IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35225-1.html
   My bibliography  Save this article

Ocular tropism of SARS-CoV-2 in animal models with retinal inflammation via neuronal invasion following intranasal inoculation

Author

Listed:
  • Gi Uk Jeong

    (Korea Research Institute of Chemical Technology)

  • Hyung-Jun Kwon

    (Korea Research Institute of Bioscience and Biotechnology
    Jeonbuk Branch, Korea Institute of Toxicology)

  • Wern Hann Ng

    (Griffith University
    Griffith University
    Griffith University)

  • Xiang Liu

    (Griffith University
    Griffith University
    Griffith University)

  • Hyun Woo Moon

    (Korea Research Institute of Chemical Technology)

  • Gun Young Yoon

    (Korea Research Institute of Chemical Technology)

  • Hye Jin Shin

    (Korea Research Institute of Chemical Technology
    Chungnam National University School of Medicine)

  • In-Chul Lee

    (Korea Research Institute of Bioscience and Biotechnology
    Jeonbuk Branch, Korea Institute of Toxicology)

  • Zheng Lung Ling

    (The University of Sydney
    The University of Sydney)

  • Alanna G. Spiteri

    (The University of Sydney
    The University of Sydney)

  • Nicholas J. C. King

    (Griffith University
    The University of Sydney
    The University of Sydney
    The University of Sydney)

  • Adam Taylor

    (Griffith University
    Griffith University
    Griffith University)

  • Ji Soo Chae

    (PerkinElmer)

  • Chonsaeng Kim

    (Korea Research Institute of Chemical Technology)

  • Dae-Gyun Ahn

    (Korea Research Institute of Chemical Technology)

  • Kyun-Do Kim

    (Korea Research Institute of Chemical Technology)

  • Young Bae Ryu

    (Korea Research Institute of Bioscience and Biotechnology)

  • Seong-Jun Kim

    (Korea Research Institute of Chemical Technology)

  • Suresh Mahalingam

    (Griffith University
    Griffith University
    Griffith University)

  • Young-Chan Kwon

    (Korea Research Institute of Chemical Technology)

Abstract

Although ocular manifestations are reported in patients with COVID-19, consensus on ocular tropism of SARS-CoV-2 is lacking. Here, we infect K18-hACE2 transgenic mice with SARS-CoV-2 using various routes. We observe ocular manifestation and retinal inflammation with production of pro-inflammatory cytokines in the eyes of intranasally (IN)-infected mice. Intratracheal (IT) infection results in dissemination of the virus from the lungs to the brain and eyes via trigeminal and optic nerves. Ocular and neuronal invasions are confirmed using intracerebral (IC) infection. Notably, the eye-dropped (ED) virus does not cause lung infection and becomes undetectable with time. Ocular and neurotropic distribution of the virus in vivo is evident in fluorescence imaging with an infectious clone of SARS-CoV-2-mCherry. The ocular tropic and neuroinvasive characteristics of SARS-CoV-2 are confirmed in wild-type Syrian hamsters. Our data can improve the understanding regarding viral transmission and clinical characteristics of SARS-CoV-2 and help in improving COVID-19 control procedures.

Suggested Citation

  • Gi Uk Jeong & Hyung-Jun Kwon & Wern Hann Ng & Xiang Liu & Hyun Woo Moon & Gun Young Yoon & Hye Jin Shin & In-Chul Lee & Zheng Lung Ling & Alanna G. Spiteri & Nicholas J. C. King & Adam Taylor & Ji Soo, 2022. "Ocular tropism of SARS-CoV-2 in animal models with retinal inflammation via neuronal invasion following intranasal inoculation," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35225-1
    DOI: 10.1038/s41467-022-35225-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35225-1
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-35225-1?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. Wei Deng & Linlin Bao & Hong Gao & Zhiguang Xiang & Yajin Qu & Zhiqi Song & Shuran Gong & Jiayi Liu & Jiangning Liu & Pin Yu & Feifei Qi & Yanfeng Xu & Fengli Li & Chong Xiao & Qi Lv & Jing Xue & Qian, 2020. "Ocular conjunctival inoculation of SARS-CoV-2 can cause mild COVID-19 in rhesus macaques," Nature Communications, Nature, vol. 11(1), pages 1-7, December.
    2. Sin Fun Sia & Li-Meng Yan & Alex W. H. Chin & Kevin Fung & Ka-Tim Choy & Alvina Y. L. Wong & Prathanporn Kaewpreedee & Ranawaka A. P. M. Perera & Leo L. M. Poon & John M. Nicholls & Malik Peiris & Hui, 2020. "Pathogenesis and transmission of SARS-CoV-2 in golden hamsters," Nature, Nature, vol. 583(7818), pages 834-838, July.
    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. Sapna Sharma & Thomas Vercruysse & Lorena Sanchez-Felipe & Winnie Kerstens & Madina Rasulova & Lindsey Bervoets & Carolien Keyzer & Rana Abdelnabi & Caroline S. Foo & Viktor Lemmens & Dominique Loover, 2022. "Updated vaccine protects against SARS-CoV-2 variants including Omicron (B.1.1.529) and prevents transmission in hamsters," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Dillon S. McBride & Sofya K. Garushyants & John Franks & Andrew F. Magee & Steven H. Overend & Devra Huey & Amanda M. Williams & Seth A. Faith & Ahmed Kandeil & Sanja Trifkovic & Lance Miller & Trusha, 2023. "Accelerated evolution of SARS-CoV-2 in free-ranging white-tailed deer," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Laura Heydemann & Małgorzata Ciurkiewicz & Georg Beythien & Kathrin Becker & Klaus Schughart & Stephanie Stanelle-Bertram & Berfin Schaumburg & Nancy Mounogou-Kouassi & Sebastian Beck & Martin Zickler, 2023. "Hamster model for post-COVID-19 alveolar regeneration offers an opportunity to understand post-acute sequelae of SARS-CoV-2," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    4. Bruno A. Rodriguez-Rodriguez & Grace O. Ciabattoni & Ralf Duerr & Ana M. Valero-Jimenez & Stephen T. Yeung & Keaton M. Crosse & Austin R. Schinlever & Lucie Bernard-Raichon & Joaquin Rodriguez Galvan , 2023. "A neonatal mouse model characterizes transmissibility of SARS-CoV-2 variants and reveals a role for ORF8," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Cedric C. S. Tan & Su Datt Lam & Damien Richard & Christopher J. Owen & Dorothea Berchtold & Christine Orengo & Meera Surendran Nair & Suresh V. Kuchipudi & Vivek Kapur & Lucy van Dorp & François Ball, 2022. "Transmission of SARS-CoV-2 from humans to animals and potential host adaptation," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    6. Carlos Ávila-Nieto & Júlia Vergara-Alert & Pep Amengual-Rigo & Erola Ainsua-Enrich & Marco Brustolin & María Luisa Rodríguez de la Concepción & Núria Pedreño-Lopez & Jordi Rodon & Victor Urrea & Edwar, 2024. "Immunization with V987H-stabilized Spike glycoprotein protects K18-hACE2 mice and golden Syrian hamsters upon SARS-CoV-2 infection," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Julia T. Castro & Patrick Azevedo & Marcílio J. Fumagalli & Natalia S. Hojo-Souza & Natalia Salazar & Gregório G. Almeida & Livia I. Oliveira & Lídia Faustino & Lis R. Antonelli & Tomas G. Marçal & Ma, 2022. "Promotion of neutralizing antibody-independent immunity to wild-type and SARS-CoV-2 variants of concern using an RBD-Nucleocapsid fusion protein," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. Ryuta Uraki & Shun Iida & Peter J. Halfmann & Seiya Yamayoshi & Yuichiro Hirata & Kiyoko Iwatsuki-Horimoto & Maki Kiso & Mutsumi Ito & Yuri Furusawa & Hiroshi Ueki & Yuko Sakai-Tagawa & Makoto Kuroda , 2023. "Characterization of SARS-CoV-2 Omicron BA.2.75 clinical isolates," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    9. Dongsheng Chen & Jian Sun & Jiacheng Zhu & Xiangning Ding & Tianming Lan & Xiran Wang & Weiying Wu & Zhihua Ou & Linnan Zhu & Peiwen Ding & Haoyu Wang & Lihua Luo & Rong Xiang & Xiaoling Wang & Jiayin, 2021. "Single cell atlas for 11 non-model mammals, reptiles and birds," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    10. Matthew R. Chang & Luke Tomasovic & Natalia A. Kuzmina & Adam J. Ronk & Patrick O. Byrne & Rebecca Johnson & Nadia Storm & Eduardo Olmedillas & Yixuan J. Hou & Alexandra Schäfer & Sarah R. Leist & Lon, 2022. "IgG-like bispecific antibodies with potent and synergistic neutralization against circulating SARS-CoV-2 variants of concern," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. 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.
    12. Liang Zhang & Yao Jiang & Jinhang He & Junyu Chen & Ruoyao Qi & Lunzhi Yuan & Tiange Shao & Hui Zhao & Congjie Chen & Yaode Chen & Xijing Wang & Xing Lei & Qingxiang Gao & Chunlan Zhuang & Ming Zhou &, 2023. "Intranasal influenza-vectored COVID-19 vaccine restrains the SARS-CoV-2 inflammatory response in hamsters," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    13. Weizhong Li & Tao Wang & Arunraj M. Rajendrakumar & Gyanada Acharya & Zizhen Miao & Berin P. Varghese & Hailiang Yu & Bibek Dhakal & Tanya LeRoith & Athira Karunakaran & Wenbin Tuo & Xiaoping Zhu, 2023. "An FcRn-targeted mucosal vaccine against SARS-CoV-2 infection and transmission," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    14. Federico Armando & Georg Beythien & Franziska K. Kaiser & Lisa Allnoch & Laura Heydemann & Malgorzata Rosiak & Svenja Becker & Mariana Gonzalez-Hernandez & Mart M. Lamers & Bart L. Haagmans & Kate Gui, 2022. "SARS-CoV-2 Omicron variant causes mild pathology in the upper and lower respiratory tract of hamsters," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    15. Magen E. Francis & Ethan B. Jansen & Anthony Yourkowski & Alaa Selim & Cynthia L. Swan & Brian K. MacPhee & Brittany Thivierge & Rachelle Buchanan & Kerry J. Lavender & Joseph Darbellay & Matthew B. R, 2023. "Previous infection with seasonal coronaviruses does not protect male Syrian hamsters from challenge with SARS-CoV-2," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    16. Anna Maria Cattelan & Lolita Sasset & Federico Zabeo & Anna Ferrari & Lucia Rossi & Maria Mazzitelli & Silvia Cocchio & Vincenzo Baldo, 2022. "Rapid Antigen Test LumiraDx TM vs. Real Time Polymerase Chain Reaction for the Diagnosis of SARS-CoV-2 Infection: A Retrospective Cohort Study," IJERPH, MDPI, vol. 19(7), pages 1-12, March.
    17. Guilherme Dias de Melo & Victoire Perraud & Flavio Alvarez & Alba Vieites-Prado & Seonhee Kim & Lauriane Kergoat & Anthony Coleon & Bettina Salome Trüeb & Magali Tichit & Aurèle Piazza & Agnès Thierry, 2023. "Neuroinvasion and anosmia are independent phenomena upon infection with SARS-CoV-2 and its variants," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    18. Julia M. Adler & Ricardo Martin Vidal & Christine Langner & Daria Vladimirova & Azza Abdelgawad & Daniela Kunecova & Xiaoyuan Lin & Geraldine Nouailles & Anne Voss & Sandra Kunder & Achim D. Gruber & , 2024. "An intranasal live-attenuated SARS-CoV-2 vaccine limits virus transmission," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    19. Kenrie P. Y. Hui & Alex W. H. Chin & John Ehret & Ka-Chun Ng & Malik Peiris & Leo L. M. Poon & Karen H. M. Wong & Michael C. W. Chan & Ian Hosegood & John M. Nicholls, 2023. "Stability of SARS-CoV-2 on Commercial Aircraft Interior Surfaces with Implications for Effective Control Measures," IJERPH, MDPI, vol. 20(16), pages 1-12, August.
    20. Zhenzhen Wang & Shiqi Hu & Kristen D. Popowski & Shuo Liu & Dashuai Zhu & Xuan Mei & Junlang Li & Yilan Hu & Phuong-Uyen C. Dinh & Xiaojie Wang & Ke Cheng, 2024. "Inhalation of ACE2-expressing lung exosomes provides prophylactic protection against SARS-CoV-2," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

    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:13:y:2022:i:1:d:10.1038_s41467-022-35225-1. 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.