Engineering, decoding and systems-level characterization of chimpanzee cytomegalovirus

The chimpanzee cytomegalovirus (CCMV) is the closest relative of human CMV (HCMV). Because of the high conservation between these two species and the ability of human cells to fully support CCMV replication, CCMV holds great potential as a model system for HCMV. To make the CCMV genome available for...

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Vydané v:PLoS pathogens Ročník 18; číslo 1; s. e1010193
Hlavní autori: Phan, Quang Vinh, Bogdanow, Boris, Wyler, Emanuel, Landthaler, Markus, Liu, Fan, Hagemeier, Christian, Wiebusch, Lüder
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States Public Library of Science 01.01.2022
Public Library of Science (PLoS)
Predmet:
Alternative splicing
Animals
Artificial chromosomes
Bacterial artificial chromosomes
Biology and life sciences
Cell cycle
Chimpanzees
Chromosomes
Cloning
Cytomegalovirus
Cytomegalovirus - genetics
Cytomegalovirus infections
Cytomegalovirus Infections - virology
Decoding
Deoxyribonucleic acid
Disease Models, Animal
DNA
DNA sequencing
Epithelial cells
Epithelium
Frameshift mutation
Gene expression
Gene manipulation
Gene sequencing
Genetic aspects
Genome, Viral
Genomes
Genomics
Health aspects
Human performance
Humans
Immunocompromised host
Infections
Medicine and Health Sciences
Mutation
Pan troglodytes - virology
Phylogeny
Proteomes
Research and analysis methods
Transcriptomes
Tropism
Viruses
Germany
United States > US
ISSN:1553-7374, 1553-7366, 1553-7374
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Abstract The chimpanzee cytomegalovirus (CCMV) is the closest relative of human CMV (HCMV). Because of the high conservation between these two species and the ability of human cells to fully support CCMV replication, CCMV holds great potential as a model system for HCMV. To make the CCMV genome available for precise and rapid gene manipulation techniques, we captured the genomic DNA of CCMV strain Heberling as a bacterial artificial chromosome (BAC). Selected BAC clones were reconstituted to infectious viruses, growing to similar high titers as parental CCMV. DNA sequencing confirmed the integrity of our clones and led to the identification of two polymorphic loci and a deletion-prone region within the CCMV genome. To re-evaluate the CCMV coding potential, we analyzed the viral transcriptome and proteome and identified several novel ORFs, splice variants, and regulatory RNAs. We further characterized the dynamics of CCMV gene expression and found that viral proteins cluster into five distinct temporal classes. In addition, our datasets revealed that the host response to CCMV infection and the de-regulation of cellular pathways are in line with known hallmarks of HCMV infection. In a first functional experiment, we investigated a proposed frameshift mutation in UL128 that was suspected to restrict CCMV’s cell tropism. In fact, repair of this frameshift re-established productive CCMV infection in endothelial and epithelial cells, expanding the options of CCMV as an infection model. Thus, BAC-cloned CCMV can serve as a powerful tool for systematic approaches in comparative functional genomics, exploiting the close phylogenetic relationship between CCMV and HCMV.
AbstractList The chimpanzee cytomegalovirus (CCMV) is the closest relative of human CMV (HCMV). Because of the high conservation between these two species and the ability of human cells to fully support CCMV replication, CCMV holds great potential as a model system for HCMV. To make the CCMV genome available for precise and rapid gene manipulation techniques, we captured the genomic DNA of CCMV strain Heberling as a bacterial artificial chromosome (BAC). Selected BAC clones were reconstituted to infectious viruses, growing to similar high titers as parental CCMV. DNA sequencing confirmed the integrity of our clones and led to the identification of two polymorphic loci and a deletion-prone region within the CCMV genome. To re-evaluate the CCMV coding potential, we analyzed the viral transcriptome and proteome and identified several novel ORFs, splice variants, and regulatory RNAs. We further characterized the dynamics of CCMV gene expression and found that viral proteins cluster into five distinct temporal classes. In addition, our datasets revealed that the host response to CCMV infection and the de-regulation of cellular pathways are in line with known hallmarks of HCMV infection. In a first functional experiment, we investigated a proposed frameshift mutation in UL128 that was suspected to restrict CCMV’s cell tropism. In fact, repair of this frameshift re-established productive CCMV infection in endothelial and epithelial cells, expanding the options of CCMV as an infection model. Thus, BAC-cloned CCMV can serve as a powerful tool for systematic approaches in comparative functional genomics, exploiting the close phylogenetic relationship between CCMV and HCMV. Human cytomegalovirus (HCMV) infection is associated with systemic disease in immunocompromised individuals and congenitally infected neonates. Animal CMVs and their bacterial artificial chromosome (BAC) clones have been utilized as models for CMV infection and thereby contributed immensely to the understanding of pathogenesis, host immune response and underlying molecular mechanism of CMV infections. As the closest relative to HCMV, the chimpanzee CMV (CCMV) holds a great potential as a model system for HCMV infection but its application was limited due to the lack of tools and data for functional genomic analyses. Here, the cloning of the CCMV as a BAC vector made its viral genome available to gene targeting techniques that allow the efficient application of reverse genetic strategies. Furthermore, the multi-omic datasets created in this study provide an in-depth view of the viral gene repertoire and the host cell responses to infection, confirming the close phylogenetic relationship between HCMV and CCMV on a system level. Taken together, the newly established CCMV-BAC system presents a framework for HCMV modelling and comparative studies to address key questions in evolutionary processes and infection mechanisms.
The chimpanzee cytomegalovirus (CCMV) is the closest relative of human CMV (HCMV). Because of the high conservation between these two species and the ability of human cells to fully support CCMV replication, CCMV holds great potential as a model system for HCMV. To make the CCMV genome available for precise and rapid gene manipulation techniques, we captured the genomic DNA of CCMV strain Heberling as a bacterial artificial chromosome (BAC). Selected BAC clones were reconstituted to infectious viruses, growing to similar high titers as parental CCMV. DNA sequencing confirmed the integrity of our clones and led to the identification of two polymorphic loci and a deletion-prone region within the CCMV genome. To re-evaluate the CCMV coding potential, we analyzed the viral transcriptome and proteome and identified several novel ORFs, splice variants, and regulatory RNAs. We further characterized the dynamics of CCMV gene expression and found that viral proteins cluster into five distinct temporal classes. In addition, our datasets revealed that the host response to CCMV infection and the de-regulation of cellular pathways are in line with known hallmarks of HCMV infection. In a first functional experiment, we investigated a proposed frameshift mutation in UL128 that was suspected to restrict CCMV's cell tropism. In fact, repair of this frameshift re-established productive CCMV infection in endothelial and epithelial cells, expanding the options of CCMV as an infection model. Thus, BAC-cloned CCMV can serve as a powerful tool for systematic approaches in comparative functional genomics, exploiting the close phylogenetic relationship between CCMV and HCMV.
The chimpanzee cytomegalovirus (CCMV) is the closest relative of human CMV (HCMV). Because of the high conservation between these two species and the ability of human cells to fully support CCMV replication, CCMV holds great potential as a model system for HCMV. To make the CCMV genome available for precise and rapid gene manipulation techniques, we captured the genomic DNA of CCMV strain Heberling as a bacterial artificial chromosome (BAC). Selected BAC clones were reconstituted to infectious viruses, growing to similar high titers as parental CCMV. DNA sequencing confirmed the integrity of our clones and led to the identification of two polymorphic loci and a deletion-prone region within the CCMV genome. To re-evaluate the CCMV coding potential, we analyzed the viral transcriptome and proteome and identified several novel ORFs, splice variants, and regulatory RNAs. We further characterized the dynamics of CCMV gene expression and found that viral proteins cluster into five distinct temporal classes. In addition, our datasets revealed that the host response to CCMV infection and the de-regulation of cellular pathways are in line with known hallmarks of HCMV infection. In a first functional experiment, we investigated a proposed frameshift mutation in UL128 that was suspected to restrict CCMV's cell tropism. In fact, repair of this frameshift re-established productive CCMV infection in endothelial and epithelial cells, expanding the options of CCMV as an infection model. Thus, BAC-cloned CCMV can serve as a powerful tool for systematic approaches in comparative functional genomics, exploiting the close phylogenetic relationship between CCMV and HCMV.The chimpanzee cytomegalovirus (CCMV) is the closest relative of human CMV (HCMV). Because of the high conservation between these two species and the ability of human cells to fully support CCMV replication, CCMV holds great potential as a model system for HCMV. To make the CCMV genome available for precise and rapid gene manipulation techniques, we captured the genomic DNA of CCMV strain Heberling as a bacterial artificial chromosome (BAC). Selected BAC clones were reconstituted to infectious viruses, growing to similar high titers as parental CCMV. DNA sequencing confirmed the integrity of our clones and led to the identification of two polymorphic loci and a deletion-prone region within the CCMV genome. To re-evaluate the CCMV coding potential, we analyzed the viral transcriptome and proteome and identified several novel ORFs, splice variants, and regulatory RNAs. We further characterized the dynamics of CCMV gene expression and found that viral proteins cluster into five distinct temporal classes. In addition, our datasets revealed that the host response to CCMV infection and the de-regulation of cellular pathways are in line with known hallmarks of HCMV infection. In a first functional experiment, we investigated a proposed frameshift mutation in UL128 that was suspected to restrict CCMV's cell tropism. In fact, repair of this frameshift re-established productive CCMV infection in endothelial and epithelial cells, expanding the options of CCMV as an infection model. Thus, BAC-cloned CCMV can serve as a powerful tool for systematic approaches in comparative functional genomics, exploiting the close phylogenetic relationship between CCMV and HCMV.
Audience Academic
Author Wyler, Emanuel
Bogdanow, Boris
Landthaler, Markus
Hagemeier, Christian
Wiebusch, Lüder
Liu, Fan
Phan, Quang Vinh
AuthorAffiliation 3 Berlin Institute for Medical Systems Biology, Max-Delbrück-Center for Molecular Medicine, Berlin, Germany
2 Department of Structural Biology, Leibniz-Forschungsinstitut für Molekulare Pharmakologie, Berlin, Germany
Oregon Health and Science University, UNITED STATES
1 Department of Pediatric Oncology/Hematology, Charité—Universitätsmedizin Berlin, Berlin, Germany
AuthorAffiliation_xml – name: 3 Berlin Institute for Medical Systems Biology, Max-Delbrück-Center for Molecular Medicine, Berlin, Germany
– name: 1 Department of Pediatric Oncology/Hematology, Charité—Universitätsmedizin Berlin, Berlin, Germany
– name: 2 Department of Structural Biology, Leibniz-Forschungsinstitut für Molekulare Pharmakologie, Berlin, Germany
– name: Oregon Health and Science University, UNITED STATES
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  surname: Phan
  fullname: Phan, Quang Vinh
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/34982803$$D View this record in MEDLINE/PubMed
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CitedBy_id crossref_primary_10_3390_pharmaceutics16091238
crossref_primary_10_1371_journal_ppat_1010992
crossref_primary_10_1007_s12268_023_1920_0
crossref_primary_10_1128_jvi_01206_24
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Current address: Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts, United States of America
The authors have declared that no competing interests exist.
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  text: 2022-01-01
  day: 01
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PLoS pathogens
PublicationTitleAlternate PLoS Pathog
PublicationYear 2022
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
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Snippet The chimpanzee cytomegalovirus (CCMV) is the closest relative of human CMV (HCMV). Because of the high conservation between these two species and the ability...
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StartPage e1010193
SubjectTerms Alternative splicing
Animals
Artificial chromosomes
Bacterial artificial chromosomes
Biology and life sciences
Cell cycle
Chimpanzees
Chromosomes
Cloning
Cytomegalovirus
Cytomegalovirus - genetics
Cytomegalovirus infections
Cytomegalovirus Infections - virology
Decoding
Deoxyribonucleic acid
Disease Models, Animal
DNA
DNA sequencing
Epithelial cells
Epithelium
Frameshift mutation
Gene expression
Gene manipulation
Gene sequencing
Genetic aspects
Genome, Viral
Genomes
Genomics
Health aspects
Human performance
Humans
Immunocompromised host
Infections
Medicine and Health Sciences
Mutation
Pan troglodytes - virology
Phylogeny
Proteomes
Research and analysis methods
Transcriptomes
Tropism
Viruses
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Title Engineering, decoding and systems-level characterization of chimpanzee cytomegalovirus
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Volume 18
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