Trex1 regulates lysosomal biogenesis and interferon-independent activation of antiviral genes

Nature Immunology

Volumn 14, Issue 1, 2013, Pages 61-71

  Hasan, Maroof ^a   Koch, James ^a   Rakheja, Dinesh ^a   Pattnaik, Asit K ^b   Brugarolas, James ^a,c,d   Dozmorov, Igor ^c   Levine, Beth ^a,c,e   Wakeland, Edward K ^c   Lee Kirsch, Min Ae ^f   Yan, Nan ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^f DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; EXONUCLEASE; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN STING; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TFEB; TREX1 ENZYME; UNCLASSIFIED DRUG;

ANTIVIRAL RESISTANCE; ARTICLE; BIOGENESIS; CELL COMPARTMENTALIZATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE; GENE ACTIVATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INTERFERON STIMULATED GENE; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; VESICULAR STOMATITIS VIRUS; VIRUS REPLICATION;

ANIMALS; ANTIGENS, VIRAL; BIOGENESIS; EXODEOXYRIBONUCLEASES; HELA CELLS; HUMANS; IMMUNITY, ACTIVE; INTERFERONS; LYSOSOMES; MICE; MICE, KNOCKOUT; MUTATION; PHOSPHOPROTEINS; RNA VIRUS INFECTIONS; RNA VIRUSES; RNA, SMALL INTERFERING;

EID: 84871222424     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2475     Document Type: Article

References (47)

1. Iwasaki, A. & Medzhitov, R. Regulation of adaptive immunity by the innate immune system. Science 327, 291-295 (2010).
2. Barber, G.N. Cytoplasmic DNA innate immune pathways. Immunol. Rev. 243, 99-108 (2011).
3. Bowie, A.G. & Unterholzner, L. Viral evasion and subversion of pattern-recognition receptor signalling. Nat. Rev. Immunol. 8, 911-922 (2008).
4. Takaoka, A. et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448, 501-505 (2007).
5. Unterholzner, L. et al. IFI16 is an innate immune sensor for intracellular DNA. Nat. Immunol. 11, 997-1004 (2010).
6. Zhang, Z. et al. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat. Immunol. 12, 959-965 (2011).
7. Burdette, D.L. et al. STING is a direct innate immune sensor of cyclic di-GMP. Nature 478, 515-518 (2011).
8. Chen, H. et al. Activation of STAT6 by STING is critical for antiviral innate immunity. Cell 147, 436-446 (2011).
9. Noyce, R.S., Collins, S.E. & Mossman, K.L. Identification of a novel pathway essential for the immediate-early, interferon-independent antiviral response to enveloped virions. J. Virol. 80, 226-235 (2006).
10. Dixit, E. et al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141, 668-681 (2010).
11. 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).
12. Gall, A. et al. Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferon-dependent autoimmune disease. Immunity 36, 120-131 (2012).
13. Crow, Y. 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).
14. Crow, Y.J. & Rehwinkel, J. Aicardi-Goutieres syndrome and related phenotypes: linking nucleic acid metabolism with autoimmunity. Hum. Mol. Genet. 18, R130-R136 (2009).
15. 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).
16. 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. 85, 531-537 (2007).
17. Richards, A. et al. C-terminal truncations in human 3′-5′ DNA exonuclease TREX1 cause autosomal dominant retinal vasculopathy with cerebral leukodystrophy. Nat. Genet. 39, 1068-1070 (2007).
18. Moser, K.L., Kelly, J.A., Lessard, C.J. & Harley, J.B. Recent insights into the genetic basis of systemic lupus erythematosus. Genes Immun. 10, 373-379 (2009).
19. Stetson, D.B., Ko, J.S., Heidmann, T. & Medzhitov, R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134, 587-598 (2008).
20. Yang, Y., Lindahl, T. & Barnes, D. Trex1 exonuclease degrades ssDNA to prevent chronic checkpoint activation and autoimmune disease. Cell 131, 873-886 (2007).
21. Das, S.C., Nayak, D., Zhou, Y. & Pattnaik, A.K. Visualization of intracellular transport of vesicular stomatitis virus nucleocapsids in living cells. J. Virol. 80, 6368-6377 (2006).
22. Orebaugh, C.D., Fye, J.M., Harvey, S., Hollis, T. & Perrino, F.W. The TREX1 exonuclease R114H mutation in Aicardi-Goutieres syndrome and lupus reveals dimeric structure requirements for DNA degradation activity. J. Biol. Chem. 286, 40246-40254 (2011).
23. Kreijtz, J.H.C.M., Fouchier, R.A.M. & Rimmelzwaan, G.F. Immune responses to influenza virus infection. Virus Res. 162, 19-30 (2011).
24. Pichlmair, A. et al. IFIT1 is an antiviral protein that recognizes 5′-triphosphate RNA. Nat. Immunol. 12, 624-630 (2011).
25. Yan, N. & Chen, Z.J. Intrinsic antiviral immunity. Nat. Immunol. 13, 214-222 (2012).
26. Brass, A.L. et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139, 1243-1254 (2009).
27. Ramantani, G. et al. Expanding the phenotypic spectrum of lupus erythematosus in aicardi-goutières syndrome. Arthritis Rheum. 62, 1469-1477 (2010).
28. Paladino, P., Cummings, D.T., Noyce, R.S. & Mossman, K.L. The IFN-independent response to virus particle entry provides a first line of antiviral defense that is independent of TLRs and retinoic acid-inducible gene I. J. Immunol. 177, 8008-8016 (2006).
29. Saftig, P. & Klumperman, J. Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat. Rev. Mol. Cell Biol. 10, 623-635 (2009).
30. Cox, T.M. & Cachón-González, M.B. The cellular pathology of lysosomal diseases. J. Pathol. 226, 241-254 (2012).
31. Palmieri, M. et al. Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum. Mol. Genet. 20, 3852-3866 (2011).
32. Sardiello, M. et al. A gene network regulating lysosomal biogenesis and function. Science 325, 473-477 (2009).
33. Settembre, C. et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 31, 1095-1108 (2012).
34. Peña-Llopis, S. et al. Regulation of TFEB and V-ATPases by mTORC1. EMBO J. 30, 3242-3258 (2011).
35. Roczniak-Ferguson, A. et al. The transcription factor TFEB links mTORC1 Signaling to transcriptional control of lysosome homeostasis. Sci. Signal. 5, ra42 (2012).
36. Vincent, M.J. et al. Chloroquine is a potent inhibitor of SARS coronavirus infection and spread. Virol. J. 2, 69 (2005).
37. Ooi, E.E., Chew, J.S., Loh, J.P. & Chua, R.C. In vitro inhibition of human influenza A virus replication by chloroquine. Virol. J. 3, 39 (2006).
38. Savarino, A., Boelaert, J.R., Cassone, A., Majori, G. & Cauda, R. Effects of chloroquine on viral infections: an old drug against today's diseases? Lancet Infect. Dis. 3, 722-727 (2003).
39. Martina, J.A., Chen, Y., Gucek, M. & Puertollano, R. MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy 8, 903-914 (2012).
40. Mata, M.A. et al. Chemical inhibition of RNA viruses reveals REDD1 as a host defense factor. Nat. Chem. Biol. 7, 712-719 (2011).
41. Grandvaux, N. et al. Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J. Virol. 76, 5532-5539 (2002).
42. Medina, D.L. et al. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev. Cell 21, 421-430 (2011).
43. Migliorini, A. & Anders, H.-J. A novel pathogenetic concept-antiviral immunity in lupus nephritis. Nat. Rev. Nephrol. 8, 183-189 (2012).
44. Holm, C.K. et al. Virus-cell fusion as a trigger of innate immunity dependent on the adaptor STING. Nat. Immunol. 13, 737-743 (2012).
45. Marshak-Rothstein, A. Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 6, 823-835 (2006).
46. 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).
47. Keller, B.C. et al. Resistance to α/β interferon is a determinant of West Nile virus replication fitness and virulence. J. Virol. 80, 9424-9434 (2006).