TRIM14 Inhibits cGAS Degradation Mediated by Selective Autophagy Receptor p62 to Promote Innate Immune Responses

Molecular Cell

Volumn 64, Issue 1, 2016, Pages 105-119

  Chen, Meixin ^a   Meng, Qingcai ^a   Qin, Yunfei ^a,e   Liang, Puping ^a   Tan, Peng ^b,c   He, Lian ^c   Zhou, Yubin ^c   Chen, Yongjun ^a   Huang, Junjiu ^a,f   Wang, Rong Fu ^b,c,d   Cui, Jun ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e ZHENGZHOU UNIVERSITY   (China)

^f SUN YAT SEN UNIVERSITY   (China)

Author keywords

autophagy; cGAS; p62; TRIM14; type I interferon (IFN) signaling; USP14

Indexed keywords

CELL PROTEIN; CYCLIC GMP AMP SYNTHASE; INTERFERON; LYSINE; PROTEIN P62; SYNTHETASE; TRIM14 PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; USP14 PROTEIN; MB21D1 PROTEIN, MOUSE; NUCLEOTIDYLTRANSFERASE; SEQUESTOSOME 1; SMALL INTERFERING RNA; SQSTM1 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN; TRIM14 PROTEIN, MOUSE; UBIQUITIN THIOLESTERASE; USP14 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; INFECTION SENSITIVITY; INNATE IMMUNITY; INTERFERON PRODUCTION; LETHALITY; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PROTEIN DEGRADATION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UBIQUITINATION; VESICULOVIRUS; ANIMAL; ANTAGONISTS AND INHIBITORS; DEFICIENCY; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEK293 CELL LINE; HERPES SIMPLEX; HOST PATHOGEN INTERACTION; HUMAN ALPHAHERPESVIRUS 1; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; METABOLISM; MORTALITY; PHYSIOLOGICAL FEEDBACK; PROTEIN PROCESSING; SURVIVAL ANALYSIS; VIROLOGY;

ANIMALS; AUTOPHAGY; FEEDBACK, PHYSIOLOGICAL; HEK293 CELLS; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; LUNG; MICE; MICE, KNOCKOUT; NUCLEOTIDYLTRANSFERASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, SMALL INTERFERING; SEQUESTOSOME-1 PROTEIN; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TRANS-ACTIVATORS; UBIQUITIN THIOLESTERASE;

EID: 84994128770     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.08.025     Document Type: Article

References (51)

1. Ahn, J., Barber, G.N., Self-DNA, STING-dependent signaling and the origins of autoinflammatory disease. Curr. Opin. Immunol. 31 (2014), 121–126.
2. Bell, J.L., Malyukova, A., Holien, J.K., Koach, J., Parker, M.W., Kavallaris, M., Marshall, G.M., Cheung, B.B., TRIM16 acts as an E3 ubiquitin ligase and can heterodimerize with other TRIM family members. PLoS ONE, 7, 2012, e37470.
3. Boyle, K.B., Randow, F., The role of ‘eat-me’ signals and autophagy cargo receptors in innate immunity. Curr. Opin. Microbiol. 16 (2013), 339–348.
4. Chan, Y.K., Gack, M.U., Viral evasion of intracellular DNA and RNA sensing. Nat. Rev. Microbiol. 14 (2016), 360–373.
5. Chen, Z.J., Sun, L.J., Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 33 (2009), 275–286.
6. Dai, P., Wang, W., Cao, H., Avogadri, F., Dai, L., Drexler, I., Joyce, J.A., Li, X.D., Chen, Z., Merghoub, T., et al. Modified vaccinia virus Ankara triggers type I IFN production in murine conventional dendritic cells via a cGAS/STING-mediated cytosolic DNA-sensing pathway. PLoS Pathog., 10, 2014, e1003989.
7. Ding, W.X., Yin, X.M., Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy 4 (2008), 141–150.
8. Finley, D., Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78 (2009), 477–513.
9. 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.
10. 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.
11. 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 153 (2013), 1094–1107.
12. Hansen, K., Prabakaran, T., Laustsen, A., Jørgensen, S.E., Rahbæk, S.H., Jensen, S.B., Nielsen, R., Leber, J.H., Decker, T., Horan, K.A., et al. Listeria monocytogenes induces IFNβ expression through an IFI16-, cGAS- and STING-dependent pathway. EMBO J. 33 (2014), 1654–1666.
13. Herzner, A.M., Hagmann, C.A., Goldeck, M., Wolter, S., Kübler, K., Wittmann, S., Gramberg, T., Andreeva, L., Hopfner, K.P., Mertens, C., et al. Sequence-specific activation of the DNA sensor cGAS by Y-form DNA structures as found in primary HIV-1 cDNA. Nat. Immunol. 16 (2015), 1025–1033.
14. Isogai, S., Morimoto, D., Arita, K., Unzai, S., Tenno, T., Hasegawa, J., Sou, Y.S., Komatsu, M., Tanaka, K., Shirakawa, M., Tochio, H., Crystal structure of the ubiquitin-associated (UBA) domain of p62 and its interaction with ubiquitin. J. Biol. Chem. 286 (2011), 31864–31874.
15. 2+ influx. Nat. Cell Biol. 17 (2015), 1339–1347.
16. Kawai, T., Akira, S., Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34 (2011), 637–650.
17. Kirkin, V., McEwan, D.G., Novak, I., Dikic, I., A role for ubiquitin in selective autophagy. Mol. Cell 34 (2009), 259–269.
18. Korolchuk, V.I., Mansilla, A., Menzies, F.M., Rubinsztein, D.C., Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol. Cell 33 (2009), 517–527.
19. Kuma, A., Matsui, M., Mizushima, N., LC3, an autophagosome marker, can be incorporated into protein aggregates independent of autophagy: caution in the interpretation of LC3 localization. Autophagy 3 (2007), 323–328.
20. 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.
21. Lam, E., Stein, S., Falck-Pedersen, E., Adenovirus detection by the cGAS/STING/TBK1 DNA sensing cascade. J. Virol. 88 (2014), 974–981.
22. Lee, B.H., Lee, M.J., Park, S., Oh, D.C., Elsasser, S., Chen, P.C., Gartner, C., Dimova, N., Hanna, J., Gygi, S.P., et al. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 467 (2010), 179–184.
23. Li, X., Shu, C., Yi, G., Chaton, C.T., Shelton, C.L., Diao, J., Zuo, X., Kao, C.C., Herr, A.B., Li, P., Cyclic GMP-AMP synthase is activated by double-stranded DNA-induced oligomerization. Immunity 39 (2013), 1019–1031.
24. 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.
25. 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 15 (2014), 228–238.
26. Liu, J., Qian, C., Cao, X., Post-Translational Modification Control of Innate Immunity. Immunity 45 (2016), 15–30.
27. Liu, X.M., Du, L.L., A selective autophagy pathway takes an unconventional route. Autophagy 11 (2015), 2381–2382.
28. 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. 371 (2014), 507–518.
29. Ma, Y., Galluzzi, L., Zitvogel, L., Kroemer, G., Autophagy and cellular immune responses. Immunity 39 (2013), 211–227.
30. Meng, Q., Cai, C., Sun, T., Wang, Q., Xie, W., Wang, R., Cui, J., Reversible ubiquitination shapes NLRC5 function and modulates NF-κB activation switch. J. Cell Biol. 211 (2015), 1025–1040.
31. Mijaljica, D., Nazarko, T.Y., Brumell, J.H., Huang, W.P., Komatsu, M., Prescott, M., Simonsen, A., Yamamoto, A., Zhang, H., Klionsky, D.J., Devenish, R.J., Receptor protein complexes are in control of autophagy. Autophagy 8 (2012), 1701–1705.
32. Münz, C., Selective macroautophagy for immunity. Immunity 32 (2010), 298–299.
33. Novak, I., Kirkin, V., McEwan, D.G., Zhang, J., Wild, P., Rozenknop, A., Rogov, V., Löhr, F., Popovic, D., Occhipinti, A., et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 11 (2010), 45–51.
34. Ozato, K., Shin, D.M., Chang, T.H., Morse, H.C. 3rd, TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 8 (2008), 849–860.
35. Paludan, S.R., Bowie, A.G., Immune sensing of DNA. Immunity 38 (2013), 870–880.
36. Qin, Y., Liu, Q., Tian, S., Xie, W., Cui, J., Wang, R.F., TRIM9 short isoform preferentially promotes DNA and RNA virus-induced production of type I interferon by recruiting GSK3β to TBK1. Cell Res. 26 (2016), 613–628.
37. Radivojac, P., Vacic, V., Haynes, C., Cocklin, R.R., Mohan, A., Heyen, J.W., Goebl, M.G., Iakoucheva, L.M., Identification, analysis, and prediction of protein ubiquitination sites. Proteins 78 (2010), 365–380.
38. Rajsbaum, R., Versteeg, G.A., Schmid, S., Maestre, A.M., Belicha-Villanueva, A., Martínez-Romero, C., Patel, J.R., Morrison, J., Pisanelli, G., Miorin, L., et al. Unanchored K48-linked polyubiquitin synthesized by the E3-ubiquitin ligase TRIM6 stimulates the interferon-IKKε kinase-mediated antiviral response. Immunity 40 (2014), 880–895.
39. Robert, X., Gouet, P., Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 42 (2014), W320–W324.
40. Schoggins, J.W., MacDuff, D.A., Imanaka, N., Gainey, M.D., Shrestha, B., Eitson, J.L., Mar, K.B., Richardson, R.B., Ratushny, A.V., Litvak, V., et al. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505 (2014), 691–695.
41. Sho, T., Tsukiyama, T., Sato, T., Kondo, T., Cheng, J., Saku, T., Asaka, M., Hatakeyama, S., TRIM29 negatively regulates p53 via inhibition of Tip60. Biochim. Biophys. Acta 1813 (2011), 1245–1253.
42. 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.
43. 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.
44. Sutton, S.K., Koach, J., Tan, O., Liu, B., Carter, D.R., Wilmott, J.S., Yosufi, B., Haydu, L.E., Mann, G.J., Thompson, J.F., et al. TRIM16 inhibits proliferation and migration through regulation of interferon beta 1 in melanoma cells. Oncotarget 5 (2014), 10127–10139.
45. Takeuchi, O., Akira, S., Pattern recognition receptors and inflammation. Cell 140 (2010), 805–820.
46. Versteeg, G.A., Rajsbaum, R., Sánchez-Aparicio, M.T., Maestre, A.M., Valdiviezo, J., Shi, M., Inn, K.S., Fernandez-Sesma, A., Jung, J., García-Sastre, A., The E3-ligase TRIM family of proteins regulates signaling pathways triggered by innate immune pattern-recognition receptors. Immunity 38 (2013), 384–398.
47. Wang, Q., Liu, X., Cui, Y., Tang, Y., Chen, W., Li, S., Yu, H., Pan, Y., Wang, C., The E3 ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 41 (2014), 919–933.
48. 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.
49. 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.
50. Yang, B., Wang, J., Wang, Y., Zhou, H., Wu, X., Tian, Z., Sun, B., Novel function of Trim44 promotes an antiviral response by stabilizing VISA. J. Immunol. 190 (2013), 3613–3619.
51. Zhou, Z., Jia, X., Xue, Q., Dou, Z., Ma, Y., Zhao, Z., Jiang, Z., He, B., Jin, Q., Wang, J., TRIM14 is a mitochondrial adaptor that facilitates retinoic acid-inducible gene-I-like receptor-mediated innate immune response. Proc. Natl. Acad. Sci. USA 111 (2014), E245–E254.