Activation of STING-dependent innate immune signaling by s-phase-specific DNA damage in breast cancer

Journal of the National Cancer Institute

Volumn 109, Issue 1, 2017, Pages

  Parkes, Eileen E ^a   Walker, Steven M ^a,b   Taggart, Laura E ^a,b   McCabe, Nuala ^a,b   Knight, Laura A ^a   Wilkinson, Richard ^a   McCloskey, Karen D ^a   Buckley, Niamh E ^a   Savage, Kienan I ^a   Salto Tellez, Manuel ^a   McQuaid, Stephen ^a   Harte, Mary T ^a,b   Mullan, Paul B ^a   Harkin, D Paul ^a,b   Kennedy, Richard D ^a,b  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b Almac Sciences   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; DNA; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON REGULATORY FACTOR 3; PEPTIDES AND PROTEINS; PROGRAMMED DEATH 1 LIGAND 1; RANTES; STING PROTEIN; UNCLASSIFIED DRUG; CD274 PROTEIN, HUMAN; CONDITIONED MEDIUM; IRF3 PROTEIN, HUMAN; MEMBRANE PROTEIN; MPYS PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; TBK1 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CYCLE S PHASE; CELL MIGRATION; CONDITIONED MEDIUM; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOSOL; DNA DAMAGE RESPONSE; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; BREAST TUMOR; CHEMISTRY; CHEMOTAXIS; DNA DAMAGE; DRUG EFFECTS; GENETICS; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; PHARMACOLOGY; PHYSIOLOGY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL LINE;

ANTIGENS, CD274; BREAST NEOPLASMS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CHEMOKINE CCL5; CHEMOKINE CXCL10; CHEMOTAXIS; CULTURE MEDIA, CONDITIONED; CYTOSOL; DNA; DNA DAMAGE; FEMALE; HUMANS; IMMUNITY, INNATE; IMMUNOHISTOCHEMISTRY; INTERFERON REGULATORY FACTOR-3; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTES, TUMOR-INFILTRATING; MEMBRANE PROTEINS; PROTEIN-SERINE-THREONINE KINASES; S PHASE; SIGNAL TRANSDUCTION;

EID: 85014839385     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djw199     Document Type: Article

References (28)

1. Loi S, Sirtaine N, Piette F, et al. Prognostic and predictive value of tumorinfiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02-98. J Clin Oncol. 2013;31(7):860-867.
2. Denkert C, Loibl S, Noske A, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol. 2010;28(1):105-113.
3. Woo SR, Corrales L, Gajewski TF. Innate immune recognition of cancer. Annu Rev Immunol. 2015;33:445-474.
4. Mulligan JM, Hill LA, Deharo S, et al. Identification and validation of an anthracycline/cyclophosphamide-based chemotherapy response assay in breast cancer. J Natl Cancer Inst. 2014;106(1):djt335. doi: 10.1093/jnci/djt335.
5. Quinn JE, Kennedy RD, Mullan PB, et al. BRCA1 functions as a differential modulator of chemotherapy-induced apoptosis. Cancer Res. 2003;63(19): 6221-6228.
6. Soria J, Gettinger S, Gordon MS, et al. Biomarkers associated with clinical activity of PD-L1 blockade in non-small cell lung carcinoma (NSCLC) patients (pts) in a phase I study of MPDL3280A. Ann Oncol. 2014;25(suppl 4):iv426, Abstract 1322 P.
7. Jenh CH, Cox MA, Cui L, et al. A selective and potent CXCR3 antagonist SCH 546738 attenuates the development of autoimmune diseases and delays graft rejection. BMC Immunol. 2012;13:2-2172-13-2.
8. Mulligan AM, Raitman I, Feeley L, et al. Tumoral lymphocytic infiltration and expression of the chemokine CXCL10 in breast cancers from the Ontario familial breast cancer registry. Clin Cancer Res. 2013;19(2):336-346.
9. Groom JR, Luster AD. CXCR3 in T cell function. Exp Cell Res. 2011;317(5): 620-631.
10. Kunz M, Toksoy A, Goebeler M, Engelhardt E, Brocker E, Gillitzer R. Strong expression of the lymphoattractant C-X-C chemokine mig is associated with heavy infiltration of T cells in human malignant melanoma. J Pathol. 1999; 189(4):552-558.
11. Ohtani H, Jin Z, Takegawa S, Nakayama T, Yoshie O. Abundant expression of CXCL9 (MIG) by stromal cells that include dendritic cells and accumulation of CXCR3 T cells in lymphocyte-rich gastric carcinoma. J Pathol. 2009;217(1): 21-31.
12. Muthuswamy R, Berk E, Junecko BF, et al. NF-kappaB hyperactivation in tumor tissues allows tumor-selective reprogramming of the chemokine microenvironment to enhance the recruitment of cytolytic T effector cells. Cancer Res. 2012;72(15):3735-3743.
13. Brzostek-Racine S, Gordon C, Van Scoy S, Reich NC. The DNA damage response induces IFN. J Immunol. 2011;187(10):5336-5345.
14. Kim T, Kim TY, Song YH, Min IM, Yim J, Kim TK. Activation of interferon regulatory factor 3 in response to DNA-damaging agents. J Biol Chem. 1999;274(43): 30686-30689.
15. Motani K, Ito S, Nagata S. DNA-mediated cyclic GMP-AMP synthasedependent and-independent regulation of innate immune responses. J Immunol. 2015;194(10):4914-4923.
16. Woo SR, Fuertes MB, Corrales L, et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity. 2014;41(5):830-842.
17. Ahn J, Xia T, Konno H, Konno K, Ruiz P, Barber GN. Inflammation-driven carcinogenesis is mediated through STING. Nat Commun. 2014;5:5166.
18. Ablasser A, Goldeck M, Cavlar T, et al. cGAS produces a 2'-5'-linked cyclic dinucleotide second messenger that activates STING. Nature. 2013;498(7454): 380-384.
19. Turner N, Tutt A, Ashworth A. Hallmarks of 'BRCAness' in sporadic cancers. Nat Rev Cancer. 2004;4(10):814-819.
20. Lan YY, Londono D, Bouley R, Rooney MS, Hacohen N. Dnase2a deficiency uncovers lysosomal clearance of damaged nuclear DNA via autophagy. Cell Rep. 2014;9(1):180-192.
21. Ahn J, Gutman D, Saijo S, Barber GN. STING manifests self DNA-dependent inflammatory disease. Proc Natl Acad Sci U S A. 2012;109(47):19386-19391.
22. Brahmer JR, Tykodi SS, Chow LQ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 2012;366(26):2455-2465.
23. Le DT, Uram JN, Wang H, et al. PD-1 blockade in tumors with mismatchrepair deficiency. N Engl J Med. 2015;372(26):2509-2520.
24. Svendsen JM, Smogorzewska A, Sowa ME, et al. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell. 2009;138(1):63-77.
25. Corrales L, Glickman LHH, McWhirter SMM, et al. Direct Activation of STING in the Tumor Microenvironment Leads to Potent and Systemic Tumor Regression and Immunity. Cell Rep. 2015;11(7):1018-1030.
26. Yang S, Imamura Y, Jenkins RW, et al. Autophagy Inhibition Dysregulates TBK1 Signaling and Promotes Pancreatic Inflammation. Cancer Immunol Res. 2016;4(6):520-530.
27. Sharpe AH, Wherry EJ, Ahmed R, Freeman GJ. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat Immunol. 2007;8(3):239-245.
28. Fu J, Kanne DB, Leong M, et al. STING agonist formulated cancer vaccines can cure established tumors resistant to PD-1 blockade. Sci Transl Med. 2015; 7(283):283ra52.