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Article: Mouse Adapted SARS-CoV-2 Model Induces "Long-COVID" Neuropathology in BALB/c Mice.

Gressett, Timothy E / Leist, Sarah R / Ismael, Saifudeen / Talkington, Grant / Dinnon, Kenneth H / Baric, Ralph S / Bix, Gregory

bioRxiv : the preprint server for biology

2023

Abstract: The novel coronavirus SARS-CoV-2 has caused significant global morbidity and mortality and continues to burden patients with persisting neurological dysfunction. COVID-19 survivors develop debilitating symptoms to include neuro-psychological dysfunction, ...

Abstract	The novel coronavirus SARS-CoV-2 has caused significant global morbidity and mortality and continues to burden patients with persisting neurological dysfunction. COVID-19 survivors develop debilitating symptoms to include neuro-psychological dysfunction, termed "Long COVID", which can cause significant reduction of quality of life. Despite vigorous model development, the possible cause of these symptoms and the underlying pathophysiology of this devastating disease remains elusive. Mouse adapted (MA10) SARS-CoV-2 is a novel mouse-based model of COVID-19 which simulates the clinical symptoms of respiratory distress associated with SARS-CoV-2 infection in mice. In this study, we evaluated the long-term effects of MA10 infection on brain pathology and neuroinflammation. 10-week and 1-year old female BALB/cAnNHsd mice were infected intranasally with 10
Language	English
Publishing date	2023-03-20
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.03.18.533204
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Article ; Online: Mouse Adapted SARS-CoV-2 Model Induces "Long-COVID" Neuropathology in BALB/c Mice

Gressett, Timothy E. / Leist, Sarah R. / Ismael, Saifudeen / Talkington, Grant / Dinnon, Kenneth H. / Baric, Ralph S. / Bix, Gregory

bioRxiv

Abstract	The novel coronavirus SARS-CoV-2 has caused significant global morbidity and mortality and continues to burden patients with persisting neurological dysfunction. COVID-19 survivors develop debilitating symptoms to include neuro-psychological dysfunction, termed "Long COVID", which can cause significant reduction of quality of life. Despite vigorous model development, the possible cause of these symptoms and the underlying pathophysiology of this devastating disease remains elusive. Mouse adapted (MA10) SARS-CoV-2 is a novel mouse-based model of COVID-19 which simulates the clinical symptoms of respiratory distress associated with SARS-CoV-2 infection in mice. In this study, we evaluated the long-term effects of MA10 infection on brain pathology and neuroinflammation. 10-week and 1-year old female BALB/cAnNHsd mice were infected intranasally with 10<sup>4</sup> plaque-forming units (PFU) and 10<sup>3</sup> PFU of SARS-CoV-2 MA10, respectively, and the brain was examined 60 days post-infection (dpi). Immunohistochemical analysis showed a decrease in the neuronal nuclear protein NeuN and an increase in Iba-1 positive amoeboid microglia in the hippocampus after MA10 infection, indicating long-term neurological changes in a brain area which is critical for long-term memory consolidation and processing. Importantly, these changes were seen in 40-50% of infected mice, which correlates to prevalence of LC seen clinically. Our data shows for the first time that MA10 infection induces neuropathological outcomes several weeks after infection at similar rates of observed clinical prevalence of "Long COVID". These observations strengthen the MA10 model as a viable model for study of the long-term effects of SARS-CoV-2 in humans. Establishing the viability of this model is a key step towards the rapid development of novel therapeutic strategies to ameliorate neuroinflammation and restore brain function in those suffering from the persistent cognitive dysfunction of "Long-COVID".
Keywords	covid19
Language	English
Publishing date	2023-03-20
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2023.03.18.533204
Database	COVID19

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Article ; Online: Critical ACE2 Determinants of SARS-CoV-2 and Group 2B Coronavirus Infection and Replication.

Adams, Lily E / Dinnon, Kenneth H / Hou, Yixuan J / Sheahan, Timothy P / Heise, Mark T / Baric, Ralph S

mBio

2021 Volume 12, Issue 2

Abstract: The angiotensin-converting enzyme 2 (ACE2) receptor is a major severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) host range determinant, and understanding SARS-CoV-2-ACE2 interactions will provide important insights into COVID-19 pathogenesis ... ...

Abstract	The angiotensin-converting enzyme 2 (ACE2) receptor is a major severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) host range determinant, and understanding SARS-CoV-2-ACE2 interactions will provide important insights into COVID-19 pathogenesis and animal model development. SARS-CoV-2 cannot infect mice due to incompatibility between its receptor binding domain and the murine ACE2 receptor. Through molecular modeling and empirical
MeSH term(s)	Amino Acid Sequence ; Angiotensin-Converting Enzyme 2/chemistry ; Angiotensin-Converting Enzyme 2/genetics ; Angiotensin-Converting Enzyme 2/metabolism ; Animals ; Betacoronavirus/metabolism ; Betacoronavirus/physiology ; Binding Sites ; COVID-19/virology ; Cell Line ; Coronavirus Infections/virology ; Host Specificity ; Humans ; Mice ; Models, Molecular ; Mutation ; Protein Binding ; Recombinant Proteins/chemistry ; Recombinant Proteins/genetics ; Recombinant Proteins/metabolism ; SARS-CoV-2/metabolism ; SARS-CoV-2/physiology ; Spike Glycoprotein, Coronavirus/chemistry ; Spike Glycoprotein, Coronavirus/metabolism ; Virus Replication
Chemical Substances	Recombinant Proteins ; Spike Glycoprotein, Coronavirus ; Angiotensin-Converting Enzyme 2 (EC 3.4.17.23)
Language	English
Publishing date	2021-03-16
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mBio.03149-20
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Host Genetic Variation Impacts SARS-CoV-2 Vaccination Response in the Diversity Outbred Mouse Population.

Vaccines

2024 Volume 12, Issue 1

Abstract: The COVID-19 pandemic led to the rapid and worldwide development of highly effective vaccines against SARS-CoV-2. However, there is significant individual-to-individual variation in vaccine efficacy due to factors including viral variants, host age, ... ...

Abstract	The COVID-19 pandemic led to the rapid and worldwide development of highly effective vaccines against SARS-CoV-2. However, there is significant individual-to-individual variation in vaccine efficacy due to factors including viral variants, host age, immune status, environmental and host genetic factors. Understanding those determinants driving this variation may inform the development of more broadly protective vaccine strategies. While host genetic factors are known to impact vaccine efficacy for respiratory pathogens such as influenza and tuberculosis, the impact of host genetic variation on vaccine efficacy against COVID-19 is not well understood. To model the impact of host genetic variation on SARS-CoV-2 vaccine efficacy, while controlling for the impact of non-genetic factors, we used the Diversity Outbred (DO) mouse model. We found that DO mice immunized against SARS-CoV-2 exhibited high levels of variation in vaccine-induced neutralizing antibody responses. While the majority of the vaccinated mice were protected from virus-induced disease, similar to human populations, we observed vaccine breakthrough in a subset of mice. Importantly, we found that this variation in neutralizing antibody, virus-induced disease, and viral titer is heritable, indicating that the DO serves as a useful model system for studying the contribution of genetic variation of both vaccines and disease outcomes.
Language	English
Publishing date	2024-01-20
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2703319-3
ISSN	2076-393X
ISSN	2076-393X
DOI	10.3390/vaccines12010103
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Article ; Online: Mouse Adapted SARS-CoV-2 (MA10) Viral Infection Induces Neuroinflammation in Standard Laboratory Mice.

Amruta, Narayanappa / Ismael, Saifudeen / Leist, Sarah R / Gressett, Timothy E / Srivastava, Akhilesh / Dinnon, Kenneth H / Engler-Chiurazzi, Elizabeth B / Maness, Nicholas J / Qin, Xuebin / Kolls, Jay K / Baric, Ralph S / Bix, Gregory

Viruses

2022 Volume 15, Issue 1

Abstract: Increasing evidence suggests that severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection impacts neurological function both acutely and chronically, even in the absence of pronounced respiratory distress. Developing clinically relevant ... ...

Abstract	Increasing evidence suggests that severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection impacts neurological function both acutely and chronically, even in the absence of pronounced respiratory distress. Developing clinically relevant laboratory mouse models of the neuropathogenesis of SARS-CoV-2 infection is an important step toward elucidating the underlying mechanisms of SARS-CoV-2-induced neurological dysfunction. Although various transgenic models and viral delivery methods have been used to study the infection potential of SARS-CoV-2 in mice, the use of commonly available laboratory mice would facilitate the study of SARS-CoV-2 neuropathology. Herein we show neuroinflammatory profiles of immunologically intact mice, C57BL/6J and BALB/c, as well as immunodeficient (
MeSH term(s)	Mice ; Male ; Female ; Animals ; SARS-CoV-2 ; COVID-19/pathology ; Lung ; Neuroinflammatory Diseases ; Mice, Inbred C57BL ; Disease Models, Animal ; Mice, Transgenic
Language	English
Publishing date	2022-12-30
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; 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/v15010114
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Article ; Online: Dual regulation of decorin by androgen and Hedgehog signaling during prostate morphogenesis.

Montano, Monica / Dinnon, Kenneth H / Jacobs, Logan / Xiang, William / Iozzo, Renato V / Bushman, Wade

Developmental dynamics : an official publication of the American Association of Anatomists

2018 Volume 247, Issue 5, Page(s) 679–685

Abstract: Background: Prostate ductal branching morphogenesis involves a complex spatiotemporal regulation of cellular proliferation and remodeling of the extracellular matrix (ECM) around the developing ducts. Decorin (Dcn) is a small leucine-rich proteoglycan ... ...

Abstract	Background: Prostate ductal branching morphogenesis involves a complex spatiotemporal regulation of cellular proliferation and remodeling of the extracellular matrix (ECM) around the developing ducts. Decorin (Dcn) is a small leucine-rich proteoglycan known to sequester several growth factors and to act as a tumor suppressor in prostate cancer. Results: Dcn expression in the developing prostate paralleled branching morphogenesis and was dynamically regulated by androgen and Hedgehog (Hh) signaling. DCN colocalized with collagen in the periductal stroma and acellular interstitium. Exogenous DCN decreased epithelial proliferation in ex vivo organ cultures of developing prostate, whereas genetic ablation of Dcn resulted in increased epithelial proliferation in the developing prostate. Conclusions: Dcn expression and localization in the developing prostate is consistent with a primary role in organizing collagen around the developing ducts. Regulation of Dcn expression appears to be complex, involving both androgen and Hh signaling. The growth inhibitory effect of Dcn suggests a unique linkage between a structural proteoglycan and epithelial growth regulation. This may serve to coordinate two elements of the morphogenetic process: ductal growth and organization of the collagen matrix around the nascent duct. Developmental Dynamics 247:679-685, 2018. © 2018 Wiley Periodicals, Inc.
MeSH term(s)	Animals ; Decorin/genetics ; Decorin/metabolism ; Female ; Male ; Mice ; Morphogenesis/physiology ; Organ Culture Techniques ; Organogenesis/physiology ; Prostate/embryology ; Prostate/growth & development ; Prostate/metabolism ; Signal Transduction/physiology
Chemical Substances	Decorin
Language	English
Publishing date	2018-02-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	1102541-4
ISSN	1097-0177 ; 1058-8388
ISSN (online)	1097-0177
ISSN	1058-8388
DOI	10.1002/dvdy.24619
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Article: A C57BL/6 Mouse model of SARS-CoV-2 infection recapitulates age- and sex-based differences in human COVID-19 disease and recovery.

Davis, Michael / Voss, Kathleen / Turnbull, J Bryan / Gustin, Andrew T / Knoll, Megan / Muruato, Antonio / Hsiang, Tien-Ying / Dinnon, Kenneth H / Leist, Sarah R / Nickel, Katie / Baric, Ralph S / Ladiges, Warren / Akilesh, Shreeram / Smith, Kelly D / Gale, Michael

Research square

2022

Abstract: We present a comprehensive analysis of SARS-CoV-2 infection and recovery in wild type C57BL/6 mice, demonstrating that this is an ideal model of infection and recovery that accurately phenocopies acute human disease arising from the ancestral SARS-CoV-2. ...

Abstract	We present a comprehensive analysis of SARS-CoV-2 infection and recovery in wild type C57BL/6 mice, demonstrating that this is an ideal model of infection and recovery that accurately phenocopies acute human disease arising from the ancestral SARS-CoV-2. Disease severity and infection kinetics are age- and sex-dependent, as has been reported for humans, with older mice and males in particular exhibiting decreased viral clearance and increased mortality. We identified key parallels with human pathology, including intense virus positivity in bronchial epithelial cells, wide-spread alveolar involvement, recruitment of immune cells to the infected lungs, and acute bronchial epithelial cell death. Moreover, older animals experienced increased virus persistence, delayed dispersal of immune cells into lung parenchyma, and morphologic evidence of tissue damage and inflammation. Parallel analysis of SCID mice revealed that the adaptive immune response was not required for recovery from COVID disease symptoms nor early phase clearance of virus but was required for efficient clearance of virus at later stages of infection. Finally, transcriptional analyses indicated that induction and duration of key innate immune gene programs may explain differences in age-dependent disease severity. Importantly, these data demonstrate that SARS-CoV-2-mediated disease in C57BL/6 mice accurately phenocopies human disease across ages and establishes a platform for future therapeutic and genetic screens for not just SARS-CoV-2 but also novel coronaviruses that have yet to emerge.
Language	English
Publishing date	2022-11-14
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-2194450/v1
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Article ; Online: Investigation of the Host Kinome Response to Coronavirus Infection Reveals PI3K/mTOR Inhibitors as Betacoronavirus Antivirals.

Fritch, Ethan J / Mordant, Angie L / Gilbert, Thomas S K / Wells, Carrow I / Yang, Xuan / Barker, Natalie K / Madden, Emily A / Dinnon, Kenneth H / Hou, Yixuan J / Tse, Longping V / Castillo, Izabella N / Sims, Amy C / Moorman, Nathaniel J / Lakshmanane, Premkumar / Willson, Timothy M / Herring, Laura E / Graves, Lee M / Baric, Ralph S

Journal of proteome research

2023 Volume 22, Issue 10, Page(s) 3159–3177

Abstract: Host kinases play essential roles in the host cell cycle, innate immune signaling, the stress response to viral infection, and inflammation. Previous work has demonstrated that coronaviruses specifically target kinase cascades to subvert host cell ... ...

Abstract	Host kinases play essential roles in the host cell cycle, innate immune signaling, the stress response to viral infection, and inflammation. Previous work has demonstrated that coronaviruses specifically target kinase cascades to subvert host cell responses to infection and rely upon host kinase activity to phosphorylate viral proteins to enhance replication. Given the number of kinase inhibitors that are already FDA approved to treat cancers, fibrosis, and other human disease, they represent an attractive class of compounds to repurpose for host-targeted therapies against emerging coronavirus infections. To further understand the host kinome response to betacoronavirus infection, we employed multiplex inhibitory bead mass spectrometry (MIB-MS) following MERS-CoV and SARS-CoV-2 infection of human lung epithelial cell lines. Our MIB-MS analyses revealed activation of mTOR and MAPK signaling following MERS-CoV and SARS-CoV-2 infection, respectively. SARS-CoV-2 host kinome responses were further characterized using paired phosphoproteomics, which identified activation of MAPK, PI3K, and mTOR signaling. Through chemogenomic screening, we found that clinically relevant PI3K/mTOR inhibitors were able to inhibit coronavirus replication at nanomolar concentrations similar to direct-acting antivirals. This study lays the groundwork for identifying broad-acting, host-targeted therapies to reduce betacoronavirus replication that can be rapidly repurposed during future outbreaks and epidemics. The proteomics, phosphoproteomics, and MIB-MS datasets generated in this study are available in the Proteomics Identification Database (PRIDE) repository under project identifiers PXD040897 and PXD040901.
MeSH term(s)	Humans ; Antiviral Agents/pharmacology ; COVID-19 ; MTOR Inhibitors ; Phosphatidylinositol 3-Kinases ; SARS-CoV-2 ; Virus Replication ; Hepatitis C, Chronic ; Middle East Respiratory Syndrome Coronavirus/physiology ; TOR Serine-Threonine Kinases
Chemical Substances	Antiviral Agents ; MTOR Inhibitors ; Phosphatidylinositol 3-Kinases (EC 2.7.1.-) ; TOR Serine-Threonine Kinases (EC 2.7.11.1)
Language	English
Publishing date	2023-08-27
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2078618-9
ISSN	1535-3907 ; 1535-3893
ISSN (online)	1535-3907
ISSN	1535-3893
DOI	10.1021/acs.jproteome.3c00182
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Article ; Online: Adjuvant-dependent impact of inactivated SARS-CoV-2 vaccines during heterologous infection by a SARS-related coronavirus.

Dillard, Jacob A / Taft-Benz, Sharon A / Knight, Audrey C / Anderson, Elizabeth J / Pressey, Katia D / Parotti, Breantié / Martinez, Sabian A / Diaz, Jennifer L / Sarkar, Sanjay / Madden, Emily A / De la Cruz, Gabriela / Adams, Lily E / Dinnon, Kenneth H / Leist, Sarah R / Martinez, David R / Schäfer, Alexandra / Powers, John M / Yount, Boyd L / Castillo, Izabella N /

Morales, Noah L / Burdick, Jane / Evangelista, Mia Katrina D / Ralph, Lauren M / Pankow, Nicholas C / Linnertz, Colton L / Lakshmanane, Premkumar / Montgomery, Stephanie A / Ferris, Martin T / Baric, Ralph S / Baxter, Victoria K / Heise, Mark T

Nature communications

2024 Volume 15, Issue 1, Page(s) 3738

Abstract: Whole virus-based inactivated SARS-CoV-2 vaccines adjuvanted with aluminum hydroxide have been critical to the COVID-19 pandemic response. Although these vaccines are protective against homologous coronavirus infection, the emergence of novel variants ... ...

Abstract	Whole virus-based inactivated SARS-CoV-2 vaccines adjuvanted with aluminum hydroxide have been critical to the COVID-19 pandemic response. Although these vaccines are protective against homologous coronavirus infection, the emergence of novel variants and the presence of large zoonotic reservoirs harboring novel heterologous coronaviruses provide significant opportunities for vaccine breakthrough, which raises the risk of adverse outcomes like vaccine-associated enhanced respiratory disease. Here, we use a female mouse model of coronavirus disease to evaluate inactivated vaccine performance against either homologous challenge with SARS-CoV-2 or heterologous challenge with a bat-derived coronavirus that represents a potential emerging disease threat. We show that inactivated SARS-CoV-2 vaccines adjuvanted with aluminum hydroxide can cause enhanced respiratory disease during heterologous infection, while use of an alternative adjuvant does not drive disease and promotes heterologous viral clearance. In this work, we highlight the impact of adjuvant selection on inactivated vaccine safety and efficacy against heterologous coronavirus infection.
MeSH term(s)	Animals ; COVID-19 Vaccines/immunology ; COVID-19 Vaccines/administration & dosage ; Female ; COVID-19/prevention & control ; COVID-19/immunology ; COVID-19/virology ; Mice ; Vaccines, Inactivated/immunology ; SARS-CoV-2/immunology ; Aluminum Hydroxide/administration & dosage ; Disease Models, Animal ; Adjuvants, Immunologic/administration & dosage ; Adjuvants, Vaccine ; Antibodies, Viral/immunology ; Mice, Inbred BALB C ; Humans ; Severe acute respiratory syndrome-related coronavirus/immunology
Chemical Substances	COVID-19 Vaccines ; Vaccines, Inactivated ; Aluminum Hydroxide (5QB0T2IUN0) ; Adjuvants, Immunologic ; SARS-CoV-2 inactivated vaccines ; Adjuvants, Vaccine ; Antibodies, Viral
Language	English
Publishing date	2024-05-03
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-024-47450-x
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Article: Newcastle disease virus (NDV) expressing the spike protein of SARS-CoV-2 as vaccine candidate.

Sun, Weina / Leist, Sarah R / McCroskery, Stephen / Liu, Yonghong / Slamanig, Stefan / Oliva, Justine / Amanat, Fatima / Schäfer, Alexandra / Dinnon, Kenneth H / García-Sastre, Adolfo / Krammer, Florian / Baric, Ralph S / Palese, Peter

bioRxiv : the preprint server for biology

2020

Abstract: Due to the lack of protective immunity of humans towards the newly emerged SARS-CoV-2, this virus has caused a massive pandemic across the world resulting in hundreds of thousands of deaths. Thus, a vaccine is urgently needed to contain the spread of the ...

Abstract	Due to the lack of protective immunity of humans towards the newly emerged SARS-CoV-2, this virus has caused a massive pandemic across the world resulting in hundreds of thousands of deaths. Thus, a vaccine is urgently needed to contain the spread of the virus. Here, we describe Newcastle disease virus (NDV) vector vaccines expressing the spike protein of SARS-CoV-2 in its wild type or a pre-fusion membrane anchored format. All described NDV vector vaccines grow to high titers in embryonated chicken eggs. In a proof of principle mouse study, we report that the NDV vector vaccines elicit high levels of antibodies that are neutralizing when the vaccine is given intramuscularly. Importantly, these COVID-19 vaccine candidates protect mice from a mouse-adapted SARS-CoV-2 challenge with no detectable viral titer and viral antigen in the lungs. Research in context: Evidence before this study:
Keywords	covid19
Language	English
Publishing date	2020-07-28
Publishing country	United States
Document type	Preprint
DOI	10.1101/2020.07.26.221861
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