Akt Kinase-Mediated Checkpoint of cGAS DNA Sensing Pathway

Cell Reports

Volumn 13, Issue 2, 2015, Pages 440-449

  Seo, Gil Ju ^a   Yang, Aerin ^c   Tan, Brandon ^a   Kim, Sungyoon ^c   Liang, Qiming ^a   Choi, Younho ^a   Yuan, Weiming ^a   Feng, Pinghui ^a   Park, Hee Sung ^c   Jung, Jae U ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BETA INTERFERON; CELL DNA; CYTOKINE; PROTEIN CGAMP; PROTEIN CGAS; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; PROTEIN PRECURSOR; SERINE; UNCLASSIFIED DRUG; MB21D1 PROTEIN, MOUSE; NUCLEOTIDYLTRANSFERASE; VIRUS DNA;

ANIMAL CELL; ARTICLE; CYTOKINE PRODUCTION; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; VACCINIA VIRUS; VIRUS INFECTION; VIRUS REPLICATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SECOND MESSENGER;

AMINO ACID SEQUENCE; ANIMALS; DNA, VIRAL; HEK293 CELLS; HERPESVIRUS 1, HUMAN; HUMANS; INTERFERON-BETA; MICE; MOLECULAR SEQUENCE DATA; NUCLEOTIDYLTRANSFERASES; PROTO-ONCOGENE PROTEINS C-AKT; SECOND MESSENGER SYSTEMS; VIRUS REPLICATION;

EID: 84944067911     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.09.007     Document Type: Article

References (44)

1. Ablasser A., Bauernfeind F., Hartmann G., Latz E., Fitzgerald K.A., Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 2009, 10:1065-1072.
2. Ablasser A., Goldeck M., Cavlar T., Deimling T., Witte G., Röhl I., Hopfner K.P., Ludwig J., Hornung V. cGAS produces a 2'-5'-linked cyclic dinucleotide second messenger that activates STING. Nature 2013, 498:380-384.
3. Ablasser A., Hemmerling I., Schmid-Burgk J.L., Behrendt R., Roers A., Hornung V. TREX1 deficiency triggers cell-autonomous immunity in a cGAS-dependent manner. J. Immunol. 2014, 192:5993-5997.
4. Bhat N., Fitzgerald K.A. Recognition of cytosolic DNA by cGAS and other STING-dependent sensors. Eur. J. Immunol. 2014, 44:634-640.
5. 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 2009, 138:576-591.
6. Deng L., Liang H., Xu M., Yang X., Burnette B., Arina A., Li X.D., Mauceri H., Beckett M., Darga T., et al. STING-dependent cytosolic DNA sensing promotes radiation-induced type i interferon-dependent antitumor immunity in immunogenic tumors. Immunity 2014, 41:843-852.
7. Dunn E.F., Connor J.H. HijAkt: The PI3K/Akt pathway in virus replication and pathogenesis. Prog. Mol. Biol. Transl. Sci. 2012, 106:223-250.
8. Elinav E., Strowig T., Henao-Mejia J., Flavell R.A. Regulation of the antimicrobial response by NLR proteins. Immunity 2011, 34:665-679.
9. Ferguson B.J., Mansur D.S., Peters N.E., Ren H., Smith G.L. DNA-PK is a DNA sensor for IRF-3-dependent innate immunity. eLife 2012, 1:e00047.
10. 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 2009, 458:509-513.
11. 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 2013, 341:903-906.
12. Gao P., Ascano M., Wu Y., Barchet W., Gaffney B.L., Zillinger T., Serganov A.A., Liu Y., Jones R.A., Hartmann G., et al. Cyclic [G(2',5')pA(3',5')p] is the metazoan second messenger produced by DNA-activated cyclic GMP-AMP synthase. Cell 2013, 153:1094-1107.
13. Härtlova A., Erttmann S.F., Raffi F.A., Schmalz A.M., Resch U., Anugula S., Lienenklaus S., Nilsson L.M., Kröger A., Nilsson J.A., et al. DNA damage primes the type I interferon system via the cytosolic DNA sensor STING to promote anti-microbial innate immunity. Immunity 2015, 42:332-343.
14. 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 2009, 458:514-518.
15. Hornung V., Hartmann R., Ablasser A., Hopfner K.P. OAS proteins and cGAS: unifying concepts in sensing and responding to cytosolic nucleic acids. Nat. Rev. Immunol. 2014, 14:521-528.
16. Hrincius E.R., Dierkes R., Anhlan D., Wixler V., Ludwig S., Ehrhardt C. Phosphatidylinositol-3-kinase (PI3K) is activated by influenza virus vRNA via the pathogen pattern receptor Rig-I to promote efficient type I interferon production. Cell. Microbiol. 2011, 13:1907-1919.
17. Kanai R., Zaupa C., Sgubin D., Antoszczyk S.J., Martuza R.L., Wakimoto H., Rabkin S.D. Effect of γ34.5 deletions on oncolytic herpes simplex virus activity in brain tumors. J. Virol. 2012, 86:4420-4431.
18. Kaur S., Sassano A., Dolniak B., Joshi S., Majchrzak-Kita B., Baker D.P., Hay N., Fish E.N., Platanias L.C. Role of the Akt pathway in mRNA translation of interferon-stimulated genes. Proc. Natl. Acad. Sci. USA 2008, 105:4808-4813.
19. Kaur S., Sassano A., Joseph A.M., Majchrzak-Kita B., Eklund E.A., Verma A., Brachmann S.M., Fish E.N., Platanias L.C. Dual regulatory roles of phosphatidylinositol 3-kinase in IFN signaling. J. Immunol. 2008, 181:7316-7323.
20. Kawai T., Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011, 34:637-650.
21. Kranzusch P.J., Lee A.S., Berger J.M., Doudna J.A. Structure of human cGAS reveals a conserved family of second-messenger enzymes in innate immunity. Cell Rep. 2013, 3:1362-1368.
22. Latz E. The inflammasomes: mechanisms of activation and function. Curr. Opin. Immunol. 2010, 22:28-33.
23. Lee S., Oh S., Yang A., Kim J., Söll D., Lee D., Park H.S. A facile strategy for selective incorporation of phosphoserine into histones. Angew. Chem. Int. Ed. Engl. 2013, 52:5771-5775.
24. Li Y., Zhang C., Chen X., Yu J., Wang Y., Yang Y., Du M., Jin H., Ma Y., He B., Cao Y. ICP34.5 protein of herpes simplex virus facilitates the initiation of protein translation by bridging eukaryotic initiation factor 2alpha (eIF2alpha) and protein phosphatase 1. J. Biol. Chem. 2011, 286:24785-24792.
25. 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 2013, 341:1390-1394.
26. Liang Q., Seo G.J., Choi Y.J., Kwak M.J., Ge J., Rodgers M.A., Shi M., Leslie B.J., Hopfner K.P., Ha T., et al. Crosstalk between the cGAS DNA sensor and Beclin-1 autophagy protein shapes innate antimicrobial immune responses. Cell Host Microbe 2014, 15:228-238.
27. Liu Y., Jesus A.A., Marrero B., Yang D., Ramsey S.E., Montealegre Sanchez G.A., Tenbrock K., Wittkowski H., Jones O.Y., Kuehn H.S., et al. Activated STING in a vascular and pulmonary syndrome. N. Engl. J. Med. 2014, 371:507-518.
28. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129:1261-1274.
29. Medzhitov R., Janeway C. The Toll receptor family and microbial recognition. Trends Microbiol. 2000, 8:452-456.
30. Münz C., Lünemann J.D., Getts M.T., Miller S.D. Antiviral immune responses: triggers of or triggered by autoimmunity?. Nat. Rev. Immunol. 2009, 9:246-258.
31. Orvedahl A., Alexander D., Tallóczy Z., Sun Q., Wei Y., Zhang W., Burns D., Leib D.A., Levine B. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 2007, 1:23-35.
32. Ou Y.H., Torres M., Ram R., Formstecher E., Roland C., Cheng T., Brekken R., Wurz R., Tasker A., Polverino T., et al. TBK1 directly engages Akt/PKB survival signaling to support oncogenic transformation. Mol. Cell 2011, 41:458-470.
33. Paludan S.R., Bowie A.G. Immune sensing of DNA. Immunity 2013, 38:870-880.
34. Park H.S., Hohn M.J., Umehara T., Guo L.T., Osborne E.M., Benner J., Noren C.J., Rinehart J., Söll D. Expanding the genetic code of Escherichia coli with phosphoserine. Science 2011, 333:1151-1154.
35. 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 2009, 323:1057-1060.
36. Schabbauer G., Luyendyk J., Crozat K., Jiang Z., Mackman N., Bahram S., Georgel P. TLR4/CD14-mediated PI3K activation is an essential component of interferon-dependent VSV resistance in macrophages. Mol. Immunol. 2008, 45:2790-2796.
37. Shi M., Cho H., Inn K.S., Yang A., Zhao Z., Liang Q., Versteeg G.A., Amini-Bavil-Olyaee S., Wong L.Y., Zlokovic B.V., et al. Negative regulation of NF-κB activity by brain-specific TRIpartite Motif protein 9. Nat. Commun. 2014, 5:4820.
38. Soares J.A., Leite F.G., Andrade L.G., Torres A.A., De Sousa L.P., Barcelos L.S., Teixeira M.M., Ferreira P.C., Kroon E.G., Souto-Padrón T., Bonjardim C.A. Activation of the PI3K/Akt pathway early during vaccinia and cowpox virus infections is required for both host survival and viral replication. J. Virol. 2009, 83:6883-6899.
39. 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 2013, 339:786-791.
40. Takaoka A., Wang Z., Choi M.K., Yanai H., Negishi H., Ban T., Lu Y., Miyagishi M., Kodama T., Honda K., et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007, 448:501-505.
41. 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. 2010, 11:997-1004.
42. Woo S.R., Fuertes M.B., Corrales L., Spranger S., Furdyna M.J., Leung M.Y., Duggan R., Wang Y., Barber G.N., Fitzgerald K.A., et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity 2014, 41:830-842.
43. 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 2013, 339:826-830.
44. Zhang Z., Yuan B., Bao M., Lu N., Kim T., Liu Y.J. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat. Immunol. 2011, 12:959-965.