A Novel Recognition by the E3 Ubiquitin Ligase of HSV-1 ICP0 Enhances the Degradation of PML Isoform I to Prevent ND10 Reformation in Late Infection
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cells and Viruses
2.2. Construction of Recombinant HSV-1
2.3. Construction of HEp-2 TetOn Cell Lines Stably Expressing PML I Mutants
2.4. TetOn-Based Protein Half-Life Assay
2.5. PML I In Vivo Ubiquitination Assay
2.6. Western Blotting
2.7. Confocal Microscopy
2.8. One-Step Viral Growth Curve
2.9. Plasmids
2.10. Antibodies
3. Results
3.1. The Two Arms of the Bipartite PML I-Interaction Domain Redundantly Ubiquitinate PML I for Its Degradation
3.2. SIM362–364 Is Required for the Right Arm to Mediate the Ubiquitination and Degradation of PML I
3.3. The Right Arm of the Bipartite PML I-Interaction Domain Recognizes Only the SUMOylated PML I, While the Left Arm Mediates PML I Degradation Independent of SUMO-SIM Interaction
3.4. The Left Arm of the Bipartite PML I-Interaction Domain Functions When Moved Downstream of the RING Domain
3.5. Both Arms of the Bipartite PML I-Interaction Domain Add Heterologous Polyubiquitin Chains to PML I
3.6. PML I Mutant Not Localized at ND10 Is Degraded via the Left Arm of the Bipartite PML I-Interaction Domain
3.7. The Left Arm of Bipartite PML I-Interaction Domain Is Required for PML I to Be Degraded in the Cytoplasm in Late Infection
3.8. The Secondary Degradation of PML I Triggered by the Left Arm Prevents the Reformation of ND10 in Late Infection
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Rape, M. Ubiquitylation at the crossroads of development and disease. Nat. Rev. Mol. Cell Biol. 2018, 19, 59–70. [Google Scholar] [CrossRef]
- Haakonsen, D.L.; Rape, M. Branching Out: Improved Signaling by Heterotypic Ubiquitin Chains. Trends Cell Biol. 2019, 29, 704–716. [Google Scholar] [CrossRef]
- Swatek, K.N.; Komander, D. Ubiquitin modifications. Cell Res. 2016, 26, 399–422. [Google Scholar] [CrossRef] [Green Version]
- Gu, H.; Jan Fada, B. Specificity in Ubiquitination Triggered by Virus Infection. Int. J. Mol. Sci. 2020, 21, 4088. [Google Scholar] [CrossRef]
- Schneider, S.M.; Lee, B.H.; Nicola, A.V. Viral entry and the ubiquitin-proteasome system. Cell. Microbiol. 2021, 23, e13276. [Google Scholar] [CrossRef]
- Masucci, M.G. Viral Ubiquitin and Ubiquitin-Like Deconjugases-Swiss Army Knives for Infection. Biomolecules 2020, 10, 1137. [Google Scholar] [CrossRef]
- Lallemand-Breitenbach, V.; de The, H. PML nuclear bodies: From architecture to function. Curr. Opin. Cell Biol. 2018, 52, 154–161. [Google Scholar] [CrossRef]
- Bernardi, R.; Papa, A.; Pandolfi, P.P. Regulation of apoptosis by PML and the PML-NBs. Oncogene 2008, 27, 6299–6312. [Google Scholar] [CrossRef] [Green Version]
- Geoffroy, M.C.; Chelbi-Alix, M.K. Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res. Off. J. Int. Soc. Interferon Cytokine Res. 2011, 31, 145–158. [Google Scholar] [CrossRef] [Green Version]
- Van Damme, E.; Laukens, K.; Dang, T.H.; Van Ostade, X. A manually curated network of the PML nuclear body interactome reveals an important role for PML-NBs in SUMOylation dynamics. Int. J. Biol. Sci. 2010, 6, 51–67. [Google Scholar] [CrossRef]
- Guldner, H.H.; Szostecki, C.; Grötzinger, T.; Will, H. IFN enhance expression of Sp100, an autoantigen in primary biliary cirrhosis. J. Immunol. 1992, 149, 4067–4073. [Google Scholar] [CrossRef] [PubMed]
- Maul, G.G.; Guldner, H.H.; Spivack, J.G. Modification of discrete nuclear domains induced by herpes simplex virus type 1 immediate early gene 1 product (ICP0). J. Gen. Virol. 1993, 74 Pt 12, 2679–2690. [Google Scholar] [CrossRef] [PubMed]
- Chee, A.V.; Lopez, P.; Pandolfi, P.P.; Roizman, B. Promyelocytic leukemia protein mediates interferon-based anti-herpes simplex virus 1 effects. J. Virol. 2003, 77, 7101–7105. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lin, R.; Noyce, R.S.; Collins, S.E.; Everett, R.D.; Mossman, K.L. The herpes simplex virus ICP0 RING finger domain inhibits IRF3- and IRF7-mediated activation of interferon-stimulated genes. J. Virol. 2004, 78, 1675–1684. [Google Scholar] [CrossRef] [Green Version]
- Everett, R.D.; Orr, A. Herpes simplex virus type 1 regulatory protein ICP0 aids infection in cells with a preinduced interferon response but does not impede interferon-induced gene induction. J. Virol. 2009, 83, 4978–4983. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- van Lint, A.L.; Murawski, M.R.; Goodbody, R.E.; Severa, M.; Fitzgerald, K.A.; Finberg, R.W.; Knipe, D.M.; Kurt-Jones, E.A. Herpes simplex virus immediate-early ICP0 protein inhibits Toll-like receptor 2-dependent inflammatory responses and NF-kappaB signaling. J. Virol. 2010, 84, 10802–10811. [Google Scholar] [CrossRef] [Green Version]
- Gu, H.; Roizman, B. Herpes simplex virus-infected cell protein 0 blocks the silencing of viral DNA by dissociating histone deacetylases from the CoREST-REST complex. Proc. Natl. Acad. Sci. USA 2007, 104, 17134–17139. [Google Scholar] [CrossRef] [Green Version]
- Cliffe, A.R.; Knipe, D.M. Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. J. Virol. 2008, 82, 12030–12038. [Google Scholar] [CrossRef] [Green Version]
- Cohen, C.; Corpet, A.; Roubille, S.; Maroui, M.A.; Poccardi, N.; Rousseau, A.; Kleijwegt, C.; Binda, O.; Texier, P.; Sawtell, N.; et al. Promyelocytic leukemia (PML) nuclear bodies (NBs) induce latent/quiescent HSV-1 genomes chromatinization through a PML NB/Histone H3.3/H3.3 Chaperone Axis. PLoS Pathog. 2018, 14, e1007313. [Google Scholar] [CrossRef] [Green Version]
- Lilley, C.E.; Chaurushiya, M.S.; Boutell, C.; Everett, R.D.; Weitzman, M.D. The intrinsic antiviral defense to incoming HSV-1 genomes includes specific DNA repair proteins and is counteracted by the viral protein ICP0. PLoS Pathog. 2011, 7, e1002084. [Google Scholar] [CrossRef] [Green Version]
- Gross, S.; Catez, F.; Masumoto, H.; Lomonte, P. Centromere architecture breakdown induced by the viral E3 ubiquitin ligase ICP0 protein of herpes simplex virus type 1. PLoS ONE 2012, 7, e44227. [Google Scholar] [CrossRef] [Green Version]
- Gu, H.; Zheng, Y.; Roizman, B. The Interaction of Herpes Simplex Virus ICP0 with ND10 Bodies: A Sequential Process of Adhesion, Fusion and Retention. J. Virol. 2013, 87, 10244–10254. [Google Scholar] [CrossRef] [Green Version]
- Chelbi-Alix, M.K.; de The, H. Herpes virus induced proteasome-dependent degradation of the nuclear bodies-associated PML and Sp100 proteins. Oncogene 1999, 18, 935–941. [Google Scholar] [CrossRef] [Green Version]
- Scherer, M.; Stamminger, T. Emerging Role of PML Nuclear Bodies in Innate Immune Signaling. J. Virol. 2016, 90, 5850–5854. [Google Scholar] [CrossRef] [Green Version]
- Maul, G.G.; Ishov, A.M.; Everett, R.D. Nuclear domain 10 as preexisting potential replication start sites of herpes simplex virus type-1. Virology 1996, 217, 67–75. [Google Scholar] [CrossRef] [Green Version]
- Gu, H.; Zheng, Y. Role of ND10 nuclear bodies in the chromatin repression of HSV-1. Virol. J. 2016, 13, 62. [Google Scholar] [CrossRef] [Green Version]
- Jan Fada, B.; Reward, E.; Gu, H. The Role of ND10 Nuclear Bodies in Herpesvirus Infection: A Frenemy for the Virus? Viruses 2021, 13, 239. [Google Scholar] [CrossRef]
- Everett, R.D.; Rechter, S.; Papior, P.; Tavalai, N.; Stamminger, T.; Orr, A. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICP0. J. Virol. 2006, 80, 7995–8005. [Google Scholar] [CrossRef] [Green Version]
- Glass, M.; Everett, R.D. Components of promyelocytic leukemia nuclear bodies (ND10) act cooperatively to repress herpesvirus infection. J. Virol. 2013, 87, 2174–2185. [Google Scholar] [CrossRef] [Green Version]
- Gu, H.; Roizman, B. The two functions of herpes simplex virus 1 ICP0, inhibition of silencing by the CoREST/REST/HDAC complex and degradation of PML, are executed in tandem. J. Virol. 2009, 83, 181–187. [Google Scholar] [CrossRef] [Green Version]
- Ferenczy, M.W.; Ranayhossaini, D.J.; Deluca, N.A. Activities of ICP0 involved in the reversal of silencing of quiescent herpes simplex virus 1. J. Virol. 2011, 85, 4993–5002. [Google Scholar] [CrossRef] [Green Version]
- Hagglund, R.; Van Sant, C.; Lopez, P.; Roizman, B. Herpes simplex virus 1-infected cell protein 0 contains two E3 ubiquitin ligase sites specific for different E2 ubiquitin-conjugating enzymes. Proc. Natl. Acad. Sci. USA 2002, 99, 631–636. [Google Scholar] [CrossRef] [Green Version]
- Boutell, C.; Sadis, S.; Everett, R.D. Herpes simplex virus type 1 immediate-early protein ICP0 and is isolated RING finger domain act as ubiquitin E3 ligases in vitro. J. Virol. 2002, 76, 841–850. [Google Scholar] [CrossRef] [Green Version]
- Kim, E.T.; Dybas, J.M.; Kulej, K.; Reyes, E.D.; Price, A.M.; Akhtar, L.N.; Orr, A.; Garcia, B.A.; Boutell, C.; Weitzman, M.D. Comparative proteomics identifies Schlafen 5 (SLFN5) as a herpes simplex virus restriction factor that suppresses viral transcription. Nat. Microbiol. 2021, 6, 234–245. [Google Scholar] [CrossRef]
- Hou, F.; Sun, Z.; Deng, Y.; Chen, S.; Yang, X.; Ji, F.; Zhou, M.; Ren, K.; Pan, D. Interactome and Ubiquitinome Analyses Identify Functional Targets of Herpes Simplex Virus 1 Infected Cell Protein 0. Front. Microbiol. 2022, 13, 856471. [Google Scholar] [CrossRef]
- Zheng, Y.; Samrat, S.K.; Gu, H. A Tale of Two PMLs: Elements Regulating a Differential Substrate Recognition by the ICP0 E3 Ubiquitin Ligase of Herpes Simplex Virus 1. J. Virol. 2016, 90, 10875–10885. [Google Scholar] [CrossRef] [Green Version]
- Jan Fada, B.; Kaadi, E.; Samrat, S.K.; Zheng, Y.; Gu, H. Effect of SUMO-SIM Interaction on the ICP0-Mediated Degradation of PML Isoform II and Its Associated Proteins in Herpes Simplex Virus 1 Infection. J. Virol. 2020, 94, e00470-20. [Google Scholar] [CrossRef]
- Zheng, Y.; Gu, H. Identification of three redundant segments responsible for herpes simplex virus 1 ICP0 to fuse with ND10 nuclear bodies. J. Virol. 2015, 89, 4214–4226. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.T.; Liu, T.Y.; Shen, C.H.; Lin, S.Y.; Hung, C.C.; Hsu, L.C.; Chen, G.C. K48/K63-linked polyubiquitination of ATG9A by TRAF6 E3 ligase regulates oxidative stress-induced autophagy. Cell Rep. 2022, 38, 110354. [Google Scholar] [CrossRef]
- Samrat, S.K.; Ha, B.L.; Zheng, Y.; Gu, H. Characterization of Elements Regulating the Nuclear-to-Cytoplasmic Translocation of ICP0 in Late Herpes Simplex Virus 1 Infection. J. Virol. 2018, 92, e01673-17. [Google Scholar] [CrossRef] [Green Version]
- Shen, T.H.; Lin, H.K.; Scaglioni, P.P.; Yung, T.M.; Pandolfi, P.P. The mechanisms of PML-nuclear body formation. Mol. Cell 2006, 24, 331–339. [Google Scholar] [CrossRef] [Green Version]
- Wang, P.; Benhenda, S.; Wu, H.; Lallemand-Breitenbach, V.; Zhen, T.; Jollivet, F.; Peres, L.; Li, Y.; Chen, S.J.; Chen, Z.; et al. RING tetramerization is required for nuclear body biogenesis and PML sumoylation. Nat. Commun. 2018, 9, 1277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lopez, P.; Van Sant, C.; Roizman, B. Requirements for the nuclear-cytoplasmic translocation of infected-cell protein 0 of herpes simplex virus 1. J. Virol. 2001, 75, 3832–3840. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gu, H. Infected cell protein 0 functional domains and their coordination in herpes simplex virus replication. World J. Virol. 2016, 5, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez, M.C.; Dybas, J.M.; Hughes, J.; Weitzman, M.D.; Boutell, C. The HSV-1 ubiquitin ligase ICP0: Modifying the cellular proteome to promote infection. Virus Res. 2020, 285, 198015. [Google Scholar] [CrossRef] [PubMed]
- Banani, S.F.; Lee, H.O.; Hyman, A.A.; Rosen, M.K. Biomolecular condensates: Organizers of cellular biochemistry. Nat. Rev. Mol. Cell Biol. 2017, 18, 285–298. [Google Scholar] [CrossRef] [PubMed]
- Hirose, T.; Ninomiya, K.; Nakagawa, S.; Yamazaki, T. A guide to membraneless organelles and their various roles in gene regulation. Nat. Rev. Mol. Cell Biol. 2022, 24, 288–304. [Google Scholar] [CrossRef]
- Uggè, M.; Simoni, M.; Fracassi, C.; Bernardi, R. PML isoforms: A molecular basis for PML pleiotropic functions. Trends Biochem. Sci. 2022, 47, 609–619. [Google Scholar] [CrossRef]
- Mai, J.; Stubbe, M.; Hofmann, S.; Masser, S.; Dobner, T.; Boutell, C.; Groitl, P.; Schreiner, S. PML Alternative Splice Products Differentially Regulate HAdV Productive Infection. Microbiol. Spectr. 2022, 10, e0078522. [Google Scholar] [CrossRef]
- Nisole, S.; Maroui, M.A.; Mascle, X.H.; Aubry, M.; Chelbi-Alix, M.K. Differential Roles of PML Isoforms. Front. Oncol. 2013, 3, 125. [Google Scholar] [CrossRef] [Green Version]
- Wang, C.; Su, L.; Shao, Y.M.; Chen, W.Z.; Bu, N.; Hao, R.; Ma, L.Y.; Hussain, L.; Lu, X.Y.; Wang, Q.Q.; et al. Involvement of PML-I in reformation of PML nuclear bodies in acute promyelocytic leukemia cells by leptomycin B. Toxicol. Appl. Pharmacol. 2019, 384, 114775. [Google Scholar] [CrossRef] [PubMed]
- Xu, P.; Mallon, S.; Roizman, B. PML plays both inimical and beneficial roles in HSV-1 replication. Proc. Natl. Acad. Sci. USA 2016, 113, E3022–E3028. [Google Scholar] [CrossRef] [PubMed] [Green Version]
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Jan Fada, B.; Guha, U.; Zheng, Y.; Reward, E.; Kaadi, E.; Dourra, A.; Gu, H. A Novel Recognition by the E3 Ubiquitin Ligase of HSV-1 ICP0 Enhances the Degradation of PML Isoform I to Prevent ND10 Reformation in Late Infection. Viruses 2023, 15, 1070. https://doi.org/10.3390/v15051070
Jan Fada B, Guha U, Zheng Y, Reward E, Kaadi E, Dourra A, Gu H. A Novel Recognition by the E3 Ubiquitin Ligase of HSV-1 ICP0 Enhances the Degradation of PML Isoform I to Prevent ND10 Reformation in Late Infection. Viruses. 2023; 15(5):1070. https://doi.org/10.3390/v15051070
Chicago/Turabian StyleJan Fada, Behdokht, Udayan Guha, Yi Zheng, Eleazar Reward, Elie Kaadi, Ayette Dourra, and Haidong Gu. 2023. "A Novel Recognition by the E3 Ubiquitin Ligase of HSV-1 ICP0 Enhances the Degradation of PML Isoform I to Prevent ND10 Reformation in Late Infection" Viruses 15, no. 5: 1070. https://doi.org/10.3390/v15051070
APA StyleJan Fada, B., Guha, U., Zheng, Y., Reward, E., Kaadi, E., Dourra, A., & Gu, H. (2023). A Novel Recognition by the E3 Ubiquitin Ligase of HSV-1 ICP0 Enhances the Degradation of PML Isoform I to Prevent ND10 Reformation in Late Infection. Viruses, 15(5), 1070. https://doi.org/10.3390/v15051070