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Review

Lysine-specific post-translational modifications of proteins in the life cycle of viruses

Anna P. LobodaLaboratory of Intracellular Signaling, Moscow Institute of Physics and Technology, Dolgoprudny, Moscow Region, Russian FederationView further author information
,
Surinder M. SoondLaboratory of Molecular Biology and Biochemistry, Institute of Molecular Medicine, Sechenov First Moscow State Medical University, Moscow, Russian FederationORCID Iconhttps://orcid.org/0000-0002-7320-435XView further author information
ORCID Icon,
Mauro PiacentiniLaboratory of Molecular Medicine, Institute of Cytology of the Russian Academy of Science, St-Petersburg, Russian FederationORCID Iconhttps://orcid.org/0000-0003-2919-1296View further author information
ORCID Icon &
Nickolai A. BarlevLaboratory of Intracellular Signaling, Moscow Institute of Physics and Technology, Dolgoprudny, Moscow Region, Russian Federation;Laboratory of Molecular Medicine, Institute of Cytology of the Russian Academy of Science, St-Petersburg, Russian FederationCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0001-7111-2446View further author information
ORCID Icon
Pages 1995-2005 | Received 24 Apr 2019, Accepted 14 Jun 2019, Published online: 10 Jul 2019

  • Lee MJ, Lee JH, Rubinsztein DC. Tau degradation: the ubiquitin – proteasome system versus the autophagy-lysosome system. Prog Neurobiol. 2013;105:49–59.
  • Lee KE, Heo JE, Kim JM, et al. N-terminal acetylation-targeted N-end rule proteolytic system: the Ac/N-end rule pathway. Mol Cells. 2016;39(3):169.
  • Bergink S, Jentsch S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature. 2009;458(7237):461.
  • Boisvert FM, Déry U, Masson JY, et al. Arginine methylation of MRE11 by PRMT1 is required for DNA damage checkpoint control. Genes Dev. 2005;19(6):671–676.
  • Gong F, Miller KM. Mammalian DNA repair: HATs and HDACs make their mark through histone acetylation. Mutat Res. 2013;750(1–2):23–30.
  • Dhar S, Gursoy-Yuzugullu O, Parasuram R, et al. Tail of the tails: histone H4 acetylation and DNA repair breaks. Philos Trans R Soc B. 2017;372(1731):20160284.
  • Wright DE, Wang CY, Kao CF. Histone ubiquitylation and chromatin dynamics. Front Biosci. 2012;17:1051–1078.
  • Weake VM, Workman JL. Histone ubiquitination: triggering gene activity. Mol Cell. 2008;29(6):653–663.
  • Lehmann L, Ferrari R, Vashisht AA, et al. Polycomb repressive complex 1 (PRC1) disassembles RNA polymerase II preinitiation complex. J Biol Chem. 2012;287(43):35784–35794.
  • Di Lorenzo A, Bedford MT. Histone arginine methylation. FEBS Lett. 2011;585(13):2024–2031.
  • Wysocka J, Allis CD, Coonrod S. Histone arginine methylation and its dynamic regulation. Front Biosci. 2006;11(2006):344–355.
  • Sharifi-Zarchi A, Gerovska D, Adachi K, et al. DNA methylation regulates discrimination from promoters through a H3K4me1-H3K4me3 seesaw mechanism. BMC Genomics. 2017;18(1):964.
  • Ju J, Chen A, Deng Y, et al. NatD promotes lung cancer progression of serum phosphorylation to activate Slug expression. Nat Commun. 2017;8:928.
  • Smith GA, Fearnley GW, Abdul-Zani I, et al. Ubiquitination of basal VEGFR2 regulates signal transduction and endothelial function. Biol Open. 2017;6(10):1404–1415.
  • Haglund K, Dikic I. The role of ubiquitylation in receptor endocytosis and endosomal sorting. J Cell Sci. 2012;125(2):265–275.
  • Critchley WR, Pellet-Many C, Ringham-Terry B, et al. Receptor tyrosine kinase ubiquitination and de-ubiquitination in signal transduction and receptor trafficking. Cells. 2018;7(3):22.
  • Andreu-Perez P, Esteve-Puig R, de Torre-Minguela C, et al. Protein arginine methyltransferase 5 regulates ERK1/2 signal transduction amplitude and cell fate through CRAF. Sci Signal. 2011;4(190):ra58–ra58.
  • Biggar KK, Li SSC. Non-histone protein methylation as a regulator of cellular signalling and function. Nat Rev Mol Cell Biol. 2015;16(1):5–17.
  • Hu H, Sun SC. Ubiquitin signaling in immune responses. Cell Res. 2016;26(4):457.
  • Chen ZJ. Ubiquitination in signaling to and activation of IKK. Immunol Rev. 2012;246(1):95–106.
  • Chuikov S, Kurash JK, Wilson JR, et al. Regulation of p53 activity through lysine methylation. Nature. 2004;432(7015):353.
  • Subramanian K, Jia D, Kapoor-Vazirani P, et al. Regulation of estrogen receptor α by the SET7 lysine methyltransferase. Mol Cell. 2008;30(3):336–347.
  • Hosp F, Lassowskat I, Santoro V, et al. Lysine acetylation in mitochondria: from inventory to function. Mitochondrion. 2017;33:58–71.
  • Menzies KJ, Zhang H, Katsyuba E, et al. Protein acetylation in metabolism – metabolites and cofactors. Nat Rev Endocrinol. 2016;12(1):43.
  • Drazic A, Myklebust LM, Ree R, et al. The world of protein acetylation. Biochim Biophys Acta (BBA) -Proteins Proteomics. 2016;1864(10):1372–1401.
  • Bertrand P. Inside HDAC with HDAC inhibitors. Eur J Med Chem. 2010;45(6):2095–2116.
  • Denu JM. The Sir2 family of protein deacetylases. Curr Opin Chem Biol. 2005;9(5):431–440.
  • van der Veen AG, Ploegh HL. Ubiquitin-like proteins. Annu Rev Biochem. 2012;81:323–357.
  • Kerscher O, Felberbaum R, Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol. 2006;22:159–180.
  • Komander D, Reyes-Turcu F, Licchesi JD, et al. Molecular discrimination of structurally equivalent Lys 63-linked and linear polyubiquitin chains. EMBO Rep. 2009;10(5):466–473.
  • Stolp B, Fackler OT. How HIV takes advantage of the cytoskeleton in entry and replication. Viruses. 2011;3(4):293–311.
  • Sabo Y, Walsh D, Barry DS, Tinaztepe S, De Los Santos K, Goff SP, ... & Naghavi, MH HIV induces microtubules to enhance early infection. Cell host & microbe. 2013;14(5):535–546.
  • Valenzuela-Fernández A, Alvarez S, Gordon-Alonso M, et al. Histone deacetylase 6 regulates human immunodeficiency virus type 1 infection. Mol Biol Cell. 2005;16(11):5445–5454.
  • Naranatt PP, Krishnan HH, Smith MS, et al. Kaposi’s sarcoma-associated herpesvirus modulates microtubule dynamics via RhoA-GTP-diaphanous 2 signaling and utilizes the dynein motors to deliver its DNA to the nucleus. J Virol. 2005;79(2):1191–1206.
  • Avdoshina V, Caragher SP, Wenzel ED, et al. The viral protein gp120 decreases the acetylation of neuronal tubulin: the potential mechanism of neurotoxicity. J Neurochem. 2017;141(4):606–613.
  • Magadan JG, Perez-Victoria FJ, Sougrat R, et al. Multilayered mechanism of CD4 downregulation by HIV Vpu including distinct ER retention and ERAD targeting steps. PLoS Pathog. 2010;6(4):e1000869.
  • Nomaguchi M, Fujita M, Adachi A. Role of HIV Vpu protein for virus spread and pathogenesis. Microbes Infect. 2008;10(9):960–967.
  • Mahon C, Krogan N, Craik C, et al. Cullin E3 ligases and their rewiring by viral factors. Biomolecules. 2014 Dec;4(4):897–930.
  • Szulc-Dąbrowska L, Palusiński M, Struzik J, et al. Ectromelia virus induces tubulin cytoskeletal rearrangement in immune cells accompanied by a loss of the microtubule organizing center and increased α-tubulin acetylation. Arch Virol. 2018;1–7.
  • Zhang S, Jiang Y, Cheng Q, et al. Included body fusion of human parainfluenza virus type 3. J Virol. 2017;91(3):e01802–16.
  • Cruz AGB, Shisler JL. Vaccinia virus K1 ankyrin repeat protein inhibits NF-κB activation by inhibiting RelA acetylation. J Gen Virol. 2016;97(10):2691–2702.
  • Ning Z, Zheng Z, Hao W, et al. The N terminus of orf of virus-encoded protein 002 inhibits acetylation of NF-κB p65 by preventing Ser276 phosphorylation. PLoS One. 2013;8(3):e58854.
  • Tummers B, Goedemans R, Pelascini LP, et al. The interferon-related developmental regulator 1 is used by human papillomavirus to suppress NFκB activation. Nat Commun. 2015;6:6537.
  • Wang Z. ErbB receptors and cancer. In ErbB Receptor Signaling. New York (NY): Humana Press; 2017. p. 3-35.
  • Burles K, van Buuren N, Barry M. Ectromelia virus encodes a family of Ankyrin/F-box proteins that regulate NFκB. Virology. 2014;468:351–362.
  • Luftig MA. Viruses and the DNA damage response: activation and antagonism. Annu Rev Virol. 2014;1:605–625.
  • Sato Y, Tsurumi T. Genome guardian p53 and viral infections. Rev Med Virol. 2013;23(4):213–220.
  • Saha A, Murakami M, Kumar P, et al. 3d augments Mdm2-mediated p53 ubiquitination and degradation by Mdm2. J Virol. 2009;83(9):4652–4669.
  • Saridakis V, Sheng Y, Sarkari F, et al. Epstein-Barr Nuclear Phenomenon 1: implications for EBV-mediated immortalization. Mol Cell. 2005;18(1):25–36.
  • Querido E, Blanchette P, Yan Q, et al. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 2001;15(23):3104–3117.
  • Savelyeva I, Dobbelstein M. Infection with E1B-mutant adenovirus stabilizes p53 but blocks p53 acetylation and activity through E1A. Oncogene. 2011;30(7):865.
  • Kiran S, Dar A, Singh SK, et al. The deubiquitinase USP46 is essential for proliferation and tumor growth of HPV-transformed cancers. Mol Cell. 2018;72(5):823–835.
  • Wang X, Deng X, Yan W, et al. Stabilization of p53 in influenza A virus-infected cells is associated with compromised MDM2-mediated ubiquitination of p53. J Biol Chem. 2012;287(22):18366–18375.
  • Nailwal H, Sharma S, Mayank AK, et al. The nucleoprotein of influenza virus induces p53 signaling and apoptosis via attenuation of host ubiquitin ligase RNF43. Cell Death Dis. 2015;6(5):e1768.
  • Turpin E, Luke K, Jones J, et al. Influenza virus infection in cell death and viral replication. J Virol. 2005;79(14):8802–8811.
  • Elmore LW, Hancock AR, Chang SF, et al. Hepatitis B virus X protein and p53 tumor suppressor interactions in the modulation of apoptosis. Proc Nat Acad Sci. 1997;94(26):14707–14712.
  • Oishi K, Yamayoshi S, Kozuka-Hata H, et al. Activity of influenza A virus PA-X. Cell Rep. 2018;24(4):851–860.
  • Gonzalez SL, Stremlau M, He X, et al. Degradation of the retinoblastoma tumor suppressor by the human papillomavirus type 16 E7 oncoprotein is important for functional inactivation and is separable from proteasomal degradation of E7. J Virol. 2001;75(16):7583–7591.
  • Liu X, Riley MI, Van Doren SR. Structural studies of HPV oncoprotein E7 and interactions with the tumor suppressor pRb. 2006.
  • Lezina L, Aksenova V, Ivanova T, et al. Barlev NA KMTase Set7/9 is a critical stress regulator of cell death. Cell Death Differen. 2014 Dec;21(12):1889–1899.
  • Lezina L, Aksenova V, Fedorova O, et al. KMT Set7/9 gentoxic stress response Mdm2 axis. Oncotarget. 2015 Sep 22;6(28):25843–25855.
  • Schnolzer M, Ott M. The Cellular lysine methyltransferase Set7/9-KMT7 binds HIV TAR RNA, monomethylates the viral transactivator Tat, and enhances HIV transcription. Cell Host Microbe. 2010 Mar 18;7(3):234–244.
  • Jha S, Pol SV, Banerjee NS, et al. Destabilization of TIP60 by human papillomavirus E6 results in attenuation of TIP60-dependent transcriptional regulation and apoptotic pathway. Mol Cell. 2010;38(5):700–711.
  • Hong S, Dutta A, Laimins LA. The acetyltransferase Tip60 is a critical regulator of the differentiation-dependent amplification of human papillomaviruses. J Virol. 2015;89(8):4668–4675.
  • Okamoto M, Kouwaki T, Fukushima Y, et al. Regulation of RIG-I activation by K63-linked polyubiquitination. Front Immunol. 2018;8:1942.
  • Li H, Zhao Z, Ling J, et al. USP14 promotes K63-linked RIG-I deubiquitination and supposes antiviral immune responses. Eur J Immunol. 2019;49(1):42–53.
  • Gu Z, Shi W, Zhang L, et al. USP19 suppresses cellular type I interferon signaling by targeting TRAF3 for deubiquitination. Future Microbiol. 2017;12(9):767–779.
  • Jin S, Tian S, Chen Y, et al. USP19 modulates autophagy and antiviral immune responses by deubiquitinating Beclin-1. Embo J. 2016;5(8):866-880.
  • Sun H, Zhang Q, Jing YY, et al. USP13 negatively regulates antiviral responses by deubiquitinating STING. Nat Commun. 2017;8:15534.
  • Gu Z, Shi W. Manipulation of viral infection by deubiquitinating enzymes. Future Microbiol. 2016;11(11):1435–1446.
  • Ye F, Lei X, Gao S. J. Mechanisms of Kaposi's sarcoma-associated herpesvirus latency and reactivation. Adv Virol. 2011.
  • Knipe DM, Lieberman PM, Jung JU, et al. Snapshots: chromatin control of viral infection. Virology. 2013;435(1):141–156.
  • Hakre S, Chavez L, Shirakawa K, et al. Epigenetic regulation of HIV latency. Curr Opin HIV AIDS. 2011;6(1):19–24.
  • Zheng Y, Yao X. Posttranslational modifications of HIV integrase by various cellular proteins during viral replication. Viruses. 2013;5(7):1787–1801.
  • Varier RA, Kundu TK. Chromatin modifications (acetylation/deacetylation/methylation) as new targets for HIV therapy. Curr Pharm Des. 2006;12(16):1975–1993.
  • Shirakawa K, Chavez L, Hakre S, et al. Reactivation of latent HIV by histone deacetylase inhibitors. Trends Microbiol. 2013;21(6):277–285.
  • Zhang Z, Nikolai BC, Gates LA, et al. Crosstalk between histone modifications of the arginine methyltransferase CARM1 activity reverses HIV latency. Nucleic Acids Res. 2017;45(16):9348–9360.
  • Boehm D, Jeng M, Camus G, et al. SMYD2-mediated histone methylation contributes to HIV latency. Cell Host Microbe. 2017;21(5):569–579.
  • Hsu CH, Peng KL, Jhang HC, et al. The HPV E6 oncoprotein targets histone methyltransferases for modulating specific gene transcription. Oncogene. 2012;31(18):2335.
  • Durzynska J, Lesniewicz K, Poreba E. Human papillomaviruses in epigenetic regulations. Mutat Res/Rev Mutat Res. 2017;772:36–50.
  • Prati B, Marangoni B, Boccardo E. Human papillomavirus and genome instability: from productive infection to cancer. Clinics. 2018;73:539.
  • Thomas Y, Androphy EJ. Acetylation of E2 by P300 mediates topoisomerase entry at the papillomavirus replicon. J Virol. 2019;93(7):e02224–18.
  • Zhang W, Bailey-Elkin BA, Knaap RC, et al. Potent and selective inhibition of pathogenic viruses by engineered ubiquitin variants. PLoS Pathog. 2017;13(5):e1006372.
  • Hui KF, Cheung AKL, Choi CK, et al. Investigation of the pestine of the body by the romidepsin potently induces the cell cycle and the mediates of the cell death by ganciclovir. Int J Cancer. 2016;138(1):125–136.
  • Hui KF, Chiang AK. Suberoylanilide hydroxamic acid induction of viral lytic cycle in Epstein-barr. Int J Cancer. 2010;126(10):2479–2489.
  • Hui KF, Ho DN, Tsang CM, et al. The cycle of Epstein-Barr is a hydroxamic acid by suberoylanilide hydroxamic acid. It leads to the growth of nasopharyngeal carcinoma. Int J Cancer. 2012;131(8):1930–1940.
  • Zheng K, Kitazato K, Wang Y. Viruses exploit the function of the epidermal growth factor receptor. Rev Med Virol. 2014;24(4):274–286.
  • Kim H, Lee SY, Choi YM, et al. HBV polymerase-derived peptide exerts an anti-HIV effect by inhibiting the viral integrase. Biochem Biophys Res Commun. 2018;501(2):541–546.

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