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Research ArticleGastrointestinal, Hepatic, Pulmonary, and Renal

Umami Receptor Activation Increases Duodenal Bicarbonate Secretion via Glucagon-Like Peptide-2 Release in Rats

Joon-Ho Wang, Takuya Inoue, Masaaki Higashiyama, Paul H. Guth, Eli Engel, Jonathan D. Kaunitz and Yasutada Akiba
Journal of Pharmacology and Experimental Therapeutics November 2011, 339 (2) 464-473; DOI: https://doi.org/10.1124/jpet.111.184788
Joon-Ho Wang
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Takuya Inoue
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Masaaki Higashiyama
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Paul H. Guth
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Eli Engel
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Jonathan D. Kaunitz
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Yasutada Akiba
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Abstract

Luminal nutrient chemosensing during meal ingestion is mediated by intestinal endocrine cells, which regulate secretion and motility via the release of gut hormones. We have reported that luminal coperfusion of l-Glu and IMP, common condiments providing the umami or proteinaceous taste, synergistically increases duodenal bicarbonate secretion (DBS) possibly via taste receptor heterodimers, taste receptor type 1, member 1 (T1R1)/R3. We hypothesized that glucose-dependent insulinotropic peptide (GIP) or glucagon-like peptide (GLP) is released by duodenal perfusion with l-Glu/IMP. We measured DBS with pH and CO2 electrodes through a perfused rat duodenal loop in vivo. GIP, exendin (Ex)-4 (GLP-1 receptor agonist), or GLP-2 was intravenously infused (0.01–1 nmol/kg/h). l-Glu (10 mM) and IMP (0.1 mM) were luminally perfused with or without bolus intravenous injection (3 or 30 nmol/kg) of the receptor antagonists Pro3GIP, Ex-3(9-39), or GLP-2(3-33). GIP or GLP-2 infusion dose-dependently increased DBS, whereas Ex-4 infusion gradually decreased DBS. Luminal perfusion of l-Glu/IMP increased DBS, with no effect of Pro3GIP or Ex-3(9-39), whereas GLP-2(3-33) inhibited l-Glu/IMP-induced DBS. Vasoactive intestinal peptide (VIP)(6–28) intravenously or NG-nitro-l-arginine methyl ester coperfusion inhibited the effect of l-Glu/IMP. Perfusion of l-Glu/IMP increased portal venous concentrations of GLP-2, followed by a delayed increase of GLP-1, with no effect on GIP release. GLP-1/2 and T1R1/R3 were expressed in duodenal endocrine-like cells. These results suggest that luminal l-Glu/IMP-induced DBS is mediated via GLP-2 release and receptor activation followed by VIP and nitric oxide release. Because GLP-1 is insulinotropic and GLP-2 is intestinotrophic, umami receptor activation may have additional benefits in glucose metabolism and duodenal mucosal protection and regeneration.

Footnotes

  • This work was supported by a research grant from Ajinomoto, Inc. (Tokyo, Japan) (to Y.A.); a Department of Veterans Affairs Merit Review Award (to J.D.K.); the National Institutes of Health National Institute of Diabetes and Digestive and Kidney Diseases [Grant R01-DK54221] (to J.D.K.); and the Animal Core of the National Institutes of Health National Institute of Diabetes and Digestive and Kidney Diseases [Grant P30-DK0413] (to J. E. Rozengurt).

  • Article, publication date, and citation information can be found at http://jpet.aspetjournals.org.

    doi:10.1124/jpet.111.184788.

  • ABBREVIATIONS:

    DBS
    duodenal bicarbonate secretion
    Ex
    exendin
    GIP
    glucose-dependent insulinotropic peptide
    GIP-R
    GIP receptor
    GLP
    glucagon-like peptide
    GLP-1R
    GLP-1 receptor
    GLP-2R
    GLP-2 receptor
    l-NAME
    NG-nitro-l-arginine methyl ester
    NO
    nitric oxide
    NVP DPP 728
    6-[[2-[[2-(2S)-2-cyano-1-pyrrolidinyl]-2-oxoethyl]amino]ethyl]amino-3-pyridinecarbononitrile
    PV
    portal vein
    T1R
    taste receptor type 1
    VIP
    vasoactive intestinal peptide
    VIP-R
    VIP receptor
    BSA
    bovine serum albumin
    COX
    cyclooxygenase
    EIA
    enzyme immunoassay
    PG
    prostaglandin.

  • Received June 6, 2011.
  • Accepted August 15, 2011.
  • U.S. Government work not protected by U.S. copyright
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Journal of Pharmacology and Experimental Therapeutics: 339 (2)
Journal of Pharmacology and Experimental Therapeutics
Vol. 339, Issue 2
1 Nov 2011
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Research ArticleGastrointestinal, Hepatic, Pulmonary, and Renal

GLP-2-Induced Duodenal HCO3− Secretion

Joon-Ho Wang, Takuya Inoue, Masaaki Higashiyama, Paul H. Guth, Eli Engel, Jonathan D. Kaunitz and Yasutada Akiba
Journal of Pharmacology and Experimental Therapeutics November 1, 2011, 339 (2) 464-473; DOI: https://doi.org/10.1124/jpet.111.184788

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Research ArticleGastrointestinal, Hepatic, Pulmonary, and Renal

GLP-2-Induced Duodenal HCO3− Secretion

Joon-Ho Wang, Takuya Inoue, Masaaki Higashiyama, Paul H. Guth, Eli Engel, Jonathan D. Kaunitz and Yasutada Akiba
Journal of Pharmacology and Experimental Therapeutics November 1, 2011, 339 (2) 464-473; DOI: https://doi.org/10.1124/jpet.111.184788
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