Interactions between neutrophils and non-small cell lung cancer cells: enhancement of tumor proliferation and inflammatory mediator synthesis

Cancer Immunology, Immunotherapy

Volumn 63, Issue 12, 2014, Pages 1297-1306

  Hattar, Katja ^a   Franz, Katharina ^a   Ludwig, Michael ^b   Sibelius, Ulf ^a   Wilhelm, Jochen ^a   Lohmeyer, Jürgen ^a   Savai, Rajkumar ^d   Subtil, Florentine S B ^c   Dahlem, Gabriele ^a   Eul, Bastian ^a   Seeger, Werner ^a,d   Grimminger, Friedrich ^a   Grandel, Ulrich ^a  

^a JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

A549 cells; COX 2; Elastase; Inflammation; Lung cancer; Neutrophils

Indexed keywords

CYCLOOXYGENASE 2; INDOMETACIN; LEUKOCYTE ELASTASE; LIPOPOLYSACCHARIDE; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; OXYGEN RADICAL; PROSTAGLANDIN E2; SUPEROXIDE; SUPEROXIDE DISMUTASE; N-(2-CYCLOHEXYLOXY-4-NITROPHENYL)METHANESULFONAMIDE; NITROBENZENE DERIVATIVE; PTGS2 PROTEIN, HUMAN; SULFONAMIDE;

A549 CELL LINE; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CELL CONTACT; CELL EXPANSION; CELL INTERACTION; CELL ISOLATION; CELL PROLIFERATION; CELL VIABILITY; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME RELEASE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INFLAMMATION; MTS ASSAY; NEUTROPHIL; NEUTROPHIL COUNT; NON SMALL CELL LUNG CANCER; NORMAL HUMAN; RESPIRATORY BURST; TUMOR MICROENVIRONMENT; BIOSYNTHESIS; CELL COMMUNICATION; CELL GROWTH; ENZYMOLOGY; IMMUNOLOGY; LUNG TUMOR; METABOLISM; TUMOR CELL LINE;

CARCINOMA, NON-SMALL-CELL LUNG; CELL COMMUNICATION; CELL GROWTH PROCESSES; CELL LINE, TUMOR; COCULTURE TECHNIQUES; CYCLOOXYGENASE 2; DINOPROSTONE; HUMANS; LEUKOCYTE ELASTASE; LIPOPOLYSACCHARIDES; LUNG NEOPLASMS; NEUTROPHILS; NITROBENZENES; SULFONAMIDES; TUMOR MICROENVIRONMENT;

EID: 84916244719     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-014-1606-z     Document Type: Article

References (50)

1. Virchow R (1863) Die krankhaften Geschwülste. Dreissig Vorlesungen, gehalten während des Wintersemesters 1862–1863 an der Universität zu Berlin. Band I-III: 1. Berlin. A. Hirschwald, 1863–[1867]
2. Balkwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow? Lancet 357:539–545
3. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674
4. Coussens LM, Werb Z (2001) Inflammatory cells and cancer: think different! J Exp Med 193:F23–F26
5. Hallam S, Escorcio-Correia M, Soper R, Schultheiss A, Hagemann T (2009) Activated macrophages in the tumour microenvironment—dancing to the tune of TLR and NF-κB. J Pathol 219:143–152
6. Mantovani A (2009) The yin-yang of tumor-associated neutrophils. Cancer Cell 16:173–174
7. Teramukai S, Kitano T, Kishida Y, Kawahara M, Kubota K, Komuta K, Minato K, Mio T, Fujita Y, Yonei T, Nakano K, Tsuboi M, Shibata K, Furuse K, Fukushima M (2009) Pretreatment neutrophil count as an independent prognostic factor in advanced non-small-cell lung cancer: an analysis of Japan Multinational Trial Organisation LC00-03. Eur J Cancer 45:1950–1958
8. Ilie M, Hofman V, Ortholan C, Bonnetaud C, Coëlle C, Mouroux J, Hofman P (2012) Predictive clinical outcome of the intratumoral CD66b-positive neutrophil-to-CD8-positive T-cell ratio in patients with resectable nonsmall cell lung cancer. Cancer 118:1726–1737
9. Carus A, Ladekarl M, Hager H, Pilegaard H, Nielsen PS, Donskov F (2013) Tumor-associated neutrophils and macrophages in non-small cell lung cancer: no immediate impact on patient outcome. Lung Cancer 81:130–137
10. Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS, Albelda SM (2009) Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell 16:183–194
11. Nozawa H, Chiu C, Hanahan D (2006) Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci USA 103:12493–12498
12. Welch DR, Schissel DJ, Howrey RP, Aeed PA (1989) Tumor-elicited polymorphonuclear cells, in contrast to “normal” circulating polymorphonuclear cells, stimulate invasive and metastatic potentials of rat mammary adenocarcinoma cells. Proc Natl Acad Sci USA 86:5859–5863
13. Gregory AD, Houghton AM (2011) Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res 71:2411–2416
14. Güngör N, Godschalk RW, Pachen DM, Van Schooten FJ, Knaapen AM (2007) Activated neutrophils inhibit nucleotide excision repair in human pulmonary epithelial cells: role of myeloperoxidase. FASEB J 21:2359–2367
15. Yang P, Bamlet WR, Sun Z, Ebbert JO, Aubry MC, Krowka MJ, Taylor WR, Marks RS, Deschamps C, Swensen SJ, Wieben ED, Cunningham JM, Melton LJ, de Andrade M (2005) Alpha-1 antitrypsin and neutrophil elastase imbalance and lung cancer risk. Chest 128:445–452
16. Houghton AM, Rzymkiewicz DM, Ji H, Gregory AD, Egea EE, Metz HE, Stolz DB, Land SR, Marconcini LA, Kliment CR, Jenkins KM, Beaulieu KA, Mouded M, Frank SJ, Wong KK, Shapiro SD (2010) Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat Med 16:219–223
17. Houghton AM (2010) The paradox of tumor-associated neutrophils. Cell Cycle 9:1732–1737
18. Wolff H, Saukkonen K, Anttila S, Karjalainen A, Vainio H, Ristimäki A (1998) Expression of cyclooxygenase-2 in human lung carcinoma. Cancer Res 58:4997–5001
19. Achiwa H, Yatabe Y, Hida T, Kuroishi T, Kozaki K, Nakamura S, Ogawa M, Sugiura T, Mitsudomi T, Takahashi T (1999) Prognostic significance of elevated cyclooxygenase 2 expression in primary, resected lung adenocarcinomas. Clin Cancer Res 5:1001–1005
20. Lin MT, Lee RC, Yang PC, Ho FM, Kuo ML (2001) Cyclooxygenase-2 inducing Mcl-1-dependent survival mechanism in human lung adenocarcinoma CL1.0 cells. Involvement of phosphatidylinositol 3-kinase/Akt pathway. J Biol Chem 276:48997–49002
21. Unkel B, Hoegner K, Clausen BE, Lewe-Schlosser P, Bodner J, Gattenloehner S, Janßen H, Seeger W, Lohmeyer J, Herold S (2012) Alveolar epithelial cells orchestrate DC function in murine viral pneumonia. J Clin Invest 122:3652–3664
22. Cory AH, Owen TC, Barltrop JA, Cory JG (1991) Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun 3:207–212
23. Cohen HJ, Chovaniec ME (1978) Superoxide generation by digitonin-stimulated guinea pig granulocytes. J Clin Invest 61:1081–1087
24. Kramps JA (1983) L-pyroglutamyl-L-propyl-L-valine-p-nitro-anilide, a highly specific substrate for granulocyte elastase. Scand J Clin Lab Invest 43:427–432
25. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/
26. Bellocq A, Antoine M, Flahault A, Philippe C, Crestani B, Bernaudin JF, Mayaud C, Milleron B, Baud L, Cadranel J (1998) Neutrophil alveolitis in bronchioloalveolar carcinoma: induction by tumor-derived interleukin-8 and relation to clinical outcome. Am J Pathol 152:83–92
27. Sarraf KM, Belcher E, Raevsky E, Nicholson AG, Goldstraw P, Lim E (2009) Neutrophil/lymphocyte ratio and its association with survival after complete resection in non-small cell lung cancer. J Thorac Cardiovasc Surg 137:425–428
28. Altznauer F, Martinelli S, Yousefi S, Thürig C, Schmid I, Conway EM, Schöni MH, Vogt P, Mueller C, Fey MF, Zangemeister-Wittke U, Simon HU (2004) Inflammation-associated cell cycle-independent block of apoptosis by survivin in terminally differentiated neutrophils. J Exp Med 199:1343–1354
29. Witko-Sarsat V, Mocek J, Bouayad D, Tamassia N, Ribeil JA, Candalh C, Davezac N, Reuter N, Mouthon L, Hermine O, Pederzoli-Ribeil M, Cassatella MA (2010) Proliferating cell nuclear antigen acts as a cytoplasmic platform controlling human neutrophil survival. J Exp Med 207:2631–2645
30. Hattar K, Fink L, Fietzner K, Himmel B, Grimminger F, Seeger W, Sibelius U (2001) Cell density regulates neutrophil IL-8 synthesis: role of IL-1 receptor antagonist and soluble TNF receptors. J Immunol 166:6287–6293
31. Wislez M, Antoine M, Rabbe N, Gounant V, Poulot V, Lavolé A, Fleury-Feith J, Cadranel J (2007) Neutrophils promote aerogenous spread of lung adenocarcinoma with bronchioloalveolar carcinoma features. Clin Cancer Res 13:3518–3527
32. Condliffe AM, Kitchen E, Chilvers ER (1998) Neutrophil priming: pathophysiological consequences and underlying mechanisms. Clin Sci (Lond) 94:461–471
33. Berghmans T, Sculier JP, Klastersky J (2003) A prospective study of infections in lung cancer patients admitted to the hospital. Chest 124:114–120
34. Putinati S, Trevisani L, Gualandi M, Guerra G, Rossi MR, Sartori S, Potena A (1994) Pulmonary infections in lung cancer patients at diagnosis. Lung Cancer 11:243–249
35. Perlin E, Bang KM, Shah A, Hursey PD, Whittingham WL, Hashmi K, Campbell L, Kassim OD (1990) The impact of pulmonary infections on the survival of lung cancer patients. Cancer 66:593–596
36. Stark JM, Godding V, Sedgwick JB, Busse WW (1996) Respiratory syncytial virus infection enhances neutrophil and eosinophil adhesion to cultured respiratory epithelial cells. Roles of CD18 and intercellular adhesion molecule-1. J Immunol 156:4774–4782
37. Jagels MA, Daffern PJ, Zuraw BL, Hugli TE (1999) Mechanisms and regulation of polymorphonuclear leukocyte and eosinophil adherence to human airway epithelial cells. Am J Respir Cell Mol Biol 21:418–427
38. Krunkosky TM, Jarrett CL (2006) Selective regulation of MAP kinases and chemokine expression after ligation of ICAM-1 on human airway epithelial cells. Respir Res 7:12
39. Bost F, McKay R, Dean N, Mercola D (1997) The JUN kinase/stress-activated protein kinase pathway is required for epidermal growth factor stimulation of growth of human A549 lung carcinoma cells. J Biol Chem 272:33422–33429
40. Barnett CC Jr, Moore EE, Mierau GW, Partrick DA, Biffl WL, Elzi DJ, Silliman CC (1998) ICAM-1-CD18 interaction mediates neutrophil cytotoxicity through protease release. Am J Physiol 274:C1634–C1644
41. Meenan J, Hommes DW, Mevissen M, Dijkhuizen S, Soule H, Moyle M, Büller HR, ten Kate FW, Tytgat GN, van Deventer SJ (1996) Attenuation of the inflammatory response in an animal colitis model by neutrophil inhibitory factor, a novel beta 2-integrin antagonist. Scand J Gastroenterol 31:786–791
42. Zeiher BG, Matsuoka S, Kawabata K, Repine JE (2002) Neutrophil elastase and acute lung injury: prospects for sivelestat and other neutrophil elastase inhibitors as therapeutics. Crit Care Med 30:S281–S287
43. Xu Y, Zhang J, Han J, Pan X, Cao Y, Guo H, Pan Y, An Y, Li X (2012) Curcumin inhibits tumor proliferation induced by neutrophil elastase through the upregulation of α1-antitrypsin in lung cancer. Mol Oncol 6:405–417
44. Surette ME, Dallaire N, Jean N, Picard S, Borgeat P (1998) Mechanisms of the priming effect of lipopolysaccharides on the biosynthesis of leukotriene B4 in chemotactic peptide-stimulated human neutrophils. FASEB J 12:1521–1531
45. Grimminger F, Sibelius U, Seeger W (1991) Amplification of LTB4 generation in AM-PMN cocultures: transcellular 5-lipoxygenase metabolism. Am J Physiol 261:L195–L203
46. Fabre JE, Goulet JL, Riche E, Nguyen M, Coggins K, Offenbacher S, Koller BH (2002) Transcellular biosynthesis contributes to the production of leukotrienes during inflammatory responses in vivo. J Clin Invest 109:1373–1380
47. McLemore TL, Hubbard WC, Litterst CL, Liu MC, Miller S, McMahon NA, Eggleston JC, Boyd MR (1988) Profiles of prostaglandin biosynthesis in normal lung and tumor tissue from lung cancer patients. Cancer Res 48:3140–3147
48. Zheng Y, Ritzenthaler JD, Sun X, Roman J, Han S (2009) Prostaglandin E2 stimulates human lung carcinoma cell growth through induction of integrin-linked kinase: the involvement of EP4 and Sp1. Cancer Res 69:896–904
49. Kimura T, Iwase M, Kondo G, Watanabe H, Ohashi M, Ito D, Nagumo M (2003) Suppressive effect of selective cyclooxygenase-2 inhibitor on cytokine release in human neutrophils. Int Immunopharmacol 3:1519–1528
50. Perng DW, Wu YC, Tsai MC, Lin CP, Hsu WH, Perng RP, Lee YC (2003) Neutrophil elastase stimulates human airway epithelial cells to produce PGE2 through activation of p44/42 MAPK and upregulation of cyclooxygenase-2. Am J Physiol Lung Cell Mol Physiol 285:L925–L930