SOCS1 restricts dendritic cells' ability to break self tolerance and induce antitumor immunity by regulating IL-12 production and signaling

Journal of Clinical Investigation

Volumn 116, Issue 1, 2006, Pages 90-100

  Evel Kabler, Kevin ^a,b   Song, Xiao Tong ^a,b   Aldrich, Melissa ^a,b   Huang, Xue F ^a,b   Chen, Si Yi ^a,b  

^a CENTER FOR CELL AND GENE THERAPY   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; CYTOKINE; DENDRITIC CELL VACCINE; INTERLEUKIN 12; SMALL INTERFERING RNA; SUPPRESSOR OF CYTOKINE SIGNALING 1; TOLL LIKE RECEPTOR; TYROSINASE RELATED PROTEIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; AUTOIMMUNITY; CANCER IMMUNIZATION; CELL ACTIVITY; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEEDBACK SYSTEM; FEMALE; GENE SILENCING; HOST; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; IMMUNOSTIMULATION; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR IMMUNITY;

ANIMALS; CARRIER PROTEINS; CELL LINE, TUMOR; DENDRITIC CELLS; FEMALE; GENE EXPRESSION REGULATION; INTERLEUKIN-12; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REPRESSOR PROTEINS; SELF TOLERANCE; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 31044453678     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI26169     Document Type: Article

References (51)

1. Akira, S., and Takeda, k. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4:499-511.
2. Beutler, B., and Rietschel, E.T. 2003. Innate immune sensing and its roots: the story of endotoxin. Nat. Rev. Immunol. 3:169-176.
3. Janeway, C.A., Jr., and Medzhitov, R. 2002. Innate immune recognition. Annu. Rev. Immunol. 20:197-216.
4. Banchereau, J., and Steinman, R.M. 1998. Dendritic cells and the control of immunity. Nature. 392:245-252.
5. Steinman, R.M., Hawiger, D., and Nussenzweig, M.C. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21:685-711.
6. Gilboa, E. 2004. The promise of cancer vaccines. Nat. Rev. Cancer. 4:401-411.
7. Dustin, M.L., and Cooper, J.A. 2000. The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling. Nat. Immunol. 1:23-29.
8. kaech, S.M., and Ahmed, R. 2001. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol. 2:415-422.
9. van Stipdonk, M.J., Lemmens, E.E., and Schoenberger, S.P. 2001. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2:423-429.
10. Lanzavecchia, A., and Sallusto, F. 2001. Antigen decoding by T lymphocytes: from synapses to fate determination. Nat. Immunol. 2:487-492.
11. Gett, A.V., Sallusto, F., Lanzavecchia, A., and Geginat, J. 2003. T cell fitness determined by signal strength. Nat. Immunol. 4:355-360.
12. Curtsinger, J.M., Lins, D.C., and Mescher, M.F. 2003. Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J. Exp. Med. 197:1141-1151.
13. Valenzuela, J., Schmidt, C., and Mescher, M. 2002. The roles of IL-12 in providing a third signal for clonal expansion of naive CD8 T cells. J. Immunol. 169:6842-6849.
14. Nakagawa, R., et al. 2002. SOCS-1 participates in negative regulation of LPS responses. Immunity. 17:677-687.
15. kinjyo, I., et al. 2002. SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity. 17:583-591.
16. Hanada, T., et al. 2003. Suppressor of cytokine signaling-1 is essential for suppressing dendritic cell activation and systemic autoimmunity. Immunity. 19:437-450.
17. kubo, M., Hanada, T., and Yoshimura, A. 2003. Suppressors of cytokine signaling and immunity. Nat. Immunol. 4:1169-1176.
18. Marine, J.C., et al. 1999. SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality. Cell. 98:609-616.
19. Alexander, W.S., et al. 1999. SOCS1 is a critical inhibitor of interferon gamma signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell. 98:597-608.
20. Shen, L., Evel-kabler, k., Strube, R., and Chen, S.Y. 2004. Silencing of SOCS1 enhances antigen presentation by dendritic cells and antigen-specific antitumor immunity. Nat. Biotechnol. 22:1546-1553.
21. Hanada, T., et al. 2005. Induction of hyper Th1 cell-type immune responses by dendritic cells lacking the suppressor of cytokine signaling-1 gene. J. Immunol. 174:4325-4332.
22. Simpson, A.J., Caballero, O.L., Jungbluth, A., Chen, Y.T., and Old, L.J. 2005. Cancer/testis antigens, gametogenesis and cancer. Nat. Rev. Cancer. 5:615-625.
23. Timmerman, J.M., and Levy, R. 1999. Dendritic cell vaccines for cancer immunotherapy. Annu. Rev. Med. 50:507-529.
24. Fong, L., and Engleman, E.G. 2000. Dendritic cells in cancer immunotherapy. Annu. Rev. Immunol. 18:245-273.
25. Rosenberg, S.A., Yang, J.C., and Restifo, N.P. 2004. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 10:909-915.
26. Sakaguchi, S. 2004. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22:531-562.
27. Yang, L., and Carbone, D.P. 2004. Tumor-host immune interactions and dendritic cell dysfunction. Adv. Cancer Res. 92:13-27.
28. van Elsas, A., et al. 2001. Elucidating the autoimmune and antitumor effector mechanisms of a treatment based on cytotoxic T lymphocyte antigen-4 blockade in combination with a B16 melanoma vaccine: comparison of prophylaxis and therapy. J. Exp. Med. 194:481-489.
29. Yang, Y., Huang, C.T., Huang, X., and Pardoll, D.M. 2004. Persistent Toll-like receptor signals are required for reversal of regulatory T cell-mediated CD8 tolerance. Nat. Immunol. 5:508-515.
30. Gautier, G., et al. 2005. A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J. Exp. Med. 201:1435-1446.
31. Langenkamp, A., Messi, M., Lanzavecchia, A., and Sallusto, F. 2000. Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat. Immunol. 1:311-316.
32. Gingras, S., Parganas, E., de Pauw, A., Ihle, J.N., and Murray, P.J. 2004. Re-examination of the role of suppressor of cytokine signaling 1 (SOCS1) in the regulation of Toll-like receptor signaling. J. Biol. Chem. 279:54702-54707.
33. Chong, M.M., Metcalf, D., Jamieson, E., Alexander, W.S., and kay, T.W. 2005. Suppressor of cytokine signaling-1 in T cells and macrophages is critical for preventing lethal inflammation. Blood. 106:1668-1675.
34. Catlett, I.M., and Hedrick, S.M. 2005. Suppressor of cytokine signaling 1 is required for the differentiation of CD4+ T cells. Nat. Immunol. 6:715-721.
35. D'Andrea, A., Ma, X., Aste-Amezaga, M., Paganin, C., and Trinchieri, G. 1995. Stimulatory and inhibitory effects of interleukin (IL)-4 and IL-13 on the production of cytokines by human peripheral blood mononuclear cells: priming for IL-12 and tumor necrosis factor alpha production. J. Exp. Med. 181:537-546.
36. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3:133-146.
37. Barnes, B.J., et al. 2004. Global and distinct targets of IRF-5 and IRF-7 during innate response to viral infection. J. Biol. Chem. 279:45194-45207.
38. Ohteki, T., et al. 1999. Interleukin 12-dependent interferon gamma production by CD8alpha+ lymphoid dendritic cells. J. Exp. Med. 189:1981-1986.
39. Garg, S., et al. 2003. Genetic tagging shows increased frequency and longevity of antigen-presenting, skin-derived dendritic cells in vivo. Nat. Immunol. 4:907-912.
40. Machen, J., et al. 2004. Antisense oligonucleotides down-regulating costimulation confer diabetes-preventive properties to nonobese diabetic mouse dendritic cells. J. Immunol. 173:4331-4341.
41. van Elsas, A., Hurwitz, A.A., and Allison, J.P. 1999. Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J. Exp. Med. 190:355-366.
42. Waldner, H., Collins, M., and kuchroo, V.k. 2004. Activation of antigen-presenting cells by microbial products breaks self tolerance and induces autoimmune disease. J. Clin. Invest. 113:990-997. doi:10.1172/JCI200419388.
43. Duan, L., Reddi, A.L., Ghosh, A., Dimri, M., and Band, H. 2004. The Cbl family and other ubiquitin ligases: destructive forces in control of antigen receptor signaling. Immunity. 21:7-17.
44. Egen, J.G., kuhns, M.S., and Allison, J.P. 2002. CTLA-4: new insights into its biological function and use in tumor immunotherapy. Nat. Immunol. 3:611-618.
45. Hodi, F.S., et al. 2003. Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc. Natl. Acad. Sci. U. S. A. 100:4712-4717.
46. Phan, G.Q., et al. 2003. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc. Natl. Acad. Sci. U. S. A. 100:8372-8377.
47. Eyles, J.L., Metcalf, D., Grusby, M.J., Hilton, D.J., and Starr, R. 2002. Negative regulation of interleukin-12 signaling by suppressor of cytokine signaling-1. J. Biol. Chem. 277:43735-43740.
48. Banchereau, J., Pascual, V., and Palucka, A.k. 2004. Autoimmunity through cytokine-induced dendritic cell activation. Immunity. 20:539-550.
49. Grohmann, U., et al. 1998. IL-12 acts directly on DC to promote nuclear localization of NF-kappaB and primes DC for IL-12 production. Immunity. 9:315-323.
50. You, Z., et al. 2000. Induction of vigorous helper and cytotoxic T cell as well as B cell responses by DCs expressing a modified antigen targeting receptor-mediated internalization pathway. J. Immunol. 165:4581-4592.
51. Hauser, H., Shen, L., Gu, Q.L., krueger, S., and Chen, S.-Y. 2004. Secretory heat-shock protein as a dendritic cell-targeting molecule: a new strategy to enhance the potency of genetic vaccines. Gene Ther. 11:924-932.