Pathogenic differences of cynomolgus macaques after Taï Forest virus infection depend on the viral stock propagation

Taï Forest virus (TAFV) is a negative-sense RNA virus in the Filoviridae family. TAFV has caused only a single human infection, but several disease outbreaks in chimpanzees have been linked to this virus. Limited research has been done on this human-pathogenic virus. We sought to establish an animal...

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Published inPLoS pathogens Vol. 20; no. 6; p. e1012290
Main Authors Fletcher, Paige, Clancy, Chad S, O'Donnell, Kyle L, Doratt, Brianna M, Malherbe, Delphine C, Rhoderick, Joseph F, Feldmann, Friederike, Hanley, Patrick W, Takada, Ayato, Messaoudi, Ilhem, Marzi, Andrea
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.06.2024
Public Library of Science (PLoS)
Subjects
Alphavirus Infections - pathology
Alphavirus Infections - virology
Animal models
Animal models in research
Animals
Biology and life sciences
Cytokines
Development and progression
Disease Models, Animal
Enzymes
Epidemics
Genomic analysis
Glycoproteins
Health aspects
Humans
Immunoglobulin G
Infections
Inoculation
Kra
Liver
Macaca fascicularis
Medicine and Health Sciences
Mice
Mice, Knockout
Necropsy
Pathogenicity
Pathogens
Pest outbreaks
Phenotypes
R&D
Receptor, Interferon alpha-beta - genetics
Research & development
Research and Analysis Methods
RNA polymerase
RNA virus infections
RNA viruses
Survival
Thrombocytopenia
Tissue analysis
Viremia
Virus Replication
Viruses
United States
West Africa
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Abstract Taï Forest virus (TAFV) is a negative-sense RNA virus in the Filoviridae family. TAFV has caused only a single human infection, but several disease outbreaks in chimpanzees have been linked to this virus. Limited research has been done on this human-pathogenic virus. We sought to establish an animal model to assess TAFV disease progression and pathogenicity at our facility. We had access to two different viral stock preparations from different institutions, both originating from the single human case. Type I interferon receptor knockout mice were inoculated with TAFV stock 1 or stock 2 by the intraperitoneal route. Inoculation resulted in 100% survival with no disease regardless of viral stock preparation or infectious dose. Next, cynomolgus macaques were inoculated with TAFV stock 1 or stock 2. Inoculation with TAFV stock 1 resulted in 100% survival and robust TAFV glycoprotein-specific IgG responses including neutralizing antibodies. In contrast, macaques infected with TAFV stock 2 developed disease and were euthanized 8-11 days after infection exhibiting viremia, thrombocytopenia, and increased inflammatory mediators identified by transcriptional analysis. Histopathologic analysis of tissue samples collected at necropsy confirmed classic filovirus disease in numerous organs. Genomic differences in both stock preparations were mapped to several viral genes which may have contributed to disease severity. Taken together, we demonstrate that infection with the two TAFV stocks resulted in no disease in mice and opposing disease phenotypes in cynomolgus macaques, highlighting the impact of viral stock propagation on pathogenicity in animal models.
AbstractList Taï Forest virus (TAFV) is a negative-sense RNA virus in the Filoviridae family. TAFV has caused only a single human infection, but several disease outbreaks in chimpanzees have been linked to this virus. Limited research has been done on this human-pathogenic virus. We sought to establish an animal model to assess TAFV disease progression and pathogenicity at our facility. We had access to two different viral stock preparations from different institutions, both originating from the single human case. Type I interferon receptor knockout mice were inoculated with TAFV stock 1 or stock 2 by the intraperitoneal route. Inoculation resulted in 100% survival with no disease regardless of viral stock preparation or infectious dose. Next, cynomolgus macaques were inoculated with TAFV stock 1 or stock 2. Inoculation with TAFV stock 1 resulted in 100% survival and robust TAFV glycoprotein-specific IgG responses including neutralizing antibodies. In contrast, macaques infected with TAFV stock 2 developed disease and were euthanized 8–11 days after infection exhibiting viremia, thrombocytopenia, and increased inflammatory mediators identified by transcriptional analysis. Histopathologic analysis of tissue samples collected at necropsy confirmed classic filovirus disease in numerous organs. Genomic differences in both stock preparations were mapped to several viral genes which may have contributed to disease severity. Taken together, we demonstrate that infection with the two TAFV stocks resulted in no disease in mice and opposing disease phenotypes in cynomolgus macaques, highlighting the impact of viral stock propagation on pathogenicity in animal models.
Taï Forest virus (TAFV) is a negative-sense RNA virus in the Filoviridae family. TAFV has caused only a single human infection, but several disease outbreaks in chimpanzees have been linked to this virus. Limited research has been done on this human-pathogenic virus. We sought to establish an animal model to assess TAFV disease progression and pathogenicity at our facility. We had access to two different viral stock preparations from different institutions, both originating from the single human case. Type I interferon receptor knockout mice were inoculated with TAFV stock 1 or stock 2 by the intraperitoneal route. Inoculation resulted in 100% survival with no disease regardless of viral stock preparation or infectious dose. Next, cynomolgus macaques were inoculated with TAFV stock 1 or stock 2. Inoculation with TAFV stock 1 resulted in 100% survival and robust TAFV glycoprotein-specific IgG responses including neutralizing antibodies. In contrast, macaques infected with TAFV stock 2 developed disease and were euthanized 8–11 days after infection exhibiting viremia, thrombocytopenia, and increased inflammatory mediators identified by transcriptional analysis. Histopathologic analysis of tissue samples collected at necropsy confirmed classic filovirus disease in numerous organs. Genomic differences in both stock preparations were mapped to several viral genes which may have contributed to disease severity. Taken together, we demonstrate that infection with the two TAFV stocks resulted in no disease in mice and opposing disease phenotypes in cynomolgus macaques, highlighting the impact of viral stock propagation on pathogenicity in animal models. The 2014–2016 West Africa Ebola virus epidemic was the largest in history affecting 10 countries globally, highlighting concerns for future filovirus outbreaks. In contrast, Taï Forest virus (TAFV), another filovirus, has caused a single human case of infection originating from a TAFV disease outbreak in chimpanzees in West Africa which demonstrates transmission to humans. However, limited research has been performed on this human pathogen. We wanted to fill this knowledge gap and characterize disease as more filovirus outbreaks occur in West Africa. We had access to two TAFV stock preparations with sequence differences from separate institutions, both originating from the single human case. The impact of sequence differences on TAFV pathogenicity was assessed in cohorts of mice and macaques by infection with either TAFV stock. While both stocks caused no disease in mice, macaques displayed opposing disease phenotypes. Infection with TAFV stock 1 resulted in 100% survival with minimal disease; in contrast, macaques infected with TAFV stock 2 developed fatal disease within 11 days. Genomic differences between stock preparations were associated with viral entry and genome replication which could contribute to disease severity. This study highlights the importance of viral genomic differences and their impact on viral pathogenicity.
Taï Forest virus (TAFV) is a negative-sense RNA virus in the Filoviridae family. TAFV has caused only a single human infection, but several disease outbreaks in chimpanzees have been linked to this virus. Limited research has been done on this human-pathogenic virus. We sought to establish an animal model to assess TAFV disease progression and pathogenicity at our facility. We had access to two different viral stock preparations from different institutions, both originating from the single human case. Type I interferon receptor knockout mice were inoculated with TAFV stock 1 or stock 2 by the intraperitoneal route. Inoculation resulted in 100% survival with no disease regardless of viral stock preparation or infectious dose. Next, cynomolgus macaques were inoculated with TAFV stock 1 or stock 2. Inoculation with TAFV stock 1 resulted in 100% survival and robust TAFV glycoprotein-specific IgG responses including neutralizing antibodies. In contrast, macaques infected with TAFV stock 2 developed disease and were euthanized 8-11 days after infection exhibiting viremia, thrombocytopenia, and increased inflammatory mediators identified by transcriptional analysis. Histopathologic analysis of tissue samples collected at necropsy confirmed classic filovirus disease in numerous organs. Genomic differences in both stock preparations were mapped to several viral genes which may have contributed to disease severity. Taken together, we demonstrate that infection with the two TAFV stocks resulted in no disease in mice and opposing disease phenotypes in cynomolgus macaques, highlighting the impact of viral stock propagation on pathogenicity in animal models.Taï Forest virus (TAFV) is a negative-sense RNA virus in the Filoviridae family. TAFV has caused only a single human infection, but several disease outbreaks in chimpanzees have been linked to this virus. Limited research has been done on this human-pathogenic virus. We sought to establish an animal model to assess TAFV disease progression and pathogenicity at our facility. We had access to two different viral stock preparations from different institutions, both originating from the single human case. Type I interferon receptor knockout mice were inoculated with TAFV stock 1 or stock 2 by the intraperitoneal route. Inoculation resulted in 100% survival with no disease regardless of viral stock preparation or infectious dose. Next, cynomolgus macaques were inoculated with TAFV stock 1 or stock 2. Inoculation with TAFV stock 1 resulted in 100% survival and robust TAFV glycoprotein-specific IgG responses including neutralizing antibodies. In contrast, macaques infected with TAFV stock 2 developed disease and were euthanized 8-11 days after infection exhibiting viremia, thrombocytopenia, and increased inflammatory mediators identified by transcriptional analysis. Histopathologic analysis of tissue samples collected at necropsy confirmed classic filovirus disease in numerous organs. Genomic differences in both stock preparations were mapped to several viral genes which may have contributed to disease severity. Taken together, we demonstrate that infection with the two TAFV stocks resulted in no disease in mice and opposing disease phenotypes in cynomolgus macaques, highlighting the impact of viral stock propagation on pathogenicity in animal models.
Audience Academic
Author Doratt, Brianna M
Fletcher, Paige
Malherbe, Delphine C
Clancy, Chad S
Messaoudi, Ilhem
Feldmann, Friederike
O'Donnell, Kyle L
Hanley, Patrick W
Rhoderick, Joseph F
Marzi, Andrea
Takada, Ayato
AuthorAffiliation University of Texas Medical Branch / Galveston National Laboratory, UNITED STATES
6 One Health Research Center, Hokkaido University, Sapporo, Japan
5 International Collaboration Unit, International Institute for Zoonosis Control, Hokkaido University, Sapporo, Japan
2 Rocky Mountain Veterinary Branch, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, United States of America
3 Department of Microbiology, Immunology, and Molecular Genetics, College of Medicine, University of Kentucky, Lexington, Kentucky, United States of America
1 Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, United States of America
4 Division of Global Epidemiology, International Institute for Zoonosis Control, Hokkaido University, Sapporo, Japan
7 Department of Disease Control, School of Veterinary Medicine, University of Z
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PublicationTitle PLoS pathogens
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Snippet Taï Forest virus (TAFV) is a negative-sense RNA virus in the Filoviridae family. TAFV has caused only a single human infection, but several disease outbreaks...
Taï Forest virus (TAFV) is a negative-sense RNA virus in the Filoviridae family. TAFV has caused only a single human infection, but several disease outbreaks...
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doaj
pubmedcentral
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StartPage e1012290
SubjectTerms Alphavirus Infections - pathology
Alphavirus Infections - virology
Animal models
Animal models in research
Animals
Biology and life sciences
Cytokines
Development and progression
Disease Models, Animal
Enzymes
Epidemics
Genomic analysis
Glycoproteins
Health aspects
Humans
Immunoglobulin G
Infections
Inoculation
Kra
Liver
Macaca fascicularis
Medicine and Health Sciences
Mice
Mice, Knockout
Necropsy
Pathogenicity
Pathogens
Pest outbreaks
Phenotypes
R&D
Receptor, Interferon alpha-beta - genetics
Research & development
Research and Analysis Methods
RNA polymerase
RNA virus infections
RNA viruses
Survival
Thrombocytopenia
Tissue analysis
Viremia
Virus Replication
Viruses
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Title Pathogenic differences of cynomolgus macaques after Taï Forest virus infection depend on the viral stock propagation
URI https://www.ncbi.nlm.nih.gov/pubmed/38861571
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http://dx.doi.org/10.1371/journal.ppat.1012290
Volume 20
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