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Article: Inhibition of Venezuelan Equine Encephalitis Virus Using Small Interfering RNAs

Haikerwal, Amrita / Barrera, Michael D. / Bhalla, Nishank / Zhou, Weidong / Boghdeh, Niloufar / Anderson, Carol / Alem, Farhang / Narayanan, Aarthi

Viruses. 2022 July 26, v. 14, no. 8

2022

Abstract: Acutely infectious new world alphaviruses such as Venezuelan Equine Encephalitis Virus (VEEV) pose important challenges to the human population due to a lack of effective therapeutic intervention strategies. Small interfering RNAs that can selectively ... ...

Abstract	Acutely infectious new world alphaviruses such as Venezuelan Equine Encephalitis Virus (VEEV) pose important challenges to the human population due to a lack of effective therapeutic intervention strategies. Small interfering RNAs that can selectively target the viral genome (vsiRNAs) has been observed to offer survival advantages in several in vitro and in vivo models of acute virus infections, including alphaviruses such as Chikungunya virus and filoviruses such as Ebola virus. In this study, novel vsiRNAs that targeted conserved regions in the nonstructural and structural genes of the VEEV genome were designed and evaluated for antiviral activity in mammalian cells in the context of VEEV infection. The data demonstrate that vsiRNAs were able to effectively decrease the infectious virus titer at earlier time points post infection in the context of the attenuated TC-83 strain and the virulent Trinidad Donkey strain, while the inhibition was overcome at later time points. Depletion of Argonaute 2 protein (Ago2), the catalytic component of the RISC complex, negated the inhibitory effect of the vsiRNAs, underscoring the involvement of the siRNA pathway in the inhibition process. Depletion of the RNAi pathway proteins Dicer, MOV10, TRBP2 and Matrin 3 decreased viral load in infected cells, alluding to an impact of the RNAi pathway in the establishment of a productive infection. Additional studies focused on rational combinations of effective vsiRNAs and delivery strategies to confer better in vivo bioavailability and distribution to key target tissues such as the brain can provide effective solutions to treat encephalitic diseases resulting from alphavirus infections.
Keywords	Chikungunya virus ; Ebolavirus ; Venezuelan equine encephalitis virus ; antiviral properties ; bioavailability ; brain ; human population ; mammals ; therapeutics ; viral genome ; viral load ; virulence ; viruses ; Trinidad and Tobago
Language	English
Dates of publication	2022-0726
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2516098-9
ISSN	1999-4915
ISSN	1999-4915
DOI	10.3390/v14081628
Database	NAL-Catalogue (AGRICOLA)

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Article: Inhibitors of Venezuelan Equine Encephalitis Virus Identified Based on Host Interaction Partners of Viral Non-Structural Protein 3

Bakovic, Allison / Bhalla, Nishank / Alem, Farhang / Campbell, Catherine / Zhou, Weidong / Narayanan, Aarthi

Viruses. 2021 Aug. 03, v. 13, no. 8

2021

Abstract: Venezuelan equine encephalitis virus (VEEV) is a new world alphavirus and a category B select agent. Currently, no FDA-approved vaccines or therapeutics are available to treat VEEV exposure and resultant disease manifestations. The C-terminus of the VEEV ...

Abstract	Venezuelan equine encephalitis virus (VEEV) is a new world alphavirus and a category B select agent. Currently, no FDA-approved vaccines or therapeutics are available to treat VEEV exposure and resultant disease manifestations. The C-terminus of the VEEV non-structural protein 3 (nsP3) facilitates cell-specific and virus-specific host factor binding preferences among alphaviruses, thereby providing targets of interest when designing novel antiviral therapeutics. In this study, we utilized an overexpression construct encoding HA-tagged nsP3 to identify host proteins that interact with VEEV nsP3 by mass spectrometry. Bioinformatic analyses of the putative interactors identified 42 small molecules with the potential to inhibit the host interaction targets, and thus potentially inhibit VEEV. Three inhibitors, tomatidine, citalopram HBr, and Z-VEID-FMK, reduced replication of both the TC-83 strain and the Trinidad donkey (TrD) strain of VEEV by at least 10-fold in astrocytoma, astroglial, and microglial cells. Further, these inhibitors reduced replication of the related New World (NW) alphavirus Eastern equine encephalitis virus (EEEV) in multiple cell types, thus demonstrating broad-spectrum antiviral activity. Time-course assays revealed all three inhibitors reduced both infectious particle production and positive-sense RNA levels post-infection. Further evaluation of the putative host targets for the three inhibitors revealed an interaction of VEEV nsP3 with TFAP2A, but not eIF2S2. Mechanistic studies utilizing siRNA knockdowns demonstrated that eIF2S2, but not TFAP2A, supports both efficient TC-83 replication and genomic RNA synthesis, but not subgenomic RNA translation. Overall, this work reveals the composition of the VEEV nsP3 proteome and the potential to identify host-based, broad spectrum therapeutic approaches to treat new world alphavirus infections.
Keywords	Eastern equine encephalitis virus ; Venezuelan equine encephalitis virus ; antiviral properties ; asses ; astrocytoma ; bioinformatics ; genomics ; mass spectrometry ; proteome ; therapeutics ; viral nonstructural proteins ; Trinidad and Tobago
Language	English
Dates of publication	2021-0803
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2516098-9
ISSN	1999-4915
ISSN	1999-4915
DOI	10.3390/v13081533
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Inhibitors of Venezuelan Equine Encephalitis Virus Identified Based on Host Interaction Partners of Viral Non-Structural Protein 3.

Bakovic, Allison / Bhalla, Nishank / Alem, Farhang / Campbell, Catherine / Zhou, Weidong / Narayanan, Aarthi

Viruses

2021 Volume 13, Issue 8

Abstract	Venezuelan equine encephalitis virus (VEEV) is a new world alphavirus and a category B select agent. Currently, no FDA-approved vaccines or therapeutics are available to treat VEEV exposure and resultant disease manifestations. The C-terminus of the VEEV non-structural protein 3 (nsP3) facilitates cell-specific and virus-specific host factor binding preferences among alphaviruses, thereby providing targets of interest when designing novel antiviral therapeutics. In this study, we utilized an overexpression construct encoding HA-tagged nsP3 to identify host proteins that interact with VEEV nsP3 by mass spectrometry. Bioinformatic analyses of the putative interactors identified 42 small molecules with the potential to inhibit the host interaction targets, and thus potentially inhibit VEEV. Three inhibitors, tomatidine, citalopram HBr, and Z-VEID-FMK, reduced replication of both the TC-83 strain and the Trinidad donkey (TrD) strain of VEEV by at least 10-fold in astrocytoma, astroglial, and microglial cells. Further, these inhibitors reduced replication of the related New World (NW) alphavirus Eastern equine encephalitis virus (EEEV) in multiple cell types, thus demonstrating broad-spectrum antiviral activity. Time-course assays revealed all three inhibitors reduced both infectious particle production and positive-sense RNA levels post-infection. Further evaluation of the putative host targets for the three inhibitors revealed an interaction of VEEV nsP3 with TFAP2A, but not eIF2S2. Mechanistic studies utilizing siRNA knockdowns demonstrated that eIF2S2, but not TFAP2A, supports both efficient TC-83 replication and genomic RNA synthesis, but not subgenomic RNA translation. Overall, this work reveals the composition of the VEEV nsP3 proteome and the potential to identify host-based, broad spectrum therapeutic approaches to treat new world alphavirus infections.
MeSH term(s)	Animals ; Antiviral Agents/pharmacology ; Cell Line ; Chlorocebus aethiops ; Encephalitis Virus, Venezuelan Equine/drug effects ; Encephalitis Virus, Venezuelan Equine/genetics ; Horses ; Host Microbial Interactions/drug effects ; Humans ; Proteome ; Vero Cells ; Viral Nonstructural Proteins/antagonists & inhibitors ; Viral Nonstructural Proteins/classification ; Viral Nonstructural Proteins/genetics ; Virus Replication/drug effects
Chemical Substances	Antiviral Agents ; Proteome ; Viral Nonstructural Proteins
Language	English
Publishing date	2021-08-03
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v13081533
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Inhibition of Venezuelan Equine Encephalitis Virus Using Small Interfering RNAs.

Haikerwal, Amrita / Barrera, Michael D / Bhalla, Nishank / Zhou, Weidong / Boghdeh, Niloufar / Anderson, Carol / Alem, Farhang / Narayanan, Aarthi

Viruses

2022 Volume 14, Issue 8

Abstract	Acutely infectious new world alphaviruses such as Venezuelan Equine Encephalitis Virus (VEEV) pose important challenges to the human population due to a lack of effective therapeutic intervention strategies. Small interfering RNAs that can selectively target the viral genome (vsiRNAs) has been observed to offer survival advantages in several in vitro and in vivo models of acute virus infections, including alphaviruses such as Chikungunya virus and filoviruses such as Ebola virus. In this study, novel vsiRNAs that targeted conserved regions in the nonstructural and structural genes of the VEEV genome were designed and evaluated for antiviral activity in mammalian cells in the context of VEEV infection. The data demonstrate that vsiRNAs were able to effectively decrease the infectious virus titer at earlier time points post infection in the context of the attenuated TC-83 strain and the virulent Trinidad Donkey strain, while the inhibition was overcome at later time points. Depletion of Argonaute 2 protein (Ago2), the catalytic component of the RISC complex, negated the inhibitory effect of the vsiRNAs, underscoring the involvement of the siRNA pathway in the inhibition process. Depletion of the RNAi pathway proteins Dicer, MOV10, TRBP2 and Matrin 3 decreased viral load in infected cells, alluding to an impact of the RNAi pathway in the establishment of a productive infection. Additional studies focused on rational combinations of effective vsiRNAs and delivery strategies to confer better in vivo bioavailability and distribution to key target tissues such as the brain can provide effective solutions to treat encephalitic diseases resulting from alphavirus infections.
MeSH term(s)	Animals ; Cell Line ; Encephalitis Virus, Venezuelan Equine/physiology ; Horses ; Humans ; RNA Helicases ; RNA, Small Interfering/pharmacology ; Virus Replication
Chemical Substances	RNA, Small Interfering ; Mov10 protein, human (EC 2.7.7.-) ; RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2022-07-26
Publishing country	Switzerland
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v14081628
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Proteomic Discovery of VEEV E2-Host Partner Interactions Identifies GRP78 Inhibitor HA15 as a Potential Therapeutic for Alphavirus Infections

Barrera, Michael D / Callahan, Victoria / Akhrymuk, Ivan / Bhalla, Nishank / Zhou, Weidong / Campbell, Catherine / Narayanan, Aarthi / Kehn-Hall, Kylene

Pathogens. 2021 Mar. 02, v. 10, no. 3

2021

Abstract: Alphaviruses are a genus of the Togaviridae family and are widely distributed across the globe. Venezuelan equine encephalitis virus (VEEV) and eastern equine encephalitis virus (EEEV), cause encephalitis and neurological sequelae while chikungunya virus ...

Abstract	Alphaviruses are a genus of the Togaviridae family and are widely distributed across the globe. Venezuelan equine encephalitis virus (VEEV) and eastern equine encephalitis virus (EEEV), cause encephalitis and neurological sequelae while chikungunya virus (CHIKV) and Sindbis virus (SINV) cause arthralgia. There are currently no approved therapeutics or vaccines available for alphaviruses. In order to identify novel therapeutics, a V5 epitope tag was inserted into the N-terminus of the VEEV E2 glycoprotein and used to identify host-viral protein interactions. Host proteins involved in protein folding, metabolism/ATP production, translation, cytoskeleton, complement, vesicle transport and ubiquitination were identified as VEEV E2 interactors. Multiple inhibitors targeting these host proteins were tested to determine their effect on VEEV replication. The compound HA15, a GRP78 inhibitor, was found to be an effective inhibitor of VEEV, EEEV, CHIKV, and SINV. VEEV E2 interaction with GRP78 was confirmed through coimmunoprecipitation and colocalization experiments. Mechanism of action studies found that HA15 does not affect viral RNA replication but instead affects late stages of the viral life cycle, which is consistent with GRP78 promoting viral assembly or viral protein trafficking.
Keywords	Chikungunya virus ; Eastern equine encephalitis virus ; RNA replication ; Sindbis virus ; Venezuelan equine encephalitis virus ; complement ; complications (disease) ; cytoskeleton ; encephalitis ; epitopes ; glycoproteins ; mechanism of action ; precipitin tests ; proteomics ; therapeutics ; ubiquitination ; virus assembly
Language	English
Dates of publication	2021-0302
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
Note	NAL-light
ZDB-ID	2695572-6
ISSN	2076-0817
ISSN	2076-0817
DOI	10.3390/pathogens10030283
Database	NAL-Catalogue (AGRICOLA)

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Article: Human Antimicrobial Peptides as Therapeutics for Viral Infections

Ahmed, Aslaa / Siman-Tov, Gavriella / Hall, Grant / Bhalla, Nishank / Narayanan, Aarthi

Viruses. 2019 Aug. 01, v. 11, no. 8

2019

Abstract: Successful in vivo infection following pathogen entry requires the evasion and subversion of multiple immunological barriers. Antimicrobial peptides (AMPs) are one of the first immune pathways upregulated during infection by multiple pathogens, in ... ...

Abstract	Successful in vivo infection following pathogen entry requires the evasion and subversion of multiple immunological barriers. Antimicrobial peptides (AMPs) are one of the first immune pathways upregulated during infection by multiple pathogens, in multiple organs in vivo. In humans, there are many classes of AMPs exhibiting broad antimicrobial activities, with defensins and the human cathelicidin LL-37 being the best studied examples. Whereas historically the efficacy and therapeutic potential of AMPs against bacterial infection has been the primary focus of research, recent studies have begun to elucidate the antiviral properties of AMPs as well as their role in regulation of inflammation and chemoattraction. AMPs as therapeutic tools seem especially promising against emerging infectious viral pathogens for which no approved vaccines or treatments are currently available, such as dengue virus (DENV) and Zika virus (ZIKV). In this review, we summarize recent studies elucidating the efficacy and diverse mechanisms of action of various classes of AMPs against multiple viral pathogens, as well as the potential use of human AMPs in novel antiviral therapeutic strategies.
Keywords	Dengue virus ; Zika virus ; antiviral properties ; bacterial infections ; cathelicidins ; chemoattractants ; humans ; inflammation ; mechanism of action ; pathogens ; therapeutics ; vaccines ; covid19
Language	English
Dates of publication	2019-0801
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2516098-9
ISSN	1999-4915
ISSN	1999-4915
DOI	10.3390/v11080704
Database	NAL-Catalogue (AGRICOLA)

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Article: Proteomic Discovery of VEEV E2-Host Partner Interactions Identifies GRP78 Inhibitor HA15 as a Potential Therapeutic for Alphavirus Infections.

Barrera, Michael D / Callahan, Victoria / Akhrymuk, Ivan / Bhalla, Nishank / Zhou, Weidong / Campbell, Catherine / Narayanan, Aarthi / Kehn-Hall, Kylene

Pathogens (Basel, Switzerland)

2021 Volume 10, Issue 3

Abstract: Alphaviruses are a genus of ... ...

Abstract	Alphaviruses are a genus of the
Language	English
Publishing date	2021-03-02
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2695572-6
ISSN	2076-0817
ISSN	2076-0817
DOI	10.3390/pathogens10030283
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Brilacidin Demonstrates Inhibition of SARS-CoV-2 in Cell Culture.

Bakovic, Allison / Risner, Kenneth / Bhalla, Nishank / Alem, Farhang / Chang, Theresa L / Weston, Warren K / Harness, Jane A / Narayanan, Aarthi

Viruses

2021 Volume 13, Issue 2

Abstract: Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), the newly emergent causative agent of coronavirus disease-19 (COVID-19), has resulted in more than two million deaths worldwide since it was first detected in 2019. There is a critical global ... ...

Abstract	Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), the newly emergent causative agent of coronavirus disease-19 (COVID-19), has resulted in more than two million deaths worldwide since it was first detected in 2019. There is a critical global need for therapeutic intervention strategies that can be deployed to safely treat COVID-19 disease and reduce associated morbidity and mortality. Increasing evidence shows that both natural and synthetic antimicrobial peptides (AMPs), also referred to as Host Defense Proteins/Peptides (HDPs), can inhibit SARS-CoV-2, paving the way for the potential clinical use of these molecules as therapeutic options. In this manuscript, we describe the potent antiviral activity exerted by brilacidin-a de novo designed synthetic small molecule that captures the biological properties of HDPs-on SARS-CoV-2 in a human lung cell line (Calu-3) and a monkey cell line (Vero). These data suggest that SARS-CoV-2 inhibition in these cell culture models is likely to be a result of the impact of brilacidin on viral entry and its disruption of viral integrity. Brilacidin demonstrated synergistic antiviral activity when combined with remdesivir. Collectively, our data demonstrate that brilacidin exerts potent inhibition of SARS-CoV-2 against different strains of the virus in cell culture.
MeSH term(s)	Adenosine Monophosphate/analogs & derivatives ; Adenosine Monophosphate/pharmacology ; Alanine/analogs & derivatives ; Alanine/pharmacology ; Animals ; Antiviral Agents/pharmacology ; COVID-19/virology ; Cell Culture Techniques ; Cell Line ; Chlorocebus aethiops ; Defensins/pharmacology ; Guanidines/pharmacology ; Humans ; Peptidomimetics/pharmacology ; Pyrimidines/pharmacology ; SARS-CoV-2/drug effects ; SARS-CoV-2/physiology ; Vero Cells ; Virus Internalization/drug effects ; Virus Replication/drug effects ; COVID-19 Drug Treatment
Chemical Substances	Antiviral Agents ; Defensins ; Guanidines ; Peptidomimetics ; Pyrimidines ; remdesivir (3QKI37EEHE) ; Adenosine Monophosphate (415SHH325A) ; brilacidin (I1679X069H) ; Alanine (OF5P57N2ZX)
Language	English
Publishing date	2021-02-09
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v13020271
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Human Antimicrobial Peptides as Therapeutics for Viral Infections.

Ahmed, Aslaa / Siman-Tov, Gavriella / Hall, Grant / Bhalla, Nishank / Narayanan, Aarthi

Viruses

2019 Volume 11, Issue 8

Abstract	Successful in vivo infection following pathogen entry requires the evasion and subversion of multiple immunological barriers. Antimicrobial peptides (AMPs) are one of the first immune pathways upregulated during infection by multiple pathogens, in multiple organs in vivo. In humans, there are many classes of AMPs exhibiting broad antimicrobial activities, with defensins and the human cathelicidin LL-37 being the best studied examples. Whereas historically the efficacy and therapeutic potential of AMPs against bacterial infection has been the primary focus of research, recent studies have begun to elucidate the antiviral properties of AMPs as well as their role in regulation of inflammation and chemoattraction. AMPs as therapeutic tools seem especially promising against emerging infectious viral pathogens for which no approved vaccines or treatments are currently available, such as dengue virus (DENV) and Zika virus (ZIKV). In this review, we summarize recent studies elucidating the efficacy and diverse mechanisms of action of various classes of AMPs against multiple viral pathogens, as well as the potential use of human AMPs in novel antiviral therapeutic strategies.
MeSH term(s)	Antimicrobial Cationic Peptides/genetics ; Antimicrobial Cationic Peptides/pharmacology ; Antimicrobial Cationic Peptides/therapeutic use ; Antiviral Agents/pharmacology ; Antiviral Agents/therapeutic use ; Humans ; Immunomodulation ; Virus Diseases/drug therapy ; Virus Diseases/prevention & control ; Virus Replication/drug effects ; Viruses/drug effects
Chemical Substances	Antimicrobial Cationic Peptides ; Antiviral Agents
Keywords	covid19
Language	English
Publishing date	2019-08-01
Publishing country	Switzerland
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v11080704
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Macromolecular Synthesis Shutoff Resistance by Myeloid Cells Is Critical to IRF7-Dependent Systemic Interferon Alpha/Beta Induction after Alphavirus Infection.

Bhalla, Nishank / Gardner, Christina L / Downs, Sierra N / Dunn, Matthew / Sun, Chengqun / Klimstra, William B

Journal of virology

2019 Volume 93, Issue 24

Abstract: Alphavirus infection of fibroblastic cell ... ...

Abstract	Alphavirus infection of fibroblastic cell types
MeSH term(s)	Alphavirus/physiology ; Alphavirus Infections/metabolism ; Animals ; Cell Line ; Disease Models, Animal ; Encephalitis Virus, Venezuelan Equine/physiology ; Fibroblasts/virology ; Humans ; Interferon Regulatory Factor-3/genetics ; Interferon Regulatory Factor-7/genetics ; Interferon Regulatory Factor-7/metabolism ; Interferon-alpha/metabolism ; Interferon-beta/metabolism ; Macromolecular Substances/metabolism ; Mice ; Mice, Knockout ; Myeloid Cells/metabolism ; Myeloid Cells/virology ; RAW 264.7 Cells ; Virus Replication
Chemical Substances	Interferon Regulatory Factor-3 ; Interferon Regulatory Factor-7 ; Interferon-alpha ; Irf3 protein, mouse ; Irf7 protein, mouse ; Macromolecular Substances ; Interferon-beta (77238-31-4)
Language	English
Publishing date	2019-11-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.00872-19
Database	MEDical Literature Analysis and Retrieval System OnLINE

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