Title: The Structure and Immune Regulatory Implications of the Ubiquitin-Like Tandem Domain Within an Avian 2’-5’ Oligoadenylate Synthetase-Like Protein

Journal Article · · Frontiers in Immunology
 [1];  [2];  [3];  [4];  [2];  [2];  [2];  [2];  [2];  [2];  [2];  [2];  [2];  [5];  [6]
  1. Univ. of Georgia, Athens, GA (United States); OSTI
  2. Univ. of Georgia, Athens, GA (United States)
  3. Centers for Disease Control and Prevention (CDC), Atlanta, GA (United States); Univ. of Texas Medical Branch, Galveston, TX (United States). Galveston National Lab.
  4. Centers for Disease Control and Prevention (CDC), Atlanta, GA (United States)
  5. Univ. of Georgia, Athens, GA (United States); Centers for Disease Control and Prevention (CDC), Atlanta, GA (United States)
  6. Univ. of California, Riverside, CA (United States)
+ Show Author Affiliations

Post-translational modification of host and viral proteins by ubiquitin and ubiquitin-like proteins plays a key role in a host’s ability to mount an effective immune response. Avian species lack a ubiquitin-like protein found in mammals and other non-avian reptiles; interferon stimulated gene product 15 (ISG15). ISG15 serves as a messenger molecule and can be conjugated to both host and viral proteins leading them to be stabilized, degraded, or sequestered. Structurally, ISG15 is comprised of a tandem ubiquitin-like domain (Ubl), which serves as the motif for post-translational modification. The 2’-5’ oligoadenylate synthetase-like proteins (OASL) also encode two Ubl domains in series near its C-terminus which binds OASL to retinoic acid inducible gene-I (RIG-I). This protein-protein interaction increases the sensitivity of RIG-I and results in an enhanced production of type 1 interferons and a robust immune response. Unlike human and other mammalian OASL homologues, avian OASLs terminate their tandem Ubl domains with the same LRLRGG motif found in ubiquitin and ISG15, a motif required for their conjugation to proteins. Chickens, however, lack RIG-I, raising the question of structural and functional characteristics of chicken OASL (chOASL). By investigating chOASL, the evolutionary history of viruses with deubiquitinases can be explored and drivers of species specificity for these viruses may be uncovered. Here we show that the chOASL tandem Ubl domains shares structural characteristics with mammalian ISG15, and that chOASL can oligomerize and conjugate to itself. In addition, the ISG15-like features of avian OASLs and how they impact interactions with viral deubiquitinases and deISGylases are explored.

Research Organization:
Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)
Sponsoring Organization:
HDTRA; National Institutes of Health (NIH); USDOE Office of Science (SC)
Grant/Contract Number:
SC0014664
OSTI ID:
1904932
Journal Information:
Frontiers in Immunology, Journal Name: Frontiers in Immunology Vol. 12; ISSN 1664-3224
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

References (46)

Comparative Protein Structure Modeling Using MODELLER journal June 2016
A central role for RNA in the induction and biological activities of type 1 interferons: Role for RNA in the induction and biological activities of type 1 IFNs journal August 2010
[20] Processing of X-ray diffraction data collected in oscillation mode book January 1997
Ovarian Tumor Domain-Containing Viral Proteases Evade Ubiquitin- and ISG15-Dependent Innate Immune Responses journal December 2007
OASL—a new player in controlling antiviral innate immunity journal June 2015
Defense genes missing from the flight division journal November 2013
Roles of myeloperoxidase and GAPDH in interferon-gamma production of GM-CSF-dependent macrophages journal February 2016
Antiviral Activity of Human OASL Protein Is Mediated by Enhancing Signaling of the RIG-I RNA Sensor journal June 2014
Inference of Macromolecular Assemblies from Crystalline State journal September 2007
Structural Insights into the Interaction of Coronavirus Papain-Like Proteases and Interferon-Stimulated Gene Product 15 from Different Species journal June 2017
Functional analysis of duck, goose, and ostrich 2′-5′-oligoadenylate synthetase journal August 2018
Extracellular ISG15 Signals Cytokine Secretion through the LFA-1 Integrin Receptor journal November 2017
The molecular mechanisms of signaling by cooperative assembly formation in innate immunity pathways journal June 2017
The Ubiquitin Code in the Ubiquitin-Proteasome System and Autophagy journal November 2017
Molecular analysis of Crimean-Congo hemorrhagic fever virus and Rickettsia in Hyalomma marginatum ticks removed from patients (Spain) and birds (Spain and Morocco), 2009–2015 journal July 2016
How ISG15 combats viral infection journal September 2020
Oligoadenylate synthase-like (OASL) proteins: dual functions and associations with diseases journal March 2015
Coronavirus avian infectious bronchitis virus journal March 2007
Regulation of IRF-3-dependent Innate Immunity by the Papain-like Protease Domain of the Severe Acute Respiratory Syndrome Coronavirus journal August 2007
Function of Ubiquitin-like Domain of Chicken 2′-5′-Oligoadenylate Synthetase in Conformational Stability journal November 2003
The Oligoadenylate Synthetase Family: An Ancient Protein Family with Multiple Antiviral Activities journal January 2011
Characterization of the 2'-5'-oligoadenylate synthetase ubiquitin-like family journal June 2003
Structural and functional analysis reveals that human OASL binds dsRNA to enhance RIG-I signaling journal April 2015
Microbial Sensing by Toll-Like Receptors and Intracellular Nucleic Acid Sensors journal October 2014
Phaser crystallographic software journal July 2007
Coot model-building tools for molecular graphics journal November 2004
Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard journal December 2007
PHENIX: a comprehensive Python-based system for macromolecular structure solution journal January 2010
Overview of the CCP 4 suite and current developments journal March 2011
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 journal January 2019
Biochemical and Structural Insights into the Preference of Nairoviral DeISGylases for Interferon-Stimulated Gene Product 15 Originating from Certain Species journal July 2016
Structurally Guided Removal of DeISGylase Biochemical Activity from Papain-Like Protease Originating from Middle East Respiratory Syndrome Coronavirus journal September 2017
2′-5′-Oligoadenylate Synthetase-Like Protein Inhibits Respiratory Syncytial Virus Replication and Is Targeted by the Viral Nonstructural Protein 1 journal October 2015
Crimean-Congo Hemorrhagic Fever Virus-Encoded Ovarian Tumor Protease Activity Is Dispensable for Virus RNA Polymerase Function journal October 2009
Severe Acute Respiratory Syndrome Coronavirus Papain-Like Protease Ubiquitin-Like Domain and Catalytic Domain Regulate Antagonism of IRF3 and NF-κB Signaling journal April 2009
Translation and processing of mouse hepatitis virus virion RNA in a cell-free system journal October 1986
Host preferences support the prominent role of Hyalomma ticks in the ecology of Crimean-Congo hemorrhagic fever journal February 2018
Inhibition of Interferon Induction and Action by the Nairovirus Nairobi Sheep Disease Virus/Ganjam Virus journal December 2011
Determining the molecular drivers of species-specific interferon-stimulated gene product 15 interactions with nairovirus ovarian tumor domain proteases journal December 2019
Consecutive Inhibition of ISG15 Expression and ISGylation by Cytomegalovirus Regulators journal August 2016
Probing the impact of nairovirus genomic diversity on viral ovarian tumor domain protease (vOTU) structure and deubiquitinase activity journal January 2019
Molecular Mechanisms for the Adaptive Switching Between the OAS/RNase L and OASL/RIG-I Pathways in Birds and Mammals journal June 2018
Herc5 Attenuates Influenza A Virus by Catalyzing ISGylation of Viral NS1 Protein journal April 2010
A human 15-kDa IFN-induced protein induces the secretion of IFN-gamma. journal October 1991
Cysteine-Reactive Free ISG15 Generates IL-1β–Producing CD8α+Dendritic Cells at the Site of Infection journal June 2018
Soldado Virus (Hughes Group) from Ornithodoros (Alectorobius) Capensis (Ixodoidea: Argasidae) Infesting Sooty Tern Colonies in the Seychelles, Indian Ocean * journal November 1975

Similar Records

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
Journal Article · 2018 · Acta Crystallographica. Section D. Structural Biology · OSTI ID:1506505
+2 more
Structurally Guided Removal of DeISGylase Biochemical Activity from Papain-Like Protease Originating from Middle East Respiratory Syndrome Coronavirus
Journal Article · 2017 · Journal of Virology · OSTI ID:1464822
+3 more
Biochemical and Structural Insights into the Preference of Nairoviral DeISGylases for Interferon-Stimulated Gene Product 15 Originating from Certain Species
Journal Article · 2016 · Journal of Virology · OSTI ID:1324784
+5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
ISG15
Immunology
Nairovirus
OASL
UBL
avian immunity
protease
ubiquitin