Regulation of antitumor immune responses by the IL-12 family cytokines, IL-12, IL-23, and IL-27

Clinical and Developmental Immunology

Volumn 2010, Issue , 2010, Pages

  Yoshimoto, Takayuki ^a   Xu, Mingli ^a   Mizoguchi, Izuru ^a   Morishima, Noriko ^a   Chiba, Yukino ^a   Mizuguchi, Junichiro ^a  

^a TOKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 27; INTERLEUKIN 35; STAT3 PROTEIN; STAT4 PROTEIN;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; CANCER IMMUNOTHERAPY; CARCINOGENESIS; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHRONIC INFLAMMATION; CLINICAL TRIAL; CYTOKINE PRODUCTION; CYTOTOXIC LYMPHOCYTE; DENDRITIC CELL; DRUG MEGADOSE; GASTROINTESTINAL TOXICITY; GENE OVEREXPRESSION; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; LEUKEMIA; LEUKOPENIA; LYMPHOCYTE DIFFERENTIATION; LYMPHOMA; MACROPHAGE; MEMORY T LYMPHOCYTE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; REVIEW; SPLENOMEGALY; TH1 CELL; TUMOR IMMUNITY;

ANTIGEN-PRESENTING CELLS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-12; INTERLEUKIN-17; INTERLEUKIN-23; NEOPLASMS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 77957866376     PISSN: 17402522     EISSN: 17402530     Source Type: Journal    
DOI: 10.1155/2010/832454     Document Type: Review

References (73)

1. Dranoff G., Jaffee E., Lazenby A., Golumbek P., Levitsky H., Brose K., Jackson V., Hamada H., Pardoll D., Mulligan R. C., Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity Proceedings of the National Academy of Sciences of the United States of America 1993 90 8 3539 3543
2. Eager R., Nemunaitis J., GM-CSF gene-transduced tumor vaccines Molecular Therapy 2005 12 1 18 27
3. Rosenberg S. A., Lotze M. T., Muul L. M., A progress report on the treatment of 157 patients with advanced cancer using lymphokine-activated killer cells and interleukin-2 or high-dose interleukin-2 alone New England Journal of Medicine 1987 316 15 889 897
4. Fisher R. I., Coltman C. A. Jr., Doroshow J. H., Rayner A. A., Hawkins M. J., Mier J. W., Wiernik P., McMannis J. D., Weiss G. R., Margolin K. A., Gemlo B. T., Hoth D. F., Parkinson D. R., Paietta E., Metastatic renal cancer treated with interleukin-2 and lymphokine-activated killer cells. A phase II clinical trial Annals of Internal Medicine 1988 108 4 518 523
5. Fyfe G., Fisher R. I., Rosenberg S. A., Sznol M., Parkinson D. R., Louie A. C., Results of treatment of 255 patients with metastatic renal cell carcinoma who received high-dose recombinant interleukin-2 therapy Journal of Clinical Oncology 1995 13 3 688 696
6. Trinchieri G., Pflanz S., Kastelein R. A., The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses Immunity 2003 19 5 641 644
7. Brunda M. J., Luistro L., Warrier R. R., Wright R. B., Hubbard B. R., Murphy M., Wolf S. F., Gately M. K., Antitumor and antimetastatic activity of interleukin 12 against murine tumors Journal of Experimental Medicine 1993 178 4 1223 1230
8. Colombo M. P., Trinchieri G., Interleukin-12 in anti-tumor immunity and immunotherapy Cytokine and Growth Factor Reviews 2002 13 2 155 168
9. Balkwill F., Mantovani A., Inflammation and cancer: back to Virchow? Lancet 2001 357 9255 539 545
10. Langowski J. L., Zhang X., Wu L., Mattson J. D., Chen T., Smith K., Basham B., McClanahan T., Kastelein R. A., Oft M., IL-23 promotes tumour incidence and growth Nature 2006 442 7101 461 465
11. Langowski J. L., Kastelein R. A., Oft M., Swords into plowshares: IL-23 repurposes tumor immune surveillance Trends in Immunology 2007 28 5 207 212
12. Kortylewski M., Xin H., Kujawski M., Lee H., Liu Y., Harris T., Drake C., Pardoll D., Yu H., Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment Cancer Cell 2009 15 2 114 123
13. Yu H., Jove R., The stats of cancernew molecular targets come of age Nature Reviews Cancer 2004 4 2 97 105
14. Kobayashi M., Fitz L., Ryan M., Hewick R. M., Clark S. C., Chan S., Loudon R., Sherman F., Perussia B., Trinchieri G., Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes Journal of Experimental Medicine 1989 170 3 827 845
15. Stern A. S., Podlaski F. J., Hulmes J. D., Pan Y.-C. E., Quinn P. M., Wolitzky A. G., Familletti P. C., Stremlo D. L., Truitt T., Chizzonite R., Gately M. K., Purification to homogeneity and partial characterization of cytotoxic lymphocyte maturation factor from human B-lymphoblastoid cells Proceedings of the National Academy of Sciences of the United States of America 1990 87 17 6808 6812
16. Wolf S. F., Temple P. A., Kobayashi M., Young D., Dicig M., Lowe L., Dzialo R., Fitz L., Ferenz C., Hewick R. M., Kelleher K., Herrmann S. H., Clark S. C., Azzoni L., Chan S. H., Trinchieri G., Perussia B., Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells Journal of Immunology 1991 146 9 3074 3081
17. Trinchieri G., Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity Annual Review of Immunology 1995 13 251 276
18. Gately M. K., Renzetti L. M., Magram J., Stern A. S., Adorini L., Gubler U., Presky D. H., The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses Annual Review of Immunology 1998 16 495 521
19. Wigginton J. M., Gruys E., Geiselhart L., Subleski J., Komschlies K. L., Park J.-W., Wiltrout T. A., Nagashima K., Back T. C., Wiltrout R. H., IFN- and Fas/FasL are required for the antitumor and antiangiogenic effects of IL-12/pulse IL-2 therapy Journal of Clinical Investigation 2001 108 1 51 62
20. Car B. D., Eng V. M., Schnyder B., LeHir M., Shakhov A. N., Woerly G., Huang S., Aguet M., Anderson T. D., Ryffel B., Role of interferon- in interleukin 12-induced pathology in mice American Journal of Pathology 1995 147 6 1693 1707
21. Ryffel B., Interleukin-12: role of interferon- in IL-12 adverse effects Clinical Immunology and Immunopathology 1997 83 1 18 20
22. Car B. D., Eng V. M., Lipman J. M., Anderson T. D., The toxicology of interleukin-12: a review Toxicologic Pathology 1999 27 1 58 63
23. Marshall E., Cancer trial of interleukin-12 halted Science 1995 268 1555
24. Haicheur N., Escudier B., Dorval T., Negrier S., De Mulder P. H. M., Dupuy J. M., Novick D., Guilloth T., Wolf S., Pouillart P., Fridman W. H., Tartour E., Cytokines and soluble cytokine receptor induction after IL-12 administration in cancer patients Clinical and Experimental Immunology 2000 119 1 28 37
25. Portielje J. E. A., Lamers C. H. J., Kruit W. H. J., Sparreboom A., Bolhuis R. L. H., Stoter G., Huber C., Gratama J. W., Repeated administrations of interleukin (IL)-12 are associated with persistently elevated plasma levels of IL-10 and declining IFN-, tumor necrosis factor-, IL-6, and IL-8 responses Clinical Cancer Research 2003 9 1 76 83
26. Beyer M., Schultze J. L., Regulatory T cells in cancer Blood 2006 108 3 804 811
27. Pflanz S., Timans J. C., Cheung J., Rosales R., Kanzler H., Gilbert J., Hibbert L., Churakova T., Travis M., Vaisberg E., Blumenschein W. M., Mattson J. D., Wagner J. L., To W., Zurawski S., McClanahan T. K., Gorman D. M., Bazan J. F., De Waal Malefyt R., Rennick D., Kastelein R. A., IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4 + T cells Immunity 2002 16 6 779 790
28. Takeda A., Hamano S., Yamanaka A., Hanada T., Ishibashi T., Mak T. W., Yoshimura A., Yoshida H., Cutting edge: role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 during initial Th1 commitment Journal of Immunology 2003 170 10 4886 4890
29. Kamiya S., Owaki T., Morishima N., Fukai F., Mizuguchi J., Yoshimoto T., An indispensable role for STAT1 in IL-27-induced T-bet expression but not proliferation of naive CD4 + T cells Journal of Immunology 2004 173 6 3871 3877
30. Owaki T., Asakawa M., Morishima N., Hata K., Fukai F., Matsui M., Mizuguchi J., Yoshimoto T., A role for IL-27 in early regulation of Th1 differentiation Journal of Immunology 2005 175 4 2191 2200
31. 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. P., Saris C. J. M., Scott P., Hunter C. A., The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity Journal of Immunology 2004 173 9 5626 5634
32. Yoshimoto T., Yoshimoto T., Yasuda K., Mizuguchi J., Nakanishi K., IL-27 suppresses Th2 cell development and Th2 cytokines production from polarized Th2 cells: a novel therapeutic way for Th2-mediated allergic inflammation Journal of Immunology 2007 179 7 4415 4423
33. Batten M., Li J., Yi S., Kljavin N. M., Danilenko D. M., Lucas S., Lee J., de Sauvage F. J., Ghilardi N., Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells Nature Immunology 2006 7 9 929 936
34. Stumhofer J. S., Laurence A., Wilson E. H., Huang E., Tato C. M., Johnson L. M., Villarino A. V., Huang Q., Yoshimura A., Sehy D., Saris C. J. M., O'Shea J. J., Hennighausen L., Ernst M., Hunter C. A., Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system Nature Immunology 2006 7 9 937 945
35. Hamano S., Himeno K., Miyazaki Y., Ishii K., Yamanaka A., Takeda A., Zhang M., Hisaeda H., Mak T. W., Yoshimura A., Yoshida H., WSX-1 is required for resistance to Trypanosoma cruzi infection by regulation of proinflammatory cytokine production Immunity 2003 19 5 657 667
36. Villarino A., Hibbert L., Lieberman L., Wilson E., Mak T., Yoshida H., Kastelein R. A., Saris C., Hunter C. A., The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection Immunity 2003 19 5 645 655
37. Stumhofer J. S., Silver J. S., Laurence A., Porrett P. M., Harris T. H., Turka L. A., Ernst M., Saris C. J. M., O'Shea J. J., Hunter C. A., Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10 Nature Immunology 2007 8 12 1363 1371
38. Fitzgerald D. C., Zhang G.-X., El-Behi M., Fonseca-Kelly Z., Li H., Yu S., Saris C. J., Gran B., Ciric B., Rostami A., Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells Nature Immunology 2007 8 12 1372 1379
39. Batten M., Kljavin N. M., Li J., Walter M. J., De Sauvage F. J., Ghilardi N., Cutting edge: IL-27 is a potent inducer of IL-10 but not FoxP3 in murine T cells Journal of Immunology 2008 180 5 2752 2756
40. Awasthi A., Carrier Y., Peron J. P. S., Bettelli E., Kamanaka M., Flavell R. A., Kuchroo V. K., Oukka M., Weiner H. L., A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells Nature Immunology 2007 8 12 1380 1389
41. Hisada M., Kamiya S., Fujita K., Belladonna M. L., Aoki T., Koyanagi Y., Mizuguchi J., Yoshimoto T., Potent antitumor activity of interleukin-27 Cancer Research 2004 64 3 1152 1156
42. Salcedo R., Stauffer J. K., Lincoln E., Back T. C., Hixon J. A., Hahn C., Shafer-Weaver K., Malyguine A., Kastelein R., Wigginton J. M., IL-27 mediates complete regression of orthotopic primary and metastatic murine neuroblastoma tumors: role for CD8+ T cells Journal of Immunology 2004 173 12 7170 7182
43. Chiyo M., Shimozato O., Iizasa T., Fujisawa T., Tagawa M., Antitumor effects produced by transduction of dendritic cells-derived heterodimeric cytokine genes in murine colon carcinoma cells Anticancer Research 2004 24 6 3763 3767
44. Chiyo M., Shimozato O., Yu L., Kawamura K., Iizasa T., Fujisawa T., Tagawa M., Expression of IL-27 in murine carcinoma cells produces antitumor effects and induces protective immunity in inoculated host animals International Journal of Cancer 2005 115 3 437 442
45. Salcedo R., Hixon J. A., Stauffer J. K., Jalah R., Brooks A. D., Khan T., Dai R. M., Scheetz L., Lincoln E., Back T. C., Powell D., Hurwitz A. A., Sayers T. J., Kastelein R., Pavlakis G. N., Felber B. K., Trinchieri G., Wigginton J. M., Immunologic and therapeutic synergy of IL-27 and IL-2: enhancement of T cell sensitization, tumor-specific CTL reactivity and complete regression of disseminated neuroblastoma metastases in the liver and bone marrow Journal of Immunology 2009 182 7 4328 4338
46. Oniki S., Nagai H., Horikawa T., Furukawa J., Belladonna M. L., Yoshimoto T., Hara I., Nishigori C., Interleukin-23 and interleukin-27 exert quite different antitumor and vaccine effects on poorly immunogenic melanoma Cancer Research 2006 66 12 6395 6404
47. Hu P., Hu H.-D., Chen M., Peng M.-L., Tang L., Tang K.-F., Matsui M., Belladonna M. L., Yoshimoto T., Zhang D.-Z., Xiang R., Ren H., Expression of interleukins-23 and 27 leads to successful gene therapy of hepatocellular carcinoma Molecular Immunology 2009 46 8-9 1654 1662
48. Liu L., Wang S., Shan B., Shao L., Sato A., Kawamura K., Li Q., Ma G., Tagawa M., IL-27-mediated activation of natural killer cells and inflammation produced antitumour effects for human oesophageal carcinoma cells Scandinavian Journal of Immunology 2008 68 1 22 29
49. Matsui M., Kishida T., Nakano H., Yoshimoto K., Shin-Ya M., Shimada T., Nakai S., Imanishi J., Yoshimoto T., Hisa Y., Mazda O., Lnterleukin-27 activates natural killer cells and suppresses NK-resistant head and neck squamous cell carcinoma through inducing antibody-dependent cellular cytotoxicity Cancer Research 2009 69 6 2523 2530
50. Shimizu M., Shimamura M., Owaki T., Asakawa M., Fujita K., Kudo M., Iwakura Y., Takeda Y., Luster A. D., Mizuguchi J., Yoshimoto T., Antiangiogenic and antitumor activities of IL-27 Journal of Immunology 2006 176 12 7317 7324
51. Yoshimoto T., Morishima N., Mizoguchi I., Shimizu M., Nagai H., Oniki S., Oka M., Nishigori C., Mizuguchi J., Antiproliferative activity of IL-27 on melanoma Journal of Immunology 2008 180 10 6527 6535
52. Ho M.-Y., Leu S.-J. J., Sun G.-H., Tao M.-H., Tang S.-J., Sun K.-H., IL-27 directly restrains lung tumorigenicity by suppressing cyclooxygenase-2- mediated activities Journal of Immunology 2009 183 10 6217 6226
53. Morishima N., Owaki T., Asakawa M., Kamiya S., Mizuguchi J., Yoshimoto T., Augmentation of effector CD8+ T cell generation with enhanced granzyme B expression by IL-27 Journal of Immunology 2005 175 3 1686 1693
54. Matsui M., Moriya O., Belladonna M. L., Kamiya S., Lemonnier F. A., Yoshimoto T., Akatsuka T., Adjuvant activities of novel cytokines, interleukin-23 (IL-23) and IL-27, for induction of hepatitis C virus-specific cytotoxic T lymphocytes in HLA-A0201 transgenic mice Journal of Virology 2004 78 17 9093 9104
55. Shinozaki Y., Wang S., Miyazaki Y., Miyazaki K., Yamada H., Yoshikai Y., Hara H., Yoshida H., Tumor-specific cytotoxic T cell generation and dendritic cell function are differentially regulated by interleukin 27 during development of anti-tumor immunity International Journal of Cancer 2009 124 6 1372 1378
56. Morishima N., Mizoguchi I., Okumura M., Chiba Y., Xu M., Shimizu M., Matsui M., Mizuguchi J., A pivotal role for interleukin-27 in CD8 + T cell functions and generation of cytotoxic T lymphocytes Journal of Biomedicine and Biotechnology 2010 2010 10
57. Oppmann B., Lesley R., Blom B., Timans J. C., Xu Y., Hunte B., Vega F., Yu N., Wang J., Singh K., Zonin F., Vaisberg E., Churakova T., Liu M.-R., Gorman D., Wagner J., Zurawski S., Liu Y.-J., Abrams J. S., Moore K. W., Rennick D., De Waal-Malefyt R., Hannum C., Bazan J. F., Kastelein R. A., Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12 Immunity 2000 13 5 715 725
58. Aggarwal S., Ghilardi N., Xie M.-H., De Sauvage F. J., Gurney A. L., Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17 Journal of Biological Chemistry 2003 278 3 1910 1914
59. Zheng Y., Danilenko D. M., Valdez P., Kasman I., Eastham-Anderson J., Wu J., Ouyang W., Interleukin-22, a TH17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis Nature 2007 445 7128 648 651
60. Cua D. J., Sherlock J., Chen Y., Murphy C. A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., Zurawski S., Wiekowski M., Lira S. A., Gorman D., Kastelein R. A., Sedgwick J. D., Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain Nature 2003 421 6924 744 748
61. Elson C. O., Cong Y., Weaver C. T., Schoeb T. R., McClanahan T. K., Fick R. B., Kastelein R. A., Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice Gastroenterology 2007 132 7 2359 2370
62. Bettelli E., Carrier Y., Gao W., Korn T., Strom T. B., Oukka M., Weiner H. L., Kuchroo V. K., Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells Nature 2006 441 7090 235 238
63. Mangan P. R., Harrington L. E., O'Quinn D. B., Helms W. S., Bullard D. C., Elson C. O., Hatton R. D., Wahl S. M., Schoeb T. R., Weaver C. T., Transforming growth factor- induces development of the T H17 lineage Nature 2006 441 7090 231 234
64. Lo C.-H., Lee S.-C., Wu P.-Y., Pan W.-Y., Su J., Cheng C.-W., Roffler S. R., Chiang B.-L., Lee C.-N., Wu C.-W., Tao M.-H., Antitumor and antimetastatic activity of IL-23 Journal of Immunology 2003 171 2 600 607
65. Wang Y.-Q., Ugai S.-I., Shimozato O., Yu L., Kawamura K., Yamamoto H., Yamaguchi T., Saisho H., Tagawa M., Induction of systemic immunity by expression of interleukin-23 in murine colon carcinoma cells International Journal of Cancer 2003 105 6 820 824
66. Kaiga T., Sato M., Kaneda H., Iwakura Y., Takayama T., Tahara H., Systemic administration of IL-23 induces potent antitumor immunity primarily mediated through Th1-type response in association with the endogenously expressed IL-12 Journal of Immunology 2007 178 12 7571 7580
67. Yu H., Kortylewski M., Pardoll D., Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment Nature Reviews Immunology 2007 7 1 41 51
68. Stewart C. A., Trinchieri G., Reinforcing suppression using regulators: a new link between STAT3, IL-23, and Tregs in tumor immunosuppression Cancer Cell 2009 15 2 81 83
69. Zou W., Regulatory T cells, tumour immunity and immunotherapy Nature Reviews Immunology 2006 6 4 295 307
70. El Kasmi K. C., Smith A. M., Williams L., Neale G., Panopolous A., Watowich S. S., Hcker H., Foxwell B. M. J., Murray P. J., Cutting edge: a transcriptional repressor and corepressor induced by the STAT3-regulated anti-inflammatory signaling pathway Journal of Immunology 2007 179 11 7215 7219
71. Wei L., Laurence A., O'Shea J. J., New insights into the roles of Stat5a/b and Stat3 in T cell development and differentiation Seminars in Cell and Developmental Biology 2008 19 4 394 400
72. Collison L. W., Workman C. J., Kuo T. T., Boyd K., Wang Y., Vignali K. M., Cross R., Sehy D., Blumberg R. S., Vignali D. A. A., The inhibitory cytokine IL-35 contributes to regulatory T-cell function Nature 2007 450 7169 566 569
73. Collison L. W., Vignali D. A. A., Interleukin-35: odd one out or part of the family? Immunological Reviews 2008 226 1 248 262