Home LiteratureArticle Details
PMID: 16223757 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The neurotransmitters glycine and GABA stimulate glucagon-like peptide-1 release from the GLUTag cell line.

The Journal of physiology ·Vol. 569 ·No. Pt 3 ·2005-12-15 ·Pages 761-72

Gameiro A, Reimann F, Habib AM, O'Malley D, Williams L, Simpson AK, Gribble FM

Abstract

The incretin hormone, glucagon-like peptide-1 (GLP-1) is released from intestinal L-cells following food ingestion. Its secretion is triggered by a range of nutrients, including fats, carbohydrates and proteins. We reported previously that Na(+)-dependent glutamine uptake triggered electrical activity and GLP-1 release from the L-cell model line GLUTag. However, whereas alanine also triggered membrane depolarization and GLP-1 secretion, the response was Na+ independent. A range of alanine analogues, including d-alanine, beta-alanine, glycine and l-serine, but not d-serine, triggered similar depolarizing currents and elevation of intracellular [Ca2+], a sensitivity profile suggesting the involvement of glycine receptors. In support of this idea, glycine-induced currents and GLP-1 release were blocked by strychnine, and currents showed a 58.5 mV shift in reversal potential per 10-fold change in [Cl-], consistent with the activation of a Cl(-)-selective current. GABA, an agonist of related Cl- channels, also triggered Cl- currents and secretion, which were sensitive to picrotoxin. GABA-triggered [Ca2+]i increments were abolished by bicuculline and partially impaired by (1,2,5,6-tetrahydropyridine-4-yl)methylphosphinic acid (TPMPA), suggesting the involvement of both GABA(A) and GABA(C) receptors. Expression of GABA(A), GABA(C) and glycine receptor subunits was confirmed by RT-PCR. Glycine-triggered GLP-1 secretion was impaired by bumetanide but not bendrofluazide, suggesting that a high intracellular [Cl-] maintained by Na(+)-K(+)-2Cl- cotransporters is necessary for the depolarizing response to glycine receptor ligands. Our results suggest that GABA and glycine stimulate electrical activity and GLP-1 release from GLUTag cells by ligand-gated ion channel activation, a mechanism that might be important in responses to endogenous ligands from the enteric nervous system or dietary sources.

MeSH Terms
Action Potentials/drug effects Animals Calcium/metabolism Cell Line, Tumor Chlorides/metabolism Dose-Response Relationship, Drug GABA Antagonists/pharmacology Glucagon-Like Peptide 1/metabolism Glycine/pharmacology Ion Channel Gating/drug effects Mice Neurotransmitter Agents/pharmacology RNA, Messenger/metabolism Receptors, GABA/drug effects,genetics,metabolism Receptors, GABA-A/drug effects,genetics,metabolism Receptors, Glycine/drug effects,genetics,metabolism Sodium Potassium Chloride Symporter Inhibitors/pharmacology Sodium-Potassium-Chloride Symporters/drug effects,metabolism Strychnine/pharmacology gamma-Aminobutyric Acid/pharmacology
Chemicals
Chlorides GABA Antagonists GABA-C receptor Neurotransmitter Agents RNA, Messenger Receptors, GABA Receptors, GABA-A Receptors, Glycine Sodium Potassium Chloride Symporter Inhibitors Sodium-Potassium-Chloride Symporters gamma-Aminobutyric Acid Glucagon-Like Peptide 1 Strychnine Calcium Glycine
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Gameiro A
Wellcome Trust/MRC Building, Addenbrooke's Hospital, Hills Road, Cambridge CB2 2XY, UK.
Reimann F
Habib A M
O'Malley D
Williams L
Simpson A K
Gribble F M
References (38)
38 references, click to expand
  1. Role of the vagus nerve in mediating proximal nutrient-induced glucagon-like peptide-1 secretion.
    Endocrinology. 1999 Apr;140(4):1687-94 PMID: 10098504
  2. Ionotropic GABA receptors with mixed pharmacological properties of GABAA and GABAC receptors.
    Eur J Pharmacol. 2004 Aug 23;497(2):139-46 PMID: 15306198
  3. Distribution and immunocytochemical colocalization of peptide YY and enteroglucagon in endocrine cells of the rabbit colon.
    Endocrinology. 1991 Jul;129(1):139-48 PMID: 1675986
  4. Glycine activates myenteric neurones in adult guinea-pigs.
    J Physiol. 2001 Nov 1;536(Pt 3):727-39 PMID: 11691868
  5. Regulation of glucagon-like peptide-1 synthesis and secretion in the GLUTag enteroendocrine cell line.
    Endocrinology. 1998 Oct;139(10):4108-14 PMID: 9751489
  6. The Na-K-Cl cotransporters.
    Am J Physiol. 1994 Oct;267(4 Pt 1):C869-85 PMID: 7943281
  7. Activation of glycine and glutamate receptors increases intracellular calcium in cells derived from the endocrine pancreas.
    Mol Pharmacol. 1998 Oct;54(4):639-46 PMID: 9765506
  8. Glucose-sensing in glucagon-like peptide-1-secreting cells.
    Diabetes. 2002 Sep;51(9):2757-63 PMID: 12196469
  9. GLP-1: target for a new class of antidiabetic agents?
    J R Soc Med. 2004 Jun;97(6):270-4 PMID: 15173327
  10. Expression of functional GABAA receptors in cholecystokinin-secreting gut neuroendocrine murine STC-1 cells.
    J Physiol. 1998 Aug 1;510 ( Pt 3):805-14 PMID: 9660895
  11. GABA(C) receptors in neuroendocrine gut cells: a new GABA-binding site in the gut.
    Pflugers Arch. 2000 Dec;441(2-3):294-300 PMID: 11211116
  12. Evidence for inhibition mediated by coassembly of GABAA and GABAC receptor subunits in native central neurons.
    J Neurosci. 2004 Aug 18;24(33):7241-50 PMID: 15317850
  13. Glucagon-like peptide-1 and glucose-dependent insulin-releasing polypeptide plasma levels in response to nutrients.
    Digestion. 1995;56(2):117-26 PMID: 7750665
  14. Glucagon-like peptide-1 cells in the gastrointestinal tract and pancreas of rat, pig and man.
    Eur J Clin Invest. 1992 Apr;22(4):283-91 PMID: 1499644
  15. Activation of proglucagon gene transcription by protein kinase-A in a novel mouse enteroendocrine cell line.
    Mol Endocrinol. 1994 Dec;8(12):1646-55 PMID: 7535893
  16. Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones.
    J Physiol. 1987 Apr;385:243-86 PMID: 2443667
  17. A novel glucose-sensing mechanism contributing to glucagon-like peptide-1 secretion from the GLUTag cell line.
    Diabetes. 2003 May;52(5):1147-54 PMID: 12716745
  18. Regulation of glucagon-like peptide-1 secretion from rat ileum by neurotransmitters and peptides.
    J Endocrinol. 1995 Oct;147(1):25-31 PMID: 7490533
  19. Asymmetric cross-inhibition between GABAA and glycine receptors in rat spinal dorsal horn neurons.
    J Biol Chem. 2003 Oct 3;278(40):38637-45 PMID: 12885784
  20. GABA in the Mammalian Enteric Nervous System.
    News Physiol Sci. 2000 Dec;15:284-290 PMID: 11390928
  21. Is there more to GABA than synaptic inhibition?
    Nat Rev Neurosci. 2002 Sep;3(9):715-27 PMID: 12209120
  22. [3H]GABA uptake and GABA localization in mucosal endocrine cells of the rat stomach and colon.
    J Auton Nerv Syst. 1994 May;47(3):225-32 PMID: 8014381
  23. Gut hormones and the control of appetite.
    Trends Endocrinol Metab. 2004 Aug;15(6):259-63 PMID: 15358278
  24. Characterization and functional role of voltage gated cation conductances in the glucagon-like peptide-1 secreting GLUTag cell line.
    J Physiol. 2005 Feb 15;563(Pt 1):161-75 PMID: 15611035
  25. The glucagon-like peptides.
    Endocr Rev. 1999 Dec;20(6):876-913 PMID: 10605628
  26. Glucagon-like peptide-1: regulation of insulin secretion and therapeutic potential.
    Basic Clin Pharmacol Toxicol. 2004 Dec;95(6):252-62 PMID: 15569269
  27. A novel domain of the inhibitory glycine receptor determining antagonist efficacies: further evidence for partial agonism resulting from self-inhibition.
    Mol Pharmacol. 1999 Sep;56(3):464-72 PMID: 10462533
  28. A new generation of Ca2+ indicators with greatly improved fluorescence properties.
    J Biol Chem. 1985 Mar 25;260(6):3440-50 PMID: 3838314
  29. Ligand-gated ion channels in the enteric nervous system.
    Neurogastroenterol Motil. 2002 Dec;14(6):611-23 PMID: 12464083
  30. Minireview: Glucagon-like peptides regulate cell proliferation and apoptosis in the pancreas, gut, and central nervous system.
    Endocrinology. 2004 Jun;145(6):2653-9 PMID: 15044356
  31. GABAC receptor ion channels.
    Clin Exp Pharmacol Physiol. 2004 Nov;31(11):800-4 PMID: 15566397
  32. Biological actions and therapeutic potential of the glucagon-like peptides.
    Gastroenterology. 2002 Feb;122(2):531-44 PMID: 11832466
  33. The metabolic response to ingested glycine.
    Am J Clin Nutr. 2002 Dec;76(6):1302-7 PMID: 12450897
  34. Glutamine potently stimulates glucagon-like peptide-1 secretion from GLUTag cells.
    Diabetologia. 2004 Sep;47(9):1592-601 PMID: 15365617
  35. The atypical M2 segment of the beta subunit confers picrotoxinin resistance to inhibitory glycine receptor channels.
    EMBO J. 1992 Dec;11(12):4305-11 PMID: 1385113
  36. Molecular structure and function of the glycine receptor chloride channel.
    Physiol Rev. 2004 Oct;84(4):1051-95 PMID: 15383648
  37. Glycine supply to human enterocytes mediated by high-affinity basolateral GLYT1.
    Gastroenterology. 2001 Feb;120(2):439-48 PMID: 11159884
  38. Therapy of type 2 diabetes mellitus based on the actions of glucagon-like peptide-1.
    Diabetes Metab Res Rev. 2002 Nov-Dec;18(6):430-41 PMID: 12469357
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
2005-12-15
Epub
2005-00-13
Pages
761-72
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1464262
Subset
IM
Grants
Wellcome Trust · 071187 · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com