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Article ; Online: 2-Bromopalmitate depletes lipid droplets to inhibit viral replication.

Liu, Dongxiao / Cruz-Cosme, Ruth / Wu, Yong / Leibowitz, Julian / Tang, Qiyi

2024 Volume 98, Issue 4, Page(s) e0017124

Abstract: The global impact of emerging viral infections emphasizes the urgent need for effective broad-spectrum antivirals. The cellular organelle, lipid droplet (LD), is utilized by many types of viruses for replication, but its reduction does not affect cell ... ...

Abstract	The global impact of emerging viral infections emphasizes the urgent need for effective broad-spectrum antivirals. The cellular organelle, lipid droplet (LD), is utilized by many types of viruses for replication, but its reduction does not affect cell survival. Therefore, LD is a potential target for developing broad-spectrum antivirals. In this study, we found that 2-bromopalmitate (2 BP), a previously defined palmitoylation inhibitor, depletes LD across all studied cell lines and exerts remarkable antiviral effects on different coronaviruses. We comprehensively utilized 2 BP, alongside other palmitoylation inhibitors such as cerulenin and 2-fluoro palmitic acid (2-FPA), as well as the enhancer palmostatin B and evaluated their impact on LD and the replication of human coronaviruses (hCoV-229E, hCoV-Oc43) and murine hepatitis virus (MHV-A59) at non-cytotoxic concentrations. While cerulenin and 2-FPA exhibited moderate inhibition of viral replication, 2 BP exhibited a much stronger suppressive effect on MHV-A59 replication, although they share similar inhibitory effects on palmitoylation. As expected, palmostatin B significantly enhanced viral replication, it failed to rescue the inhibitory effects of 2 BP, whereas it effectively counteracted the effects of cerulenin and 2-FPA. This suggests that the mechanism that 2 BP used to inhibit viral replication is beyond palmitoylation inhibition. Further investigations unveil that 2 BP uniquely depletes LDs, a phenomenon not exhibited by 2-FPA and cerulenin. Importantly, the depletion of LDs was closely associated with the inhibition of viral replication because the addition of oleic acid to 2 BP significantly rescued LD depletion and its inhibitory effects on MHV-A59. Our findings indicate that the inhibitory effects of 2 BP on viral replication primarily stem from LD disruption rather than palmitoylation inhibition. Intriguingly, fatty acid (FA) assays demonstrated that 2 BP reduces the FA level in mitochondria while concurrently increasing FA levels in the cytoplasm. These results highlight the crucial role of LDs in viral replication and uncover a novel biological activity of 2 BP. These insights contribute to the development of broad-spectrum antiviral strategies. Importance: In our study, we conducted a comparative investigation into the antiviral effects of palmitoylation inhibitors including 2-bromopalmitate (2-BP), 2-fluoro palmitic acid (2-FPA), and cerulenin. Surprisingly, we discovered that 2-BP has superior inhibitory effects on viral replication compared to 2-FPA and cerulenin. However, their inhibitory effects on palmitoylation were the same. Intrigued by this finding, we delved deeper into the underlying mechanism of 2-BP's potent antiviral activity, and we unveiled a novel biological activity of 2-BP: depletion of lipid droplets (LDs). Importantly, we also highlighted the crucial role of LDs in viral replication. Our insights shed new light on the antiviral mechanism of LD depletion paving the way for the development of broad-spectrum antiviral strategies by targeting LDs.
MeSH term(s)	Animals ; Humans ; Mice ; Antiviral Agents/pharmacology ; Antiviral Agents/metabolism ; Cerulenin/metabolism ; Cerulenin/pharmacology ; Coronavirus/drug effects ; Coronavirus/physiology ; Lipid Droplets/drug effects ; Palmitates/pharmacology ; Palmitic Acid/pharmacology ; Palmitic Acid/metabolism ; Propiolactone/analogs & derivatives ; Virus Replication/drug effects ; Murine hepatitis virus/drug effects ; Murine hepatitis virus/physiology
Chemical Substances	2-bromopalmitate (18263-25-7) ; Antiviral Agents ; Cerulenin (17397-89-6) ; Palmitates ; Palmitic Acid (2V16EO95H1) ; palmostatin B ; Propiolactone (6RC3ZT4HB0)
Language	English
Publishing date	2024-03-15
Publishing country	United States
Document type	Journal Article
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/jvi.00171-24
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Article: Antiviral Effect of Antimicrobial Peptoid TM9 and Murine Model of Respiratory Coronavirus Infection.

Lebedev, Maxim / Benjamin, Aaron B / Kumar, Sathish / Molchanova, Natalia / Lin, Jennifer S / Koster, Kent J / Leibowitz, Julian L / Barron, Annelise E / Cirillo, Jeffrey D

Pharmaceutics

2024 Volume 16, Issue 4

Abstract: New antiviral agents are essential to improving treatment and control of SARS-CoV-2 infections that can lead to the disease COVID-19. Antimicrobial peptoids are sequence-specific oligo- ...

Abstract	New antiviral agents are essential to improving treatment and control of SARS-CoV-2 infections that can lead to the disease COVID-19. Antimicrobial peptoids are sequence-specific oligo-
Language	English
Publishing date	2024-03-27
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527217-2
ISSN	1999-4923
ISSN	1999-4923
DOI	10.3390/pharmaceutics16040464
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Article ; Online: Uncovering the Vital Role of Lipid Droplets in Coronavirus Replication: A Novel Insight Arising from the Biological Activity of 2-Bromopalmitate

Liu, Dongxiao / Cruz-Cosme, Ruth / Wu, Yong / Leibowitz, Julian L. / Tang, Qiyi

bioRxiv

Abstract: The emergence of viral infections with global impact highlights the urgent need for broad-spectrum antivirals. In this study, we evaluated the effect of palmitoylation inhibitors [2-bromopalmitate (2-BP), cerulenin, and 2-fluoro palmitic acid (2-FPA)] ... ...

Abstract	The emergence of viral infections with global impact highlights the urgent need for broad-spectrum antivirals. In this study, we evaluated the effect of palmitoylation inhibitors [2-bromopalmitate (2-BP), cerulenin, and 2-fluoro palmitic acid (2-FPA)] and the enhancer palmostatin B on the replication of human coronaviruses (hCoV-229E, hCoV-Oc43) and murine hepatitis virus (MHV-A59) at non-cytotoxic concentrations. The results demonstrated that 2-BP strongly suppressed MHV-A59 replication, while cerulenin and 2-FPA only moderately inhibited viral replication. Palmostatin B significantly enhanced viral replication. Notably, 2-BP exhibited superior efficacy. Interestingly, palmostatin B failed to rescue the inhibitory effects of 2-BP but effectively rescued cerulenin and 2-FPA, suggesting additional biological activities of 2-BP beyond palmitoylation inhibition. Furthermore, we discovered that 2-BP specifically disrupted lipid droplets (LDs), and this LD disruption was correlated with viral replication inhibition. Based on our findings, we conclude that the inhibitory effects of 2-BP on viral replication primarily stem from LD disruption rather than palmitoylation inhibition. Therefore, we revealed the crucial role of LDs in the viral replication. Our study provides insights into the development of wide-spectrum antiviral strategies.
Keywords	covid19
Language	English
Publishing date	2023-06-30
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2023.06.29.547086
Database	COVID19

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Article ; Online: The structure and functions of coronavirus genomic 3' and 5' ends.

Yang, Dong / Leibowitz, Julian L

Virus research

2015 Volume 206, Page(s) 120–133

Abstract: Coronaviruses (CoVs) are an important cause of illness in humans and animals. Most human coronaviruses commonly cause relatively mild respiratory illnesses; however two zoonotic coronaviruses, SARS-CoV and MERS-CoV, can cause severe illness and death. ... ...

Abstract	Coronaviruses (CoVs) are an important cause of illness in humans and animals. Most human coronaviruses commonly cause relatively mild respiratory illnesses; however two zoonotic coronaviruses, SARS-CoV and MERS-CoV, can cause severe illness and death. Investigations over the past 35 years have illuminated many aspects of coronavirus replication. The focus of this review is the functional analysis of conserved RNA secondary structures in the 5' and 3' of the betacoronavirus genomes. The 5' 350 nucleotides folds into a set of RNA secondary structures which are well conserved, and reverse genetic studies indicate that these structures play an important role in the discontinuous synthesis of subgenomic RNAs in the betacoronaviruses. These cis-acting elements extend 3' of the 5'UTR into ORF1a. The 3'UTR is similarly conserved and contains all of the cis-acting sequences necessary for viral replication. Two competing conformations near the 5' end of the 3'UTR have been shown to make up a potential molecular switch. There is some evidence that an association between the 3' and 5'UTRs is necessary for subgenomic RNA synthesis, but the basis for this association is not yet clear. A number of host RNA proteins have been shown to bind to the 5' and 3' cis-acting regions, but the significance of these in viral replication is not clear. Two viral proteins have been identified as binding to the 5' cis-acting region, nsp1 and N protein. A genetic interaction between nsp8 and nsp9 and the region of the 3'UTR that contains the putative molecular switch suggests that these two proteins bind to this region.
MeSH term(s)	3' Untranslated Regions ; 5' Untranslated Regions ; Animals ; Conserved Sequence ; Coronavirus/genetics ; Coronavirus/physiology ; Genome, Viral ; Host-Pathogen Interactions ; Humans ; Models, Biological ; Nucleic Acid Conformation ; Promoter Regions, Genetic ; RNA, Viral/chemistry ; RNA, Viral/genetics ; RNA, Viral/metabolism ; RNA-Binding Proteins/metabolism ; Transcription, Genetic ; Virus Replication
Chemical Substances	3' Untranslated Regions ; 5' Untranslated Regions ; RNA, Viral ; RNA-Binding Proteins
Keywords	covid19
Language	English
Publishing date	2015-08-03
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	605780-9
ISSN	1872-7492 ; 0168-1702
ISSN (online)	1872-7492
ISSN	0168-1702
DOI	10.1016/j.virusres.2015.02.025
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Article ; Online: PRESCIENT: platform for the rapid evaluation of antibody success using integrated microfluidics enabled technology.

Wippold, Jose A / Wang, Han / Tingling, Joseph / Leibowitz, Julian L / de Figueiredo, Paul / Han, Arum

Lab on a chip

2020 Volume 20, Issue 9, Page(s) 1628–1638

Abstract: Identifying antibodies (Abs) that neutralize infectious agents is the first step for developing therapeutics, vaccines, and diagnostic tools for these infectious agents. However, current approaches for identifying neutralizing Abs (nAbs) typically rely ... ...

Abstract	Identifying antibodies (Abs) that neutralize infectious agents is the first step for developing therapeutics, vaccines, and diagnostic tools for these infectious agents. However, current approaches for identifying neutralizing Abs (nAbs) typically rely on dilution-based assays that are costly, inefficient, and only survey a small subset of the entire repertoire. There are also intrinsic biases in many steps of conventional nAb identification processes. More importantly, conventional assays rely on simple Ab-antigen binding assays, which may not result in identifying the most potent nAbs, as the strongest binder may not be the most potent nAb. Droplet microfluidic systems have the capability to overcome such limitations by conducting complex multi-step assays with high reliability, resolution, and throughput in a pico-liter volume water-in-oil emulsion droplet format. Here, we describe the development of PRESCIENT (Platform for the Rapid Evaluation of antibody SucCess using Integrated microfluidics ENabled Technology), a droplet microfluidic system that can enable high-throughput single-cell resolution identification of nAb repertoires elicited in response to viral infection. We demonstrate PRESCIENT's ability to identify Abs that neutralize a model viral agent, Murine coronavirus (murine hepatitis virus), which causes high mortality rates in experimentally infected mice. In-droplet infection of host cells by the virus was first demonstrated, followed by demonstration of in-droplet neutralization by nAbs produced from a single Ab-producing hybridoma cell. Finally, fluorescence intensity analyses of two populations of hybridoma cell lines (nAb-producing and non-nAb-producing hybridoma cell lines) successfully discriminated between the two populations. The presented strategy and platform have the potential to identify and investigate neutralizing activities against a broad range of potential infectious agents for which nAbs have yet to be discovered, significantly advancing the nAb identification process as well as reinvigorating the field of Ab discovery, characterization, and development.
MeSH term(s)	Animals ; Antibodies, Neutralizing/immunology ; Antibodies, Viral/immunology ; Cell Line ; Coronavirus/immunology ; Coronavirus/isolation & purification ; Lab-On-A-Chip Devices ; Mice ; Microfluidics/methods ; Virus Diseases/diagnosis ; Virus Diseases/veterinary ; Virus Diseases/virology
Chemical Substances	Antibodies, Neutralizing ; Antibodies, Viral
Keywords	covid19
Language	English
Publishing date	2020-03-20
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2056646-3
ISSN	1473-0189 ; 1473-0197
ISSN (online)	1473-0189
ISSN	1473-0197
DOI	10.1039/c9lc01165j
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Article ; Online: Sub-second heat inactivation of coronavirus using a betacoronavirus model.

Jiang, Yuqian / Zhang, Han / Wippold, Jose A / Gupta, Jyotsana / Dai, Jing / de Figueiredo, Paul / Leibowitz, Julian L / Han, Arum

Biotechnology and bioengineering

2021 Volume 118, Issue 5, Page(s) 2067–2075

Abstract: Heat treatment denatures viral proteins that comprise the virion, making the virus incapable of infecting a host. Coronavirus (CoV) virions contain single-stranded RNA genomes with a lipid envelope and four proteins, three of which are associated with ... ...

Abstract	Heat treatment denatures viral proteins that comprise the virion, making the virus incapable of infecting a host. Coronavirus (CoV) virions contain single-stranded RNA genomes with a lipid envelope and four proteins, three of which are associated with the lipid envelope and thus are thought to be easily denatured by heat or surfactant-type chemicals. Prior studies have shown that a temperature as low as 75°C with a treatment duration of 15 min can effectively inactivate CoV. The degree of CoV heat inactivation greatly depends on the length of heat treatment time and the temperature applied. With the goal of finding whether sub-second heat exposure of CoV can sufficiently inactivate CoV, we designed and developed a simple fluidic system that can measure sub-second heat inactivation of CoV. The system is composed of a stainless-steel capillary immersed in a temperature-controlled oil bath followed by an ice bath, through which virus solution can flow at various speeds. Flowing virus solution at different speeds, along with temperature control and monitoring system, allows the virus to be exposed to the desired temperature and treatment durations with high accuracy. Using mouse hepatitis virus, a betacoronavirus, as a model CoV system, we identified that 71.8°C for 0.51 s exposure is sufficient to obtain >5 Log
MeSH term(s)	Betacoronavirus/physiology ; Hot Temperature ; Murine hepatitis virus/physiology ; Viral Plaque Assay ; Virus Inactivation
Language	English
Publishing date	2021-03-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	280318-5
ISSN	1097-0290 ; 0006-3592
ISSN (online)	1097-0290
ISSN	0006-3592
DOI	10.1002/bit.27720
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Article ; Online: Equine bronchial epithelial cells are susceptible to cell entry with a SARS-CoV-2 pseudovirus but reveal low replication efficiency.

Legere, Rebecca M / Allegro, Angelica R / Affram, Yvonne / Silveira, Bibiana Petri da / Fridley, Jennifer L / Wells, Kelsey M / Oezguen, Numan / Burghardt, Robert C / Wright, Gus A / Pollet, Jeroen / Bordin, Angela I / Figueiredo, Paul de / Leibowitz, Julian L / Cohen, Noah D

American journal of veterinary research

2023 Volume 84, Issue 9

Abstract: Objective: To examine the susceptibility of cultured primary equine bronchial epithelial cells (EBECs) to a severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pseudovirus relative to human bronchial epithelial cells (HBECs).: Sample: ... ...

Abstract	Objective: To examine the susceptibility of cultured primary equine bronchial epithelial cells (EBECs) to a severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pseudovirus relative to human bronchial epithelial cells (HBECs). Sample: Primary EBEC cultures established from healthy adult horses and commercially sourced human bronchial epithelial cells (HBECs) were used as a positive control. Methods: Angiotensin-converting enzyme 2 (ACE2) expression by EBECs was demonstrated using immunofluorescence, western immunoblot, and flow cytometry. EBECs were transduced with a lentivirus pseudotyped with the SARS-CoV-2 spike protein that binds to ACE2 and expresses the enhanced green fluorescent protein (eGFP) as a reporter. Cells were transduced with the pseudovirus at a multiplicity of infection of 0.1 for 6 hours, washed, and maintained in media for 96 hours. After 96 hours, eGFP expression in EBECs was assessed by fluorescence microscopy of cell cultures and quantitative PCR. Results: ACE2 expression in EBECs detected by immunofluorescence, western immunoblotting, and flow cytometry was lower in EBECs than in HBECs. After 96 hours, eGFP expression in EBECs was demonstrated by fluorescence microscopy, and mean ΔCt values from quantitative PCR were significantly (P < .0001) higher in EBECs (8.78) than HBECs (3.24) indicating lower infectivity in EBECs. Clinical relevance: Equine respiratory tract cells were susceptible to cell entry with a SARS-CoV-2 pseudovirus. Lower replication efficiency in EBECs suggests that horses are unlikely to be an important zoonotic host of SARS-CoV-2, but viral mutations could render some strains more infective to horses. Serological and virological monitoring of horses in contact with persons shedding SARS-CoV-2 is warranted.
MeSH term(s)	Horses ; Animals ; Humans ; SARS-CoV-2/metabolism ; Angiotensin-Converting Enzyme 2/metabolism ; Virus Internalization ; COVID-19/veterinary ; Epithelial Cells ; Horse Diseases
Chemical Substances	spike protein, SARS-CoV-2 ; Angiotensin-Converting Enzyme 2 (EC 3.4.17.23)
Language	English
Publishing date	2023-07-18
Publishing country	United States
Document type	Journal Article
ZDB-ID	390796-x
ISSN	1943-5681 ; 0002-9645
ISSN (online)	1943-5681
ISSN	0002-9645
DOI	10.2460/ajvr.23.06.0132
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Article ; Online: Coronaviruses: Molecular and Cellular Biology

Leibowitz, Julian L.

Emerg Infect Dis

Abstract: Coronaviruses: Molecular and Cellular ... ...

Abstract	Coronaviruses: Molecular and Cellular Biology
Keywords	covid19
Publisher	PMC
Document type	Article ; Online
DOI	10.3201/eid1404.080016
Database	COVID19

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Article: The structure and functions of coronavirus genomic 3′ and 5′ ends

Yang, Dong / Leibowitz, Julian L

Virus research. 2015 Aug. 03, v. 206

2015

Abstract	Coronaviruses (CoVs) are an important cause of illness in humans and animals. Most human coronaviruses commonly cause relatively mild respiratory illnesses; however two zoonotic coronaviruses, SARS-CoV and MERS-CoV, can cause severe illness and death. Investigations over the past 35 years have illuminated many aspects of coronavirus replication. The focus of this review is the functional analysis of conserved RNA secondary structures in the 5′ and 3′ of the betacoronavirus genomes. The 5′ 350 nucleotides folds into a set of RNA secondary structures which are well conserved, and reverse genetic studies indicate that these structures play an important role in the discontinuous synthesis of subgenomic RNAs in the betacoronaviruses. These cis-acting elements extend 3′ of the 5′UTR into ORF1a. The 3′UTR is similarly conserved and contains all of the cis-acting sequences necessary for viral replication. Two competing conformations near the 5′ end of the 3′UTR have been shown to make up a potential molecular switch. There is some evidence that an association between the 3′ and 5′UTRs is necessary for subgenomic RNA synthesis, but the basis for this association is not yet clear. A number of host RNA proteins have been shown to bind to the 5′ and 3′ cis-acting regions, but the significance of these in viral replication is not clear. Two viral proteins have been identified as binding to the 5′ cis-acting region, nsp1 and N protein. A genetic interaction between nsp8 and nsp9 and the region of the 3′UTR that contains the putative molecular switch suggests that these two proteins bind to this region.
Keywords	3' untranslated regions ; 5' untranslated regions ; Middle East respiratory syndrome coronavirus ; Severe acute respiratory syndrome coronavirus ; death ; disease severity ; genome ; genomics ; humans ; nucleotides ; respiratory tract diseases ; viral proteins ; virus replication ; covid19
Language	English
Dates of publication	2015-0803
Size	p. 120-133.
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	605780-9
ISSN	1872-7492 ; 0168-1702
ISSN (online)	1872-7492
ISSN	0168-1702
DOI	10.1016/j.virusres.2015.02.025
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Coronavirus pathogenesis.

Weiss, Susan R / Leibowitz, Julian L

Advances in virus research

2011 Volume 81, Page(s) 85–164

Abstract: Coronaviruses infect many species of animals including humans, causing acute and chronic diseases. This review focuses primarily on the pathogenesis of murine coronavirus mouse hepatitis virus (MHV) and severe acute respiratory coronavirus (SARS-CoV). ... ...

Abstract	Coronaviruses infect many species of animals including humans, causing acute and chronic diseases. This review focuses primarily on the pathogenesis of murine coronavirus mouse hepatitis virus (MHV) and severe acute respiratory coronavirus (SARS-CoV). MHV is a collection of strains, which provide models systems for the study of viral tropism and pathogenesis in several organs systems, including the central nervous system, the liver, and the lung, and has been cited as providing one of the few animal models for the study of chronic demyelinating diseases such as multiple sclerosis. SARS-CoV emerged in the human population in China in 2002, causing a worldwide epidemic with severe morbidity and high mortality rates, particularly in older individuals. We review the pathogenesis of both viruses and the several reverse genetics systems that made much of these studies possible. We also review the functions of coronavirus proteins, structural, enzymatic, and accessory, with an emphasis on roles in pathogenesis. Structural proteins in addition to their roles in virion structure and morphogenesis also contribute significantly to viral spread in vivo and in antagonizing host cell responses. Nonstructural proteins include the small accessory proteins that are not at all conserved between MHV and SARS-CoV and the 16 conserved proteins encoded in the replicase locus, many of which have enzymatic activities in RNA metabolism or protein processing in addition to functions in antagonizing host response.
MeSH term(s)	Animals ; Coronavirus Infections/pathology ; Coronavirus Infections/virology ; Humans ; Mice ; Murine hepatitis virus/genetics ; Murine hepatitis virus/pathogenicity ; Severe acute respiratory syndrome-related coronavirus/genetics ; Severe acute respiratory syndrome-related coronavirus/pathogenicity ; Viral Nonstructural Proteins/genetics ; Viral Nonstructural Proteins/metabolism ; Viral Structural Proteins/genetics ; Viral Structural Proteins/metabolism ; Viral Tropism ; Virulence ; Virulence Factors/genetics ; Virulence Factors/metabolism
Chemical Substances	Viral Nonstructural Proteins ; Viral Structural Proteins ; Virulence Factors
Keywords	covid19
Language	English
Publishing date	2011-11-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	195-8
ISSN	1557-8399 ; 0065-3527
ISSN (online)	1557-8399
ISSN	0065-3527
DOI	10.1016/B978-0-12-385885-6.00009-2
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