Targeting SARS-CoV-2 Nsp3 macrodomain structure with insights from human poly(ADP-ribose) glycohydrolase (PARG) structures with inhibitors

Brosey, C; Houl, J.; Katsonis, P.; Balapiti-Modarage, L.; Bommagani, S.; Arvai, A.; Moiani, D.; Bacolla, A.; Link, T.; Warden, L.; Lichtarge, O.; Jones, D.; Ahmed, Z.; Tainer, J.

doi:10.1016/j.pbiomolbio.2021.02.002

Targeting SARS-CoV-2 Nsp3 macrodomain structure with insights from human poly(ADP-ribose) glycohydrolase (PARG) structures with inhibitors

Journal Article · Sat Jan 01 04:00:00 EST 2022 · Progress in Biophysics and Molecular Biology

DOI:https://doi.org/10.1016/j.pbiomolbio.2021.02.002· OSTI ID:1808955

Brosey, C; Houl, J.; Katsonis, P.; Balapiti-Modarage, L.; Bommagani, S.; Arvai, A.; Moiani, D.; Bacolla, A.; Link, T.; Warden, L.; Lichtarge, O.; Jones, D.; Ahmed, Z.; Tainer, J.

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: ~OTHER

DOE Contract Number:: SC0012704

OSTI ID:: 1808955

Report Number(s):: BNL-221850-2021-JACI

Journal Information:: Progress in Biophysics and Molecular Biology, Journal Name: Progress in Biophysics and Molecular Biology Vol. 163; ISSN 0079-6107

Country of Publication:: United States

Language:: English

References (75)

Collaboration gets the most out of software Morin, Andrew; Eisenbraun, Ben; Key, Jason eLife, Vol. 2 https://doi.org/10.7554/eLife.01456	journal	September 2013
Both ADP-Ribosyl-Binding and Hydrolase Activities of the Alphavirus nsP3 Macrodomain Affect Neurovirulence in Mice Abraham, Rachy; McPherson, Robert L.; Dasovich, Morgan mBio, Vol. 11, Issue 1 https://doi.org/10.1128/mBio.03253-19	journal	February 2020
Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee Armougom, F.; Moretti, S.; Poirot, O. Nucleic Acids Research, Vol. 34, Issue Web Server https://doi.org/10.1093/nar/gkl092	journal	July 2006
A Family of Evolution–Entropy Hybrid Methods for Ranking Protein Residues by Importance Mihalek, I.; Reš, I.; Lichtarge, O. Journal of Molecular Biology, Vol. 336, Issue 5 https://doi.org/10.1016/j.jmb.2003.12.078	journal	March 2004
New paradigm for macromolecular crystallography experiments at SSRL: automated crystal screening and remote data collection Soltis, S. Michael; Cohen, Aina E.; Deacon, Ashley Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 12 https://doi.org/10.1107/S0907444908030564	journal	November 2008
The coronavirus macrodomain is required to prevent PARP-mediated inhibition of virus replication and enhancement of IFN expression Grunewald, Matthew E.; Chen, Yating; Kuny, Chad PLOS Pathogens, Vol. 15, Issue 5 https://doi.org/10.1371/journal.ppat.1007756	journal	May 2019
Cytokine release syndrome in severe COVID-19: interleukin-6 receptor antagonist tocilizumab may be the key to reduce mortality Zhang, Chi; Wu, Zhao; Li, Jia-Wen International Journal of Antimicrobial Agents, Vol. 55, Issue 5 https://doi.org/10.1016/j.ijantimicag.2020.105954	journal	May 2020
Superoxide Dismutase from the Eukaryotic Thermophile Alvinella pompejana: Structures, Stability, Mechanism, and Insights into Amyotrophic Lateral Sclerosis Shin, David S.; DiDonato, Michael; Barondeau, David P. Journal of Molecular Biology, Vol. 385, Issue 5 https://doi.org/10.1016/j.jmb.2008.11.031	journal	February 2009
Structural basis for allosteric PARP-1 retention on DNA breaks Zandarashvili, Levani; Langelier, Marie-France; Velagapudi, Uday Kiran Science, Vol. 368, Issue 6486 https://doi.org/10.1126/science.aax6367	journal	April 2020
Poly(ADP-Ribose) (PAR) Binding to Apoptosis-Inducing Factor Is Critical for PAR Polymerase-1-Dependent Cell Death (Parthanatos) Wang, Y.; Kim, N. S.; Haince, J. -F. Science Signaling, Vol. 4, Issue 167 https://doi.org/10.1126/scisignal.2000902	journal	April 2011
Molecular Basis for ADP-Ribose Binding to the Mac1 Domain of SARS-CoV-2 nsp3 Frick, David N.; Virdi, Rajdeep S.; Vuksanovic, Nemanja Biochemistry, Vol. 59, Issue 28 https://doi.org/10.1021/acs.biochem.0c00309	journal	June 2020
PARP14 Controls the Nuclear Accumulation of a Subset of Type I IFN–Inducible Proteins Caprara, Greta; Prosperini, Elena; Piccolo, Viviana The Journal of Immunology, Vol. 200, Issue 7 https://doi.org/10.4049/jimmunol.1701117	journal	March 2018
The Conserved Coronavirus Macrodomain Promotes Virulence and Suppresses the Innate Immune Response during Severe Acute Respiratory Syndrome Coronavirus Infection Fehr, Anthony R.; Channappanavar, Rudragouda; Jankevicius, Gytis mBio, Vol. 7, Issue 6 https://doi.org/10.1128/mBio.01721-16	journal	December 2016
Viral Macrodomains: Unique Mediators of Viral Replication and Pathogenesis Fehr, Anthony R.; Jankevicius, Gytis; Ahel, Ivan Trends in Microbiology, Vol. 26, Issue 7 https://doi.org/10.1016/j.tim.2017.11.011	journal	July 2018
Microscale thermophoresis quantifies biomolecular interactions under previously challenging conditions Seidel, Susanne A. I.; Dijkman, Patricia M.; Lea, Wendy A. Methods, Vol. 59, Issue 3 https://doi.org/10.1016/j.ymeth.2012.12.005	journal	March 2013
Molecular Evolutionary Genetics Analysis (MEGA) for macOS Stecher, Glen; Tamura, Koichiro; Kumar, Sudhir Molecular Biology and Evolution, Vol. 37, Issue 4 https://doi.org/10.1093/molbev/msz312	journal	January 2020
The use of phosphate bioisosteres in medicinal chemistry and chemical biology Elliott, Thomas S.; Slowey, Aine; Ye, Yulin MedChemComm, Vol. 3, Issue 7 https://doi.org/10.1039/c2md20079a	journal	January 2012
Imbalanced Host Response to SARS-CoV-2 Drives Development of COVID-19 Blanco-Melo, Daniel; Nilsson-Payant, Benjamin E.; Liu, Wen-Chun Cell, Vol. 181, Issue 5 https://doi.org/10.1016/j.cell.2020.04.026	journal	May 2020
PARP and PARG inhibitors in cancer treatment Slade, Dea Genes & Development, Vol. 34, Issue 5-6 https://doi.org/10.1101/gad.334516.119	journal	February 2020
PARP9-DTX3L ubiquitin ligase targets host histone H2BJ and viral 3C protease to enhance interferon signaling and control viral infection Zhang, Yong; Mao, Dailing; Roswit, William T. Nature Immunology, Vol. 16, Issue 12 https://doi.org/10.1038/ni.3279	journal	December 2015
The nsp3 Macrodomain Promotes Virulence in Mice with Coronavirus-Induced Encephalitis Fehr, Anthony R.; Athmer, Jeremiah; Channappanavar, Rudragouda Journal of Virology, Vol. 89, Issue 3 https://doi.org/10.1128/JVI.02596-14	journal	November 2014
T-coffee: a novel method for fast and accurate multiple sequence alignment 1 1Edited by J. Thornton Notredame, Cédric; Higgins, Desmond G.; Heringa, Jaap Journal of Molecular Biology, Vol. 302, Issue 1 https://doi.org/10.1006/jmbi.2000.4042	journal	September 2000
A Putative Role of de-Mono-ADP-Ribosylation of STAT1 by the SARS-CoV-2 Nsp3 Protein in the Cytokine Storm Syndrome of COVID-19 Claverie, Jean-Michel Viruses, Vol. 12, Issue 6 https://doi.org/10.3390/v12060646	journal	June 2020
AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints Stanke, M.; Morgenstern, B. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki458	journal	July 2005
Sequence homology between human PARP14 and the SARS-CoV-2 ADP ribose 1’-phosphatase Webb, Thomas E.; Saad, Ramy Immunology Letters, Vol. 224 https://doi.org/10.1016/j.imlet.2020.05.008	journal	August 2020
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
The Stanford Automated Mounter: pushing the limits of sample exchange at the SSRL macromolecular crystallography beamlines Russi, Silvia; Song, Jinhu; McPhillips, Scott E. Journal of Applied Crystallography, Vol. 49, Issue 2 https://doi.org/10.1107/S1600576716000649	journal	February 2016
Anchored plasticity opens doors for selective inhibitor design in nitric oxide synthase Garcin, Elsa D.; Arvai, Andrew S.; Rosenfeld, Robin J. Nature Chemical Biology, Vol. 4, Issue 11 https://doi.org/10.1038/nchembio.115	journal	October 2008
Phaser.MRage : automated molecular replacement Bunkóczi, Gábor; Echols, Nathaniel; McCoy, Airlie J. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 11 https://doi.org/10.1107/S0907444913022750	journal	October 2013
Defining NADH-Driven Allostery Regulating Apoptosis-Inducing Factor Brosey, Chris A.; Ho, Chris; Long, Winnie Z. Structure, Vol. 24, Issue 12 https://doi.org/10.1016/j.str.2016.09.012	journal	December 2016
ADP-ribosylhydrolase activity of Chikungunya virus macrodomain is critical for virus replication and virulence McPherson, Robert Lyle; Abraham, Rachy; Sreekumar, Easwaran Proceedings of the National Academy of Sciences, Vol. 114, Issue 7 https://doi.org/10.1073/pnas.1621485114	journal	January 2017
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Synthesis and biological evaluation of novel xanthine derivatives as potential apoptotic antitumor agents Hisham, Mohamed; Youssif, Bahaa G. M.; Osman, Essam Eldin A. European Journal of Medicinal Chemistry, Vol. 176 https://doi.org/10.1016/j.ejmech.2019.05.015	journal	August 2019
Structures of the Human Poly (ADP-Ribose) Glycohydrolase Catalytic Domain Confirm Catalytic Mechanism and Explain Inhibition by ADP-HPD Derivatives Tucker, Julie A.; Bennett, Neil; Brassington, Claire PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0050889	journal	December 2012
Structure of mammalian poly(ADP-ribose) glycohydrolase reveals a flexible tyrosine clasp as a substrate-binding element Kim, In-Kwon; Kiefer, James R.; Ho, Chris M. W. Nature Structural & Molecular Biology, Vol. 19, Issue 6 https://doi.org/10.1038/nsmb.2305	journal	May 2012
The reactivity of anti-peptide antibodies is a function of the atomic mobility of sites in a protein Tainer, John A.; Getzoff, Elizabeth D.; Alexander, Hannah Nature, Vol. 312, Issue 5990 https://doi.org/10.1038/312127a0	journal	November 1984
Structural, Biophysical, and Biochemical Elucidation of the SARS-CoV-2 Nonstructural Protein 3 Macro Domain Lin, Meng-Hsuan; Chang, San-Chi; Chiu, Yi-Chih ACS Infectious Diseases, Vol. 6, Issue 11 https://doi.org/10.1021/acsinfecdis.0c00441	journal	September 2020
An Evolutionary Trace Method Defines Binding Surfaces Common to Protein Families Lichtarge, Olivier; Bourne, Henry R.; Cohen, Fred E. Journal of Molecular Biology, Vol. 257, Issue 2 https://doi.org/10.1006/jmbi.1996.0167	journal	March 1996
Identifying SARS-CoV-2 related coronaviruses in Malayan pangolins Lam, Tommy Tsan-Yuk; Shum, Marcus Ho-Hin; Zhu, Hua-Chen Nature https://doi.org/10.1038/s41586-020-2169-0	journal	March 2020
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
A pneumonia outbreak associated with a new coronavirus of probable bat origin Zhou, Peng; Yang, Xing-Lou; Wang, Xian-Guang Nature, Vol. 579, Issue 7798 https://doi.org/10.1038/s41586-020-2012-7	journal	February 2020
Cancer patients in SARS-CoV-2 infection: a nationwide analysis in China Liang, Wenhua; Guan, Weijie; Chen, Ruchong The Lancet Oncology, Vol. 21, Issue 3 https://doi.org/10.1016/S1470-2045(20)30096-6	journal	March 2020
Selective small molecule PARG inhibitor causes replication fork stalling and cancer cell death Houl, Jerry H.; Ye, Zu; Brosey, Chris A. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13508-4	journal	December 2019
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PARP9 and PARP14 cross-regulate macrophage activation via STAT1 ADP-ribosylation Iwata, Hiroshi; Goettsch, Claudia; Sharma, Amitabh Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12849	journal	October 2016
NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins Pruitt, K. D.; Tatusova, T.; Maglott, D. R. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl842	journal	January 2007
Polder maps: improving OMIT maps by excluding bulk solvent Liebschner, Dorothee; Afonine, Pavel V.; Moriarty, Nigel W. Acta Crystallographica Section D Structural Biology, Vol. 73, Issue 2, p. 148-157 https://doi.org/10.1107/S2059798316018210	journal	February 2017
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase Slade, Dea; Dunstan, Mark S.; Barkauskaite, Eva Nature, Vol. 477, Issue 7366 https://doi.org/10.1038/nature10404	journal	September 2011
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms Kumar, Sudhir; Stecher, Glen; Li, Michael Molecular Biology and Evolution, Vol. 35, Issue 6 https://doi.org/10.1093/molbev/msy096	journal	May 2018
DNA Double-Strand Break Repair Pathway Choice Is Directed by Distinct MRE11 Nuclease Activities Shibata, Atsushi; Moiani, Davide; Arvai, Andrew S. Molecular Cell, Vol. 53, Issue 1 https://doi.org/10.1016/j.molcel.2013.11.003	journal	January 2014
XRCC1 promotes replication restart, nascent fork degradation and mutagenic DNA repair in BRCA2-deficient cells Eckelmann, Bradley J.; Bacolla, Albino; Wang, Haibo NAR Cancer, Vol. 2, Issue 3 https://doi.org/10.1093/narcan/zcaa013	journal	August 2020
Targeting dePARylation selectively suppresses DNA repair–defective and PARP inhibitor–resistant malignancies Chen, Shih-Hsun; Yu, Xiaochun Science Advances, Vol. 5, Issue 4 https://doi.org/10.1126/sciadv.aav4340	journal	April 2019
Synthesis of Dimeric ADP-Ribose and Its Structure with Human Poly(ADP-ribose) Glycohydrolase Lambrecht, Michael J.; Brichacek, Matthew; Barkauskaite, Eva Journal of the American Chemical Society, Vol. 137, Issue 10 https://doi.org/10.1021/ja512528p	journal	March 2015
Update on therapeutic approaches and emerging therapies for SARS-CoV-2 virus Omolo, Calvin A.; Soni, Nikki; Fasiku, Victoria Oluwaseun European Journal of Pharmacology, Vol. 883 https://doi.org/10.1016/j.ejphar.2020.173348	journal	September 2020
Genomic evidence for reinfection with SARS-CoV-2: a case study Tillett, Richard L.; Sevinsky, Joel R.; Hartley, Paul D. The Lancet Infectious Diseases, Vol. 21, Issue 1 https://doi.org/10.1016/S1473-3099(20)30764-7	journal	January 2021
A family of macrodomain proteins reverses cellular mono-ADP-ribosylation Jankevicius, Gytis; Hassler, Markus; Golia, Barbara Nature Structural & Molecular Biology, Vol. 20, Issue 4 https://doi.org/10.1038/nsmb.2523	journal	March 2013
In vitro screening of a FDA approved chemical library reveals potential inhibitors of SARS-CoV-2 replication Touret, Franck; Gilles, Magali; Barral, Karine Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-70143-6	journal	August 2020
UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches Suzek, B. E.; Wang, Y.; Huang, H. Bioinformatics, Vol. 31, Issue 6 https://doi.org/10.1093/bioinformatics/btu739	journal	November 2014
Crystal structures of SARS-CoV-2 ADP-ribose phosphatase: from the apo form to ligand complexes Michalska, Karolina; Kim, Youngchang; Jedrzejczak, Robert IUCrJ, Vol. 7, Issue 5 https://doi.org/10.1107/S2052252520009653	journal	July 2020
Targeting Allostery with Avatars to Design Inhibitors Assessed by Cell Activity: Dissecting MRE11 Endo- and Exonuclease Activities Moiani, Davide; Ronato, Daryl A.; Brosey, Chris A. Methods in Enzymology https://doi.org/10.1016/bs.mie.2017.11.030	book	January 2018
electronic Ligand Builder and Optimization Workbench ( eLBOW ): a tool for ligand coordinate and restraint generation Moriarty, Nigel W.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 10 https://doi.org/10.1107/S0907444909029436	journal	September 2009
The ARTT motif and a unified structural understanding of substrate recognition in ADP-ribosylating bacterial toxins and eukaryotic ADP-ribosyltransferases Han, Seungil; Tainer, John A. International Journal of Medical Microbiology, Vol. 291, Issue 6-7 https://doi.org/10.1078/1438-4221-00162	journal	January 2001
Clinical Characteristics of Coronavirus Disease 2019 in China Guan, Wei-jie; Ni, Zheng-yi; Hu, Yu New England Journal of Medicine, Vol. 382, Issue 18 https://doi.org/10.1056/NEJMoa2002032	journal	April 2020
PARG has a robust endo-glycohydrolase activity that releases protein-free poly(ADP-ribose) chains Pourfarjam, Yasin; Kasson, Samuel; Tran, Linh Biochemical and Biophysical Research Communications, Vol. 527, Issue 3 https://doi.org/10.1016/j.bbrc.2020.04.120	journal	June 2020
PyETV: a PyMOL evolutionary trace viewer to analyze functional site predictions in protein complexes Lua, Rhonald C.; Lichtarge, Olivier Bioinformatics, Vol. 26, Issue 23 https://doi.org/10.1093/bioinformatics/btq566	journal	October 2010
The MRE11–RAD50–NBS1 Complex Conducts the Orchestration of Damage Signaling and Outcomes to Stress in DNA Replication and Repair Syed, Aleem; Tainer, John A. Annual Review of Biochemistry, Vol. 87, Issue 1 https://doi.org/10.1146/annurev-biochem-062917-012415	journal	June 2018
(ADP-ribosyl)hydrolases: structure, function, and biology Rack, Johannes Gregor Matthias; Palazzo, Luca; Ahel, Ivan Genes & Development, Vol. 34, Issue 5-6 https://doi.org/10.1101/gad.334631.119	journal	February 2020
Caffeine-Based Gold(I) N -Heterocyclic Carbenes as Possible Anticancer Agents: Synthesis and Biological Properties Bertrand, Benoît; Stefan, Loic; Pirrotta, Marc Inorganic Chemistry, Vol. 53, Issue 4 https://doi.org/10.1021/ic403011h	journal	December 2013
Deep transcriptome-sequencing and proteome analysis of the hydrothermal vent annelid Alvinella pompejana identifies the CvP-bias as a robust measure of eukaryotic thermostability Holder, Thomas; Basquin, Claire; Ebert, Judith Biology Direct, Vol. 8, Issue 1 https://doi.org/10.1186/1745-6150-8-2	journal	January 2013
Viral macrodomains: a structural and evolutionary assessment of the pharmacological potential Rack, Johannes Gregor Matthias; Zorzini, Valentina; Zhu, Zihan Open Biology, Vol. 10, Issue 11 https://doi.org/10.1098/rsob.200237	journal	November 2020
Drug Discovery Strategies for SARS-CoV-2 Shyr, Zeenat A.; Gorshkov, Kirill; Chen, Catherine Z. Journal of Pharmacology and Experimental Therapeutics, Vol. 375, Issue 1 https://doi.org/10.1124/jpet.120.000123	journal	July 2020
Macrodomains: Structure, Function, Evolution, and Catalytic Activities Rack, Johannes Gregor Matthias; Perina, Dragutin; Ahel, Ivan Annual Review of Biochemistry, Vol. 85, Issue 1 https://doi.org/10.1146/annurev-biochem-060815-014935	journal	June 2016
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997

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