Positive-strand RNA viruses-a Keystone Symposia report

Jennifer Cable¹, Mark R Denison², Margaret Kielian³, William T Jackson⁴, Ralf Bartenschlager⁵, Tero Ahola⁶, Suchetana Mukhopadhyay⁷, Daved H Fremont⁸, Richard J Kuhn⁹, Ashleigh Shannon¹⁰, Meredith N Frazier¹¹, Kwok-Yung Yuen^{12

13}, Carolyn B Coyne¹⁴, Katja C Wolthers¹⁵, Guo-Li Ming¹⁶, Camy S Guenther¹⁷, Jasmine Moshiri¹⁸, Sonja M Best¹⁹, John W Schoggins²⁰, Kellie Ann Jurado²¹, Gregory D Ebel²², Alexandra Schäfer²³, Lisa F P Ng^{24

25}, Marjolein Kikkert²⁶, Alessandro Sette^{27

28}, Eva Harris²⁹, Peter A C Wing³⁰, Julie Eggenberger³¹, Siddharth R Krishnamurthy³², Marcus G Mah³³, Rita M Meganck²³, Donghoon Chung³⁴, Sebastian Maurer-Stroh^{35

36}, Raul Andino³⁷, Bette Korber³⁸, Stanley Perlman³⁹, Pei-Yong Shi⁴⁰, Montserrat Bárcena⁴¹, Sophie-Marie Aicher⁴², Michelle N Vu⁴³, Devin J Kenney⁴⁴, Brett D Lindenbach⁴⁵, Yukiko Nishida^{46

47}, Laurent Rénia²⁴, Evan P Williams⁴⁸

Affiliations

¹ PhD Science Writer, New York, New York, USA.
² Department of Pediatrics and Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center; and Vanderbilt Institute for Infection, Immunology, and Inflammation, Nashville, Tennessee, USA.
³ Department of Cell Biology, Albert Einstein College of Medicine, New York, New York, USA.
⁴ Department of Microbiology and Immunology and Center for Pathogen Research, University of Maryland School of Medicine, Baltimore, Maryland, USA.
⁵ Department of Infectious Diseases, Molecular Virology, Heidelberg University and German Cancer Research Center (DKFZ), Research Division Virus-associated Carcinogenesis, Heidelberg, Germany.
⁶ Department of Microbiology, Faculty of Agriculture and Forestry, University of Helsinki, Helsinki, Finland.
⁷ Department of Biology, Indiana University, Bloomington, Indiana, USA.
⁸ Department of Pathology & Immunology; Department of Molecular Microbiology; and Department of Biochemistry & Molecular Biophysics, Washington University School of Medicine, St. Louis, Missouri, USA.
⁹ Department of Biological Sciences, Purdue University, West Lafayette, Indiana, USA.
¹⁰ Architecture et Fonction des Macromolécules Biologiques, CNRS and Aix Marseille Université, Marseille, France.
¹¹ Signal Transduction Laboratory, National Institute of Environmental Health Sciences, National Institutes of Health, Department of Health and Human Services, Research Triangle Park, North Carolina, USA.
¹² Department of Microbiology, Li Ka Shing Faculty of Medicine and State Key Laboratory of Emerging Infectious Diseases, The University of Hong Kong, Hong Kong, People's Republic of China.
¹³ Centre for Virology, Vaccinology and Therapeutics, Hong Kong Science and Technology Park, Hong Kong, People's Republic of China.
¹⁴ Department of Molecular Genetics and Microbiology, Duke University, Durham, North Carolina, USA.
¹⁵ Department of Medical Microbiology, Amsterdam UMC, University of Amsterdam and Amsterdam Institute for Infection and Immunity, OrganoVIR Labs, Amsterdam, The Netherlands.
¹⁶ Department of Neuroscience and Mahoney Institute for Neurosciences, Institute for Regenerative Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
¹⁷ Colorado State University, Fort Collins, Colorado, USA.
¹⁸ Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, California, USA.
¹⁹ Laboratory of Virology, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA.
²⁰ Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, Texas, USA.
²¹ Department of Microbiology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
²² Center for Vector-borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.
²³ Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
²⁴ ASTAR Infectious Diseases Labs (A*STAR ID Labs), Agency for Science Technology and Research (A*STAR), Singapore City, Singapore.
²⁵ National Institute of Health Research, Health Protection Research Unit in Emerging and Zoonotic Infections; Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool, UK.
²⁶ Department of Medical Microbiology, Leiden University Medical Center, Leiden, The Netherlands.
²⁷ Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, California, USA.
²⁸ Division of Infectious Diseases and Global Public Health, Department of Medicine, University of California, San Diego, La Jolla, California, USA.
²⁹ Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, California, USA.
³⁰ Nuffield Department of Medicine and Chinese Academy of Medical Sciences Oxford Institute, University of Oxford, Oxford, UK.
³¹ Department of Immunology, University of Washington School of Medicine, Seattle, Washington, USA.
³² Metaorganism Immunity Section, Laboratory of Immune System Biology and NIAID Microbiome Program, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA.
³³ Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore City, Singapore.
³⁴ Department of Experimental Therapeutics, MD Anderson Cancer Center, Houston, Texas, USA.
³⁵ Yong Loo Lin School of Medicine and Department of Biological Sciences, National University of Singapore, Singapore City, Singapore.
³⁶ Bioinformatics Institute, Agency for Science, Technology and Research, Singapore City, Singapore.
³⁷ Department of Microbiology and Immunology, University of California, San Francisco, San Francisco, California, USA.
³⁸ Los Alamos National Laboratory, Los Alamos, New Mexico, USA.
³⁹ Department of Microbiology and Immunology, and Department of Pediatrics, University of Iowa, Iowa City, Iowa, USA.
⁴⁰ Department of Biochemistry and Molecular Biology, University of Texas Medical Branch, Galveston, Texas, USA.
⁴¹ Section Electron Microscopy, Department of Cell and Chemical Biology, Leiden University Medical Center, Leiden, The Netherlands.
⁴² Institut Pasteurgrid, Université de Paris Cité, Virus Sensing and Signaling Unit, Paris, France.
⁴³ Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USA.
⁴⁴ Department of Microbiology and National Emerging Infectious Diseases Laboratories, Boston University School of Medicine, Boston, Massachusetts, USA.
⁴⁵ Department of Microbial Pathogenesis, Yale University School of Medicine, New Haven, Connecticut, USA.
⁴⁶ Chugai Pharmaceutical, Co., Tokyo, Japan.
⁴⁷ Lee Kong Chian School of Medicine and School of Biological Sciences, Nanyang Technological University, Singapore City, Singapore.
⁴⁸ Department of Microbiology, Immunology, and Biochemistry, The University of Tennessee Health Science Center, Memphis, Tennessee, USA.

PMID: 36697369
PMCID: PMC10347887
DOI: 10.1111/nyas.14957

Positive-strand RNA viruses-a Keystone Symposia report

Jennifer Cable et al. Ann N Y Acad Sci. 2023 Mar.

. 2023 Mar;1521(1):46-66.

doi: 10.1111/nyas.14957. Epub 2023 Jan 25.

Authors

Affiliations

¹ PhD Science Writer, New York, New York, USA.
² Department of Pediatrics and Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center; and Vanderbilt Institute for Infection, Immunology, and Inflammation, Nashville, Tennessee, USA.
³ Department of Cell Biology, Albert Einstein College of Medicine, New York, New York, USA.
⁴ Department of Microbiology and Immunology and Center for Pathogen Research, University of Maryland School of Medicine, Baltimore, Maryland, USA.
⁵ Department of Infectious Diseases, Molecular Virology, Heidelberg University and German Cancer Research Center (DKFZ), Research Division Virus-associated Carcinogenesis, Heidelberg, Germany.
⁶ Department of Microbiology, Faculty of Agriculture and Forestry, University of Helsinki, Helsinki, Finland.
⁷ Department of Biology, Indiana University, Bloomington, Indiana, USA.
⁸ Department of Pathology & Immunology; Department of Molecular Microbiology; and Department of Biochemistry & Molecular Biophysics, Washington University School of Medicine, St. Louis, Missouri, USA.
⁹ Department of Biological Sciences, Purdue University, West Lafayette, Indiana, USA.
¹⁰ Architecture et Fonction des Macromolécules Biologiques, CNRS and Aix Marseille Université, Marseille, France.
¹¹ Signal Transduction Laboratory, National Institute of Environmental Health Sciences, National Institutes of Health, Department of Health and Human Services, Research Triangle Park, North Carolina, USA.
¹² Department of Microbiology, Li Ka Shing Faculty of Medicine and State Key Laboratory of Emerging Infectious Diseases, The University of Hong Kong, Hong Kong, People's Republic of China.
¹³ Centre for Virology, Vaccinology and Therapeutics, Hong Kong Science and Technology Park, Hong Kong, People's Republic of China.
¹⁴ Department of Molecular Genetics and Microbiology, Duke University, Durham, North Carolina, USA.
¹⁵ Department of Medical Microbiology, Amsterdam UMC, University of Amsterdam and Amsterdam Institute for Infection and Immunity, OrganoVIR Labs, Amsterdam, The Netherlands.
¹⁶ Department of Neuroscience and Mahoney Institute for Neurosciences, Institute for Regenerative Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
¹⁷ Colorado State University, Fort Collins, Colorado, USA.
¹⁸ Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, California, USA.
¹⁹ Laboratory of Virology, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA.
²⁰ Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, Texas, USA.
²¹ Department of Microbiology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
²² Center for Vector-borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.
²³ Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
²⁴ ASTAR Infectious Diseases Labs (A*STAR ID Labs), Agency for Science Technology and Research (A*STAR), Singapore City, Singapore.
²⁵ National Institute of Health Research, Health Protection Research Unit in Emerging and Zoonotic Infections; Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool, UK.
²⁶ Department of Medical Microbiology, Leiden University Medical Center, Leiden, The Netherlands.
²⁷ Center for Infectious Disease and Vaccine Research, La Jolla Institute for Immunology, La Jolla, California, USA.
²⁸ Division of Infectious Diseases and Global Public Health, Department of Medicine, University of California, San Diego, La Jolla, California, USA.
²⁹ Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, California, USA.
³⁰ Nuffield Department of Medicine and Chinese Academy of Medical Sciences Oxford Institute, University of Oxford, Oxford, UK.
³¹ Department of Immunology, University of Washington School of Medicine, Seattle, Washington, USA.
³² Metaorganism Immunity Section, Laboratory of Immune System Biology and NIAID Microbiome Program, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA.
³³ Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore City, Singapore.
³⁴ Department of Experimental Therapeutics, MD Anderson Cancer Center, Houston, Texas, USA.
³⁵ Yong Loo Lin School of Medicine and Department of Biological Sciences, National University of Singapore, Singapore City, Singapore.
³⁶ Bioinformatics Institute, Agency for Science, Technology and Research, Singapore City, Singapore.
³⁷ Department of Microbiology and Immunology, University of California, San Francisco, San Francisco, California, USA.
³⁸ Los Alamos National Laboratory, Los Alamos, New Mexico, USA.
³⁹ Department of Microbiology and Immunology, and Department of Pediatrics, University of Iowa, Iowa City, Iowa, USA.
⁴⁰ Department of Biochemistry and Molecular Biology, University of Texas Medical Branch, Galveston, Texas, USA.
⁴¹ Section Electron Microscopy, Department of Cell and Chemical Biology, Leiden University Medical Center, Leiden, The Netherlands.
⁴² Institut Pasteurgrid, Université de Paris Cité, Virus Sensing and Signaling Unit, Paris, France.
⁴³ Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USA.
⁴⁴ Department of Microbiology and National Emerging Infectious Diseases Laboratories, Boston University School of Medicine, Boston, Massachusetts, USA.
⁴⁵ Department of Microbial Pathogenesis, Yale University School of Medicine, New Haven, Connecticut, USA.
⁴⁶ Chugai Pharmaceutical, Co., Tokyo, Japan.
⁴⁷ Lee Kong Chian School of Medicine and School of Biological Sciences, Nanyang Technological University, Singapore City, Singapore.
⁴⁸ Department of Microbiology, Immunology, and Biochemistry, The University of Tennessee Health Science Center, Memphis, Tennessee, USA.

PMID: 36697369
PMCID: PMC10347887
DOI: 10.1111/nyas.14957

Abstract

Positive-strand RNA viruses have been the cause of several recent outbreaks and epidemics, including the Zika virus epidemic in 2015, the SARS outbreak in 2003, and the ongoing SARS-CoV-2 pandemic. On June 18-22, 2022, researchers focusing on positive-strand RNA viruses met for the Keystone Symposium "Positive-Strand RNA Viruses" to share the latest research in molecular and cell biology, virology, immunology, vaccinology, and antiviral drug development. This report presents concise summaries of the scientific discussions at the symposium.

Keywords: RNA virus; SARS-CoV-2; alphavirus; coronavirus; enterovirus; flavivirus.

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Conflict of interest statement

Competing Interests

A. Sette is a consultant for Gritstone Bio, Flow Pharma, Moderna, AstraZeneca, Qiagen, Avalia, Fortress, Gilead, Sanofi, Merck, RiverVest, MedaCorp, Turnstone, NA Vaccine Institute, Gerson Lehrman Group, and Guggenheim; La Jolla Institute for Immunology has filed for patent protection for various aspects of T-cell epitope and vaccine design work.

L. Renia: a patent application for the S-flow assay has been filed (Singapore patent #10202009679P: A Method of Detecting Antibodies And Related Products).

Figures

**Figure 1.**
Factors commonly involved in double membrane vesicle formation.

**Figure 3.**
Structure of MERS-CoV PLpro (in green) in complex with ubiquitin (orange), adapted from Bailey-Elkin et al. J Biol Chem. 2014.

**Figure 4.**
Schematic of nucleotide sequences within the spike and ORF4 gene regions. Colored filled rectangles represent parts of the genome in C2R1, C2R5, and C2R10 viruses that are present in the respective passage. Virus isolates names are in bold. Horizontal black lines indicate deleted parts of the genome with the respective size denoted by Δ, starts and ends of the deletions are indicated by the respective nucleotide position.

See this image and copyright information in PMC

References

1. Smith EC, Sexton NR & Denison MR 2014. Thinking Outside the Triangle: Replication Fidelity of the Largest RNA Viruses. Annu. Rev. Virol 1: 111–132. - PubMed
1. Minskaia E, Hertzig T, Gorbalenya AE, et al. 2006. Discovery of an RNA virus 3’->5’ exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc. Natl. Acad. Sci. U. S. A 103: 5108–5113. - PMC - PubMed
1. Eckerle LD, Lu X, Sperry SM, et al. 2007. High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. J. Virol 81: 12135–12144. - PMC - PubMed
1. Eckerle LD, Becker MM, Halpin RA, et al. 2010. Infidelity of SARS-CoV Nsp14-exonuclease mutant virus replication is revealed by complete genome sequencing. PLoS Pathog. 6: e1000896. - PMC - PubMed
1. Smith EC, Blanc H, Surdel MC, et al. 2013. Coronaviruses lacking exoribonuclease activity are susceptible to lethal mutagenesis: evidence for proofreading and potential therapeutics. PLoS Pathog. 9: e1003565. - PMC - PubMed

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Positive-strand RNA viruses-a Keystone Symposia report

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Positive-strand RNA viruses-a Keystone Symposia report

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