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

OncoImmunology

Volumn 5, Issue 6, 2016, Pages

  Saxon, Jamie A ^a   Sherrill, Taylor P ^b   Polosukhin, Vasiliy V ^b   Sai, Jiqing ^a   Zaynagetdinov, Rinat ^b   McLoed, Allyson G ^a   Gulleman, Peter M ^b   Barham, Whitney ^a   Cheng, Dong Sheng ^b   Hunt, Raphael P ^b   Gleaves, Linda A ^b   Richmond, Ann ^a,c   Young, Lisa R ^a,b   Yull, Fiona E ^a   Blackwell, Timothy S ^a,b,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

EGFR; lung cancer; macrophage; neutrophil; NF B

Indexed keywords

DOXYCYCLINE; ERLOTINIB; GEFITINIB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G;

ARTICLE; CELL POPULATION; CELL SURVIVAL; COMPUTER ASSISTED TOMOGRAPHY; FLOW CYTOMETRY; HISTOLOGY; HUMAN; LUNG CARCINOGENESIS; MACROPHAGE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR VOLUME; WESTERN BLOTTING;

EID: 84976522840     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1168549     Document Type: Article

References (45)

1. A.R.Li, D.Chitale, G.J.Riely, W.Pao, V.A.Miller, M.F.Zakowski, V.Rusch, M.G.Kris, M.Ladanyi. 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; 10.2353/jmoldx.2008.070178
2. R.Rosell, T.Moran, C.Queralt, R.Porta, F.Cardenal, C.Camps, M.Majem, G.Lopez-Vivanco, D.Isla, M.Provencio et al. Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med 2009; 361:958-67; PMID:19692684; 10.1056/NEJMoa0904554
3. C.H.Yun, T.J.Boggon, Y.Li, M.S.Woo, H.Greulich, M.Meyerson, M.J.Eck. 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; 10.1016/j.ccr.2006.12.017
4. W.Pao, V.A.Miller, K.A.Politi, G.J.Riely, R.Somwar, M.F.Zakowski, M.G.Kris, H.Varmus. 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; 10.1371/journal.pmed.0020073
5. C.H.Yun, K.E.Mengwasser, A.V.Toms, M.S.Woo, H.Greulich, K.K.Wong, M.Meyerson, M.J.Eck. 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; 10.1073/pnas.0709662105
6. Z.Zhang, J.Ma, N.Li, N.Sun, C.Wang. Expression of nuclear factor-κB and its clinical significance in nonsmall-cell lung cancer. Ann Thorac Surg 2006; 82:243-8; PMID:16798222; 10.1016/j.athoracsur.2006.01.049
7. X.Tang, D.Liu, S.Shishodia, N.Ozburn, C.Behrens, J.J.Lee, W.K.Hong, B.B.Aggarwal, I.I.Wistuba. Nuclear factor-κB (NF-κB) is frequently expressed in lung cancer and preneoplastic lesions. Cancer 2006; 107:2637-46; PMID:17078054; 10.1002/cncr.22315
8. J.W.Tichelaar, Y.Zhang, J.C.LeRiche, P.W.Biddinger, S.Lam, M.W.Anderson. Increased staining for phospho-Akt, p65/RELA and cIAP-2 in pre-neoplastic human bronchial biopsies. BMC Cancer 2005; 5:155; PMID:16332260; 10.1186/1471-2407-5-155
9. R.Zaynagetdinov, G.T.Stathopoulos, T.P.Sherrill, D.-S.Cheng, A.G.McLoed, J.A.Ausborn, V.V.Polosukhin, L.Connelly, W.Zhou, B.Fingleton et al. Epithelial nuclear factor-κB signaling promotes lung carcinogenesis via recruitment of regulatory T lymphocytes. Oncogene 2011; 31:3164-76; PMID:22002309; 10.1038/onc.2011.480
10. G.T.Stathopoulos, T.P.Sherrill, D.S.Cheng, R.M.Scoggins, W.Han, V.V.Polosukhin, L.Connelly, F.E.Yull, B.Fingleton, T.S.Blackwell. Epithelial NF-κB activation promotes urethane-induced lung carcinogenesis. Proc Natl Acad Sci U S A 2007; 104:18514-9; PMID:18000061; 10.1073/pnas.0705316104
11. E.Meylan, A.L.Dooley, D.M.Feldser, L.Shen, E.Turk, C.Ouyang, T.Jacks. Requirement for NF-κB signalling in a mouse model of lung adenocarcinoma. Nature 2009; 462:104-7; PMID:19847165; 10.1038/nature08462
12. D.S.Bassères, A.Ebbs, E.Levantini, A.S.Baldwin. Requirement of the NF-κB subunit p65/RelA for K-Ras-induced lung tumorigenesis. Cancer Res 2010; 70:3537-46; PMID:20406971; 10.1158/0008-5472.CAN-09-4290
13. C.Alberti, P.Pinciroli, B.Valeri, R.Ferri, A.Ditto, K.Umezawa, M.Sensi, S.Canevari, A.Tomassetti. 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; 10.1038/onc.2011.572
14. S.De, J.K.T.Dermawan, G.R.Stark. 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; 10.1073/pnas.1412390111
15. T.G.Bivona, H.Hieronymus, J.Parker, K.Chang, M.Taron, R.Rosell, P.Moonsamy, K.Dahlman, V.A.Miller, C.Costa et al. FAS and NF-κB signalling modulate dependence of lung cancers on mutant EGFR. Nature 2011; 471:523-6; PMID:21430781; 10.1038/nature09870
16. E.Galvani, J.Sun, L.G.Leon, R.Sciarrillo, R.S.Narayan, R.Tjin Tham Sjin, K.Lee, K.Ohashi, D.A.M.Heideman, R.R.Alfieri et al. NF-κB drives acquired resistance to a novel mutant-selective EGFR inhibitor. Oncotarget 2015; 6:42717-32; PMID:26015408; 10.18632/oncotarget.3956
17. C.M.Blakely, E.Pazarentzos, V.Olivas, S.Asthana, J.J.Yan, I.Tan, G.Hrustanovic, E.Chan, L.Lin, D.S.Neel 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; 10.1016/j.celrep.2015.03.012
18. A.B.Lantermann, D.Chen, K.McCutcheon, G.Hoffman, E.Frias, D.Ruddy, D.Rakiec, J.Korn, G.McAllister, F.Stegmeier 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; 10.1158/0008-5472.CAN-15-1113
19. K.Politi, M.F.Zakowski, P.D.Fan, E.A.Schonfeld, W.Pao, H.E.Varmus. 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; 10.1101/gad.1417406
20. D.S.Cheng, W.Han, S.M.Chen, T.P.Sherrill, M.Chont, G.Y.Park, J.R.Sheller, V.V.Polosukhin, J.W.Christman, F.E.Yull et al. Airway epithelium controls lung inflammation and injury through the through the NF-κB pathway. J Immunol 2007; 178:6504-13; PMID:17475880; 10.4049/jimmunol.178.10.6504
21. J.Pierce, R.Schoenleber, G.Jesmok, J.Best, S.Moore, T.Collins, M.Gerritsen. 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; 10.1074/jbc.272.34.21096
22. R.D.Ramirez, S.Sheridan, L.Girard, M.Sato, Y.Kim, J.Pollack, M.Peyton, Y.Zou, J.M.Kurie, J.M.Dimaio et al. Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res 2004; 64:9027-34; PMID:15604268; 10.1158/0008-5472.CAN-04-3703
23. M.Sato, M.B.Vaughan, L.Girard, M.Peyton, W.Lee, D.S.Shames, R.D.Ramirez, N.Sunaga, A.F.Gazdar, J.W.Shay 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; 10.1158/0008-5472.CAN-05-2521
24. L.Regales, M.N.Balak, Y.Gong, K.Politi, A.Sawai, C.Le, J.A.Koutcher, D.B.Solit, N.Rosen, M.F.Zakowski 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; 10.1371/journal.pone.0000810
25. M.B.Everhart, W.Han, K.S.Parman, V.V.Polosukhin, H.Zeng, R.T.Sadikot, B.Li, F.E.Yull, J.W.Christman, T.S.Blackwell. Intratracheal administration of liposomal clodronate accelerates alveolar macrophage reconstitution following fetal liver transplantation. J Leukoc Biol 2005; 77:173-80; PMID:15563581; 10.1189/jlb.1203647
26. R.Zaynagetdinov, T.P.Sherrill, V.V.Polosukhin, W.Han, J.A.Ausborn, A.G.McLoed, F.B.McMahon, L.A.Gleaves, A.L.Degryse, G.T.Stathopoulos et al. A critical role for macrophages in promotion of urethane-induced lung carcinogenesis. J Immunol 2011; 187:5703-11; PMID:22048774; 10.4049/jimmunol.1100558
27. H.J.Lee, G.Zhuang, Y.Cao, P.Du, H.J.Kim, J.Settleman. Drug resistance via feedback activation of Stat3 in oncogene-addicted cancer cells. Cancer Cell 2014; 26:207-21; PMID:25065853; 10.1016/j.ccr.2014.05.019
28. A.Mantovani, P.Allavena, A.Sica, F.Balkwill. Cancer-related inflammation. Nature 2008; 454:436-44; PMID:18650914; 10.1038/nature07205
29. H.Ji, A.M.Houghton, T.J.Mariani, S.Perera, C.B.Kim, R.Padera, G.Tonon, K.McNamara, L.A.Marconcini, A.Hezel et al. K-ras activation generates an inflammatory response in lung tumors. Oncogene 2006; 25:2105-12; PMID:16288213; 10.1038/sj.onc.1209237
30. Y.Xia, N.Yeddula, M.Leblanc, E.Ke, Y.Zhang, E.Oldfield, R.J.Shaw, I.M.Verma. Reduced cell proliferation by IKK2 depletion in a mouse lung-cancer model. Nat Cell Biol 2012; 14:257-65; PMID:22327365; 10.1038/ncb2428
31. E.L.Hopewell, W.Zhao, W.J.Fulp, C.C.Bronk, A.S.Lopez, M.Massengill, S.Antonia, E.Celis, E.B.Haura, S.A.Enkemann et al. Lung tumor NF-κB signaling promotes T cell-mediated immune surveillance. J Clin Invest 2013; 123:2509-22; PMID:23635779; 10.1172/JCI67250
32. A.D.Gregory, A.M.Houghton. Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res 2011; 71:2411-6; PMID:21427354; 10.1158/0008-5472.CAN-10-2583
33. A.Sparmann, D.Bar-Sagi. Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell 2004; 6:447-58; PMID:15542429; 10.1016/j.ccr.2004.09.028
34. A.Bellocq, M.Antoine, A.Flahault, C.Philippe, B.Crestani, J.F.Bernaudin, C.Mayaud, B.Milleron, L.Baud, J.Cadranel. 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
35. A.M.Houghton, D.M.Rzymkiewicz, H.Ji, A.D.Gregory, E.E.Egea, H.E.Metz, D.B.Stolz, S.R.Land, L.A.Marconcini, C.R.Kliment et al. Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat Med 2010; 16:219-23; PMID:20081861; 10.1038/nm.2084
36. R.Noy, J.Pollard. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014; 41:49-61; PMID:25035953; 10.1016/j.immuni.2014.06.010
37. J.W.Tichelaar, W.Lu, J.A.Whitsett. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J Biol Chem 2000; 275:11858-64; PMID:10766812; 10.1074/jbc.275.16.11858
38. 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; 10.1152/ajplung.00302.2001
39. A.Spandidos, X.Wang, H.Wang, B.Seed. 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; 10.1093/nar/gkp1005
40. A.Spandidos, X.Wang, H.Wang, S.Dragnev, T.Thurber, B.Seed. A comprehensive collection of experimentally validated primers for polymerase chain reaction quantitation of murine transcript abundance. BMC Genomics 2008; 9:633; PMID:19108745; 10.1186/1471-2164-9-633
41. X.Wang, B.Seed. A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 2003; 31:e154; PMID:14654707; 10.1093/nar/gng154
42. R.Boxio, C.Bossenmeyer-Pourie, N.Steinckwich, C.Dournon, O.Nu. Mouse bone marrow contains large numbers of functionally competent neutrophils. J Leukoc Biol 2004; 75:604-11; PMID:14694182; 10.1189/jlb.0703340
43. J.Sai, D.Raman, Y.Liu, J.Wikswo, A.Richmond. 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; 10.1074/jbc.M805611200
44. P.Munder, M.Modolell, D.Hoelzl Wallach. 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; 10.1016/0014-5793(71)80309-5
45. W.Xue, E.Meylan, T.G.Oliver, D.M.Feldser, M.M.Winslow, R.Bronson, T.Jacks. Response and resistance to NF-κB inhibitors in mouse models of lung adenocarcinoma. Cancer Discov 2011; 1:236-47; PMID:21874163; 10.1158/2159-8290.CD-11-0073