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ResearchIn-Press PreviewCOVID-19Virology Open Access | 10.1172/jci.insight.160989

Markers of fungal translocation are elevated during post-acute sequelae of SARS-CoV-2 and induce NF-κB signaling

Leila B. Giron,1 Michael J. Peluso,2 Jianyi Ding,1 Grace Kenny,3 Netanel F. Zilberstein,4 Jane Koshy,1 Kai Ying Hong,1 Heather Rasmussen,5 Gregory E. Miller,6 Faraz Bishehsari,4 Robert A. Balk,4 James N. Moy,4 Rebecca Hoh,7 Scott Lu,7 Aaron R. Goldman,1 Hsin-Yao Tang,1 Brandon C. Yee,8 Ahmed Chenna,9 John W. Winslow,9 Christos J. Petropoulos,9 J. Daniel Kelly,7 Haimanot Wasse,4 Jeffrey N. Martin,7 Qin Liu,1 Ali Keshavarzian,10 Alan Landay,4 Steven G. Deeks,2 Timothy J. Henrich,7 and Mohamed Abdel-Mohsen1

1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

Find articles by Giron, L. in: JCI | PubMed | Google Scholar |

1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

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3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

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3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

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3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

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3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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1Vaccine and Immunotherapy Center, The Wistar Institute, Philadelphia, United States of America

2The University of California, San Francisco, San Francisco, United States of America

3Department of Infectious Diseases, University College Dublin, Dublin, Ireland

4Department of Internal Medicine, Rush University, Chicago, United States of America

5Department of Nutrition and Health Sciences, University of Nebraska–Lincoln, Lincoln, United States of America

6Department of Psychology, Northwestern University, Chicago, United States of America

7Department of Medicine, The University of California, San Francisco, San Francisco, United States of America

8Monogram Biosciences, South San Francisco, United States of America

9Oncology Group, Monogram Biosciences, South San Francisco, United States of America

10Department of Digestive Diseases, Rush University, Chicago, United States of America

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Published June 21, 2022 - More info

JCI Insight. https://doi.org/10.1172/jci.insight.160989.
Copyright © 2022, Giron et al. This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
Published June 21, 2022 - Version history
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Abstract

Long COVID, a type of Post-Acute Sequelae of SARS-CoV-2 (PASC), has been associated with sustained elevated levels of immune activation and inflammation. However, the mechanisms that drive this inflammation remain unknown. Inflammation during acute Coronavirus Disease 2019 could be exacerbated by microbial translocation (from gut and/or lung) to blood. Whether microbial translocation contributes to inflammation during PASC is unknown. We did not observe a significant elevation in plasma markers of bacterial translocation during PASC. However, we observed higher levels of fungal translocation – measured as β-glucan, a fungal cell wall polysaccharide – in the plasma of individuals experiencing PASC compared to those without PASC or SARS-CoV-2 negative controls. The higher β-glucan correlated with higher inflammation and elevated levels of host metabolites involved in activating N-Methyl-D-aspartate receptors (such as metabolites within the tryptophan catabolism pathway) with established neuro-toxic properties. Mechanistically, β-glucan can directly induce inflammation by binding to myeloid cells (via Dectin-1) and activating Syk/NF-κB signaling. Using a Dectin-1/NF-κB reporter model, we found that plasma from individuals experiencing PASC induced higher NF-κB signaling compared to plasma from negative controls. This higher NF-κB signaling was abrogated by Piceatannol (Syk inhibitor). These data suggest a potential targetable mechanism linking fungal translocation and inflammation during PASC.

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