cGAS and Ifi204 cooperate to produce type I IFNs in response to Francisella infection

Journal of Immunology

Volumn 194, Issue 7, 2015, Pages 3236-3245

  Storek, Kelly M ^a   Gertsvolf, Nina A ^a   Ohlson, Maikke B ^b   Monack, Denise M ^a  

^a STANFORD UNIVERSITY   (United States)

^b GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; CELL DNA; CELL PROTEIN; CYCLIC GMP; CYCLIC GMP AMP SYNTHASE; DOUBLE STRANDED DNA; IFI204 PROTEIN; INFLAMMASOME; INTERFERON; INTERFERON REGULATORY FACTOR 3; LIGAND; MELANOMA 2 INFLAMMASOME; PROTEIN STING; SYNTHETASE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; DNA; IFI16 PROTEIN, MOUSE; MB21D1 PROTEIN, MOUSE; MEMBRANE PROTEIN; MPYS PROTEIN, MOUSE; NUCLEAR PROTEIN; NUCLEOTIDYLTRANSFERASE; PHOSPHOPROTEIN; PROTEIN BINDING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; CELL IMMORTALIZATION; CELL LINE; CELL LINE RAW264 7; CGAS GENE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSOL; ENZYME ACTIVITY; FRANCISELLA NOVICIDA; GENE INACTIVATION; GRAM NEGATIVE INFECTION; HOST CELL; HOST PATHOGEN INTERACTION; IFI204 GENE; IMMUNE RESPONSE; IMMUNOSTIMULATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; STING GENE; ANIMAL; BONE MARROW CELL; DEFICIENCY; DISEASE MODEL; FRANCISELLA; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MORTALITY; RNA INTERFERENCE; TRANSGENIC MOUSE;

ANIMALS; BONE MARROW CELLS; CELL LINE; CYTOSOL; DISEASE MODELS, ANIMAL; DNA; FRANCISELLA; GENE EXPRESSION; GENE EXPRESSION REGULATION; GRAM-NEGATIVE BACTERIAL INFECTIONS; INFLAMMASOMES; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; NUCLEAR PROTEINS; NUCLEOTIDYLTRANSFERASES; PHOSPHOPROTEINS; PROTEIN BINDING; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84925841637     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402764     Document Type: Article

References (57)

1. Vance, R. E., R. R. Isberg, and D. A. Portnoy. 2009. Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6: 10-21.
2. Hardy, M. P., C. M. Owczarek, L. S. Jermiin, M. Ejdebäck, and P. J. Hertzog. 2004. Characterization of the type I interferon locus and identification of novel genes. Genomics 84: 331-345.
3. Stetson, D. B., and R. Medzhitov. 2006. Type I interferons in host defense. Immunity 25: 373-381.
4. Perry, A. K., G. Chen, D. Zheng, H. Tang, and G. Cheng. 2005. The host type I interferon response to viral and bacterial infections. Cell Res. 15: 407-422.
5. Barker, J. R., B. J. Koestler, V. K. Carpenter, D. L. Burdette, C. M. Waters, R. E. Vance, and R. H. Valdivia. 2013. STING-dependent recognition of cyclic di-AMP mediates type I interferon responses during Chlamydia trachomatis infection. MBio 4: e00018-e13.
6. Trinchieri, G. 2010. Type I interferon: friend or foe? J. Exp. Med. 207: 2053-2063.
7. Wu, J., and Z. J. Chen. 2014. Innate immune sensing and signaling of cytosolic nucleic acids. Annu. Rev. Immunol. 32: 461-488.
8. Zhang, X., H. Shi, J. Wu, X. Zhang, L. Sun, C. Chen, and Z. J. Chen. 2013. Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol. Cell 51: 226-235.
9. Tanaka, Y., and Z. J. Chen. 2012. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci. Signal. 5: ra20.
10. Sun, L., J. Wu, F. Du, X. Chen, and Z. J. Chen. 2013. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339: 786-791.
11. Woodward, J. J., A. T. Iavarone, and D. A. Portnoy. 2010. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328: 1703-1705.
12. Takaoka, A., Z. Wang, M. K. Choi, H. Yanai, H. Negishi, T. Ban, Y. Lu, M. Miyagishi, T. Kodama, K. Honda, et al. 2007. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448: 501-505.
13. 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.
14. Yang, P., H. An, X. Liu, M. Wen, Y. Zheng, Y. Rui, and X. Cao. 2010. The cytosolic nucleic acid sensor LRRFIP1 mediates the production of type I interferon via a beta-catenin-dependent pathway. Nat. Immunol. 11: 487-494.
15. Kondo, T., J. Kobayashi, T. Saitoh, K. Maruyama, K. J. Ishii, G. N. Barber, K. Komatsu, S. Akira, and T. Kawai. 2013. DNA damage sensor MRE11 recognizes cytosolic double-stranded DNA and induces type I interferon by regulating STING trafficking. Proc. Natl. Acad. Sci. USA 110: 2969-2974.
16. Zhang, X., T. W. Brann, M. Zhou, J. Yang, R. M. Oguariri, K. B. Lidie, H. Imamichi, D. W. Huang, R. A. Lempicki, M. W. Baseler, et al. 2011. Cutting edge: Ku70 is a novel cytosolic DNA sensor that induces type III rather than type I IFN. J. Immunol. 186: 4541-4545.
17. 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.
18. Jones, C. L., B. A. Napier, T. R. Sampson, A. C. Llewellyn, M. R. Schroeder, and D. S. Weiss. 2012. Subversion of host recognition and defense systems by Francisella spp. Microbiol. Mol. Biol. Rev. 76: 383-404.
19. Chong, A., T. D. Wehrly, V. Nair, E. R. Fischer, J. R. Barker, K. E. Klose, and J. Celli. 2008. The early phagosomal stage of Francisella tularensis determines optimal phagosomal escape and Francisella pathogenicity island protein expression. Infect. Immun. 76: 5488-5499.
20. Henry, T., A. Brotcke, D. S. Weiss, L. J. Thompson, and D. M. Monack. 2007. Type I interferon signaling is required for activation of the inflammasome during Francisella infection. J. Exp. Med. 204: 987-994.
21. Mariathasan, S., D. S. Weiss, V. M. Dixit, and D. M. Monack. 2005. Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J. Exp. Med. 202: 1043-1049.
22. Jin, L., K. K. Hill, H. Filak, J. Mogan, H. Knowles, B. Zhang, A. L. Perraud, J. C. Cambier, and L. L. Lenz. 2011. MPYS is required for IFN response factor 3 activation and type I IFN production in the response of cultured phagocytes to bacterial second messengers cyclic-di-AMP and cyclic-di-GMP. J. Immunol. 187: 2595-2601.
23. Jones, J. W., N. Kayagaki, P. Broz, T. Henry, K. Newton, K. O'Rourke, S. Chan, J. Dong, Y. Qu, M. Roose-Girma, et al. 2010. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc. Natl. Acad. Sci. USA 107: 9771-9776.
24. Fernandes-Alnemri, T., J. W. Yu, P. Datta, J. Wu, and E. S. Alnemri. 2009. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458: 509-513.
25. 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.
26. Bürckstümmer, T., C. Baumann, S. Blüml, E. Dixit, G. Dürnberger, H. Jahn, M. Planyavsky, M. Bilban, J. Colinge, K. L. Bennett, and G. Superti-Furga. 2009. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10: 266-272.
27. Landolfo, S., M. Gariglio, G. Gribaudo, and D. Lembo. 1998. The Ifi 200 genes: an emerging family of IFN-inducible genes. Biochimie 80: 721-728.
28. Weiss, D. S., A. Brotcke, T. Henry, J. J. Margolis, K. Chan, and D. M. Monack. 2007. In vivo negative selection screen identifies genes required for Francisella virulence. Proc. Natl. Acad. Sci. USA 104: 6037-6042.
29. Peng, K., P. Broz, J. Jones, L. M. Joubert, and D. Monack. 2011. Elevated AIM2-mediated pyroptosis triggered by hypercytotoxic Francisella mutant strains is attributed to increased intracellular bacteriolysis. Cell. Microbiol. 13: 1586-1600.
30. 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.
31. 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.
32. Mali, P., L. Yang, K. M. Esvelt, J. Aach, M. Guell, J. E. DiCarlo, J. E. Norville, and G. M. Church. 2013. RNA-guided human genome engineering via Cas9. Science 339: 823-826.
33. Broz, P., K. Newton, M. Lamkanfi, S. Mariathasan, V. M. Dixit, and D. M. Monack. 2010. Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J. Exp. Med. 207: 1745-1755.
34. Schoggins, J. W., D. A. MacDuff, N. Imanaka, M. D. Gainey, B. Shrestha, J. L. Eitson, K. B. Mar, R. B. Richardson, A. V. Ratushny, V. Litvak, et al. 2014. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505: 691-695.
35. Broz, P., J. von Moltke, J. W. Jones, R. E. Vance, and D. M. Monack. 2010. Differential requirement for Caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe 8: 471-483.
36. Jiang, Z., P. Georgel, X. Du, L. Shamel, S. Sovath, S. Mudd, M. Huber, C. Kalis, S. Keck, C. Galanos, et al. 2005. CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 6: 565-570.
37. Stetson, D. B., and R. Medzhitov. 2006. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24: 93-103.
38. Sato, M., H. Suemori, N. Hata, M. Asagiri, K. Ogasawara, K. Nakao, T. Nakaya, M. Katsuki, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13: 539-548.
39. Daffis, S., M. S. Suthar, K. J. Szretter, M. Gale, Jr., and M. S. Diamond. 2009. Induction of IFN-beta and the innate antiviral response in myeloid cells occurs through an IPS-1-dependent signal that does not require IRF-3 and IRF-7. PLoS Pathog. 5: e1000607.
40. 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.
41. Schmerk, C. L., B. N. Duplantis, P. L. Howard, and F. E. Nano. 2009. A Francisella novicida pdpA mutant exhibits limited intracellular replication and remains associated with the lysosomal marker LAMP-1. Microbiology 155: 1498-1504.
42. Bryan, N. B., A. Dorfleutner, S. J. Kramer, C. Yun, Y. Rojanasakul, and C. Stehlik. 2010. Differential splicing of the apoptosis-associated speck like protein containing a caspase recruitment domain (ASC) regulates inflammasomes. J. Inflamm. (Lond.) 7: 23.
43. Pelegrin, P., C. Barroso-Gutierrez, and A. Surprenant. 2008. P2X7 receptor differentially couples to distinct release pathways for IL-1beta in mouse macrophage. J. Immunol. 180: 7147-7157.
44. Uematsu, S., and S. Akira. 2007. Toll-like receptors and Type I interferons. J. Biol. Chem. 282: 15319-15323.
45. Yoneyama, M., M. Kikuchi, K. Matsumoto, T. Imaizumi, M. Miyagishi, K. Taira, E. Foy, Y. M. Loo, M. Gale, Jr., S. Akira, et al. 2005. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175: 2851-2858.
46. Ishikawa, H., Z. Ma, and G. N. Barber. 2009. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461: 788-792.
47. Stetson, D. B., J. S. Ko, T. Heidmann, and R. Medzhitov. 2008. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134: 587-598.
48. Volkman, H. E., and D. B. Stetson. 2014. The enemy within: endogenous retroelements and autoimmune disease. Nat. Immunol. 15: 415-422.
49. Brunette, R. L., J. M. Young, D. G. Whitley, I. E. Brodsky, H. S. Malik, and D. B. Stetson. 2012. Extensive evolutionary and functional diversity among mammalian AIM2-like receptors. J. Exp. Med. 209: 1969-1983.
50. Stanley, S. A., J. E. Johndrow, P. Manzanillo, and J. S. Cox. 2007. The Type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J. Immunol. 178: 3143-3152.
51. Auerbuch, V., D. G. Brockstedt, N. Meyer-Morse, M. O'Riordan, and D. A. Portnoy. 2004. Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J. Exp. Med. 200: 527-533.
52. Henry, T., G. S. Kirimanjeswara, T. Ruby, J. W. Jones, K. Peng, M. Perret, L. Ho, J. D. Sauer, Y. Iwakura, D. W. Metzger, and D. M. Monack. 2010. Type I IFN signaling constrains IL-17A/F secretion by gammadelta T cells during bacterial infections. J. Immunol. 184: 3755-3767.
53. Hiscott, J. 2007. Triggering the innate antiviral response through IRF-3 activation. J. Biol. Chem. 282: 15325-15329.
54. Li, X. D., J. Wu, D. Gao, H. Wang, L. Sun, and Z. J. Chen. 2013. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341: 1390-1394.
55. Ablasser, A., I. Hemmerling, J. L. Schmid-Burgk, R. Behrendt, A. Roers, and V. Hornung. 2014. TREX1 deficiency triggers cell-autonomous immunity in a cGAS-dependent manner. J. Immunol. 192: 5993-5997.
56. Manzanillo, P. S., M. U. Shiloh, D. A. Portnoy, and J. S. Cox. 2012. Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11: 469-480.
57. Hansen, K., T. Prabakaran, A. Laustsen, S. E. Jørgensen, S. H. Rahbæk, S. B. Jensen, R. Nielsen, J. H. Leber, T. Decker, K. A. Horan, et al. 2014. Listeria monocytogenes induces IFNβ expression through an IFI16-, cGAS- and STING-dependent pathway. EMBO J. 33: 1654-1666.