Attenuated activation of pulmonary immune cells in mRNA-1273–vaccinated hamsters after SARS-CoV-2 infection
The mRNA-1273 vaccine is effective against SARS-CoV-2 and was granted emergency use authorization by the FDA. Clinical studies, however, cannot provide the controlled response to infection and complex immunological insight that are only possible with preclinical studies. Hamsters are the only model...
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| Published in | The Journal of clinical investigation Vol. 131; no. 20; pp. 1 - 16 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Society for Clinical Investigation
15.10.2021
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| Subjects | |
| Online Access | Get full text |
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| Abstract | The mRNA-1273 vaccine is effective against SARS-CoV-2 and was granted emergency use authorization by the FDA. Clinical studies, however, cannot provide the controlled response to infection and complex immunological insight that are only possible with preclinical studies. Hamsters are the only model that reliably exhibits severe SARS-CoV-2 disease similar to that in hospitalized patients, making them pertinent for vaccine evaluation. We demonstrate that prime or prime-boost administration of mRNA-1273 in hamsters elicited robust neutralizing antibodies, ameliorated weight loss, suppressed SARS-CoV-2 replication in the airways, and better protected against disease at the highest prime-boost dose. Unlike in mice and nonhuman primates, low-level virus replication in mRNA-1273-vaccinated hamsters coincided with an anamnestic response. Single-cell RNA sequencing of lung tissue permitted high-resolution analysis that is not possible in vaccinated humans. mRNA-1273 prevented inflammatory cell infiltration and the reduction of lymphocyte proportions, but enabled antiviral responses conducive to lung homeostasis. Surprisingly, infection triggered transcriptome programs in some types of immune cells from vaccinated hamsters that were shared, albeit attenuated, with mock-vaccinated hamsters. Our results support the use of mRNA-1273 in a 2-dose schedule and provide insight into the potential responses within the lungs of vaccinated humans who are exposed to SARS-CoV-2. |
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| AbstractList | The mRNA-1273 vaccine is effective against SARS-CoV-2 and was granted emergency use authorization by the FDA. Clinical studies, however, cannot provide the controlled response to infection and complex immunological insight that are only possible with preclinical studies. Hamsters are the only model that reliably exhibits severe SARS-CoV-2 disease similar to that in hospitalized patients, making them pertinent for vaccine evaluation. We demonstrate that prime or prime-boost administration of mRNA-1273 in hamsters elicited robust neutralizing antibodies, ameliorated weight loss, suppressed SARS-CoV-2 replication in the airways, and better protected against disease at the highest prime-boost dose. Unlike in mice and nonhuman primates, low-level virus replication in mRNA-1273–vaccinated hamsters coincided with an anamnestic response. Single-cell RNA sequencing of lung tissue permitted high-resolution analysis that is not possible in vaccinated humans. mRNA-1273 prevented inflammatory cell infiltration and the reduction of lymphocyte proportions, but enabled antiviral responses conducive to lung homeostasis. Surprisingly, infection triggered transcriptome programs in some types of immune cells from vaccinated hamsters that were shared, albeit attenuated, with mock-vaccinated hamsters. Our results support the use of mRNA-1273 in a 2-dose schedule and provide insight into the potential responses within the lungs of vaccinated humans who are exposed to SARS-CoV-2. The mRNA-1273 vaccine is effective against SARS-CoV-2 and was granted emergency use authorization by the FDA. Clinical studies, however, cannot provide the controlled response to infection and complex immunological insight that are only possible with preclinical studies. Hamsters are the only model that reliably exhibits severe SARS-CoV-2 disease similar to that in hospitalized patients, making them pertinent for vaccine evaluation. We demonstrate that prime or prime-boost administration of mRNA-1273 in hamsters elicited robust neutralizing antibodies, ameliorated weight loss, suppressed SARS-CoV-2 replication in the airways, and better protected against disease at the highest prime-boost dose. Unlike in mice and nonhuman primates, low-level virus replication in mRNA-1273-vaccinated hamsters coincided with an anamnestic response. Single-cell RNA sequencing of lung tissue permitted high-resolution analysis that is not possible in vaccinated humans. mRNA-1273 prevented inflammatory cell infiltration and the reduction of lymphocyte proportions, but enabled antiviral responses conducive to lung homeostasis. Surprisingly, infection triggered transcriptome programs in some types of immune cells from vaccinated hamsters that were shared, albeit attenuated, with mock-vaccinated hamsters. Our results support the use of mRNA-1273 in a 2-dose schedule and provide insight into the potential responses within the lungs of vaccinated humans who are exposed to SARS-CoV-2.The mRNA-1273 vaccine is effective against SARS-CoV-2 and was granted emergency use authorization by the FDA. Clinical studies, however, cannot provide the controlled response to infection and complex immunological insight that are only possible with preclinical studies. Hamsters are the only model that reliably exhibits severe SARS-CoV-2 disease similar to that in hospitalized patients, making them pertinent for vaccine evaluation. We demonstrate that prime or prime-boost administration of mRNA-1273 in hamsters elicited robust neutralizing antibodies, ameliorated weight loss, suppressed SARS-CoV-2 replication in the airways, and better protected against disease at the highest prime-boost dose. Unlike in mice and nonhuman primates, low-level virus replication in mRNA-1273-vaccinated hamsters coincided with an anamnestic response. Single-cell RNA sequencing of lung tissue permitted high-resolution analysis that is not possible in vaccinated humans. mRNA-1273 prevented inflammatory cell infiltration and the reduction of lymphocyte proportions, but enabled antiviral responses conducive to lung homeostasis. Surprisingly, infection triggered transcriptome programs in some types of immune cells from vaccinated hamsters that were shared, albeit attenuated, with mock-vaccinated hamsters. Our results support the use of mRNA-1273 in a 2-dose schedule and provide insight into the potential responses within the lungs of vaccinated humans who are exposed to SARS-CoV-2. The mRNA-1273 vaccine is effective against SARS-CoV-2 and was granted emergency use authorization by the FDA. Clinical studies, however, cannot provide the controlled response to infection and complex immunological insight that are only possible with preclinical studies. Hamsters are the only model that reliably exhibits severe SARS-CoV-2 disease similar to that in hospitalized patients, making them pertinent for vaccine evaluation. We demonstrate that prime or prime-boost administration of mRNA-1273 in hamsters elicited robust neutralizing antibodies, ameliorated weight loss, suppressed SARSCoV-2 replication in the airways, and better protected against disease at the highest prime-boost dose. Unlike in mice and nonhuman primates, low-level virus replication in mRNA-1273-vaccinated hamsters coincided with an anamnestic response. Single-cell RNA sequencing of lung tissue permitted high-resolution analysis that is not possible in vaccinated humans. mRNA-1273 prevented inflammatory cell infiltration and the reduction of lymphocyte proportions, but enabled antiviral responses conducive to lung homeostasis. Surprisingly, infection triggered transcriptome programs in some types of immune cells from vaccinated hamsters that were shared, albeit attenuated, with mock-vaccinated hamsters. Our results support the use of mRNA-1273 in a 2-dose schedule and provide insight into the potential responses within the lungs of vaccinated humans who are exposed to SARS-CoV-2. |
| Audience | Academic |
| Author | Mire, Chad E. Chen, Xi Periasamy, Sivakumar Bock, Kevin W. Wang, Yuan Troyanskaya, Olga G. Carfi, Andrea Woods, Angela Zaslavsky, Elena Rubenstein, Aliza B. Pietzsch, Colette Ramos, Irene Shi, Pei-Yong Ma, LingZhi Graham, Barney S. Minai, Mahnaz Sealfon, Stuart C. Ramanathan, Palaniappan Meyer, Michelle Ge, Yongchao Cheng, Wan Sze Edwards, Darin Smith, Gregory R. Nagata, Bianca M. Bukreyev, Alexander Henry, Carole Stewart-Jones, Guillaume B.E. Moore, Ian N. |
| AuthorAffiliation | 3 Department of Computer Science and 5 Moderna Inc., Cambridge, Massachusetts, USA 4 Lewis-Sigler Institute of Integrative Genomics, Princeton University, Princeton, New Jersey, USA 10 Department of Biochemistry and Molecular Biology, University of Texas Medical Branch, Galveston, Texas, USA 1 Department of Pathology, University of Texas Medical Branch, Galveston, Texas, USA 6 Department of Neurology, Icahn School of Medicine at Mount Sinai, New York, New York, USA 2 Galveston National Laboratory, Galveston, Texas, USA 7 Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USA 9 Infectious Disease Pathogenesis Section, Comparative Medicine Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland, USA 11 Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA 8 Center for Computational Biology, Flatiron Institute, Simon |
| AuthorAffiliation_xml | – name: 11 Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, USA – name: 2 Galveston National Laboratory, Galveston, Texas, USA – name: 6 Department of Neurology, Icahn School of Medicine at Mount Sinai, New York, New York, USA – name: 7 Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USA – name: 8 Center for Computational Biology, Flatiron Institute, Simons Foundation, New York, New York, USA – name: 10 Department of Biochemistry and Molecular Biology, University of Texas Medical Branch, Galveston, Texas, USA – name: 1 Department of Pathology, University of Texas Medical Branch, Galveston, Texas, USA – name: 3 Department of Computer Science and – name: 4 Lewis-Sigler Institute of Integrative Genomics, Princeton University, Princeton, New Jersey, USA – name: 5 Moderna Inc., Cambridge, Massachusetts, USA – name: 9 Infectious Disease Pathogenesis Section, Comparative Medicine Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland, USA |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34449440$$D View this record in MEDLINE/PubMed |
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| Snippet | The mRNA-1273 vaccine is effective against SARS-CoV-2 and was granted emergency use authorization by the FDA. Clinical studies, however, cannot provide the... |
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| SubjectTerms | 2019-nCoV Vaccine mRNA-1273 Animals Antibodies Antibodies, Neutralizing - biosynthesis Antibodies, Viral - biosynthesis Antiviral drugs Biomedical research Cell activation Coronaviruses COVID-19 - immunology COVID-19 - prevention & control COVID-19 - virology COVID-19 vaccines COVID-19 Vaccines - administration & dosage COVID-19 Vaccines - immunology COVID-19 Vaccines - pharmacology Development and progression Disease Models, Animal Disease transmission FDA approval Female Hamsters Health aspects Homeostasis Humans Immune response Immunization, Secondary Immunological research Infections Inflammation Leukocytes Lung - immunology Lung - pathology Lung - virology Lung diseases Lungs Lymphocyte Activation Lymphocytes Mesocricetus Messenger RNA Physiological aspects Prevention Replication SARS-CoV-2 - immunology SARS-CoV-2 - physiology Severe acute respiratory syndrome coronavirus 2 Single-Cell Analysis Transcriptomes Vaccines Virus Replication |
| Title | Attenuated activation of pulmonary immune cells in mRNA-1273–vaccinated hamsters after SARS-CoV-2 infection |
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