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10.3390/cells10123305
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Article

Endocannabinoid Anandamide Attenuates Acute Respiratory Distress Syndrome through Modulation of Microbiome in the Gut-Lung Axis

by
Muthanna Sultan
1,
Kiesha Wilson
1,
Osama A. Abdulla
1,
Philip Brandon Busbee
1,
Alina Hall
1,
Taylor Carter
1,
Narendra Singh
1,
Saurabh Chatterjee
2,
Prakash Nagarkatti
1 and
Mitzi Nagarkatti
1,*
1
Department of Pathology, Microbiology and Immunology, School of Medicine, University of South Carolina School of Medicine, Columbia, SC 29209, USA
2
Environmental Health and Disease Laboratory, Arnold School of Public Health, University of South Carolina, Columbia, SC 29208, USA
*
Author to whom correspondence should be addressed.
Cells 2021, 10(12), 3305; https://doi.org/10.3390/cells10123305
Submission received: 7 September 2021 / Revised: 8 November 2021 / Accepted: 17 November 2021 / Published: 25 November 2021
(This article belongs to the Special Issue Exploring the Molecular Functionality of Microbiome-Immune System Interaction)
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Abstract

Acute respiratory distress syndrome (ARDS) is a serious lung condition characterized by severe hypoxemia leading to limitations of oxygen needed for lung function. In this study, we investigated the effect of anandamide (AEA), an endogenous cannabinoid, on Staphylococcal enterotoxin B (SEB)-mediated ARDS in female mice. Single-cell RNA sequencing data showed that the lung epithelial cells from AEA-treated mice showed increased levels of antimicrobial peptides (AMPs) and tight junction proteins. MiSeq sequencing data on 16S RNA and LEfSe analysis demonstrated that SEB caused significant alterations in the microbiota, with increases in pathogenic bacteria in both the lungs and the gut, while treatment with AEA reversed this effect and induced beneficial bacteria. AEA treatment suppressed inflammation both in the lungs as well as gut-associated mesenteric lymph nodes (MLNs). AEA triggered several bacterial species that produced increased levels of short-chain fatty acids (SCFAs), including butyrate. Furthermore, administration of butyrate alone could attenuate SEB-mediated ARDS. Taken together, our data indicate that AEA treatment attenuates SEB-mediated ARDS by suppressing inflammation and preventing dysbiosis, both in the lungs and the gut, through the induction of AMPs, tight junction proteins, and SCFAs that stabilize the gut-lung microbial axis driving immune homeostasis.
Keywords: acute respiratory distress syndrome (ARDS); Staphylococcus enterotoxin B (SEB); anandamide (AEA); COVID-19; microbiome; MiSeq sequencing; gut-lung axis; antimicrobial peptides (AMPs); single-cell RNA (Sc-RNA); short-chain fatty acids (SCFAs) acute respiratory distress syndrome (ARDS); Staphylococcus enterotoxin B (SEB); anandamide (AEA); COVID-19; microbiome; MiSeq sequencing; gut-lung axis; antimicrobial peptides (AMPs); single-cell RNA (Sc-RNA); short-chain fatty acids (SCFAs)
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MDPI and ACS Style

Sultan, M.; Wilson, K.; Abdulla, O.A.; Busbee, P.B.; Hall, A.; Carter, T.; Singh, N.; Chatterjee, S.; Nagarkatti, P.; Nagarkatti, M. Endocannabinoid Anandamide Attenuates Acute Respiratory Distress Syndrome through Modulation of Microbiome in the Gut-Lung Axis. Cells 2021, 10, 3305. https://doi.org/10.3390/cells10123305

AMA Style

Sultan M, Wilson K, Abdulla OA, Busbee PB, Hall A, Carter T, Singh N, Chatterjee S, Nagarkatti P, Nagarkatti M. Endocannabinoid Anandamide Attenuates Acute Respiratory Distress Syndrome through Modulation of Microbiome in the Gut-Lung Axis. Cells. 2021; 10(12):3305. https://doi.org/10.3390/cells10123305

Chicago/Turabian Style

Sultan, Muthanna, Kiesha Wilson, Osama A. Abdulla, Philip Brandon Busbee, Alina Hall, Taylor Carter, Narendra Singh, Saurabh Chatterjee, Prakash Nagarkatti, and Mitzi Nagarkatti. 2021. "Endocannabinoid Anandamide Attenuates Acute Respiratory Distress Syndrome through Modulation of Microbiome in the Gut-Lung Axis" Cells 10, no. 12: 3305. https://doi.org/10.3390/cells10123305

APA Style

Sultan, M., Wilson, K., Abdulla, O. A., Busbee, P. B., Hall, A., Carter, T., Singh, N., Chatterjee, S., Nagarkatti, P., & Nagarkatti, M. (2021). Endocannabinoid Anandamide Attenuates Acute Respiratory Distress Syndrome through Modulation of Microbiome in the Gut-Lung Axis. Cells, 10(12), 3305. https://doi.org/10.3390/cells10123305

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