The AIM2-like Receptors Are Dispensable for the Interferon Response to Intracellular DNA

Immunity

Volumn 45, Issue 2, 2016, Pages 255-266

  Gray, Elizabeth E ^a   Winship, Damion ^a   Snyder, Jessica M ^a   Child, Stephanie J ^a,b   Geballe, Adam P ^a,b   Stetson, Daniel B ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AIM2 LIKE RECEPTOR PROTEIN; DNA; INTERFERON; INTERLEUKIN 1BETA; PROTEIN; UNCLASSIFIED DRUG; AIM2 PROTEIN, MOUSE; DNA BINDING PROTEIN; EXODEOXYRIBONUCLEASE; IFI16 PROTEIN, HUMAN; MEMBRANE PROTEIN; MPYS PROTEIN, MOUSE; NUCLEAR PROTEIN; PHOSPHOPROTEIN; THREE PRIME REPAIR EXONUCLEASE 1;

AICARDI GOUTIERES SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; DNA VIRUS INFECTION; FIBROBLAST; GENE EXPRESSION; HUMAN CYTOMEGALOVIRUS; HUMAN IMMUNODEFICIENCY VIRUS; LENTIVIRUS INFECTION; MACROPHAGE; MOUSE; MOUSE EMBRYONIC STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; REVERSE TRANSCRIPTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS STRAIN; ANIMAL; C57BL MOUSE; CELL LINE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DISEASE MODEL; GENE LOCUS; GENETICS; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; LENTIVIRINAE; METABOLISM; NERVOUS SYSTEM MALFORMATION; NEUROLOGIC DISEASE;

ANIMALS; AUTOIMMUNE DISEASES OF THE NERVOUS SYSTEM; CELL LINE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DISEASE MODELS, ANIMAL; DNA; DNA-BINDING PROTEINS; EXODEOXYRIBONUCLEASES; GENETIC LOCI; HUMANS; INTERFERON TYPE I; LENTIVIRUS; LENTIVIRUS INFECTIONS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVOUS SYSTEM MALFORMATIONS; NUCLEAR PROTEINS; PHOSPHOPROTEINS;

EID: 84997751528     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.06.015     Document Type: Article

References (55)

1. Abate, D.A., Watanabe, S., Mocarski, E.S., Major human cytomegalovirus structural protein pp65 (ppUL83) prevents interferon response factor 3 activation in the interferon response. J. Virol. 78 (2004), 10995–11006.
2. Browne, E.P., Shenk, T., Human cytomegalovirus UL83-coded pp65 virion protein inhibits antiviral gene expression in infected cells. Proc. Natl. Acad. Sci. USA 100 (2003), 11439–11444.
3. Brunette, R.L., Young, J.M., Whitley, D.G., Brodsky, I.E., Malik, H.S., Stetson, D.B., Extensive evolutionary and functional diversity among mammalian AIM2-like receptors. J. Exp. Med. 209 (2012), 1969–1983.
4. Bürckstümmer, T., Baumann, C., Blüml, S., Dixit, E., Dürnberger, G., Jahn, H., Planyavsky, M., Bilban, M., Colinge, J., Bennett, K.L., Superti-Furga, G., An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10 (2009), 266–272.
5. Cagliani, R., Forni, D., Biasin, M., Comabella, M., Guerini, F.R., Riva, S., Pozzoli, U., Agliardi, C., Caputo, D., Malhotra, S., et al. Ancient and recent selective pressures shaped genetic diversity at AIM2-like nucleic acid sensors. Genome Biol. Evol. 6 (2014), 830–845.
6. Clackson, T., Yang, W., Rozamus, L.W., Hatada, M., Amara, J.F., Rollins, C.T., Stevenson, L.F., Magari, S.R., Wood, S.A., Courage, N.L., et al. Redesigning an FKBP-ligand interface to generate chemical dimerizers with novel specificity. Proc. Natl. Acad. Sci. USA 95 (1998), 10437–10442.
7. Collins, A.C., Cai, H., Li, T., Franco, L.H., Li, X.D., Nair, V.R., Scharn, C.R., Stamm, C.E., Levine, B., Chen, Z.J., Shiloh, M.U., Cyclic GMP-AMP Synthase Is an Innate Immune DNA Sensor for Mycobacterium tuberculosis. Cell Host Microbe 17 (2015), 820–828.
8. Corrales, L., Woo, S.R., Williams, J.B., McWhirter, S.M., Dubensky, T.W. Jr., Gajewski, T.F., Antagonism of the STING Pathway via Activation of the AIM2 Inflammasome by Intracellular DNA. J Immunol, 2016.
9. Cridland, J.A., Curley, E.Z., Wykes, M.N., Schroder, K., Sweet, M.J., Roberts, T.L., Ragan, M.A., Kassahn, K.S., Stacey, K.J., The mammalian PYHIN gene family: phylogeny, evolution and expression. BMC Evol. Biol., 12, 2012, 140.
10. Crow, Y.J., Hayward, B.E., Parmar, R., Robins, P., Leitch, A., Ali, M., Black, D.N., van Bokhoven, H., Brunner, H.G., Hamel, B.C., et al. Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 cause Aicardi-Goutières syndrome at the AGS1 locus. Nat. Genet. 38 (2006), 917–920.
11. Crow, Y.J., Chase, D.S., Lowenstein Schmidt, J., Szynkiewicz, M., Forte, G.M., Gornall, H.L., Oojageer, A., Anderson, B., Pizzino, A., Helman, G., et al. Characterization of human disease phenotypes associated with mutations in TREX1, RNASEH2A, RNASEH2B, RNASEH2C, SAMHD1, ADAR, and IFIH1. Am. J. Med. Genet. A. 167A (2015), 296–312.
12. Fernandes-Alnemri, T., Yu, J.W., Datta, P., Wu, J., Alnemri, E.S., AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458 (2009), 509–513.
13. Fernando, M.M., de Smith, A.J., Coin, L., Morris, D.L., Froguel, P., Mangion, J., Blakemore, A.I., Graham, R.R., Behrens, T.W., Vyse, T.J., Investigation of the HIN200 locus in UK SLE families identifies novel copy number variants. Ann. Hum. Genet. 75 (2011), 383–397.
14. Gall, A., Treuting, P., Elkon, K.B., Loo, Y.M., Gale, M. Jr., Barber, G.N., Stetson, D.B., Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferon-dependent autoimmune disease. Immunity 36 (2012), 120–131.
15. Gao, D., Wu, J., Wu, Y.T., Du, F., Aroh, C., Yan, N., Sun, L., Chen, Z.J., Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341 (2013), 903–906.
16. Gao, D., Li, T., Li, X.D., Chen, X., Li, Q.Z., Wight-Carter, M., Chen, Z.J., Activation of cyclic GMP-AMP synthase by self-DNA causes autoimmune diseases. Proc. Natl. Acad. Sci. USA 112 (2015), E5699–E5705.
17. Gray, E.E., Treuting, P.M., Woodward, J.J., Stetson, D.B., Cutting Edge: cGAS Is Required for Lethal Autoimmune Disease in the Trex1-Deficient Mouse Model of Aicardi-Goutières Syndrome. J. Immunol. 195 (2015), 1939–1943.
18. Haywood, M.E., Rogers, N.J., Rose, S.J., Boyle, J., McDermott, A., Rankin, J.M., Thiruudaian, V., Lewis, M.R., Fossati-Jimack, L., Izui, S., et al. Dissection of BXSB lupus phenotype using mice congenic for chromosome 1 demonstrates that separate intervals direct different aspects of disease. J. Immunol. 173 (2004), 4277–4285.
19. Hornung, V., Ablasser, A., Charrel-Dennis, M., Bauernfeind, F., Horvath, G., Caffrey, D.R., Latz, E., Fitzgerald, K.A., AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458 (2009), 514–518.
20. Ishikawa, H., Barber, G.N., STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455 (2008), 674–678.
21. Jakobsen, M.R., Bak, R.O., Andersen, A., Berg, R.K., Jensen, S.B., Tengchuan, J., Laustsen, A., Hansen, K., Ostergaard, L., Fitzgerald, K.A., et al. IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc. Natl. Acad. Sci. USA 110 (2013), E4571–E4580.
22. Jin, T., Perry, A., Jiang, J., Smith, P., Curry, J.A., Unterholzner, L., Jiang, Z., Horvath, G., Rathinam, V.A., Johnstone, R.W., et al. Structures of the HIN domain:DNA complexes reveal ligand binding and activation mechanisms of the AIM2 inflammasome and IFI16 receptor. Immunity 36 (2012), 561–571.
23. Jones, J.W., Kayagaki, N., Broz, P., Henry, T., Newton, K., O'Rourke, K., Chan, S., Dong, J., Qu, Y., Roose-Girma, M., et al. Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc. Natl. Acad. Sci. USA 107 (2010), 9771–9776.
24. Jørgensen, T.N., Alfaro, J., Enriquez, H.L., Jiang, C., Loo, W.M., Atencio, S., Bupp, M.R., Mailloux, C.M., Metzger, T., Flannery, S., et al. Development of murine lupus involves the combined genetic contribution of the SLAM and FcgammaR intervals within the Nba2 autoimmune susceptibility locus. J. Immunol. 184 (2010), 775–786.
25. Kerur, N., Veettil, M.V., Sharma-Walia, N., Bottero, V., Sadagopan, S., Otageri, P., Chandran, B., IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi Sarcoma-associated herpesvirus infection. Cell Host Microbe 9 (2011), 363–375.
26. Lahaye, X., Satoh, T., Gentili, M., Cerboni, S., Conrad, C., Hurbain, I., El Marjou, A., Lacabaratz, C., Lelièvre, J.D., Manel, N., The capsids of HIV-1 and HIV-2 determine immune detection of the viral cDNA by the innate sensor cGAS in dendritic cells. Immunity 39 (2013), 1132–1142.
27. Lau, L., Gray, E.E., Brunette, R.L., Stetson, D.B., DNA tumor virus oncogenes antagonize the cGAS-STING DNA-sensing pathway. Science 350 (2015), 568–571.
28. Lebon, P., Badoual, J., Ponsot, G., Goutières, F., Hémeury-Cukier, F., Aicardi, J., Intrathecal synthesis of interferon-alpha in infants with progressive familial encephalopathy. J. Neurol. Sci. 84 (1988), 201–208.
29. Lee-Kirsch, M.A., Gong, M., Chowdhury, D., Senenko, L., Engel, K., Lee, Y.A., de Silva, U., Bailey, S.L., Witte, T., Vyse, T.J., et al. Mutations in the gene encoding the 3′-5′ DNA exonuclease TREX1 are associated with systemic lupus erythematosus. Nat. Genet. 39 (2007), 1065–1067.
30. Li, T., Chen, J., Cristea, I.M., Human cytomegalovirus tegument protein pUL83 inhibits IFI16-mediated DNA sensing for immune evasion. Cell Host Microbe 14 (2013), 591–599.
31. Li, X.D., Wu, J., Gao, D., Wang, H., Sun, L., Chen, Z.J., Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341 (2013), 1390–1394.
32. Manzanillo, P.S., Shiloh, M.U., Portnoy, D.A., Cox, J.S., Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 11 (2012), 469–480.
33. Monroe, K.M., Yang, Z., Johnson, J.R., Geng, X., Doitsh, G., Krogan, N.J., Greene, W.C., IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 343 (2014), 428–432.
34. Morita, M., Stamp, G., Robins, P., Dulic, A., Rosewell, I., Hrivnak, G., Daly, G., Lindahl, T., Barnes, D.E., Gene-targeted mice lacking the Trex1 (DNase III) 3′–>5′ DNA exonuclease develop inflammatory myocarditis. Mol. Cell. Biol. 24 (2004), 6719–6727.
35. Moser, K.L., Neas, B.R., Salmon, J.E., Yu, H., Gray-McGuire, C., Asundi, N., Bruner, G.R., Fox, J., Kelly, J., Henshall, S., et al. Genome scan of human systemic lupus erythematosus: evidence for linkage on chromosome 1q in African-American pedigrees. Proc. Natl. Acad. Sci. USA 95 (1998), 14869–14874.
36. Orzalli, M.H., DeLuca, N.A., Knipe, D.M., Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc. Natl. Acad. Sci. USA 109 (2012), E3008–E3017.
37. Orzalli, M.H., Broekema, N.M., Diner, B.A., Hancks, D.C., Elde, N.C., Cristea, I.M., Knipe, D.M., cGAS-mediated stabilization of IFI16 promotes innate signaling during herpes simplex virus infection. Proc. Natl. Acad. Sci. USA 112 (2015), E1773–E1781.
38. Panchanathan, R., Duan, X., Shen, H., Rathinam, V.A., Erickson, L.D., Fitzgerald, K.A., Choubey, D., Aim2 deficiency stimulates the expression of IFN-inducible Ifi202, a lupus susceptibility murine gene within the Nba2 autoimmune susceptibility locus. J. Immunol. 185 (2010), 7385–7393.
39. Rathinam, V.A., Jiang, Z., Waggoner, S.N., Sharma, S., Cole, L.E., Waggoner, L., Vanaja, S.K., Monks, B.G., Ganesan, S., Latz, E., et al. The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat. Immunol. 11 (2010), 395–402.
40. Rice, G., Patrick, T., Parmar, R., Taylor, C.F., Aeby, A., Aicardi, J., Artuch, R., Montalto, S.A., Bacino, C.A., Barroso, B., et al. Clinical and molecular phenotype of Aicardi-Goutieres syndrome. Am. J. Hum. Genet. 81 (2007), 713–725.
41. Roberts, T.L., Idris, A., Dunn, J.A., Kelly, G.M., Burnton, C.M., Hodgson, S., Hardy, L.L., Garceau, V., Sweet, M.J., Ross, I.L., et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323 (2009), 1057–1060.
42. Rozzo, S.J., Allard, J.D., Choubey, D., Vyse, T.J., Izui, S., Peltz, G., Kotzin, B.L., Evidence for an interferon-inducible gene, Ifi202, in the susceptibility to systemic lupus. Immunity 15 (2001), 435–443.
43. Stavrou, S., Blouch, K., Kotla, S., Bass, A., Ross, S.R., Nucleic acid recognition orchestrates the anti-viral response to retroviruses. Cell Host Microbe 17 (2015), 478–488.
44. Stetson, D.B., Medzhitov, R., Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24 (2006), 93–103.
45. Stetson, D.B., Ko, J.S., Heidmann, T., Medzhitov, R., Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134 (2008), 587–598.
46. Storek, K.M., Gertsvolf, N.A., Ohlson, M.B., Monack, D.M., cGAS and Ifi204 cooperate to produce type I IFNs in response to Francisella infection. J. Immunol. 194 (2015), 3236–3245.
47. 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 339 (2013), 786–791.
48. Tallquist, M.D., Soriano, P., Epiblast-restricted Cre expression in MORE mice: a tool to distinguish embryonic vs. extra-embryonic gene function. Genesis 26 (2000), 113–115.
49. Taylor, R.T., Bresnahan, W.A., Human cytomegalovirus immediate-early 2 protein IE86 blocks virus-induced chemokine expression. J. Virol. 80 (2006), 920–928.
50. 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. 11 (2010), 997–1004.
51. Vanden Berghe, T., Hulpiau, P., Martens, L., Vandenbroucke, R.E., Van Wonterghem, E., Perry, S.W., Bruggeman, I., Divert, T., Choi, S.M., Vuylsteke, M., et al. Passenger Mutations Confound Interpretation of All Genetically Modified Congenic Mice. Immunity 43 (2015), 200–209.
52. Watson, R.O., Bell, S.L., MacDuff, D.A., Kimmey, J.M., Diner, E.J., Olivas, J., Vance, R.E., Stallings, C.L., Virgin, H.W., Cox, J.S., The Cytosolic Sensor cGAS Detects Mycobacterium tuberculosis DNA to Induce Type I Interferons and Activate Autophagy. Cell Host Microbe 17 (2015), 811–819.
53. 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 339 (2013), 826–830.
54. Yan, N., Regalado-Magdos, A.D., Stiggelbout, B., Lee-Kirsch, M.A., Lieberman, J., The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat. Immunol. 11 (2010), 1005–1013.
55. Yin, Q., Sester, D.P., Tian, Y., Hsiao, Y.S., Lu, A., Cridland, J.A., Sagulenko, V., Thygesen, S.J., Choubey, D., Hornung, V., et al. Molecular mechanism for p202-mediated specific inhibition of AIM2 inflammasome activation. Cell Rep. 4 (2013), 327–339.