Myeloid-derived macrophages and secreted HSP90α induce pancreatic ductal adenocarcinoma development

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics. CA Cancer J Clin 2016; 66:7–30; doi:10.3322/caac.21332 PMID:26742998.
   PubMed Web of Science ®Google Scholar
• Hruban RH, van Mansfeld AD, Offerhaus GJ, van Weering DH, Allison DC, Goodman SN, Kensler TW, Bose KK, Cameron JL, Bos JL. K-ras oncogene activation in adenocarcinoma of the human pancreas. A study of 82 carcinomas using a combination of mutant-enriched polymerase chain reaction analysis and allele-specific oligonucleotide hybridization. Am J Pathol 1993; 143:545–54; PMID:8342602.
   PubMed Web of Science ®Google Scholar
• Moskaluk CA, Hruban RH, Kern SE. p16 and K-ras gene mutations in the intraductal precursors of human pancreatic adenocarcinoma. Cancer Res 1997; 57:2140–3; PMID:9187111.
   PubMed Web of Science ®Google Scholar
• Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008; 321:1801–6; doi:10.1126/science.1164368 PMID:18772397.
   PubMed Web of Science ®Google Scholar
• Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, Ross S, Conrads TP, Veenstra TD, Hitt BA et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003; 4:437–50; doi:10.1016/S1535-6108(03)00309-X PMID:14706336.
   PubMed Web of Science ®Google Scholar
• Aguirre AJ, Bardeesy N, Sinha M, Lopez L, Tuveson DA, Horner J, Redston MS, DePinho RA. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev 2003; 17:3112–26; doi:10.1101/gad.1158703 PMCID:PMC305262.
   PubMed Web of Science ®Google Scholar
• Herreros-Villanueva M, Hijona E, Cosme A, Bujanda L. Mouse models of pancreatic cancer. World J Gastroenterol 2012; 18:1286–94; doi:10.3748/wjg.v18.i12.1286 PMID:22493542.
   PubMed Web of Science ®Google Scholar
• Hruban RH, Goggins M, Parsons J, Kern SE. Progression model for pancreatic cancer. Clin Cancer Res 2000; 6:2969–72; PMID:10955772.
   PubMed Web of Science ®Google Scholar
• Shi C, Hong SM, Lim P, Kamiyama H, Khan M, Anders RA, Goggins M, Hruban RH, Eshleman JR. KRAS2 mutations in human pancreatic acinar-ductal metaplastic lesions are limited to those with PanIN: implications for the human pancreatic cancer cell of origin. Mol Cancer Res 2009; 7:230–6; doi:10.1158/1541-7786.MCR-08-0206 PMCID:PMC2708114.
   PubMed Web of Science ®Google Scholar
• Yanagisawa A, Ohtake K, Ohashi K, Hori M, Kitagawa T, Sugano H, Kato Y. Frequent c-Ki-ras oncogene activation in mucous cell hyperplasias of pancreas suffering from chronic inflammation. Cancer Res 1993; 53:953–6; http://cancerres.aacrjournals.org/content/canres/53/5/953.full.pdf PMID:8439969
   PubMed Web of Science ®Google Scholar
• Funahashi H, Satake M, Dawson D, Huynh NA, Reber HA, Hines OJ, Eibl G. Delayed progression of pancreatic intraepithelial neoplasia in a conditional Kras(G12D) mouse model by a selective cyclooxygenase-2 inhibitor. Cancer Res 2007; 67:7068–71; doi:10.1158/0008-5472.CAN-07-0970 PMID:17652141.
   PubMed Web of Science ®Google Scholar
• Turley SJ, Cremasco V, Astarita JL. Immunological hallmarks of stromal cells in the tumour microenvironment. Nat Rev Immunol 2015; 15:669–82; doi:10.1038/nri3902 PMID:26471778.
   PubMed Web of Science ®Google Scholar
• Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 1996; 56:4625–9; PMID:8840975.
   PubMed Web of Science ®Google Scholar
• Chen JJW, Yao PL, Yuan A, Hong TM, Shun CT, Kuo ML, Lee YC, Yang PC. Up-regulation of tumor interleukin-8 expression by infiltrating macrophages. Its correlation with tumor angiogenesis and patient survival in non-small cell lung cancer. Clin Cancer Res 2003; 9:729–37; PMID:12576442.
   PubMed Web of Science ®Google Scholar
• Kurahara H, Shinchi H, Mataki Y, Maemura K, Noma H, Kubo F, Sakoda M, Ueno S, Natsugoe S, Takao S. Significance of M2-polarized tumor-associated macrophage in pancreatic cancer. J Surg Res 2011; 167:e211–9; doi:10.1016/j.jss.2009.05.026 PMID:19765725.
   PubMed Web of Science ®Google Scholar
• Bingle L, Brown NJ, Lewis CE. The role of tumor-associated macrophages in tumor progression: implications for new anticancer therapies. J Pathol 2002; 196:254–65; doi:10.1002/path.1027 PMID:11857487.
   PubMed Web of Science ®Google Scholar
• Pollard JW. Tumor-educated macrophages promote tumor progression and metastasis. Nat Rev Cancer 2004; 4:71–8; doi:10.1038/nrc1256 PMID:14708027.
   PubMed Web of Science ®Google Scholar
• Sica A, Schioppa T, Mantovani A, Allavena P. Tumor-associated macrophages are a distinct M2 polarised population promoting tumor progression: potential targets of anti-cancer therapy. Eur J Cancer 2006; 42:717–27; doi:10.1016/j.ejca.2006.01.003 PMID:16520032.
   PubMed Web of Science ®Google Scholar
• Liou GY, Döppler H, Necela B, Krishna M, Crawford HC, Raimondo M, Storz P. Macrophage-secreted cytokines drive pancreatic acinar-to-ductal metaplasia through NF-κB and MMPs. J Cell Biol 2013; 202:563–77; doi:10.1083/jcb.201301001 PMID:23918941.
   PubMed Web of Science ®Google Scholar
• Ray KC, Moss ME, Franklin JL, Weaver CJ, Higginbotham J, Song Y, Revetta FL, Blaine SA, Bridges LR, Guess KE et al. Heparin-binding epidermal growth factor-like growth factor eliminates constraints on activated Kras to promote rapid onset of pancreatic neoplasia. Oncogene 2014; 33:823–31; doi:10.1038/onc.2013.3 PMID:23376846.
   PubMed Web of Science ®Google Scholar
• Nozawa H, Chiu C, Hanahan D. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci USA 2006; 103:12493–8; doi:10.1073/pnas.0601807103 PMCID:PMC1531646.
   PubMed Web of Science ®Google Scholar
• Zhang J, Xu X, Shi M, Chen Y, Yu D, Zhao C, Gu Y, Yang B, Guo S, Ding G et al. CD13hi neutrophil-like myeloid-derived suppressor cells exert immune suppression through arginase 1 expression in pancreatic ductal adenocarcinoma. OncoImmunology 2017; 6:e1258504; https://doi.org/10.1080/2162402X.2016.1258504 PMID:28344866.
   PubMed Web of Science ®Google Scholar
• Trepel JB, Mollapour M, Giaccone G, Neckers, L. Targeting the dynamic Hsp90 complex in cancer. Nat Rev Cancer 2010; 10:537–49; doi:10.1080/2162402X.2016.1258504. doi:10.1038/nrc2887 PMID:20651736.
   PubMed Web of Science ®Google Scholar
• Sawarkar R, Sievers C, Paro R. Hsp90 globally targets paused RNA polymerase to regulate gene expression in response to environmental stimuli. Cell 2012; 149:807–18; doi:10.1016/j.cell.2012.02.061 PMID: 22579285.
   PubMed Web of Science ®Google Scholar
• Li W, Li Y, Guan S, Fan J, Cheng C-F, Bright AM, Chinn C, Chen M, Woodley DT. Extracellular heat shock protein-90α: linking hypoxia to skin cell motility and wound healing. EMBO J 2007; 26:1221–33; doi:10.1038/sj.emboj.7601579 PMID:17304217.
   PubMed Web of Science ®Google Scholar
• Cheng C-F, Fan J, Fedesco M, Guan S, Li Y, Bandyopadhyay B, Bright AM, Yerushalmi D, Liang M, Chen M et al. Transforming Growth Factor α (TGFα)-stimulated secretion of HSP90a: using the receptor LRP-1/CD91 to promote human skin cell migration against a TGFβ-rich environment during wound healing. Mol Cell Biol 2008; 28:3344–58; doi:10.1128/MCB.01287-07.
   PubMed Web of Science ®Google Scholar
• Xu A, Tian T, Hao J, Liu J, Zhang Z, Hao J, Wu S, Huang L, Xiao X, He D. Elevation of serum HSP90α correlated with the clinical stage of non-small cell lung cancer. J Cancer Mol 2007; 3:107–12; http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.516.63&rep=rep1&type=pdf
   Google Scholar
• Wang X, Song X, Zhuo W, Fu Y, Shi H, Liang Y, Tong M, Chang G, Luo Y. The regulatory mechanism of HSP90α secretion and its function in tumor malignancy. Proc Natl Acad Sci USA 2009; 106:21288–93; doi:10.1073/pnas.0908151106 PMID:19965370.
   PubMed Web of Science ®Google Scholar
• Chen JS, Hsu YM, Chen CC, Chen LL, Lee CC, Huang TS. Secreted heat shock protein 90α induces colorectal cancer cell invasion through CD91/LRP-1 and NF-κB-mediated integrin αV expression. J Biol Chem 2010; 285:25458–66; doi:10.1074/jbc.M110.139345 PMID:20558745.
   PubMed Web of Science ®Google Scholar
• Chen WS, Chen CC, Chen LL, Lee CC, Huang TS. Secreted heat shock protein 90α (HSP90α) induces nuclear factor-κB-mediated TCF12 protein expression to down-regulate E-cadherin and to enhance colorectal cancer cell migration and invasion. J Biol Chem 2013; 288:9001–10; doi:10.1074/jbc.M112.437897 PMID:23386606.
   PubMed Web of Science ®Google Scholar
• Gopal U, Bohonowych JE, Lema-Tome C, Liu A, Garrett-Mayer E, Wang B, Isaacs JS. A novel extracellular Hsp90 mediated co-receptor function for LRP1 regulates EphA2 dependent glioblastoma cell invasion. PLoS ONE 2011; 6:e17649; doi:10.1371/journal.pone.0017649 PMID:21408136.
   PubMed Web of Science ®Google Scholar
• Nolan KD, Kaur J, Isaacs JS. Secreted heat shock protein 90 promotes prostate cancer stem cell heterogeneity. Oncotarget 2017; 8:19323–41; https://doi.org/10.18632/oncotarget.14252 PMID:28038472.
   PubMedGoogle Scholar
• Fan CS, Chen WS, Chen LL, Chen CC, Hsu YT, Chua KV, Wang HD, Huang TS. Osteopontin–integrin engagement induces HIF-1α–TCF12-mediated endothelial-mesenchymal transition to exacerbate colorectal cancer. Oncotarget 2018; 9: 4998–5015; https://doi.org/10.18632/oncotarget.23578
   Google Scholar
• Tsutsumi S, Scroggins B, Koga F, Lee MJ, Trepel J, Felts S, Carreras C, Neckers L. A small molecule cell-impermeant Hsp90 antagonist inhibits tumor cell motility and invasion. Oncogene 2008; 27:2478–87; doi:10.1038/sj.onc.1210897 PMID:17968312.
   PubMed Web of Science ®Google Scholar
• Ahn GO, Tseng D, Liao CH, Dorie MJ, Czechowicz A, Brown JM. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc Natl Acad Sci USA 2010; 107:8363–8; doi:10.1073/pnas.0911378107 PMID:20404138.
   PubMed Web of Science ®Google Scholar
• Bissell MJ, Hines WC. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med 2011; 17:320–9; doi:10.1038/nm.2328 PMID:21383745.
   PubMed Web of Science ®Google Scholar
• Lesina M, Kurkowski MU, Ludes K, Rose-John S, Treiber M, Klöppel G, Yoshimura A, Reindl W, Sipos B, Akira S et al. Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell 2011; 19:456–69; doi:10.1016/j.ccr.2011.03.009 PMID:21481788.
   PubMed Web of Science ®Google Scholar
• Zou M, Bhatia A, Dong H, Jayaprakash P, Guo J, Sahu D, Hou Y, Tsen F, Tong C, O'Brien K et al. Evolutionarily conserved dual lysine motif determines the non-chaperone function of secreted Hsp90α in tumour progression. Oncogene 2017; 36:2160–71; doi:10.1038/onc.2016.375 PMCID:PMC5386837.
   PubMed Web of Science ®Google Scholar
• Schneider C, Schmidt T, Ziske C, Tiemann K, Lee KM, Uhlinsky V, Behrens P, Sauerbruch T, Schmidt-Wolf IGH, Mühlradt PF et al. Tumour suppression induced by the macrophage activating lipopeptide MALP-2 in an ultrasound guided pancreatic carcinoma mouse model. Gut 2004; 53:355–61; doi:10.1136/gut.2003.026005.
   PubMed Web of Science ®Google Scholar
• Liu N, Furukawa T, Kobari M, Tsao MS. Comparative phenotypic studies of duct epithelial cell lines derived from normal human pancreas and pancreatic carcinoma. Am J Pathol 1998; 153:263–9; doi:10.1016/S0002-9440(10)65567-8 PMID:9665487.
   PubMed Web of Science ®Google Scholar
• Hruban RH, Volkan Adsay N, Albores-Saavedra J, Anver MR, Biankin AV, Boivin GP, Furth EE, Furukawa T, Klein A, Klimstra DS et al. Pathology of genetically engineered mouse models of pancreatic exocrine cancer: consensus report and recommendations. Cancer Res 2006; 66:95–106; doi:10.1158/0008-5472.CAN-05-2168 PMID:16397221.
   PubMed Web of Science ®Google Scholar