IL-1β induces IL-6 expression in human orbital fibroblasts: Identification of an anatomic-site specific phenotypic attribute relevant to thyroid-associated ophthalmopathy

Journal of Immunology

Volumn 175, Issue 2, 2005, Pages 1310-1319

  Chen, Beiling ^b   Tsui, Shamli ^b   Smith, Terry J ^a  

^a HARBOR UCLA MEDICAL CENTER   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; RECOMBINANT INTERLEUKIN 6; STAT3 PROTEIN;

ADIPOCYTE; ARTICLE; B LYMPHOCYTE ACTIVATION; CELL METABOLISM; CYTOKINE PRODUCTION; ENDOCRINE OPHTHALMOPATHY; FIBROBLAST; GENE EXPRESSION; GRAVES DISEASE; HUMAN; HUMAN CELL; IMMUNOREGULATION; INFLAMMATION; ORBIT; ORBIT FIBROBLAST; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKIN FIBROBLAST;

EID: 23244464983     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.2.1310     Document Type: Article

References (67)

1. Hufnagel, T. J., W. F. Hickey, W. H. Cobbs, F. A. Jakobiec, T. Iwamoto, and R. C. Eagle. 1984. Immunohistochemical and ultrastructural studies on the exenterated orbital tissues of a patient with Graves' disease. Ophthalmology 91: 1411-1419.
2. Smith, T. J., R. S. Bahn, and C. A. Gorman. 1989. Connective tissue, glycosaminoglycans, and diseases of the thyroid. Endocr. Rev. 10: 366-391.
3. de Carli, M., M. M. D'Elios, S. Mariotti, C. Marcocci, A. Pinchera, M. Ricci, S. Romagnani, and G. del Prete. 1993. Cytolytic T cells with Thl-like cytokine profile predominate in retroorbital lymphocytic infiltrates of Graves' ophthalmopathy. J. Clin. Endocrinol. Metab. 77: 1120-1124.
4. + and specifically recognize autologous fibroblasts. J. Clin. Invest. 93: 2738-2743.
5. Jaume, J. C., S. Portolano, M. F. Prummel, S. M. McLachlan, and B. Rapoport. 1994. Molecular cloning and characterization of genes for antibodies generated by orbital tissue-infiltrating B-cells in Graves' ophthalmopathy. J. Clin. Endocrinol. Metab. 78: 348-352.
6. Kazim, M., R. A. Goldberg, and T. J. Smith. 2002. Insights into the pathogenesis of thyroid-associated orbitopathy: evolving rationale for therapy. Arch. Ophthalmol. 120: 380-386.
7. Pritchard, J., R. Han, N. Horst, W. W. Cruikshank, and T. J. Smith. 2003. Immunoglobulin activation of T cell chemoattractant expression in fibroblasts from patients with Graves' disease is mediated through the IGF-1 receptor pathway. J. Immunol. 170: 6348-6354.
8. Smith, T. J., R. J. Kottke, H. Lum, and T. T. Andersen. 1993. Human orbital fibroblasts in culture bind and respond to endothelin. Am. J. Physiol. 265(1 Pt. 1): C138-C142.
9. Cao, H. J., H.-S. Wang, Y. Zhang, H.-Y. Lin, R. P. Phipps, and T. J. Smith. 1998. Activation of human orbital fibroblasts through CD40 engagement results in a dramatic induction of hyaluronan synthesis and prostaglandin endoperoxide H synthase-2 expression: insights into potential pathogenic mechanisms of thyroid associated ophthalmopathy. J. Biol. Chem. 273: 29615-29625.
10. Wang, H.-S., H. J. Cao, V. D. Winn, L. J. Rezanka, Y. Frobert, C. H. Evans, D. Sciaky, D. A. Young, and T. J. Smith. 1996. Leukoregulin induction of prostaglandin endoperoxide H synthase-2 in human orbital fibroblasts: an in vitro model for connective tissue inflammation. J. Biol. Chem. 271: 22718-22728.
11. Sempowski, G. D., J. Rozenblit, T. J. Smith, and R. P. Phipps. 1998. Human orbital fibroblasts are activated through CD40 to induce pro-inflammatory cytokine production. Am. J. Physiol. 274: C707-C714.
12. Sciaky, D., W. Brazer, D. M. Center, W. W. Cruikshank, and T. J. Smith. 2000. Cultured human fibroblasts express constitutive IL-16 mRNA: cytokine induction of active IL-16 protein synthesis through a caspase-3-dependent mechanism. J. Immunol. 164: 3806-3814.
13. Smith, T. J., L. Koumas, A. Gagnon, A. Bell, G. D. Sempowski, R. P. Phipps, and A. Sorisky. 2002. Orbital fibroblast heterogeneity may determine the clinical presentation of thyroid-associated ophthalmopathy. J. Clin. Endocrinol. Metab. 87: 385-392.
14. Sorisky, A., D. Pardasani, A. Gagnon, and T. J. Smith. 1996. Evidence of adipocyte differentiation in human orbital fibroblasts in primary culture. J. Clin. Endocrinol. Metab. 81: 3428-3431.
15. Tackey, E., P. E. Lipsky, and G. G. Illei. 2004. Rationale for interleukin-6 blockade in systemic lupus erythematosus. Lupus 13: 339-343.
16. Ishihara, K., and T. Hirano. 2002. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev. 13: 357-368.
17. Salvi, M., G. Girasole, M. Pedrazzoni, M. Passeri, N. Giuliani, R. Minelli, L. E. Braverman, and E. Roti. 1996. Increased serum concentrations of interleukin-6 (IL-6) and soluble IL-6 receptor in patients with Graves' disease. J. Clin. Endocrinol. Metab. 81 2976-2979.
18. Salvi, M., M. Pedrazzoni, G. Girasole, N. Giuliani, R. Minelli, J. R. Wall, and E. Roti. 2000. Serum concentrations of proinflammatory cytokines in Graves' disease: effect of treatment, thyroid function, ophthalmopathy and cigarette smoking. Eur. J. Endocrinol. 143: 197-202.
19. Hidaka, Y., M. Okumura, Y. Shimaoka, K. Takeoka, H. Tada, and N. Amino. 1998. Increased serum concentration of interleukin-5 in patients with Graves' disease and Hashimoto's thyroiditis. Thyroid 8: 235-239.
20. Bossowski, A., and M. Urban. 2001. Serum levels of cytokines in children and adolescents with Graves' disease and non-toxic nodular goiter. J. Pediatr. Endocrinol. Metab. 14: 741-747.
21. Molnar, I., and C. Balazs. 1997. High circulating IL-6 level in Graves' ophthalmopathy. Autoimmunity 25: 91-96.
22. Wakelkamp, I. M., M. N. Gerding, J. W. Van Der Meer, M. F. Prummel, and W. M. Wiersinga. 2000. Both Th1- and Th2-derived cytokines in serum are elevated in Graves' ophthalmopathy. Clin. Exp. Immunol. 121: 453-457.
23. Hiromatsu, Y., D. Yang, T. Bednarczuk, I. Miyake, K. Nonaka, and Y. Inoue. 2000, Cytokine profiles in eye muscle tissue and orbital fat tissue from patients with thyroid-associated ophthalmopathy. J. Clin. Endocrinol. Metab. 85: 1194-1199.
24. Wahrenberg, H., A. Wennlund, and J. Hoffstedt. 2002. Increased adipose tissue secretion of interleukin-6, but not of leptin, plasminogen activator inhibitor-1 or tumour necrosis factor α, in Graves' hyperthyroidism. Eur. J. Endocrinol. 146: 607-611.
25. Taga, T., and T. Kishimoto. 1997. Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol. 15: 797-819.
26. Kishimoto, T., S. Akira, and T. Taga. 1992. Interleukin-6 and its receptor: a paradigm for cytokines. Science 258: 593-597.
27. Heinrich, P. C., I. Behrmann, G. Muller-Newen, F. Schaper, and L. Graeve. 1998. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 334: 297-314.
28. Kehry, M. R., and B. E. Castle. 1994. Regulation of CD40 ligand expression and use of recombinant CD40 ligand for studying B cell growth and differentiation. Semin. Immunol. 6: 287-294.
29. Smith, T. J. 1987. n-Butyrate inhibition of hyaluronate synthesis in cultured human fibroblasts. J. Clin. Invest. 79: 1493-1497.
30. Smith, T. J., G. D. Sempowski, H.-S. Wang, P. J. Del Vecchio, S. D. Lippe, and R. P. Phipps. 1995. Evidence for cellular heterogeneity in primary cultures of human orbital fibroblasts. J. Clin. Endocrinol. Metab. 80: 2620-2625.
31. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159.
32. 2 synthase expression. J. Biol. Chem. 277: 16355-16364.
33. Vannier, E., and C. A. Dinarello. 1994. Histamine enhances interleukin (IL)-1-induced IL-6 gene expression and protein synthesis via H2 receptors in peripheral blood mononuclear cells. J. Biol. Chem. 269: 9952-9956.
34. Smoak, K. A., and J. A. Cidlowski. 2004. Mechanisms of glucocorticoid receptor signaling during inflammation. Mech. Ageing Dev. 125: 697-706.
35. Smith, T. J. 1988. Glucocorticoid regulation of glycosaminoglycan synthesis in cultured human skin fibroblasts: evidence for a receptor-mediated mechanism involving effects on specific de novo protein synthesis. Metabolism 37: 179-184.
36. Hirano, T. 1998. Interleukin 6 and its receptor: 10 years later. Int. Rev. Immunol. 16: 249-284.
37. Mori, N., F. Shirakawa, H. Shimizu, S. Murakami, S. Oda, K. Yamamoto, and S. Eto. 1994. Transcriptional regulation of the human interleukin-6 gene promoter in human T cell leukemia virus type I-infected T cell lines: evidence for the involvement of NF-κB. Blood 84: 2904-2911.
38. Saklatvala, J., L. Rawlinson, R. J. Waller, S. Sarsfield, J. C. Lee, L. F. Morton, M. J. Barnes, and R. W. Farndale. 1996. Role for p38 mitogen-activated protein kinase in platelet aggregation caused by collagen or a thromboxane analogue. J. Biol. Chem. 271: 6586-6589.
39. Pang, L., T. Sawada, S. J. Decker, and A. R. Saltiel. 1995. Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J. Biol. Chem. 270: 13585-13588.
40. Hershko, D. D., B. W. Robb, G. Luo, and P.-O. Hasselgren. 2002. Multiple transcription factors regulating the IL-6 gene are activated by cAMP in cultured Caco-2 cells. Am. J. Physiol Regul. Integr. Comp. Physiol. 283: R1140-R1148.
41. Radeff, J. M., Z. Nagy, and P. H. Stern. 2001. Involvement of PKC-β in PTH, TNF-α, and IL-1β effects on IL-6 promoter in osteoblastic cells and on PTH-stimulated bone resorption. Exp. Cell Res. 268: 179-188.
42. Vgontzas, A. N., D. A. Papanicolaou, E. O. Bixler, A. Kales, K. Tyson, and G. P. Chrousos. 1997. Elevation of plasma cytokines in disorders of excessive daytime sleepiness: role of sleep disturbance and obesity. J. Clin. Endocrinol. Metab. 82: 1313-1316.
43. Mohamed-Ali, V., L. Flower, J. Sethi, G. Hotamisligil, R. Gray, S. E. Humphries, D. A. York, and J. Pinkney. 2001. β-Adrenergic regulation of IL-6 release from adipose tissue: in vivo and in vitro studies. J. Clin. Endocrinol. Metab. 86: 5864-5869.
44. Päth, G., S. R. Bornstein, M. Gurniak, G. P. Chrousos, W. A. Scherbaum, and H. Hauner. 2001. Human breast adipocytes express interleukin-6 (IL-6) and its receptor system: increased IL-6 production by β-adrenergic activation and effects of IL-6 on adipocyte function. J. Clin. Endocrinol. Metab. 86: 2281-2288.
45. Diehl, S., and M. Rincon. 2002. The two faces of IL-6 on Th1/Th2 differentiation. Mol. Immunol. 39: 531-536.
46. Weissenbach, M., T. Clahsen, C. Weber, D. Spitzer, D. Wirth, D. Vestweber, P. C. Heinrich, and F. Schaper. 2004. Interleukin-6 is a direct mediator of T cell migration. Eur. J. Immunol. 34: 2895-2906.
47. Chomarat, P., J. Banchereau, J. Davoust, and A. K. Palucka. 2000. IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat. Immunol. 1: 510-514.
48. Bernhard, H., M. Lohmann, W. Y. Batten, J. Metzger, H. F. Lohr, C. Peschel, K. M. zum Buschenfelde, and S. Rose-John. 2000. The gp130-stimulatmg designer cytokine hyper-IL-6 promotes the expansion of human hematopoietic progenitor cells capable to differentiate into functional dendritic cells. Exp. Hematol. 28: 365-372.
49. Park, S. J., T. Nakagawa, H. Kitamura, T. Atsumi, H. Kamon, S. Sawa, D. Kamimura, N. Ueda, Y. Iwakura, K. Ishihara, M. Murakami, and T. Hirano. 2004. IL-6 regulates in vivo dendritic cell differentiation through STAT3 activation. J. Immunol. 173: 3844-3854.
50. Pramanik, R., T. N. Jørgensen, H. Xin, B. L. Kotzin, and D. Choubey. 2004. Interleukin-6 induces expression of Ifi202, an interferon-inducible candidate gene for lupus susceptibility. J. Biol. Chem. 279: 16121-16127.
51. Radtke, S., H. M. Hermanns, C. Haan, H. Schmitz-Van De Leur, H. Gascan, P. C. Heinrich, and I. Behrmann. 2002. Novel role of Janus kinase 1 in the regulation of oncostatin M receptor surface expression. J. Biol. Chem. 277: 11297-11305.
52. Haan, C., P. C. Heinrich, and I. Behrmann. 2002. Structural requirements of the interleukin-6 signal transducer gp130 for its interaction with Janus kinase 1: the receptor is crucial for kinase activation. Biochem. J. 361: 105-111.
53. Huang, L. J., S. N. Constantinescu, and H. F. Lodish. 2001. The N-terminal domain of Janus kinase 2 is required for Golgi processing and cell surface expression of erythropoietin receptor. Mol. Cell 8: 1327-1338.
54. Faruqi, T. R., D. Gomez, X. R. Bustelo, D. Bar-Sagi, and N. C. Reich. 2001. Rac1 mediates STAT3 activation by autocrine IL-6. Proc. Natl. Acad. Sci. USA 98: 9014-9019.
55. Heinrich, P. C., I. Behrmann, S. Haan, H. M. Hermanns, G. Muller-Newen, and F. Schaper. 2003. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 374: 1-20.
56. Schmitz, J., H. Dahmen, C. Grimm, C. Gendo, G. Muller-Newen, P. C. Heinrich, and F. Schaper. 2000. The cytoplasmic tyrosine motifs in full-length glycoprotein 130 have different roles in IL-6 signal transduction. J. Immunol. 164: 848-854.
57. Kaptein, A., V. Paillard, and M. Saunders. 1996. Dominant negative Stat3 mutant inhibits interleukin-6-induced Jak-STAT signal transduction. J. Biol. Chem. 271: 5961-5964.
58. Shuai, K., C. M. Horvath, L. H. Huang, S. A. Qureshi, D. Cowburn, and J. E. Darnell. Jr. 1994. Interferon activation of the transcription factor Stat91 involves dimerization through SH2-phosphotyrosyl peptide interactions. Cell 76: 821-828.
59. Brocke-Heidrich, K., A. K. Kretzschmar, G. Pfeifer, C. Henze, D. Loffler, D. Koczan, H. J. Thiesen, R. Burger, M. Gramatzki, and F. Horn. 2004. Interleukin-6-dependent gene expression profiles in multiple myeloma INA-6 cells reveal a Bcl-2 family-independent survival pathway closely associated with Stat3 activation. Blood 103: 242-251.
60. Yoshizaki, K., N. Nishimoto, M. Mihara, and T. Kishimoto. 1998. Therapy of rheumatoid arthritis by blocking IL-6 signal transduction with a humanized anti-IL-6 receptor antibody. Springer Semin. Immunopathol 20: 247-259.
61. Naka, T., N. Nishimoto, and T. Kishimoto. 2002. The paradigm of IL-6: from basic science to medicine. Arthritis Res. 4(Suppl. 3): S233-S242.
62. Guerne, P. A., B. L. Zuraw, J. H. Vaughan, D. A. Carson, and M. Lotz. 1989. Synovium as a source of interleukin 6 in vitro: contribution to local and systemic manifestations of arthritis. J. Clin. Invest. 83: 585-592.
63. Miyazawa, K., A. Mori, H. Miyata, M. Akahane, Y. Ajisawa, and H. Okudaira. 1998. Regulation of interleukin-1β-induced interleukin-6 gene expression in human fibroblast-like synoviocytes by p38 mitogen-activated protein kinase. J. Biol. Chem. 273: 24832-24838.
64. Aust, G., and W. A. Scherbaum. 1996. Expression of cytokines in the thyroid: thyrocytes as potential cytokine producers. Exp. Clin. Endocrinol. Diabetes 104(Suppl. 4): 64-67.
65. Gianoukakis, A. G., and T. J. Smith. 2004. The role of cytokines in the pathogenesis of endocrine disease. Can. J. Diabetes 28: 30-42.
66. Pritchard, J., N. Horst, W. Cruikshank, and T. J. Smith. 2002. Igs from patients with Graves' disease induce the expression of T cell chemoattractants in their fibroblasts. J. Immunol. 168: 942-950.
67. Pritchard, J., S. Tsui, N. Horst, W. W. Cruikshank, and T. J. Smith. 2004. Synovial fibroblasts from patients with rheumatoid arthritis, like fibroblasts from Graves' disease, express high levels of IL-16 when treated with immunoglobulins against the IGF-1 receptor. J. Immunol. 173: 3564-3569.