Differences in Susceptibility to SARS-CoV-2 Infection Among Transgenic hACE2-Hamster Founder Lines
Animal models that are susceptible to SARS-CoV-2 infection and develop clinical signs like human COVID-19 are desired to understand viral pathogenesis and develop effective medical countermeasures. The golden Syrian hamster is important for the study of SARS-CoV-2 since hamsters are naturally suscep...
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| Published in | Viruses Vol. 16; no. 10; p. 1625 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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MDPI AG
01.10.2024
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| Abstract | Animal models that are susceptible to SARS-CoV-2 infection and develop clinical signs like human COVID-19 are desired to understand viral pathogenesis and develop effective medical countermeasures. The golden Syrian hamster is important for the study of SARS-CoV-2 since hamsters are naturally susceptible to SARS-CoV-2. However, infected hamsters show only limited clinical disease and resolve infection quickly. In this study, we describe development of human angiotensin-converting enzyme 2 (hACE2) transgenic hamsters as a model for COVID-19. During development of the model for SARS-CoV-2, we observed that different hACE2 transgenic hamster founder lines varied in their susceptibility to SARS-CoV-2 lethal infection. The highly susceptible hACE2 founder lines F0F35 and F0M41 rapidly progress to severe infection and death within 6 days post-infection (p.i.). Clinical signs included lethargy, weight loss, dyspnea, and mortality. Lethality was observed in a viral dose-dependent manner with a lethal dose as low as 1 × 100.15 CCID50. In addition, virus shedding from highly susceptible lines was detected in oropharyngeal swabs on days 2–5 p.i., and virus titers were observed at 105.5−6.5 CCID50 in lung and brain tissue by day 4 p.i.. Histopathology revealed that infected hACE2-hamsters developed rhinitis, tracheitis, bronchointerstitial pneumonia, and encephalitis. Mortality in highly susceptible hACE2-hamsters can be attributed to neurologic disease with contributions from the accompanying respiratory disease. In contrast, virus challenge of animals from less susceptible founder lines, F0M44 and F0M51, resulted in only 0–20% mortality. To demonstrate utility of this SARS-CoV-2 infection model, we determined the protective effect of the TLR3 agonist polyinosinic-polycytidylic acid (Poly (I:C)). Prophylactic treatment with Poly (I:C) significantly improved survival in highly susceptible hACE2-hamsters. In summary, our studies demonstrate that hACE2 transgenic hamsters differ in their susceptibility to SARS-CoV-2 infection, based on the transgenic hamster founder line, and that prophylactic treatment with Poly (I:C) was protective in this COVID-19 model of highly susceptible hACE2-hamsters. |
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| AbstractList | Animal models that are susceptible to SARS-CoV-2 infection and develop clinical signs like human COVID-19 are desired to understand viral pathogenesis and develop effective medical countermeasures. The golden Syrian hamster is important for the study of SARS-CoV-2 since hamsters are naturally susceptible to SARS-CoV-2. However, infected hamsters show only limited clinical disease and resolve infection quickly. In this study, we describe development of human angiotensin-converting enzyme 2 (hACE2) transgenic hamsters as a model for COVID-19. During development of the model for SARS-CoV-2, we observed that different hACE2 transgenic hamster founder lines varied in their susceptibility to SARS-CoV-2 lethal infection. The highly susceptible hACE2 founder lines F0F35 and F0M41 rapidly progress to severe infection and death within 6 days post-infection (p.i.). Clinical signs included lethargy, weight loss, dyspnea, and mortality. Lethality was observed in a viral dose-dependent manner with a lethal dose as low as 1 × 10
CCID
. In addition, virus shedding from highly susceptible lines was detected in oropharyngeal swabs on days 2-5 p.i., and virus titers were observed at 10
CCID
in lung and brain tissue by day 4 p.i.. Histopathology revealed that infected hACE2-hamsters developed rhinitis, tracheitis, bronchointerstitial pneumonia, and encephalitis. Mortality in highly susceptible hACE2-hamsters can be attributed to neurologic disease with contributions from the accompanying respiratory disease. In contrast, virus challenge of animals from less susceptible founder lines, F0M44 and F0M51, resulted in only 0-20% mortality. To demonstrate utility of this SARS-CoV-2 infection model, we determined the protective effect of the TLR3 agonist polyinosinic-polycytidylic acid (Poly (I:C)). Prophylactic treatment with Poly (I:C) significantly improved survival in highly susceptible hACE2-hamsters. In summary, our studies demonstrate that hACE2 transgenic hamsters differ in their susceptibility to SARS-CoV-2 infection, based on the transgenic hamster founder line, and that prophylactic treatment with Poly (I:C) was protective in this COVID-19 model of highly susceptible hACE2-hamsters. Animal models that are susceptible to SARS-CoV-2 infection and develop clinical signs like human COVID-19 are desired to understand viral pathogenesis and develop effective medical countermeasures. The golden Syrian hamster is important for the study of SARS-CoV-2 since hamsters are naturally susceptible to SARS-CoV-2. However, infected hamsters show only limited clinical disease and resolve infection quickly. In this study, we describe development of human angiotensin-converting enzyme 2 (hACE2) transgenic hamsters as a model for COVID-19. During development of the model for SARS-CoV-2, we observed that different hACE2 transgenic hamster founder lines varied in their susceptibility to SARS-CoV-2 lethal infection. The highly susceptible hACE2 founder lines F0F35 and F0M41 rapidly progress to severe infection and death within 6 days post-infection (p.i.). Clinical signs included lethargy, weight loss, dyspnea, and mortality. Lethality was observed in a viral dose-dependent manner with a lethal dose as low as 1 × 10[sup.0.15] CCID[sub.50] . In addition, virus shedding from highly susceptible lines was detected in oropharyngeal swabs on days 2–5 p.i., and virus titers were observed at 10[sup.5.5−6.5] CCID[sub.50] in lung and brain tissue by day 4 p.i.. Histopathology revealed that infected hACE2-hamsters developed rhinitis, tracheitis, bronchointerstitial pneumonia, and encephalitis. Mortality in highly susceptible hACE2-hamsters can be attributed to neurologic disease with contributions from the accompanying respiratory disease. In contrast, virus challenge of animals from less susceptible founder lines, F0M44 and F0M51, resulted in only 0–20% mortality. To demonstrate utility of this SARS-CoV-2 infection model, we determined the protective effect of the TLR3 agonist polyinosinic-polycytidylic acid (Poly (I:C)). Prophylactic treatment with Poly (I:C) significantly improved survival in highly susceptible hACE2-hamsters. In summary, our studies demonstrate that hACE2 transgenic hamsters differ in their susceptibility to SARS-CoV-2 infection, based on the transgenic hamster founder line, and that prophylactic treatment with Poly (I:C) was protective in this COVID-19 model of highly susceptible hACE2-hamsters. Animal models that are susceptible to SARS-CoV-2 infection and develop clinical signs like human COVID-19 are desired to understand viral pathogenesis and develop effective medical countermeasures. The golden Syrian hamster is important for the study of SARS-CoV-2 since hamsters are naturally susceptible to SARS-CoV-2. However, infected hamsters show only limited clinical disease and resolve infection quickly. In this study, we describe development of human angiotensin-converting enzyme 2 (hACE2) transgenic hamsters as a model for COVID-19. During development of the model for SARS-CoV-2, we observed that different hACE2 transgenic hamster founder lines varied in their susceptibility to SARS-CoV-2 lethal infection. The highly susceptible hACE2 founder lines F0F35 and F0M41 rapidly progress to severe infection and death within 6 days post-infection (p.i.). Clinical signs included lethargy, weight loss, dyspnea, and mortality. Lethality was observed in a viral dose-dependent manner with a lethal dose as low as 1 × 100.15 CCID50. In addition, virus shedding from highly susceptible lines was detected in oropharyngeal swabs on days 2–5 p.i., and virus titers were observed at 105.5−6.5 CCID50 in lung and brain tissue by day 4 p.i.. Histopathology revealed that infected hACE2-hamsters developed rhinitis, tracheitis, bronchointerstitial pneumonia, and encephalitis. Mortality in highly susceptible hACE2-hamsters can be attributed to neurologic disease with contributions from the accompanying respiratory disease. In contrast, virus challenge of animals from less susceptible founder lines, F0M44 and F0M51, resulted in only 0–20% mortality. To demonstrate utility of this SARS-CoV-2 infection model, we determined the protective effect of the TLR3 agonist polyinosinic-polycytidylic acid (Poly (I:C)). Prophylactic treatment with Poly (I:C) significantly improved survival in highly susceptible hACE2-hamsters. In summary, our studies demonstrate that hACE2 transgenic hamsters differ in their susceptibility to SARS-CoV-2 infection, based on the transgenic hamster founder line, and that prophylactic treatment with Poly (I:C) was protective in this COVID-19 model of highly susceptible hACE2-hamsters. Animal models that are susceptible to SARS-CoV-2 infection and develop clinical signs like human COVID-19 are desired to understand viral pathogenesis and develop effective medical countermeasures. The golden Syrian hamster is important for the study of SARS-CoV-2 since hamsters are naturally susceptible to SARS-CoV-2. However, infected hamsters show only limited clinical disease and resolve infection quickly. In this study, we describe development of human angiotensin-converting enzyme 2 (hACE2) transgenic hamsters as a model for COVID-19. During development of the model for SARS-CoV-2, we observed that different hACE2 transgenic hamster founder lines varied in their susceptibility to SARS-CoV-2 lethal infection. The highly susceptible hACE2 founder lines F0F35 and F0M41 rapidly progress to severe infection and death within 6 days post-infection (p.i.). Clinical signs included lethargy, weight loss, dyspnea, and mortality. Lethality was observed in a viral dose-dependent manner with a lethal dose as low as 1 × 10 0.15 CCID 50 . In addition, virus shedding from highly susceptible lines was detected in oropharyngeal swabs on days 2–5 p.i., and virus titers were observed at 10 5.5−6.5 CCID 50 in lung and brain tissue by day 4 p.i.. Histopathology revealed that infected hACE2-hamsters developed rhinitis, tracheitis, bronchointerstitial pneumonia, and encephalitis. Mortality in highly susceptible hACE2-hamsters can be attributed to neurologic disease with contributions from the accompanying respiratory disease. In contrast, virus challenge of animals from less susceptible founder lines, F0M44 and F0M51, resulted in only 0–20% mortality. To demonstrate utility of this SARS-CoV-2 infection model, we determined the protective effect of the TLR3 agonist polyinosinic-polycytidylic acid (Poly (I:C)). Prophylactic treatment with Poly (I:C) significantly improved survival in highly susceptible hACE2-hamsters. In summary, our studies demonstrate that hACE2 transgenic hamsters differ in their susceptibility to SARS-CoV-2 infection, based on the transgenic hamster founder line, and that prophylactic treatment with Poly (I:C) was protective in this COVID-19 model of highly susceptible hACE2-hamsters. Animal models that are susceptible to SARS-CoV-2 infection and develop clinical signs like human COVID-19 are desired to understand viral pathogenesis and develop effective medical countermeasures. The golden Syrian hamster is important for the study of SARS-CoV-2 since hamsters are naturally susceptible to SARS-CoV-2. However, infected hamsters show only limited clinical disease and resolve infection quickly. In this study, we describe development of human angiotensin-converting enzyme 2 (hACE2) transgenic hamsters as a model for COVID-19. During development of the model for SARS-CoV-2, we observed that different hACE2 transgenic hamster founder lines varied in their susceptibility to SARS-CoV-2 lethal infection. The highly susceptible hACE2 founder lines F0F35 and F0M41 rapidly progress to severe infection and death within 6 days post-infection (p.i.). Clinical signs included lethargy, weight loss, dyspnea, and mortality. Lethality was observed in a viral dose-dependent manner with a lethal dose as low as 1 × 100.15 CCID50. In addition, virus shedding from highly susceptible lines was detected in oropharyngeal swabs on days 2-5 p.i., and virus titers were observed at 105.5-6.5 CCID50 in lung and brain tissue by day 4 p.i.. Histopathology revealed that infected hACE2-hamsters developed rhinitis, tracheitis, bronchointerstitial pneumonia, and encephalitis. Mortality in highly susceptible hACE2-hamsters can be attributed to neurologic disease with contributions from the accompanying respiratory disease. In contrast, virus challenge of animals from less susceptible founder lines, F0M44 and F0M51, resulted in only 0-20% mortality. To demonstrate utility of this SARS-CoV-2 infection model, we determined the protective effect of the TLR3 agonist polyinosinic-polycytidylic acid (Poly (I:C)). Prophylactic treatment with Poly (I:C) significantly improved survival in highly susceptible hACE2-hamsters. In summary, our studies demonstrate that hACE2 transgenic hamsters differ in their susceptibility to SARS-CoV-2 infection, based on the transgenic hamster founder line, and that prophylactic treatment with Poly (I:C) was protective in this COVID-19 model of highly susceptible hACE2-hamsters.Animal models that are susceptible to SARS-CoV-2 infection and develop clinical signs like human COVID-19 are desired to understand viral pathogenesis and develop effective medical countermeasures. The golden Syrian hamster is important for the study of SARS-CoV-2 since hamsters are naturally susceptible to SARS-CoV-2. However, infected hamsters show only limited clinical disease and resolve infection quickly. In this study, we describe development of human angiotensin-converting enzyme 2 (hACE2) transgenic hamsters as a model for COVID-19. During development of the model for SARS-CoV-2, we observed that different hACE2 transgenic hamster founder lines varied in their susceptibility to SARS-CoV-2 lethal infection. The highly susceptible hACE2 founder lines F0F35 and F0M41 rapidly progress to severe infection and death within 6 days post-infection (p.i.). Clinical signs included lethargy, weight loss, dyspnea, and mortality. Lethality was observed in a viral dose-dependent manner with a lethal dose as low as 1 × 100.15 CCID50. In addition, virus shedding from highly susceptible lines was detected in oropharyngeal swabs on days 2-5 p.i., and virus titers were observed at 105.5-6.5 CCID50 in lung and brain tissue by day 4 p.i.. Histopathology revealed that infected hACE2-hamsters developed rhinitis, tracheitis, bronchointerstitial pneumonia, and encephalitis. Mortality in highly susceptible hACE2-hamsters can be attributed to neurologic disease with contributions from the accompanying respiratory disease. In contrast, virus challenge of animals from less susceptible founder lines, F0M44 and F0M51, resulted in only 0-20% mortality. To demonstrate utility of this SARS-CoV-2 infection model, we determined the protective effect of the TLR3 agonist polyinosinic-polycytidylic acid (Poly (I:C)). Prophylactic treatment with Poly (I:C) significantly improved survival in highly susceptible hACE2-hamsters. In summary, our studies demonstrate that hACE2 transgenic hamsters differ in their susceptibility to SARS-CoV-2 infection, based on the transgenic hamster founder line, and that prophylactic treatment with Poly (I:C) was protective in this COVID-19 model of highly susceptible hACE2-hamsters. |
| Audience | Academic |
| Author | Li, Rong Siddharthan, Venkatraman Tarbet, E. Bart Larson, Deanna P. Polejaeva, Irina A. Hurst, Brett L. Wang, Zhongde Liu, Yanan Sheesley, Ashley Y. Gibson, Scott A. Morrey, John D. Fan, Zhiqiang Kunzler, Madelyn Moisyadi, Stefan Stewart, Rebekah Van Wettere, Arnaud J |
| AuthorAffiliation | 2 Institute for Antiviral Research, Utah State University, Logan, UT 84322, USA 1 Department of Animal, Diary and Veterinary Sciences, Utah State University, Logan, UT 84322, USA; scott.gibson@usu.edu (S.A.G.); yanan.liu@usu.edu (Y.L.); rong.li@aggiemail.usu.edu (R.L.); brett.hurst@usu.edu (B.L.H.); zhiqiang.fan@aggiemail.usu.edu (Z.F.); venkat.siddharthan@usu.edu (V.S.); dpassarolarson@gmail.com (D.P.L.); ashley.sheesley@usu.edu (A.Y.S.); rebekah.stewart@aggiemail.usu.edu (R.S.); madelyn.kunzler@usu.edu (M.K.); irina.polejaeva@usu.edu (I.A.P.); john.morrey@usu.edu (J.D.M.); zonda.wang@usu.edu (Z.W.) 3 Department of Veterinary, Clinical, and Life Sciences, Utah State University, Logan, UT 84322, USA; arnaud.vanwettere@usu.edu 5 Institute of Biogenesis Research, John A. Burns School of Medicine, University of Hawaii, Honolulu, HI 96822, USA; moisyadi@hawaii.edu 4 Utah Veterinary Diagnostic Laboratory, Utah State University, Logan, UT 84322, USA |
| AuthorAffiliation_xml | – name: 1 Department of Animal, Diary and Veterinary Sciences, Utah State University, Logan, UT 84322, USA; scott.gibson@usu.edu (S.A.G.); yanan.liu@usu.edu (Y.L.); rong.li@aggiemail.usu.edu (R.L.); brett.hurst@usu.edu (B.L.H.); zhiqiang.fan@aggiemail.usu.edu (Z.F.); venkat.siddharthan@usu.edu (V.S.); dpassarolarson@gmail.com (D.P.L.); ashley.sheesley@usu.edu (A.Y.S.); rebekah.stewart@aggiemail.usu.edu (R.S.); madelyn.kunzler@usu.edu (M.K.); irina.polejaeva@usu.edu (I.A.P.); john.morrey@usu.edu (J.D.M.); zonda.wang@usu.edu (Z.W.) – name: 4 Utah Veterinary Diagnostic Laboratory, Utah State University, Logan, UT 84322, USA – name: 5 Institute of Biogenesis Research, John A. Burns School of Medicine, University of Hawaii, Honolulu, HI 96822, USA; moisyadi@hawaii.edu – name: 2 Institute for Antiviral Research, Utah State University, Logan, UT 84322, USA – name: 3 Department of Veterinary, Clinical, and Life Sciences, Utah State University, Logan, UT 84322, USA; arnaud.vanwettere@usu.edu |
| Author_xml | – sequence: 1 givenname: Scott A. surname: Gibson fullname: Gibson, Scott A. – sequence: 2 givenname: Yanan surname: Liu fullname: Liu, Yanan – sequence: 3 givenname: Rong surname: Li fullname: Li, Rong – sequence: 4 givenname: Brett L. orcidid: 0000-0003-1025-5878 surname: Hurst fullname: Hurst, Brett L. – sequence: 5 givenname: Zhiqiang surname: Fan fullname: Fan, Zhiqiang – sequence: 6 givenname: Venkatraman surname: Siddharthan fullname: Siddharthan, Venkatraman – sequence: 7 givenname: Deanna P. surname: Larson fullname: Larson, Deanna P. – sequence: 8 givenname: Ashley Y. surname: Sheesley fullname: Sheesley, Ashley Y. – sequence: 9 givenname: Rebekah surname: Stewart fullname: Stewart, Rebekah – sequence: 10 givenname: Madelyn surname: Kunzler fullname: Kunzler, Madelyn – sequence: 11 givenname: Irina A. orcidid: 0000-0002-0858-5889 surname: Polejaeva fullname: Polejaeva, Irina A. – sequence: 12 givenname: Arnaud J orcidid: 0000-0002-9611-1316 surname: Van Wettere fullname: Van Wettere, Arnaud J – sequence: 13 givenname: Stefan orcidid: 0000-0002-5320-4133 surname: Moisyadi fullname: Moisyadi, Stefan – sequence: 14 givenname: John D. surname: Morrey fullname: Morrey, John D. – sequence: 15 givenname: E. Bart orcidid: 0000-0002-4255-9094 surname: Tarbet fullname: Tarbet, E. Bart – sequence: 16 givenname: Zhongde orcidid: 0000-0003-2441-4729 surname: Wang fullname: Wang, Zhongde |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39459957$$D View this record in MEDLINE/PubMed |
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| Keywords | viral pathogenesis SARS-CoV-2 transgenic hamster animal model |
| Language | English |
| License | https://creativecommons.org/licenses/by/4.0 Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). |
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| PublicationTitle | Viruses |
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| SubjectTerms | ACE2 Angiotensin Angiotensin-converting enzyme 2 Angiotensin-Converting Enzyme 2 - genetics Angiotensin-Converting Enzyme 2 - metabolism animal model Animal models Animals Animals, Genetically Modified Comparative analysis COVID-19 COVID-19 - pathology COVID-19 - veterinary COVID-19 - virology Cricetinae Disease Models, Animal Disease Susceptibility Disease transmission Dyspnea Embryos Encephalitis Enzymes Females Histopathology Humans Infections Lethal dose Lethality Lung - pathology Lung - virology Male Males Mesocricetus Mortality Neurological diseases Peptidyl-dipeptidase A Polyinosinic:polycytidylic acid Respiratory diseases Rhinitis SARS-CoV-2 SARS-CoV-2 - genetics SARS-CoV-2 - pathogenicity Severe acute respiratory syndrome coronavirus 2 TLR3 protein Toll-like receptors Tracheitis Transgenic animals transgenic hamster Viral infections viral pathogenesis Viruses |
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| Title | Differences in Susceptibility to SARS-CoV-2 Infection Among Transgenic hACE2-Hamster Founder Lines |
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