IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50339-4.html
   My bibliography  Save this article

Non-human primate model of long-COVID identifies immune associates of hyperglycemia

Author

Listed:
  • Clovis S. Palmer

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

  • Chrysostomos Perdios

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

  • Mohamed Abdel-Mohsen

    (The Wistar Institute)

  • Joseph Mudd

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

  • Prasun K. Datta

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

  • Nicholas J. Maness

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

  • Gabrielle Lehmicke

    (Tulane National Primate Research Center)

  • Nadia Golden

    (Tulane National Primate Research Center)

  • Linh Hellmers

    (Tulane National Primate Research Center)

  • Carol Coyne

    (Tulane National Primate Research Center)

  • Kristyn Moore Green

    (Tulane National Primate Research Center)

  • Cecily Midkiff

    (Tulane National Primate Research Center)

  • Kelsey Williams

    (Tulane National Primate Research Center)

  • Rafael Tiburcio

    (University of San Francisco)

  • Marissa Fahlberg

    (Tulane National Primate Research Center)

  • Kyndal Boykin

    (Tulane National Primate Research Center)

  • Carys Kenway

    (Tulane National Primate Research Center)

  • Kasi Russell-Lodrigue

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

  • Angela Birnbaum

    (Tulane National Primate Research Center)

  • Rudolf Bohm

    (Oregon Health and Science University)

  • Robert Blair

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

  • Jason P. Dufour

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

  • Tracy Fischer

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

  • Ahmad A. Saied

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

  • Jay Rappaport

    (Tulane National Primate Research Center
    Tulane University School of Medicine)

Abstract

Hyperglycemia, and exacerbation of pre-existing deficits in glucose metabolism, are manifestations of the post-acute sequelae of SARS-CoV-2. Our understanding of metabolic decline after acute COVID-19 remains unclear due to the lack of animal models. Here, we report a non-human primate model of metabolic post-acute sequelae of SARS-CoV-2 using SARS-CoV-2 infected African green monkeys. Using this model, we identify a dysregulated blood chemokine signature during acute COVID-19 that correlates with elevated and persistent hyperglycemia four months post-infection. Hyperglycemia also correlates with liver glycogen levels, but there is no evidence of substantial long-term SARS-CoV-2 replication in the liver and pancreas. Finally, we report a favorable glycemic effect of the SARS-CoV-2 mRNA vaccine, administered on day 4 post-infection. Together, these data suggest that the African green monkey model exhibits important similarities to humans and can be utilized to assess therapeutic candidates to combat COVID-related metabolic defects.

Suggested Citation

  • Clovis S. Palmer & Chrysostomos Perdios & Mohamed Abdel-Mohsen & Joseph Mudd & Prasun K. Datta & Nicholas J. Maness & Gabrielle Lehmicke & Nadia Golden & Linh Hellmers & Carol Coyne & Kristyn Moore Gr, 2024. "Non-human primate model of long-COVID identifies immune associates of hyperglycemia," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50339-4
    DOI: 10.1038/s41467-024-50339-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50339-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-50339-4?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. Sydney R. Stein & Sabrina C. Ramelli & Alison Grazioli & Joon-Yong Chung & Manmeet Singh & Claude Kwe Yinda & Clayton W. Winkler & Junfeng Sun & James M. Dickey & Kris Ylaya & Sung Hee Ko & Andrew P. , 2022. "SARS-CoV-2 infection and persistence in the human body and brain at autopsy," Nature, Nature, vol. 612(7941), pages 758-763, December.
    2. M. D. Fahlberg & R. V. Blair & L. A. Doyle-Meyers & C. C. Midkiff & G. Zenere & K. E. Russell-Lodrigue & C. J. Monjure & E. H. Haupt & T. P. Penney & G. Lehmicke & B. M. Threeton & N. Golden & P. K. D, 2020. "Cellular events of acute, resolving or progressive COVID-19 in SARS-CoV-2 infected non-human primates," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    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.
    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. 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.
    2. 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.
    3. 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.
    4. Sung Hee Ko & Pierce Radecki & Frida Belinky & Jinal N. Bhiman & Susan Meiring & Jackie Kleynhans & Daniel Amoako & Vanessa Guerra Canedo & Margaret Lucas & Dikeledi Kekana & Neil Martinson & Limakats, 2024. "Rapid intra-host diversification and evolution of SARS-CoV-2 in advanced HIV infection," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Kim McFann & Bridget A. Baxter & Stephanie M. LaVergne & Sophia Stromberg & Kailey Berry & Madison Tipton & Jared Haberman & Jeremy Ladd & Tracy L. Webb & Julie A. Dunn & Elizabeth P. Ryan, 2021. "Quality of Life (QoL) Is Reduced in Those with Severe COVID-19 Disease, Post-Acute Sequelae of COVID-19, and Hospitalization in United States Adults from Northern Colorado," IJERPH, MDPI, vol. 18(21), pages 1-9, October.
    6. S. Jaumdally & M. Tomasicchio & A. Pooran & A. Esmail & A. Kotze & S. Meier & L. Wilson & S. Oelofse & C. Merwe & A. Roomaney & M. Davids & T. Suliman & R. Joseph & T. Perumal & A. Scott & M. Shaw & W, 2024. "Frequency, kinetics and determinants of viable SARS-CoV-2 in bioaerosols from ambulatory COVID-19 patients infected with the Beta, Delta or Omicron variants," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Quy Xiao Xuan Lin & Deepa Rajagopalan & Akshamal M. Gamage & Le Min Tan & Prasanna Nori Venkatesh & Wharton O. Y. Chan & Dilip Kumar & Ragini Agrawal & Yao Chen & Siew-Wai Fong & Amit Singh & Louisa J, 2024. "Longitudinal single cell atlas identifies complex temporal relationship between type I interferon response and COVID-19 severity," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    8. Scott Lu & Michael J. Peluso & David V. Glidden & Michelle C. Davidson & Kara Lugtu & Jesus Pineda-Ramirez & Michel Tassetto & Miguel Garcia-Knight & Amethyst Zhang & Sarah A. Goldberg & Jessica Y. Ch, 2024. "Early biological markers of post-acute sequelae of SARS-CoV-2 infection," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    9. Al Ozonoff & Naresh Doni Jayavelu & Shanshan Liu & Esther Melamed & Carly E. Milliren & Jingjing Qi & Linda N. Geng & Grace A. McComsey & Charles B. Cairns & Lindsey R. Baden & Joanna Schaenman & Albe, 2024. "Features of acute COVID-19 associated with post-acute sequelae of SARS-CoV-2 phenotypes: results from the IMPACC study," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    10. Noel G. Panagiotides & Fritz Zimprich & Klaus Machold & Oliver Schlager & Markus Müller & Sebastian Ertl & Henriette Löffler-Stastka & Renate Koppensteiner & Patricia P. Wadowski, 2023. "A Case of Autoimmune Small Fiber Neuropathy as Possible Post COVID Sequelae," IJERPH, MDPI, vol. 20(6), pages 1-12, March.
    11. Wei Feng & Joanne C. Beer & Qinyu Hao & Ishara S. Ariyapala & Aparna Sahajan & Andrei Komarov & Katie Cha & Mason Moua & Xiaolei Qiu & Xiaomei Xu & Shweta Iyengar & Thu Yoshimura & Rajini Nagaraj & Li, 2023. "NULISA: a proteomic liquid biopsy platform with attomolar sensitivity and high multiplexing," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Tiago Fazolo & Karina Lima & Julia C. Fontoura & Priscila Oliveira Souza & Gabriel Hilario & Renata Zorzetto & Luiz Rodrigues Júnior & Veridiane Maria Pscheidt & Jayme Castilhos Ferreira Neto & Alisso, 2021. "Pediatric COVID-19 patients in South Brazil show abundant viral mRNA and strong specific anti-viral responses," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    13. Fábio Santos Lira & Telmo Pereira & Luciele Guerra Minuzzi & Caique Figueiredo & Tiago Olean-Oliveira & Ana Paula Coelho Figueira Freire & Manuel João Coelho-e-Silva & Armando Caseiro & Ronaldo Vagner, 2021. "Modulatory Effects of Physical Activity Levels on Immune Responses and General Clinical Functions in Adult Patients with Mild to Moderate SARS-CoV-2 Infections—A Protocol for an Observational Prospect," IJERPH, MDPI, vol. 18(24), pages 1-13, December.
    14. 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.
    15. 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.
    16. Olga Scudiero & Barbara Lombardo & Mariarita Brancaccio & Cristina Mennitti & Arturo Cesaro & Fabio Fimiani & Luca Gentile & Elisabetta Moscarella & Federica Amodio & Annaluisa Ranieri & Felice Gragna, 2021. "Exercise, Immune System, Nutrition, Respiratory and Cardiovascular Diseases during COVID-19: A Complex Combination," IJERPH, MDPI, vol. 18(3), pages 1-20, January.
    17. 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.
    18. Minami Nagai & Miyu Moriyama & Chiharu Ishii & Hirotake Mori & Hikaru Watanabe & Taku Nakahara & Takuji Yamada & Dai Ishikawa & Takamasa Ishikawa & Akiyoshi Hirayama & Ikuo Kimura & Akihito Nagahara &, 2023. "High body temperature increases gut microbiota-dependent host resistance to influenza A virus and SARS-CoV-2 infection," Nature Communications, Nature, vol. 14(1), pages 1-13, 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:15:y:2024:i:1:d:10.1038_s41467-024-50339-4. 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.