IL-1α modulates neutrophil recruitment in chronic inflammation induced by hydrocarbon oil

Journal of Immunology

Volumn 186, Issue 3, 2011, Pages 1747-1754

  Lee, Pui Y ^a   Kumagai, Yutaro ^a,b   Xu, Yuan ^a   Li, Yi ^a   Barker, Tolga ^a   Liu, Chao ^a   Sobel, Eric S ^a   Takeuchi, Osamu ^b   Akira, Shizuo ^b   Satoh, Minoru ^a,c   Reeves, Westley H ^a,c  

^a UNIVERSITY OF FLORIDA   (United States)

^b OSAKA UNIVERSITY   (Japan)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CXCR2; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; HYDROCARBON; INTERFERON RECEPTOR; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; INTERLEUKIN 1ALPHA; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 7;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CELL STRAIN 3T3; CHRONIC INFLAMMATION; CONTROLLED STUDY; IN VITRO STUDY; INNATE IMMUNITY; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PERITONEAL CAVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; CHRONIC DISEASE; HYDROCARBONS; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-1ALPHA; MICE; MICE, 129 STRAIN; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; NIH 3T3 CELLS; OILS; PICOLINES; RECEPTORS, INTERLEUKIN-1; SIGNAL TRANSDUCTION;

EID: 79251569905     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001328     Document Type: Article

References (63)

1. Kumar, V., A. K. Abbas, N. Fausto, S. L. Robbins, and R. S. Cotran. 2004. Acute and Chronic Inflammation. In Robbins & Cotran Pathologic Basis of Disease, 7th Ed. V. Kumar, A. Abbas, and N. Fausto, eds. Elsevier Health Sciences, Philadephia, PA, p. 50-88.
2. Reeves, W. H., P. Y. Lee, J. S. Weinstein, M. Satoh, and L. Lu. 2009. Induction of autoimmunity by pristane and other naturally occurring hydrocarbons. Trends Immunol. 30: 455-464.
3. Spickard, A., III, and J. V. Hirschmann. 1994. Exogenous lipoid pneumonia. Arch. Intern. Med. 154: 686-692.
4. Satoh, M., and W. H. Reeves. 1994. Induction of lupus-associated autoantibodies in BALB/c mice by intraperitoneal injection of pristane. J. Exp. Med. 180: 2341-2346.
5. Anderson, P. N., and M. Potter. 1969. Induction of plasma cell tumours in BALB-c mice with 2,6,10,14-tetramethylpentadecane (pristane). Nature 222: 994-995.
6. Wilner, B. I., M. A. Evers, H. D. Troutman, F. W. Trader, and I. W. McLean. 1963. Vaccine Potentiation by Emulsification with Pure Hydrocarbon Compounds. J. Immunol. 91: 210-229.
7. Ehrich, W. E., S. P. Halbert, E. Mertens, and S. Mudd. 1945. Mechanism of the Augmenting Action of Mineral Oil on Antibody Production: Tissue Reactions and Antibody Response to Dysentery Vaccine in Saline, and in Saline-Lanolin-Mineral Oil Emulsion. J. Exp. Med. 82: 343-360.
8. Cancro, M., and M. Potter. 1976. The requirement of an adherent cell substratum for the growth of developing plasmacytoma cells in vivo. J. Exp. Med. 144: 1554-1567.
9. Nacionales, D. C., K. M. Kelly, P. Y. Lee, H. Zhuang, Y. Li, J. S. Weinstein, E. Sobel, Y. Kuroda, J. Akaogi, M. Satoh, and W. H. Reeves. 2006. Type I interferon production by tertiary lymphoid tissue developing in response to 2,6,10,14-tetramethyl-pentadecane (pristane). Am. J. Pathol. 168: 1227-1240.
10. Patten, C., K. Bush, I. Rioja, R. Morgan, P. Wooley, J. Trill, and P. Life. 2004. Characterization of pristane-induced arthritis, a murine model of chronic disease: response to antirheumatic agents, expression of joint cytokines, and immunopathology. Arthritis Rheum. 50: 3334-3345.
11. Satoh, M., K. J. Hamilton, A. K. Ajmani, X. Dong, J. Wang, Y. S. Kanwar, and W. H. Reeves. 1996. Autoantibodies to ribosomal P antigens with immune complex glomerulonephritis in SJL mice treated with pristane. J. Immunol. 157: 3200-3206.
12. Satoh, M., A. Kumar, Y. S. Kanwar, and W. H. Reeves. 1995. Anti-nuclear antibody production and immune-complex glomerulonephritis in BALB/c mice treated with pristane. Proc. Natl. Acad. Sci. USA 92: 10934-10938.
13. Chowdhary, V. R., J. P. Grande, H. S. Luthra, and C. S. David. 2007. Characterization of haemorrhagic pulmonary capillaritis: another manifestation of Pristane-induced lupus. Rheumatology (Oxford) 46: 1405-1410.
14. Hoogenraad, N., T. Helman, and J. Hoogenraad. 1983. The effect of pre-injection of mice with pristane on ascites tumour formation and monoclonal antibody production. J. Immunol. Methods 61: 317-320. (Pubitemid 13034065)
15. Lee, P. Y., Y. Kumagai, Y. Li, O. Takeuchi, H. Yoshida, J. Weinstein, E. S. Kellner, D. Nacionales, T. Barker, K. Kelly-Scumpia, et al. 2008. TLR7-dependent and FcgammaR-independent production of type I interferon in experimental mouse lupus. J. Exp. Med. 205: 2995-3006.
16. Lee, P. Y., Y. Li, Y. Kumagai, Y. Xu, J. S. Weinstein, E. S. Kellner, D. C. Nacionales, E. J. Butfiloski, N. van Rooijen, S. Akira, et al. 2009. Type I interferon modulates monocyte recruitment and maturation in chronic inflammation. Am. J. Pathol. 175: 2023-2033.
17. Lee, P. Y., J. S. Weinstein, D. C. Nacionales, P. O. Scumpia, Y. Li, E. Butfiloski, N. van Rooijen, L. Moldawer, M. Satoh, and W. H. Reeves. 2008. A novel type I IFN-producing cell subset in murine lupus. J. Immunol. 180: 5101-5108.
18. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
19. Voehringer, D., N. van Rooijen, and R. M. Locksley. 2007. Eosinophils develop in distinct stages and are recruited to peripheral sites by alternatively activated macrophages. J. Leukoc. Biol. 81: 1434-1444.
20. Kuroda, Y., J. Akaogi, D. C. Nacionales, S. C. Wasdo, N. J. Szabo, W. H. Reeves, and M. Satoh. 2004. Distinctive patterns of autoimmune response induced by different types of mineral oil. Toxicol. Sci. 78: 222-228.
21. Franchi, L., T. Eigenbrod, R. Muñoz-Planillo, and G. Nuñez. 2009. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 10: 241-247.
22. Hornung, V., F. Bauernfeind, A. Halle, E. O. Samstad, H. Kono, K. L. Rock, K. A. Fitzgerald, and E. Latz. 2008. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9: 847-856.
23. Martinon, F., V. Pétrilli, A. Mayor, A. Tardivel, and J. Tschopp. 2006. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237-241. (Pubitemid 43372104)
24. Suzuki, N., S. Suzuki, G. S. Duncan, D. G. Millar, T. Wada, C. Mirtsos, H. Takada, A. Wakeham, A. Itie, S. Li, et al. 2002. Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4. Nature 416: 750-756.
25. Adachi, O., T. Kawai, K. Takeda, M. Matsumoto, H. Tsutsui, M. Sakagami, K. Nakanishi, and S. Akira. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150. (Pubitemid 28361303)
26. Muzio, M., J. Ni, P. Feng, and V. M. Dixit. 1997. IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 278: 1612-1615.
27. Kawagoe, T., S. Sato, K. Matsushita, H. Kato, K. Matsui, Y. Kumagai, T. Saitoh, T. Kawai, O. Takeuchi, and S. Akira. 2008. Sequential control of Toll-like receptor-dependent responses by IRAK1 and IRAK2. Nat. Immunol. 9: 684-691.
28. Honda, K., H. Yanai, H. Negishi, M. Asagiri, M. Sato, T. Mizutani, N. Shimada, Y. Ohba, A. Takaoka, N. Yoshida, and T. Taniguchi. 2005. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434: 772-777.
29. Uematsu, S., S. Sato, M. Yamamoto, T. Hirotani, H. Kato, F. Takeshita, M. Matsuda, C. Coban, K. J. Ishii, T. Kawai, et al. 2005. Interleukin-1 receptor-associated kinase-1 plays an essential role for Toll-like receptor (TLR)7- and TLR9-mediated interferon-alpha induction. J. Exp. Med. 201: 915-923.
30. Groves, R. W., T. Rauschmayr, K. Nakamura, S. Sarkar, I. R. Williams, and T. S. Kupper. 1996. Inflammatory and hyperproliferative skin disease in mice that express elevated levels of the IL-1 receptor (type I) on epidermal keratinocytes. Evidence that IL-1-inducible secondary cytokines produced by keratinocytes in vivo can cause skin disease. J. Clin. Invest. 98: 336-344.
31. Tumpey, T. M., R. Fenton, S. Molesworth-Kenyon, J. E. Oakes, and R. N. Lausch. 2002. Role for macrophage inflammatory protein 2 (MIP-2), MIP-1alpha, and interleukin-1alpha in the delayed-type hypersensitivity response to viral antigen. J. Virol. 76: 8050-8057.
32. West-Mays, J. A., P. M. Sadow, T. W. Tobin, K. J. Strissel, C. Cintron, and M. E. Fini. 1997. Repair phenotype in corneal fibroblasts is controlled by an interleukin-1 alpha autocrine feedback loop. Invest. Ophthalmol. Vis. Sci. 38: 1367-1379.
33. Dinarello, C. A. 2009. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27: 519-550.
34. Leung, K., J. C. Betts, L. Xu, and G. J. Nabel. 1994. The cytoplasmic domain of the interleukin-1 receptor is required for nuclear factor-kappa B signal transduction. J. Biol. Chem. 269: 1579-1582.
35. Chen, C. J., H. Kono, D. Golenbock, G. Reed, S. Akira, and K. L. Rock. 2007. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat. Med. 13: 851-856.
36. Cohen, I., P. Rider, Y. Carmi, A. Braiman, S. Dotan, M. R. White, E. Voronov, M. U. Martin, C. A. Dinarello, and R. N. Apte. 2010. Differential release of chromatin-bound IL-1alpha discriminates between necrotic and apoptotic cell death by the ability to induce sterile inflammation. Proc. Natl. Acad. Sci. USA 107: 2574-2579.
37. Barrat, F. J., T. Meeker, J. Gregorio, J. H. Chan, S. Uematsu, S. Akira, B. Chang, O. Duramad, and R. L. Coffman. 2005. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med. 202: 1131-1139.
38. Lau, C. M., C. Broughton, A. S. Tabor, S. Akira, R. A. Flavell, M. J. Mamula, S. R. Christensen, M. J. Shlomchik, G. A. Viglianti, I. R. Rifkin, and A. Marshak-Rothstein. 2005. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 202: 1171-1177.
39. Vollmer, J., S. Tluk, C. Schmitz, S. Hamm, M. Jurk, A. Forsbach, S. Akira, K. M. Kelly, W. H. Reeves, S. Bauer, and A. M. Krieg. 2005. Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J. Exp. Med. 202: 1575-1585.
40. Eigenbrod, T., J. H. Park, J. Harder, Y. Iwakura, and G. Núñez. 2008. Cutting edge: critical role for mesothelial cells in necrosis-induced inflammation through the recognition of IL-1 alpha released from dying cells. J. Immunol. 181: 8194-8198.
41. Niki, Y., H. Yamada, S. Seki, T. Kikuchi, H. Takaishi, Y. Toyama, K. Fujikawa, and N. Tada. 2001. Macrophage- and neutrophil-dominant arthritis in human IL-1 alpha transgenic mice. J. Clin. Invest. 107: 1127-1135.
42. Potter, M., and J. S. Wax. 1981. Genetics of susceptibility to pristane-induced plasmacytomas in BALB/cAn: reduced susceptibility in BALB/cJ with a brief description of pristane-induced arthritis. J. Immunol. 127: 1591-1595.
43. Stork, L. C., V. M. Peterson, C. H. Rundus, and W. A. Robinson. 1988. Interleukin-1 enhances murine granulopoiesis in vivo. Exp. Hematol. 16: 163-167.
44. Ueda, Y., D. W. Cain, M. Kuraoka, M. Kondo, and G. Kelsoe. 2009. IL-1R type I-dependent hemopoietic stem cell proliferation is necessary for inflammatory granulopoiesis and reactive neutrophilia. J. Immunol. 182: 6477-6484.
45. Corbett, M. S., I. Schmitt, O. Riess, and A. Walz. 1994. Characterization of the gene for human neutrophil-activating peptide 78 (ENA-78). Biochem. Biophys. Res. Commun. 205: 612-617.
46. Walz, A., R. Burgener, B. Car, M. Baggiolini, S. L. Kunkel, and R. M. Strieter. 1991. Structure and neutrophil-activating properties of a novel inflammatory peptide (ENA-78) with homology to interleukin 8. J. Exp. Med. 174: 1355-1362.
47. Grespan, R., S. Y. Fukada, H. P. Lemos, S. M. Vieira, M. H. Napimoga, M. M. Teixeira, A. R. Fraser, F. Y. Liew, I. B. McInnes, and F. Q. Cunha. 2008. CXCR2-specific chemokines mediate leukotriene B4-dependent recruitment of neutrophils to inflamed joints in mice with antigen-induced arthritis. Arthritis Rheum. 58: 2030-2040.
48. Halloran, M. M., J. M. Woods, R. M. Strieter, Z. Szekanecz, M. V. Volin, S. Hosaka, G. K. Haines, III, S. L. Kunkel, M. D. Burdick, A. Walz, and A. E. Koch. 1999. The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvant-induced arthritis. J. Immunol. 162: 7492-7500.
49. Colletti, L. M., S. L. Kunkel, A. Walz, M. D. Burdick, R. G. Kunkel, C. A. Wilke, and R. M. Strieter. 1995. Chemokine expression during hepatic ischemia/reperfusion-induced lung injury in the rat. The role of epithelial neutrophil activating protein. J. Clin. Invest. 95: 134-141.
50. Koch, A. E., S. L. Kunkel, L. A. Harlow, D. D. Mazarakis, G. K. Haines, M. D. Burdick, R. M. Pope, A. Walz, and R. M. Strieter. 1994. Epithelial neutrophil activating peptide-78: a novel chemotactic cytokine for neutrophils in arthritis. J. Clin. Invest. 94: 1012-1018.
51. Fillmore, R. A., S. E. Nelson, R. N. Lausch, and J. E. Oakes. 2003. Differential regulation of ENA-78 and GCP-2 gene expression in human corneal keratocytes and epithelial cells. Invest. Ophthalmol. Vis. Sci. 44: 3432-3437.
52. Chang, M. S., J. McNinch, R. Basu, and S. Simonet. 1994. Cloning and characterization of the human neutrophil-activating peptide (ENA-78) gene. J. Biol. Chem. 269: 25277-25282.
53. Lee, Y. R., S. H. Kweon, K. B. Kwon, J. W. Park, T. R. Yoon, and B. H. Park. 2009. Inhibition of IL-1beta-mediated inflammatory responses by the IkappaB alpha super-repressor in human fibroblast-like synoviocytes. Biochem. Biophys. Res. Commun. 378: 90-94.
54. Madorin, W. S., T. Rui, N. Sugimoto, O. Handa, G. Cepinskas, and P. R. Kvietys. 2004. Cardiac myocytes activated by septic plasma promote neutrophil transendothelial migration: role of platelet-activating factor and the chemokines LIX and KC. Circ. Res. 94: 944-951.
55. Wuyts, A., S. Struyf, K. Gijsbers, E. Schutyser, W. Put, R. Conings, J. P. Lenaerts, K. Geboes, G. Opdenakker, P. Menten, et al. 2003. The CXC chemokine GCP-2/CXCL6 is predominantly induced in mesenchymal cells by interleukin-1beta and is down-regulated by interferon-gamma: comparison with interleukin-8/CXCL8. Lab. Invest. 83: 23-34.
56. Schnyder-Candrian, S., R. M. Strieter, S. L. Kunkel, and A. Walz. 1995. Interferon-alpha and interferon-gamma down-regulate the production of interleukin-8 and ENA-78 in human monocytes. J. Leukoc. Biol. 57: 929-935.
57. Duchene, J., F. Lecomte, S. Ahmed, C. Cayla, J. Pesquero, M. Bader, M. Perretti, and A. Ahluwalia. 2007. A novel inflammatory pathway involved in leukocyte recruitment: role for the kinin B1 receptor and the chemokine CXCL5. J. Immunol. 179: 4849-4856.
58. Lemos, H. P., R. Grespan, S. M. Vieira, T. M. Cunha, W. A. Verri, Jr., K. S. Fernandes, F. O. Souto, I. B. McInnes, S. H. Ferreira, F. Y. Liew, and F. Q. Cunha. 2009. Prostaglandin mediates IL-23/IL-17-induced neutrophil migration in inflammation by inhibiting IL-12 and IFNgamma production. Proc. Natl. Acad. Sci. USA 106: 5954-5959.
59. Horai, R., M. Asano, K. Sudo, H. Kanuka, M. Suzuki, M. Nishihara, M. Takahashi, and Y. Iwakura. 1998. 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. 187: 1463-1475.
60. Zheng, H., D. Fletcher, W. Kozak, M. Jiang, K. J. Hofmann, C. A. Conn, D. Soszynski, C. Grabiec, M. E. Trumbauer, A. Shaw, et al. 1995. Resistance to fever induction and impaired acute-phase response in interleukin-1 beta-deficient mice. Immunity 3: 9-19.
61. Johnston, B., A. R. Burns, M. Suematsu, T. B. Issekutz, R. C. Woodman, and P. Kubes. 1999. Chronic inflammation upregulates chemokine receptors and induces neutrophil migration to monocyte chemoattractant protein-1. J. Clin. Invest. 103: 1269-1276.
62. Furie, M. B., and D. D. McHugh. 1989. Migration of neutrophils across endothelial monolayers is stimulated by treatment of the monolayers with interleukin-1 or tumor necrosis factor-alpha. J. Immunol. 143: 3309-3317.
63. Denny, M. F., S. Yalavarthi, W. Zhao, S. G. Thacker, M. Anderson, A. R. Sandy, W. J. McCune, and M. J. Kaplan. 2010. A distinct subset of proinflammatory neutrophils isolated from patients with systemic lupus erythematosus induces vascular damage and synthesizes type I IFNs. J. Immunol. 184: 3284-3297.