Discovery of a Metastatic Immune Escape Mechanism Initiated by the Loss of Expression of the Tumour Biomarker Interleukin-33

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Saranchova, Iryna ^a,b   Han, Jeffrey ^a,b   Huang, Hui ^a,b   Fenninger, Franz ^a,b   Choi, Kyung Bok ^a   Munro, Lonna ^a   Pfeifer, Cheryl ^a   Welch, Ian ^b   Wyatt, Alexander W ^b   Fazli, Ladan ^b   Gleave, Martin E ^b   Jefferies, Wilfred A ^a,b,c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HLA ANTIGEN CLASS 1; IL33 PROTEIN, HUMAN; INTERLEUKIN 33; TUMOR MARKER;

ANIMAL; DISEASE EXACERBATION; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; KIDNEY TUMOR; MALE; METABOLISM; METASTASIS; MOUSE; PROSTATE TUMOR; RENAL CELL CARCINOMA; TUMOR CELL LINE; TUMOR ESCAPE;

ANIMALS; BIOMARKERS, TUMOR; CARCINOMA, RENAL CELL; CELL LINE, TUMOR; DISEASE PROGRESSION; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INTERLEUKIN-33; KIDNEY NEOPLASMS; MALE; MICE; NEOPLASM METASTASIS; PROSTATIC NEOPLASMS; TUMOR ESCAPE;

EID: 84987858623     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep30555     Document Type: Article

References (62)

1. Workd Health Organization; Media Centre: Cancer: Fact sheet N°297, Updated February 2015, http://www.who.int/mediacentre/ factsheets/fs297/en/; Access Date: 25/05/2016.
2. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674, doi: 10.1016/j.cell.2011.02.01 3S0092-8674(11)00127-9 (2011).
3. Janeway, C., Travers, P., Walport, M. & Murphy, K. Immunobiology: the Immune System in Health and Disease. 7th ed. edn, (NY Garland Publishing, 2008).
4. Gabathuler, R., Reid, G., Kolaitis, G., Driscoll, J. & Jefferies, W. A. Comparison of cell lines deficient in antigen presentation reveals a functional role for TAP-1 alone in antigen processing. The Journal of experimental medicine 180, 1415-1425 (1994).
5. Alimonti, J. et al. TAP expression provides a general method for improving the recognition of malignant cells in vivo. Nat Biotechnol 18, 515-520 (2000).
6. Martin, M. U. Special aspects of interleukin-33 and the IL-33 receptor complex. Semin Immunol 25, 449-457, doi: 10.1016/j. smim.2013.10.006 (2013).
7. Pascual-Figal, D. A. & Januzzi, J. L. The biology of ST2: the International ST2 Consensus Panel. Am J Cardiol 115, 3B-7B, doi: 10.1016/j.amjcard.2015.01.034 (2015).
8. Cayrol, C. & Girard, J. P. IL-33: an alarmin cytokine with crucial roles in innate immunity, inflammation and allergy. Curr Opin Immunol 31, 31-37, doi: 10.1016/j.coi.2014.09.004 (2014).
9. Musolino, C. et al. Reduction in IL-33 plasma levels might be involved in T cell dysregulation in chronic lymphocytic leukemia. Acta Haematol 131, 165-166, doi: 10.1159/000353476 (2014).
10. Gao, Q., Li, Y. & Li, M. The potential role of IL-33/ST2 signaling in fibrotic diseases. J Leukoc Biol 98, 15-22, doi: 10.1189/ jlb.3RU0115-012R (2015).
11. Carriere, V. et al. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc Natl Acad Sci USA 104, 282-287, doi: 10.1073/pnas.0606854104 (2007).
12. Guo, L., Junttila, I. S. & Paul, W. E. Cytokine-induced cytokine production by conventional and innate lymphoid cells. Trends Immunol 33, 598-606, doi: 10.1016/j.it.2012.07.006 (2012).
13. Moro, K. et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+ )Sca-1(+ ) lymphoid cells. Nature 463, 540-544, doi: 10.1038/nature08636 (2010).
14. Neill, D. R. et al. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464, 1367-1370, doi: 10.1038/nature08900 (2010).
15. Eberl, G., Colonna, M., Di Santo, J. P. & McKenzie, A. N. Innate lymphoid cells. Innate lymphoid cells: a new paradigm in immunology. Science 348, aaa6566, doi: 10.1126/science.aaa6566 (2015).
16. Rostan, O. et al. Crucial and diverse role of the interleukin-33/ST2 axis in infectious diseases. Infect Immun 83, 1738-1748, doi: 10.1128/IAI.02908-14 (2015).
17. Saluja, R. et al. The role of the IL-33/IL-1RL1 axis in mast cell and basophil activation in allergic disorders. Mol Immunol 63, 80-85, doi: 10.1016/j.molimm.2014.06.018 (2015).
18. Bouffi, C. et al. IL-33 markedly activates murine eosinophils by an NF-kappaB-dependent mechanism differentially dependent upon an IL-4-driven autoinflammatory loop. J Immunol 191, 4317-4325, doi: 10.4049/jimmunol.1301465 (2013).
19. Pecaric-Petkovic, T., Didichenko, S. A., Kaempfer, S., Spiegl, N. & Dahinden, C. A. Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood 113, 1526-1534, doi: 10.1182/blood-2008-05-157818 (2009).
20. Cherry, W. B., Yoon, J., Bartemes, K. R., Iijima, K. & Kita, H. A novel IL-1 family cytokine, IL-33, potently activates human eosinophils. J Allergy Clin Immunol 121, 1484-1490, doi: 10.1016/j.jaci.2008.04.005 (2008).
21. Smithgall, M. D. et al. 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 20, 1019-1030, doi: 10.1093/intimm/dxn060 (2008).
22. Suzukawa, M. et al. An IL-1 cytokine member, IL-33, induces human basophil activation via its ST2 receptor. J Immunol 181, 5981-5989 (2008).
23. Bourgeois, E. et al. The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-gamma production. Eur J Immunol 39, 1046-1055, doi: 10.1002/eji.200838575 (2009).
24. Yang, Q. et al. IL-33 synergizes with TCR and IL-12 signaling to promote the effector function of CD8+ T cells. Eur J Immunol 41, 3351-3360, doi: 10.1002/eji.201141629 (2011).
25. Baumann, C. et al. T-bet-and STAT4-dependent IL-33 receptor expression directly promotes antiviral Th1 cell responses. Proc Natl Acad Sci USA 112, 4056-4061, doi: 10.1073/pnas.1418549112 (2015).
26. Brunner, S. M. et al. Tumor-infiltrating, interleukin-33-producing effector-memory CD8(+ ) T cells in resected hepatocellular carcinoma prolong patient survival. Hepatology 61, 1957-1967, doi: 10.1002/hep.27728 (2015).
27. Jovanovic, I. P. et al. Interleukin-33/ST2 axis promotes breast cancer growth and metastases by facilitating intratumoral accumulation of immunosuppressive and innate lymphoid cells. Int J Cancer 134, 1669-1682, doi: 10.1002/ijc.28481 (2014).
28. Maywald, R. L. et al. IL-33 activates tumor stroma to promote intestinal polyposis. Proc Natl Acad Sci USA 112, E2487-E2496, doi: 10.1073/pnas.1422445112 (2015).
29. Liu, X. et al. IL-33/ST2 pathway contributes to metastasis of human colorectal cancer. Biochem Biophys Res Commun 453, 486-492, doi: 10.1016/j.bbrc.2014.09.106 (2014).
30. Liu, J., Shen, J. X., Hu, J. L., Huang, W. H. & Zhang, G. J. Significance of interleukin-33 and its related cytokines in patients with breast cancers. Front Immunol 5, 141, doi: 10.3389/fimmu.2014.00141 (2014).
31. Ye, X. L. et al. IL-33-induced JNK pathway activation confers gastric cancer chemotherapy resistance. Oncol Rep 33, 2746-2752, doi: 10.3892/or.2015.3898 (2015).
32. Yu, X. X. et al. IL-33 Promotes Gastric Cancer Cell Invasion and Migration Via ST2-ERK1/2 Pathway. Dig Dis Sci 60, 1265-1272, doi: 10.1007/s10620-014-3463-1 (2015).
33. Yamada, D. et al. IL-33 facilitates oncogene-induced cholangiocarcinoma in mice by an interleukin-6-sensitive mechanism. Hepatology 61, 1627-1642, doi: 10.1002/hep.27687 (2015).
34. Zhang, H. et al. Concordant down-regulation of proto-oncogene PML and major histocompatibility antigen HLA class I expression in high-grade prostate cancer. Cancer Immun 3, 2, doi: 030102 (2003).
35. Blades, R. A., Keating, P. J., McWilliam, L. J., George, N. J. & Stern, P. L. Loss of HLA class I expression in prostate cancer: implications for immunotherapy. Urology 46, 681-686; discussion 686-687 (1995).
36. Naoe, M. et al. Correlation between major histocompatibility complex class I molecules and CD8+ T lymphocytes in prostate, and quantification of CD8 and interferon-gamma mRNA in prostate tissue specimens. BJU Int 90, 748-753, doi: 2993 (2002).
37. Lou, Y. et al. Restoration of the expression of transporters associated with antigen processing in lung carcinoma increases tumorspecific immune responses and survival. Cancer Res 65, 7926-7933 (2005).
38. Setiadi, A. F., David, M. D., Chen, S. S., Hiscott, J. & Jefferies, W. A. Identification of mechanisms underlying transporter associated with antigen processing deficiency in metastatic murine carcinomas. Cancer research 65, 7485-7492 (2005).
39. Setiadi, A. F. et al. Epigenetic control of the immune escape mechanisms in malignant carcinomas. Molecular and cellular biology 27, 7886-7894 (2007).
40. Rooney, M. S., Shukla, S. A., Wu, C. J., Getz, G. & Hacohen, N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell 160, 48-61, doi: 10.1016/j.cell.2014.12.033 (2015).
41. Setiadi, A. F. et al. Epigenetic enhancement of antigen processing and presentation promotes immune recognition of tumors. Cancer Research 68, 9601-9607 (2008).
42. Karttunen, J., Sanderson, S. & Shastri, N. Detection of rare antigen-presenting cells by the lacZ T-cell activation assay suggests an expression cloning strategy for T-cell antigens. Proc Natl Acad Sci USA 89, 6020-6024 (1992).
43. Fridman, W. H., Pages, F., Sautes-Fridman, C. & Galon, J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12, 298-306, doi: 10.1038/nrc3245 (2012).
44. deLeeuw, R. J. et al. CD25 identifies a subset of CD4(+ )FoxP3(- ) TIL that are exhausted yet prognostically favorable in human ovarian cancer. Cancer Immunol Res 3, 245-253, doi: 10.1158/2326-6066.CIR-14-0146 (2015).
45. Taylor, B. S. et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 18, 11-22, doi: 10.1016/j.ccr.2010.05.026 (2010).
46. TCGA. The Cancer Genome Atlas, https://tcga-data.nci.nih.gov/tcga/tcgaCancerDetails.jsp?diseaseType= KIRC&diseaseName= Kidney%20renal%20clear%20cell%20carcinoma; Access date: 15/11/2015.
47. Seliger, B., Wollscheid, U., Momburg, F., Blankenstein, T. & Huber, C. Coordinate downregulation of multiple MHC class I antigen processing genes in chemical-induced murine tumor cell lines of distinct origin. Tissue Antigens 56, 327-336 (2000).
48. Seliger, B., Maeurer, M. J. & Ferrone, S. TAP off-tumors on. Immunol Today 18, 292-299, doi: S0167569997010529 (1997).
49. Tao, K., Fang, M., Alroy, J. & Sahagian, G. G. Imagable 4T1 model for the study of late stage breast cancer. BMC Cancer 8, 228, doi: 1471-2407-8-228[pii]10.1186/1471-2407-8-228 (2008).
50. Kitamura, H. et al. Down-regulation of HLA class I antigen is an independent prognostic factor for clear cell renal cell carcinoma. J Urol 177, 1269-1272; discussion 1272, doi: 10.1016/j.juro.2006.11.082 (2007).
51. Watson, N. F. et al. Immunosurveillance is active in colorectal cancer as downregulation but not complete loss of MHC class I expression correlates with a poor prognosis. Int J Cancer 118, 6-10, doi: 10.1002/ijc.21303 (2006).
52. Andratschke, M., Pauli, C., Stein, M., Chaubal, S. & Wollenberg, B. MHC-class I antigen expression on micrometastases in bone marrow of patients with head and neck squamous cell cancer. Anticancer Res 23, 1467-1471 (2003).
53. Mehta, A. M., Jordanova, E. S., Kenter, G. G., Ferrone, S. & Fleuren, G. J. Association of antigen processing machinery and HLA class I defects with clinicopathological outcome in cervical carcinoma. Cancer Immunol Immunother 57, 197-206, doi: 10.1007/s00262-007-0362-8 (2008).
54. Zia, A., Schildberg, F. W. & Funke, I. MHC class I negative phenotype of disseminated tumor cells in bone marrow is associated with poor survival in R0M0 breast cancer patients. Int J Cancer 93, 566-570 (2001).
55. Slovin, S. Biomarkers for immunotherapy in genitourinary malignancies. Urol Oncol, doi: 10.1016/j.urolonc.2015.02.007 (2015).
56. Rigamonti, N. & Bellone, M. Prostate cancer, tumor immunity and a renewed sense of optimism in immunotherapy. Cancer Immunol Immunother 61, 453-468, doi: 10.1007/s00262-012-1216-6 (2012).
57. Lee, H. M., Timme, T. L. & Thompson, T. C. Resistance to lysis by cytotoxic T cells: a dominant effect in metastatic mouse prostate cancer cells. Cancer Res 60, 1927-1933 (2000).
58. Smahel, M. et al. Immunisation with modified HPV16 E7 genes against mouse oncogenic TC-1 cell sublines with downregulated expression of MHC class I molecules. Vaccine 21, 1125-1136 (2003).
59. Zhang, Q. J. et al. TAP expression reduces IL-10 expressing tumor infiltrating lymphocytes and restores immunosurveillance against melanoma. Int J Cancer (2007).
60. Halim, T. Y. et al. Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 37, 463-474, doi: 10.1016/j.immuni.2012.06.012 (2012).
61. Wyatt, A. W. et al. Heterogeneity in the inter-tumor transcriptome of high risk prostate cancer. Genome Biol 15, 426, doi: 10.1186/ s13059-014-0426-y (2014).
62. Cerami, E. et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2, 401-404, doi: 10.1158/2159-8290.CD-12-0095 (2012).