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Article ; Online: Rethinking human cytomegalovirus latency reservoir.

Schwartz, Michal / Stern-Ginossar, Noam

Annals of the New York Academy of Sciences

2023 Volume 1524, Issue 1, Page(s) 30–36

Abstract: Human cytomegalovirus (HCMV) is a prevalent herpesvirus, infecting the majority of the human population. Like other herpesviruses, it causes lifelong infection through the establishment of latency. Although reactivation from latency can cause significant ...

Abstract	Human cytomegalovirus (HCMV) is a prevalent herpesvirus, infecting the majority of the human population. Like other herpesviruses, it causes lifelong infection through the establishment of latency. Although reactivation from latency can cause significant morbidity and mortality in immunocompromised hosts, our understanding of HCMV latency and how it is maintained remains limited. Here, we discuss the characterized latency reservoir in hematopoietic cells in the bone marrow and the gaps in our knowledge of mechanisms that facilitate HCMV genome maintenance in dividing cells. We further review clinical evidence that strongly suggests the tissue origin of HCMV reactivation, and we outline similarities to murine cytomegalovirus where latency in tissue-resident cells has been demonstrated. Overall, we think these observations call for a rethinking of HCMV latency reservoirs and point to potential sources of HCMV latency that reside in tissues.
MeSH term(s)	Animals ; Humans ; Mice ; Cytomegalovirus/isolation & purification ; Cytomegalovirus/physiology ; Cytomegalovirus Infections/virology ; Muromegalovirus/physiology ; Virus Activation ; Virus Latency/physiology
Language	English
Publishing date	2023-04-07
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	211003-9
ISSN	1749-6632 ; 0077-8923
ISSN (online)	1749-6632
ISSN	0077-8923
DOI	10.1111/nyas.14994
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Article ; Online: Translation-A tug of war during viral infection.

Rozman, Batsheva / Fisher, Tal / Stern-Ginossar, Noam

Molecular cell

2022 Volume 83, Issue 3, Page(s) 481–495

Abstract: Viral reproduction is contingent on viral protein synthesis that relies on the host ribosomes. As such, viruses have evolved remarkable strategies to hijack the host translational apparatus in order to favor viral protein production and to interfere with ...

Abstract	Viral reproduction is contingent on viral protein synthesis that relies on the host ribosomes. As such, viruses have evolved remarkable strategies to hijack the host translational apparatus in order to favor viral protein production and to interfere with cellular innate defenses. Here, we describe the approaches viruses use to exploit the translation machinery, focusing on commonalities across diverse viral families, and discuss the functional relevance of this process. We illustrate the complementary strategies host cells utilize to block viral protein production and consider how cells ensure an efficient antiviral response that relies on translation during this tug of war over the ribosome. Finally, we highlight potential roles mRNA modifications and ribosome quality control play in translational regulation and innate immunity. We address these topics in the context of the COVID-19 pandemic and focus on the gaps in our current knowledge of these mechanisms, specifically in viruses with pandemic potential.
MeSH term(s)	Humans ; COVID-19/genetics ; COVID-19/immunology ; Pandemics ; Protein Biosynthesis/genetics ; Protein Biosynthesis/immunology ; RNA, Viral/genetics ; RNA, Viral/immunology ; Viral Proteins/genetics ; Viral Proteins/immunology ; Virus Diseases/genetics ; Virus Diseases/immunology ; Viruses/genetics ; Viruses/immunology ; Ribosomes/genetics ; Ribosomes/immunology ; Ribosomes/virology
Chemical Substances	RNA, Viral ; Viral Proteins
Language	English
Publishing date	2022-11-04
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2022.10.012
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Article ; Online: The RNA modification N

Shulman, Ziv / Stern-Ginossar, Noam

Nature immunology

2020 Volume 21, Issue 5, Page(s) 501–512

Abstract: Protection from harmful pathogens depends on activation of the immune system, which relies on tight regulation of gene expression. Recently, the RNA modification ... ...

Abstract	Protection from harmful pathogens depends on activation of the immune system, which relies on tight regulation of gene expression. Recently, the RNA modification N
MeSH term(s)	Adaptive Immunity/genetics ; Adenosine/analogs & derivatives ; Adenosine/genetics ; Animals ; Cell Differentiation ; Humans ; Immune System ; Immunity, Innate/genetics ; Immunomodulation ; RNA/genetics ; RNA Processing, Post-Transcriptional/immunology
Chemical Substances	RNA (63231-63-0) ; N-methyladenosine (CLE6G00625) ; Adenosine (K72T3FS567)
Language	English
Publishing date	2020-04-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2016987-5
ISSN	1529-2916 ; 1529-2908
ISSN (online)	1529-2916
ISSN	1529-2908
DOI	10.1038/s41590-020-0650-4
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Article ; Online: The Transcriptome of Latent Human Cytomegalovirus.

Schwartz, Michal / Stern-Ginossar, Noam

Journal of virology

2019 Volume 93, Issue 11

Abstract: The latent human cytomegalovirus (HCMV) transcriptome has been extremely difficult to define due to the scarcity of naturally latent cells and the complexity of available models. The genomic era offers many approaches to transcriptome profiling that hold ...

Abstract	The latent human cytomegalovirus (HCMV) transcriptome has been extremely difficult to define due to the scarcity of naturally latent cells and the complexity of available models. The genomic era offers many approaches to transcriptome profiling that hold great potential for elucidating this challenging issue. The results from two recent studies applying different transcriptomic methodologies and analyses of both experimental and natural samples challenge the dogma of a restricted latency-associated transcription program. Instead, they portray the hallmark of HCMV latent infection as low-level expression of a broad spectrum of canonical viral lytic genes.
MeSH term(s)	Cell Line ; Cells, Cultured ; Cytomegalovirus/genetics ; Cytomegalovirus/physiology ; Cytomegalovirus Infections/virology ; Gene Expression Profiling/methods ; Gene Expression Regulation, Viral/genetics ; Humans ; Transcriptome/genetics ; Viral Proteins/metabolism ; Virus Latency/genetics
Chemical Substances	Viral Proteins
Language	English
Publishing date	2019-05-15
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.00047-19
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Article ; Online: Essentiality and dynamic expression of the human tRNA pool during viral infection

Aharon-Hefetz, Noa / Schwartz, Michal / Dahan, Orna / Stern-Ginossar, Noam / Pilpel, Yitzhak

bioRxiv

Abstract: Human viruses depend on the translation resources of the host cell. A significant translation resource is the tRNA pool of the cell, as human viruses do not encode tRNA genes. Through tRNA sequencing, we inspected the human tRNA pool upon infection of ... ...

Abstract	Human viruses depend on the translation resources of the host cell. A significant translation resource is the tRNA pool of the cell, as human viruses do not encode tRNA genes. Through tRNA sequencing, we inspected the human tRNA pool upon infection of human Cytomegalovirus (HCMV) and SARS-CoV-2. HCMV-induced alterations in tRNA expression were predominantly virus-driven, with minimal influence from the cellular immune response. Notably, specific tRNA post-transcriptional modifications appeared to modulate stability and were susceptible to HCMV manipulation. In contrast, SARS-CoV-2 infection did not significantly impact tRNA expression or modifications. We compared the codon usage of viral genes to the proliferation-differentiation codon-usage signatures of human genes. We found a marked difference between the viruses, with HCMV genes aligning with differentiation codon usage and SARS-CoV-2 genes reflecting proliferation codon usage. We further found that codon usage of structural and gene expression-related viral genes displayed high adaptation to host cell tRNA pools. Through a systematic CRISPR screen targeting human tRNA genes and modification enzymes, we identified specific tRNAs and enzymes that improve or reduce HCMV infectivity and cellular growth. These findings highlight the dynamic interplay between the tRNA pool and viral infection dynamics, shedding light on mechanisms governing host-virus interactions.
Keywords	covid19
Language	English
Publishing date	2024-04-30
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2024.04.25.591047
Database	COVID19

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Article ; Online: Temporal dynamics of HCMV gene expression in lytic and latent infections.

Rozman, Batsheva / Nachshon, Aharon / Levi Samia, Roi / Lavi, Michael / Schwartz, Michal / Stern-Ginossar, Noam

Cell reports

2022 Volume 39, Issue 2, Page(s) 110653

Abstract: During productive human cytomegalovirus (HCMV) infection, viral genes are expressed in a coordinated cascade that conventionally relies on the dependencies of viral genes on protein synthesis and viral DNA replication. By contrast, the transcriptional ... ...

Abstract	During productive human cytomegalovirus (HCMV) infection, viral genes are expressed in a coordinated cascade that conventionally relies on the dependencies of viral genes on protein synthesis and viral DNA replication. By contrast, the transcriptional landscape of HCMV latency is poorly understood. Here, we examine viral gene expression dynamics during the establishment of both productive and latent HCMV infections. We redefine HCMV gene expression kinetics during productive infection and reveal that viral gene regulation does not represent a simple sequential cascade; many viral genes are regulated by multiple independent modules. Using our improved gene expression classification combined with transcriptome-wide measurements of the effects of a wide array of epigenetic inhibitors on viral gene expression during latency, we show that a defining feature of latency is the unique repression of immediate-early (IE) genes. Altogether, we recharacterize HCMV gene expression kinetics and reveal governing principles of lytic and latent gene expression.
MeSH term(s)	Cytomegalovirus/genetics ; DNA Replication ; DNA, Viral ; Gene Expression Regulation, Viral ; Humans ; Latent Infection ; Transcriptome ; Virus Latency/genetics ; Virus Replication/genetics
Chemical Substances	DNA, Viral
Language	English
Publishing date	2022-04-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2022.110653
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Article ; Online: Decoding viral infection by ribosome profiling.

Stern-Ginossar, Noam

Journal of virology

2015 Volume 89, Issue 12, Page(s) 6164–6166

Abstract: Ribosome profiling is an emerging technique that uses deep sequencing to monitor translation in live cells. Studies using ribosome profiling have already provided novel insights into the identities and amounts of the proteins being produced in cells, as ... ...

Abstract	Ribosome profiling is an emerging technique that uses deep sequencing to monitor translation in live cells. Studies using ribosome profiling have already provided novel insights into the identities and amounts of the proteins being produced in cells, as well as novel insights into the mechanism of protein synthesis and translation regulation. Application of ribosome profiling to cells infected with human cytomegalovirus and Kaposi's sarcoma-associated herpesvirus revealed unanticipated complexity in the coding capacity of herpesviruses. Here, I discuss these results and how the application of ribosome profiling to cells infected with other viruses can reveal novel insights into the process of infection.
MeSH term(s)	Cytomegalovirus/genetics ; Cytomegalovirus/growth & development ; Cytomegalovirus Infections/virology ; Gene Expression Profiling/methods ; Herpesviridae Infections/virology ; Herpesvirus 8, Human/genetics ; Herpesvirus 8, Human/growth & development ; Humans ; Molecular Biology/methods ; Protein Biosynthesis ; RNA, Messenger/genetics ; Ribosomes/genetics
Chemical Substances	RNA, Messenger
Language	English
Publishing date	2015-06
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.02528-14
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Article ; Online: Viral Short ORFs and Their Possible Functions.

Finkel, Yaara / Stern-Ginossar, Noam / Schwartz, Michal

Proteomics

2018 Volume 18, Issue 10, Page(s) e1700255

Abstract: Definition of functional genomic elements is one of the greater challenges of the genomic era. Traditionally, putative short open reading frames (sORFs) coding for less than 100 amino acids were disregarded due to computational and experimental ... ...

Abstract	Definition of functional genomic elements is one of the greater challenges of the genomic era. Traditionally, putative short open reading frames (sORFs) coding for less than 100 amino acids were disregarded due to computational and experimental limitations; however, it has become clear over the past several years that translation of sORFs is pervasive and serves diverse functions. The development of ribosome profiling, allowing identification of translated sequences genome wide, revealed wide spread, previously unidentified translation events. New computational methodologies as well as improved mass spectrometry approaches also contributed to the task of annotating translated sORFs in different organisms. Viruses are of special interest due to the selective pressure on their genome size, their rapid and confining evolution, and the potential contribution of novel peptides to the host immune response. Indeed, many functional viral sORFs were characterized to date, and ribosome profiling analyses suggest that this may be the tip of the iceberg. Our computational analyses of sORFs identified by ribosome profiling in DNA viruses demonstrate that they may be enriched in specific features implying that at least some of them are functional. Combination of systematic genome editing strategies with synthetic tagging will take us into the next step-elucidation of the biological relevance and function of this intriguing class of molecules.
MeSH term(s)	Genomics ; Molecular Sequence Annotation ; Open Reading Frames ; Peptide Fragments/genetics ; Peptide Fragments/metabolism ; Viral Proteins/genetics ; Viral Proteins/metabolism ; Viruses/genetics ; Viruses/metabolism
Chemical Substances	Peptide Fragments ; Viral Proteins
Keywords	covid19
Language	English
Publishing date	2018-01-19
Publishing country	Germany
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2032093-0
ISSN	1615-9861 ; 1615-9853
ISSN (online)	1615-9861
ISSN	1615-9853
DOI	10.1002/pmic.201700255
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Article ; Online: Translational Control in Virus-Infected Cells.

Stern-Ginossar, Noam / Thompson, Sunnie R / Mathews, Michael B / Mohr, Ian

Cold Spring Harbor perspectives in biology

2019 Volume 11, Issue 3

Abstract: As obligate intracellular parasites, virus reproduction requires host cell functions. Despite variations in genome size and configuration, nucleic acid composition, and their repertoire of encoded functions, all viruses remain unconditionally dependent ... ...

Abstract	As obligate intracellular parasites, virus reproduction requires host cell functions. Despite variations in genome size and configuration, nucleic acid composition, and their repertoire of encoded functions, all viruses remain unconditionally dependent on the protein synthesis machinery resident within their cellular hosts to translate viral messenger RNAs (mRNAs). A complex signaling network responsive to physiological stress, including infection, regulates host translation factors and ribosome availability. Furthermore, access to the translation apparatus is patrolled by powerful host immune defenses programmed to restrict viral invaders. Here, we review the tactics and mechanisms used by viruses to appropriate control over host ribosomes, subvert host defenses, and dominate the infected cell translational landscape. These not only define aspects of infection biology paramount for virus reproduction, but continue to drive fundamental discoveries into how cellular protein synthesis is controlled in health and disease.
MeSH term(s)	Animals ; Gene Expression Regulation, Viral ; Host-Pathogen Interactions ; Humans ; Plant Viruses/metabolism ; Protein Biosynthesis ; RNA Processing, Post-Transcriptional ; Ribosomes/metabolism ; Stress, Physiological ; Viral Proteins/biosynthesis ; Virus Diseases/metabolism ; Virus Replication
Chemical Substances	Viral Proteins
Language	English
Publishing date	2019-03-01
Publishing country	United States
Document type	Journal Article ; Review
ISSN	1943-0264
ISSN (online)	1943-0264
DOI	10.1101/cshperspect.a033001
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Article ; Online: Molecular characterization of human cytomegalovirus infection with single-cell transcriptomics.

Schwartz, Michal / Shnayder, Miri / Nachshon, Aharon / Arazi, Tamar / Kitsberg, Yaarit / Levi Samia, Roi / Lavi, Michael / Kuint, Rottem / Tsabari, Reuven / Stern-Ginossar, Noam

Nature microbiology

2023 Volume 8, Issue 3, Page(s) 455–468

Abstract: Human cytomegalovirus (HCMV) can result in either productive or non-productive infection, with the latter potentially leading to viral latency. The molecular factors dictating these outcomes are poorly understood. Here we used single-cell transcriptomics ...

Abstract	Human cytomegalovirus (HCMV) can result in either productive or non-productive infection, with the latter potentially leading to viral latency. The molecular factors dictating these outcomes are poorly understood. Here we used single-cell transcriptomics to analyse HCMV infection progression in monocytes, which are latently infected, and macrophages, considered to be permissive for productive infection. We show that early viral gene expression levels, specifically of those encoding immediate early proteins IE1 and IE2, are a major factor dictating productive infection. We also revealed that intrinsic, not induced, host cell interferon-stimulated gene expression level is a main determinant of infection outcome. Intrinsic interferon-stimulated gene expression is downregulated with monocyte to macrophage differentiation, partially explaining increased macrophage susceptibility to productive HCMV infection. Furthermore, non-productive macrophages could reactivate, making them potential latent virus reservoirs. Overall, we decipher molecular features underlying HCMV infection outcomes and propose macrophages as a potential HCMV reservoir.
MeSH term(s)	Humans ; Transcriptome ; Cytomegalovirus/genetics ; Cytomegalovirus/metabolism ; Cytomegalovirus Infections/genetics ; Immediate-Early Proteins/genetics ; Interferons/metabolism
Chemical Substances	Immediate-Early Proteins ; Interferons (9008-11-1)
Language	English
Publishing date	2023-02-02
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	2058-5276
ISSN (online)	2058-5276
DOI	10.1038/s41564-023-01325-x
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