Epithelial NF-κB signaling promotes EGFR-driven lung carcinogenesis via macrophage recruitment

References

• Li AR, Chitale D, Riely GJ, Pao W, Miller VA, Zakowski MF, Rusch V, Kris MG, Ladanyi M. EGFR mutations in lung adenocarcinomas: clinical testing experience and relationship to EGFR gene copy number and immunohistochemical expression. J Mol Diagnostics 2008; 10:242-8; PMID:18403609; http://dx.doi.org/10.2353/jmoldx.2008.070178
   PubMed Web of Science ®Google Scholar
• Rosell R, Moran T, Queralt C, Porta R, Cardenal F, Camps C, Majem M, Lopez-Vivanco G, Isla D, Provencio M et al. Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med 2009; 361:958-67; PMID:19692684; http://dx.doi.org/10.1056/NEJMoa0904554
   PubMed Web of Science ®Google Scholar
• Yun CH, Boggon TJ, Li Y, Woo MS, Greulich H, Meyerson M, Eck MJ. Structures of lung cancer-derived EGFR mutants and inhibitor complexes: mechanism of activation and insights into differential inhibitor sensitivity. Cancer Cell 2007; 11:217-27; PMID:17349580; http://dx.doi.org/10.1016/j.ccr.2006.12.017
   PubMed Web of Science ®Google Scholar
• Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski MF, Kris MG, Varmus H. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005; 2:e73; PMID:15737014; http://dx.doi.org/10.1371/journal.pmed.0020073
   PubMed Web of Science ®Google Scholar
• Yun CH, Mengwasser KE, Toms AV, Woo MS, Greulich H, Wong KK, Meyerson M, Eck MJ. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci U S A 2008; 105:2070-5; PMID:18227510; http://dx.doi.org/10.1073/pnas.0709662105
   PubMed Web of Science ®Google Scholar
• Zhang Z, Ma J, Li N, Sun N, Wang C. Expression of nuclear factor-κB and its clinical significance in nonsmall-cell lung cancer. Ann Thorac Surg 2006; 82:243-8; PMID:16798222; http://dx.doi.org/10.1016/j.athoracsur.2006.01.049
   PubMed Web of Science ®Google Scholar
• Tang X, Liu D, Shishodia S, Ozburn N, Behrens C, Lee JJ, Hong WK, Aggarwal BB, Wistuba II. Nuclear factor-κB (NF-κB) is frequently expressed in lung cancer and preneoplastic lesions. Cancer 2006; 107:2637-46; PMID:17078054; http://dx.doi.org/10.1002/cncr.22315
   PubMed Web of Science ®Google Scholar
• Tichelaar JW, Zhang Y, LeRiche JC, Biddinger PW, Lam S, Anderson MW. Increased staining for phospho-Akt, p65/RELA and cIAP-2 in pre-neoplastic human bronchial biopsies. BMC Cancer 2005; 5:155; PMID:16332260; http://dx.doi.org/10.1186/1471-2407-5-155
   PubMed Web of Science ®Google Scholar
• Zaynagetdinov R, Stathopoulos GT, Sherrill TP, Cheng D-S, McLoed AG, Ausborn JA, Polosukhin VV, Connelly L, Zhou W, Fingleton B et al. Epithelial nuclear factor-κB signaling promotes lung carcinogenesis via recruitment of regulatory T lymphocytes. Oncogene 2011; 31:3164-76; PMID:22002309; http://dx.doi.org/10.1038/onc.2011.480
   PubMed Web of Science ®Google Scholar
• Stathopoulos GT, Sherrill TP, Cheng DS, Scoggins RM, Han W, Polosukhin VV, Connelly L, Yull FE, Fingleton B, Blackwell TS. Epithelial NF-κB activation promotes urethane-induced lung carcinogenesis. Proc Natl Acad Sci U S A 2007; 104:18514-9; PMID:18000061; http://dx.doi.org/10.1073/pnas.0705316104
   PubMed Web of Science ®Google Scholar
• Meylan E, Dooley AL, Feldser DM, Shen L, Turk E, Ouyang C, Jacks T. Requirement for NF-κB signalling in a mouse model of lung adenocarcinoma. Nature 2009; 462:104-7; PMID:19847165; http://dx.doi.org/10.1038/nature08462
   PubMed Web of Science ®Google Scholar
• Bassères DS, Ebbs A, Levantini E, Baldwin AS. Requirement of the NF-κB subunit p65/RelA for K-Ras-induced lung tumorigenesis. Cancer Res 2010; 70:3537-46; PMID:20406971; http://dx.doi.org/10.1158/0008-5472.CAN-09-4290
   PubMed Web of Science ®Google Scholar
• Alberti C, Pinciroli P, Valeri B, Ferri R, Ditto A, Umezawa K, Sensi M, Canevari S, Tomassetti A. Ligand-dependent EGFR activation induces the co-expression of IL-6 and PAI-1 via the NFkB pathway in advanced-stage epithelial ovarian cancer. Oncogene 2012; 31:4139-49; PMID:22158046; http://dx.doi.org/10.1038/onc.2011.572
   PubMed Web of Science ®Google Scholar
• De S, Dermawan JKT, Stark GR. EGF receptor uses SOS1 to drive constitutive activation of NFκB in cancer cells. Proc Natl Acad Sci U S A 2014; 111:11721-6; PMID:25071181; http://dx.doi.org/10.1073/pnas.1412390111
   PubMed Web of Science ®Google Scholar
• Bivona TG, Hieronymus H, Parker J, Chang K, Taron M, Rosell R, Moonsamy P, Dahlman K, Miller VA, Costa C et al. FAS and NF-κB signalling modulate dependence of lung cancers on mutant EGFR. Nature 2011; 471:523-6; PMID:21430781; http://dx.doi.org/10.1038/nature09870
   PubMed Web of Science ®Google Scholar
• Galvani E, Sun J, Leon LG, Sciarrillo R, Narayan RS, Tjin Tham Sjin R, Lee K, Ohashi K, Heideman DAM, Alfieri RR et al. NF-κB drives acquired resistance to a novel mutant-selective EGFR inhibitor. Oncotarget 2015; 6:42717-32; PMID:26015408; http://dx.doi.org/10.18632/oncotarget.3956
   PubMed Web of Science ®Google Scholar
• Blakely CM, Pazarentzos E, Olivas V, Asthana S, Yan JJ, Tan I, Hrustanovic G, Chan E, Lin L, Neel DS et al. NF-κB-activating complex engaged in response to EGFR oncogene inhibition drives tumor cell survival and residual disease in lung cancer. Cell Rep 2015; 11:98-110; PMID:25843712; http://dx.doi.org/10.1016/j.celrep.2015.03.012
   PubMed Web of Science ®Google Scholar
• Lantermann AB, Chen D, McCutcheon K, Hoffman G, Frias E, Ruddy D, Rakiec D, Korn J, McAllister G, Stegmeier F et al. Inhibition of casein kinase 1 α prevents acquired drug resistance to erlotinib in EGFR-mutant non–small cell lung cancer. Cancer Res 2015; 75:1-12; PMID:26490646; http://dx.doi.org/10.1158/0008-5472.CAN-15-1113
   Web of Science ®Google Scholar
• Politi K, Zakowski MF, Fan PD, Schonfeld EA, Pao W, Varmus HE. Lung adenocarcinomas induced in mice by mutant EGF receptors found in human lung cancers respond to a tyrosine kinase inhibitor or to down-regulation of the receptors. Genes Dev 2006; 20:1496-510; PMID:16705038; http://dx.doi.org/10.1101/gad.1417406
   PubMed Web of Science ®Google Scholar
• Cheng DS, Han W, Chen SM, Sherrill TP, Chont M, Park GY, Sheller JR, Polosukhin VV, Christman JW, Yull FE et al. Airway epithelium controls lung inflammation and injury through the through the NF-κB pathway. J Immunol 2007; 178:6504-13; PMID:17475880; http://dx.doi.org/10.4049/jimmunol.178.10.6504
   PubMed Web of Science ®Google Scholar
• Pierce J, Schoenleber R, Jesmok G, Best J, Moore S, Collins T, Gerritsen M. Novel inhibitors of cytokine-induced IκBα phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem 1997; 272:21096-103; PMID:9261113; http://dx.doi.org/10.1074/jbc.272.34.21096
   PubMed Web of Science ®Google Scholar
• Ramirez RD, Sheridan S, Girard L, Sato M, Kim Y, Pollack J, Peyton M, Zou Y, Kurie JM, Dimaio JM et al. Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res 2004; 64:9027-34; PMID:15604268; http://dx.doi.org/10.1158/0008-5472.CAN-04-3703
   PubMed Web of Science ®Google Scholar
• Sato M, Vaughan MB, Girard L, Peyton M, Lee W, Shames DS, Ramirez RD, Sunaga N, Gazdar AF, Shay JW et al. Multiple oncogenic changes (K-RAS(V12), p53 knockdown, mutant EGFRs, p16 bypass, telomerase) are not sufficient to confer a full malignant phenotype on human bronchial epithelial cells. Cancer Res 2006; 66:2116-28; PMID:16489012; http://dx.doi.org/10.1158/0008-5472.CAN-05-2521
   PubMed Web of Science ®Google Scholar
• Regales L, Balak MN, Gong Y, Politi K, Sawai A, Le C, Koutcher JA, Solit DB, Rosen N, Zakowski MF et al. Development of new mouse lung tumor models expressing EGFR T790M mutants associated with clinical resistance to kinase inhibitors. PLoS One 2007; 2:e810; PMID:17726540; http://dx.doi.org/10.1371/journal.pone.0000810
   PubMed Web of Science ®Google Scholar
• Everhart MB, Han W, Parman KS, Polosukhin VV, Zeng H, Sadikot RT, Li B, Yull FE, Christman JW, Blackwell TS. Intratracheal administration of liposomal clodronate accelerates alveolar macrophage reconstitution following fetal liver transplantation. J Leukoc Biol 2005; 77:173-80; PMID:15563581; http://dx.doi.org/10.1189/jlb.1203647
   PubMed Web of Science ®Google Scholar
• Zaynagetdinov R, Sherrill TP, Polosukhin V V, Han W, Ausborn JA, McLoed AG, McMahon FB, Gleaves LA, Degryse AL, Stathopoulos GT et al. A critical role for macrophages in promotion of urethane-induced lung carcinogenesis. J Immunol 2011; 187:5703-11; PMID:22048774; http://dx.doi.org/10.4049/jimmunol.1100558
   PubMed Web of Science ®Google Scholar
• Lee HJ, Zhuang G, Cao Y, Du P, Kim HJ, Settleman J. Drug resistance via feedback activation of Stat3 in oncogene-addicted cancer cells. Cancer Cell 2014; 26:207-21; PMID:25065853; http://dx.doi.org/10.1016/j.ccr.2014.05.019
   PubMed Web of Science ®Google Scholar
• Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008; 454:436-44; PMID:18650914; http://dx.doi.org/10.1038/nature07205
   PubMed Web of Science ®Google Scholar
• Ji H, Houghton AM, Mariani TJ, Perera S, Kim CB, Padera R, Tonon G, McNamara K, Marconcini LA, Hezel A et al. K-ras activation generates an inflammatory response in lung tumors. Oncogene 2006; 25:2105-12; PMID:16288213; http://dx.doi.org/10.1038/sj.onc.1209237
   PubMed Web of Science ®Google Scholar
• Xia Y, Yeddula N, Leblanc M, Ke E, Zhang Y, Oldfield E, Shaw RJ, Verma IM. Reduced cell proliferation by IKK2 depletion in a mouse lung-cancer model. Nat Cell Biol 2012; 14:257-65; PMID:22327365; http://dx.doi.org/10.1038/ncb2428
   PubMed Web of Science ®Google Scholar
• Hopewell EL, Zhao W, Fulp WJ, Bronk CC, Lopez AS, Massengill M, Antonia S, Celis E, Haura EB, Enkemann SA et al. Lung tumor NF-κB signaling promotes T cell-mediated immune surveillance. J Clin Invest 2013; 123:2509-22; PMID:23635779; http://dx.doi.org/10.1172/JCI67250
   PubMed Web of Science ®Google Scholar
• Gregory AD, Houghton AM. Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res 2011; 71:2411-6; PMID:21427354; http://dx.doi.org/10.1158/0008-5472.CAN-10-2583
   PubMed Web of Science ®Google Scholar
• Sparmann A, Bar-Sagi D. Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell 2004; 6:447-58; PMID:15542429; http://dx.doi.org/10.1016/j.ccr.2004.09.028
   PubMed Web of Science ®Google Scholar
• Bellocq A, Antoine M, Flahault A, Philippe C, Crestani B, Bernaudin JF, Mayaud C, Milleron B, Baud L, Cadranel J. Neutrophil alveolitis in bronchioloalveolar carcinoma: induction by tumor-derived interleukin-8 and relation to clinical outcome. Am J Pathol 1998; 152:83-92; PMID:9422526
   PubMed Web of Science ®Google Scholar
• Houghton AM, Rzymkiewicz DM, Ji H, Gregory AD, Egea EE, Metz HE, Stolz DB, Land SR, Marconcini LA, Kliment CR et al. Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat Med 2010; 16:219-23; PMID:20081861; http://dx.doi.org/10.1038/nm.2084
   PubMed Web of Science ®Google Scholar
• Noy R, Pollard J. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014; 41:49-61; PMID:25035953; http://dx.doi.org/10.1016/j.immuni.2014.06.010
   PubMed Web of Science ®Google Scholar
• Tichelaar JW, Lu W, Whitsett JA. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J Biol Chem 2000; 275:11858-64; PMID:10766812; http://dx.doi.org/10.1074/jbc.275.16.11858
   PubMed Web of Science ®Google Scholar
• Rice WR, Conkright JJ, Na CL, Ikegami M, Shannon JM, Weaver TE. Maintenance of the mouse type II cell phenotype in vitro. Am J Physiol Lung Cell Mol Physiol 2002; 283:L256-64; PMID:12114186; http://dx,doi.org/10.1152/ajplung.00302.2001
   PubMed Web of Science ®Google Scholar
• Spandidos A, Wang X, Wang H, Seed B. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 2010; 38:D792-9; PMID:19906719; http://dx.doi.org/10.1093/nar/gkp1005
   PubMed Web of Science ®Google Scholar
• Spandidos A, Wang X, Wang H, Dragnev S, Thurber T, Seed B. A comprehensive collection of experimentally validated primers for polymerase chain reaction quantitation of murine transcript abundance. BMC Genomics 2008; 9:633; PMID:19108745; http://dx.doi.org/10.1186/1471-2164-9-633
   PubMed Web of Science ®Google Scholar
• Wang X, Seed B. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 2003; 31:e154; PMID:14654707; http://dx.doi.org/10.1093/nar/gng154
   PubMed Web of Science ®Google Scholar
• Boxio R, Bossenmeyer-Pourie C, Steinckwich N, Dournon C, Nu O. Mouse bone marrow contains large numbers of functionally competent neutrophils. J Leukoc Biol 2004; 75:604-11; PMID:14694182; http://dx.doi.org/10.1189/jlb.0703340
   PubMed Web of Science ®Google Scholar
• Sai J, Raman D, Liu Y, Wikswo J, Richmond A. Parallel phosphatidylinositol 3-kinase (PI3K)-dependent and Src-dependent pathways lead to CXCL8-mediated Rac2 activation and chemotaxis. J Biol Chem 2008; 283:26538-47; PMID:18662984; http://dx.doi.org/10.1074/jbc.M805611200
   PubMed Web of Science ®Google Scholar
• Munder P, Modolell M, Hoelzl Wallach D. Cell propagation on films of polymeric fluorocarbon as a means to regulate pericellular pH and pO(2) in cultured monolayers. FEBS Lett 1971; 15:191-6; PMID:11945843; http://dx.doi.org/10.1016/0014-5793(71)80309-5
   PubMed Web of Science ®Google Scholar
• Xue W, Meylan E, Oliver TG, Feldser DM, Winslow MM, Bronson R, Jacks T. Response and resistance to NF-κB inhibitors in mouse models of lung adenocarcinoma. Cancer Discov 2011; 1:236-47; PMID:21874163; http://dx.doi.org/10.1158/2159-8290.CD-11-0073
   PubMed Web of Science ®Google Scholar