Mouse, but not human sting, binds and signals in response to the vascular disrupting agent 5,6-dimethylxanthenone-4-acetic acid

Journal of Immunology

Volumn 190, Issue 10, 2013, Pages 5216-5225

  Conlon, Joseph ^a   Burdette, Dara L ^b   Sharma, Shruti ^a   Bhat, Numana ^a   Thompson, Mikayla ^a   Jiang, Zhaozhao ^a   Rathinam, Vijay A K ^a   Monks, Brian ^a   Jin, Tengchuan ^c   Xiao, T Sam ^c   Vogel, Stefanie N ^d   Vance, Russell E ^b   Fitzgerald, Katherine A ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; DINUCLEOTIDE; INTERFERON REGULATORY FACTOR 3; PHOSPHOTRANSFERASE; STING PROTEIN; TANK BINDING KINASE 1; UNCLASSIFIED DRUG; VADIMEZAN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG PROTEIN BINDING; EMBRYO; HUMAN; HUMAN CELL; IN VITRO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; SECOND MESSENGER; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE; HEK293 CELLS; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; LEUKOCYTES, MONONUCLEAR; MACROPHAGES; MEMBRANE PROTEINS; MICE; NEOPLASMS; NF-KAPPA B; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; XANTHONES;

EID: 84877795529     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300097     Document Type: Article

References (58)

1. Rakoff-Nahoum, S., and R. Medzhitov. 2008. Role of Toll-like receptors in tissue repair and tumorigenesis. Biochemistry (Mosc.) 73: 555-561. (Pubitemid 351775078)
2. Rakoff-Nahoum, S., and R. Medzhitov. 2009. Toll-like receptors and cancer. Nat. Rev. Cancer 9: 57-63.
3. Baguley, B. C., and L. M. Ching. 1997. Immunomodulatory actions of xanthenone anticancer agents. BioDrugs 8: 119-127. (Pubitemid 27316546)
4. Wallace, A., D. F. LaRosa, V. Kapoor, J. Sun, G. Cheng, A. Jassar, A. Blouin, L. M. Ching, and S. M. Albelda. 2007. The vascular disrupting agent, DMXAA, directly activates dendritic cells through a MyD88-independent mechanism and generates antitumor cytotoxic T lymphocytes. Cancer Res. 67: 7011-7019. (Pubitemid 47105550)
5. + T-cellmediated antitumor immune response in murine models of lung cancer and mesothelioma. Cancer Res. 65: 11752-11761. (Pubitemid 41821737)
6. Roberts, Z. J., N. Goutagny, P. Y. Perera, H. Kato, H. Kumar, T. Kawai, S. Akira, R. Savan, D. van Echo, K. A. Fitzgerald, et al. 2007. The chemotherapeutic agent DMXAA potently and specifically activates the TBK1-IRF-3 signaling axis. J. Exp. Med. 204: 1559-1569. (Pubitemid 47049627)
7. Perera, P. Y., S. A. Barber, L. M. Ching, and S. N. Vogel. 1994. Activation of LPS-inducible genes by the antitumor agent 5,6-dimethylxanthenone- 4-Acetic acid in primary murine macrophages: dissection of signaling pathways leading to gene induction and tyrosine phosphorylation. J. Immunol. 153: 4684-4693.
8. Head, M., and M. B. Jameson. 2010. The development of the tumor vasculardisrupting agent ASA404 (vadimezan, DMXAA): current status and future opportunities. Expert Opin. Investig. Drugs 19: 295-304.
9. Roberts, Z. J., L. M. Ching, and S. N. Vogel. 2008. IFN-b-dependent inhibition of tumor growth by the vascular disrupting agent 5,6- dimethylxanthenone-4-Acetic acid (DMXAA). J. Interferon Cytokine Res. 28: 133-139. (Pubitemid 351380153)
10. McKeage, M. J., M. Reck, M. B. Jameson, M. A. Rosenthal, D. Gibbs, P. N. Mainwaring, L. Freitag, R. Sullivan, and J. Von Pawel. 2009. Phase II study of ASA404 (vadimezan, 5,6-dimethylxanthenone-4-Acetic acid/DMXAA) 1800mg/m (2) combined with carboplatin and paclitaxel in previously untreated advanced nonsmall cell lung cancer. Lung Cancer 65: 192-197.
11. McKeage, M. J. 2008. The potential of DMXAA (ASA404) in combination with docetaxel in advanced prostate cancer. Expert Opin. Investig. Drugs 17: 23-29. (Pubitemid 351578208)
12. Sun, J., L. C. Wang, Z. G. Fridlender, V. Kapoor, G. Cheng, L. M. Ching, and S. M. Albelda. 2011. Activation of mitogen-Activated protein kinases by 5,6-dimethylxanthenone-4-Acetic acid (DMXAA) plays an important role in macrophage stimulation. Biochem. Pharmacol. 82: 1175-1185.
13. Wang, L. C., L. Thomsen, R. Sutherland, C. B. Reddy, S. M. Tijono, C. J. Chen, C. E. Angel, P. R. Dunbar, and L. M. Ching. 2009. Neutrophil influx and chemokine production during the early phases of the antitumor response to the vascular disrupting agent DMXAA (ASA404). Neoplasia 11: 793-803.
14. Woon, S. T., S. S. Hung, D. C. Wu, M. A. Schooltink, R. Sutherland, B. C. Baguley, Q. Chen, L. W. Chamley, and L. M. Ching. 2007. NFkB-independent induction of endothelial cell apoptosis by the vascular disrupting agent DMXAA. Anticancer Res. 27(1A): 327-334. (Pubitemid 46363350)
15. Wang, L. C., S. T. Woon, B. C. Baguley, and L. M. Ching. 2006. Inhibition of DMXAA-induced tumor necrosis factor production in murine splenocyte cultures by NF-kB inhibitors. Oncol. Res. 16: 1-14. (Pubitemid 44195045)
16. Woon, S. T., C. B. Reddy, C. J. Drummond, M. A. Schooltink, B. C. Baguley, C. Kieda, and L. M. Ching. 2005. A comparison of the ability of DMXAA and xanthenone analogues to activate NF-kB in murine and human cell lines. Oncol. Res. 15: 351-364. (Pubitemid 43198592)
17. Fitzgerald, K. A., S. M. McWhirter, K. L. Faia, D. C. Rowe, E. Latz, D. T. Golenbock, A. J. Coyle, S. M. Liao, and T. Maniatis. 2003. IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4: 491-496. (Pubitemid 36592443)
18. McWhirter, S. M., K. A. Fitzgerald, J. Rosains, D. C. Rowe, D. T. Golenbock, and T. Maniatis. 2004. IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc. Natl. Acad. Sci. USA 101: 233-238. (Pubitemid 38084233)
19. Sharma, S., B. R. tenOever, N. Grandvaux, G. P. Zhou, R. Lin, and J. Hiscott. 2003. Triggering the interferon antiviral response through an IKK-related pathway. Science 300: 1148-1151. (Pubitemid 36583100)
20. Uematsu, S., and S. Akira. 2004. [TLR family and viral infection]. Uirusu 54: 145-151.
21. Akira, S., T. Saitoh, and T. Kawai. 2012. [Nucleic acids recognition by innate immunity]. Uirusu 62: 39-45.
22. Zhang, Z., B. Yuan, M. Bao, N. Lu, T. Kim, and Y. J. Liu. 2011. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat. Immunol. 12: 959-965.
23. Unterholzner, L., S. E. Keating, M. Baran, K. A. Horan, S. B. Jensen, S. Sharma, C. M. Sirois, T. Jin, E. Latz, T. S. Xiao, et al. 2010. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11: 997-1004.
24. Roberts, T. L., A. Idris, J. A. Dunn, G. M. Kelly, C. M. Burnton, S. Hodgson, L. L. Hardy, V. Garceau, M. J. Sweet, I. L. Ross, et al. 2009. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323: 1057-1060.
25. Rathinam, V. A., Z. Jiang, S. N. Waggoner, S. Sharma, L. E. Cole, L. Waggoner, S. K. Vanaja, B. G. Monks, S. Ganesan, E. Latz, et al. 2010. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11: 395-402.
26. Hornung, V., A. Ablasser, M. Charrel-Dennis, F. Bauernfeind, G. Horvath, D. R. Caffrey, E. Latz, and K. A. Fitzgerald. 2009. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-Activating inflammasome with ASC. Nature 458: 514-518.
27. Chiu, Y. H., J. B. Macmillan, and Z. J. Chen. 2009. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138: 576-591.
28. Ablasser, A., F. Bauernfeind, G. Hartmann, E. Latz, K. A. Fitzgerald, and V. Hornung. 2009. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 10: 1065-1072.
29. Barber, G. N. 2011. STING-dependent signaling. Nat. Immunol. 12: 929-930.
30. Ishikawa, H., and G. N. Barber. 2011. The STING pathway and regulation of innate immune signaling in response to DNA pathogens. Cell. Mol. Life Sci. 68: 1157-1165.
31. Ishikawa, H., Z. Ma, and G. N. Barber. 2009. STING regulates intracellular DNAmediated, type I interferon-dependent innate immunity. Nature 461: 788-792.
32. Ishikawa, H., and G. N. Barber. 2008. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455: 674-678.
33. Burdette, D. L., K. M. Monroe, K. Sotelo-Troha, J. S. Iwig, B. Eckert, M. Hyodo, Y. Hayakawa, and R. E. Vance. 2011. STING is a direct innate immune sensor of cyclic di-GMP. Nature 478: 515-518.
34. Prantner, D., D. J. Perkins, W. Lai, M. S. Williams, S. Sharma, K. A. Fitzgerald, and S. N. Vogel. 2012. 5,6-Dimethylxanthenone-4-Acetic acid (DMXAA) activates stimulator of interferon gene (STING)-dependent innate immune pathways and is regulated by mitochondrial membrane potential. J. Biol. Chem. 287: 39776-39788.
35. Hornung, V., F. Bauernfeind, A. Halle, E. O. Samstad, H. Kono, K. L. Rock, K. A. Fitzgerald, and E. Latz. 2008. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9: 847-856.
36. Rothenfusser, S., N. Goutagny, G. DiPerna, M. Gong, B. G. Monks, A. Schoenemeyer, M. Yamamoto, S. Akira, and K. A. Fitzgerald. 2005. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 175: 5260-5268. (Pubitemid 41456411)
37. Parvatiyar, K., Z. Zhang, R. M. Teles, S. Ouyang, Y. Jiang, S. S. Iyer, S. A. Zaver, M. Schenk, S. Zeng, W. Zhong, et al. 2012. The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat. Immunol. 13: 1155-1161.
38. Shu, C., G. Yi, T. Watts, C. C. Kao, and P. Li. 2012. Structure of STING bound to cyclic di-GMP reveals the mechanism of cyclic dinucleotide recognition by the immune system. Nat. Struct. Mol. Biol. 19: 722-724.
39. Shang, G., D. Zhu, N. Li, J. Zhang, C. Zhu, D. Lu, C. Liu, Q. Yu, Y. Zhao, S. Xu, and L. Gu. 2012. Crystal structures of STING protein reveal basis for recognition of cyclic di-GMP. Nat. Struct. Mol. Biol. 19: 725-727.
40. Ouyang, S., X. Song, Y. Wang, H. Ru, N. Shaw, Y. Jiang, F. Niu, Y. Zhu, W. Qiu, K. Parvatiyar, et al. 2012. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 36: 1073-1086.
41. Huang, Y. H., X. Y. Liu, X. X. Du, Z. F. Jiang, and X. D. Su. 2012. The structural basis for the sensing and binding of cyclic di-GMP by STING. Nat. Struct. Mol. Biol. 19: 728-730.
42. Smith, G. P., S. B. Calveley, M. J. Smith, and B. C. Baguley. 1987. Flavone acetic acid (NSC 347512) induces haemorrhagic necrosis of mouse colon 26 and 38 tumours. Eur. J. Cancer Clin. Oncol. 23: 1209-1211. (Pubitemid 17112486)
43. Jameson, M. B., P. I. Thompson, B. C. Baguley, B. D. Evans, V. J. Harvey, D. J. Porter, M. R. McCrystal, M. Small, K. Bellenger, L. Gumbrell, et al. 2003. Clinical aspects of a phase I trial of 5,6-dimethylxanthenone-4-Acetic acid (DMXAA), a novel antivascular agent. Br. J. Cancer 88: 1844-1850. (Pubitemid 36829657)
44. Baguley, B. C. 2003. Antivascular therapy of cancer: DMXAA. Lancet Oncol. 4: 141-148. (Pubitemid 36322304)
45. Philpott, M., B. C. Baguley, and L. M. Ching. 1995. Induction of tumour necrosis factor-A by single and repeated doses of the antitumour agent 5,6-dimethylxanthenone-4-Acetic acid. Cancer Chemother. Pharmacol. 36: 143-148.
46. Ching, L. M., D. Goldsmith, W. R. Joseph, H. Korner, J. D. Sedgwick, and B. C. Baguley. 1999. Induction of intratumoral tumor necrosis factor (TNF) synthesis and hemorrhagic necrosis by 5,6-dimethylxanthenone-4-Acetic acid (DMXAA) in TNF knockout mice. Cancer Res. 59: 3304-3307. (Pubitemid 29334480)
47. Ching, L. M., H. A. Young, K. Eberly, and C. R. Yu. 1999. Induction of STAT and NFkB activation by the antitumor agents 5,6-dimethylxanthenone-4-Acetic acid and flavone acetic acid in a murine macrophage cell line. Biochem. Pharmacol. 58: 1173-1181. (Pubitemid 29381518)
48. Gresser, I., F. Belardelli, C. Maury, M. T. Maunoury, and M. G. Tovey. 1983. Injection of mice with antibody to interferon enhances the growth of transplantable murine tumors. J. Exp. Med. 158: 2095-2107.
49. Dunn, G. P., C. M. Koebel, and R. D. Schreiber. 2006. Interferons, immunity and cancer immunoediting. Nat. Rev. Immunol. 6: 836-848. (Pubitemid 44631652)
50. Mantovani, A., T. Schioppa, C. Porta, P. Allavena, and A. Sica. 2006. Role of tumor-Associated macrophages in tumor progression and invasion. Cancer Metastasis Rev. 25: 315-322. (Pubitemid 44922352)
51. Diamond, M. S., M. Kinder, H. Matsushita, M. Mashayekhi, G. P. Dunn, J. M. Archambault, H. Lee, C. D. Arthur, J. M. White, U. Kalinke, et al. 2011. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J. Exp. Med. 208: 1989-2003.
52. Fuertes, M. B., S. R. Woo, B. Burnett, Y. X. Fu, and T. F. Gajewski. 2012. Type I interferon response and innate immune sensing of cancer. Trends Immunol. 34: 67-73
53. Dinney, C. P., D. R. Bielenberg, P. Perrotte, R. Reich, B. Y. Eve, C. D. Bucana, and I. J. Fidler. 1998. Inhibition of basic fibroblast growth factor expression, angiogenesis, and growth of human bladder carcinoma in mice by systemic interferon-A administration. Cancer Res. 58: 808-814. (Pubitemid 28099496)
54. Singh, R. K., M. Gutman, C. D. Bucana, R. Sanchez, N. Llansa, and I. J. Fidler. 1995. Interferons a and b down-regulate the expression of basic fibroblast growth factor in human carcinomas. Proc. Natl. Acad. Sci. USA 92: 4562-4566.
55. Strieter, R. M., P. J. Polverini, D. A. Arenberg, A. Walz, G. Opdenakker, J. Van Damme, and S. L. Kunkel. 1995. Role of C-X-C chemokines as regulators of angiogenesis in lung cancer. J. Leukoc. Biol. 57: 752-762.
56. Sauer, J. D., K. Sotelo-Troha, J. von Moltke, K. M. Monroe, C. S. Rae, S. W. Brubaker, M. Hyodo, Y. Hayakawa, J. J. Woodward, D. A. Portnoy, and R. E. Vance. 2011. The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect. Immun. 79: 688-694.
57. Tanaka, Y., and Z. J. Chen. 2012. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci. Signal. 5: ra20.
58. Yin, Q., Y. Tian, V. Kabaleeswaran, X. Jiang, D. Tu, M. J. Eck, Z. J. Chen, and H. Wu. 2012. Cyclic di-GMP sensing via the innate immune signaling protein STING. Mol. Cell 46: 735-745.