Antiviral responses in a Jamaican fruit bat intestinal organoid model of SARS-CoV-2 infection

Marziah Hashimi, T. Andrew Sebrell, Jodi F. Hedges, Deann Snyder, Katrina N. Lyon, Stephanie D. Byrum, Samuel G. Mackintosh, Dan Crowley, Michelle D. Cherne, David Skwarchuk, Amanda Robison, Barkan Sidar, Anja Kunze, Emma K. Loveday, Matthew P. Taylor, Connie B. Chang, James N. Wilking, Seth T. Walk, Tony Schountz, Mark A. Jutila and Diane Bimczok ()
Additional contact information
Marziah Hashimi: Montana State University, Department of Microbiology and Cell Biology
T. Andrew Sebrell: Montana State University, Department of Microbiology and Cell Biology
Jodi F. Hedges: Montana State University, Department of Microbiology and Cell Biology
Deann Snyder: Montana State University, Department of Microbiology and Cell Biology
Katrina N. Lyon: Montana State University, Department of Microbiology and Cell Biology
Stephanie D. Byrum: University of Arkansas for Medical Sciences, Department of Biochemistry and Molecular Biology
Samuel G. Mackintosh: University of Arkansas for Medical Sciences, Department of Biochemistry and Molecular Biology
Dan Crowley: Montana State University, Department of Microbiology and Cell Biology
Michelle D. Cherne: Montana State University, Department of Microbiology and Cell Biology
David Skwarchuk: Montana State University, Department of Microbiology and Cell Biology
Amanda Robison: Montana State University, Department of Microbiology and Cell Biology
Barkan Sidar: Montana State University, Chemical and Biological Engineering Department
Anja Kunze: Montana State University, Electrical and Computer Engineering Department
Emma K. Loveday: Montana State University, Chemical and Biological Engineering Department
Matthew P. Taylor: Montana State University, Department of Microbiology and Cell Biology
Connie B. Chang: Montana State University, Chemical and Biological Engineering Department
James N. Wilking: Montana State University, Chemical and Biological Engineering Department
Seth T. Walk: Montana State University, Department of Microbiology and Cell Biology
Tony Schountz: Colorado State University, Fort
Mark A. Jutila: Montana State University, Department of Microbiology and Cell Biology
Diane Bimczok: Montana State University, Department of Microbiology and Cell Biology

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract Bats are natural reservoirs for several zoonotic viruses, potentially due to an enhanced capacity to control viral infection. However, the mechanisms of antiviral responses in bats are poorly defined. Here we established a Jamaican fruit bat (JFB, Artibeus jamaicensis) intestinal organoid model of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) infection. Upon infection with SARS-CoV-2, increased viral RNA and subgenomic RNA was detected, but no infectious virus was released, indicating that JFB organoids support only limited viral replication but not viral reproduction. SARS-CoV-2 replication was associated with significantly increased gene expression of type I interferons and inflammatory cytokines. Interestingly, SARS-CoV-2 also caused enhanced formation and growth of JFB organoids. Proteomics revealed an increase in inflammatory signaling, cell turnover, cell repair, and SARS-CoV-2 infection pathways. Collectively, our findings suggest that primary JFB intestinal epithelial cells mount successful antiviral interferon responses and that SARS-CoV-2 infection in JFB cells induces protective regenerative pathways.

Date: 2023
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DOI: 10.1038/s41467-023-42610-x

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