IL-10-induced gp130 expression in mouse mast cells permits IL-6 trans-signaling

Journal of Leukocyte Biology

Volumn 91, Issue 3, 2012, Pages 427-435

  Traum, Daniel ^a   Timothee, Patricia ^a   Silver, Jonathan ^b   Rose John, Stefan ^c   Ernst, Matthias ^d   LaRosa, David F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^c UNIVERSITY OF KIEL   (Germany)

^d ROYAL MELBOURNE HOSPITAL   (Australia)

Author keywords

IL 27; SOCS3; STAT3

Indexed keywords

GLYCOPROTEIN GP 130; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 27; INTERLEUKIN 6; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL SURFACE; CELL SURVIVAL; CYTOKINE RELEASE; GLYCOSYLATION; MAST CELL; MOUSE; NONHUMAN; PERITONEUM MAST CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; BONE MARROW CELLS; CELL SURVIVAL; CELLS, CULTURED; CYTOKINE RECEPTOR GP130; CYTOKINES; G0 PHASE; GENE EXPRESSION REGULATION; INTERLEUKIN-10; INTERLEUKIN-6; INTERLEUKINS; MAST CELLS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84857834738     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0411209     Document Type: Article

References (71)

1. Abe, T., Nawa, Y. (1987) Reconstitution of mucosal mast cells in W/WV mice by adoptive transfer of bone marrow-derived cultured mast cells and its effects on the protective capacity to Strongyloides ratti-infection. Parasite Immunol. 9, 31-38.
2. Kamiya, M., Oku, Y., Itayama, H., Ohbayashi, M. (1985) Prolonged expulsion of adult Trichinella spiralis and eosinophil infiltration in mast celldeficient W/Wv mice. J. Helminthol. 59, 233-239.
3. Echtenacher, B., Mannel, D. N., Hultner, L. (1996) Critical protective role of mast cells in a model of acute septic peritonitis. Nature 381, 75-77.
4. Secor, V. H., Secor, W. E., Gutekunst, C. A., Brown, M. A. (2000) Mast cells are essential for early onset and severe disease in a murine model of multiple sclerosis. J. Exp. Med. 191, 813-822.
5. Metz, M., Grimbaldeston, M. A., Nakae, S., Piliponsky, A. M., Tsai, M., Galli, S. J. (2007) Mast cells in the promotion and limitation of chronic inflammation. Immunol. Rev. 217, 304-328.
6. Eklund, K. K. (2007) Mast cells in the pathogenesis of rheumatic diseases and as potential targets for anti-rheumatic therapy. Immunol. Rev. 217, 38-52.
7. Hueber, A. J., Asquith, D. L., Miller, A. M., Reilly, J., Kerr, S., Leipe, J., Melendez, A. J., McInnes, I. B. (2010) Mast cells express IL-17A in rheumatoid arthritis synovium. J. Immunol. 184, 3336-3340.
8. Kovanen, P. T. (2007) Mast cells: multipotent local effector cells in atherothrombosis. Immunol. Rev. 217, 105-122.
9. Weller, K., Foitzik, K., Paus, R., Syska, W., Maurer, M. (2006) Mast cells are required for normal healing of skin wounds in mice. FASEB J. 20, 2366-2368.
10. Lu, L. F., Lind, E. F., Gondek, D. C., Bennett, K. A., Gleeson, M. W., Pino-Lagos, K., Scott, Z. A., Coyle, A. J., Reed, J. L., Van Snick, J., Strom, T. B., Zheng, X. X., Noelle, R. J. (2006) Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 442, 997-1002.
11. Gilfillan, A. M., Tkaczyk, C. (2006) Integrated signalling pathways for mast-cell activation. Nat. Rev. Immunol. 6, 218-230.
12. Silver, J. S., Hunter, C. A. (2010) gp130 at the nexus of inflammation, autoimmunity, and cancer. J. Leukoc. Biol. 88, 1145-1156.
13. Saito, M., Yoshida, K., Hibi, M., Taga, T., Kishimoto, T. (1992) Molecular cloning of a murine IL-6 receptor-associated signal transducer, gp130, and its regulated expression in vivo. J. Immunol. 148, 4066-4071.
14. Radtke, S., Wuller, S., Yang, X. P., Lippok, B. E., Mutze, B., Mais, C., de Leur, H. S., Bode, J. G., Gaestel, M., Heinrich, P. C., Behrmann, I., Schaper, F., Hermanns, H. M. (2010) Cross-regulation of cytokine signalling: pro-inflammatory cytokines restrict IL-6 signalling through receptor internalisation and degradation. J. Cell Sci. 123, 947-959.
15. Yasukawa, H., Ohishi, M., Mori, H., Murakami, M., Chinen, T., Aki, D., Hanada, T., Takeda, K., Akira, S., Hoshijima, M., Hirano, T., Chien, K. R., Yoshimura, A. (2003) IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat. Immunol. 4, 551-556.
16. Doganci, A., Eigenbrod, T., Krug, N., De Sanctis, G. T., Hausding, M., Erpenbeck, V. J., Haddad el, B., Lehr, H. A., Schmitt, E., Bopp, T., Kallen, K. J., Herz, U., Schmitt, S., Luft, C., Hecht, O., Hohlfeld, J. M., Ito, H., Nishimoto, N., Yoshizaki, K., Kishimoto, T., Rose-John, S., Renz, H., Neurath, M. F., Galle, P. R., Finotto, S. (2005) The IL-6R α chain controls lung CD4+CD25+ Treg development and function during allergic airway inflammation in vivo. J. Clin. Invest. 115, 313-325.
17. Finotto, S., Eigenbrod, T., Karwot, R., Boross, I., Doganci, A., Ito, H., Nishimoto, N., Yoshizaki, K., Kishimoto, T., Rose-John, S., Galle, P. R., Neurath, M. F. (2007) Local blockade of IL-6R signaling induces lung CD4+ T cell apoptosis in a murine model of asthma via regulatory T cells. Int. Immunol. 19, 685-693.
18. Miyazaki, Y., Inoue, H., Matsumura, M., Matsumoto, K., Nakano, T., Tsuda, M., Hamano, S., Yoshimura, A., Yoshida, H. (2005) Exacerbation of experimental allergic asthma by augmented Th2 responses in WSX-1-deficient mice. J. Immunol. 175, 2401-2407.
19. Rose-John, S., Scheller, J., Elson, G., Jones, S. A. (2006) Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J. Leukoc. Biol. 80, 227-236.
20. Stumhofer, J. S., Hunter, C. A. (2008) Advances in understanding the anti-inflammatory properties of IL-27. Immunol. Lett. 117, 123-130.
21. Pflanz, S., Hibbert, L., Mattson, J., Rosales, R., Vaisberg, E., Bazan, J. F., Phillips, J. H., McClanahan, T. K., de Waal Malefyt, R., Kastelein, R. A. (2004) WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27. J. Immunol. 172, 2225-2231.
22. Artis, D., Villarino, A., Silverman, M., He, W., Thornton, E. M., Mu, S., Summer, S., Covey, T. M., Huang, E., Yoshida, H., Koretzky, G., Goldschmidt, M., Wu, G. D., de Sauvage, F., Miller, H. R., Saris, C. J., Scott, P., Hunter, C. A. (2004) The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity. J. Immunol. 173, 5626-5634.
23. Tebbutt, N. C., Giraud, A. S., Inglese, M., Jenkins, B., Waring, P., Clay, F. J., Malki, S., Alderman, B. M., Grail, D., Hollande, F., Heath, J. K., Ernst, M. (2002) Reciprocal regulation of gastrointestinal homeostasis by SHP2 and STAT-mediated trefoil gene activation in gp130 mutant mice. Nat. Med. 8, 1089-1097.
24. Galli, S. J., Dvorak, A. M., Marcum, J. A., Ishizaka, T., Nabel, G., Der Simonian, H., Pyne, K., Goldin, J. M., Rosenberg, R. D., Cantor, H., Dvorak, H. F. (1982) Mast cell clones: a model for the analysis of cellular maturation. J. Cell Biol. 95, 435-444.
25. Hunter, C. A. (2005) New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat. Rev. Immunol. 5, 521-531.
26. Hu, Z. Q., Zhao, W. H., Shimamura, T. (2007) Regulation of mast cell development by inflammatory factors. Curr. Med. Chem. 14, 3044-3050.
27. Townsend, J. M., Fallon, G. P., Matthews, J. D., Smith, P., Jolin, E. H., McKenzie, N. A. (2000) IL-9-deficient mice establish fundamental roles for IL-9 in pulmonary mastocytosis and goblet cell hyperplasia but not T cell development. Immunity 13, 573-583.
28. Conti, P., Kempuraj, D., Kandere, K., Di Gioacchino, M., Barbacane, R. C., Castellani, M. L., Felaco, M., Boucher, W., Letourneau, R., Theo-harides, T. C. (2003) IL-10, an inflammatory/inhibitory cytokine, but not always. Immunol. Lett. 86, 123-129.
29. Thompson-Snipes, L., Dhar, V., Bond, M. W., Mosmann, T. R., Moore, K. W., Rennick, D. M. (1991) Interleukin 10: a novel stimulatory factor for mast cells and their progenitors. J. Exp. Med. 173, 507-510.
30. Ho, L. H., Ohno, T., Oboki, K., Kajiwara, N., Suto, H., Iikura, M., Okayama, Y., Akira, S., Saito, H., Galli, S. J., Nakae, S. (2007) IL-33 induces IL-13 production by mouse mast cells independently of IgE-FcεRI signals. J. Leukoc. Biol. 82, 1481-1490.
31. Qiao, H., Andrade, M. V., Lisboa, F. A., Morgan, K., Beaven, M. A. (2006) Fc_R1 and Toll-like receptors mediate synergistic signals to markedly augment production of inflammatory cytokines in murine mast cells. Blood 107, 610-618.
32. Jones, S. A., Richards, P. J., Scheller, J., Rose-John, S. (2005) IL-6 transsignaling: the in vivo consequences. J. Interferon Cytokine Res. 25, 241-253.
33. Klouche, M., Bhakdi, S., Hemmes, M., Rose-John, S. (1999) Novel path to activation of vascular smooth muscle cells: up-regulation of gp130 creates an autocrine activation loop by IL-6 and its soluble receptor. J. Immunol. 163, 4583-4589.
34. Marz, P., Otten, U., Rose-John, S. (1999) Neural activities of IL-6-type cytokines often depend on soluble cytokine receptors. Eur. J. Neurosci. 11, 2995-3004.
35. Romano, M., Sironi, M., Toniatti, C., Polentarutti, N., Fruscella, P., Ghezzi, P., Faggioni, R., Luini, W., van Hinsbergh, V., Sozzani, S., Bussolino, F., Poli, V., Ciliberto, G., Mantovani, A. (1997) Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity 6, 315-325.
36. Peters, M., Blinn, G., Solem, F., Fischer, M., Meyer zum Buschenfelde, K. H., Rose-John, S. (1998) In vivo and in vitro activities of the gp130-stimulating designer cytokine Hyper-IL-6. J. Immunol. 161, 3575-3581.
37. Yoshimura, A., Naka, T., Kubo, M. (2007) SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 7, 454-465.
38. Qin, H., Roberts, K. L., Niyongere, S. A., Cong, Y., Elson, C. O., Benveniste, E. N. (2007) Molecular mechanism of lipopolysaccharide-induced SOCS-3 gene expression in macrophages and microglia. J. Immunol. 179, 5966-5976.
39. El Kasmi, K. C., Holst, J., Coffre, M., Mielke, L., de Pauw, A., Lhocine, N., Smith, A. M., Rutschman, R., Kaushal, D., Shen, Y., Suda, T., Donnelly, R. P., Myers Jr., M. G., Alexander, W., Vignali, D. A., Watowich, S. S., Ernst, M., Hilton, D. J., Murray, P. J. (2006) General nature of the STAT3-activated anti-inflammatory response. J. Immunol. 177, 7880-7888.
40. Jenkins, B. J., Roberts, A. W., Najdovska, M., Grail, D., Ernst, M. (2005) The threshold of gp130-dependent STAT3 signaling is critical for normal regulation of hematopoiesis. Blood 105, 3512-3520.
41. Jenkins, B. J., Grail, D., Nheu, T., Najdovska, M., Wang, B., Waring, P., Inglese, M., McLoughlin, R. M., Jones, S. A., Topley, N., Baumann, H., Judd, L. M., Giraud, A. S., Boussioutas, A., Zhu, H. J., Ernst, M. (2005) Hyperactivation of Stat3 in gp130 mutant mice promotes gastric hyperproliferation and desensitizes TGF-β signaling. Nat. Med. 11, 845-852.
42. Jones, S. A. (2005) Directing transition from innate to acquired immunity: defining a role for IL-6. J. Immunol. 175, 3463-3468.
43. Teague, T. K., Marrack, P., Kappler, J. W., Vella, A. T. (1997) IL-6 rescues resting mouse T cells from apoptosis. J. Immunol. 158, 5791-5796.
44. Cruse, G., Cockerill, S., Bradding, P. (2008) IgE alone promotes human lung mast cell survival through the autocrine production of IL-6. BMC Immunol. 9, 2.
45. Xing, W., Austen, K. F., Gurish, M. F., Jones, T. G. (2011) Protease phenotype of constitutive connective tissue and of induced mucosal mast cells in mice is regulated by the tissue. Proc. Natl. Acad. Sci. USA 108, 14210-14215.
46. Bancroft, A. J., Humphreys, N. E., Worthington, J. J., Yoshida, H., Grencis, R. K. (2004) WSX-1: a key role in induction of chronic intestinal nematode infection. J. Immunol. 172, 7635-7641.
47. Blanchard, F., Wang, Y., Kinzie, E., Duplomb, L., Godard, A., Baumann, H. (2001) Oncostatin M regulates the synthesis and turnover of gp130, leukemia inhibitory factor receptor α, and oncostatin M receptor β by distinct mechanisms. J. Biol. Chem. 276, 47038-47045.
48. Gibson, R. M., Schiemann, W. P., Prichard, L. B., Reno, J. M., Ericsson, L. H., Nathanson, N. M. (2000) Phosphorylation of human gp130 at Ser-782 adjacent to the Di-leucine internalization motif. Effects on expression and signaling. J. Biol. Chem. 275, 22574-22582.
49. Thiel, S., Behrmann, I., Dittrich, E., Muys, L., Tavernier, J., Wijdenes, J., Heinrich, P. C., Graeve, L. (1998) Internalization of the interleukin 6 signal transducer gp130 does not require activation of the Jak/STAT pathway. Biochem. J. 330, 47-54.
50. Thiel, S., Dahmen, H., Martens, A., Müller-Newen, G., Schaper, F., Heinrich, P. C., Graeve, L. (1998) Constitutive internalization and association with adaptor protein-2 of the interleukin-6 signal transducer gp130. FEBS Lett. 441, 231-234.
51. Waetzig, G. H., Chalaris, A., Rosenstiel, P., Suthaus, J., Holland, C., Karl, N., Valles Uriarte, L., Till, A., Scheller, J., Grotzinger, J., Schreiber, S., Rose-John, S., Seegert, D. (2010) N-linked glycosylation is essential for the stability but not the signaling function of the interleukin-6 signal transducer glycoprotein 130. J. Biol. Chem. 285, 1781-1789.
52. Shelburne, C. P., McCoy, M. E., Piekorz, R., Sexl, V., Roh, K. H., Jacobs-Helber, S. M., Gillespie, S. R., Bailey, D. P., Mirmonsef, P., Mann, M. N., Kashyap, M., Wright, H. V., Chong, H. J., Bouton, L. A., Barnstein, B., Ramirez, C. D., Bunting, K. D., Sawyer, S., Lantz, C. S., Ryan, J. J. (2003) Stat5 expression is critical for mast cell development and survival. Blood 102, 1290-1297.
53. Magrangeas, F., Boisteau, O., Denis, S., Jacques, Y., Minvielle, S. (2001) Negative cross-talk between interleukin-3 and interleukin-11 is mediated by suppressor of cytokine signalling-3 (SOCS-3). Biochem. J. 353, 223-230.
54. Barclay, J. L., Anderson, S. T., Waters, M. J., Curlewis, J. D. (2007) Regulation of suppressor of cytokine signaling 3 (SOC3) by growth hormone in pro-B cells. Mol. Endocrinol. 21, 2503-2515.
55. Story, D. J., Stephens, J. M. (2006) Modulation and lack of cross-talk between signal transducer and activator of transcription 5 and suppressor of cytokine signaling-3 in insulin and growth hormone signaling in 3T3-L1 adipocytes. Obesity (Silver Spring) 14, 1303-1311.
56. Moore, K. W., de Waal Malefyt, R., Coffman, R. L., O'Garra, A. (2001) Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683-765.
57. Mocellin, S., Panelli, M. C., Wang, E., Nagorsen, D., Marincola, F. M. (2003) The dual role of IL-10. Trends Immunol. 24, 36-43.
58. Chen, W. F., Zlotnik, A. (1991) IL-10: a novel cytotoxic T cell differentiation factor. J. Immunol. 147, 528-534.
59. Santin, A. D., Hermonat, P. L., Ravaggi, A., Bellone, S., Pecorelli, S., Roman, J. J., Parham, G. P., Cannon, M. J. (2000) Interleukin-10 increases Th1 cytokine production and cytotoxic potential in human papillomavirus-specific CD8(+) cytotoxic T lymphocytes. J. Virol. 74, 4729-4737.
60. Rousset, F., Garcia, E., Defrance, T., Peronne, C., Vezzio, N., Hsu, D. H., Kastelein, R., Moore, K. W., Banchereau, J. (1992) Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc. Natl. Acad. Sci. USA 89, 1890-1893.
61. Burdin, N., Van Kooten, C., Galibert, L., Abrams, J. S., Wijdenes, J., Banchereau, J., Rousset, F. (1995) Endogenous IL-6 and IL-10 contribute to the differentiation of CD40-activated human B lymphocytes. J. Immunol. 154, 2533-2544.
62. Rennick, D., Hunte, B., Holland, G., Thompson-Snipes, L. (1995) Cofactors are essential for stem cell factor-dependent growth and maturation of mast cell progenitors: comparative effects of interleukin-3 (IL-3), IL-4, IL-10, and fibroblasts. Blood 85, 57-65.
63. Kennedy Norton, S., Barnstein, B., Brenzovich, J., Bailey, D. P., Kashyap, M., Speiran, K., Ford, J., Conrad, D., Watowich, S., Moralle, M. R., Kepley, C. L., Murray, P. J., Ryan, J. J. (2008) IL-10 suppresses mast cell IgE receptor expression and signaling in vitro and in vivo. J. Immunol. 180, 2848-2854.
64. Gillespie, S. R., DeMartino, R. R., Zhu, J., Chong, H. J., Ramirez, C., Shelburne, C. P., Bouton, L. A., Bailey, D. P., Gharse, A., Mirmonsef, P., Odom, S., Gomez, G., Rivera, J., Fischer-Stenger, K., Ryan, J. J. (2004) IL-10 inhibits Fc ε RI expression in mouse mast cells. J. Immunol. 172, 3181-3188.
65. Bouton, L. A., Ramirez, C. D., Bailey, D. P., Yeatman, C. F., Yue, J., Wright, H. V., Domen, J., Rosato, R. R., Grant, S., Fischer-Stenger, K., Ryan, J. J. (2004) Costimulation with interleukin-4 and interleukin-10 induces mast cell apoptosis and cell-cycle arrest: the role of p53 and the mitochondrion. Exp. Hematol. 32, 1137-1145.
66. Yeatman 2nd, C. F., Jacobs-Helber, S. M., Mirmonsef, P., Gillespie, S. R., Bouton, L. A., Collins, H. A., Sawyer, S. T., Shelburne, C. P., Ryan, J. J. (2000) Combined stimulation with the T helper cell type 2 cytokines interleukin (IL)-4 and IL-10 induces mouse mast cell apoptosis. J. Exp. Med. 192, 1093-1103.
67. O'Brien, C. A., Manolagas, S. C. (1997) Isolation and characterization of the human gp130 promoter. Regulation by STATS. J. Biol. Chem. 272, 15003-15010.
68. Mirmonsef, P., Shelburne, C. P., Fitzhugh Yeatman 2nd, C., Chong, H. J., Ryan, J. J. (1999) Inhibition of Kit expression by IL-4 and IL-10 in murine mast cells: role of STAT6 and phosphatidylinositol 3_-kinase. J. Immunol. 163, 2530-2539.
69. Shoji, J., Kawaguchi, A., Gotoh, A., Inada, N., Sawa, M. (2007) Concentration of soluble interleukin-6 receptors in tears of allergic conjunctival disease patients. Jpn. J. Ophthalmol. 51, 332-337.
70. Klimiuk, P. A., Sierakowski, S., Latosiewicz, R., Cylwik, J. P., Cylwik, B., Skowronski, J., Chwiecko, J. (2003) Interleukin-6, soluble interleukin-2 receptor and soluble interleukin-6 receptor in the sera of patients with different histological patterns of rheumatoid synovitis. Clin. Exp. Rheumatol. 21, 63-69.
71. Yokoyama, A., Kohno, N., Sakai, K., Kondo, K., Hirasawa, Y., Hiwada, K. (1997) Circulating levels of soluble interleukin-6 receptor in patients with bronchial asthma. Am. J. Respir. Crit. Care Med. 156, 1688-1691.