ST2 deletion enhances innate and acquired immunity to murine mammary carcinoma

European Journal of Immunology

Volumn 41, Issue 7, 2011, Pages 1902-1912

  Jovanovic, Ivan ^a   Radosavljevic, Gordana ^a   Mitrovic, Maja ^b   Lisnic Juranic, Vanda ^b   Mckenzie, Andrew N J ^c   Arsenijevic, Nebojsa ^a   Jonjic, Stipan ^b   Lukic, Miodrag L ^a  

^a UNIVERSITY OF KRAGUJEVAC   (Serbia)

^b UNIVERSITY OF RIJEKA   (Croatia)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

4T1 mouse breast cancer; Cytotoxicity; NK cells; ST2; Th1 Th2 cells

Indexed keywords

CD11B ANTIGEN; CD27 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 17; INTERLEUKIN 4; ST2 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL MODEL; ARTICLE; BREAST CARCINOMA; CANCER GROWTH; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; FEMALE; GENE DELETION; IN VITRO STUDY; INNATE IMMUNITY; METASTASIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SPLEEN CELL; TUMOR IMMUNITY;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, CD; ANTIGENS, CD11B; ANTIGENS, CD27; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DISEASE PROGRESSION; FEMALE; IMMUNITY, INNATE; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKIN-4; INTERLEUKINS; KILLER CELLS, NATURAL; LECTINS, C-TYPE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; RECEPTORS, IMMUNOLOGIC; RECEPTORS, INTERLEUKIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79959763551     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141417     Document Type: Article

References (45)

1. Klemenz, R., Hoffmann, S. and Werenskiold, A. K., Serum- and oncoprotein-mediated induction of a gene with sequence similarity to the gene encoding carcinoembryonic antigen. Proc. Natl. Acad. Sci. USA 1989. 86: 5708-5712.
2. Tominaga, S., A putative protein of a growth specific cDNA from BALB/c-3T3 cells is highly similar to the extracellular portion of mouse interleukin 1 receptor. FEBS Lett. 1989. 258: 301-304.
3. Liew, F. Y., Pitman, N. I. and McInnes, I. B., Disease-associated function of IL-33: the new kid in the IL-1 family. Nat. Rev. Immunol. 2010. 10: 103-110.
4. Tago, K., Noda, T., Hayakawa, M., Iwahana, H., Yanagisawa, K., Yashiro, T. and Tominaga, S., Tissue distribution and subcellular localization of a variant form of the human ST2 gene product, ST2V. Biochem. Biophys. Res. Commun. 2001. 285: 1377-1383.
5. Trajkovic, V., Sweet, M. J., Xu, D., T1/ST2-an IL-1 receptor-like modulator of immune responses. Cytokine Growth Factor Rev. 2004. 15: 87-95.
6. Gachter, T., Werenskiold, A. K. and Klemenz, R., Transcription of the interleukin-1 receptor-related T1 gene is initiated at different promoters in mast cells and fibroblasts. J. Biol. Chem. 1996. 271: 124-129.
7. Moritz, D. R., Rodewald, H. R., Gheyselinck, J. and Klemenz, R., The IL-1 receptor-related T1 antigen is expressed on immature and mature mast cells and on fetal blood mast cell progenitors. J. Immunol. 1998. 161: 4866-4874.
8. Lohning, M., Stroehmann, A., Coyle, A. J., Grogan, J. L., Lin, S., Gutierrez-Ramos, J. C., Levinson, D. et al., T1/ST2 is preferentially expressed on murine Th2 cells, independent of interleukin 4, interleukin 5, and interleukin 10, and important for Th2 effector function. Proc. Natl. Acad. Sci. USA 1998. 95: 6930-6935.
9. Bourgeois, E., Van, L. P., Samson, M., Diem, S., Barra, A., Roga, S., Gombert, J. M. et al., The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-γ production. Eur. J. Immunol. 2009. 39: 1046-1055.
10. Smithgall, M. D., Comeau, M. R., Yoon, B. R. P., Kaufman, D., Armitage, R. and Smith, D. E., IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int. Immunol. 2008. 20: 1019-1030.
11. Pecaric-Petkovic, T., Didichenko, S. A., Kaempfer, S., Spiegl, N. and Dahinden, C. A., Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood 2009. 113: 1526-1534.
12. Brint, E. K., Xu, D., Liu, H., Dunne, A., McKenzie, A. N. J., O'Neill, L. A. J. and Liew, F. Y., ST2 is an inhibitor of IL-1R and TLR4 signaling and maintains endotoxin tolerance. Nat. Immunol. 2004. 5: 373-379.
13. Mayuzumi, N., Matsushima, H. and Takashima, A., IL-33 promotes DC development in BM culture by triggering GM-CSF production. Eur. J. Immunol. 2009. 39: 3331-3342.
14. Kurowska-Stolarska, M., Stolarski, B., Kewin, P., Murphy, G., Corrigan, C. J., Ying, S., Pitman, N. et al., IL-33 Amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J. Immunol. 2009. 183: 6469-6477.
15. Chan, W. L., Pejnovic, N., Lee, C. A. and Al-Ali, N. A., Human Il-18 receptor and ST2L are stable and selective markers for the respective type 1 and type 2 circulating tymphocytes. J. Immunol. 2001. 167: 1238-1244.
16. Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., McClanahan, T. K., Zurawski, G. et al., IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 2005. 23: 479-490.
17. Ohto-Ozaki, H., Kuriowa, K., Mato, N., Matsuyama, Y., Hayakawa, M., Tamemoto, H. and Tominaga, S., Characterization of ST2 transgenic mice with resistance to IL-33. Eur. J. Immunol. 2010. 40: 2632-2642.
18. Ferlay, J., Parkin, D. M. and Sreliarova-Foucher, E., Estimates of cancer incidence and mortality in Europe in 2008. Eur. J. Cancer 2010. 46: 765-781.
19. Schmitt, C. A., Senescence, apoptosis and therapy-cutting the life lines of cancer. Nat. Rev. Cancer 2003. 3: 286-295.
20. Lu, X., Kang, Y., Organotropism of breast cancer metastasis. J. Mammary Gland Biol. Neoplasia 2007. 12: 153-162.
21. Plunkett, T. A., Correa, I., Miles, D. W. and Taylor-Papadimitriou, J., Breast cancer and the immune system: opportunities and pitfalls. J. Mammary Gland Biol. Neoplasia 2001. 6: 467-475.
22. Ito, N., Nakamura, H., Tanaka, Y. and Ohgi, S., Lung carcinoma: analysis of T-helper type 1 and 2 cells and T-cytotoxic type 1 and 2 cells by intracellular cytokine detection with flow cytometry. Cancer 1999. 85: 2359-2367.
23. Nishimura, T., Nakui, M., Sato, M., Iwakabe, K., Kitamura, H., Sekimoto, M., Ohta, A. et al., The critical role of Th1-dominant immunity in tumor immunology. Cancer Chemother. Pharmacol. 2000. 46: 52-61.
24. Dobrzanski, M. J., Reome, J. B., Hylindand, J. C. and Rewers-Felkins, K. A., CD8-mediated type 1 antitumor responses selectively modulate endogenous differentiated and nondifferentiated t cell localization, activation, and function in progressive breast cancer. J. Immunol. 2006. 177: 8191-8201.
25. Hung, K., Hayashi, R., Lafond-Walker, A., Lowenstein, C., Pardoll, D. and Levitsky, H., The central role of CD4+ T cells in the antitumor immune response. J. Exp. Med. 1998. 188: 2357-2368.
26. Ellyard, J. I., Simson, L., Parish, C. R., Th2-mediated anti-tumour immunity: friend or foe? Tissue Antigens 2007. 70: 1-11.
27. Xu, D., Chan, W. L., Leung, B. P., Huang, F., Wheeler, R., Piedrafita, D., Robinson, J. H. and Liew, F. Y., Selective expression of a stable cell surface molecule on type 2 but not type 1 helper T cells. J. Exp. Med. 1998. 187: 787-794.
28. Townsend, M. J., Fallon, P. G., Matthews, D. J., Jolin, H. E. and McKenzie, A. N., T1/ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses. J. Exp. Med. 2000. 191: 1069-1076.
29. Meisel, C., Bonhagen, K., Lohning, M., Coyle, A. J., Gutierrez-Ramos, J. C., Radbruch, A. and Kamradt, T., Regulation and function of T1/ST2 expression on CD4+ T cells: Induction of type 2 cytokine production by T1/ST2 cross-linking. J. Immunol. 2001. 166: 3143-3150.
30. Jones, L. A., Roberts, F., Nickdel, M. B., Brombacher, F., McKenzie, A. N., Henriquez, F. L., Alexander, J. et al., IL-33 receptor (T1/ST2) signalling is necessary to prevent the development of encephalitis in mice infected with Toxoplasma gondii. Eur. J. Immunol. 2010. 40: 426-436.
31. Coyle, A. J., Lloyd, C., Tian, J., Nguyen, T., Erikkson, C., Wang, L., Ottoson, P. et al., Crucial role of the interleukin 1 receptor family member T1/ST2 in T helper cell type 2-mediated lung mucosal immune responses. J. Exp. Med. 1999. 190: 895-902.
32. Vujanovic, N. L., Basse, P., Herberman, R. B. and Whiteside, T. L., Antitumor functions of natural killer cells and control of metastasis. Methods 1996. 9: 394-408.
33. Tao, K., Fang, M., Alroy, J. and Sahagian, G. G., Imagable 4T1 model for study of late stage breast cancer. Biomed. Chromatogr. Cancer 2008. 8: 228-248.
34. Stout, R. D. and Bottomly, K., Antigen- specific activation of effector macrophages by IFN-γ producing (TH1) T cell clones. Failure of IL-4-producing (TH2) T cell clones to activate effector function of macrophages. J. Immunol. 1989. 142: 760-765.
35. Hu, H. M., Urba, W. J. and Fox, B. A., Gene-modified tumor vaccine with therapeutic potential shifts tumor-specific T cell response from a type 2 to a type 1 cytokine profile. J. Immunol. 1998. 161: 3033-3041.
36. Zdravkovic, N., Shahin, A., Arsenijevic, N., Lukic, M. L. and Mensah-Brown, E., Regulatory T cells and ST2 signaling control diabetes induction with multiple low doses of streptozotocin. Mol. Immunol. 2009. 47: 28-36.
37. Mensah-Brown, E., Shahin, A., Parekh, K., Hakim, A. A., Shamisi, M. A., Hsu, D. K. and Lukic, M. L., Functional capacity of macrophages determines the induction of type 1 diabetes. Ann. NY Acad. Sci. 2006. 1084: 49-57.
38. Sweet, M. J., Leung, B. P., Kang, D., Sogaard, M., Schultz, K., Trajkovic, V., Campbell, C. C. et al., A novel pathway regulating lipopolysaccharide-induced shock by ST2/T1 via inhibition of Toll-like receptor 4 expression. J. Immunol. 2001. 166: 6633-6639.
39. Foti, M., Granucci, F. and Ricciardi-Castagnoli, P., A central role for tissue-resident dendritic cells in innate responses. Trends Immunol. 2004. 25: 650-654.
40. Hayakawa, Y. and Smyth, M. J., CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 2006. 176: 1517-1524.
41. Borrego, F., Robertson, M. J., Ritz, J., Pena, J. and Solana, R., CD69 is a stimulatory receptor for natural killer cell and its cytotoxic effect is blocked by CD94 inhibitory receptor. Immunology 1999. 97: 159-165.
42. Tessmer, M. S., Fugere, C., Stevenaert, F., Naidenko, O. V., Chong, H. J., Leclercq, G. and Brossay, L., KLRG1 binds cadherins and preferentially associated with SHIP-1. Int. Immunol. 2007. 19: 391-400.
43. Jovanovic, I., Radosavljevic, G., Pavlovic, S., Zdravkovic, N., Martinova, K., Knezevic, M., Zivic, D. et al., Th-17 cells as novel participant in immunity to breast cancer. Serb. J. Exp. Clin. Res. 2010. 11: 59-65.
44. Carlsson, G., Ekelund, E., Stigsson, L. and Hafstrom, L., Vascularization and tumour volume estimations of solitary liver tumours in rats. Ann. Chir. Gynaecol. 1983. 72: 187-191.
45. Janjic, B. M., Lu, G., Pimenov, A., Whiteside, T. L., Storkus, W. J. and Vujanovic, N. L., Innate direct anticancer effector function of human immature dendritic cells. I. Involvement of an apoptosis-inducing pathway. J. Immunol. 2002. 168: 1823-1830.