IFN-γ is required for cytotoxic T cell-dependent cancer genome immunoediting

Nature Communications

Volumn 8, Issue , 2017, Pages

  Takeda, Kazuyoshi ^a,b,c   Nakayama, Masafumi ^d   Hayakawa, Yoshihiro ^c,e   Kojima, Yuko ^f   Ikeda, Hiroaki ^g,h   Imai, Naoko ^g,i   Ogasawara, Kouetsu ^d   Okumura, Ko ^a,b   Thomas, David M ^j   Smyth, Mark J ^c,k,l  

^a JUNTENDO UNIVERSITY   (Japan)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c PETER MACCALLUM CANCER CENTRE   (Australia)

^d TOHOKU UNIVERSITY   (Japan)

^e UNIVERSITY OF TOYAMA   (Japan)

^f JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^g MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^h NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

ⁱ MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^j GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^k QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^l UNIVERSITY OF QUEENSLAND   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 1; CONCANAMYCIN A; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR; GENOMIC DNA; GENOMIC RNA; HEMAGGLUTININ; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; STAT1 PROTEIN; TUMOR ANTIGEN;

CANCER; CELLS AND CELL COMPONENTS; ENZYME; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC DIFFERENTIATION; GENOME; IMMUNE RESPONSE; RODENT; TUMOR;

ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGENICITY; ARTICLE; CANCER GENETICS; CD8+ T LYMPHOCYTE; CELL CLONE; CELL STIMULATION; COMPARATIVE GENOMIC HYBRIDIZATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DNA DAMAGE; DNA DAMAGE RESPONSE; DNA REPAIR; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EDITING; GENE EXPRESSION; GENE LOSS; GENOMIC INSTABILITY; IMMUNE EVASION; IMMUNITY; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL INOCULATION; TUMOR MICROENVIRONMENT; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DISEASE EXACERBATION; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; MOLECULAR EVOLUTION; MUTATION; NEOPLASM; PATHOLOGY;

ANIMALS; ANTIGENS, NEOPLASM; DISEASE PROGRESSION; DNA DAMAGE; DNA REPAIR; EVOLUTION, MOLECULAR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMIC INSTABILITY; HUMANS; IMMUNE TOLERANCE; INTERFERON-GAMMA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MUTATION; NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85013802550     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14607     Document Type: Article

References (65)

1. Schreiber, R. D., Old, L. J. & Smyth, M. J. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331, 1565-1570 (2011).
2. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
3. Matsushita, H. et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 482, 400-404 (2012).
4. DuPage, M., Mazumdar, C., Schmidt, L. M., Cheung, A. F. & Jacks, T. Expression of tumour-specific antigens underlies cancer immunoediting. Nature 482, 405-409 (2012).
5. Shankaran, V. et al. IFNg and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410, 1107-1111 (2001).
6. Braumüller, H. et al. T-helper-1-cell cytokines drive cancer into senescence. Nature 494, 361-365 (2013).
7. Zaretsky, J. M. et al. Mutations associated with acquired resistance to PD-1 blockade in melanoma. N. Engl. J. Med. 375, 819-829 (2016).
8. Textor, A. et al. Preventing tumor escape by targeting a post-proteasomal trimming independent epitope. J. Exp. Med. 213, 2333-2348 (2016).
9. Helmich, B. K. & Dutton, R. W. The role of adoptively transferred CD8 T cells and host cells in the control of the growth of the EG7 thymoma: factors that determine the relative effectiveness and homing properties of Tc1 and Tc2 effectors. J. Immunol. 166, 6500-6508 (2001).
10. Tanaka, N. et al. Cooperation of the tumour suppressors IRF-1 and p53 in response to DNA damage. Nature 382, 816-818 (1996).
11. Dighe, A. S., Richards, E., Old, L. J. & Schreiber, R. D. Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN g receptors. Immunity 1, 447-456 (1994).
12. Hanada, T. et al. IFNg-dependent, spontaneous development of colorectal carcinomas in SOCS1-deficient mice. J. Exp. Med. 203, 1391-1397 (2006).
13. Zaidi, M. R. et al. Interferon-g links ultraviolet radiation to melanomagenesis in mice. Nature 469, 548-553 (2011).
14. Taube, J. M. et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci. Transl. Med. 4, 127ra137 (2012).
15. Schürch, C., Riether, C., Amrein, M. A. & Ochsenbein, A. F. Cytotoxic T cells induce proliferation of chronic myeloid leukemia stem cells by secreting interferon-g. J. Exp. Med. 210, 605-621 (2013).
16. Katsurano, M. et al. Early-stage formation of an epigenetic field defect in a mouse colitis model, and non-essential roles of T- and B-cells in DNA methylation induction. Oncogene 31, 342-351 (2012).
17. Dunn, G. P., Koebel, C. M. & Schreiber, R. D. Interferons, immunity and cancer immunoediting. Nat. Rev. Immunol. 6, 836-848 (2006).
18. Zaidi, M. R. & Merlino, G. The two faces of interferon-g in cancer. Clin. Cancer Res. 17, 6118-6124 (2011).
19. Zou, Q. et al. T cell intrinsic USP15 deficiency promotes excessive IFN-g production and an immunosuppressive tumor microenvironment in MCAinduced fibrosarcoma. Cell Rep. 13, 2470-2479 (2015).
20. Zack, T. I. et al. Pan-cancer patterns of somatic copy number alteration. Nat. Genet. 45, 1134-1140 (2013).
21. Pinkel, D. & Albertson, D. G. Array comparative genomic hybridization and its applications in cancer. Nat. Genet. 37(Suppl): S11-S17 (2005).
22. Maser, R. S. et al. Chromosomally unstable mouse tumours have genomic alterations similar to diverse human cancers. Nature 447, 966-971 (2007).
23. Westcott, P. M. et al. The mutational landscapes of genetic and chemical models of Kras-driven lung cancer. Nature 517, 489-492 (2015).
24. McFadden, D. G. et al. Genetic and clonal dissection of murine small cell lung carcinoma progression by genome sequencing. Cell 156, 1298-1311 (2014).
25. Gao, R. et al. Punctuated copy number evolution and clonal stasis in triple-negative breast cancer. Nat. Genet. 48, 1119-1130 (2016).
26. Notta, F. et al. A renewed model of pancreatic cancer evolution based on genomic rearrangement patterns. Nature 538, 378-382 (2016).
27. Markowetz, F. A saltationist theory of cancer evolution. Nat. Genet. 48, 1102-1103 (2016).
28. Kottke, T. et al. Detecting and targeting tumor relapse by its resistance to innate effectors at early recurrence. Nat. Med. 19, 1625-1631 (2013).
29. Matsui, K., O'Mara, L. A. & Allen, P. M. Successful elimination of large established tumors and avoidance of antigen-loss variants by aggressive adoptive T cell immunotherapy. Int. Immunol. 15, 797-805 (2003).
30. Swanton, C., McGranahan, N., Starrett, G. J. & Harris, R. S. APOBEC enzymes: mutagenic fuel for cancer evolution and heterogeneity. Cancer Discov. 5, 704-712 (2015).
31. Mehta, H. V., Jones, P. H., Weiss, J. P. & Okeoma, C. M. IFN-a and lipopolysaccharide upregulate APOBEC3 mRNA through different signaling pathways. J. Immunol. 189, 4088-4103 (2012).
32. Chiu, Y. T. et al. Inactivation of ATM/ATR DNA damage checkpoint promotes androgen induced chromosomal instability in prostate epithelial cells. PLoS ONE 7, e51108 (2012).
33. Uno, T. et al. Eradication of established tumors in mice by a combination antibody-based therapy. Nat. Med. 12, 693-698 (2006).
34. Smyth, M. J. et al. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) contributes to interferon g-dependent natural killer cell protection from tumor metastasis. J. Exp. Med. 193, 661-670 (2001).
35. Takeda, K. et al. IFN-g production by lung NK cells is critical for the natural resistance to pulmonary metastasis of B16 melanoma in mice. J. Leukoc. Biol. 90, 777-785 (2011).
36. Benci, J. L. et al. Tumor interferon signaling regulates a multigenic resistance program to immune checkpoint blockade. Cell 167, 1540-1554 (2016).
37. Magnus, N. et al. Tissue factor expression provokes escape from tumor dormancy and leads to genomic alterations. Proc. Natl Acad. Sci. USA 111, 3544-3549 (2014).
38. Hölzel, M., Bovier, A. & Tuting, T. Plasticity of tumour and immune cells: a source of heterogeneity and a cause for therapy resistance? Nat. Rev. Cancer 13, 365-376 (2013).
39. Wang, Y. et al. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 512, 155-160 (2014).
40. Landsberg, J. et al. Melanomas resist T-cell therapy through inflammationinduced reversible dedifferentiation. Nature 490, 412-416 (2012).
41. Restifo, N. P., Dudley, M. E. & Rosenberg, S. A. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol. 12, 269-281 (2012).
42. Khong, H. T. & Restifo, N. P. Natural selection of tumor variants in the generation of 'tumor escape' phenotypes. Nat. Immunol. 3, 999-1005 (2002).
43. Willimsky, G. & Blankenstein, T. Sporadic immunogenic tumours avoid destruction by inducing T-cell tolerance. Nature 437, 141-146 (2005).
44. 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 (2015).
45. Champiat, S., Ferte, C., Lebel-Binay, S., Eggermont, A. & Soria, J. C. Exomics and immunogenics: bridging mutational load and immune checkpoints efficacy. Oncoimmunology 3, e27817 (2014).
46. Engels, B. et al. Relapse or eradication of cancer is predicted by peptide-major histocompatibility complex affinity. Cancer Cell 23, 516-526 (2013).
47. Leisegang, M. et al. Eradication of large solid tumors by gene therapy with a T cell receptor targeting a single cancer-specific point mutation. Clin. Cancer Res. 22, 2734-2743 (2015).
48. Lollini, P. L., Cavallo, F., Nanni, P. & Forni, G. Vaccines for tumour prevention. Nat. Rev. Cancer 6, 204-216 (2006).
49. Cretney, E. et al. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J. Immunol. 168, 1356-1361 (2002).
50. Kodama, T. et al. Perforin-dependent NK cell cytotoxicity is sufficient for anti-metastatic effect of IL-12. Eur J. Immunol. 29, 1390-1396 (1999).
51. Berner, V. et al. IFN-g mediates CD4+ T-cell loss and impairs secondary antitumor responses after successful initial immunotherapy. Nat. Med. 13, 354-360 (2007).
52. Marzo, A. L. et al. Tumor antigens are constitutively presented in the draining lymph nodes. J. Immunol. 162, 5838-5845 (1999).
53. Coughlin, C. M. et al. Tumor cell responses to IFNg affect tumorigenicity and response to IL-12 therapy and antiangiogenesis. Immunity 9, 25-34 (1998).
54. Nakajima, K. et al. A central role for Stat3 in IL-6-induced regulation of growth and differentiation in M1 leukemia cells. EMBO J. 15, 3651-3658 (1996).
55. Takeda, K., Hatakeyama, K., Tsuchiya, Y., Rikiishi, H. & Kumagai, K. A correlation between GM-CSF gene expression and metastases in murine tumors. Int. J. Cancer 47, 413-420 (1991).
56. Norbury, C. C., Chambers, B. J., Prescott, A. R., Ljunggren, H. G. & Watts, C. Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrowderived dendritic cells. Eur. J. Immunol. 27, 280-288 (1997).
57. Hayakawa, Y. et al. NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J. Immunol. 172, 123-129 (2004).
58. Fokas, E. et al. Targeting ATR in vivo using the novel inhibitor VE-822 results in selective sensitization of pancreatic tumors to radiation. Cell Death Dis. 3, e441 (2012).
59. Takeda, K. et al. Critical role for tumor necrosis factor-related apoptosisinducing ligand in immune surveillance against tumor development. J. Exp. Med. 195, 161-169 (2002).
60. Masuda, H. et al. Stem cell-like properties of the endometrial side population: implication in endometrial regeneration. PLoS ONE 5, e10387 (2010).
61. Dalerba, P. et al. Phenotypic characterization of human colorectal cancer stem cells. Proc. Natl Acad. Sci. USA 104, 10158-10163 (2007).
62. Trask, B. J. Fluorescence in situ hybridization: applications in cytogenetics and gene mapping. Trends Genet. 7, 149-154 (1991).
63. Lipson, D., Aumann, Y., Ben-Dor, A., Linial, N. & Yakhini, Z. Efficient calculation of interval scores for DNA copy number data analysis. J. Comput. Biol. 13, 215-228 (2006).
64. Kawamura, T. et al. Critical role of NK1+ T cells in IL-12-induced immune responses in vivo. J. Immunol. 160, 16-19 (1998).
65. Takeda, K. et al. Induction of tumor-specific T cell immunity by anti-DR5 antibody therapy. J. Exp. Med. 199, 437-448 (2004).