IL6 trans-signaling promotes KRAS-driven lung carcinogenesis

Cancer Research

Volumn 76, Issue 4, 2016, Pages 866-876

  Brooks, Gavin D ^a   McLeod, Louise ^a   Alhayyani, Sultan ^a   Miller, Alistair ^a   Russell, Prudence A ^b,c   Ferlin, Walter ^d   Rose John, Stefan ^e   Ruwanpura, Saleela ^a   Jenkins, Brendan J ^a  

^a MONASH UNIVERSITY   (Australia)

^b ST VINCENT S HOSPITAL   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d NOVIMMUNE SA   (Switzerland)

^e UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; INTERLEUKIN 6 RECEPTOR ANTIBODY; RECEPTOR ANTIBODY; SGP 130FC; STAT3 PROTEIN; UNCLASSIFIED DRUG; PROTEIN P21;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOMA IN SITU; CONTROLLED STUDY; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; KNOCKOUT MOUSE; KRAS GENE; LUNG ADENOCARCINOMA; LUNG CARCINOGENESIS; MALE; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FAMILY; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR INVASION; UPREGULATION; ANIMAL; CELL TRANSFORMATION; DISEASE MODEL; GENETICS; LUNG TUMOR; METABOLISM; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; HUMANS; INTERLEUKIN-6; LUNG NEOPLASMS; MICE; PROTO-ONCOGENE PROTEINS P21(RAS); SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84960338835     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-2388     Document Type: Article

References (50)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
2. Walser T, Cui X, Yanagawa J, Lee JM, Heinrich E, Lee G, et al. Smoking and lung cancer: the role of inflammation. Proc Am Thorac Soc 2008;5:811-5.
3. Gerber DE. EGFR inhibition in the treatment of non-small cell lung cancer. Drug Dev Res 2008;69:359-72.
4. Ahrendt S, Decker PA, Alawi EA, Zhu YR, Sanchez-Cespedes M, Yang SC, et al. Cigarette smoking is strongly associated with mutation of the K-ras gene in patients with primary adenocarcinoma of the lung. Cancer 2001 92:1525-30.
5. BroseMS, Volpe P, FeldmanM, KumarM, Rishi I,Gerrero R, et al. BRAF and RAS mutations in human lung cancer and melanoma. Cancer Res 2002; 62:6997-7000.
6. Riely GJ, Kris MG, Rosenbaum D, Marks J, Li A, Chitale DA, et al. Frequency and distinctive spectrum of KRAS mutations in never smokers with lung adenocarcinoma. Clin Cancer Res 2008;14:5731-4.
7. Jackson E, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev 2001;15:3243-8.
8. DuPage M, Dooley AL, Jacks T. Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase. Nat Protoc 2009;4:1064-72.
9. Zhu Z, Aref AR, Cohoon TJ, Barbie TU, Imamura Y, Yang S, et al. Inhibition of KRAS-driven tumorigenicity by interruption of an autocrine cytokine circuit. Cancer Discov 2014;4:452-65.
10. Garbers C, Hermanns H, Schaper F, Müller-Newen G, Grötzinger J, Rose-John S, et al. Plasticity and cross-talk of interleukin 6-type cytokines. Cytokine Growth Factor Rev 2012;23:85-97.
11. Lapeire L, Hendrix A, Lambein K, Van Bockstal M, Braems G, Van Den Broecke R, et al. Cancer-associated adipose tissue promotes breast cancer progression by paracrine oncostatin M and Jak/STAT3 signaling. Cancer Res 2014;74:6806-19.
12. SommerJ, Effenberger T, Volpi E, Waetzig GH, BernhardtM, Suthaus J, et al. Constitutively active mutant gp130 receptor protein from inflammatory hepatocellular adenoma is inhibited by an anti-gp130 antibody that specifically neutralizes interleukin 11 signaling. J Biol Chem 2012;287: 13743-51.
13. Ernst M, Najdovska M, Grail D, Lundgren-May T, Buchert M, Tye H, et al. STAT3 and STAT1 mediate IL-11-dependent and inflammation-associated gastric tumorigenesis in gp130 receptor mutant mice. J Clin Invest 2008; 118:1727-38.
14. Yu H, Yue X, Zhao Y, Li X, Wu L, Zhang C, et al. LIF negatively regulates tumor-suppressor p53 through Stat3/ID1/MDM2 in colorectal cancers. Nat Commun 2014;5:5218.
15. Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S, et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009;15:103-13.
16. Lesina M, Kurkowski MU, Ludes K, Rose-John S, Treiber M, Klöppel G, 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.
17. Tan X, Carretero J, Chen Z, Zhang J, Wang Y, Chen J, et al. Loss of p53 attenuates the contribution of IL-6 deletion on suppressed tumor progression and extended survival in Kras-driven murine lung cancer. PLoS One 2013;8:e80885.
18. Ochoa CE,Mirabolfathinejad S, Venado AR, Evans SE, GageaM, Evans CM, et al. Interleukin 6, but not T helper 2 cytokines, promotes lung carcinogenesis. Cancer Prev Res 2010;4:51-64.
19. Yanagawa H, Sone S, Takahashi Y, Haku T, Yano S, Shinohara T, et al. Serum levels of interleukin 6 in patients with lung cancer. Br J Cancer 1995 71:1095-8.
20. Yeh H, Lai WW, Chen HH, Liu HS, Su WC. Autocrine IL-6-induced Stat3 activation contributes to the pathogenesis of lung adenocarcinoma and malignant pleural effusion. Oncogene 2006 25:4300-9.
21. Gao S, Mark KG, Leslie K, Pao W, Motoi N, Gerald WL, et al. Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. J Clin Invest 2007;117:3846-56.
22. Haura EB, Livingston S, Coppola D. Autocrine interleukin-6/interleukin-6 receptor stimulation in non-small-cell lung cancer. Clin Lung Cancer 2006;7:273-5.
23. Gomes M, Coelho A, Araujo A, Azevedo A, Teixeira AL, Catarino R, et al. IL-6 polymorphism in non-small cell lung cancer: a prognostic value? Tumor Biol 2015;36:3679-84.
24. Rose-John S, Scheller J, Elson G, Jones SA. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol 2006;80:227-36.
25. Heinrich P, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signaling and its regulation. Biochem J 2003;374:1-20.
26. Nowell M, Williams AS, Carty SA, Scheller J, Hayes AJ, Jones GW, et al. Therapeutic targeting of IL-6 trans signaling counteracts STAT3 control of experimental inflammatory arthritis. J Immunol 2009;182:613-22.
27. Greenhill CJ, Rose-John S, Lissilaa R, Ferlin W, Ernst M, Hertzog PJ, et al. IL-6 trans-signaling modulates TLR4-dependent inflammatory responses via STAT3. J Immunol 2011;186:1199-208.
28. Atreya R, Mudter J, Finotto S, Mullberg J, Jostock T, Wirtz S, et al. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in crohn disease and experimental colitis in vivo. Nat Med 2000;6:583-8.
29. Becker C, Fantini MC, SchrammC, Lehr HA, Wirtz S, Nikolaev A, et al. TGFbeta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity 2004;21:491-501.
30. Ruwanpura SM, McLeod L, Miller A, Jones J, Bozinovski S, Vlahos R, et al. Interleukin-6 promotes pulmonary emphysema associated with apoptosis in mice. Am J Respir Cell Mol Biol 2011;45:720-30.
31. Jenkins BJ, Grail D, Nheu T, Najdovska M, Wang B, Waring P, et al. Hyperactivation of Stat3 in gp130 mutant mice promotes gastric hyperproliferation and desensitizes TGF-beta signaling. Nat Med 2005; 11:845-52.
32. Ruwanpura SM, McLeod L, Miller A, Jones J, Vlahos R, Ramm G, et al. Deregulated Stat3 signaling dissociates pulmonary inflammation from emphysema in gp130 mutant mice. Am J Physiol Lung Cell Mol Physiol 2012;302:L627-39.
33. Rabe B, Chalaris A, May U, Waetzig GH, Seegert D, Williams AS, et al. Transgenic blockade of interleukin 6 transsignaling abrogates inflammation. Blood 2008;111:1021-8.
34. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 1994;368:339-42.
35. Lissilaa R, Buatois V, Magistrelli G,Williams AS, Jones GW, Herren S, et al. Although IL-6 trans-signaling is sufficient to drive local immune responses, classical IL-6 signaling is obligate for the induction of T cell-mediated autoimmunity. J Immunol 2010;185:5512-21.
36. Lacroix M, Rousseau F, Guilhot F, Malinge P, Magistrelli G, Herren S, et al. Novel insights into IL-6 cis-and trans-signaling pathways by differentially manipulating the assembly of the IL-6 signaling complex. J Biol Chem 2015 Sep 11. [Epub ahead of print].
37. Miller A, McLeod L, Brooks G, Ruwanpura S, Jenkins BJ. Differential involvement of gp130 signaling pathways in modulating tobacco carcinogen-induced lung tumorigenesis. Oncogene 2015;34:1510-9.
38. Kennedy CL, Najdovska M, Tye H, McLeod L, Yu L, Jarnicki A, et al. Differential role of MyD88 and Mal/TIRAP in TLR2-mediated gastric tumorigenesis. Oncogene 2014;33:2540-6.
39. Tye H, Kennedy C, Najdovska M, McLeod L, McCormackW, Hughes N, et al. STAT3-Driven Upregulation of TLR2 Promotes Gastric Tumorigenesis Independent of Tumor Inflammation. Cancer Cell 2012;22: 466-78.
40. Grabner B, Schramek D, Mueller KM,Moll HP, Svinka J, Hoffmann T, et al. Disruption of STAT3 signaling promotes KRAS-induced lung tumorigenesis. Nat Commun 2015;6:6285-98.
41. Jerome-Marson V,Mazieres J, Groussard O, Garcia O, Berjaud J, Dahan M, et al. Expression of TTF-1 and cytokeratins in primary and secondary epithelial lung tumors: correlation with histological type and grade. Histopathology 2004;45:125-34.
42. Ji H, Houghton AM, Mariani TJ, Perera S, Kim CB, Padera R, et al. K-ras activation generates an inflammatory response in lung tumors. Oncogene 2006;25:2105-12.
43. McClelland MR, Carskadon S, Zhao L, White ES, Beer DG, Orringer MB, et al. Diversity of the angiogenic phenotype in non-small cell lung cancer. Am J Respir Cell Mol Biol 2007;36:343-50.
44. Yang Q, Shen SS, Zhou S, Ni J, Chen D, Wang G, et al. STAT3 activation and aberrant ligand-dependent sonic hedgehog signaling in human pulmonary adenocarcinoma. Exp Mol Pathol 2012;93:227-36.
45. Jostock T, Müllberg J, Ozbek S, Atreya R, Blinn G, Voltz N, et al. Soluble gp130 is the natural inhibitor of soluble interleukin-6 receptor transsignaling responses. Eur J Biochem 2001;268:160-7.
46. Calabrese LH, Rose-John S. IL-6 biology: implications for clinical targeting in rheumatic disease. Nat Rev Rheumatol 2014;10:720-7.
47. Song L, Rawal B, Nemeth JA, Haura EB. JAK1 activates STAT3 activity in non-small-cell lung cancer cells and IL-6 neutralizing antibodies can suppress JAK1-STAT3 signaling. Mol Cancer Ther 2011;10:481-94.
48. Bayliss TJ, Smith JT, Schuster M, Dragnev KH, Rigas JR. A humanized anti-IL-6 antibody (ALD518) in non-small cell lung cancer. Expert Opin Biol Ther 2011;11:1663-8.
49. Ancrile B, Lim K, Counter CM. Oncogenic Ras-induced secretion of IL6 is required for tumorigenesis. Genes Dev 2007;21:1714-9.
50. Takeda K, Clausen BE, Kaisho T, Tsujimura T, Terada N, Forster I, et al. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 1999; 10:39-49.