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PMID: 18852458 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

A noncovalent class of papain-like protease/deubiquitinase inhibitors blocks SARS virus replication.

Ratia K, Pegan S, Takayama J, Sleeman K, Coughlin M, Baliji S, Chaudhuri R, Fu W, Prabhakar BS, Johnson ME, Baker SC, Ghosh AK, Mesecar AD

Abstract

We report the discovery and optimization of a potent inhibitor against the papain-like protease (PLpro) from the coronavirus that causes severe acute respiratory syndrome (SARS-CoV). This unique protease is not only responsible for processing the viral polyprotein into its functional units but is also capable of cleaving ubiquitin and ISG15 conjugates and plays a significant role in helping SARS-CoV evade the human immune system. We screened a structurally diverse library of 50,080 compounds for inhibitors of PLpro and discovered a noncovalent lead inhibitor with an IC(50) value of 20 microM, which was improved to 600 nM via synthetic optimization. The resulting compound, GRL0617, inhibited SARS-CoV viral replication in Vero E6 cells with an EC(50) of 15 microM and had no associated cytotoxicity. The X-ray structure of PLpro in complex with GRL0617 indicates that the compound has a unique mode of inhibition whereby it binds within the S4-S3 subsites of the enzyme and induces a loop closure that shuts down catalysis at the active site. These findings provide proof-of-principle that PLpro is a viable target for development of antivirals directed against SARS-CoV, and that potent noncovalent cysteine protease inhibitors can be developed with specificity directed toward pathogenic deubiquitinating enzymes without inhibiting host DUBs.

MeSH Terms
Antiviral Agents/chemistry,classification,metabolism,pharmacology Coronavirus 3C Proteases Crystallography, X-Ray Cysteine Endopeptidases/chemistry,metabolism Endopeptidases/chemistry,metabolism Enzyme Inhibitors/chemistry,classification,metabolism,pharmacology Models, Molecular Protein Binding SARS Virus/drug effects,physiology Substrate Specificity Viral Proteins/antagonists & inhibitors,chemistry,metabolism Virus Replication/drug effects
Chemicals
Antiviral Agents Enzyme Inhibitors Viral Proteins Endopeptidases Cysteine Endopeptidases Coronavirus 3C Proteases ubiquitin isopeptidase
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Ratia Kiira
Center for Pharmaceutical Biotechnology and Department of Medicinal Chemistry and Pharmacognosy, University of Illinois, Chicago, IL 60607, USA.
Pegan Scott
Takayama Jun
Sleeman Katrina
Coughlin Melissa
Baliji Surendranath
Chaudhuri Rima
Fu Wentao
Prabhakar Bellur S
Johnson Michael E
Baker Susan C
Ghosh Arun K
Mesecar Andrew D
References (33)
33 references, click to expand
  1. Deubiquitination, a new function of the severe acute respiratory syndrome coronavirus papain-like protease?
    J Virol. 2005 Apr;79(7):4550-1 PMID: 15767458
  2. The coronavirus replicase.
    Curr Top Microbiol Immunol. 2005;287:57-94 PMID: 15609509
  3. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats.
    Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):14040-5 PMID: 16169905
  4. Bats are natural reservoirs of SARS-like coronaviruses.
    Science. 2005 Oct 28;310(5748):676-9 PMID: 16195424
  5. Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14.
    EMBO J. 2005 Nov 2;24(21):3747-56 PMID: 16211010
  6. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity.
    J Virol. 2005 Dec;79(24):15189-98 PMID: 16306590
  7. The papain-like protease from the severe acute respiratory syndrome coronavirus is a deubiquitinating enzyme.
    J Virol. 2005 Dec;79(24):15199-208 PMID: 16306591
  8. Binding site-based classification of coronaviral papain-like proteases.
    Proteins. 2006 Mar 15;62(3):760-75 PMID: 16358325
  9. Severe acute respiratory syndrome coronavirus papain-like protease: structure of a viral deubiquitinating enzyme.
    Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):5717-22 PMID: 16581910
  10. Structural basis of ubiquitin recognition by the deubiquitinating protease USP2.
    Structure. 2006 Aug;14(8):1293-302 PMID: 16905103
  11. Targeting proteases: successes, failures and future prospects.
    Nat Rev Drug Discov. 2006 Sep;5(9):785-99 PMID: 16955069
  12. Drug design targeting the main protease, the Achilles' heel of coronaviruses.
    Curr Pharm Des. 2006;12(35):4573-90 PMID: 17168763
  13. Structure of a herpesvirus-encoded cysteine protease reveals a unique class of deubiquitinating enzymes.
    Mol Cell. 2007 Mar 9;25(5):677-87 PMID: 17349955
  14. Deubiquitinating enzymes as novel anticancer targets.
    Future Oncol. 2007 Apr;3(2):191-9 PMID: 17381419
  15. Human coronavirus 229E papain-like proteases have overlapping specificities but distinct functions in viral replication.
    J Virol. 2007 Apr;81(8):3922-32 PMID: 17251282
  16. A detergent-based assay for the detection of promiscuous inhibitors.
    Nat Protoc. 2006;1(2):550-3 PMID: 17191086
  17. Deubiquitination in virus infection.
    Virology. 2007 Jun 5;362(2):245-56 PMID: 17291557
  18. Proteolytic processing and deubiquitinating activity of papain-like proteases of human coronavirus NL63.
    J Virol. 2007 Jun;81(11):6007-18 PMID: 17392370
  19. Selectivity in ISG15 and ubiquitin recognition by the SARS coronavirus papain-like protease.
    Arch Biochem Biophys. 2007 Oct 1;466(1):8-14 PMID: 17692280
  20. Mechanisms, biology and inhibitors of deubiquitinating enzymes.
    Nat Chem Biol. 2007 Nov;3(11):697-705 PMID: 17948018
  21. Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus.
    J Biol Chem. 2007 Nov 2;282(44):32208-21 PMID: 17761676
  22. Targeting ubiquitin specific proteases for drug discovery.
    Biochimie. 2008 Feb;90(2):270-83 PMID: 17961905
  23. A new model for protein stereospecificity.
    Nature. 2000 Feb 10;403(6770):614-5 PMID: 10688187
  24. A novel active site-directed probe specific for deubiquitylating enzymes reveals proteasome association of USP14.
    EMBO J. 2001 Sep 17;20(18):5187-96 PMID: 11566882
  25. Thiol-dependent enzymes and their inhibitors: a review.
    Curr Med Chem. 2002 May;9(9):979-1002 PMID: 11966457
  26. Protease inhibitors: current status and future prospects.
    J Med Chem. 2000 Feb 10;43(3):305-41 PMID: 10669559
  27. Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family.
    Chem Biol. 2002 Oct;9(10):1149-59 PMID: 12401499
  28. Crystal structure of a UBP-family deubiquitinating enzyme in isolation and in complex with ubiquitin aldehyde.
    Cell. 2002 Dec 27;111(7):1041-54 PMID: 12507430
  29. A novel coronavirus associated with severe acute respiratory syndrome.
    N Engl J Med. 2003 May 15;348(20):1953-66 PMID: 12690092
  30. Crystallographic structure at 1.6-A resolution of the human adenovirus proteinase in a covalent complex with its 11-amino-acid peptide cofactor: insights on a new fold.
    Biochim Biophys Acta. 2003 May 30;1648(1-2):1-11 PMID: 12758141
  31. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B.
    Nature. 2003 Jun 12;423(6941):773-7 PMID: 12802339
  32. Cloning and enzymatic analysis of 22 novel human ubiquitin-specific proteases.
    Biochem Biophys Res Commun. 2004 Jan 30;314(1):54-62 PMID: 14715245
  33. A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae.
    Mol Cell. 2005 Aug 19;19(4):547-57 PMID: 16109378
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2008-10-21
Epub
2008-00-13
Pages
16119-24
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2571001
Subset
IM
Grants
NIAID NIH HHS · P01 AI060915 · United States
NIGMS NIH HHS · R37 GM053386 · United States
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