Inhibition of IL-6 signaling by a p38-dependent pathway occurs in the absence of new protein synthesis

Journal of Leukocyte Biology

Volumn 72, Issue 1, 2002, Pages 154-162

  Ahmed, Simi T ^a   Mayer, Alexander ^b   Ji, Jong Dae ^b   Ivashkiv, Lionel B ^a,b,c  

^a Weill Cornell Graduate School of Biomedical Sciences   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

Cytokines; Monocytes macrophages; Signal transduction

Indexed keywords

ALPHA INTERFERON; FC RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; STAT PROTEIN; SYNAPTOPHYSIN; TOLL LIKE RECEPTOR;

ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; HOMEOSTASIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; RECEPTOR INTRINSIC ACTIVITY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

CELLS, CULTURED; CYCLOHEXIMIDE; HUMANS; INTERLEUKIN-1; INTERLEUKIN-6; KINETICS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; MONOCYTES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROSTAGLANDINS; PROTEIN BIOSYNTHESIS; PROTEIN SYNTHESIS INHIBITORS; PROTEIN-TYROSINE-PHOSPHATASE; SIGNAL TRANSDUCTION;

EID: 0036659520     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Schindler, C., Darnell Jr., J. E. (1995) Transcriptional responses to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 64, 621-651.
2. Ivashkiv, L. (2000) Jak-STAT signaling pathways in cells of the immune system. Rev. Immunogenet. 2, 220-230.
3. Azam, M., Lee, C., Strehlow, I., Schindler, C. (1997) Functionally distinct isoforms of STAT5 are generated by protein processing. Immunity 6, 691-701.
4. Kim, T. K., Maniatis, T. (1996) Regulation of interferon-gamma-activated STAT1 by the ubiquitin-proteasome pathway. Science 273, 1717-1719.
5. Haspel, R. L., Salditt-Georgieff, M., Darnell Jr., J. E. (1996) The rapid inactivation of nuclear tyrosine phosphorylated Stat1 depends upon a protein tyrosine phosphatase. EMBO J. 15, 6262-6268.
6. Shuai, K., Liao, J., Song, M. M. (1996) Enhancement of antiproliferative activity of gamma interferon by the specific inhibition of tyrosine dephosphorylation of Stat1. Mol. Cell. Biol. 16, 4932-4941.
7. Aragane, Y., Kulms, D., Luger, T. A., Schwarz, T. (1997) Down-regulation of interferon gamma-activated STAT1 by UV light. Proc. Natl. Acad. Sci. USA 94, 11490-11495.
8. Chung, C. D., Liao, J., Liu, B., Rao, X., Jay, P., Berta, P., Shuai, K. (1997) Specific inhibition of stat3 signal transduction by PIAS3. Science 278, 1803-1805.
9. Wang, D., Moriggl, R., Stravopodis, D., Carpino, N., Marine, J. C., Teglund, S., Feng, J., Ihle, J. N. (2000) A small amphipathic alpha-helical region is required for transcriptional activities and proteasome-dependent turnover of the tyrosine-phosphorylated Stat5. EMBO J. 19, 392-399.
10. Yu, C. L., Jin, Y. J., Burakoff, S. J. (2000) Cytosolic tyrosine dephosphorvlation of STAT5. Potential role of SHP-2 in STAT5 regulation. J. Biol. Chem. 275, 599-604.
11. Pernis, A., Gupta, S., Gollob, K. J., Garfein, E., Coffman, R. L., Schindler, C., Rothman, P. (1995) Lack of interferon gamma receptor beta chain and the prevention of interferon gamma signaling in TH1 cells. Science 269, 245-247.
12. Bach, E. A., Szabo, S. J., Dighe, A. S., Ashkenazi, A., Aguet, M., Murphy, K. M., Schreiber, R. D. (1995) Ligand-induced autoregulation of IFN-gamma receptor beta chain expression in T helper cell subsets. Science 270, 1215-1218.
13. Bianchi, M., Meng, C., Ivashkiv, L. B. (2000) Inhibition of IL-2-induced Jak-STAT signaling by glucocorticoids. Proc. Natl. Acad. Sci. USA 97, 9573-9578.
14. Wu, C. Y., Wang, K., McDyer, J. F., Seder, R. A. (1998) Prostaglandin E2 and dexamethasone inhibit IL-12 receptor expression and IL-12 responsiveness. J. Immunol. 161, 2723-2730.
15. Endo, T. A., Masuhara, M., Yokouchi, M., Suzuki, R., Sakamoto, H., Mitsui, K., Matsumoto, A., Tanimura, S., Ohtsubo, M., Misawa, H., Miyazaki, T., Leonor, N., Taniguchi, T., Fujita, T., Kanakura, Y., Komiya, S., Yoshimura, A. (1997) A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387, 921-924.
16. Naka, T., Narazaki, M., Hirata, M., Matsumoto, T., Minamoto, S., Aono, A., Nishimoto, N., Kajita, T., Taga, T., Yoshizaki, K., Akira, S., Kishimoto, T. (1997) Structure and function of a new STAT-induced STAT inhibitor. Nature 387, 924-929.
17. Starr, R., Willson, T. A., Viney, E. M., Murray, L. J., Rayner, J. R., Jenkins, B. J., Gonda, T. J., Alexander, W. S., Metcalf, D., Nicola, N. A., Hilton, D. J. (1997) A family of cytokine-inducible inhibitors of signalling. Nature 387, 917-921.
18. Yoshimura, A., Ohkubo, T., Kiguchi, T., Jenkins, N. A., Gilbert, D. J., Copeland, N. G., Hara, T., Miyajima, A. (1995) A novel cytokine-inducible gene CIS encodes an SH2-containing protein that binds to tyrosine-phosphorylated interleukin 3 and erythropoietin receptors. EMBO J. 14, 2816-2826.
19. Yasukawa, H., Sasaki, A., Yoshimura, A. (2000) Negative regulation of cytokine signaling pathways. Annu. Rev. Immunol. 18, 143-164.
20. Chen, X. P., Losman, J. A., Rothman, P. (2000) SOCS proteins, regulators of intracellular signaling. Immunity 13, 287-290.
21. Sengupta, T. K., Talbot, E. S., Scherle, P. A., Ivashkiv, L. B. (1998) Rapid inhibition of interleukin-6 signaling and Stat3 activation mediated by mitogen-activated protein kinases. Proc. Natl. Acad. Sci. USA 95, 11107-11112.
22. Sengupta, T. K., Schmitt, E. M., Ivashkiv, L. B. (1996) Inhibition of cytokines and JAK-STAT activation by distinct signaling pathways. Proc. Natl. Acad. Sci. USA 93, 9499-9504.
23. Lee, I. H., Li, W. P., Hisert, K. B., Ivashkiv, L. B. (1999) Inhibition of interleukin 2 signaling and signal transducer and activator of transcription (STAT)5 activation during T cell receptor-mediated feedback inhibition of T cell expansion. J. Exp. Med. 190, 1263-1274.
24. Zhu, J., Huang, H., Guo, L., Stonehouse, T., Watson, C. J., Hu-Li, J., Paul, W. E. (2000) Transient inhibition of interleukin 4 signaling by T cell receptor ligation. J. Exp. Med. 192, 1125-1134.
25. Ahmed, S. T., Ivashkiv, L. B. (2000) Inhibition of IL-6 and IL-10 signaling and stat activation by inflammatory and stress pathways. J. Immunol. 165, 5227-5237.
26. Kovanen, P. E., Junttila, I., Takaluoma, K., Saharinen, P., Valmu, L., Li, W., Silvennoinen, O. (2000) Regulation of jak2 tyrosine kinase by protein kinase C during macrophage differentiation of IL-3-dependent myeloid progenitor cells. Blood 95, 1626-1632.
27. Tian, Z., Shen, X., Feng, H., Gao, B. (2000) IL-1beta attenuates IFN-alphabeta-induced antiviral activity and STAT1 activation in the liver: involvement of proteasome-dependent pathway. J. Immunol. 165, 3959-3965.
28. Alexander, W. S., Starr, R., Metcalf, D., Nicholson, S. E., Farley, A., Elefanty, A. G., Brysha, M., Kile, B. T., Richardson, R., Baca, M., Zhang, J. G., Willson, T. A., Viney, E. M., Sprigg, N. S., Rakar, S., Corbin, J., Mifsud, S., DiRago, L., Cary, D., Nicola, N. A., Hilton, D. J. (1999) Suppressors of cytokine signaling (SOCS): negative regulators of signal transduction. J. Leukuc. Biol. 66, 588-592.
29. Schmitz, J. Weissenbach, M., Haan, S., Heinrich, P. C., Schaper, F. (2000) SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J. Biol. Chem. 275, 12848-12856.
30. Nicholson, S. E., De Souza, D., Fabri, L. J., Corbin, J., Willson, T. A., Zhang, J. G., Silva, A., Asimakis, M., Farley, A., Nash, A. D., Metcalf, D., Hilton, D. J., Nicola, N. A., Baca, M. (2000) Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc. Natl. Acad. Sci. USA 97, 6493-6498.
31. Marine, J. C., McKay, C., Wang, D., Topham, D. J., Parganas, E., Nakajima, H., Pendeville, H., Yasukawa, H., Sasaki, A., Yoshimura, A., Ihle, J. N. (1999) SOCS3 is essential in the regulation of fetal liver erythropoiesis. Cell 98, 617-627.
32. Marine, J. C., Topham, D. J., McKay, C., Wang, D., Parganas, E., Stravopodis, D., Yoshimura, A., Ihle, J. N. (1999) SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality. Cell 98, 609-616.
33. Baumann, H., Prowse, K. R., Marinkovic, S., Won, K. A., Jahreis, G. P. (1989) Stimulation of hepatic acute phase response by cytokines and glucocorticoids. Ann. N. Y. Acad. Sci. 557, 280-295, discussion 295-296.
34. Chomarat, P., Banchereau, J., Davoust, J., Palucka, A. K. (2000) IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat. Immunol. 1, 510-514.
35. Bode, J. G., Nimmesgern, A., Schmitz, J., Schaper, F., Schmitt, M., Frisch, W., Haussinger, D., Heinrich, P. C., Graeve, L. (1999) LPS and TNFalpha induce SOCS3 mRNA and inhibit IL-6-induced activation of STAT3 in macrophages. FEBS Lett. 463, 365-370.
36. Shen, X., Tian, Z., Holtzman, M. J., Gao, B. (2000) Cross-talk between interleukin lbeta (IL-1beta) and IL-6 signalling pathways: IL-1beta selectively inhibits IL-6-activated signal transducer and activator of transcription factor 1 (STAT1) by a proteasome-dependent mechanism. Biochem. J. 352, 913-919.
37. Castro, A., Sengupta, T. K., Ruiz, D. C., Yang, E., Ivashkiv, L. B. (1999) IL-4 selectively inhibits IL-2-triggered Stat5 activation, but not proliferation, in human T cells. J. Immunol. 162, 1261-1269.
38. Sengupta, T. K., Chen, A., Zhong, Z., Darnell Jr., J. E., Ivashkiv, L. B. (1995) Activation of monocyte effector genes and STAT family transcription factors by inflammatory synovial fluid is independent of interferon gamma. J. Exp. Med. 181, 1015-1025.
39. Whitmarsh, A. J., Yang, S. H., Su, M. S., Sharrocks, A. D., Davis, R. J. (1997) Role of p38 and JNK mitogen-activated protein kinases in the activation of ternary complex factors. Mol. Cell. Biol. 17, 2360-2371.
40. Karin, M. (1998) Mitogen-activated protein kinase cascades as regulators of stress responses. Ann. N. Y. Acad. Sci. 851, 139-146.
41. Lasa, M., Mahtani, K. R., Finch, A., Brewer, G., Saklatvala, J., Clark, A. R. (2000) Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell. Biol. 20, 4265-4274.
42. Brook, M., Sully, G., Clark, A. R., Saklatvala, J. (2000) Regulation of tumour necrosis factor alpha mRNA stability by the mitogen-activated protein kinase p38 signalling cascade. FEBS Lett. 483, 57-61.
43. Cohen, P. S., Nakshatri, H., Dennis, J., Caragine, T., Bianchi, M., Cerami, A., Tracey, K. J. (1996) CNI-1493 inhibits monocyte/macrophage tumor necrosis factor by suppression of translation efficiency. Proc. Natl. Acad. Sci. USA 93, 3967-3971.
44. Kontoyiannis, D., Pasparakis, M., Pizarro, T. T., Cominelli, F., Kollias, G. (1999) Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 10, 387-398.
45. Prichett, W., Hand, A., Sheilds, J., Dunnington, D. (1995) Mechanism of action of bicyclic imidazoles defines a translational regulatory pathway for tumor necrosis factor alpha. J. Inflamm. 45, 97-105.
46. Wang, X., Flynn, A., Waskiewicz, A. J., Webb, B. L., Vries, R. G., Baines, I. A., Cooper, J. A., Proud, C. G. (1998) The phosphorylation of eukaryotic initiation factor eIF4E in response to phorbol esters, cell stresses, and cytokines is mediated by distinct MAP kinase pathways. J. Biol. Chem. 273, 9373-9377.
47. Shifrin, V. I., Anderson, P. (1999) Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J. Biol. Chem. 274, 13985-13992.
48. Fuchs, S. Y., Tappin, I., Ronai, Z. (2000) Stability of the ATF2 transcription factor is regulated by phosphorylation and dephosphorylation. J. Biol. Chem. 275, 12560-12564.
49. Bode, J. G., Gatsios, P., Ludwig, S., Rapp, U. R., Haussinger, D., Heinrich, P. C., Graeve, L. (1999) The mitogen-activated protein (MAP) kinase p38 and its upstream activator MAP kinase kinase 6 are involved in the activation of signal transducer and activator of transcription by hyperosmolarity. J. Biol. Chem. 274, 30222-30227.
50. Quelle, F. W., Thierfelder, W., Witthuhn, B. A., Tang, B., Cohen, S., Ihle, J. N. (1995) Phosphorylation and activation of the DNA binding activity of purified Stat1 by the Janus protein-tyrosine kinases and the epidermal growth factor receptor. J. Biol. Chem. 270, 20775-20780.
51. Taga, T., Kishimoto, T. (1997) Gp130 and the interleukin-6 family of cytokines. Annu. Rev. Immunol. 15, 797-819.
52. Delgado, M., Ganea, D. (2000) Inhibition of IFN-gamma-induced janus kinase-1-STAT1 activation in macrophages by vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. J. Immunol. 165, 3051-3057.
53. Seki, E., Tsutsui, H., Nakano, H., Tsuji, N., Hoshino, K., Adachi, O., Adachi, K., Futatsugi, S., Kuida, K., Takeuchi, O., Okamura, H., Fujimoto, J., Akira, S., Nakanishi, K. (2001) Lipopolysaccharide-induced IL-18 secretion from murine Kupffer cells independently of myeloid differentiation factor 88 that is critically involved in induction of production of IL-12 and IL-1beta. J. Immunol. 166, 2651-2657.
54. Taga, T., Hibi, M., Hirata, Y., Yamasaki, K., Yasukawa, K., Matsuda, T., Hirano, T., Kishimoto, T. (1989) Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130. Cell 58, 573-581.
55. Bright, J. J., Kerr, L. D., Sriram, S. (1997) TGF-beta inhibits IL-2-induced tyrosine phosphorylation and activation of Jak-1 and Stat 5 in T lymphocytes. J. Immunol. 159, 175-183.
56. Decker, T., Kovarik, P. (2000) Serine phosphorylation of STATs. Oncogene 19, 2628-2637.
57. Bowie, A. G., O'Neill, L. A. (2000) Vitamin C inhibits NF-kappaB activation by TNF via the activation of p38 mitogen-activated protein kinase. J. Immunol. 165, 7180-7188.
58. Lohoff, M., Ferrick, D., Mittrucker, H. W., Duncan, G. S., Bischof, S., Rollinghoff, M., Mak, T. W. (1997) Interferon regulatory factor-1 is required for a T helper 1 immune response in vivo. Immunity 6, 681-689.
59. Hurst, S. M., Wilkinson, T. S., McLoughlin, R. M., Jones, S., Horiuchi, S., Yamamoto, N., Rose-John, S., Fuller, G. M., Topley, N., Jones, S. A. (2001) IL-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen (luring acute inflammation. Immunity 14, 705-714.
60. Osborn, M. T., Chambers, T. C. (1996) Role of the stress-activated/c-Jun NH2-terminal protein kinase pathway in the cellular response to adriamycin and other chemotherapeutic drugs. J. Biol. Chem. 271, 30950-30955.
61. Wang, T. H., Wang, H. S., Ichijo, H., Giannakakou, P., Foster, J. S., Fojo, T., Wimalasena, J. (1998) Microtubule-interfering agents activate c-Jun N-terminal kinase/stress-activated protein kinase through both Ras and apoptosis signal-regulating kinase pathways. J. Biol. Chem, 273, 4928-4936.
62. Gollob, J. A., Schnipper, C. P., Murphy, E. A., Ritz, J., Frank, D. A. (1999) The functional synergy between IL-12 and IL-2 involves p38 mitogen-activated protein kinase and is associated with the augmentation of STAT serine phosphorylation. J. Immunol. 162, 4472-4481.
63. Kovarik, P., Stoiber, D., Novy, M., Decker, T. (1998) Stat1 combines signals derived from IFN-gamma and LPS receptors during macrophage activation. EMBO J. 17, 3660-3668.