USP12 translocation maintains interferon antiviral efficacy by inhibiting CBP acetyltransferase activity

English version

Autoři: Jin Liu ^aff001; Lincong Jin ^aff001; Xiangjie Chen ^aff001; Yukang Yuan ^aff001; Yibo Zuo ^aff001; Ying Miao ^aff001; Qian Feng ^aff001; Hongguang Zhang ^aff001; Fan Huang ^aff001; Tingting Guo ^aff001; Liting Zhang ^aff001; Li Zhu ^aff003; Feng Qian ^aff003; Chuanwu Zhu ^aff003; Hui Zheng ^aff001
Působiště autorů: International Institute of Infection and Immunity, Institutes of Biology and Medical Sciences, Soochow University, Suzhou, China ^aff001; Jiangsu Key Laboratory of Infection and Immunity, Soochow University, Suzhou, China ^aff002; The Affiliated Infectious Diseases Hospital of Soochow University, Suzhou, China ^aff003
Vyšlo v časopise: USP12 translocation maintains interferon antiviral efficacy by inhibiting CBP acetyltransferase activity. PLoS Pathog 16(1): e32767. doi:10.1371/journal.ppat.1008215
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008215

Souhrn

CREB-binding protein (CBP) participates in numerous transcription events. However, cell-intrinsic inhibitors of CBP are poorly defined. Here, we found that cellular USP12 interacts with the HAT domain of CBP and inhibits CBP’s acetyltransferase activity. Interestingly, USP12 positively regulates interferon (IFN) antiviral signaling independently of its deubiquitinase activity. Furthermore, we found that in IFN signaling USP12 translocates from the cytoplasm to the nucleus. The decrease in cytoplasmic USP12 facilitates CBP-induced acetylation and activation of IFN signaling proteins in the cytoplasm. Moreover, USP12 accumulation in the nucleus blocks CBP-induced acetylation of phosphorylated STAT1 (p-STAT1) and therefore inhibits the dephosphorylation effects of TCPTP on p-STAT1, which finally maintains nuclear p-STAT1 levels and IFN antiviral efficacy. USP12 nuclear translocation extends our understanding of the regulation of the strength of IFN antiviral signaling. Our study uncovers a cell-intrinsic regulation of CBP acetyltransferase activity and may provide potential strategies for IFN-based antiviral therapy.

Klíčová slova:

Acetylation – Antiviral immune response – Cytoplasm – Immunoprecipitation – Interferons – Small interfering RNAs – Vesicular stomatitis virus – TCR signaling cascade

Zdroje

1. Berger SL. Gene activation by histone and factor acetyltransferases. Curr Opin Cell Biol. 1999;11(3):336–41. Epub 1999/07/08. doi: 10.1016/S0955-0674(99)80046-5 10395565.

2. Bararia D, Trivedi AK, Zada AA, Greif PA, Mulaw MA, Christopeit M, et al. Proteomic identification of the MYST domain histone acetyltransferase TIP60 (HTATIP) as a co-activator of the myeloid transcription factor C/EBPalpha. Leukemia. 2008;22(4):800–7. Epub 2008/02/02. doi: 10.1038/sj.leu.2405101 18239623.

3. Grienenberger A, Miotto B, Sagnier T, Cavalli G, Schramke V, Geli V, et al. The MYST domain acetyltransferase Chameau functions in epigenetic mechanisms of transcriptional repression. Curr Biol. 2002;12(9):762–6. Epub 2002/05/15. doi: 10.1016/s0960-9822(02)00814-x 12007422.

4. Dumay-Odelot H, Marck C, Durrieu-Gaillard S, Lefebvre O, Jourdain S, Prochazkova M, et al. Identification, molecular cloning, and characterization of the sixth subunit of human transcription factor TFIIIC. J Biol Chem. 2007;282(23):17179–89. Epub 2007/04/06. doi: 10.1074/jbc.M611542200 17409385.

5. Ishii S, Yamada M, Satoh T, Monden T, Hashimoto K, Shibusawa N, et al. Aberrant dynamics of histone deacetylation at the thyrotropin-releasing hormone gene in resistance to thyroid hormone. Mol Endocrinol. 2004;18(7):1708–20. doi: 10.1210/me.2004-0067 WOS:000222259000011. 15131262

6. Vries RGJ, Prudenziati M, Zwartjes C, Verlaan M, Kalkhoven E, Zantema A. A specific lysine in c-Jun is required for transcriptional repression by E1A and is acetylated by p300. Embo J. 2001;20(21):6095–103. doi: 10.1093/emboj/20.21.6095 WOS:000172104000028. 11689449

7. Sterner DE, Berger SL. Acetylation of histones and transcription-related factors. Microbiol Mol Biol R. 2000;64(2):435–+. doi: 10.1128/Mmbr.64.2.435–459.2000 WOS:000087486200006.

8. Bordoli L, Netsch M, Luthi U, Lutz W, Eckner R. Plant orthologs of p300/CBP: conservation of a core domain in metazoan p300/CBP acetyltransferase-related proteins. Nucleic Acids Res. 2001;29(3):589–97. doi: 10.1093/nar/29.3.589 WOS:000166786300001. 11160878

9. Yuan LWC, Giordano A. Acetyltransferase machinery conserved in p300/CBP-family proteins. Oncogene. 2002;21(14):2253–60. doi: 10.1038/sj.onc.1205283 WOS:000174555300014. 11948408

10. Weinert BT, Narita T, Satpathy S, Srinivasan B, Hansen BK, Scholz C, et al. Time-Resolved Analysis Reveals Rapid Dynamics and Broad Scope of the CBP/p300 Acetylome. Cell. 2018;174(1):231–+. doi: 10.1016/j.cell.2018.04.033 WOS:000437005800023. 29804834

11. Bedford DC, Kasper LH, Fukuyama T, Brindle PK. Target gene context influences the transcriptional requirement for the KAT3 family of CBP and p300 histone acetyltransferases. Epigenetics-Us. 2010;5(1):9–15. doi: 10.4161/epi.5.1.10449 WOS:000274790700002. 20110770

12. Dyson HJ, Wright PE. Role of Intrinsic Protein Disorder in the Function and Interactions of the Transcriptional Coactivators CREB-binding Protein (CBP) and p300. J Biol Chem. 2016;291(13):6714–22. Epub 2016/02/07. doi: 10.1074/jbc.R115.692020 26851278; PubMed Central PMCID: PMC4807259.

13. Kasper LH, Fukuyama T, Biesen MA, Boussouar F, Tong C, de Pauw A, et al. Conditional knockout mice reveal distinct functions for the global transcriptional coactivators CBP and p300 in T-cell development. Mol Cell Biol. 2006;26(3):789–809. Epub 2006/01/24. doi: 10.1128/MCB.26.3.789-809.2006 16428436; PubMed Central PMCID: PMC1347027.

14. Chan HM, La Thangue NB. p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J Cell Sci. 2001;114(Pt 13):2363–73. Epub 2001/09/18. 11559745.

15. Das C, Lucia MS, Hansen KC, Tyler JK. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature. 2009;459(7243):113–U23. doi: 10.1038/nature07861 WOS:000265801300040. 19270680

16. Kramer OH, Knauer SK, Greiner G, Jandt E, Reichardt S, Guhrs KH, et al. A phosphorylation-acetylation switch regulates STAT1 signaling. Gene Dev. 2009;23(2):223–35. doi: 10.1101/gad.479209 WOS:000262796700010. 19171783

17. Sakaguchi K, Herrera JE, Saito S, Miki T, Bustin M, Vassilev A, et al. DNA damage activates p53 through a phosphorylation-acetylation cascade. Gene Dev. 1998;12(18):2831–41. doi: 10.1101/gad.12.18.2831 WOS:000076154600003. 9744860

18. Jang ER, Choi JD, Lee JS. Acetyltransferase p300 regulates NBS1-mediated DNA damage response. FEBS Lett. 2011;585(1):47–52. Epub 2010/11/27. doi: 10.1016/j.febslet.2010.11.034 21108945.

19. Santer FR, Hoschele PPS, Oh SJ, Erb HHH, Bouchal J, Cavarretta IT, et al. Inhibition of the Acetyltransferases p300 and CBP Reveals a Targetable Function for p300 in the Survival and Invasion Pathways of Prostate Cancer Cell Lines. Mol Cancer Ther. 2011;10(9):1644–55. doi: 10.1158/1535-7163.MCT-11-0182 WOS:000294668900012. 21709130

20. Gang EJ, Hsieh YT, Pham J, Zhao Y, Nguyen C, Huantes S, et al. Small-molecule inhibition of CBP/catenin interactions eliminates drug-resistant clones in acute lymphoblastic leukemia. Oncogene. 2014;33(17):2169–78. doi: 10.1038/onc.2013.169 WOS:000334996000003. 23728349

21. Chan KC, Chan LS, Ip JC, Lo C, Yip TT, Ngan RK, et al. Therapeutic targeting of CBP/beta-catenin signaling reduces cancer stem-like population and synergistically suppresses growth of EBV-positive nasopharyngeal carcinoma cells with cisplatin. Sci Rep. 2015;5:9979. Epub 2015/04/22. doi: 10.1038/srep09979 25897700; PubMed Central PMCID: PMC4404684.

22. Legube G, Trouche D. Regulating histone acetyltransferases and deacetylases. EMBO Rep. 2003;4(10):944–7. Epub 2003/10/07. doi: 10.1038/sj.embor.embor941 14528264; PubMed Central PMCID: PMC1326399.

23. Schwartz C, Beck K, Mink S, Schmolke M, Budde B, Wenning D, et al. Recruitment of p300 by C/EBPbeta triggers phosphorylation of p300 and modulates coactivator activity. EMBO J. 2003;22(4):882–92. Epub 2003/02/08. doi: 10.1093/emboj/cdg076 12574124; PubMed Central PMCID: PMC145436.

24. Ceschin DG, Walia M, Wenk SS, Duboe C, Gaudon C, Xiao Y, et al. Methylation specifies distinct estrogen-induced binding site repertoires of CBP to chromatin. Genes Dev. 2011;25(11):1132–46. Epub 2011/06/03. doi: 10.1101/gad.619211 PubMed Central PMCID: PMC3110952. 21632823

25. Joo HY, Jones A, Yang C, Zhai L, Smith ADt, Zhang Z, et al. Regulation of histone H2A and H2B deubiquitination and Xenopus development by USP12 and USP46. J Biol Chem. 2011;286(9):7190–201. Epub 2010/12/25. doi: 10.1074/jbc.M110.158311 21183687; PubMed Central PMCID: PMC3044976.

26. Moretti J, Chastagner P, Liang CC, Cohn MA, Israel A, Brou C. The Ubiquitin-specific Protease 12 (USP12) Is a Negative Regulator of Notch Signaling Acting on Notch Receptor Trafficking toward Degradation. J Biol Chem. 2012;287(35):29429–41. doi: 10.1074/jbc.M112.366807 WOS:000308286900021. 22778262

27. Jahan AS, Lestra M, Swee LK, Fan Y, Lamers MM, Tafesse FG, et al. Usp12 stabilizes the T-cell receptor complex at the cell surface during signaling. P Natl Acad Sci USA. 2016;113(6):E705–E14. doi: 10.1073/pnas.1521763113 WOS:000369571700007. 26811477

28. Tang XL, Gao JS, Guan YJ, McLane KE, Yuan ZL, Ramratnam B, et al. Acetylation-dependent signal transduction for type I interferon receptor. Cell. 2007;131(1):93–105. doi: 10.1016/j.cell.2007.07.034 WOS:000249934700014. 17923090

29. Cohn MA, Kee Y, Haas W, Gygi SP, D'Andrea AD. UAF1 Is a Subunit of Multiple Deubiquitinating Enzyme Complexes. J Biol Chem. 2009;284(8):5343–51. doi: 10.1074/jbc.M808430200 WOS:000263416600064. 19075014

30. Aron R, Pellegrini P, Green EW, Maddison DC, Opoku-Nsiah K, Wong JS, et al. Deubiquitinase Usp12 functions noncatalytically to induce autophagy and confer neuroprotection in models of Huntington's disease. Nat Commun. 2018;9(1):3191. Epub 2018/09/30. doi: 10.1038/s41467-018-05653-z 30266909; PubMed Central PMCID: PMC6162324.

31. Xu W, Chen HW, Du KY, Asahara H, Tini M, Emerson BM, et al. A transcriptional switch mediated by cofactor methylation. Science. 2001;294(5551):2507–11. doi: 10.1126/science.1065961 WOS:000172927700046. 11701890

32. Thompson PR, Wang DX, Wang L, Fulco M, Pediconi N, Zhang DZ, et al. Regulation of the p300 HAT domain via a novel activation loop. Nat Struct Mol Biol. 2004;11(4):308–15. doi: 10.1038/nsmb740 WOS:000220692900013. 15004546

33. Karukurichi KR, Wang L, Uzasci L, Manlandro CM, Wang Q, Cole PA. Analysis of p300/CBP Histone Acetyltransferase Regulation Using Circular Permutation and Semisynthesis. J Am Chem Soc. 2010;132(4):1222–+. doi: 10.1021/ja909466d WOS:000275084800021. 20063892

34. Arany Z, Newsome D, Oldread E, Livingston DM, Eckner R. A family of transcriptional adaptor proteins targeted by the E1A oncoprotein. Nature. 1995;374(6517):81–4. Epub 1995/03/02. doi: 10.1038/374081a0 7870178.

35. Kwok RPS, Laurance ME, Lundblad JR, Goldman PS, Shih HM, Connor LM, et al. Control of cAMP-regulated enhancers by the viral transactivator Tax through CREB and the co-activator CBP. Nature. 1996;380(6575):642–6. doi: 10.1038/380642a0 WOS:A1996UF74100051. 8602268

36. Chakravarti D, Ogryzko V, Kao HY, Nash A, Chen H, Nakatani Y, et al. A viral mechanism for inhibition of p300 and PCAF acetyltransferase activity. Cell. 1999;96(3):393–403. Epub 1999/02/20. doi: 10.1016/s0092-8674(00)80552-8 10025405.