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Oral NaHCO3 Activates a Splenic Anti-Inflammatory Pathway: Evidence That Cholinergic Signals Are Transmitted via Mesothelial Cells

Sarah C. Ray, Babak Baban, Matthew A. Tucker, Alec J. Seaton, Kyu Chul Chang, Elinor C. Mannon, Jingping Sun, Bansari Patel, Katie Wilson, Jacqueline B. Musall, Hiram Ocasio, Debra Irsik, Jessica A. Filosa, Jennifer C. Sullivan, Brendan Marshall, Ryan A. Harris and Paul M. O’Connor
J Immunol April 16, 2018, ji1701605; DOI: https://doi.org/10.4049/jimmunol.1701605
Sarah C. Ray
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Babak Baban
†Department of Oral Biology, Augusta University, Augusta, GA 30912;
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Matthew A. Tucker
‡Georgia Prevention Institute, Augusta University, Augusta, GA 30912; and
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Alec J. Seaton
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Kyu Chul Chang
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Elinor C. Mannon
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Jingping Sun
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Bansari Patel
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Katie Wilson
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Jacqueline B. Musall
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Hiram Ocasio
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Debra Irsik
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Jessica A. Filosa
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Jennifer C. Sullivan
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Brendan Marshall
§Department of Cell Biology and Anatomy, Augusta University, Augusta, GA 30912
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Ryan A. Harris
‡Georgia Prevention Institute, Augusta University, Augusta, GA 30912; and
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Paul M. O’Connor
*Department of Physiology, Augusta University, Augusta, GA 30912;
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Abstract

We tested the hypothesis that oral NaHCO3 intake stimulates splenic anti-inflammatory pathways. Following oral NaHCO3 loading, macrophage polarization was shifted from predominantly M1 (inflammatory) to M2 (regulatory) phenotypes, and FOXP3+CD4+ T-lymphocytes increased in the spleen, blood, and kidneys of rats. Similar anti-inflammatory changes in macrophage polarization were observed in the blood of human subjects following NaHCO3 ingestion. Surprisingly, we found that gentle manipulation to visualize the spleen at midline during surgical laparotomy (sham splenectomy) was sufficient to abolish the response in rats and resulted in hypertrophy/hyperplasia of the capsular mesothelial cells. Thin collagenous connections lined by mesothelial cells were found to connect to the capsular mesothelium. Mesothelial cells in these connections stained positive for the pan-neuronal marker PGP9.5 and acetylcholine esterase and contained many ultrastructural elements, which visually resembled neuronal structures. Both disruption of the fragile mesothelial connections or transection of the vagal nerves resulted in the loss of capsular mesothelial acetylcholine esterase staining and reduced splenic mass. Our data indicate that oral NaHCO3 activates a splenic anti-inflammatory pathway and provides evidence that the signals that mediate this response are transmitted to the spleen via a novel neuronal-like function of mesothelial cells.

Footnotes

  • This work was supported by National Institutes of Health Grants DK099548 and 1P01HL134604 (to P.M.O.).

  • The online version of this article contains supplemental material.

  • Received November 21, 2017.
  • Accepted March 10, 2018.
  • Copyright © 2018 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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Oral NaHCO3 Activates a Splenic Anti-Inflammatory Pathway: Evidence That Cholinergic Signals Are Transmitted via Mesothelial Cells
Sarah C. Ray, Babak Baban, Matthew A. Tucker, Alec J. Seaton, Kyu Chul Chang, Elinor C. Mannon, Jingping Sun, Bansari Patel, Katie Wilson, Jacqueline B. Musall, Hiram Ocasio, Debra Irsik, Jessica A. Filosa, Jennifer C. Sullivan, Brendan Marshall, Ryan A. Harris, Paul M. O’Connor
The Journal of Immunology April 16, 2018, ji1701605; DOI: 10.4049/jimmunol.1701605

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Oral NaHCO3 Activates a Splenic Anti-Inflammatory Pathway: Evidence That Cholinergic Signals Are Transmitted via Mesothelial Cells
Sarah C. Ray, Babak Baban, Matthew A. Tucker, Alec J. Seaton, Kyu Chul Chang, Elinor C. Mannon, Jingping Sun, Bansari Patel, Katie Wilson, Jacqueline B. Musall, Hiram Ocasio, Debra Irsik, Jessica A. Filosa, Jennifer C. Sullivan, Brendan Marshall, Ryan A. Harris, Paul M. O’Connor
The Journal of Immunology April 16, 2018, ji1701605; DOI: 10.4049/jimmunol.1701605
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Print ISSN 0022-1767        Online ISSN 1550-6606