Identification of regulators of the innate immune response to cytosolic DNA and retroviral infection by an integrative approach

Nature Immunology

Volumn 14, Issue 2, 2013, Pages 179-185

  Lee, Mark N ^a,b,c   Roy, Matthew ^a,b,c   Ong, Shao En ^a,f   Mertins, Philipp ^a   Villani, Alexandra Chloé ^a   Li, Weibo ^a,b   Dotiwala, Farokh ^c,d   Sen, Jayita ^c   Doench, John G ^a   Orzalli, Megan H ^c   Kramnik, Igor ^e   Knipe, David M ^c   Lieberman, Judy ^c,d   Carr, Steven A ^a   Hacohen, Nir ^a,b,c  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN 37; DNA; DOUBLE STRANDED DNA; GENOMIC DNA; HEAT SHOCK PROTEIN 90; HIGH MOBILITY GROUP A2 PROTEIN; VIRUS DNA;

ARTICLE; CYTOSOL; GENE IDENTIFICATION; GENE SILENCING; HUMAN; HUMAN CELL; INNATE IMMUNITY; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEOMICS; RETROVIRUS INFECTION; RNA INTERFERENCE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELL CYCLE PROTEINS; CHAPERONINS; CYTOSOL; DENDRITIC CELLS; DNA, VIRAL; FIBROBLASTS; GENE EXPRESSION REGULATION; GENE SILENCING; HIV-1; HMGB2 PROTEIN; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMUNITY, INNATE; MICE; MICE, TRANSGENIC; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMALL MOLECULE LIBRARIES; VESICULOVIRUS;

EID: 84872684650     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2509     Document Type: Article

References (49)

1. Barbalat, R., Ewald, S.E., Mouchess, M.L. & Barton, G.M. Nucleic acid recognition by the innate immune system. Annu. Rev. Immunol. 29, 185-214 (2011).
2. Altfeld, M., Fadda, L., Frleta, D. & Bhardwaj, N. DCs and NK cells: critical effectors in the immune response to HIV-1. Nat. Rev. Immunol. 11, 176-186 (2011).
3. 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, 1005-1013 (2010).
4. Stetson, D.B., Ko, J.S., Heidmann, T. & Medzhitov, R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134, 587-598 (2008).
5. Gall, A. et al. Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferon-dependent autoimmune disease. Immunity 36, 120-131 (2012).
6. Lee-Kirsch, M.A. et al. Mutations in the gene encoding the 3'-5' DNA exonuclease TREX1 are associated with systemic lupus erythematosus. Nat. Genet. 39, 1065-1067 (2007). (Pubitemid 47340647)
7. Lee-Kirsch, M.A. et al. A mutation in TREX1 that impairs susceptibility to granzyme A-mediated cell death underlies familial chilblain lupus. J. Mol. Med. (Berl.) 85, 531-537 (2007). (Pubitemid 46701663)
8. Rotem, Z., Cox, R.A. & Isaacs, A. Inhibition of virus multiplication by foreign nucleic acid. Nature 197, 564-566 (1963).
9. Chiu, Y.H., Macmillan, J.B. & Chen, Z.J. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 138, 576-591 (2009).
10. Ablasser, A. et al. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 10, 1065-1072 (2009).
11. Yoneyama, M. et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5, 730-737 (2004). (Pubitemid 39023305)
12. Stetson, D.B. & Medzhitov, R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 24, 93-103 (2006). (Pubitemid 43077203)
13. Ishii, K.J. et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat. Immunol. 7, 40-48 (2006). (Pubitemid 41823867)
14. Ishikawa, H. & Barber, G.N. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455, 674-678 (2008).
15. Ishikawa, H., Ma, Z. & Barber, G.N. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461, 788-792 (2009).
16. Tanaka, Y. & Chen, Z.J. STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci. Signal. 5, ra20 (2012).
17. Unterholzner, L. et al. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11, 997-1004 (2010).
18. Yanai, H. et al. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 462, 99-103 (2009).
19. Li, S., Wang, L., Berman, M., Kong, Y.Y. & Dorf, M.E. Mapping a dynamic innate immunity protein interaction network regulating type I interferon production. Immunity 35, 426-440 (2011).
20. Tsuchida, T. et al. The ubiquitin ligase TRIM56 regulates innate immune responses to intracellular double-stranded DNA. Immunity 33, 765-776 (2010).
21. Nijman, S.M. et al. A genomic and functional inventory of deubiquitinating enzymes. Cell 123, 773-786 (2005). (Pubitemid 41721026)
22. Ong, S.E. et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386 (2002).
23. Roberts, T.L. et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323, 1057-1060 (2009).
24. Yan, N., Cherepanov, P., Daigle, J.E., Engelman, A. & Lieberman, J. The SET complex acts as a barrier to autointegration of HIV-1. PLoS Pathog. 5, e1000327 (2009).
25. Crow, Y.J. et al. Mutations in the gene encoding the 3'-5' DNA exonuclease TREX1 cause Aicardi-Goutieres syndrome at the AGS1 locus. Nat. Genet. 38, 917-920 (2006). (Pubitemid 44141660)
26. Rice, G.I. et al. Mutations involved in Aicardi-Goutières syndrome implicate SAMHD1 as regulator of the innate immune response. Nat. Genet. 41, 829-832 (2009).
27. Laguette, N. & Benkirane, M. How SAMHD1 changes our view of viral restriction. Trends Immunol. 33, 26-33 (2012).
28. Okabe, Y., Sano, T. & Nagata, S. Regulation of the innate immune response by threonine-phosphatase of Eyes absent. Nature 460, 520-524 (2009).
29. Paytubi, S. et al. ABC50 promotes translation initiation in mammalian cells. J. Biol. Chem. 284, 24061-24073 (2009).
30. Rozenblatt-Rosen, O. et al. Interpreting cancer genomes using systematic host network perturbations by tumour virus proteins. Nature 487, 491-495 (2012).
31. Zhang, T. et al. A novel Hsp90 inhibitor to disrupt Hsp90/Cdc37 complex against pancreatic cancer cells. Mol. Cancer Ther. 7, 162-170 (2008).
32. Gray, P.J. Jr., Prince, T., Cheng, J., Stevenson, M.A. & Calderwood, S.K. Targeting the oncogene and kinome chaperone CDC37. Nat. Rev. Cancer 8, 491-495 (2008). (Pubitemid 351881851)
33. Bouwmeester, T. et al. A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat. Cell Biol. 6, 97-105 (2004). (Pubitemid 38425708)
34. Myers, M.P. et al. TYK2 and JAK2 are substrates of protein-tyrosine phosphatase 1B. J. Biol. Chem. 276, 47771-47774 (2001).
35. Pan, H. et al. Ipr1 gene mediates innate immunity to tuberculosis. Nature 434, 767-772 (2005). (Pubitemid 44739520)
36. Chowdhury, D. & Lieberman, J. Death by a thousand cuts: granzyme pathways of programmed cell death. Annu. Rev. Immunol. 26, 389-420 (2008). (Pubitemid 351611623)
37. Yang, Y.G., Lindahl, T. & Barnes, D.E. Trex1 exonuclease degrades ssDNA to prevent chronic checkpoint activation and autoimmune disease. Cell 131, 873-886 (2007). (Pubitemid 350138088)
38. Yan, N., O'Day, E., Wheeler, L.A., Engelman, A. & Lieberman, J. HIV DNA is heavily uracilated, which protects it from autointegration. Proc. Natl. Acad. Sci. USA 108, 9244-9249 (2011).
39. Ishii, K.J. et al. TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines. Nature 451, 725-729 (2008). (Pubitemid 351220566)
40. Shimp, S.K. III et al. HSP90 inhibition by 17-DMAG reduces inflammation in J774 macrophages through suppression of Akt and nuclear factor-kappaB pathways. Inflamm. Res. 61, 521-533 (2012).
41. Corson, T.W. & Crews, C.M. Molecular understanding and modern application of traditional medicines: triumphs and trials. Cell 130, 769-774 (2007). (Pubitemid 47332575)
42. Klaman, L.D. et al. Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice. Mol. Cell. Biol. 20, 5479-5489 (2000). (Pubitemid 30482885)
43. Amit, I. et al. Unbiased reconstruction of a mammalian transcriptional network mediating pathogen responses. Science 326, 257-263 (2009).
44. Samaniego, L.A., Neiderhiser, L. & DeLuca, N.A. Persistence and expression of the herpes simplex virus genome in the absence of immediate-early proteins. J. Virol. 72, 3307-3320 (1998). (Pubitemid 28175576)
45. Hornung, V. et al. 5'-Triphosphate RNA is the ligand for RIG-I. Science 314, 994-997 (2006).
46. Moffat, J. et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124, 1283-1298 (2006).
47. Burckstummer, T. et al. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10, 266-272 (2009).
48. Pichlmair, A. et al. Viral immune modulators perturb the human molecular network by common and unique strategies. Nature 487, 486-490 (2012).
49. Cristea, I.M. et al. Human cytomegalovirus pUL83 stimulates activity of the viral immediate-early promoter through its interaction with the cellular IFI16 protein. J. Virol. 84, 7803-7814 (2010).