Abstract
The extracellular calcium (Ca(2+)(o))-sensing receptor (CaR) recognizes and responds to (i.e., "senses") Ca(2+)(o) as its principal physiological ligand. In the present studies, we document that the CaR is activated not only by extracellular calcium ions but also by amino acids, establishing its capacity to sense nutrients of two totally different classes. l-Amino acids, especially aromatic amino acids, including l-phenylalanine and l-tryptophan, stereoselectively mobilized Ca(2+) ions in the presence of the CaR agonists, Ca(2+)(o), gadolinium (Gd(3+)(o)), and spermine in fura-2-loaded human embryonic kidney (HEK-293) cells stably transfected with the human CaR. l-amino acid-dependent effects were observed above, but not below, a threshold level of Ca(2+)(o) of approximately 1.0 mM. l-Amino acids, particularly aromatic amino acids, also stereoselectively enhanced the sensitivity of the CaR to its agonists, Ca(2+)(o) and spermine. Branched-chain amino acids were almost inactive, and charged amino acids, including arginine and lysine, were much less effective than aromatic and other amino acids. l-amino acid mixtures emulating the amino acid composition of fasting human plasma reproduced the effects of high concentrations of individual l-amino acids on Ca(2+) mobilization and enhanced the sensitivity of the CaR to Ca(2+)(o). The data presented herein identify the CaR as a molecular target for aromatic and other l-amino acids. Thus, the CaR can integrate signals arising from distinct classes of nutrients: mineral ions and amino acids. The actions of l-amino acids on the CaR may provide explanations for several long recognized but poorly understood actions of dietary protein on calcium metabolism.
MeSH Terms
Amino Acids/pharmacology,physiology
Calcium/pharmacology,physiology
Cell Line
Cloning, Molecular
Fura-2
Gadolinium/pharmacology
Humans
Kidney
Kinetics
Phenylalanine/pharmacology
Receptors, Calcium-Sensing
Receptors, Cell Surface/drug effects,genetics,physiology
Recombinant Proteins/drug effects,metabolism
Spermine/pharmacology
Tryptophan/pharmacology
Chemicals
Amino Acids
Receptors, Calcium-Sensing
Receptors, Cell Surface
Recombinant Proteins
Spermine
Phenylalanine
Tryptophan
Gadolinium
Calcium
Fura-2
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Conigrave A D
Endocrine-Hypertension Division, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA 02115, USA. a.conigrave@biochem.usyd.edu.au
Quinn S J
Brown E M
References (29)
29 references, click to expand
-
Effect of level of protein intake on urinary and fecal calcium and calcium retention of young adult males.
J Nutr. 1970 Dec;100(12):1425-30
PMID: 5481677
-
Comparison of D- and L-phenylalanine as pancreatic stimulants.
Am J Physiol. 1972 Apr;222(4):1058-63
PMID: 5027085
-
D- and L-isomers of serine and alanine equally effective as releasers of gastrin.
Experientia. 1972 Nov 15;28(11):1306-7
PMID: 4638897
-
Protein digestion in human intestine as reflected in luminal, mucosal, and plasma amino acid concentrations after meals.
J Clin Invest. 1973 Jul;52(7):1586-94
PMID: 4718954
-
Intravenous infusion of amino acids stimulates gastric acid secretion in man.
N Engl J Med. 1978 Jan 5;298(1):27-9
PMID: 618447
-
Stimulation of gastrin release in dogs by individual amino acids.
Proc Soc Exp Biol Med. 1978 Mar;157(3):440-1
PMID: 634985
-
Comparison of intravenous amino acids in the stimulation of gastric secretion.
Gastroenterology. 1978 Nov;75(5):817-24
PMID: 700324
-
Protein-induced hypercalciuria: a longer term study.
Am J Clin Nutr. 1979 Apr;32(4):741-9
PMID: 433806
-
Liver extract and its free amino acids equally stimulate gastric acid secretion.
Am J Physiol. 1980 Dec;239(6):G493-6
PMID: 7446742
-
Intravenous infusion of L-isomers of phenylalanine and tryptophan stimulate gastric acid secretion at physiologic plasma concentrations in normal subjects and after parietal cell vagotomy.
J Clin Invest. 1983 May;71(5):1254-62
PMID: 6853713
-
Calcium response of single adrenal glomerulosa cells to external potassium.
Am J Physiol. 1988 Oct;255(4 Pt 1):E488-95
PMID: 3177635
-
The ligand-binding domain in metabotropic glutamate receptors is related to bacterial periplasmic binding proteins.
Neuron. 1993 Jul;11(1):41-52
PMID: 8338667
-
Cloning and characterization of an extracellular Ca(2+)-sensing receptor from bovine parathyroid.
Nature. 1993 Dec 9;366(6455):575-80
PMID: 8255296
-
A cloned extracellular Ca(2+)-sensing receptor: molecular mediator of the actions of extracellular Ca2+ on parathyroid and kidney cells?
Kidney Int. 1996 Apr;49(4):1042-6
PMID: 8691723
-
Expression of the calcium-sensing receptor on human antral gastrin cells in culture.
J Clin Invest. 1997 May 15;99(10):2328-33
PMID: 9153273
-
Effect of a protein-rich meal on urinary and salivary free amino acid concentrations in human subjects.
Clin Chim Acta. 1997 Aug 8;264(1):37-47
PMID: 9267701
-
Ca2+-sensing receptors in intestinal epithelium.
Am J Physiol. 1997 Oct;273(4 Pt 1):C1168-75
PMID: 9357760
-
Increased circulating concentrations of parathyroid hormone in healthy, young women consuming a protein-restricted diet.
Am J Clin Nutr. 1997 Nov;66(5):1188-96
PMID: 9356538
-
HEK293 human embryonic kidney cells endogenously express the P2Y1 and P2Y2 receptors.
Neuropharmacology. 1997 Sep;36(9):1181-7
PMID: 9364473
-
Identification and localization of extracellular Ca(2+)-sensing receptor in rat intestine.
Am J Physiol. 1998 Jan;274(1 Pt 1):G122-30
PMID: 9458781
-
Structural basis for a Ca2+-sensing function of the metabotropic glutamate receptors.
Science. 1998 Mar 13;279(5357):1722-5
PMID: 9497291
-
Calcimimetics with potent and selective activity on the parathyroid calcium receptor.
Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):4040-5
PMID: 9520489
-
Cholecystokinin- and secretin-releasing peptides in the intestine--a new regulatory interendocrine mechanism in the gastrointestinal tract.
Regul Pept. 1998 Feb 2;73(2):89-94
PMID: 9533812
-
Sodium and ionic strength sensing by the calcium receptor.
J Biol Chem. 1998 Jul 31;273(31):19579-86
PMID: 9677383
-
Extracellular calcium-sensing receptor in rat oligodendrocytes: expression and potential role in regulation of cellular proliferation and an outward K+ channel.
Glia. 1998 Dec;24(4):449-58
PMID: 9814825
-
Expression of an extracellular calcium-sensing receptor in rat stomach.
Gastroenterology. 1999 Jan;116(1):118-26
PMID: 9869609
-
RhoA-sensitive trafficking of muscarinic acetylcholine receptors.
J Pharmacol Exp Ther. 1999 Jan;288(1):36-42
PMID: 9862750
-
Molecular and functional identification of a Ca2+ (polyvalent cation)-sensing receptor in rat pancreas.
J Biol Chem. 1999 Jul 16;274(29):20561-8
PMID: 10400686
-
Physiological determination of release of secretin and pancreozymin from intestine of dogs with transplanted pancreas.
Am J Physiol. 1951 Feb;164(2):527-45
PMID: 14810962