STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors

Immunity

Volumn 41, Issue 5, 2014, Pages 830-842

  Woo, Seng Ryong ^a   Fuertes, Mercedes B ^a   Corrales, Leticia ^a   Spranger, Stefani ^a   Furdyna, Michael J ^a   Leung, Michael Y K ^a   Duggan, Ryan ^c   Wang, Ying ^b   Barber, Glen N ^d   Fitzgerald, Katherine A ^e   Alegre, Maria Luisa ^b   Gajewski, Thomas F ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CYCLIC GMP; CYCLIC GMP AMP SYNTHASE; DNA; INTERFERON REGULATORY FACTOR 3; PROTEIN; STIMULATOR OF INTERFERON GENE COMPLEX; UNCLASSIFIED DRUG; IPS-1 PROTEIN, MOUSE; IRF3 PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; MB21D1 PROTEIN, MOUSE; MEMBRANE PROTEIN; MPYS PROTEIN, MOUSE; MYD88 PROTEIN, MOUSE; MYELOID DIFFERENTIATION FACTOR 88; NUCLEOTIDYLTRANSFERASE; PURINERGIC P2X7 RECEPTOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TLR4 PROTEIN, MOUSE; TLR9 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTICLE; CANCER CONTROL; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CYTOKINE PRODUCTION; DENDRITIC CELL; DNA SENSING; FEMALE; GENETIC PROCEDURES; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; EXPERIMENTAL MELANOMA; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; TUMOR CELL LINE;

ADAPTIVE IMMUNITY; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADOPTIVE TRANSFER; ANIMALS; ANTIGEN-PRESENTING CELLS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELL PROLIFERATION; DENDRITIC CELLS; DNA; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; LYMPHOCYTE ACTIVATION; MELANOMA, EXPERIMENTAL; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; NUCLEOTIDYLTRANSFERASES; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, PURINERGIC P2X7; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 9; TUMOR MICROENVIRONMENT;

EID: 84912120595     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2014.10.017     Document Type: Article

References (51)

1. Abe T., Harashima A., Xia T., Konno H., Konno K., Morales A., Ahn J., Gutman D., Barber G.N. STING recognition of cytoplasmic DNA instigates cellular defense. Mol. Cell 2013, 50:5-15.
2. Ahn J., Gutman D., Saijo S., Barber G.N. STING manifests self DNA-dependent inflammatory disease. Proc. Natl. Acad. Sci. USA 2012, 109:19386-19391.
3. Apetoh L., Ghiringhelli F., Tesniere A., Obeid M., Ortiz C., Criollo A., Mignot G., Maiuri M.C., Ullrich E., Saulnier P., et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 2007, 13:1050-1059.
4. Blank C., Brown I., Peterson A.C., Spiotto M., Iwai Y., Honjo T., Gajewski T.F. PD-L1/B7H-1 inhibits the effector phase of tumor rejection by Tcell receptor (TCR) transgenic CD8+ Tcells. Cancer Res. 2004, 64:1140-1145.
5. Blank C., Brown I., Kacha A.K., Markiewicz M.A., Gajewski T.F. ICAM-1 contributes to but is not essential for tumor antigen cross-priming andCD8+ Tcell-mediated tumor rejection invivo. J.Immunol. 2005, 174:3416-3420.
6. Burdette D.L., Monroe K.M., Sotelo-Troha K., Iwig J.S., Eckert B., Hyodo M., Hayakawa Y., Vance R.E. STING is a direct innate immune sensor of cyclic di-GMP. Nature 2011, 478:515-518.
7. Dankort D., Curley D.P., Cartlidge R.A., Nelson B., Karnezis A.N., Damsky W.E., You M.J., DePinho R.A., McMahon M., Bosenberg M. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 2009, 41:544-552.
8. Diamond M.S., Kinder M., Matsushita H., Mashayekhi M., Dunn G.P., Archambault J.M., Lee H., Arthur C.D., White J.M., Kalinke U., et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J.Exp. Med. 2011, 208:1989-2003.
9. Fuertes M.B., Kacha A.K., Kline J., Woo S.R., Kranz D.M., Murphy K.M., Gajewski T.F. Host type I IFN signals are required for antitumor CD8+ Tcell responses through CD8alpha+ dendritic cells. J.Exp. Med. 2011, 208:2005-2016.
10. Fuertes M.B., Woo S.R., Burnett B., Fu Y.X., Gajewski T.F. Type I interferon response and innate immune sensing of cancer. Trends Immunol. 2013, 34:67-73.
11. Gajewski T.F. Identifying and overcoming immune resistance mechanisms in the melanoma tumor microenvironment. Clin. Cancer Res. 2006, 12:2326s-2330s.
12. Gajewski T.F., Schumacher T. Cancer immunotherapy. Curr. Opin. Immunol. 2013, 25:259-260.
13. Gajewski T.F., Louahed J., Brichard V.G. Gene signature in melanoma associated with clinical activity: a potential clue to unlock cancer immunotherapy. Cancer J. 2010, 16:399-403.
14. Galon J., Costes A., Sanchez-Cabo F., Kirilovsky A., Mlecnik B., Lagorce-Pagès C., Tosolini M., Camus M., Berger A., Wind P., et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006, 313:1960-1964.
15. Ghiringhelli F., Apetoh L., Tesniere A., Aymeric L., Ma Y., Ortiz C., Vermaelen K., Panaretakis T., Mignot G., Ullrich E., et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med. 2009, 15:1170-1178.
16. Hamid O., Schmidt H., Nissan A., Ridolfi L., Aamdal S., Hansson J., Guida M., Hyams D.M., Gómez H., Bastholt L., et al. A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J.Transl. Med. 2011, 9:204.
17. Harlin H., Meng Y., Peterson A.C., Zha Y., Tretiakova M., Slingluff C., McKee M., Gajewski T.F. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 2009, 69:3077-3085.
18. Henry T., Brotcke A., Weiss D.S., Thompson L.J., Monack D.M. Type I interferon signaling is required for activation of the inflammasome during Francisella infection. J.Exp. Med. 2007, 204:987-994.
19. Hoebe K., Janssen E.M., Kim S.O., Alexopoulou L., Flavell R.A., Han J., Beutler B. Upregulation of costimulatory molecules induced by lipopolysaccharide and double-stranded RNA occurs by Trif-dependent and Trif-independent pathways. Nat. Immunol. 2003, 4:1223-1229.
20. Hwang W.T., Adams S.F., Tahirovic E., Hagemann I.S., Coukos G. Prognostic significance of tumor-infiltrating Tcells in ovarian cancer: A meta-analysis. Gynecol. Oncol. 2012, 124:192-198.
21. Ishii K.J., Coban C., Kato H., Takahashi K., Torii Y., Takeshita F., Ludwig H., Sutter G., Suzuki K., Hemmi H., et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat. Immunol. 2006, 7:40-48.
22. Ishikawa H., Ma Z., Barber G.N. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009, 461:788-792.
23. Ji R.R., Chasalow S.D., Wang L., Hamid O., Schmidt H., Cogswell J., Alaparthy S., Berman D., Jure-Kunkel M., Siemers N.O., et al. An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol. Immunother. 2012, 61:1019-1031.
24. Jounai N., Kobiyama K., Takeshita F., Ishii K.J. Recognition of damage-associated molecular patterns related to nucleic acids during inflammation and vaccination. Frontiers in cellular and infection microbiology 2012, 2:168.
25. Kawane K., Ohtani M., Miwa K., Kizawa T., Kanbara Y., Yoshioka Y., Yoshikawa H., Nagata S. Chronic polyarthritis caused by mammalian DNA that escapes from degradation in macrophages. Nature 2006, 443:998-1002.
26. Kono H., Rock K.L. How dying cells alert the immune system to danger. Nat. Rev. Immunol. 2008, 8:279-289.
27. Kroemer G., Galluzzi L., Kepp O., Zitvogel L. Immunogenic cell death in cancer therapy. Annu. Rev. Immunol. 2013, 31:51-72.
28. Lande R., Gregorio J., Facchinetti V., Chatterjee B., Wang Y.H., Homey B., Cao W., Wang Y.H., Su B., Nestle F.O., et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007, 449:564-569.
29. Li Y., Wang L.X., Yang G., Hao F., Urba W.J., Hu H.M. Efficient cross-presentation depends on autophagy in tumor cells. Cancer Res. 2008, 68:6889-6895.
30. Mahmoud S.M., Paish E.C., Powe D.G., Macmillan R.D., Grainge M.J., Lee A.H., Ellis I.O., Green A.R. Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 2011, 29:1949-1955.
31. Marichal T., Ohata K., Bedoret D., Mesnil C., Sabatel C., Kobiyama K., Lekeux P., Coban C., Akira S., Ishii K.J., et al. DNA released from dying host cells mediates aluminum adjuvant activity. Nat. Med. 2011, 17:996-1002.
32. Matsushita H., Vesely M.D., Koboldt D.C., Rickert C.G., Uppaluri R., Magrini V.J., Arthur C.D., White J.M., Chen Y.S., Shea L.K., et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012, 482:400-404.
33. McKee A.S., Burchill M.A., Munks M.W., Jin L., Kappler J.W., Friedman R.S., Jacobelli J., Marrack P. Host DNA released in response to aluminum adjuvant enhances MHC class II-mediated antigen presentation and prolongs CD4 T-cell interactions with dendritic cells. Proc. Natl. Acad. Sci. USA 2013, 110:E1122-E1131.
34. Molinero L.L., Zhou P., Wang Y., Harlin H., Kee B., Abraham C., Alegre M.L. Epidermal Langerhans cells promote skin allograft rejection in mice with NF-kappa B-impaired Tcells. American journal of transplantation: official journal of the American Society of Transplantation and the American Society of Transplant Surgeons 2008, 8:21-31.
35. Napirei M., Karsunky H., Zevnik B., Stephan H., Mannherz H.G., Möröy T. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 2000, 25:177-181.
36. Obeid M., Tesniere A., Ghiringhelli F., Fimia G.M., Apetoh L., Perfettini J.L., Castedo M., Mignot G., Panaretakis T., Casares N., et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 2007, 13:54-61.
37. Oka T., Hikoso S., Yamaguchi O., Taneike M., Takeda T., Tamai T., Oyabu J., Murakawa T., Nakayama H., Nishida K., et al. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 2012, 485:251-255.
38. Pagès F., Kirilovsky A., Mlecnik B., Asslaber M., Tosolini M., Bindea G., Lagorce C., Wind P., Marliot F., Bruneval P., et al. In situ cytotoxic and memory Tcells predict outcome in patients with early-stage colorectal cancer. J.Clin. Oncol. 2009, 27:5944-5951.
39. Sancho D., Joffre O.P., Keller A.M., Rogers N.C., Martínez D., Hernanz-Falcón P., Rosewell I., Reis Sousa C. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 2009, 458:899-903.
40. Sharma S., DeOliveira R.B., Kalantari P., Parroche P., Goutagny N., Jiang Z., Chan J., Bartholomeu D.C., Lauw F., Hall J.P., et al. Innate immune recognition of an AT-rich stem-loop DNA motif in the Plasmodium falciparum genome. Immunity 2011, 35:194-207.
41. Spranger S., Spaapen R.M., Zha Y., Williams J., Meng Y., Ha T.T., Gajewski T.F. Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) Tcells. Sci Transl Med 2013, 5:200ra116.
42. Spranger S., Koblish H.K., Horton B., Scherle P.A., Newton R., Gajewski T.F. Mechanism of tumor rejection with doublets of CTLA-4, PD-1/PD-L1, or IDO blockade involves restored IL-2 production and proliferation of CD8(+) Tcells directly within the tumor microenvironment. Journal for immunotherapy of cancer 2014, 2:3.
43. Stetson D.B., Medzhitov R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 2006, 24:93-103.
44. Sun L., Wu J., Du F., Chen X., Chen Z.J. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 2013, 339:786-791.
45. Takaoka A., Wang Z., Choi M.K., Yanai H., Negishi H., Ban T., Lu Y., Miyagishi M., Kodama T., Honda K., et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007, 448:501-505.
46. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., Powderly J.D., Carvajal R.D., Sosman J.A., Atkins M.B., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N.Engl. J. Med. 2012, 366:2443-2454.
47. Twitty C.G., Jensen S.M., Hu H.M., Fox B.A. Tumor-derived autophagosome vaccine: induction of cross-protective immune responses against short-lived proteins through a p62-dependent mechanism. Clin. Cancer Res. 2011, 17:6467-6481.
48. Unterholzner L., Keating S.E., Baran M., Horan K.A., Jensen S.B., Sharma S., Sirois C.M., Jin T., Latz E., Xiao T.S., et al. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 2010, 11:997-1004.
49. Wu J., Sun L., Chen X., Du F., Shi H., Chen C., Chen Z.J. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 2013, 339:826-830.
50. Yanai H., Ban T., Wang Z., Choi M.K., Kawamura T., Negishi H., Nakasato M., Lu Y., Hangai S., Koshiba R., et al. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 2009, 462:99-103.
51. Zhou S., Kurt-Jones E.A., Cerny A.M., Chan M., Bronson R.T., Finberg R.W. MyD88 intrinsically regulates CD4 T-cell responses. J.Virol. 2009, 83:1625-1634.