Class II cytokine receptors and their ligands: Key antiviral and inflammatory modulators

Nature Reviews Immunology

Volumn 3, Issue 8, 2003, Pages 667-676

  Renauld, Jean Christophe ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CYTOKINE; CYTOKINE RECEPTOR; GAMMA INTERFERON; INTERFERON; INTERFERON RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; LIGAND;

ANOREXIA; BONE MARROW SUPPRESSION; CHEMICAL STRUCTURE; DEPRESSION; FATIGUE; FEVER; HUMAN; IMMUNOMODULATION; INFLAMMATION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; VIRUS INFECTION; VIRUS RESISTANCE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETICS; IMMUNOLOGY; METABOLISM; PHYLOGENY; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; CYTOKINES; HUMANS; LIGANDS; PHYLOGENY; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, CYTOKINE;

EID: 0141720769     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri1153     Document Type: Review

References (90)

1. Isaacs, A. & Lindenmann, J. Virus interference: 1. The interferon. Proc. R. Soc. Lond. B 147, 258-267 (1957).
2. Goodbourn, S., Didcock, L. & Randall, R. E. Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81, 2341-2364 (2000).
3. Dalton, D. K. et al. Multiple defects of immune cell function in mice with disrupted interferon-γ genes. Science 259, 1739-1742 (1993).
4. Stark, G. R., Kerr, I. M., Williams, B. R., Silverman, R. H. & Schreiber, R. D. How cells respond to interferons. Annu. Rev. Biochem. 67, 227-264 (1998).
5. Kotenko, S. V. & Pestka, S. Jak-Stat signal transduction pathway through the eyes of cytokine class II receptor complexes. Oncogene 19, 2557-2565 (2000).
6. Moore, K. W., de Waal Malefyt, R., Coffman, R. L. & O'Garra, A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683-765 (2001).
7. Walter, M. R. Crystal structures of α-helical cytokine-receptor complexes: we've only scratched the surface. Biotechniques Suppl. S50-S57 (2002).
8. Kotenko, S. V. The family of IL-10-related cytokines and their receptors: related, but to what extent? Cytokine Growth Factor Rev. 13, 223-240 (2002).
9. Dumoutier, L. & Renauld, J. C. Viral and cellular interleukin-10 (IL-10)-related cytokines: from structures to functions. Eur. Cytokine Netw. 13, 5-15 (2002).
10. Fickenscher, H. et al. The interleukin-10 family of cytokines Trends Immunol. 23, 89-96 (2002).
11. Jiang, H., Lin, J. J., Su, Z. Z., Goldstein, N. I. & Fisher, P. B. Subtraction hybridization identifies a novel melanoma differentiation associated gene, mda-7, modulated during human melanoma differentiation, growth and progression. Oncogene 11, 2477-2486 (1995).
12. Knappe, A., Hor, S., Wittmann, S. & Fickenscher, H. Induction of a novel cellular homolog of interleukin-10, AK155, by transformation of T lymphocytes with herpesvirus saimiri. J. Virol. 74, 3881-3887 (2000).
13. Dumoutier, L., Louahed, J. & Renauld, J. C. Cloning and characterization of IL-10-related T cell-derived inducible factor (IL-TIF), a novel cytokine structurally related to IL-10 and inducible by IL-9. J. Immunol. 164, 1814-1819 (2000).
14. Gallagher, G. et al. Cloning, expression and initial characterization of interleukin-19 (IL-19), a novel homologue of human interleukin-10 (IL-10). Genes Immun. 1, 442-450 (2000).
15. Blumberg, H. et al, Interleukin 20: discovery, receptor identification, and role in epidermal function. Cell 104, 9-19 (2001). This study showed that overexpression of interleukin-20 (IL-20) in transgenic mice results in abnormal differentiation and proliferation of keratinocytes - a phenotype reminiscent of psoriatic skin in humans.
16. Sheppard, P. et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nature Immunol. 4, 63-68 (2003). This paper described the cloning of IL-28A, IL-28B, IL-29 and their receptor, and shows that they exert antiviral activity. Similar observations were reported by Kotenko et al. in reference 17.
17. Kotenko, S. V. et al. IFN-λs mediate antiviral protection through a distinct class II cytokine receptor complex. Nature Immunol. 4, 69-77 (2003).
18. Oritani, K. et al. Limitin: An interferon-like cytokine that preferentially influences B-lymphocyte precursors. Nature Med. 6, 659-666 (2000).
19. Chang, C. et al. Crystal structure of interleukin-19 defines a new subfamily of helical cytokines. J. Biol. Chem. 278, 3308-3313 (2003).
20. Nagem, R. A. et al. Crystal structure of recombinant human interleukin-22. Structure (Camb) 10, 1051-1062 (2002).
21. Karpusas, M. et al. The crystal structure of human interferon β at 2. 2-A resolution. Proc. Natl Acad. Sci. USA 94, 11813-11818 (1997).
22. Zdanov, A. et al. Crystal structure of interleukin-10 reveals the functional dimer with an unexpected topological similanty to interferon γ. Structure 3, 591-601 (1995).
23. Walter, M. R. & Nagabhushan, T. L. Crystal structure of interleukin 10 reveals an interferon γ-like fold. Biochemistry 34, 12118-12125 (1995).
24. Bazan, J. F. Shared architecture of hormone binding domains in type I and II interferon receptors. Cell 61, 753-754 (1990).
25. Josephson, K., Logsdon, N. J. & Walter, M. R. Crystal structure of the IL-10/IL-10R1 complex reveals a shared receptor binding site. Immunity 15, 35-46 (2001). This study described the crystal structure of IL-10 bound to a soluble form of IL-10 receptor 1 (sIL-10R1), showing that several residues in the IL-10-sIL-10R1 interface are conserved in all IL-10 homologues and their receptors.
26. Kotenko, S. V. et al. Identification and functional characterization of a second chain of the interleukin-10 receptor complex. EMBO J. 16, 5894-5903 (1997).
27. Kotenko, S. V. et al Identification of the functional interleukin-22 (IL-22) receptor complex: the IL-10R2 chain (IL-10Rβ) is a common chain of both the IL-10 and IL-22 (IL-10-related T cell-derived inducible factor, IL-TIF) receptor complexes. J. Biol. Chem. 276, 2725-2732 (2001).
28. Dumoutier, L., Van Roost, E., Colau, D. & Renauld, J. C. Human interleukin-10-related T cell-derived inducible factor: molecular cloning and functional characterization as an hepatocyte-stimulating factor Proc. Natl Acad. Sci. USA 97, 10144-10149 (2000). This study reported the cloning of human IL-22 and showed its activity as an inducer of the acute-phase response through the IL-10Rβ chain.
29. Xie, M. H. et al. Interleukin (IL)-22, a novel human cytokine that signals through the interferon receptor-related proteins CRF2-4 and IL-22R. J. Biol. Chem. 275, 31335-31339 (2000).
30. Lewerenz, M., Mogensen, K. E. & Uze, G. Shared receptor components but distinct complexes for α and β interferons. J. Mol. Biol. 282, 585-599 (1998).
31. Riewald, M. & Ruf, W. Orchestration of coagulation protease signaling by tissue factor. Trends Cardiovasc. Med. 12, 149-154 (2002).
32. Dumoutier, L., Lejeune, D., Colau, D. & Renauld, J. C. Cloning and characterization of IL-22 binding protein, a natural antagonist of IL-10-related T cell-derived inducible factor/IL-22. J. Immunol. 166, 7090-7095 (2001).
33. Kotenko, S. V. et al. Identification, cloning, and characterization of a novel soluble receptor that binds IL-22 and neutralizes its activity. J. Immunol. 166, 7096-7103 (2001).
34. Xu, W. et al. A soluble class II cytokine receptor, IL-22RA2, is a naturally occurring IL-22 antagonist. Proc. Natl Acad. Sci. USA 98, 9511-9516 (2001).
35. Gruenberg, B. H. et al. A novel, soluble homologue of the human IL-10 receptor with preferential expression in placenta. Genes Immun. 2, 329-334 (2001).
36. Mantovani, A., Locati, M., Vecchi, A., Sozzani, S. & Allavena, P. Decoy receptors: a strategy to regulate inflammatory cytokines and chemokines. Trends Immunol. 22, 328-336 (2001).
37. Lejeune, D. et al. Interleukin-22 (IL-22) activates the JAK/STAT ERK, JNK, and p38 MAP kinase pathways in a rat hepatoma cell line. Pathways that are shared with and distinct from IL-10. J. Biol. Chem. 277, 33676-33682 (2002).
38. Decker, T., Stockinger, S., Karaghiosoff, M., Muller, M. & Kovarik, P. IFNs and STATs in innate immunity to microorganisms. J. Clin. Invest. 109, 1271-1277 (2002).
39. Muller, U. et al. Functional role of type I and type II interferons in antiviral defense. Science 264, 1918-1921 (1994).
40. Dumoutier, L., Lejeune, D., Hor, S., Fickenscher, H. & Renauld, J. C. Cloning of a new type II cytokine receptor activating signal transducer and activator of transcription (STAT)1, STAT2 and STAT3. Biochem. J. 370, 391-396 (2003).
41. Schijns, V. E., Wierda, C. M., van Hoeij, M. & Horzinek, M. C. Exacerbated viral hepatitis in IFN-γ receptor-deficient mice is not suppressed by IL-12 J. Immunol. 157, 815-821 (1996).
42. Jouanguy, E. et al. IL-12 and IFN-γ in host defense against mycobacteria and salmonella in mice and men. Curr. Opin. Immunol. 11, 346-351 (1999).
43. Katze, M. G., He, Y. & Gale, M., Jr. Viruses and interferon: a fight for supremacy. Nature Rev. Immunol. 2, 675-687 (2002).
44. Alcami, A. & Smith, G. L. Cytokine receptors encoded by poxviruses: a lesson in cytokine biology. Immunol. Today 16, 474-478 (1995).
45. Smith, G. L., Symons, J. A. & Alcami, A. Immune modulation by proteins secreted from cells infected by vaccinia virus. Arch. Virol. 15, 111-129 (1999).
46. Symons, J. A., Alcami, A. & Smith, G. L. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81, 551-560 (1995).
47. Colamonici, O. R., Domanski, P., Sweitzer, S. M., Larner, A. & Buller, R. M. Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon α transmembrane signaling. J. Biol. Chem. 270, 15974-15978 (1995).
48. Moore, K. W. et al. Homology of cytokine synthesis inhibitory factor (IL-10) to the Epstein-Barr virus gene BCRFI. Science 248, 1230-1234 (1990).
49. Hsu, D. H., et al. Expression of interleukin-10 activity by Epstein-Barr virus protein BCRF1. Science 250, 830-832 (1990). This study showed that the Epstein-Barr virus BCRF1 protein mimics the activity of IL-10, indicating that BCRF1 might have a role in the interaction of the virus with the host's immune system.
50. Liu, Y. et al. The EBV IL-10 homologue is a selective agonist with impaired binding to the IL-10 receptor. J. Immunol. 158, 604-613 (1997).
51. Rode, H. J. et al. The genome of equine herpesvirus type 2 harbors an interleukin 10 (IL10)-like gene. Virus Genes 7, 111-116 (1993).
52. Fleming, S. B., McCaughan, C. A., Andrews, A. E., Nash, A. D. & Mercer, A. A. A homolog of interleukin-10 is encoded by the poxvirus orf virus J. Virol. 71, 4857-4861 (1997).
53. Kotenko, S. V. Saccani, S., Izotova, L. S., Mirochnitchenko, O. V. & Pestka, S. Human cytomegalovirus harbors its own unique IL-10 homolog (cmvIL-10). Proc. Natl Acad. Sci. USA 97, 1695-1700 (2000).
54. Lockridge, K. M. et al. Primate cytomegaloviruses encode and express an IL-10-like protein. Virology 268, 272-280 (2000).
55. Spencer, J. V. et al. Potent immunosuppressive activities of cytomegalovirus-encoded interleukin-10. J. Virol. 76, 1285-1292 (2002).
56. Lee, H. J., Essani, K. & Smith, G. L. The genome sequence of Yaba-like disease virus, a yatapoxvirus. Virology 281, 170-192 (2001).
57. Burdin, N., Peronne, C., Banchereau, J. & Rousset, F. Epstein-Barr virus transformation induces B lymphocytes to produce human interleukin 10. J. Exp. Med 177, 295-304 (1993).
58. Howard, M., Muchamuel, T., Andrade, S. & Menon, S. Interleukin 10 protects mice from lethal endotoxemia. J. Exp. Med. 177, 1205-1208 (1993).
59. Gerard, C. et al. Interleukin 10 reduces the release of tumor necrosis factor and prevents lethality in experimental endotoxemia. J. Exp. Med. 177, 547-550 (1993).
60. Ishida, H., Hastings, R., Thompson-Seipes, L. & Howard, M. Modified immunological status of anti-IL-10 treated mice. Cell. Immunol. 148, 371-384 (1993).
61. Heremans, H., Van Damme, J., Dillen, C., Dijkmans, R. & Billiau, A. Interferon-γ, a mediator of lethal lipopolysaccharide-induced Shwartzman-like shock reactions in mice. J. Exp. Med. 171, 1853-1869 (1990).
62. -/- mice: an overview. J. Leukoc. Biol. 61, 389-396 (1997).
63. Hall, G. L., Compston, A. & Scolding, N. J. β-interferon and multiple sclerosis. Trends Neurosci. 20, 63-67 (1997).
64. H2 paradigm. Immunol. Today 18, 263-266 (1997).
65. Renauld, J. C. New insights into the role of cytokines in asthma. J. Clin. Pathol. 54, 577-589 (2001).
66. H1 clones. J. Exp. Med. 170, 2081-2095 (1989).
67. H1 cells. J. Immunol. 146, 3444-3451 (1991).
68. Maloy, K. J. & Powrie, F. Regulatory T cells in the control of immune pathology. Nature Immunol. 2, 816-822 (2001).
69. R cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med 197, 111-119 (2003).
70. Wolk, K., Kunz, S., Asadullah, K. & Sabat, R. Cutting edge: immune cells as sources and targets of the IL-10 family members? J. Immunol. 168, 5397-5402 (2002).
71. H2 cells. J. Immunol. 166, 5859-5863 (2001).
72. Liao, Y. C. et al. IL-19 induces production of IL-6 and TNF-α and results in cell apoptosis through TNF-α. J. Immunol. 169, 4288-4297 (2002).
73. Caudell, E. G. et al. The protein product of the tumor suppressor gene, melanoma differentiation-associated gene 7, exhibits immunostimulatory activity and is designated IL-24. J. Immunol. 168, 6041-6046 (2002).
74. Dinarello, C. A. Interleukin-1 and the pathogenesis of the acute-phase response. N. Engl. J. Med. 311, 1413-1418 (1984).
75. Heinrich, P. C., Castell, J. V. & Andus, T. Interleukin-6 and the acute phase response. Biochem. J. 265, 621-636 (1990).
76. Aggarwal, S. Xie, M. H., Maruoka, M., Foster, J. & Gurney, A. L. Acinar cells of the pancreas are a target of interleukin-22. J. Interferon Cytokine Res. 21, 1047-1053 (2001).
77. Wang, M., Tan, Z., Zhang, R., Kotenko, S. V. & Liang, P. Interleukin 24 (MDA-7/MOB-5) signals through two heterodimeric receptors, IL-22R1/IL-20R2 and IL-20R1/IL-20R2. J. Biol. Chem. 277, 7341-7347 (2002).
78. Parrish-Novak, J. et al. Interleukins 19, 20, and 24 signal through two distinct receptor complexes. Differences in receptor-ligand interactions mediate unique biological functions. J. Biol. Chem. 277, 47517-47523 (2002).
79. Dumoutier, L., Leemans, C., Lejeune, D., Kotenko, S. V. & Renauld, J. C. Cutting edge: STAT activation by IL-19, IL-20 and mda-7 through IL-20 receptor complexes of two types. J. Immunol. 167, 3545-3549 (2001). This study showed that IL-19, IL-20 and IL-24, also known as melanocyte differentiation antigen 7 (MDA7), share similar receptor complexes, indicating that they should have overlapping activities.
80. Kirkwood, J. Cancer immunotherapy: the interferon-α experience. Semin. Oncol. 29, 18-26 (2002).
81. Ellerhorst, J. A. et al. Loss of MDA-7 expression with progression of melanoma. J. Clin. Oncol. 20, 1069-1074 (2002).
82. Ekmekcioglu, S. et al. Downregulated melanoma differentiation associated gene (mda-7) expression in human melanomas. Int. J. Cancer 94, 54-59 (2001).
83. Lebedeva, I. V. et al. The cancer growth suppressing gene mda-7 induces apoptosis selectively in human melanoma cells. Oncogene 21, 708-718 (2002).
84. Sauane, M. et al. MDA-7/IL-24: novel cancer growth suppressing and apoptosis inducing cytokine. Cytokine Growth Factor Rev. 14, 35-51 (2003).
85. Su, Z. Z. et al. The cancer growth suppressor gene mda-7 selectively induces apoptosis in human breast cancer cells and inhibits tumor growth in nude mice. Proc. Natl Acad. Sci. USA 95, 14400-14405 (1998).
86. Zhan, Q. et al. The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth. Mol. Cell. Biol. 14, 2361-2371 (1994).
87. Sarkar, D. et al. mda-7 (IL-24) mediates selective apoptosis in human melanoma cells by inducing the coordinated overexpression of the GADD family of genes by means of p38 MAPK. Proc. Natl Acad. Sci. USA 99, 10054-10059 (2002).
88. Su, Z. Z. et al. Melanoma differentiation associated gene-7, mda-7/IL-24, selectively induces growth suppression, apoptosis and radiosensitization in malignant gliomas in a p53-independent manner. Oncogene 22, 1164-1180 (2003).
89. Pataer, A. et al. Adenoviral transfer of the melanoma differentiation-associated gene 7 (mda7) induces apoptosis of lung cancer cells via upregulation of the double-stranded RNA-dependent protein kinase (PKR). Cancer Res. 62, 2239-2243 (2002).
90. Huang, E. Y. et al. Genomic structure, chromosomal localization and expression profile of a novel melanoma differentiation associated (mda-7) gene with cancer specific growth suppressing and apoptosis inducing properties. Oncogene 20, 7051-7063 (2001).