:48. doi:10.1186/1479-5876-4-48. PMID:17096856
  • Hussain SP, Harris CC. Inflammation and cancer: an ancient link with novel potentials. Int J Cancer. 2007;121:2373-80. doi:10.1002/ijc.23173. PMID:17893866
  • Liao Q, Zeng Z, Guo X, Li X, Wei F, Zhang W, Li X, Chen P, Liang F, Xiang B, et al. LPLUNC1 suppresses IL-6-induced nasopharyngeal carcinoma cell proliferation via inhibiting the Stat3 activation. Oncogene. 2014; 33, 2098–109. doi:10.1038/onc.2013.161. PMID:23708661
  • Sun Q, Liu Q, Zheng Y, Cao X. Rapamycin suppresses TLR4-triggered IL-6 and PGE(2) production of colon cancer cells by inhibiting TLR4 expression and NF-kappaB activation. Mol Immunol. 2008;45:2929-36. doi:10.1016/j.molimm.2008.01.025. PMID:18343502
  • Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2002;2:161-74. doi:10.1038/nrc745. PMID:11990853
  • Gu FM, Li QL, Gao Q, Jiang JH, Zhu K, Huang XY, Pan JF, Yan J, Hu JH, Wang Z, et al. IL-17 induces AKT-dependent IL-6/JAK2/STAT3 activation and tumor progression in hepatocellular carcinoma. Mol Cancer. 2011;10:150. doi:10.1186/1476-4598-10-150. PMID:22171994
  • Liu Q, Li G, Li R, Shen J, He Q, Deng L, Zhang C, Zhang J. IL-6 promotion of glioblastoma cell invasion and angiogenesis in U251 and T98G cell lines. J Neurooncol. 2010;100:165-76. doi:10.1007/s11060-010-0158-0. PMID:20361349
  • Hou CH, Hsiao YC, Fong YC, Tang CH. Bone morphogenetic protein-2 enhances the motility of chondrosarcoma cells via activation of matrix metalloproteinase-13. Bone. 2009;44:233-42. doi:10.1016/j.bone.2008.09.021. PMID:19038372
  • Akira S. IL-6-regulated transcription factors. Int J Biochem Cell Biol. 1997;29:1401-18. doi:10.1016/S1357-2725(97)00063-0. PMID:9570135
  • Aaronson DS, Horvath CM. A road map for those who don't know JAK-STAT. Science. 2002;296:1653-5. doi:10.1126/science.1071545. PMID:12040185
  • Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol. 2003;21:335-76. doi:10.1146/annurev.immunol.21.120601.141126. PMID:12524386
  • Vabulas RM, Wagner H, Schild H. Heat shock proteins as ligands of toll-like receptors. Curr Top Microbiol. 2002;270:169-84. doi:10.1007/978-3-642-59430-4_11. PMID:12467251
  • Chen TY, Guo J, Yang MJ, Zhu XH, Cao XT. Chemokine-Containing Exosomes Are Released from Heat-Stressed Tumor Cells via Lipid Raft-Dependent Pathway and Act as Efficient Tumor Vaccine. J Immunol. 2011;186:2219-28. doi:10.4049/jimmunol.1002991. PMID:21242526
  • Chalmin F, Ladoire S, Mignot G, Vincent J, Bruchard M, Remy-Martin JP, Boireau W, Rouleau A, Simon B, Lanneau D, et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest. 2010;120:457-71. doi:10.1172/JCI40483. PMID:20093776
  • Galloway E, Shin T, Huber N, Eismann T, Kuboki S, Schuster R, Blanchard J, Wong HR, Lentsch AB. Activation of hepatocytes by extracellular heat shock protein 72. Am J Physiol Cell Physiol. 2008;295:C514−20. doi:10.1152/ajpcell.00032.2008. PMID:18508912
  • Yamagishi N, Fujii H, Saito Y, Hatayama T. Hsp105beta upregulates hsp70 gene expression through signal transducer and activator of transcription-3. FEBS J. 2009;276:5870-80. doi:10.1111/j.1742-4658.2009.07311.x. PMID:19754877
  • Ridgway D. The first 1000 dendritic cell vaccinees. Cancer Invest. 2003;21:873-86. doi:10.1081/CNV-120025091. PMID:14735692
  • Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer. 2012;12:265-77. doi:10.1038/nrc3258. PMID:22437871
  • Melo SA, Luecke LB, Kahlert C, Fernandez AF, Gammon ST, Kaye J, LeBleu VS, Mittendorf EA, Weitz J, Rahbari N, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523:177-82. doi:10.1038/nature14581. PMID:26106858
  • Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, Flament C, Pouzieux S, Faure F, Tursz T, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med. 2001;7:297-303. doi:10.1038/85438. PMID:11231627
  • Mignot G, Roux S, Thery C, Segura E, Zitvogel L. Prospects for exosomes in immunotherapy of cancer. J Cell Mol Med. 2006;10:376-88. doi:10.1111/j.1582-4934.2006.tb00406.x. PMID:16796806
  • Rao Q, Zuo B, Lu Z, Gao X, You A, Wu C, Du Z, Yin H. Tumor-derived exosomes elicit tumor suppression in murine hepatocellular carcinoma models and human in vitro. Hepatology. 2016; 64, 456–72. doi:10.1002/hep.28549. PMID:26990897
  • Koh E, Lee EJ, Nam GH, Hong Y, Cho E, Yang Y, Kim IS. Exosome-SIRPalpha, a CD47 blockade increases cancer cell phagocytosis. Biomaterials. 2017;121:121-9. doi:10.1016/j.biomaterials.2017.01.004. PMID:28086180
  • Whiteside TL. Exosomes and tumor-mediated immune suppression. J Clin Invest. 2016;126:1216-23. doi:10.1172/JCI81136. PMID:26927673
  • Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang HY, Thakur BK, Becker A, Hoshino A, Mark MT, Molina H, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17:816-26. doi:10.1038/ncb3169. PMID:25985394
  • Liu CR, Yu SH, Zinn K, Wang JH, Zhang LM, Jia YJ, Kappes JC, Barnes S, Kimberly RP, Grizzle WE, et al. Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J Immunol. 2006;176:1375-85. doi:10.4049/jimmunol.176.3.1375. PMID:16424164
  • Clayton A, Mitchell JP, Court J, Linnane S, Mason MD, Tabi Z. Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol. 2008;180:7249-58. doi:10.4049/jimmunol.180.11.7249. PMID:18490724
  • Wang YZ, Yi J, Chen XG, Zhang Y, Xu M, Yang ZX. The regulation of cancer cell migration by lung cancer cell-derived exosomes through TGF-beta and IL-10. Oncol Lett. 2016;11:1527-30. doi:10.3892/ol.2015.4044. PMID:26893774
  • Clayton A, Mitchell JP, Court J, Mason MD, Tabi Z. Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res. 2007;67:7458-66. doi:10.1158/0008-5472.CAN-06-3456. PMID:17671216
  • Zhang MH, Tang H, Guo ZH, An HZ, Zhu XJ, Song WG, Guo J, Huang X, Chen T, Wang J, et al. Splenic stroma drives mature dendritic cells to differentiate into regulatory dendritic cells. Nat Immunol. 2004;5:1124-33. doi:10.1038/ni1130. PMID:15475957
  • Cai Z, Zhang W, Yang F, Yu L, Yu Z, Pan J, Wang L, Cao X, Wang J. Immunosuppressive exosomes from TGF-beta1 gene-modified ?dendritic cells attenuate Th17-mediated inflammatory autoimmune disease by inducing regulatory T cells. Cell Res. 2012;22:607-10. doi:10.1038/cr.2011.196. PMID:22157651
  • Baillat D, Hakimi MA, Naar AM, Shilatifard A, Cooch N, Shiekhattar R. Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell. 2005;123:265-76. doi:10.1016/j.cell.2005.08.019. PMID:16239144

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.