Varicella Zoster Virus Impairs Expression of the Nonclassical Major Histocompatibility Complex Class I-Related Gene Protein (MR1)
The antigen presentation molecule MR1 (major histocompatibility complex, class I-related) presents ligands derived from the riboflavin (vitamin B) synthesis pathway, which is not present in mammalian species or viruses, to mucosal-associated invariant T (MAIT) cells. In this study, we demonstrate th...
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| Published in | The Journal of infectious diseases Vol. 227; no. 3; pp. 391 - 401 |
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| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Oxford University Press
01.02.2023
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| Abstract | The antigen presentation molecule MR1 (major histocompatibility complex, class I-related) presents ligands derived from the riboflavin (vitamin B) synthesis pathway, which is not present in mammalian species or viruses, to mucosal-associated invariant T (MAIT) cells. In this study, we demonstrate that varicella zoster virus (VZV) profoundly suppresses MR1 expression. We show that VZV targets the intracellular reservoir of immature MR1 for degradation, while preexisting, ligand-bound cell surface MR1 is protected from such targeting, thereby highlighting an intricate temporal relationship between infection and ligand availability. We also identify VZV open reading frame (ORF) 66 as functioning to suppress MR1 expression when this viral protein is expressed during transient transfection, but this is not apparent during infection with a VZV mutant virus lacking ORF66 expression. This indicates that VZV is likely to encode multiple viral genes that target MR1. Overall, we identify an immunomodulatory function of VZV whereby infection suppresses the MR1 biosynthesis pathway. |
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| AbstractList | The antigen presentation molecule MR1 (major histocompatibility complex, class I-related) presents ligands derived from the riboflavin (vitamin B) synthesis pathway, which is not present in mammalian species or viruses, to mucosal-associated invariant T (MAIT) cells. In this study, we demonstrate that varicella zoster virus (VZV) profoundly suppresses MR1 expression. We show that VZV targets the intracellular reservoir of immature MR1 for degradation, while preexisting, ligand-bound cell surface MR1 is protected from such targeting, thereby highlighting an intricate temporal relationship between infection and ligand availability. We also identify VZV open reading frame (ORF) 66 as functioning to suppress MR1 expression when this viral protein is expressed during transient transfection, but this is not apparent during infection with a VZV mutant virus lacking ORF66 expression. This indicates that VZV is likely to encode multiple viral genes that target MR1. Overall, we identify an immunomodulatory function of VZV whereby infection suppresses the MR1 biosynthesis pathway. The antigen presentation molecule MR1 (major histocompatibility complex, class I–related) presents ligands derived from the riboflavin (vitamin B) synthesis pathway, which is not present in mammalian species or viruses, to mucosal-associated invariant T (MAIT) cells. In this study, we demonstrate that varicella zoster virus (VZV) profoundly suppresses MR1 expression. We show that VZV targets the intracellular reservoir of immature MR1 for degradation, while preexisting, ligand-bound cell surface MR1 is protected from such targeting, thereby highlighting an intricate temporal relationship between infection and ligand availability. We also identify VZV open reading frame (ORF) 66 as functioning to suppress MR1 expression when this viral protein is expressed during transient transfection, but this is not apparent during infection with a VZV mutant virus lacking ORF66 expression. This indicates that VZV is likely to encode multiple viral genes that target MR1. Overall, we identify an immunomodulatory function of VZV whereby infection suppresses the MR1 biosynthesis pathway. In this study, we demonstrate that varicella zoster virus profoundly suppresses expression of the antigen presentation molecule major histocompatibility complex, class I–related (MR1), thus identifying an additional immunomodulatory function encoded by this virus. |
| Author | Abendroth, Allison McSharry, Brian P Kinchington, Paul R Steain, Megan McWilliam, Hamish E G Traves, Renee Purohit, Shivam K Villadangos, Jose A Rossjohn, Jamie Tscharke, David C Slobedman, Barry Samer, Carolyn |
| Author_xml | – sequence: 1 givenname: Shivam K surname: Purohit fullname: Purohit, Shivam K organization: Infection, Immunity and Inflammation, School of Medical Sciences, Faculty of Medicine and Health, Charles Perkins Centre, University of Sydney, Sydney, Australia – sequence: 2 givenname: Carolyn surname: Samer fullname: Samer, Carolyn organization: Infection, Immunity and Inflammation, School of Medical Sciences, Faculty of Medicine and Health, Charles Perkins Centre, University of Sydney, Sydney, Australia – sequence: 3 givenname: Hamish E G surname: McWilliam fullname: McWilliam, Hamish E G organization: Department of Biochemistry and Pharmacology, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria, Australia – sequence: 4 givenname: Renee surname: Traves fullname: Traves, Renee organization: Infection, Immunity and Inflammation, School of Medical Sciences, Faculty of Medicine and Health, Charles Perkins Centre, University of Sydney, Sydney, Australia – sequence: 5 givenname: Megan surname: Steain fullname: Steain, Megan organization: Infection, Immunity and Inflammation, School of Medical Sciences, Faculty of Medicine and Health, Charles Perkins Centre, University of Sydney, Sydney, Australia – sequence: 6 givenname: Brian P surname: McSharry fullname: McSharry, Brian P organization: Infection, Immunity and Inflammation, School of Medical Sciences, Faculty of Medicine and Health, Charles Perkins Centre, University of Sydney, Sydney, Australia – sequence: 7 givenname: Paul R surname: Kinchington fullname: Kinchington, Paul R organization: Department of Ophthalmology and Department of Microbiology and Molecular Genetics, University of Pittsburgh, Pittsburgh, Pennsylvania, USA – sequence: 8 givenname: David C surname: Tscharke fullname: Tscharke, David C organization: John Curtin School of Medical Research, Australian National University, Canberra, Australian Capital Territory, Australia – sequence: 9 givenname: Jose A surname: Villadangos fullname: Villadangos, Jose A organization: Department of Biochemistry and Pharmacology, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria, Australia – sequence: 10 givenname: Jamie surname: Rossjohn fullname: Rossjohn, Jamie organization: Institute of Infection and Immunity, Cardiff University School of Medicine, Wales, United Kingdom – sequence: 11 givenname: Allison surname: Abendroth fullname: Abendroth, Allison organization: Infection, Immunity and Inflammation, School of Medical Sciences, Faculty of Medicine and Health, Charles Perkins Centre, University of Sydney, Sydney, Australia – sequence: 12 givenname: Barry surname: Slobedman fullname: Slobedman, Barry organization: Infection, Immunity and Inflammation, School of Medical Sciences, Faculty of Medicine and Health, Charles Perkins Centre, University of Sydney, Sydney, Australia |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34648018$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1371_journal_ppat_1011485 crossref_primary_10_3389_fimmu_2023_1107497 crossref_primary_10_3389_fimmu_2023_1281881 crossref_primary_10_4049_jimmunol_2300147 crossref_primary_10_1038_s41577_023_00934_1 crossref_primary_10_1016_j_isci_2024_108801 crossref_primary_10_3389_fimmu_2023_1121714 crossref_primary_10_1093_infdis_jiad512 |
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| Copyright | The Author(s) 2021. Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved. For permissions, e-mail: journals.permissions@oup.com. The Author(s) 2021. Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved. For permissions, e-mail: journals.permissions@oup.com. 2021 |
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| Keywords | varicella zoster virus VZV immune modulation MR1 |
| Language | English |
| License | The Author(s) 2021. Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved. For permissions, e-mail: journals.permissions@oup.com. https://academic.oup.com/pages/standard-publication-reuse-rights This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model) |
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| Snippet | The antigen presentation molecule MR1 (major histocompatibility complex, class I-related) presents ligands derived from the riboflavin (vitamin B) synthesis... The antigen presentation molecule MR1 (major histocompatibility complex, class I–related) presents ligands derived from the riboflavin (vitamin B) synthesis... |
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| SubjectTerms | Animals Herpesvirus 3, Human - genetics Histocompatibility Antigens Class I Ligands Major Major Histocompatibility Complex Mammals Minor Histocompatibility Antigens |
| Title | Varicella Zoster Virus Impairs Expression of the Nonclassical Major Histocompatibility Complex Class I-Related Gene Protein (MR1) |
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