Determining the molecular drivers of species-specific interferon-stimulated gene product 15 interactions with nairovirus ovarian tumor domain proteases

Dzimianski, John V.; Scholte, Florine E. M.; Williams, Isabelle L.; Langley, Caroline; Freitas, Brendan T.; Spengler, Jessica R.; Bergeron, Éric; Pegan, Scott D.

doi:10.1371/journal.pone.0226415

Title: Determining the molecular drivers of species-specific interferon-stimulated gene product 15 interactions with nairovirus ovarian tumor domain proteases

Journal Article · Mon Dec 23 00:00:00 EST 2019 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0226415· OSTI ID:1837272

Dzimianski, John V. ^[1];

^[2]; Williams, Isabelle L. ^[1];

^[1];

^[2];

^[1]

Univ. of Georgia, Athens, GA (United States). Dept. of Pharmaceutical and Biomedical Sciences
Centers for Disease Control and Prevention (CDC), Atlanta, GA (United States). Division of High Consequence Pathogens and Pathology. Viral Special Pathogens Branch

Tick-borne nairoviruses (order Bunyavirales) encode an ovarian tumor domain protease (OTU) that suppresses the innate immune response by reversing the post-translational modification of proteins by ubiquitin (Ub) and interferon-stimulated gene product 15 (ISG15). Ub is highly conserved across eukaryotes, whereas ISG15 is only present in vertebrates and shows substantial sequence diversity. Prior attempts to address the effect of ISG15 diversity on viral protein-ISG15 interactions have focused on only a single species’ ISG15 or a limited selection of nairovirus OTUs. To gain a more complete perspective of OTU-ISG15 interactions, we biochemically assessed the relative activities of 14 diverse nairovirus OTUs for 12 species’ ISG15 and found that ISG15 activity is predominantly restricted to particular nairovirus lineages reflecting, in general, known virus-host associations. To uncover the underlying molecular factors driving OTUs affinity for ISG15, X-ray crystal structures of Kupe virus and Ganjam virus OTUs bound to sheep ISG15 were solved and compared to complexes of Crimean-Congo hemorrhagic fever virus and Erve virus OTUs bound to human and mouse ISG15, respectively. Through mutational and structural analysis seven residues in ISG15 were identified that predominantly influence ISG15 species specificity among nairovirus OTUs. Additionally, OTU residues were identified that influence ISG15 preference, suggesting the potential for viral OTUs to adapt to different host ISG15s. These findings provide a foundation to further develop research methods to trace nairovirus-host relationships and delineate the full impact of ISG15 diversity on nairovirus infection.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-06CH11357; SC0012704

OSTI ID:: 1837272

Journal Information:: PLoS ONE, Vol. 14, Issue 12; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (66)

Structural basis of the specificity of USP18 toward ISG15 Basters, Anja; Geurink, Paul P.; Röcker, Annika Nature Structural & Molecular Biology, Vol. 24, Issue 3 https://doi.org/10.1038/nsmb.3371	journal	February 2017
The ISG15 Conjugation System Broadly Targets Newly Synthesized Proteins: Implications for the Antiviral Function of ISG15 Durfee, Larissa A.; Lyon, Nancy; Seo, Kyungwoon Molecular Cell, Vol. 38, Issue 5 https://doi.org/10.1016/j.molcel.2010.05.002	journal	June 2010
STAT2 is an essential adaptor in USP18-mediated suppression of type I interferon signaling Arimoto, Kei-ichiro; Löchte, Sara; Stoner, Samuel A. Nature Structural & Molecular Biology, Vol. 24, Issue 3 https://doi.org/10.1038/nsmb.3378	journal	February 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
Human intracellular ISG15 prevents interferon-α/β over-amplification and auto-inflammation Zhang, Xianqin; Bogunovic, Dusan; Payelle-Brogard, Béatrice Nature, Vol. 517, Issue 7532 https://doi.org/10.1038/nature13801	journal	October 2014
Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V. Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 1 https://doi.org/10.1107/S090744490705024X	journal	December 2007
Kupe Virus, a New Virus in the Family Bunyaviridae , Genus Nairovirus , Kenya Crabtree, Mary B.; Sang, Rosemary; Miller, Barry R. Emerging Infectious Diseases, Vol. 15, Issue 2 https://doi.org/10.3201/eid1502.080851	journal	February 2009
Structural basis for the sequence-specific recognition of human ISG15 by the NS1 protein of influenza B virus Guan, R.; Ma, L. -C.; Leonard, P. G. Proceedings of the National Academy of Sciences, Vol. 108, Issue 33 https://doi.org/10.1073/pnas.1107032108	journal	August 2011
Influenza B virus non-structural protein 1 counteracts ISG15 antiviral activity by sequestering ISGylated viral proteins Zhao, Chen; Sridharan, Haripriya; Chen, Ran Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12754	journal	September 2016
Inhibition of Interferon Induction and Action by the Nairovirus Nairobi Sheep Disease Virus/Ganjam Virus Holzer, Barbara; Bakshi, Siddharth; Bridgen, Anne PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0028594	journal	December 2011
Molecular basis for ubiquitin and ISG15 cross-reactivity in viral ovarian tumor domains Akutsu, M.; Ye, Y.; Virdee, S. Proceedings of the National Academy of Sciences, Vol. 108, Issue 6 https://doi.org/10.1073/pnas.1015287108	journal	January 2011
Structural Insights into the Interaction of Coronavirus Papain-Like Proteases and Interferon-Stimulated Gene Product 15 from Different Species Daczkowski, Courtney M.; Dzimianski, John V.; Clasman, Jozlyn R. Journal of Molecular Biology, Vol. 429, Issue 11 https://doi.org/10.1016/j.jmb.2017.04.011	journal	June 2017
Decoding the Ubiquitin-Mediated Pathway of Arthropod Disease Vectors Choy, Anthony; Severo, Maiara S.; Sun, Ruobai PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0078077	journal	October 2013
A chronological review of experimental infection studies of the role of wild animals and livestock in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus Spengler, Jessica R.; Estrada-Peña, Agustín; Garrison, Aura R. Antiviral Research, Vol. 135 https://doi.org/10.1016/j.antiviral.2016.09.013	journal	November 2016
ISG15 deficiency and increased viral resistance in humans but not mice Speer, Scott D.; Li, Zhi; Buta, Sofija Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11496	journal	May 2016
Crimean-Congo hemorrhagic fever: History, epidemiology, pathogenesis, clinical syndrome and genetic diversity Bente, Dennis A.; Forrester, Naomi L.; Watts, Douglas M. Antiviral Research, Vol. 100, Issue 1 https://doi.org/10.1016/j.antiviral.2013.07.006	journal	October 2013
Ovarian Tumor Domain-Containing Viral Proteases Evade Ubiquitin- and ISG15-Dependent Innate Immune Responses Frias-Staheli, Natalia; Giannakopoulos, Nadia V.; Kikkert, Marjolein Cell Host & Microbe, Vol. 2, Issue 6 https://doi.org/10.1016/j.chom.2007.09.014	journal	December 2007
Comparative Protein Structure Modeling Using MODELLER Webb, Benjamin; Sali, Andrej Current Protocols in Protein Science, Vol. 86, Issue 1 https://doi.org/10.1002/cpps.20	journal	November 2016
Protein ISGylation modulates the JAK-STAT signaling pathway Malakhova, Oxana A.; Yan, Ming; Malakhov, Michael P. Genes & Development, Vol. 17, Issue 4 https://doi.org/10.1101/gad.1056303	journal	January 2003
A Global Genomic Characterization of Nairoviruses Identifies Nine Discrete Genogroups with Distinctive Structural Characteristics and Host-Vector Associations Walker, Peter J.; Widen, Steven G.; Wood, Thomas G. The American Journal of Tropical Medicine and Hygiene, Vol. 94, Issue 5 https://doi.org/10.4269/ajtmh.15-0917	journal	May 2016
A nairovirus isolated from African bats causes haemorrhagic gastroenteritis and severe hepatic disease in mice Ishii, Akihiro; Ueno, Keisuke; Orba, Yasuko Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6651	journal	December 2014
Extracellular ISG15 Signals Cytokine Secretion through the LFA-1 Integrin Receptor Swaim, Caleb D.; Scott, Ariella F.; Canadeo, Larissa A. Molecular Cell, Vol. 68, Issue 3 https://doi.org/10.1016/j.molcel.2017.10.003	journal	November 2017
Kasokero Virus: a New Human Pathogen from Bats (Rousettus Aegyptiacus) in Uganda Kalunda, M.; Mukwaya, L. G.; Mukuye, A. The American Journal of Tropical Medicine and Hygiene, Vol. 35, Issue 2 https://doi.org/10.4269/ajtmh.1986.35.387	journal	March 1986
Structural Analysis of a Viral Ovarian Tumor Domain Protease from the Crimean-Congo Hemorrhagic Fever Virus in Complex with Covalently Bonded Ubiquitin Capodagli, G. C.; McKercher, M. A.; Baker, E. A. Journal of Virology, Vol. 85, Issue 7 https://doi.org/10.1128/JVI.02496-10	journal	January 2011
Deciphering key features in protein structures with the new ENDscript server Robert, Xavier; Gouet, Patrice Nucleic Acids Research, Vol. 42, Issue W1 https://doi.org/10.1093/nar/gku316	journal	April 2014
Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features Kabsch, Wolfgang; Sander, Christian Biopolymers, Vol. 22, Issue 12 https://doi.org/10.1002/bip.360221211	journal	December 1983
HyperISGylation of Old World Monkey ISG15 in Human Cells Pattyn, Els; Verhee, Annick; Uyttendaele, Isabel PLoS ONE, Vol. 3, Issue 6 https://doi.org/10.1371/journal.pone.0002427	journal	June 2008
Dugbe virus ovarian tumour domain interferes with ubiquitin/ISG15-regulated innate immune cell signalling Bakshi, S.; Holzer, B.; Bridgen, A. Journal of General Virology, Vol. 94, Issue Pt_2 https://doi.org/10.1099/vir.0.048322-0	journal	November 2012
Mycobacterial Disease and Impaired IFN- Immunity in Humans with Inherited ISG15 Deficiency Bogunovic, D.; Byun, M.; Durfee, L. A. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224026	journal	August 2012
Taxonomy of the order Bunyavirales: second update 2018 Maes, Piet; Adkins, Scott; Alkhovsky, Sergey V. Archives of Virology, Vol. 164, Issue 3 https://doi.org/10.1007/s00705-018-04127-3	journal	January 2019
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Taxonomy of the family Arenaviridae and the order Bunyavirales: update 2018 Maes, Piet; Alkhovsky, Sergey V.; Bào, Yīmíng Archives of Virology, Vol. 163, Issue 8 https://doi.org/10.1007/s00705-018-3843-5	journal	April 2018
The vOTU domain of highly-pathogenic porcine reproductive and respiratory syndrome virus displays a differential substrate preference Deaton, Michelle K.; Spear, Allyn; Faaberg, Kay S. Virology, Vol. 454-455 https://doi.org/10.1016/j.virol.2014.02.026	journal	April 2014
Lethal Crimean-Congo Hemorrhagic Fever Virus Infection in Interferon α/β Receptor Knockout Mice Is Associated With High Viral Loads, Proinflammatory Responses, and Coagulopathy Zivcec, Marko; Safronetz, David; Scott, Dana The Journal of Infectious Diseases, Vol. 207, Issue 12 https://doi.org/10.1093/infdis/jit061	journal	February 2013
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
Species Specificity of the NS1 Protein of Influenza B Virus: NS1 BINDS ONLY HUMAN AND NON-HUMAN PRIMATE UBIQUITIN-LIKE ISG15 PROTEINS Sridharan, Haripriya; Zhao, Chen; Krug, Robert M. Journal of Biological Chemistry, Vol. 285, Issue 11 https://doi.org/10.1074/jbc.C109.095703	journal	January 2010
Structural basis for the removal of ubiquitin and interferon-stimulated gene 15 by a viral ovarian tumor domain-containing protease James, T. W.; Frias-Staheli, N.; Bacik, J. -P. Proceedings of the National Academy of Sciences, Vol. 108, Issue 6 https://doi.org/10.1073/pnas.1013388108	journal	January 2011
A cynomolgus macaque model for Crimean–Congo haemorrhagic fever Haddock, Elaine; Feldmann, Friederike; Hawman, David W. Nature Microbiology, Vol. 3, Issue 5 https://doi.org/10.1038/s41564-018-0141-7	journal	April 2018
A new bioinformatics analysis tools framework at EMBL-EBI Goujon, M.; McWilliam, H.; Li, W. Nucleic Acids Research, Vol. 38, Issue Web Server https://doi.org/10.1093/nar/gkq313	journal	May 2010
Calculation of protein extinction coefficients from amino acid sequence data Gill, Stanley C.; von Hippel, Peter H. Analytical Biochemistry, Vol. 182, Issue 2 https://doi.org/10.1016/0003-2697(89)90602-7	journal	November 1989
Seroepidemiological Studies of Crimean-Congo Hemorrhagic Fever Virus in Domestic and Wild Animals Spengler, Jessica R.; Bergeron, Éric; Rollin, Pierre E. PLOS Neglected Tropical Diseases, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pntd.0004210	journal	January 2016
Crimean-Congo Hemorrhagic Fever Virus Suppresses Innate Immune Responses via a Ubiquitin and ISG15 Specific Protease Scholte, Florine E. M.; Zivcec, Marko; Dzimianski, John V. Cell Reports, Vol. 20, Issue 10 https://doi.org/10.1016/j.celrep.2017.08.040	journal	September 2017
How USP 18 deals with ISG 15‐modified proteins: structural basis for the specificity of the protease Basters, Anja; Knobeloch, Klaus‐Peter; Fritz, Günter The FEBS Journal, Vol. 285, Issue 6 https://doi.org/10.1111/febs.14260	journal	September 2017
Probing the impact of nairovirus genomic diversity on viral ovarian tumor domain protease (vOTU) structure and deubiquitinase activity Dzimianski, John V.; Beldon, Brianna S.; Daczkowski, Courtney M. PLOS Pathogens, Vol. 15, Issue 1 https://doi.org/10.1371/journal.ppat.1007515	journal	January 2019
Soldado Virus (Hughes Group) from Ornithodoros (Alectorobius) Capensis (Ixodoidea: Argasidae) Infesting Sooty Tern Colonies in the Seychelles, Indian Ocean * Moussa, Mahmoud I.; Hoogstraal, Harry; Converse, James D. The American Journal of Tropical Medicine and Hygiene, Vol. 24, Issue 6 https://doi.org/10.4269/ajtmh.1975.24.1010	journal	November 1975
Tickborne Arbovirus Surveillance in Market Livestock, Nairobi, Kenya Sang, Rosemary; Onyango, Clayton; Gachoya, John Emerging Infectious Diseases, Vol. 12, Issue 7 https://doi.org/10.3201/eid1207.060253	journal	July 2006
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Thunderclap headache caused by Erve virus? Treib, J.; Dobler, G.; Haass, A. Neurology, Vol. 50, Issue 2 https://doi.org/10.1212/WNL.50.2.509	journal	February 1998
Comparative Protein Structure Modeling Using MODELLER Webb, Benjamin; Sali, Andrej Current Protocols in Bioinformatics, Vol. 47, Issue 1 https://doi.org/10.1002/0471250953.bi0506s47	journal	September 2014
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011
Taxonomy of the family Arenaviridae and the order Bunyavirales: update 2018 Maes, Piet; Alkhovsky, Sergey V.; Bào, Yīmíng Springer https://doi.org/10.5167/uzh-161218	text	January 2018
Structural insights into the species preference of the influenza B virus NS1 protein in ISG15 binding Jiang, Yinan; Wang, Xinquan Protein & Cell, Vol. 10, Issue 9 https://doi.org/10.1007/s13238-018-0598-4	journal	December 2018
ISG15: It's Complicated Dzimianski, John V.; Scholte, Florine E. M.; Bergeron, Éric Journal of Molecular Biology, Vol. 431, Issue 21 https://doi.org/10.1016/j.jmb.2019.03.013	journal	October 2019
On a Tick-Borne Gastro-Enteritis of Sheep and Goats Occurring in British East Africa Montgomery, Eustace Journal of Comparative Pathology and Therapeutics, Vol. 30 https://doi.org/10.1016/s0368-1742(17)80002-3	journal	January 1917
Host ANP32A mediates the assembly of the influenza virus replicase Carrique, Loïc; Fan, Haitian; Walker, Alexander P. Nature, Vol. 587, Issue 7835 https://doi.org/10.1038/s41586-020-2927-z	journal	November 2020
UBP43 (USP18) Specifically Removes ISG15 from Conjugated Proteins Malakhov, Michael P.; Malakhova, Oxana A.; Kim, Keun Il Journal of Biological Chemistry, Vol. 277, Issue 12 https://doi.org/10.1074/jbc.m109078200	journal	March 2002
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
Structure of interferon-stimulated gene product 15 (ISG15) from the bat species Myotis davidii and the impact of interdomain ISG15 interactions on viral protein engagement Langley, Caroline; Goodwin, Octavia; Dzimianski, John V. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 1 https://doi.org/10.1107/s2059798318015322	journal	January 2019
Biochemical and Structural Insights into the Preference of Nairoviral DeISGylases for Interferon-Stimulated Gene Product 15 Originating from Certain Species Deaton, M. K.; Dzimianski, J. V.; Daczkowski, C. M. Journal of Virology, Vol. 90, Issue 18 https://doi.org/10.1128/jvi.00975-16	journal	July 2016
Structurally Guided Removal of DeISGylase Biochemical Activity from Papain-Like Protease Originating from Middle East Respiratory Syndrome Coronavirus Daczkowski, Courtney M.; Goodwin, Octavia Y.; Dzimianski, John V. Journal of Virology, Vol. 91, Issue 23 https://doi.org/10.1128/jvi.01067-17	journal	September 2017
Species-Specific Antagonism of Host ISGylation by the Influenza B Virus NS1 Protein Versteeg, G. A.; Hale, B. G.; van Boheemen, S. Journal of Virology, Vol. 84, Issue 10 https://doi.org/10.1128/jvi.02395-09	journal	March 2010
Diversity of Ubiquitin and ISG15 Specificity among Nairoviruses' Viral Ovarian Tumor Domain Proteases Capodagli, G. C.; Deaton, M. K.; Baker, E. A. Journal of Virology, Vol. 87, Issue 7 https://doi.org/10.1128/jvi.03252-12	journal	January 2013
LRRC25 inhibits type I IFN signaling by targeting ISG15‐associated RIG‐I for autophagic degradation Du, Yang; Duan, Tianhao; Feng, Yanchun The EMBO Journal, Vol. 37, Issue 3 https://doi.org/10.15252/embj.201796781	journal	December 2017
Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V. International Union of Crystallography (IUCr) https://doi.org/10.17863/cam.52329	journalarticle	January 2008
Phosphorylated peptide of G protein-coupled receptor induces dimerization in activated arrestin Stadler, Andreas M.; Granzin, Joachim; Cousin, Anneliese RWTH Aachen University https://doi.org/10.18154/rwth-2020-08655	text	January 2020

Similar Records

Probing the impact of nairovirus genomic diversity on viral ovarian tumor domain protease (vOTU) structure and deubiquitinase activity

Journal Article · Thu Jan 10 00:00:00 EST 2019 · PLoS Pathogens · OSTI ID:1837272

Dzimianski, John V.; Beldon, Brianna S.; Daczkowski, Courtney M.; +4 more

Biochemical and Structural Insights into the Preference of Nairoviral DeISGylases for Interferon-Stimulated Gene Product 15 Originating from Certain Species

Journal Article · Wed Jul 13 00:00:00 EDT 2016 · Journal of Virology · OSTI ID:1837272

Deaton, M. K.; Dzimianski, J. V.; Daczkowski, C. M.; +5 more

Structural Analysis of a Viral Ovarian Tumor Domain Protease from the Crimean-Congo Hemorrhagic Fever Virus in Complex with Covalently Bonded Ubiquitin

Journal Article · Thu Oct 02 00:00:00 EDT 2014 · J. Virol. · OSTI ID:1837272

Capodagli, Glenn C.; McKercher, Marissa A.; Baker, Erica A.; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Determining the molecular drivers of species-specific interferon-stimulated gene product 15 interactions with nairovirus ovarian tumor domain proteases

Citation Formats

References (66)

Similar Records

Related Subjects