Crystalline silica-induced leukotriene B4-dependent inflammation promotes lung tumour growth

Nature Communications

Volumn 6, Issue , 2015, Pages

  Satpathy, Shuchismita R ^a,b   Jala, Venkatakrishna R ^a,b   Bodduluri, Sobha R ^a,b   Krishnan, Elangovan ^a,b   Hegde, Bindu ^a,b   Hoyle, Gary W ^a   Fraig, Mostafa ^b   Luster, Andrew D ^c   Haribabu, Bodduluri ^a,b  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b University of Louisville School of Medicine   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLAMMASOME; INTERLEUKIN 1BETA; LEUKOTRIENE B4; LEUKOTRIENE B4 RECEPTOR; SILICON DIOXIDE; AUTACOID; CHEMOKINE; CHEMOTACTIC FACTOR; KRAS2 PROTEIN, MOUSE; PROTEIN P21;

CANCER; CRYSTAL STRUCTURE; GENE EXPRESSION; GENETIC ENGINEERING; RESPIRATORY DISEASE; RODENT; SIGNALING; SILICA; TUMOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; LUNG CANCER; MACROPHAGE; MAST CELL; MOUSE; NEUTROPHIL; NONHUMAN; PNEUMONIA; REGULATORY MECHANISM; SILICOSIS; TUMOR GROWTH; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; C57BL MOUSE; CELL PROLIFERATION; CRYSTALLIZATION; DEFICIENCY; DISEASE COURSE; INFLAMMATION; LUNG TUMOR; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; TRANSGENIC MOUSE;

MUS;

ANIMALS; CELL PROLIFERATION; CHEMOKINES; CHEMOTACTIC FACTORS; CRYSTALLIZATION; DISEASE PROGRESSION; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; LEUKOTRIENE B4; LUNG NEOPLASMS; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NEUTROPHIL INFILTRATION; PROTO-ONCOGENE PROTEINS P21(RAS); RECEPTORS, LEUKOTRIENE B4; SILICON DIOXIDE;

EID: 84928958216     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8064     Document Type: Article

References (53)

1. Mantovani, A. et al. Cancer-related inflammation. Nature 454, 436-444 (2008).
2. Houghton, A. M. Mechanistic links between COPD and lung cancer. Nat. Rev. Cancer 13, 233-245 (2013).
3. Colotta, F. et al. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 30, 1073-1081 (2009).
4. Russo, M., Di Nicolantonio, F. & Bardelli, A. Climbing RAS, the everest of oncogenes. Cancer Discov. 4, 19-21 (2014).
5. Ji, H. et al. K-ras activation generates an inflammatory response in lung tumors. Oncogene 25, 2105-2112 (2006).
6. Elinav, E. et al. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat. Rev. Cancer 13, 759-771 (2013).
7. Takahashi, H. et al. Tobacco smoke promotes lung tumorigenesis by triggering IKKbeta-and JNK1-dependent inflammation. Cancer Cell 17, 89-97 (2010).
8. Leung, C. C., Yu, I. T. & Chen, W. Silicosis. Lancet 379, 2008-2018 (2012).
9. Huaux, F. New developments in the understanding of immunology in silicosis. Curr. Opin. Allergy Clin. Immunol. 7, 168-173 (2007).
10. Takato, H. et al. The specific chymase inhibitor TY-51469 suppresses the accumulation of neutrophils in the lung and reduces silica-induced pulmonary fibrosis in mice. Exp. Lung Res. 37, 101-108 (2011).
11. Brown, T. Silica exposure, smoking, silicosis and lung cancer-complex interactions. Occup. Med. (Lond) 59, 89-95 (2009).
12. Cox, Jr. L. A. An exposure-response threshold for lung diseases and lung cancer caused by crystalline silica. Risk Anal. 31, 1543-1560 (2011).
13. Liu, Y. et al. Exposure-response analysis and risk assessment for lung cancer in relationship to silica exposure: a 44-year cohort study of 34, 018 workers. Am. J. Epidemiol. 178, 1424-1433 (2013).
14. Kachuri, L. et al. Occupational exposure to crystalline silica and the risk of lung cancer in Canadian men. Int. J. Cancer 135, 138-148 (2013).
15. Balkwill, F. Cancer and the chemokine network. Nat. Rev. Cancer 4, 540-550 (2004).
16. Ruffini, P. A. et al. Manipulating the chemokine-chemokine receptor network to treat cancer. Cancer 109, 2392-2404 (2007).
17. Oyoshi, M. K. et al. Leukotriene B4-driven neutrophil recruitment to the skin is essential for allergic skin inflammation. Immunity 37, 747-758 (2012).
18. Li, R. C. et al. Leukotriene B4 Receptor-1 Mediates Intermittent Hypoxia-induced Atherogenesis. Am. J. Respir. Crit. Care Med. 184, 124-131 (2011).
19. Spite, M. et al. Deficiency of the leukotriene B4 receptor, BLT-1, protects against systemic insulin resistance in diet-induced obesity. J. Immunol. 187, 1942-1949 (2011).
20. Chou, R. C. et al. Lipid-cytokine-chemokine cascade drives neutrophil recruitment in a murine model of inflammatory arthritis. Immunity 33, 266-278 (2010).
21. Johnson, L. et al. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410, 1111-1116 (2001).
22. Houghton, A. M. et al. Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat. Med. 16, 219-223 (2010).
23. Gong, L. et al. Promoting effect of neutrophils on lung tumorigenesis is mediated by CXCR2 and neutrophil elastase. Mol. Cancer 12, 154 (2013).
24. Wislez, M. et al. High expression of ligands for chemokine receptor CXCR2 in alveolar epithelial neoplasia induced by oncogenic kras. Cancer Res. 66, 4198-4207 (2006).
25. Grivennikov, S. I., Greten, F. R. & Karin, M. Immunity, inflammation, and cancer. Cell 140, 883-899 (2010).
26. Brown, J. M. et al. Silica-directed mast cell activation is enhanced by scavenger receptors. Am. J. Respir. Cell Mol. Biol. 36, 43-52 (2007).
27. Colville-Nash, P. & Lawrence, T. Air-pouch models of inflammation and modifications for the study of granuloma-mediated cartilage degradation. Methods Mol. Biol. 225, 181-189 (2003).
28. McCarthy, N. Tumorigenesis: Inflammatory debate. Nature Reviews Cancer 4, 753 (2004).
29. Bode, C. et al. Suppressive oligodeoxynucleotides reduce lung cancer susceptibility in mice with silicosis. Carcinogenesis 35, 1078-1083 (2014).
30. Hamilton, Jr. R. F., Thakur, S. A. & Holian, A. Silica binding and toxicity in alveolar macrophages. Free Radic. Biol. Med. 44, 1246-1258 (2008).
31. Suzuki, N. et al. Mast cells are essential for the full development of silica-induced pulmonary inflammation: a study with mast cell-deficient mice. Am. J. Respir. Cell Mol. Biol. 9, 475-483 (1993).
32. Beamer, C. A. et al. Innate immune processes are sufficient for driving silicosis in mice. J. Leukoc. Biol. 88, 547-557 (2010).
33. Piguet, P. F. et al. Requirement of tumour necrosis factor for development of silica-induced pulmonary fibrosis. Nature 344, 245-247 (1990).
34. Yao, S. Q. et al. Role of Fas/FasL pathway-mediated alveolar macrophages releasing inflammatory cytokines in human silicosis. Biomed. Environ. Sci. 26, 930-933 (2013).
35. Chen, Y. et al. Neutralization of interleukin-17A delays progression of silica-induced lung inflammation and fibrosis in C57BL/6 mice. Toxicol. Appl. Pharmacol. 275, 62-72 (2014).
36. Cassel, S. L. et al. The Nalp3 inflammasome is essential for the development of silicosis. Proc. Natl Acad. Sci. USA 105, 9035-9040 (2008).
37. Wang, X. et al. Silencing CD36 gene expression results in the inhibition of latent-TGF-beta1 activation and suppression of silica-induced lung fibrosis in the rat. Respir. Res. 10, 36 (2009).
38. Dostert, C. et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320, 674-677 (2008).
39. Guo, J. et al. Neutralization of interleukin-1 beta attenuates silica-induced lung inflammation and fibrosis in C57BL/6 mice. Arch. Toxicol. 87, 1963-1973 (2013).
40. Hornung, V. et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847-856 (2008).
41. Lammermann, T. et al. Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature 498, 371-375 (2013).
42. Fridlender, Z. G. & Albelda, S. M. Tumor-associated neutrophils: friend or foe? Carcinogenesis 33, 949-955 (2012).
43. Gregory, A. D. & Houghton, A. M. Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res. 71, 2411-2416 (2011).
44. Mantovani, A. et al. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11, 519-531 (2011).
45. Shang, K. et al. Crucial involvement of tumor-associated neutrophils in the regulation of chronic colitis-associated carcinogenesis in mice. PLoS ONE 7, e51848 (2012).
46. Tazzyman, S. et al. Inhibition of neutrophil infiltration into A549 lung tumors in vitro and in vivo using a CXCR2-specific antagonist is associated with reduced tumor growth. Int. J. Cancer 129, 847-858 (2011).
47. Ilie, M. et al. 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 (2012).
48. Carpagnano, G. E. et al. Neutrophilic airways inflammation in lung cancer: the role of exhaled LTB-4 and IL-8. BMC Cancer 11, 226 (2011).
49. Haribabu, B. et al. Targeted disruption of the leukotriene B(4) receptor in mice reveals its role in inflammation and platelet-activating factor-induced anaphylaxis. J. Exp. Med. 192, 433-438 (2000).
50. Sin, Y. M. et al. Mast cells in newly formed lining tissue during acute inflammation: a six day air pouch model in the mouse. Ann. Rheum. Dis. 45, 873-877 (1986).
51. Zhang, L. et al. A novel immunocompetent murine model for replicating oncolytic adenoviral therapy. Cancer Gene Ther. 22, 17-22 (2015).
52. Nikitin, A. Y. et al. Classification of proliferative pulmonary lesions of the mouse: recommendations of the mouse models of human cancers consortium. Cancer Res. 64, 2307-2316 (2004).
53. Mathis, S. P. et al. Nonredundant roles for leukotriene B4 receptors BLT1 and BLT2 in inflammatory arthritis. J. Immunol. 185, 3049-3056 (2010).