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Research Article

Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation

Jennifer L. Pluznick, Ryan J. Protzko, Haykanush Gevorgyan, Zita Peterlin, Arnold Sipos, Jinah Han, Isabelle Brunet, La-Xiang Wan, Federico Rey, Tong Wang, Stuart J. Firestein, Masashi Yanagisawa, Jeffrey I. Gordon, Anne Eichmann, Janos Peti-Peterdi, and Michael J. Caplan
PNAS March 12, 2013 110 (11) 4410-4415; https://doi.org/10.1073/pnas.1215927110
Jennifer L. Pluznick
aDepartment of Physiology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205;
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  • For correspondence: jpluznick@jhmi.edu
Ryan J. Protzko
aDepartment of Physiology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205;
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Haykanush Gevorgyan
bDepartments of Physiology and Biophysics and Medicine, University of Southern California, Los Angeles, CA 90033;
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Zita Peterlin
cDepartment of Biological Sciences, Columbia University, New York, NY 10027;
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Arnold Sipos
bDepartments of Physiology and Biophysics and Medicine, University of Southern California, Los Angeles, CA 90033;
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Jinah Han
dDepartment of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520;
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Isabelle Brunet
eCenter for Interdisciplinary Research in Biology, College de France, 75231 Paris, France;
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La-Xiang Wan
fDepartment of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT 06520;
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Federico Rey
gCenter for Genome Sciences and Systems Biology, Washington University School of Medicine, St. Louis, MO 63108; and
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Tong Wang
fDepartment of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT 06520;
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Stuart J. Firestein
cDepartment of Biological Sciences, Columbia University, New York, NY 10027;
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Masashi Yanagisawa
hHoward Hughes Medical Institute, and
iDepartment of Molecular Genetics, University of Texas Southwestern Medical Center, Dallas, TX 75390
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Jeffrey I. Gordon
gCenter for Genome Sciences and Systems Biology, Washington University School of Medicine, St. Louis, MO 63108; and
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Anne Eichmann
dDepartment of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520;
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Janos Peti-Peterdi
bDepartments of Physiology and Biophysics and Medicine, University of Southern California, Los Angeles, CA 90033;
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Michael J. Caplan
fDepartment of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT 06520;
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  1. Edited* by Gerhard Giebisch, Yale University School of Medicine, New Haven, CT, and approved January 4, 2013 (received for review October 2, 2012)

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Abstract

Olfactory receptors are G protein-coupled receptors that mediate olfactory chemosensation and serve as chemosensors in other tissues. We find that Olfr78, an olfactory receptor expressed in the kidney, responds to short chain fatty acids (SCFAs). Olfr78 is expressed in the renal juxtaglomerular apparatus, where it mediates renin secretion in response to SCFAs. In addition, both Olfr78 and G protein-coupled receptor 41 (Gpr41), another SCFA receptor, are expressed in smooth muscle cells of small resistance vessels. Propionate, a SCFA shown to induce vasodilation ex vivo, produces an acute hypotensive response in wild-type mice. This effect is differentially modulated by disruption of Olfr78 and Gpr41 expression. SCFAs are end products of fermentation by the gut microbiota and are absorbed into the circulation. Antibiotic treatment reduces the biomass of the gut microbiota and elevates blood pressure in Olfr78 knockout mice. We conclude that SCFAs produced by the gut microbiota modulate blood pressure via Olfr78 and Gpr41.

  • GPCR
  • MOL2.3
  • MOR18-2
  • OR51E2

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: jpluznick{at}jhmi.edu.
  • Author contributions: J.L.P., J.P.-P., and M.J.C. designed research; J.L.P., R.J.P., H.G., Z.P., A.S., J.H., I.B., L.-X.W., F.R., T.W., and J.P.-P. performed research; M.Y. and J.I.G. contributed new reagents/analytic tools; J.L.P., R.J.P., H.G., Z.P., A.S., I.B., F.R., S.J.F., J.I.G., A.E., and M.J.C. analyzed data; and J.L.P. and M.J.C. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1215927110/-/DCSupplemental.

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SCFA-sensing olfactory GPCR induces renin release
Jennifer L. Pluznick, Ryan J. Protzko, Haykanush Gevorgyan, Zita Peterlin, Arnold Sipos, Jinah Han, Isabelle Brunet, La-Xiang Wan, Federico Rey, Tong Wang, Stuart J. Firestein, Masashi Yanagisawa, Jeffrey I. Gordon, Anne Eichmann, Janos Peti-Peterdi, Michael J. Caplan
Proceedings of the National Academy of Sciences Mar 2013, 110 (11) 4410-4415; DOI: 10.1073/pnas.1215927110

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SCFA-sensing olfactory GPCR induces renin release
Jennifer L. Pluznick, Ryan J. Protzko, Haykanush Gevorgyan, Zita Peterlin, Arnold Sipos, Jinah Han, Isabelle Brunet, La-Xiang Wan, Federico Rey, Tong Wang, Stuart J. Firestein, Masashi Yanagisawa, Jeffrey I. Gordon, Anne Eichmann, Janos Peti-Peterdi, Michael J. Caplan
Proceedings of the National Academy of Sciences Mar 2013, 110 (11) 4410-4415; DOI: 10.1073/pnas.1215927110
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