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Coronaviruses

Structure of the multiple functional domains from coronavirus nonstructural protein 3

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 66-80 | Received 10 Aug 2020, Accepted 15 Dec 2020, Published online: 17 Jan 2021

References

  • Gorbalenya AE, Enjuanes L, Ziebuhr J, et al. Nidovirales: evolving the largest RNA virus genome. Virus Res. 2006 Apr;117(1):17–37.
  • Weiss SR, Leibowitz JL. Coronavirus pathogenesis. Adv Virus Res. 2011;81:85–164.
  • Fehr AR, Channappanavar R, Jankevicius G, et al. The conserved coronavirus macrodomain promotes virulence and suppresses the innate immune response during severe acute respiratory syndrome coronavirus infection. MBio. 2016 Dec 13;7(6):e01721-16.
  • Wang C, Horby PW, Hayden FG, et al. A novel coronavirus outbreak of global health concern. Lancet. 2020 Feb 15;395(10223):470–473.
  • Lei J, Kusov Y, Hilgenfeld R. Nsp3 of coronaviruses: structures and functions of a large multi-domain protein. Antiviral Res. 2018 Jan;149:58–74.
  • Balint A, Farsang A, Zadori Z, et al. Molecular characterization of feline infectious peritonitis virus strain DF-2 and studies of the role of ORF3abc in viral cell tropism. J Virol. 2012 Jun;86(11):6258–6267.
  • Brian DA, Baric RS. Coronavirus genome structure and replication. Curr Top Microbiol Immunol. 2005;287:1–30.
  • Ziebuhr J. The coronavirus replicase. Curr Top Microbiol Immunol. 2005;287:57–94.
  • Thiel V, Herold J, Schelle B, et al. Viral replicase gene products suffice for coronavirus discontinuous transcription. J Virol. 2001 Jul;75(14):6676–6681.
  • Neuman BW. Bioinformatics and functional analyses of coronavirus nonstructural proteins involved in the formation of replicative organelles. Antiviral Res. 2016 Nov;135:97–107.
  • Zeng Z, Deng F, Shi K, et al. Dimerization of coronavirus nsp9 with diverse modes enhances its nucleic acid binding affinity. J Virol. 2018 Sep 1;92(17):e00692-18.
  • Han W, Li X, Fu X. The macro domain protein family: structure, functions, and their potential therapeutic implications. Mutat Res. 2011 May–Jun;727(3):86–103.
  • Gorbalenya AE, Koonin EV, Lai MM. Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi- and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-, alpha- and coronaviruses. FEBS Lett. 1991 Aug 19;288(1–2):201–205.
  • Koonin EV, Gorbalenya AE, Purdy MA, et al. Computer-assisted assignment of functional domains in the nonstructural polyprotein of hepatitis E virus: delineation of an additional group of positive-strand RNA plant and animal viruses. Proc Natl Acad Sci USA. 1992 Sep 1;89(17):8259–8263.
  • Chakravarthy S, Gundimella SK, Caron C, et al. Structural characterization of the histone variant macroH2A. Mol Cell Biol. 2005 Sep;25(17):7616–7624.
  • Cho CC, Lin MH, Chuang CY, et al. Macro domain from middle east respiratory syndrome coronavirus (MERS-CoV) is an efficient ADP-ribose binding module: crystal structure and biochemical studies. J Biol Chem. 2016 Mar 4;291(10):4894–4902.
  • Xu Y, Cong L, Chen C, et al. Crystal structures of two coronavirus ADP-ribose-1''-monophosphatases and their complexes with ADP-ribose: a systematic structural analysis of the viral ADRP domain. J Virol. 2009 Jan;83(2):1083–1092.
  • Putics A, Gorbalenya AE, Ziebuhr J. Identification of protease and ADP-ribose 1''-monophosphatase activities associated with transmissible gastroenteritis virus non-structural protein 3. J Gen Virol. 2006 Mar;87(Pt 3):651–656.
  • Kuri T, Eriksson KK, Putics A, et al. The ADP-ribose-1''-monophosphatase domains of severe acute respiratory syndrome coronavirus and human coronavirus 229E mediate resistance to antiviral interferon responses. J Gen Virol. 2011 Aug;92(Pt 8):1899–1905.
  • Deng X, Mettelman RC, O'Brien A, et al. Analysis of coronavirus temperature-sensitive mutants reveals an interplay between the macrodomain and papain-like protease impacting replication and pathogenesis. J Virol. 2019 Jun 15;93(12):e02140-18.
  • Wojdyla JA, Manolaridis I, Snijder EJ, et al. Structure of the X (ADRP) domain of nsp3 from feline coronavirus. Acta Crystallogr D Biol Crystallogr. 2009 Dec;65(Pt 12):1292–1300.
  • Egloff MP, Malet H, Putics A, et al. Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains. J Virol. 2006 Sep;80(17):8493–8502.
  • Lin MH, Chang SC, Chiu YC, et al. Structural, biophysical, and biochemical elucidation of the SARS-CoV-2 nonstructural protein 3 macro domain. ACS Infect Dis. 2020 Nov 13;6(11):2970–2978.
  • Kong L, Shaw N, Yan L, et al. Structural view and substrate specificity of papain-like protease from avian infectious bronchitis virus. J Biol Chem. 2015 Mar 13;290(11):7160–7168.
  • Chen Y, Savinov SN, Mielech AM, et al. X-ray structural and functional studies of the three tandemly linked domains of non-structural protein 3 (nsp3) from murine hepatitis virus reveal conserved functions. J Biol Chem. 2015 Oct 16;290(42):25293–25306.
  • Wojdyla JA, Manolaridis I, van Kasteren PB, et al. Papain-like protease 1 from transmissible gastroenteritis virus: crystal structure and enzymatic activity toward viral and cellular substrates. J Virol. 2010 Oct;84(19):10063–10073.
  • Ratia K, Saikatendu KS, Santarsiero BD, et al. Severe acute respiratory syndrome coronavirus papain-like protease: structure of a viral deubiquitinating enzyme. Proc Natl Acad Sci USA. 2006 Apr 11;103(15):5717–5722.
  • Bailey-Elkin BA, Knaap RC, Johnson GG, et al. Crystal structure of the middle east respiratory syndrome coronavirus (MERS-CoV) papain-like protease bound to ubiquitin facilitates targeted disruption of deubiquitinating activity to demonstrate its role in innate immune suppression. J Biol Chem. 2014 Dec 12;289(50):34667–34682.
  • Niemeyer D, Mosbauer K, Klein EM, et al. The papain-like protease determines a virulence trait that varies among members of the SARS-coronavirus species. PLoS Pathog. 2018 Sep;14(9):e1007296.
  • Mielech AM, Chen Y, Mesecar AD, et al. Nidovirus papain-like proteases: multifunctional enzymes with protease, deubiquitinating and deISGylating activities. Virus Res. 2014 Dec 19;194:184–190.
  • Lei J, Hilgenfeld R. Structural and mutational analysis of the interaction between the middle-east respiratory syndrome coronavirus (MERS-CoV) papain-like protease and human ubiquitin. Virol Sin. 2016 Aug;31(4):288–299.
  • Jeon YJ, Yoo HM, Chung CH. ISG15 and immune diseases. Biochim Biophys Acta. 2010 May;1802(5):485–496.
  • Clementz MA, Chen Z, Banach BS, et al. Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J Virol. 2010 May;84(9):4619–4629.
  • Herold J, Siddell SG, Gorbalenya AE. A human RNA viral cysteine proteinase that depends upon a unique Zn2+-binding finger connecting the two domains of a papain-like fold. J Biol Chem. 1999 May 21;274(21):14918–14925.
  • van Kasteren PB, Bailey-Elkin BA, James TW, et al. Deubiquitinase function of arterivirus papain-like protease 2 suppresses the innate immune response in infected host cells. Proc Natl Acad Sci USA. 2013 Feb 26;110(9):E838–E847.
  • Pfoh R, Lacdao IK, Georges AA, et al. Crystal structure of USP7 ubiquitin-like domains with an ICP0 peptide reveals a novel mechanism used by viral and cellular proteins to target USP7. PLoS Pathog. 2015 Jun;11(6):e1004950.
  • Mielech AM, Deng X, Chen Y, et al. Murine coronavirus ubiquitin-like domain is important for papain-like protease stability and viral pathogenesis. J Virol. 2015 May;89(9):4907–4917.
  • Minor W, Cymborowski M, Otwinowski Z, et al. HKL-3000: the integration of data reduction and structure solution–from diffraction images to an initial model in minutes. Acta Crystallogr D Biol Crystallogr. 2006 Aug;62(Pt 8):859–866.
  • McCoy AJ, Grosse-Kunstleve RW, Adams PD, et al. Phaser crystallographic software. J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658–674.
  • Adams PD, Grosse-Kunstleve RW, Hung LW, et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr. 2002 Nov;58(Pt 11):1948–1954.
  • Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126–2132.
  • Grell L, Parkin C, Slatest L, et al. EZ-Viz, a tool for simplifying molecular viewing in PyMOL. Biochem Mol Biol Educ. 2006 Nov;34(6):402–407.
  • Larkin MA, Blackshields G, Brown NP, et al. Clustal W and clustal X version 2.0. Bioinformatics. 2007 Nov 1;23(21):2947–2948.
  • Robert X, Gouet P. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res. 2014 Jul;42:W320–W324.
  • Franke D, Petoukhov MV, Konarev PV, et al. ATSAS 2.8: a comprehensive data analysis suite for small-angle scattering from macromolecular solutions. J Appl Crystallogr. 2017 Aug 1;50(Pt 4):1212–1225.
  • Bekes M, Ekkebus R, Ovaa H, et al. Recognition of Lys48-linked Di-ubiquitin and deubiquitinating activities of the SARS coronavirus papain-like protease. Mol Cell. 2016 May 19;62(4):572–585.
  • Saikatendu KS, Joseph JS, Subramanian V, et al. Structural basis of severe acute respiratory syndrome coronavirus ADP-ribose-1''-phosphate dephosphorylation by a conserved domain of nsP3. Structure. 2005 Nov;13(11):1665–1675.
  • Hu M, Li P, Song L, et al. Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14. EMBO J. 2005 Nov 2;24(21):3747–3756.
  • Barretto N, Jukneliene D, Ratia K, et al. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. J Virol. 2005 Dec;79(24):15189–15198.
  • Hu M, Li P, Li M, et al. Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde. Cell. 2002 Dec 27;111(7):1041–1054.
  • Tan J, Vonrhein C, Smart OS, et al. The SARS-unique domain (SUD) of SARS coronavirus contains two macrodomains that bind G-quadruplexes. PLoS Pathog. 2009 May;5(5):e1000428.
  • Woo PC, Lau SK, Lam CS, et al. Discovery of seven novel mammalian and avian coronaviruses in the genus deltacoronavirus supports bat coronaviruses as the gene source of alphacoronavirus and betacoronavirus and avian coronaviruses as the gene source of gammacoronavirus and deltacoronavirus. J Virol. 2012 Apr;86(7):3995–4008.
  • Alfuwaires M, Altaher A, Kandeel M. Molecular dynamic studies of interferon and innate immunity resistance in MERS CoV non-structural protein 3. Biol Pharm Bull. 2017;40(3):345–351.
  • Lindner HA, Lytvyn V, Qi H, et al. Selectivity in ISG15 and ubiquitin recognition by the SARS coronavirus papain-like protease. Arch Biochem Biophys. 2007 Oct 1;466(1):8–14.
  • Wolff G, Limpens R, Zevenhoven-Dobbe JC, et al. A molecular pore spans the double membrane of the coronavirus replication organelle. Science. 2020 Sep 11;369(6509):1395–1398.
  • Serrano P, Johnson MA, Almeida MS, et al. Nuclear magnetic resonance structure of the N-terminal domain of nonstructural protein 3 from the severe acute respiratory syndrome coronavirus. J Virol. 2007 Nov;81(21):12049–12060.
  • Shin D, Mukherjee R, Grewe D, et al. Papain-like protease regulates SARS-CoV-2 viral spread and innate immunity. Nature. 2020 Nov;587(7835):657–662.
  • Rut W, Lv Z, Zmudzinski M, et al. Activity profiling and crystal structures of inhibitor-bound SARS-CoV-2 papain-like protease: a framework for anti-COVID-19 drug design. Sci Adv. 2020 Oct;6(42).
  • Klemm T, Ebert G, Calleja DJ, et al. Mechanism and inhibition of the papain-like protease, PLpro, of SARS-CoV-2. EMBO J 2020 Aug 26;39(18):e106275.
  • Lee H, Lei H, Santarsiero BD, et al. Inhibitor recognition specificity of MERS-CoV papain-like protease may differ from that of SARS-CoV. ACS Chem Biol. 2015 Jun 19;10(6):1456–1465.