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Original Research

Interleukin-1β provided by KIT-competent mast cells is required for KRAS-mutant lung adenocarcinoma

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Article: e1593802 | Received 01 Aug 2018, Accepted 28 Feb 2019, Published online: 11 Apr 2019

References

  • Alberg AJ, Ford JG, Samet JM, American College of Chest Physicians. Epidemiology of lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest. 2007;132(3 Suppl):29S–55S. doi:10.1378/chest.07-1347.
  • Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108. doi:10.3322/caac.21262.
  • Cancer Genome Atlas Research Network. Comprehensive molecular profiling of lung adenocarcinoma. Nature. 2014;511(7511):543–550. doi:10.1038/nature13385.
  • Houghton AM. Mechanistic links between COPD and lung cancer. Nat Rev Cancer. 2013;13(4):233–245. doi:10.1038/nrc3477.
  • Houghton AM, Mouded M, Shapiro SD. Common origins of lung cancer and COPD. Nat Med. 2008;14(10):1023–1024. doi:10.1038/nm1008-1023.
  • Vestbo J, Hurd SS, Agusti AG, Jones PW, Vogelmeier C, Anzueto A, Barnes PJ, Fabbri LM, Martinez FJ, Nishimura M, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med. 2013;187(4):347–365. doi:10.1164/rccm.201204-0596PP.
  • Young RP, Hopkins RJ, Christmas T, Black PN, Metcalf P, Gamble GD. COPD prevalence is increased in lung cancer, independent of age, sex and smoking history. Eur Respir J. 2009;34(2):380–386. doi:10.1183/09031936.00144208.
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674. doi:10.1016/j.cell.2011.02.013.
  • Coussens LM, Pollard JW. Leukocytes in mammary development and cancer. Cold Spring Harb Perspect Biol. 2011;3(3). doi:10.1101/cshperspect.a003285.
  • Floor SL, Dumont JE, Maenhaut C, Raspe E. Hallmarks of cancer: of all cancer cells, all the time? Trends Mol Med. 2012;18(9):509–515. doi:10.1016/j.molmed.2012.06.005.
  • Swamy M, Jamora C, Havran W, Hayday A. Epithelial decision makers: in search of the ‘epimmunome’. Nat Immunol. 2010;11(8):656–665. doi:10.1038/ni.1905.
  • Blair RJ, Meng H, Marchese MJ, Ren S, Schwartz LB, Tonnesen MG, Gruber BL. Human mast cells stimulate vascular tube formation. Tryptase is a novel, potent angiogenic factor. J Clin Invest. 1997;99(11):2691–2700. doi:10.1172/JCI119458.
  • Chen R, Ning G, Zhao ML, Fleming MG, Diaz LA, Werb Z, Liu Z. Mast cells play a key role in neutrophil recruitment in experimental bullous pemphigoid. J Clin Invest. 2001;108(8):1151–1158. doi:10.1172/JCI11494.
  • Galli SJ, Kalesnikoff J, Grimbaldeston MA, Piliponsky AM, Williams CM, Tsai M. Mast cells as “tunable” effector and immunoregulatory cells: recent advances. Annu Rev Immunol. 2005:23749–23786. doi:10.1146/annurev.immunol.21.120601.141025.
  • Theoharides TC, Kempuraj D, Tagen M, Conti P, Kalogeromitros D. Differential release of mast cell mediators and the pathogenesis of inflammation. Immunol Rev. 2007:21765–21778. doi:10.1111/j.1600-065X.2007.00519.x.
  • Galli SJ, Nakae S, Tsai M. Mast cells in the development of adaptive immune responses. Nat Immunol. 2005;6(2):135–142. doi:10.1038/ni1158.
  • Kitamura Y. Heterogeneity of mast cells and phenotypic change between subpopulations. Annu Rev Immunol. 1989:759–776. doi:10.1146/annurev.iy.07.040189.000423.
  • Marone G, Triggiani M, Genovese A, De Paulis A. Role of human mast cells and basophils in bronchial asthma. Adv Immunol. 2005:88 97–160. doi:10.1016/S0065-2776(05)88004-6.
  • Metcalfe DD, Baram D, Mekori YA. Mast cells. Physiol Rev. 1997;77(4):1033–1079. doi:10.1152/physrev.1997.77.4.1033.
  • Dalton DK, Noelle RJ. The roles of mast cells in anticancer immunity. Cancer Immunol Immunother. 2012;61(9):1511–1520. doi:10.1007/s00262-012-1246-0.
  • Pittoni P, Colombo MP. The dark side of mast cell-targeted therapy in prostate cancer. Cancer Res. 2012;72(4):831–835. doi:10.1158/0008-5472.CAN-11-3110.
  • Sinnamon MJ, Carter KJ, Sims LP, Lafleur B, Fingleton B, Matrisian LM. A protective role of mast cells in intestinal tumorigenesis. Carcinogenesis. 2008;29(4):880–886. doi:10.1093/carcin/bgn040.
  • Soucek L, Lawlor ER, Soto D, Shchors K, Swigart LB, Evan GI. Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors. Nat Med. 2007;13(10):1211–1218. doi:10.1038/nm1649.
  • Theoharides TC. Mast cells and pancreatic cancer. New Eng J Med. 2008;358(17):1860–1861. doi:10.1056/NEJMcibr0801519.
  • Varricchi G, Galdiero MR, Loffredo S, Marone G, Iannone R, Marone G, Granata F. Are mast cells MASTers in cancer? Front Immunol. 2017:8424. doi:10.3389/fimmu.2017.00424.
  • Dudeck A, Dudeck J, Scholten J, Petzold A, Surianarayanan S, Kohler A, Peschke K, Vohringer D, Waskow C, Krieg T, et al. Mast cells are key promoters of contact allergy that mediate the adjuvant effects of haptens. Immunity. 2011;34(6):973–984. doi:10.1016/j.immuni.2011.03.028.
  • Feyerabend TB, Weiser A, Tietz A, Stassen M, Harris N, Kopf M, Radermacher P, Moller P, Benoist C, Mathis D, et al. Cre-mediated cell ablation contests mast cell contribution in models of antibody- and T cell-mediated autoimmunity. Immunity. 2011;35(5):832–844. doi:10.1016/j.immuni.2011.09.015.
  • Imada A, Shijubo N, Kojima H, Abe S. Mast cells correlate with angiogenesis and poor outcome in stage I lung adenocarcinoma. Eur Respir J. 2000;15(6):1087–1093. PMID:10885428.
  • Redente EF, Orlicky DJ, Bouchard RJ, Malkinson AM. Tumor signaling to the bone marrow changes the phenotype of monocytes and pulmonary macrophages during urethane-induced primary lung tumorigenesis in A/J mice. Am J Pathol. 2007;170(2):693–708. doi:10.2353/ajpath.2007.060566.
  • Stoyanov E, Uddin M, Mankuta D, Dubinett SM, Levi-Schaffer F. Mast cells and histamine enhance the proliferation of non-small cell lung cancer cells. Lung Cancer. 2012;75(1):38–44. doi:10.1016/j.lungcan.2011.05.029.
  • Xiao H, Lasser C, Shelke GV, Wang J, Radinger M, Lunavat TR, Malmhall C, Lin LH, Li J, Li L, et al. Mast cell exosomes promote lung adenocarcinoma cell proliferation - role of KIT-stem cell factor signaling. Cell Commun Signal. 2014;1264. doi:10.1186/s12964-014-0064-8.
  • Agalioti T, Giannou AD, Krontira AC, Kanellakis NI, Kati D, Vreka M, Pepe M, Spella M, Lilis I, Zazara DE, et al. Mutant KRAS promotes malignant pleural effusion formation. Nat Commun. 2017;815205. doi:10.1038/ncomms15205.
  • Giannou AD, Marazioti A, Spella M, Kanellakis NI, Apostolopoulou H, Psallidas I, Prijovich ZM, Vreka M, Zazara DE, Lilis I, et al. Mast cells mediate malignant pleural effusion formation. J Clin Invest. 2015;125(6):2317–2334. doi:10.1172/JCI79840.
  • Marazioti A, Lilis I, Vreka M, Apostolopoulou H, Kalogeropoulou A, Giopanou I, Giotopoulou GA, Krontira AC, Iliopoulou M, Kanellakis NI, et al. Myeloid-derived interleukin-1beta drives oncogenic KRAS-NF-kappaBeta addiction in malignant pleural effusion. Nat Commun. 2018;9(1):672. doi:10.1038/s41467-018-03051-z.
  • Nikitin AY, Alcaraz A, Anver MR, Bronson RT, Cardiff RD, Dixon D, Fraire AE, Gabrielson EW, Gunning WT, Haines DC, et al. Classification of proliferative pulmonary lesions of the mouse: recommendations of the mouse models of human cancers consortium. Cancer Res. 2004;64(7):2307–2316. doi:10.1158/0008-5472.CAN-03-3376.
  • Spella MLI, Vreka M, Marazioti A, Giopanou I, Aidinis V, Stathopoulos GT. An airway epithelial origin for tobacco carcinogen-induced lung adenocarcinoma. Eur Respir J. 2015:46OA4980. doi:10.1183/13993003.congress-2015.OA4980.
  • Stathopoulos GT, Sherrill TP, Cheng DS, Scoggins RM, Han W, Polosukhin VV, Connelly L, Yull FE, Fingleton B, Blackwell TS. Epithelial NF-kappaB activation promotes urethane-induced lung carcinogenesis. Proc Natl Acad Sci U S A. 2007;104(47):18514–18519. doi:10.1073/pnas.0705316104.
  • Westcott PM, Halliwill KD, To MD, Rashid M, Rust AG, Keane TM, Delrosario R, Jen KY, Gurley KE, Kemp CJ, et al. The mutational landscapes of genetic and chemical models of Kras-driven lung cancer. Nature. 2015;517(7535):489–492. doi:10.1038/nature13898.
  • Desai TJ, Brownfield DG, Krasnow MA. Alveolar progenitor and stem cells in lung development, renewal and cancer. Nature. 2014;507(7491):190–194. doi:10.1038/nature12930.
  • Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Montoya R, Jacks T, Tuveson DA. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Dev. 2001;15(24):3243–3248. doi:10.1101/gad.943001.
  • Giannou AD, Marazioti A, Kanellakis NI, Giopanou I, Lilis I, Zazara DE, Ntaliarda G, Kati D, Armenis V, Giotopoulou GA, et al. NRAS destines tumor cells to the lungs. EMBO Mol Med. 2017;9(5):672–686. doi:10.15252/emmm.201606978.
  • Giopanou I, Lilis I, Papaleonidopoulos V, Agalioti T, Kanellakis NI, Spiropoulou N, Spella M, Stathopoulos GT. Tumor-derived osteopontin isoforms cooperate with TRP53 and CCL2 to promote lung metastasis. Oncoimmunology. 2017;6(1):e1256528. doi:10.1080/2162402X.2016.1256528.
  • Stathopoulos GT, Sherrill TP, Karabela SP, Goleniewska K, Kalomenidis I, Roussos C, Fingleton B, Yull FE, Peebles RS Jr., Blackwell TS. Host-derived interleukin-5 promotes adenocarcinoma-induced malignant pleural effusion. Am J Respir Crit Care Med. 2010;182(10):1273–1281. doi:10.1164/rccm.201001-0001OC.
  • Tono T, Tsujimura T, Koshimizu U, Kasugai T, Adachi S, Isozaki K, Nishikawa S, Morimoto M, Nishimune Y, Nomura S, et al. c-kit Gene was not transcribed in cultured mast cells of mast cell-deficient Wsh/Wsh mice that have a normal number of erythrocytes and a normal c-kit coding region. Blood. 1992;80(6):1448–1453. PMID:1381627.
  • Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999;8(4):265–277. doi:10.1023/A:1008942828960.
  • Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J, et al. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature. 1992;356(6372):768–774. doi:10.1038/356768a0.
  • Michel A, Schuler A, Friedrich P, Doner F, Bopp T, Radsak M, Hoffmann M, Relle M, Distler U, Kuharev J, et al. Mast cell-deficient Kit(W-sh) “Sash” mutant mice display aberrant myelopoiesis leading to the accumulation of splenocytes that act as myeloid-derived suppressor cells. J Immunol. 2013;190(11):5534–5544. doi:10.4049/jimmunol.1203355.
  • Horai R, Asano M, Sudo K, Kanuka H, Suzuki M, Nishihara M, Takahashi M, Iwakura Y. Production of mice deficient in genes for interleukin (IL)-1alpha, IL-1beta, IL-1alpha/beta, and IL-1 receptor antagonist shows that IL-1beta is crucial in turpentine-induced fever development and glucocorticoid secretion. J Exp Med. 1998;187(9):1463–1475. doi:10.1084/jem.187.9.1463.
  • Boring L, Gosling J, Chensue SW, Kunkel SL, Farese RV Jr., Broxmeyer HE, Charo IF. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J Clin Invest. 1997;100(10):2552–2561. doi:10.1172/JCI119798.
  • Giopanou I, Lilis I, Papaleonidopoulos V, Marazioti A, Spella M, Vreka M, Papadaki H, Stathopoulos GT. Comprehensive evaluation of nuclear factor-kappaBeta expression patterns in non-small cell lung cancer. PLoS One. 2015;10(7):e0132527. doi:10.1371/journal.pone.0132527.
  • Kasprzyk A. BioMart: driving a paradigm change in biological data management. Database (Oxford). 2011:2011bar049. doi:10.1093/database/bar049.
  • Marwitz S, Depner S, Dvornikov D, Merkle R, Szczygiel M, Muller-Decker K, Lucarelli P, Wasch M, Mairbaurl H, Rabe KF, et al. Downregulation of the TGFbeta pseudoreceptor BAMBI in non-small cell lung cancer enhances TGFbeta signaling and invasion. Cancer Res. 2016;76(13):3785–3801. doi:10.1158/0008-5472.CAN-15-1326.
  • Kabbout M, Garcia MM, Fujimoto J, Liu DD, Woods D, Chow CW, Mendoza G, Momin AA, James BP, Solis L, et al. ETS2 mediated tumor suppressive function and MET oncogene inhibition in human non-small cell lung cancer. Clin Cancer Res. 2013;19(13):3383–3395. doi:10.1158/1078-0432.CCR-13-0341.
  • Gyorffy B, Surowiak P, Budczies J, Lanczky A. Online survival analysis software to assess the prognostic value of biomarkers using transcriptomic data in non-small-cell lung cancer. PLoS One. 2013;8(12):e82241. doi:10.1371/journal.pone.0082241.
  • Blumenschein GR Jr., Saintigny P, Liu S, Kim ES, Tsao AS, Herbst RS, Alden C, Lee JJ, Tang X, Stewart DJ, et al. Comprehensive biomarker analysis and final efficacy results of sorafenib in the BATTLE trial. Clin Cancer Res. 2013;19(24):6967–6975. doi:10.1158/1078-0432.CCR-12-1818.
  • Byers LA, Diao L, Wang J, Saintigny P, Girard L, Peyton M, Shen L, Fan Y, Giri U, Tumula PK, et al. An epithelial-mesenchymal transition gene signature predicts resistance to EGFR and PI3K inhibitors and identifies Axl as a therapeutic target for overcoming EGFR inhibitor resistance. Clin Cancer Res. 2013;19(1):279–290. doi:10.1158/1078-0432.CCR-12-1558.
  • Morita H, Arae K, Unno H, Miyauchi K, Toyama S, Nambu A, Oboki K, Ohno T, Motomura K, Matsuda A, et al. An interleukin-33-mast cell-interleukin-2 axis suppresses papain-induced allergic inflammation by promoting regulatory T cell numbers. Immunity. 2015;43(1):175–186. doi:10.1016/j.immuni.2015.06.021.
  • Zaynagetdinov R, Stathopoulos GT, Sherrill TP, Cheng DS, McLoed AG, Ausborn JA, Polosukhin VV, Connelly L, Zhou W, Fingleton B, et al. Epithelial nuclear factor-kappaB signaling promotes lung carcinogenesis via recruitment of regulatory T lymphocytes. Oncogene. 2012;31(26):3164–3176. doi:10.1038/onc.2011.480.
  • Ridker PM, MacFadyen JG, Thuren T, Everett BM, Libby P, Glynn RJ, Group CT. Effect of interleukin-1beta inhibition with canakinumab on incident lung cancer in patients with atherosclerosis: exploratory results from a randomised, double-blind, placebo-controlled trial. Lancet. 2017;390(10105):1833–1842. doi:10.1016/S0140-6736(17)32247-X.
  • Ridker PM, MacFadyen JG, Everett BM, Libby P, Thuren T, Glynn RJ, Group CT. Relationship of C-reactive protein reduction to cardiovascular event reduction following treatment with canakinumab: a secondary analysis from the CANTOS randomised controlled trial. Lancet. 2018;391(10118):319–328. doi:10.1016/S0140-6736(17)32814-3.
  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–682. doi:10.1038/nmeth.2019.
  • Hsia CC, Hyde DM, Ochs M, Weibel ER, Structure AEJTFoQAoL. An official research policy statement of the American Thoracic Society/European Respiratory Society: standards for quantitative assessment of lung structure. Am J Respir Crit Care Med. 2010;181(4):394–418. doi:10.1164/rccm.200809-1522ST.
  • Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, Beer DG, Powell CA, Riely GJ, Van Schil PE, et al. International association for the study of lung cancer/american thoracic society/european respiratory society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 2011;6(2):244–285. doi:10.1097/JTO.0b013e318206a221.
  • Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29(9):e45. PMID:11328886. doi:10.1093/nar/29.9.e45.
  • Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545–15550. doi:10.1073/pnas.0506580102.
  • Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175–191. PMID:17695343.