IL-17 promotes p38 MAPK-dependent endothelial activation enhancing neutrophil recruitment to sites of inflammation

Journal of Immunology

Volumn 184, Issue 8, 2010, Pages 4531-4537

  Roussel, Lucie ^a   Houle, François ^d   Chan, Carlos ^b   Yao, Yu ^a   Bérubé, Julie ^a   Olivenstein, Ron ^c   Martin, James G ^a   Huot, Jacques ^d   Hamid, Qutayba ^a   Ferri, Lorenzo ^b   Rousseau, Simon ^a  

^a MCGILL UNIVERSITY   (Canada)

^b ROYAL VICTORIA HOSPITAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 8; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; VASCULAR CELL ADHESION MOLECULE 1; AUTACOID; IL17A PROTEIN, HUMAN; IL8 PROTEIN, HUMAN;

ARTICLE; ASTHMA; CANCER CELL; CELL ADHESION; CELL MIGRATION; COLON CARCINOMA; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LUNG METASTASIS; NEUTROPHIL CHEMOTAXIS; PRIORITY JOURNAL; VASCULAR ENDOTHELIUM; ADULT; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL STRAIN HT29; ENZYMOLOGY; IMMUNOLOGY; INFLAMMATION; LEUKEMIA CELL LINE; MALE; METABOLISM; MOUSE; NEUTROPHIL; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADULT; ANIMALS; ASTHMA; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; HT29 CELLS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-17; INTERLEUKIN-8; JURKAT CELLS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; NEUTROPHIL INFILTRATION; NEUTROPHILS; P38 MITOGEN-ACTIVATED PROTEIN KINASES;

EID: 77952758245     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903162     Document Type: Article

References (43)

1. Hällgren, R., T. Borg, P. Venge, and J. Modig. 1984. Signs of neutrophil and eosinophil activation in adult respiratory distress syndrome. Crit. Care Med. 12: 14-18.
2. Lacoste, J. Y., J. Bousquet, P. Chanez, T. Van Vyve, J. Simony-Lafontaine, N. Lequeu, P. Vic, I. Enander, P. Godard, and F. B. Michel. 1993. Eosinophilic and neutrophilic inflammation in asthma, chronic bronchitis, and chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 92: 537-548.
3. Rosenfeld, M., R. L. Gibson, S. McNamara, J. Emerson, J. L. Burns, R. Castile, P. Hiatt, K. McCoy, C. B. Wilson, A. Inglis, et al. 2001. Early pulmonary infection, inflammation, and clinical outcomes in infants with cystic fibrosis. Pediatr. Pulmonol. 32: 356-366.
4. Jatakanon, A., C. Uasuf, W. Maziak, S. Lim, K. F. Chung, and P. J. Barnes. 1999. Neutrophilic inflammation in severe persistent asthma. Am. J. Respir. Crit. Care Med. 160: 1532-1539.
5. Fahy, J. V., K. W. Kim, J. Liu, and H. A. Boushey. 1995. Prominent neutrophilic inflammation in sputum from subjects with asthma exacerbation. J. Allergy Clin. Immunol. 95: 843-852.
6. Barnes, P. J., and I. M. Adcock. 2009. Glucocorticoid resistance in inflammatory diseases. Lancet 373: 1905-1917.
7. Ford-Hutchinson, A. W., M. A. Bray, M. V. Doig, M. E. Shipley, and M. J. Smith. 1980. Leukotriene B, a potent chemokinetic and aggregating substance released from polymorphonuclear leukocytes. Nature 286: 264-265.
8. Powell, W. S., S. Gravel, R. J. MacLeod, E. Mills, and M. Hashefi. 1993. Stimulation of human neutrophils by 5-oxo-6,8,11,14-eicosatetraenoic acid by a mechanism independent of the leukotriene B4 receptor. J. Biol. Chem. 268: 9280-9286.
9. Schenkel, E., P. C. Atkins, R. Yost, and B. Zweiman. 1982. Antigen-induced neutrophil chemotactic activity from sensitized lung. J. Allergy Clin. Immunol. 70: 321-325.
10. Kolls, J. K., and A. Lindén. 2004. Interleukin-17 family members and inflammation. Immunity 21: 467-476.
11. Chakir, J., J. Shannon, S. Molet, M. Fukakusa, J. Elias, M. Laviolette, L. P. Boulet, and Q. Hamid. 2003. Airway remodeling-associated mediators in moderate to severe asthma: effect of steroids on TGF-beta, IL-11, IL-17, and type I and type III collagen expression. J. Allergy Clin. Immunol. 111: 1293-1298.
12. McAllister, F., A. Henry, J. L. Kreindler, P. J. Dubin, L. Ulrich, C. Steele, J. D. Finder, J. M. Pilewski, B. M. Carreno, S. J. Goldman, et al. 2005. Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogenealpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J. Immunol. 175: 404-412.
13. Liang, S. C., A. J. Long, F. Bennett, M. J. Whitters, R. Karim, M. Collins, S. J. Goldman, K. Dunussi-Joannopoulos, C. M. Williams, J. F. Wright, and L. A. Fouser. 2007. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J. Immunol. 179: 7791-7799.
14. Song, C., L. Luo, Z. Lei, B. Li, Z. Liang, G. Liu, D. Li, G. Zhang, B. Huang, and Z. H. Feng. 2008. IL-17-producing alveolar macrophages mediate allergic lung inflammation related to asthma. J. Immunol. 181: 6117-6124.
15. Liu, C., W. Qian, Y. Qian, N. V. Giltiay, Y. Lu, S. Swaidani, S. Misra, L. Deng, Z. J. Chen, and X. Li. 2009. Act1, a U-box E3 ubiquitin ligase for IL-17 signaling. Sci. Signal. 2: ra63.
16. Rahman, M. S., A. Yamasaki, J. Yang, L. Shan, A. J. Halayko, and A. S. Gounni. 2006. IL-17A induces eotaxin-1/CC chemokine ligand 11 expression in human airway smooth muscle cells: role of MAPK (Erk1/2, JNK, and p38) pathways. J. Immunol. 177: 4064-4071.
17. Vanaudenaerde, B. M., W. A. Wuyts, L. J. Dupont, D. E. Van Raemdonck, M. M. Demedts, and G. M. Verleden. 2003. Interleukin-17 stimulates release of interleukin-8 by human airway smooth muscle cells in vitro: a potential role for interleukin-17 and airway smooth muscle cells in bronchiolitis obliterans syndrome. J. Heart Lung Transplant. 22: 1280-1283.
18. American Thoracic Society. 2000. Proceedings of the ATS workshop on refractory asthma: current understanding, recommendations, and unanswered questions. Am. J. Respir. Crit. Care Med. 162: 2341-2351.
19. Laferriere, J., F. Houle, M. M. Taher, K. Valerie, and J. Huot. 2001. Transendothelial migration of colon carcinoma cells requires expression of E-selectin by endothelial cells and activation of stress-activated protein kinase-2 (SAPK2/p38) in the tumor cells. J. Biol. Chem. 276: 33762-33772.
20. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
21. Ferri, L. E., J. Pascual, A. J. Seely, P. Chaudhury, and N. V. Christou. 2002. Soluble L-selectin attenuates tumor necrosis factor-alpha-mediated leukocyte adherence and vascular permeability: a protective role for elevated soluble L-selectin in sepsis. Crit. Care Med. 30: 1842-1847.
22. Beasley, R., S. Nishima, N. Pearce, and J. Crane. 1998. Beta-agonist therapy and asthma mortality in Japan. Lancet 351: 1406-1407.
23. Al-Ramli, W., D. Préfontaine, F. Chouiali, J. G. Martin, R. Olivenstein, C. Lemière, and Q. Hamid. 2009. T(H)17-associated cytokines (IL-17A and IL-17F) in severe asthma. J. Allergy Clin. Immunol. 123: 1185-1187.
24. Ge, D., and Z. You. 2008. Expression of interleukin-17RC protein in normal human tissues. Int. Arch. Med. 1: 19.
25. Fossiez, F., O. Djossou, P. Chomarat, L. Flores-Romo, S. Ait-Yahia, C. Maat, J. J. Pin, P. Garrone, E. Garcia, S. Saeland, et al. 1996. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J. Exp. Med. 183: 2593-2603.
26. Cuenda, A., J. Rouse, Y. N. Doza, R. Meier, P. Cohen, T. F. Gallagher, P. R. Young, and J. C. Lee. 1995. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364: 229-233.
27. Kuma, Y., G. Sabio, J. Bain, N. Shpiro, R. Márquez, and A. Cuenda. 2005. BIRB796 inhibits all p38 MAPK isoforms in vitro and in vivo. J. Biol. Chem. 280: 19472-19479.
28. Bérubé, J., C. Bourdon, Y. Yao, and S. Rousseau. 2009. Distinct intracellular signaling pathways control the synthesis of IL-8 and RANTES in TLR1/TLR2, TLR3 or NOD1 activated human airway epithelial cells. Cell. Signal. 21: 448-456.
29. Friedman, B. S., E. H. Bel, A. Buntinx, W. Tanaka, Y. H. Han, S. Shingo, R. Spector, and P. Sterk. 1993. Oral leukotriene inhibitor (MK-886) blocks allergen-induced airway responses. Am. Rev. Respir. Dis. 147: 839-844.
30. Simon, S. I., and C. E. Green. 2005. Molecular mechanics and dynamics of leukocyte recruitment during inflammation. Annu. Rev. Biomed. Eng. 7: 151-185.
31. Vandermeeren, M., S. Janssens, M. Borgers, and J. Geysen. 1997. Dimethylfumarate is an inhibitor of cytokine-induced E-selectin, VCAM-1, and ICAM-1 expression in human endothelial cells. Biochem. Biophys. Res. Commun. 234: 19-23.
32. Yang, J., T. Hirata, K. Croce, G. Merrill-Skoloff, B. Tchernychev, E. Williams, R. Flaumenhaft, B. C. Furie, and B. Furie. 1999. Targeted gene disruption demonstrates that P-selectin glycoprotein ligand 1 (PSGL-1) is required for P-selectin-mediated but not E-selectin-mediated neutrophil rolling and migration. J. Exp. Med. 190: 1769-1782.
33. Ferri, L. E., S. Chia, C. Benay, B. Giannias, and N. V. Christou. 2009. L-selectin shedding in sepsis limits leukocyte mediated microvascular injury at remote sites. Surgery 145: 384-391.
34. Pepe, C., S. Foley, J. Shannon, C. Lemiere, R. Olivenstein, P. Ernst, M. S. Ludwig, J. G. Martin, and Q. Hamid. 2005. Differences in airway remodeling between subjects with severe and moderate asthma. J. Allergy Clin. Immunol. 116: 544-549.
35. Charan, N. B., E. M. Baile, and P. D. Paré. 1997. Bronchial vascular congestion and angiogenesis. Eur. Respir. J. 10: 1173-1180.
36. Lee, C. G., H. Link, P. Baluk, R. J. Homer, S. Chapoval, V. Bhandari, M. J. Kang, L. Cohn, Y. K. Kim, D. M. McDonald, and J. A. Elias. 2004. Vascular endothelial growth factor (VEGF) induces remodeling and enhances TH2-mediated sensitization and inflammation in the lung. Nat. Med. 10: 1095-1103.
37. Idelman, G., J. G. Taylor, R. Tongbai, R. A. Chen, C. M. Haggerty, S. Bilke, S. J. Chanock, and K. Gardner. 2007. Functional profiling of uncommon VCAM1 promoter polymorphisms prevalent in African American populations. Hum. Mutat. 28: 824-829.
38. Chu, S. J., L. O. Tang, E. Watney, E. Y. Chi, and W. R. Henderson, Jr. 2000. In situ amplification of 5-lipoxygenase and 5-lipoxygenase-activating protein in allergic airway inflammation and inhibition by leukotriene blockade. J. Immunol. 165: 4640-4648.
39. Werz, O., D. Szellas, D. Steinhilber, and O. Rådmark. 2002. Arachidonic acid promotes phosphorylation of 5-lipoxygenase at Ser-271 by MAPK-activated protein kinase 2 (MK2). J. Biol. Chem. 277: 14793-14800.
40. In, K. H., K. Asano, D. Beier, J. Grobholz, P. W. Finn, E. K. Silverman, E. S. Silverman, T. Collins, A. R. Fischer, T. P. Keith, et al. 1997. Naturally occurring mutations in the human 5-lipoxygenase gene promoter that modify transcription factor binding and reporter gene transcription. J. Clin. Invest. 99: 1130-1137.
41. Cuenda, A., and S. Rousseau. 2007. p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim. Biophys. Acta 1773: 1358-1375.
42. Wang, L., T. Yi, M. Kortylewski, D. M. Pardoll, D. Zeng, and H. Yu. 2009. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J. Exp. Med. 206: 1457-1464.
43. Kryczek, I., S. Wei, W. Szeliga, L. Vatan, and W. Zou. 2009. Endogenous IL-17 contributes to reduced tumor growth and metastasis. Blood 114: 357-359.