Interleukin-17 regulates expression of the CXC chemokine LIX/CXCL5 in osteoblasts: Implications for inflammation and neutrophil recruitment

Journal of Leukocyte Biology

Volumn 76, Issue 1, 2004, Pages 135-144

  Ruddy, Matthew J ^a   Shen, Fang ^b   Smith, Jeffrey B ^c   Sharma, Ashu ^b   Gaffen, Sarah L ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c MATTEL CHILDREN S HOSPITAL   (United States)

Author keywords

Bone cells; Cytokine; GCP 2; Synergy; TNF

Indexed keywords

ALPHA CHEMOKINE; CELL SURFACE MARKER; CXC CHEMOKINE LIGAND 5; CYTOKINE; INTERLEUKIN 17; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL INFECTION; BONE CELL; BONE DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE TARGETING; GENETIC TRANSCRIPTION; IMMUNE RESPONSE; INFLAMMATION; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OSTEOBLAST; OSTEOLYSIS; PATHOGENESIS; PERIODONTAL DISEASE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION;

ANIMALS; ARTHRITIS; BLOTTING, NORTHERN; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINES, CXC; CULTURE MEDIA, CONDITIONED; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; INFLAMMATION; INTERLEUKIN-17; MICE; NEUTROPHIL INFILTRATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOBLASTS; PERIODONTAL DISEASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA; BACTERIA (MICROORGANISMS); MURINAE;

EID: 3042737420     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0204065     Document Type: Article

References (66)

1. Yao, Z., Painter, S. L., Fanslow, W. C., Ulrich, D., Macduff, B. M., Spriggs, M. K., Armitage, R. J. (1995) Human IL-17: a novel cytokine derived from T cells. J. Immunol. 155, 5483-5486.
2. Fossiez, F., Djossou, O., Chomarat, P., Flores-Romo, L., Ait-Yahia, S., Maat, C., Pin, J-J., Garrone, P., Garcia, E., Saeland, S., Blanchard, D., Gaillard, C., Das Mahapatra, B., Rouvier, E., Golstein, P., Banchereau, J., Lebecque, S. (1996) T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J. Exp. Med. 183, 2593-2603.
3. Aggarwal, S., Gurney, A. L. (2002) IL-17: prototype member of an emerging cytokine family. J. Leukoc. Biol. 71, 1-8.
4. Yao, Z., Fanslow, W. C., Seldin, M. F., Rousseau, A-M., Painter, S. L., Comeau, M. R., Cohen, J. I., Spriggs, M. K. (1995) Herpesvirus saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3, 811-821.
5. Spriggs, M. K. (1997) Interleukin-17 and its receptor. J. Clin. Immunol. 17, 366-369.
6. Ruddy, M. J., Wong, G. C., Liu, X. K., Yamamoto, H., Kasayama, S., Kirkwood, K. L., Gaffen, S. L. (2004) Functional cooperation between interleukin-17 and tumor necrosis factor-α is mediated by CCAAT/enhancer binding protein family members. J. Biol. Chem. 279, 2559-2567.
7. Shalom-Barak, T., Quach, J., Lotz, M. (1998) Interleukin-17-induced gene expression in articular chondrocytes is associated with activation of mitogen-activated protein kinases and NF-κB. J. Biol. Chem. 273, 27467-27473.
8. Jovanovic, D. V., Di Battista, J. A., Martel-Pelletier, J., Jolicoeur, F. C., He, Y., Zhang, M., Mineau, F., Pelletier, J. P. (1998) IL-17 stimulates the production and expression of proinflammatory cytokines, IL-β and TNF-α, by human macrophages. J. Immunol. 160, 3513-3521.
9. Andoh, A., Shimada, M., Bamba, S., Okuno, T., Araki, Y., Fujiyama, Y., Bamba, T. (2002) Extracellular signal-regulated kinases 1 and 2 participate in interleukin-17 plus tumor necrosis factor-α-induced stabilization of interleukin-6 mRNA in human pancreatic myofibroblasts. Biochim. Biophys. Acta 1591, 69-74.
10. Shimada, M., Andoh, A., Hata, K., Tasaki, K., Araki, Y., Fujiyama, Y., Bamba, T. (2002) IL-6 secretion by human pancreatic periacinar myofibroblasts in response to inflammatory mediators. J. Immunol. 168, 861-868.
11. Witowski, J., Pawlaczyk, K., Breborowicz, A., Scheuren, A., Kuzlan-Pawlaczyk, M., Wisniewska, J., Polubinska, A., Friess, H., Gahl, G. M., Frei, U., Jorres, A. (2000) IL-17 stimulates intraperitoneal neutrophil infiltration through the release of GRO α chemokine from mesothelial cells. J. Immunol. 165, 5814-5821.
12. Albanesi, C., Cavani, A., Girolomoni, G. (1999) IL-17 is produced by nickel-specific T lymphocytes and regulates ICAM-1 expression and chemokine production in human keratinocvtes: synergistic or antagonist effects with IFN-γ and TNF-α. J. Immunol. 162, 494-502.
13. Maertzdorf, J., Osterhaus, A. D., Verjans, G. M. (2002) IL-17 expression in human herpetic stromal keratitis: modulatory effects on chemokine production by corneal fibroblasts. J. Immunol. 169, 5897-5903.
14. Andoh, A., Takaya, H., Makino, J., Sato, H., Bamba, S., Araki, Y., Hata, K., Shimada, M., Okuno, T., Fujiyama, Y., Bamba, T. (2001) Cooperation of interleukin-17 and interferon-γ on chemokine secretion in human fetal intestinal epithelial cells. Clin. Exp. Immunol. 125, 56-63.
15. Chabaud, M., Durand, J. M., Buchs, N., Fossiez, F., Page, G., Frappart, L., Miossec, P. (1999) Human interleukin-17: a T cell-derived proinflammatory cytokine produced by the rheumatoid synovium. Arthritis Rheum. 42, 963-970.
16. Kotake, S., Udagawa, N., Takahashi, N., Matsuzaki, K., Itoh, K., Ishiyama, S., Saito, S., Inoue, K., Kamatani, N., Gillespie, M. T., Martin, T. J., Suda, T. (1999) IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J. Clin. Invest. 103, 1345-1352.
17. Chabaud, M., Miossec, P. (2001) The combination of tumor necrosis factor α blockade with interleukin-1 and interleukin-17 blockade is more effective for controlling synovial inflammation and bone resorption in an ex vivo model. Arthritis Rheum. 44, 1293-1303.
18. Nakae, S., Nambu, A., Sudo, K., Iwakura, Y. (2003) Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 171, 6173-6177.
19. Molet, S., Hamid, Q., Davoine, F., Nutku, E., Taha, R., Page, N., Olivenstein, R., Elias, J., Chakir, J. (2001) IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J. Allergy Clin. Immunol. 108, 430-438.
20. Laan, M., Cui, Z. H., Hoshino, H., Lotvall, J., Sjostrand, M., Gruenert, D. C., Skoogh, B. E., Linden, A. (1999) Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J. Immunol. 162, 2347-2352.
21. Kurasawa, K., Hirose, K., Sano, H., Endo, H., Shinkai, H., Nawata, Y., Takabayashi, K., Iwamoto, I. (2000) Increased interleukin-17 production in patients with systemic sclerosis. Arthritis Rheum. 43, 2455-2463.
22. Teunissen, M. B., Koomen, C. W., de Waal Malefyt, R., Wierenga, E. A., Bos, J. D. (1998) Interleukin-17 and interferon-γ synergize in the enhancement of proinflammatory cytokine production by human keratinocytes. J. Invest. Dermatol. 111, 645-649.
23. Albanesi, C., Scarponi, C., Sebastiani, S., Cavani, A., Federici, M., De Pita, O., Puddu, P., Girolomoni, G., Nasorri, F. (2000) IL-4 enhances keratinocyte expression of CXCR3 agonistic chemokines. J. Immunol. 165, 1395-1402.
24. Albanesi, C., Scarponi, C., Cavani, A., Federici, M., Nasorri, F., Girolomoni, G. (2000) Interleukin-17 is produced by both Th1 and Th2 lymphocytes, and modulates interferon-γ- and interleukin-4-induced activation of human keratinocytes. J. Invest. Dermatol. 115, 81-87.
25. Homey, B., Dieu-Nosjean, M. C., Wiesenborn, A., Massacrier, C., Pin, J. J., Oldham, E., Catron, D., Buchanan, M. E., Muller, A., deWaal Malefyt, R., Deng, G., Orozco, R., Ruzicka, T., Lehmann, P., Lebecque, S., Caux, C., Zlotnik, A. (2000) Up-regulation of macrophage inflammatory protein-3 α/CCL20 and CC chemokine receptor 6 in psoriasis. J. Immunol. 164, 6621-6632.
26. Kato, T., Furumoto, H., Ogura, T., Onishi, Y., Irahara, M., Yamano, S., Kamada, M., Aono, T. (2001) Expression of IL-17 mRNA in ovarian cancer. Biochem. Biophys. Res. Commun. 282, 735-738.
27. Tartour, E., Fossiez, F., Joyeux, I., Galinha, A., Gey, A., Claret, E., Sastre-Garau, X., Couturier, J., Mosseri, V., Vives, V., Banchereau, J., Fridman, W. H., Wijdenes, J., Lebecque, S., Sautes-Fridman, C. (1999) Interleukin 17, a T-cell-derived cytokine, promotes tumorigenicity of human cervical tumors in nude mice. Cancer Res. 59, 3698-3704.
28. Kehlen, A., Thiele, K., Riemann, D., Rainov, N., Langner, J. (1999) Interleukin-17 stimulates the expression of IκB α mRNA and the secretion of IL-6 and IL-8 in glioblastoma cell lines. J. Neuroimmunol. 101, 1-6.
29. Luzza, F., Parrello, T., Monteleone, G., Sebkova, L., Romano, M., Zarrilli, R., Imeneo, M., Pallone, F. (2000) Up-regulation of IL-17 is associated with bioactive IL-8 expression in Helicobacter pylori-infected human gastric mucosa. J. Immunol. 165, 5332-5337.
30. Ye, P., Garvey, P. B., Zhang, P., Nelson, S., Bagby, G., Summer, W. R., Schwarzenberger, P., Shellito, J. E., Kolls, J. K. (2001) Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am. J. Respir. Cell Mol. Biol. 25, 335-340.
31. Ye, P., Rodriguez, F. H., Kanaly, S., Stocking, K. L., Schurr, J., Schwarzenberger, P., Oliver, P., Huang, W., Zhang, P., Zhang, J., Shelliot, J. E., Bagby, G. J., Nelson, S., Charrier, K., Peschon, J. J., Kolls, J. K. (2001) Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194, 519-527.
32. Smith, J. B., Herschman, H. R. (1995) Glucocorticoid-attenuated response genes encode intercellular mediators, including a new C-X-C chemokine. J. Biol. Chem. 270, 16756-16765.
33. Rovai, L. E., Herschman, H. R., Smith, J. B. (1998) The murine neutrophil-chemoattractant chemokines LIX, KC, and MIP-2 have distinct induction kinetics, tissue distributions, and tissue-specific sensitivities to glucocorticoid regulation in endotoxemia. J. Leukoc. Biol. 64, 494-502.
34. Lukacs, N. W., Hogaboam, C., Campbell, E., Kunkel, S. L. (1999) Chemokines: function, regulation and alteration of inflammatory responses. Chem. Immunol. 72, 102-120.
35. Baggiolini, M., Dewald, B., Moser, B. (1994) Interleukin-8 and related chemotactic cytokines-CXC and CC chemokines. Adv. Immunol. 55, 97-179.
36. Wuyts, A., Haelens, A., Proost, P., Lenaerts, J. P., Conings, R., Opdenakker, G., Van Damme, J. (1996) Identification of mouse granulocyte chemotactic protein-2 from fibroblasts and epithelial cells. Functional comparison with natural KC and macrophage inflammatory protein-2. J. Immunol. 157, 1736-1743.
37. Chandrasekar, B., Smith, J. B., Freeman, G. L. (2001) Ischemia-reperfusion of rat myocardium activates nuclear factor-κB and induces neutrophil infiltration via lipopolysaccharide-induced CXC chemokine. Circulation 103, 2296-2302.
38. Rovai, L. E., Herschman, H. R., Smith, J. B. (1997) Cloning and characterization of the human granulocyte chemotactic protein-2 gene. J. Immunol. 158, 5257-5266.
39. Smith, J. B., Wadleigh, D. J., Xia, Y. R., Mar, R. A., Herschman, H. R., Lusis, A. J. (2002) Cloning and genomic localization of the murine LPS-induced CXC chemokine (LIX) gene, Scyb5. Immunogenetics 54, 599-603.
40. Smith, J. B., Rovai, L. E., Herschman, H. R. (1997) Sequence similarities of a subgroup of CXC chemokines related to murine LIX: implications for the interpretation of evolutionary relationships among chemokines. J. Leukoc. Biol. 62, 598-603.
41. Prause, O., Laan, M., Lotvall, J., Linden, A. (2003) Pharmacological modulation of interleukin-17-induced GCP-2-, GRO-α- and interleukin-8 release in human bronchial epithelial cells. Eur. J. Pharmacol. 462, 193-198.
42. Koch, A. E., Kunkel, S. L., Harlow, L. A., Mazarakis, D. D., Haines, G. K., Burdick, M. D., Pope, R. M., Walz, A., Strieter, R. M. (1994) Epithelial neutrophil activating peptide-78: a novel chemotactic cytokine for neutrophils in arthritis. J. Clin. Invest. 94, 1012-1018.
43. Sharma, A., Sojar, H. T., Glurich, I., Honma, K., Kuramitsu, H. K., Genco, R. J. (1998) Cloning, expression, and sequencing of a cell surface antigen containing a leucine-rich repeat motif from Bacteroides forsythus ATCC 43037. Infect. Immun. 66, 5703-5710.
44. Atasoy, U., Curry, S. L., Lopez de Silanes, I., Shyu, A. B., Casolaro, V., Gorospe, M., Stellato, C. (2003) Regulation of eotaxin gene expression by TNF-α and IL-4 through mRNA stabilization: involvement of the RNA-binding protein HuR. J. Immunol. 171, 4369-4378.
45. Van bezooijen, R. L., Farih-Sips, H. C., Papapoulos, S. E., Lowik, C. W. (1999) Interleukin-17: a new bone acting cytokine in vitro. J. Bone Miner. Res. 14, 1513-1521.
46. Roger, T., Out, T. A., Jansen, H. M., Lutter, R. (1998) Superinduction of interleukin-6 mRNA in lung epithelial H292 cells depends on transiently increased C/EBP activity and durable increased mRNA stability. Biochim. Biophys. Acta 1398, 275-284.
47. Moseley, T. A., Haudenschild, D. R., Rose, L., Reddi, A. H. (2003) Interleukin-17 family and IL-17 receptors. Cytokine Growth Factor Rev. 14, 155-174.
48. Miossec, P. (2003) Interleukin-17 in rheumatoid arthritis: if T cells were to contribute to inflammation and destruction through synergy. Arthritis Rheum. 48, 594-601.
49. Oda, T., Yoshie, H., Yamazaki, K. (2003) Porphyromonas gingivalis antigen preferentially stimulates T cells to express IL-17 but not receptor activator of NF-κB ligand in vitro. Oral Microbiol. Immunol. 18, 30-36.
50. Grossi, S. G., Zambon, J. J., Ho, A. W., Koch, G., Dunford, R. G., Machtei, E. E., Norderyd, O. M., Genco, R. J. (1994) Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J. Periodontol. 65, 260-267.
51. Grossi, S. G., Genco, R. J., Machtei, E. E., Ho, A. W., Koch, G., Dunford, R., Zambon, J. J., Hausmann, E. (1995) Assessment of risk for periodontal disease. II. Risk indicators for alveolar bone loss. J. Periodontol. 66, 23-29.
52. Schwarzenberger, P., Kolls, J. K. (2002) Interleukin 17: an example for gene therapy as a tool to study cytokine mediated regulation of hematopoiesis. J. Cell. Biochem. Suppl. 38, 88-95.
53. De Boer, W. I. (2002) Cytokines and therapy in COPD: a promising combination? Chest 121, 209S-218S.
54. Kantarci, A., Oyaizu, K., Van Dyke, T. E. (2003) Neutrophil-mediated tissue injury in periodontal disease pathogenesis: findings from localized aggressive periodontitis. J. Periodontol. 74, 66-75.
55. Baker, P. J. (2000) The role of immune responses in bone loss during periodontal disease. Microbes Infect. 2, 1181-1192.
56. Hamilton, T. A., Ohmori, Y., Tebo, J. (2002) Regulation of chemokine expression by antiinflammatory cytokines. Immunol. Res. 25, 229-245.
57. Bevilacqua, A., Ceriani, M. C., Capaccioli, S., Nicolin, A. (2003) Post-transcriptional regulation of gene expression by degradation of messenger RNAs. J. Cell. Physiol. 195, 356-372.
58. O'Dell, J. (1999) Anticytokine therapy-a new era in the treatment of rheumatoid arthritis? N. Engl. J. Med. 340, 310-312.
59. Iwakura, Y., Tosu, M., Yoshida, E., Takiguchi, M., Sato, K., Kitajima, I., Nishioka, K., Yamamoto, K., Takeda, T., Hatanaka, M., et al. (1991) Induction of inflammatory arthropathy resembling rheumatoid arthritis in mice transgenic for HTLV-I. Science 253, 1026-1028.
60. Horai, R., Saijo, S., Tanioka, H., Nakae, S., Sudo, K., Okahara, A., Ikuse, T., Asano, M., Iwakura, Y. (2000) Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. J. Exp. Med. 191, 313-320.
61. Halloran, M., Woods, J., Strieter, R., Szekanecz, Z., Volin, M., Hosaka, S., Haines, G., Kunkel, S., Burdick, M., Walz, A., Koch, A. (1999) The role of an epithelial neutrophil-activating peptide-78-like protein in rat adjuvent-induced arthritis. J. Immunol. 162, 7492-7500.
62. Rieder, G., Einsiedl, W., Hatz, R., Stolte, M., Enders, G., Walz, A. (2001) Comparison of CXC chemokines ENA-78 and interleukin-8 expression in Helicobacter pylori-associated gastritis. Infect. Immun. 69, 81-88.
63. Thorpe, C., Smith, W., Hurley, B., Acheson, D. (2001) Shiga toxins induce, superinduce, and stabilize a variety of C-X-C chemokine mRNAs in intestinal epithelial cells, resulting in increased chemokine expression. Infect. Immun. 69, 6140-6147.
64. Donninger, H., Glashoff, R., Haitchi, H-M., Syce, J., Ghildyal, R., van Rensburg, E., Bardin, P. (2003) Rhinovirus induction of the CXC chemokine epithelial-neutrophil activating peptide-78 in bronchial epithelium. J. Infect. Dis. 187, 1809-1817.
65. Jones, C. E., Chan, K. (2002) Interleukin-17 stimulates the expression of interleukin-8, growth-related oncogene-α, and granulocyte-colony- stimulating factor by human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 26, 748-753.
66. Van Dyke, T. E., Serhan, C. N. (2003) Resolution of inflammation: a new paradigm for the pathogenesis of periodontal diseases. J. Dent. Res. 82, 82-90.