IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42610-x.html
   My bibliography  Save this article

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

Author

Listed:
  • 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
    Arkansas Children’s Research Institute)

  • 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
    Cornell University College of Veterinary Medicine)

  • 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
    Center for Biofilm Engineering)

  • Anja Kunze

    (Montana State University, Electrical and Computer Engineering Department)

  • Emma K. Loveday

    (Montana State University, Chemical and Biological Engineering Department
    Center for Biofilm Engineering)

  • Matthew P. Taylor

    (Montana State University, Department of Microbiology and Cell Biology)

  • Connie B. Chang

    (Montana State University, Chemical and Biological Engineering Department
    Center for Biofilm Engineering
    Mayo Clinic)

  • James N. Wilking

    (Montana State University, Chemical and Biological Engineering Department
    Center for Biofilm Engineering
    Mayo Clinic)

  • 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
    Center for Biofilm Engineering)

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.

Suggested Citation

  • 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 , 2023. "Antiviral responses in a Jamaican fruit bat intestinal organoid model of SARS-CoV-2 infection," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42610-x
    DOI: 10.1038/s41467-023-42610-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42610-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-42610-x?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Bryan A. Johnson & Xuping Xie & Adam L. Bailey & Birte Kalveram & Kumari G. Lokugamage & Antonio Muruato & Jing Zou & Xianwen Zhang & Terry Juelich & Jennifer K. Smith & Lihong Zhang & Nathen Bopp & C, 2021. "Loss of furin cleavage site attenuates SARS-CoV-2 pathogenesis," Nature, Nature, vol. 591(7849), pages 293-299, March.
    2. Roman Wölfel & Victor M. Corman & Wolfgang Guggemos & Michael Seilmaier & Sabine Zange & Marcel A. Müller & Daniela Niemeyer & Terry C. Jones & Patrick Vollmar & Camilla Rothe & Michael Hoelscher & To, 2020. "Author Correction: Virological assessment of hospitalized patients with COVID-2019," Nature, Nature, vol. 588(7839), pages 35-35, December.
    3. Aaron T. Irving & Matae Ahn & Geraldine Goh & Danielle E. Anderson & Lin-Fa Wang, 2021. "Lessons from the host defences of bats, a unique viral reservoir," Nature, Nature, vol. 589(7842), pages 363-370, January.
    4. Peng Zhou & Xing-Lou Yang & Xian-Guang Wang & Ben Hu & Lei Zhang & Wei Zhang & Hao-Rui Si & Yan Zhu & Bei Li & Chao-Lin Huang & Hui-Dong Chen & Jing Chen & Yun Luo & Hua Guo & Ren-Di Jiang & Mei-Qin L, 2020. "Addendum: A pneumonia outbreak associated with a new coronavirus of probable bat origin," Nature, Nature, vol. 588(7836), pages 6-6, December.
    5. Eric M. Leroy & Brice Kumulungui & Xavier Pourrut & Pierre Rouquet & Alexandre Hassanin & Philippe Yaba & André Délicat & Janusz T. Paweska & Jean-Paul Gonzalez & Robert Swanepoel, 2005. "Fruit bats as reservoirs of Ebola virus," Nature, Nature, vol. 438(7068), pages 575-576, December.
    6. Peng Zhou & Xing-Lou Yang & Xian-Guang Wang & Ben Hu & Lei Zhang & Wei Zhang & Hao-Rui Si & Yan Zhu & Bei Li & Chao-Lin Huang & Hui-Dong Chen & Jing Chen & Yun Luo & Hua Guo & Ren-Di Jiang & Mei-Qin L, 2020. "A pneumonia outbreak associated with a new coronavirus of probable bat origin," Nature, Nature, vol. 579(7798), pages 270-273, March.
    7. Brian C. Searle & Lindsay K. Pino & Jarrett D. Egertson & Ying S. Ting & Robert T. Lawrence & Brendan X. MacLean & Judit Villén & Michael J. MacCoss, 2018. "Chromatogram libraries improve peptide detection and quantification by data independent acquisition mass spectrometry," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    8. Roman Wölfel & Victor M. Corman & Wolfgang Guggemos & Michael Seilmaier & Sabine Zange & Marcel A. Müller & Daniela Niemeyer & Terry C. Jones & Patrick Vollmar & Camilla Rothe & Michael Hoelscher & To, 2020. "Virological assessment of hospitalized patients with COVID-2019," Nature, Nature, vol. 581(7809), pages 465-469, May.
    9. Xiaobo Lei & Xiaojing Dong & Ruiyi Ma & Wenjing Wang & Xia Xiao & Zhongqin Tian & Conghui Wang & Ying Wang & Li Li & Lili Ren & Fei Guo & Zhendong Zhao & Zhuo Zhou & Zichun Xiang & Jianwei Wang, 2020. "Activation and evasion of type I interferon responses by SARS-CoV-2," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    10. Smriti Mallapaty, 2021. "Closest known relatives of virus behind COVID-19 found in Laos," Nature, Nature, vol. 597(7878), pages 603-603, September.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Susanne Kessler & Bradly Burke & Geoffroy Andrieux & Jan Schinköthe & Lea Hamberger & Johannes Kacza & Shijun Zhan & Clara Reasoner & Taru S. Dutt & Maria Kaukab Osman & Marcela Henao-Tamayo & Julian , 2024. "Deciphering bat influenza H18N11 infection dynamics in male Jamaican fruit bats on a single-cell level," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Juan Liu & Fengfeng Mao & Jianhe Chen & Shuaiyao Lu & Yonghe Qi & Yinyan Sun & Linqiang Fang & Man Lung Yeung & Chunmei Liu & Guimei Yu & Guangyu Li & Ximing Liu & Yuansheng Yao & Panpan Huang & Dongx, 2023. "An IgM-like inhalable ACE2 fusion protein broadly neutralizes SARS-CoV-2 variants," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Maria de Lourdes Aguiar-Oliveira & Aline Campos & Aline R. Matos & Caroline Rigotto & Adriana Sotero-Martins & Paulo F. P. Teixeira & Marilda M. Siqueira, 2020. "Wastewater-Based Epidemiology (WBE) and Viral Detection in Polluted Surface Water: A Valuable Tool for COVID-19 Surveillance—A Brief Review," IJERPH, MDPI, vol. 17(24), pages 1-19, December.
    4. Monica Neagu & Carolina Constantin & Mihaela Surcel, 2021. "Testing Antigens, Antibodies, and Immune Cells in COVID-19 as a Public Health Topic—Experience and Outlines," IJERPH, MDPI, vol. 18(24), pages 1-16, December.
    5. Amit A. Upadhyay & Elise G. Viox & Timothy N. Hoang & Arun K. Boddapati & Maria Pino & Michelle Y.-H. Lee & Jacqueline Corry & Zachary Strongin & David A. Cowan & Elizabeth N. Beagle & Tristan R. Hort, 2023. "TREM2+ and interstitial-like macrophages orchestrate airway inflammation in SARS-CoV-2 infection in rhesus macaques," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Ho‐fung Hung, 2022. "The Virus, the Dollar, and the Global Order: The COVID‐19 Crisis in Comparative Perspective," Development and Change, International Institute of Social Studies, vol. 53(6), pages 1177-1199, November.
    7. Sebastian Weigang & Jonas Fuchs & Gert Zimmer & Daniel Schnepf & Lisa Kern & Julius Beer & Hendrik Luxenburger & Jakob Ankerhold & Valeria Falcone & Janine Kemming & Maike Hofmann & Robert Thimme & Ch, 2021. "Within-host evolution of SARS-CoV-2 in an immunosuppressed COVID-19 patient as a source of immune escape variants," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    8. Maritza Puray-Chavez & Jenna E. Eschbach & Ming Xia & Kyle M. LaPak & Qianzi Zhou & Ria Jasuja & Jiehong Pan & Jian Xu & Zixiang Zhou & Shawn Mohammed & Qibo Wang & Dana Q. Lawson & Sanja Djokic & Gao, 2024. "A basally active cGAS-STING pathway limits SARS-CoV-2 replication in a subset of ACE2 positive airway cell models," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Yelin Han & Panpan Xu & Yuyang Wang & Wenliang Zhao & Junpeng Zhang & Shuyi Zhang & Jianwei Wang & Qi Jin & Zhiqiang Wu, 2023. "Panoramic analysis of coronaviruses carried by representative bat species in Southern China to better understand the coronavirus sphere," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    10. Shufeng Liu & Charles B. Stauft & Prabhuanand Selvaraj & Prabha Chandrasekaran & Felice D’Agnillo & Chao-Kai Chou & Wells W. Wu & Christopher Z. Lien & Clement A. Meseda & Cyntia L. Pedro & Matthew F., 2022. "Intranasal delivery of a rationally attenuated SARS-CoV-2 is immunogenic and protective in Syrian hamsters," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Christopher Cyrus Kuhn & Nirakar Basnet & Satish Bodakuntla & Pelayo Alvarez-Brecht & Scott Nichols & Antonio Martinez-Sanchez & Lorenzo Agostini & Young-Min Soh & Junichi Takagi & Christian Biertümpf, 2023. "Direct Cryo-ET observation of platelet deformation induced by SARS-CoV-2 spike protein," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Jun-Yu Si & Yuan-Mei Chen & Ye-Hui Sun & Meng-Xue Gu & Mei-Ling Huang & Lu-Lu Shi & Xiao Yu & Xiao Yang & Qing Xiong & Cheng-Bao Ma & Peng Liu & Zheng-Li Shi & Huan Yan, 2024. "Sarbecovirus RBD indels and specific residues dictating multi-species ACE2 adaptiveness," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    13. Shanlin Ke & Scott T. Weiss & Yang-Yu Liu, 2022. "Dissecting the role of the human microbiome in COVID-19 via metagenome-assembled genomes," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Tobias Schlager & Ashley V. Whillans, 2022. "People underestimate the probability of contracting the coronavirus from friends," Palgrave Communications, Palgrave Macmillan, vol. 9(1), pages 1-11, December.
    15. Shahadat Uddin & Arif Khan & Haohui Lu & Fangyu Zhou & Shakir Karim, 2022. "Suburban Road Networks to Explore COVID-19 Vulnerability and Severity," IJERPH, MDPI, vol. 19(4), pages 1-9, February.
    16. Kirsten R.C. Hensgens & Inge H.T. van Rensen & Anita W. Lekx & Frits H.M. van Osch & Lieve H.H. Knarren & Caroline E. Wyers & Joop P. van den Bergh & Dennis G. Barten, 2021. "Sort and Sieve: Pre-Triage Screening of Patients with Suspected COVID-19 in the Emergency Department," IJERPH, MDPI, vol. 18(17), pages 1-11, September.
    17. Quan-Hoang Vuong & Tam-Tri Le & Viet-Phuong La & Huyen Thanh Thanh Nguyen & Manh-Toan Ho & Quy Khuc & Minh-Hoang Nguyen, 2022. "Covid-19 vaccines production and societal immunization under the serendipity-mindsponge-3D knowledge management theory and conceptual framework," Palgrave Communications, Palgrave Macmillan, vol. 9(1), pages 1-12, December.
    18. Joseph Pateras & Preetam Ghosh, 2022. "A Computational Framework for Exploring SARS-CoV-2 Pharmacodynamic Dose and Timing Regimes," Mathematics, MDPI, vol. 10(20), pages 1-12, October.
    19. Hengrui Liu & Sho Iketani & Arie Zask & Nisha Khanizeman & Eva Bednarova & Farhad Forouhar & Brandon Fowler & Seo Jung Hong & Hiroshi Mohri & Manoj S. Nair & Yaoxing Huang & Nicholas E. S. Tay & Sumin, 2022. "Development of optimized drug-like small molecule inhibitors of the SARS-CoV-2 3CL protease for treatment of COVID-19," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    20. Graziella Orrù & Ciro Conversano & Eleonora Malloggi & Francesca Francesconi & Rebecca Ciacchini & Angelo Gemignani, 2020. "Neurological Complications of COVID-19 and Possible Neuroinvasion Pathways: A Systematic Review," IJERPH, MDPI, vol. 17(18), pages 1-18, September.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42610-x. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.