IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40076-5.html
   My bibliography  Save this article

Genetically diverse mouse models of SARS-CoV-2 infection reproduce clinical variation in type I interferon and cytokine responses in COVID-19

Author

Listed:
  • Shelly J. Robertson

    (National Institute of Allergy and Infectious Diseases, NIH
    National Institute of Allergy and Infectious Diseases, NIH)

  • Olivia Bedard

    (The Jackson Laboratory)

  • Kristin L. McNally

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Carl Shaia

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Chad S. Clancy

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Matthew Lewis

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Rebecca M. Broeckel

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Abhilash I. Chiramel

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Jeffrey G. Shannon

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Gail L. Sturdevant

    (National Institute of Allergy and Infectious Diseases, NIH
    National Institute of Allergy and Infectious Diseases, NIH)

  • Rebecca Rosenke

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Sarah L. Anzick

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Elvira Forte

    (The Jackson Laboratory
    Springer Nature)

  • Christoph Preuss

    (The Jackson Laboratory)

  • Candice N. Baker

    (The Jackson Laboratory)

  • Jeffrey M. Harder

    (The Jackson Laboratory)

  • Catherine Brunton

    (The Jackson Laboratory)

  • Steven Munger

    (The Jackson Laboratory)

  • Daniel P. Bruno

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Justin B. Lack

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Jacqueline M. Leung

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Amirhossein Shamsaddini

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Paul Gardina

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Daniel E. Sturdevant

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Jian Sun

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Craig Martens

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Steven M. Holland

    (National Institute of Allergy and Infectious Diseases, NIH)

  • Nadia A. Rosenthal

    (The Jackson Laboratory
    Imperial College London)

  • Sonja M. Best

    (National Institute of Allergy and Infectious Diseases, NIH
    National Institute of Allergy and Infectious Diseases, NIH)

Abstract

Inflammation in response to severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) infection drives severity of coronavirus disease 2019 (COVID-19) and is influenced by host genetics. To understand mechanisms of inflammation, animal models that reflect genetic diversity and clinical outcomes observed in humans are needed. We report a mouse panel comprising the genetically diverse Collaborative Cross (CC) founder strains crossed to human ACE2 transgenic mice (K18-hACE2) that confers susceptibility to SARS-CoV-2. Infection of CC x K18-hACE2 resulted in a spectrum of survival, viral replication kinetics, and immune profiles. Importantly, in contrast to the K18-hACE2 model, early type I interferon (IFN-I) and regulated proinflammatory responses were required for control of SARS-CoV-2 replication in PWK x K18-hACE2 mice that were highly resistant to disease. Thus, virus dynamics and inflammation observed in COVID-19 can be modeled in diverse mouse strains that provide a genetically tractable platform for understanding anti-coronavirus immunity.

Suggested Citation

  • Shelly J. Robertson & Olivia Bedard & Kristin L. McNally & Carl Shaia & Chad S. Clancy & Matthew Lewis & Rebecca M. Broeckel & Abhilash I. Chiramel & Jeffrey G. Shannon & Gail L. Sturdevant & Rebecca , 2023. "Genetically diverse mouse models of SARS-CoV-2 infection reproduce clinical variation in type I interferon and cytokine responses in COVID-19," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40076-5
    DOI: 10.1038/s41467-023-40076-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40076-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-40076-5?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. Takehiro Takahashi & Mallory K. Ellingson & Patrick Wong & Benjamin Israelow & Carolina Lucas & Jon Klein & Julio Silva & Tianyang Mao & Ji Eun Oh & Maria Tokuyama & Peiwen Lu & Arvind Venkataraman & , 2020. "Sex differences in immune responses that underlie COVID-19 disease outcomes," Nature, Nature, vol. 588(7837), pages 315-320, December.
    2. Elizabeth J. Williamson & Alex J. Walker & Krishnan Bhaskaran & Seb Bacon & Chris Bates & Caroline E. Morton & Helen J. Curtis & Amir Mehrkar & David Evans & Peter Inglesby & Jonathan Cockburn & Helen, 2020. "Factors associated with COVID-19-related death using OpenSAFELY," Nature, Nature, vol. 584(7821), pages 430-436, August.
    3. Carolina Lucas & Patrick Wong & Jon Klein & Tiago B. R. Castro & Julio Silva & Maria Sundaram & Mallory K. Ellingson & Tianyang Mao & Ji Eun Oh & Benjamin Israelow & Takehiro Takahashi & Maria Tokuyam, 2020. "Longitudinal analyses reveal immunological misfiring in severe COVID-19," Nature, Nature, vol. 584(7821), pages 463-469, August.
    4. Jian Zheng & Lok-Yin Roy Wong & Kun Li & Abhishek Kumar Verma & Miguel E. Ortiz & Christine Wohlford-Lenane & Mariah R. Leidinger & C. Michael Knudson & David K. Meyerholz & Paul B. McCray & Stanley P, 2021. "COVID-19 treatments and pathogenesis including anosmia in K18-hACE2 mice," Nature, Nature, vol. 589(7843), pages 603-607, January.
    5. Toni M. Delorey & Carly G. K. Ziegler & Graham Heimberg & Rachelly Normand & Yiming Yang & Åsa Segerstolpe & Domenic Abbondanza & Stephen J. Fleming & Ayshwarya Subramanian & Daniel T. Montoro & Karth, 2021. "COVID-19 tissue atlases reveal SARS-CoV-2 pathology and cellular targets," Nature, Nature, vol. 595(7865), pages 107-113, July.
    6. Rita E. Chen & Emma S. Winkler & James Brett Case & Ishmael D. Aziati & Traci L. Bricker & Astha Joshi & Tamarand L. Darling & Baoling Ying & John M. Errico & Swathi Shrihari & Laura A. VanBlargan & X, 2021. "In vivo monoclonal antibody efficacy against SARS-CoV-2 variant strains," Nature, Nature, vol. 596(7870), pages 103-108, August.
    7. 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.
    8. Erola Pairo-Castineira & Sara Clohisey & Lucija Klaric & Andrew D. Bretherick & Konrad Rawlik & Dorota Pasko & Susan Walker & Nick Parkinson & Max Head Fourman & Clark D. Russell & James Furniss & Ann, 2021. "Genetic mechanisms of critical illness in COVID-19," Nature, Nature, vol. 591(7848), pages 92-98, March.
    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. Maik Pietzner & Robert Lorenz Chua & Eleanor Wheeler & Katharina Jechow & Julian D. S. Willett & Helena Radbruch & Saskia Trump & Bettina Heidecker & Hugo Zeberg & Frank L. Heppner & Roland Eils & Mar, 2022. "ELF5 is a potential respiratory epithelial cell-specific risk gene for severe COVID-19," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Tomoko Nakanishi & Julian Willett & Yossi Farjoun & Richard J. Allen & Beatriz Guillen-Guio & Darin Adra & Sirui Zhou & J. Brent Richards, 2023. "Alternative splicing in lung influences COVID-19 severity and respiratory diseases," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Lei Peng & Yingxia Hu & Madeleine C. Mankowski & Ping Ren & Rita E. Chen & Jin Wei & Min Zhao & Tongqing Li & Therese Tripler & Lupeng Ye & Ryan D. Chow & Zhenhao Fang & Chunxiang Wu & Matthew B. Dong, 2022. "Monospecific and bispecific monoclonal SARS-CoV-2 neutralizing antibodies that maintain potency against B.1.617," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Yvonne M. Mueller & Thijs J. Schrama & Rik Ruijten & Marco W. J. Schreurs & Dwin G. B. Grashof & Harmen J. G. van de Werken & Giovanna Jona Lasinio & Daniel Álvarez-Sierra & Caoimhe H. Kiernan & Melis, 2022. "Stratification of hospitalized COVID-19 patients into clinical severity progression groups by immuno-phenotyping and machine learning," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Lucie Bernard-Raichon & Mericien Venzon & Jon Klein & Jordan E. Axelrad & Chenzhen Zhang & Alexis P. Sullivan & Grant A. Hussey & Arnau Casanovas-Massana & Maria G. Noval & Ana M. Valero-Jimenez & Jua, 2022. "Gut microbiome dysbiosis in antibiotic-treated COVID-19 patients is associated with microbial translocation and bacteremia," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    6. Brandily, Paul & Brébion, Clément & Briole, Simon & Khoury, Laura, 2021. "A poorly understood disease? The impact of COVID-19 on the income gradient in mortality over the course of the pandemic," European Economic Review, Elsevier, vol. 140(C).
    7. Sunil K. Ahuja & Muthu Saravanan Manoharan & Grace C. Lee & Lyle R. McKinnon & Justin A. Meunier & Maristella Steri & Nathan Harper & Edoardo Fiorillo & Alisha M. Smith & Marcos I. Restrepo & Anne P. , 2023. "Immune resilience despite inflammatory stress promotes longevity and favorable health outcomes including resistance to infection," Nature Communications, Nature, vol. 14(1), pages 1-31, December.
    8. Borau, Sylvie & Couprie, Hélène & Hopfensitz, Astrid, 2022. "The prosociality of married people: Evidence from a large multinational sample," Journal of Economic Psychology, Elsevier, vol. 92(C).
    9. Anna Adamecz-Völgyi & Ágnes Szabó-Morvai, 2021. "Confidence in public institutions is critical in containing the COVID-19 pandemic," CERS-IE WORKING PAPERS 2126, Institute of Economics, Centre for Economic and Regional Studies.
    10. Biao Zhou & Runhong Zhou & Bingjie Tang & Jasper Fuk-Woo Chan & Mengxiao Luo & Qiaoli Peng & Shuofeng Yuan & Hang Liu & Bobo Wing-Yee Mok & Bohao Chen & Pui Wang & Vincent Kwok-Man Poon & Hin Chu & Ch, 2022. "A broadly neutralizing antibody protects Syrian hamsters against SARS-CoV-2 Omicron challenge," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Anna R. Mäkelä & Hasan Uğurlu & Liina Hannula & Ravi Kant & Petja Salminen & Riku Fagerlund & Sanna Mäki & Anu Haveri & Tomas Strandin & Lauri Kareinen & Jussi Hepojoki & Suvi Kuivanen & Lev Levanov &, 2023. "Intranasal trimeric sherpabody inhibits SARS-CoV-2 including recent immunoevasive Omicron subvariants," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    12. Dorn, Florian & Lange, Berit & Braml, Martin & Gstrein, David & Nyirenda, John L.Z. & Vanella, Patrizio & Winter, Joachim & Fuest, Clemens & Krause, Gérard, 2023. "The challenge of estimating the direct and indirect effects of COVID-19 interventions – Toward an integrated economic and epidemiological approach," Economics & Human Biology, Elsevier, vol. 49(C).
    13. Changli Wei & Prasun K. Datta & Florian Siegerist & Jing Li & Sudhini Yashwanth & Kwi Hye Koh & Nicholas W. Kriho & Anis Ismail & Shengyuan Luo & Tracy Fischer & Kyle T. Amber & David Cimbaluk & Alan , 2023. "SuPAR mediates viral response proteinuria by rapidly changing podocyte function," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    14. Elizabeth M. Parzych & Jianqiu Du & Ali R. Ali & Katherine Schultheis & Drew Frase & Trevor R. F. Smith & Jiayan Cui & Neethu Chokkalingam & Nicholas J. Tursi & Viviane M. Andrade & Bryce M. Warner & , 2022. "DNA-delivered antibody cocktail exhibits improved pharmacokinetics and confers prophylactic protection against SARS-CoV-2," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    15. Simona Bignami-Van Assche & Daniela Ghio, 2022. "Comparing COVID-19 fatality across countries: a synthetic demographic indicator," Journal of Population Research, Springer, vol. 39(4), pages 513-525, December.
    16. Nikaïa Smith & Céline Possémé & Vincent Bondet & Jamie Sugrue & Liam Townsend & Bruno Charbit & Vincent Rouilly & Violaine Saint-André & Tom Dott & Andre Rodriguez Pozo & Nader Yatim & Olivier Schwart, 2022. "Defective activation and regulation of type I interferon immunity is associated with increasing COVID-19 severity," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    17. Dominik Menges & Kyra D. Zens & Tala Ballouz & Nicole Caduff & Daniel Llanas-Cornejo & Hélène E. Aschmann & Anja Domenghino & Céline Pellaton & Matthieu Perreau & Craig Fenwick & Giuseppe Pantaleo & C, 2022. "Heterogenous humoral and cellular immune responses with distinct trajectories post-SARS-CoV-2 infection in a population-based cohort," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    18. McKee, Martin & Altmann, Danny & Costello, Anthony & Friston, Karl & Haque, Zubaida & Khunti, Kamlesh & Michie, Susan & Oni, Tolullah & Pagel, Christina & Pillay, Deenan & Reicher, Steve & Salisbury, , 2022. "Open science communication: The first year of the UK's Independent Scientific Advisory Group for Emergencies," Health Policy, Elsevier, vol. 126(3), pages 234-244.
    19. Katarzyna Orlewska & Justyna Klusek & Dorota Zarębska-Michaluk & Kamila Kocańda & Ruslan Oblap & Anna Cedro & Bartosz Witczak & Jolanta Klusek & Andrzej Śliwczyński & Ewa Orlewska, 2023. "Association between Glutathione S-Transferases Gene Variants and COVID-19 Severity in Previously Vaccinated and Unvaccinated Polish Patients with Confirmed SARS-CoV-2 Infection," IJERPH, MDPI, vol. 20(4), pages 1-11, February.
    20. João Faro-Viana & Marie-Louise Bergman & Lígia A. Gonçalves & Nádia Duarte & Teresa P. Coutinho & Patrícia C. Borges & Christian Diwo & Rute Castro & Paula Matoso & Vanessa Malheiro & Ana Brennand & L, 2022. "Population homogeneity for the antibody response to COVID-19 BNT162b2/Comirnaty vaccine is only reached after the second dose across all adult age ranges," Nature Communications, Nature, vol. 13(1), pages 1-8, 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:14:y:2023:i:1:d:10.1038_s41467-023-40076-5. 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.