IL-17 and TNF-α sustain neutrophil recruitment during inflammation through synergistic effects on endothelial activation

Journal of Immunology

Volumn 188, Issue 12, 2012, Pages 6287-6299

  Griffin, Gabriel K ^a,b   Newton, Gail ^b   Tarrio, Margarite L ^b   Bu, De Xiu ^b,c   Maganto Garcia, Elena ^b,c   Azcutia, Veronica ^b,c   Alcaide, Pilar ^b,c   Grabie, Nir ^b,c   Luscinskas, Francis W ^b,c   Croce, Kevin J ^b,c   Lichtman, Andrew H ^b,c  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL9 CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 17; PADGEM PROTEIN; RANTES; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; INFLAMMATION; LEUKOCYTE ADHERENCE; LEUKOCYTE ROLLING; LYMPHOCYTE FUNCTION; LYMPHOCYTE MIGRATION; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TH1 CELL;

ANIMALS; CHEMOKINES; ENDOTHELIAL CELLS; FLOW CYTOMETRY; INFLAMMATION; INTERLEUKIN-17; LEUKOCYTE ROLLING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84862624810     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200385     Document Type: Article

References (70)

1. Harrington, L. E., R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132. (Pubitemid 41541790)
2. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141. (Pubitemid 41541791)
3. Cua, D. J., and C. M. Tato. 2010. Innate IL-17-producing cells: the sentinels of the immune system. Nat. Rev. Immunol. 10: 479-489.
4. Li, L., L. Huang, A. L. Vergis, H. Ye, A. Bajwa, V. Narayan, R. M. Strieter, D. L. Rosin, and M. D. Okusa. 2010. IL-17 produced by neutrophils regulates IFN-gamma-mediated neutrophil migration in mouse kidney ischemia-reperfusion injury. J. Clin. Invest. 120: 331-342.
5. Lockhart, E., A. M. Green, and J. L. Flynn. 2006. IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J. Immunol. 177: 4662-4669. (Pubitemid 44469799)
6. Gaffen, S. L. 2009. Structure and signalling in the IL-17 receptor family. Nat. Rev. Immunol. 9: 556-567.
7. Iwakura, Y., H. Ishigame, S. Saijo, and S. Nakae. 2011. Functional specialization of interleukin-17 family members. Immunity 34: 149-162.
8. Huang, W., L. Na, P. L. Fidel, and P. Schwarzenberger. 2004. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190: 624-631. (Pubitemid 38982105)
9. Ishigame, H., S. Kakuta, T. Nagai, M. Kadoki, A. Nambu, Y. Komiyama, N. Fujikado, Y. Tanahashi, A. Akitsu, H. Kotaki, et al. 2009. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30: 108-119.
10. Khader, S. A., G. K. Bell, J. E. Pearl, J. J. Fountain, J. Rangel-Moreno, G. E. Cilley, F. Shen, S. M. Eaton, S. L. Gaffen, S. L. Swain, et al. 2007. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8: 369-377. (Pubitemid 46745412)
11. Lock, C., G. Hermans, R. Pedotti, A. Brendolan, E. Schadt, H. Garren, A. Langer-Gould, S. Strober, B. Cannella, J. Allard, et al. 2002. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8: 500-508. (Pubitemid 34546753)
12. Ziolkowska, M., A. Koc, G. Luszczykiewicz, K. Ksiezopolska-Pietrzak, E. Klimczak, H. Chwalinska-Sadowska, and W. Maslinski. 2000. High levels of IL-17 in rheumatoid arthritis patients: IL-15 triggers in vitro IL-17 production via cyclosporin A-sensitive mechanism. J. Immunol. 164: 2832-2838. (Pubitemid 30115519)
13. Cai, Y., X. Shen, C. Ding, C. Qi, K. Li, X. Li, V. R. Jala, H. G. Zhang, T. Wang, J. Zheng, and J. Yan. 2011. Pivotal role of dermal IL-17-producing γδ T cells in skin inflammation. Immunity 35: 596-610.
14. Komiyama, Y., S. Nakae, T. Matsuki, A. Nambu, H. Ishigame, S. Kakuta, K. Sudo, and Y. Iwakura. 2006. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177: 566-573. (Pubitemid 43939170)
15. Nakae, S., A. Nambu, K. Sudo, and Y. Iwakura. 2003. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 171: 6173-6177. (Pubitemid 37467240)
16. Baldeviano, G. C., J. G. Barin, M. V. Talor, S. Srinivasan, D. Bedja, D. Zheng, K. Gabrielson, Y. Iwakura, N. R. Rose, and D. Cihakova. 2010. Interleukin-17A is dispensable for myocarditis but essential for the progression to dilated cardiomyopathy. Circ. Res. 106: 1646-1655.
17. Erbel, C., L. Chen, F. Bea, S. Wangler, S. Celik, F. Lasitschka, Y. Wang, D. Böckler, H. A. Katus, and T. J. Dengler. 2009. Inhibition of IL-17A attenuates atherosclerotic lesion development in apoE-deficient mice. J. Immunol. 183: 8167-8175.
18. Smith, E., K. M. Prasad, M. Butcher, A. Dobrian, J. K. Kolls, K. Ley, and E. Galkina. 2010. Blockade of interleukin-17A results in reduced atherosclerosis in apolipoprotein E-deficient mice. Circulation 121: 1746-1755.
19. Erbel, C., T. J. Dengler, S. Wangler, F. Lasitschka, F. Bea, N. Wambsganss, M. Hakimi, D. Böckler, H. A. Katus, and C. A. Gleissner. 2011. Expression of IL-17A in human atherosclerotic lesions is associated with increased inflammation and plaque vulnerability. Basic Res. Cardiol. 106: 125-134.
20. Liang, J., Z. Zheng, M. Wang, L. Han, Z. Zheng, J. Peng, Z. Liu, and Y. Wei. 2009. Myeloperoxidase (MPO) and interleukin-17 (IL-17) plasma levels are increased in patients with acute coronary syndromes. J. Int. Med. Res. 37: 862-866.
21. Yuan, X., J. Paez-Cortez, I. Schmitt-Knosalla, F. D'Addio, B. Mfarrej, M. Donnarumma, A. Habicht, M. R. Clarkson, J. Iacomini, L. H. Glimcher, et al. 2008. A novel role of CD4 Th17 cells in mediating cardiac allograft rejection and vasculopathy. J. Exp. Med. 205: 3133-3144.
22. Itoh, S., N. Kimura, R. C. Axtell, J. B. Velotta, Y. Gong, X. Wang, N. Kajiwara, A. Nambu, E. Shimura, H. Adachi, et al. 2011. Interleukin-17 accelerates allograft rejection by suppressing regulatory T cell expansion. Circulation 124 (Suppl 1): S187-S196.
23. Sohn, M. H., S. Y. Noh, W. Chang, K. M. Shin, and D. S. Kim. 2003. Circulating interleukin 17 is increased in the acute stage of Kawasaki disease. Scand. J. Rheumatol. 32: 364-366. (Pubitemid 38177793)
24. Madhur, M. S., S. A. Funt, L. Li, A. Vinh, W. Chen, H. E. Lob, Y. Iwakura, Y. Blinder, A. Rahman, A. A. Quyyumi, and D. G. Harrison. 2011. Role of interleukin 17 in inflammation, atherosclerosis, and vascular function in apolipoprotein e-deficient mice. Arterioscler. Thromb. Vasc. Biol. 31: 1565-1572.
25. Hueber, W., D. D. Patel, T. Dryja, A. M. Wright, I. Koroleva, G. Bruin, C. Antoni, Z. Draelos, M. H. Gold, P. Durez, et al Psoriasis Study Group; Rheumatoid Arthritis Study Group; Uveitis Study Group. 2010. Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci. Transl. Med. 2: 52ra72.
26. Genovese, M. C., F. Van den Bosch, S. A. Roberson, S. Bojin, I. M. Biagini, P. Ryan, and J. Sloan-Lancaster. 2010. LY2439821, a humanized antiinterleukin-17 monoclonal antibody, in the treatment of patients with rheumatoid arthritis: A phase I randomized, double-blind, placebo-controlled, proof-of-concept study. Arthritis Rheum. 62: 929-939.
27. Bevilacqua, M. P., J. S. Pober, M. E. Wheeler, R. S. Cotran, and M. A. Gimbrone, Jr. 1985. Interleukin-1 activation of vascular endothelium. Effects on procoagulant activity and leukocyte adhesion. Am. J. Pathol. 121: 394-403.
28. Pober, J. S., M. P. Bevilacqua, D. L. Mendrick, L. A. Lapierre, W. Fiers, and M. A. Gimbrone, Jr. 1986. Two distinct monokines, interleukin 1 and tumor necrosis factor, each independently induce biosynthesis and transient expression of the same antigen on the surface of cultured human vascular endothelial cells. J. Immunol. 136: 1680-1687. (Pubitemid 16119575)
29. Milstone, D. S., D. Fukumura, R. C. Padgett, P. E. O'Donnell, V. M. Davis, O. J. Benavidez, W. L. Monsky, R. J. Melder, R. K. Jain, and M. A. Gimbrone, Jr. 1998. Mice lacking E-selectin show normal numbers of rolling leukocytes but reduced leukocyte stable arrest on cytokine-activated microvascular endothelium. Microcirculation 5: 153-171. (Pubitemid 128647891)
30. Ley, K., C. Laudanna, M. I. Cybulsky, and S. Nourshargh. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7: 678-689. (Pubitemid 47327397)
31. Doukas, J., and J. S. Pober. 1990. IFN-gamma enhances endothelial activation induced by tumor necrosis factor but not IL-1. J. Immunol. 145: 1727-1733. (Pubitemid 20336736)
32. Marfaing-Koka, A., O. Devergne, G. Gorgone, A. Portier, T. J. Schall, P. Galanaud, and D. Emilie. 1995. Regulation of the production of the RANTES chemokine by endothelial cells. Synergistic induction by IFN-gamma plus TNF-alpha and inhibition by IL-4 and IL-13. J. Immunol. 154: 1870-1878.
33. Maganto-García, E., D. X. Bu, M. L. Tarrio, P. Alcaide, G. Newton, G. K. Griffin, K. J. Croce, F. W. Luscinskas, A. H. Lichtman, and N. Grabie. 2011. Foxp3+-inducible regulatory T cells suppress endothelial activation and leukocyte recruitment. J. Immunol. 187: 3521-3529.
34. Roussel, L., F. Houle, C. Chan, Y. Yao, J. Bérubé, R. Olivenstein, J. G. Martin, J. Huot, Q. Hamid, L. Ferri, and S. Rousseau. 2010. IL-17 promotes p38 MAPK-dependent endothelial activation enhancing neutrophil recruitment to sites of inflammation. J. Immunol. 184: 4531-4537.
35. Hartupee, J., C. Liu, M. Novotny, X. Li, and T. Hamilton. 2007. IL-17 enhances chemokine gene expression through mRNA stabilization. J. Immunol. 179: 4135-4141.
36. Shen, F., M. J. Ruddy, P. Plamondon, and S. L. Gaffen. 2005. Cytokines link osteoblasts and inflammation: microarray analysis of interleukin-17- and TNF-alpha-induced genes in bone cells. J. Leukoc. Biol. 77: 388-399. (Pubitemid 40289569)
37. Lim, Y. C., G. Garcia-Cardena, J. R. Allport, M. Zervoglos, A. J. Connolly, M. A. Gimbrone, Jr., and F. W. Luscinskas. 2003. Heterogeneity of endothelial cells from different organ sites in T-cell subset recruitment. Am. J. Pathol. 162: 1591-1601. (Pubitemid 36512842)
38. Baez, S. 1973. An open cremaster muscle preparation for the study of blood vessels by in vivo microscopy. Microvasc. Res. 5: 384-394.
39. Ley, K., D. C. Bullard, M. L. Arbonés, R. Bosse, D. Vestweber, T. F. Tedder, and A. L. Beaudet. 1995. Sequential contribution of L- and P-selectin to leukocyte rolling in vivo. J. Exp. Med. 181: 669-675.
40. Kunkel, E. J., and K. Ley. 1996. Distinct phenotype of E-selectin-deficient mice. E-selectin is required for slow leukocyte rolling in vivo. Circ. Res. 79: 1196-1204. (Pubitemid 26404152)
41. Norman, M. U., L. Zbytnuik, and P. Kubes. 2008. Interferon-gamma limits Th1 lymphocyte adhesion to inflamed endothelium: a nitric oxide regulatory feedback mechanism. Eur. J. Immunol. 38: 1368-1380.
42. Khandoga, A., S. Huettinger, A. G. Khandoga, H. Li, S. Butz, K. W. Jauch, D. Vestweber, and F. Krombach. 2009. Leukocyte transmigration in inflamed liver: A role for endothelial cell-selective adhesion molecule. J. Hepatol. 50: 755-765.
43. Allport, J. R., Y. C. Lim, J. M. Shipley, R. M. Senior, S. D. Shapiro, N. Matsuyoshi, D. Vestweber, and F. W. Luscinskas. 2002. Neutrophils from MMP-9- or neutrophil elastase-deficient mice show no defect in transendothelial migration under flow in vitro. J. Leukoc. Biol. 71: 821-828.
44. Jung, U., D. C. Bullard, T. F. Tedder, and K. Ley. 1996. Velocity differences between L- and P-selectin-dependent neutrophil rolling in venules of mouse cremaster muscle in vivo. Am. J. Physiol. 271: H2740-H2747.
45. Jung, U., K. E. Norman, K. Scharffetter-Kochanek, A. L. Beaudet, and K. Ley. 1998. Transit time of leukocytes rolling through venules controls cytokine-induced inflammatory cell recruitment in vivo. J. Clin. Invest. 102: 1526-1533. (Pubitemid 28492219)
46. Rot, A., and U. H. von Andrian. 2004. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 22: 891-928. (Pubitemid 38680444)
47. Yuo, A., S. Kitagawa, A. Ohsaka, M. Ohta, K. Miyazono, T. Okabe, A. Urabe, M. Saito, and F. Takaku. 1989. Recombinant human granulocyte colony-stimulating factor as an activator of human granulocytes: potentiation of responses triggered by receptor-mediated agonists and stimulation of C3bi receptor expression and adherence. Blood 74: 2144-2149. (Pubitemid 19269122)
48. Weisbart, R. H., L. Kwan, D. W. Golde, and J. C. Gasson. 1987. Human GM-CSF primes neutrophils for enhanced oxidative metabolism in response to the major physiological chemoattractants. Blood 69: 18-21. (Pubitemid 17007069)
49. Yong, K. L. 1996. Granulocyte colony-stimulating factor (G-CSF) increases neutrophil migration across vascular endothelium independent of an effect on adhesion: comparison with granulocyte-macrophage colony-stimulating factor (GM-CSF). Br. J. Haematol. 94: 40-47. (Pubitemid 26232537)
50. Muller, W. A., and F. W. Luscinskas. 2008. Assays of transendothelial migration in vitro. Methods Enzymol. 443: 155-176.
51. Bevilacqua, M. P., J. S. Pober, D. L. Mendrick, R. S. Cotran, and M. A. Gimbrone, Jr. 1987. Identification of an inducible endothelial-leukocyte adhesion molecule. Proc. Natl. Acad. Sci. USA 84: 9238-9242.
52. Ramos, C. L., E. J. Kunkel, M. B. Lawrence, U. Jung, D. Vestweber, R. Bosse, K. W. McIntyre, K. M. Gillooly, C. R. Norton, B. A. Wolitzky, and K. Ley. 1997. Differential effect of E-selectin antibodies on neutrophil rolling and recruitment to inflammatory sites. Blood 89: 3009-3018. (Pubitemid 27172589)
53. Yan, H. C., H. M. Delisser, J. M. Pilewski, K. M. Barone, P. J. Szklut, X. J. Chang, T. J. Ahern, P. Langer-Safer, and S. M. Albelda. 1994. Leukocyte recruitment into human skin transplanted onto severe combined immunodeficient mice induced by TNF-alpha is dependent on E-selectin. J. Immunol. 152: 3053-3063. (Pubitemid 24098004)
54. Zarbock, A., C. A. Lowell, and K. Ley. 2007. Spleen tyrosine kinase Syk is necessary for E-selectin-induced alpha(L)beta(2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity 26: 773-783. (Pubitemid 46907666)
55. Smith, M. L., T. S. Olson, and K. Ley. 2004. CXCR2- and E-selectin-induced neutrophil arrest during inflammation in vivo. J. Exp. Med. 200: 935-939. (Pubitemid 39362929)
56. Sun, D., M. Novotny, K. Bulek, C. Liu, X. Li, and T. Hamilton. 2011. Treatment with IL-17 prolongs the half-life of chemokine CXCL1 mRNA via the adaptor TRAF5 and the splicing-regulatory factor SF2 (ASF). Nat. Immunol. 12: 853-860.
57. Datta, S., M. Novotny, P. G. Pavicic, Jr., C. Zhao, T. Herjan, J. Hartupee, and T. Hamilton. 2010. IL-17 regulates CXCL1 mRNA stability via an AUUUA/tristetraprolin-independent sequence. J. Immunol. 184: 1484-1491.
58. Henness, S., E. van Thoor, Q. Ge, C. L. Armour, J. M. Hughes, and A. J. Ammit. 2006. IL-17A acts via p38 MAPK to increase stability of TNF-alpha-induced IL-8 mRNA in human ASM. Am. J. Physiol Lung Cell Mol. Physiol. 290: L1283-L1290. (Pubitemid 43830874)
59. Faour, W. H., A. Mancini, Q. W. He, and J. A. Di Battista. 2003. T-cell-derived interleukin-17 regulates the level and stability of cyclooxygenase-2 (COX-2) mRNA through restricted activation of the p38 mitogen-activated protein kinase cascade: role of distal sequences in the 3′-untranslated region of COX-2 mRNA. J. Biol. Chem. 278: 26897-26907. (Pubitemid 36876841)
60. Martin, B., K. Hirota, D. J. Cua, B. Stockinger, and M. Veldhoen. 2009. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 31: 321-330.
61. Sutton, C. E., S. J. Lalor, C. M. Sweeney, C. F. Brereton, E. C. Lavelle, and K. H. Mills. 2009. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31: 331-341.
62. Alcaide, P., E. Maganto-Garcia, G. Newton, R. Travers, K. J. Croce, D. X. Bu, F. W. Luscinskas, and A. H. Lichtman. 2012. Difference in Th1 and Th17 lymphocyte adhesion to endothelium. J. Immunol. 188: 1421-1430.
63. Jovanovic, D. V., J. A. Di Battista, J. Martel-Pelletier, F. C. Jolicoeur, Y. He, M. Zhang, F. Mineau, and J. P. Pelletier. 1998. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J. Immunol. 160: 3513-3521. (Pubitemid 28164746)
64. Pelletier, M., L. Maggi, A. Micheletti, E. Lazzeri, N. Tamassia, C. Costantini, L. Cosmi, C. Lunardi, F. Annunziato, S. Romagnani, and M. A. Cassatella. 2010. Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 115: 335-343.
65. Hot, A., V. Lenief, and P. Miossec. 2012. Combination of IL-17 and TNFα induces a pro-inflammatory, pro-coagulant and pro-thrombotic phenotype in human endothelial cells. Ann. Rheum. Dis. 71: 768-776.
66. Soehnlein, O. 2012. Multiple roles for neutrophils in atherosclerosis. Circ. Res. 110: 875-888.
67. Libby, P., P. M. Ridker, and G. K. Hansson; Leducq Transatlantic Network on Atherothrombosis. 2009. Inflammation in atherosclerosis: from pathophysiology to practice. J. Am. Coll. Cardiol. 54: 2129-2138.
68. Solomon, D. H., E. W. Karlson, E. B. Rimm, C. C. Cannuscio, L. A. Mandl, J. E. Manson, M. J. Stampfer, and G. C. Curhan. 2003. Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation 107: 1303-1307. (Pubitemid 36314415)
69. Solomon, D. H., N. J. Goodson, J. N. Katz, M. E. Weinblatt, J. Avorn, S. Setoguchi, C. Canning, and S. Schneeweiss. 2006. Patterns of cardiovascular risk in rheumatoid arthritis. Ann. Rheum. Dis. 65: 1608-1612. (Pubitemid 44799673)
70. Lee, M. S., W. Finch, G. Weisz, and A. J. Kirtane. 2011. Cardiac allograft vasculopathy. Rev. Cardiovasc. Med. 12: 143-152.