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Endocrine Reviews 20 (6): 876-913
Copyright © 1999 by The Endocrine Society

The Glucagon-Like Peptides

Timothy James Kieffer1 and Joel Francis Habener2

Departments of Medicine and Physiology (T.J.K.), University of Alberta, Edmonton, Alberta, Canada T6G 2S2; and Laboratory of Molecular Endocrinology (J.F.H.), Massachusetts General Hospital, Howard Hughes Medical Institute, Harvard Medical School, Boston, Massachusetts 02114

I. Introduction
II. History of the Incretin Concept: Discovery of Gastric Inhibitory Polypeptide
III. Discovery of GLP-1
IV. Structures of GLPs and Family of Glucagon-Related Peptides
V. Tissue Distribution of the Expression of GLPs
A. Pancreatic {alpha}-cells
B. Intestinal L cells
C. Central nervous system
VI. Proglucagon Biosynthesis
A. Organization/structure of the proglucagon gene
B. Regulation of glucagon gene expression
C. Posttranslational processing of proglucagon
VII. Regulation of GLP Secretion
A. Overview
B. Intracellular signals
C. Carbohydrates
D. Fats
E. Proteins
F. Endocrine
G. Neural
H. GLP-2
VIII. Metabolism of GLPs
A. GLP-1
B. GLP-2
IX. Physiological Actions of GLPs
A. Overview
B. Pancreatic islets
C. Counterregulatory actions of GLP-1 and leptin on ß-cells
D. Stomach
E. Lung
F. Brain
G. Liver, skeletal muscle, and fat
H. Pituitary, hypothalamus, and thyroid
I. Cardiovascular system
J. GLP-2
X. GLP Receptors
A. Structure
B. Signaling
C. Distribution
D. Regulation
E. GLP-2
XI. Pathophysiology of GLP-1
XII. GLP-1 as a Potential Treatment for Diabetes Mellitus

XIII. Future Directions




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 Diabetes CareHome page
H. Harder, L. Nielsen, T. D.T. Thi, and A. Astrup
The Effect of Liraglutide, a Long-Acting Glucagon-Like Peptide 1 Derivative, on Glycemic Control, Body Composition, and 24-h Energy Expenditure in Patients With Type 2 Diabetes
Diabetes Care, August 1, 2004; 27(8): 1915 - 1921.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
B. K. C. Chow, T. W. Moon, R. L. C. Hoo, C.-M. Yeung, M. Muller, P. J. Christos, and S. Mojsov
Identification and Characterization of a Glucagon Receptor from the Goldfish Carassius auratus: Implications for the Evolution of the Ligand Specificity of Glucagon Receptors in Vertebrates
Endocrinology, July 1, 2004; 145(7): 3273 - 3288.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
D. Dardevet, M. C. Moore, D. Neal, C. A. DiCostanzo, W. Snead, and A. D. Cherrington
Insulin-independent effects of GLP-1 on canine liver glucose metabolism: duration of infusion and involvement of hepatoportal region
Am J Physiol Endocrinol Metab, July 1, 2004; 287(1): E75 - E81.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
J. F. List and J. F. Habener
Glucagon-like peptide 1 agonists and the development and growth of pancreatic {beta}-cells
Am J Physiol Endocrinol Metab, June 1, 2004; 286(6): E875 - E881.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
D. A. D'Alessio and T. P. Vahl
Glucagon-like peptide 1: evolution of an incretin into a treatment for diabetes
Am J Physiol Endocrinol Metab, June 1, 2004; 286(6): E882 - E890.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
S. Tomimoto, H. Hashimoto, N. Shintani, K. Yamamoto, Y. Kawabata, K.-I. Hamagami, K. Yamagata, J.-I. Miyagawa, and A. Baba
Overexpression of Pituitary Adenylate Cyclase-Activating Polypeptide in Islets Inhibits Hyperinsulinemia and Islet Hyperplasia in Agouti Yellow Mice
J. Pharmacol. Exp. Ther., May 1, 2004; 309(2): 796 - 803.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
A. P. Goldstone, E. L. Thomas, A. E. Brynes, G. Castroman, R. Edwards, M. A. Ghatei, G. Frost, A. J. Holland, A. B. Grossman, M. Korbonits, et al.
Elevated Fasting Plasma Ghrelin in Prader-Willi Syndrome Adults Is Not Solely Explained by Their Reduced Visceral Adiposity and Insulin Resistance
J. Clin. Endocrinol. Metab., April 1, 2004; 89(4): 1718 - 1726.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. A. Hinke, S. Manhart, K. Kuhn-Wache, C. Nian, H.-U. Demuth, R. A. Pederson, and C. H. S. McIntosh
[Ser2]- and [Ser(P)2]Incretin Analogs: COMPARISON OF DIPEPTIDYL PEPTIDASE IV RESISTANCE AND BIOLOGICAL ACTIVITIES IN VITRO AND IN VIVO
J. Biol. Chem., February 6, 2004; 279(6): 3998 - 4006.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
G. G. Holz
Epac: A New cAMP-Binding Protein in Support of Glucagon-Like Peptide-1 Receptor-Mediated Signal Transduction in the Pancreatic {beta}-Cell
Diabetes, January 1, 2004; 53(1): 5 - 13.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
C. A. Leech and J. F. Habener
Regulation of Glucagon-Like Peptide-1 Receptor and Calcium-Sensing Receptor Signaling by L-Histidine
Endocrinology, November 1, 2003; 144(11): 4851 - 4858.
[Abstract] [Full Text] [PDF]

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 J. Nutr.Home page
D. Burrin, X. Guan, B. Stoll, Y. M. Petersen, and P. T. Sangild
Glucagon-Like Peptide 2: A Key Link between Nutrition and Intestinal Adaptation in Neonates?
J. Nutr., November 1, 2003; 133(11): 3712 - 3716.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
J. Wang, G. Webb, Y. Cao, and D. F. Steiner
Contrasting patterns of expression of transcription factors in pancreatic {alpha} and {beta} cells
PNAS, October 28, 2003; 100(22): 12660 - 12665.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
J. W. Ensinck, E. C. Laschansky, R. E. Vogel, and D. A. D'Alessio
Effect of Ingested Nutrients on the Release of Thrittene into the Human Circulation
J. Clin. Endocrinol. Metab., October 1, 2003; 88(10): 4798 - 4804.
[Abstract] [Full Text] [PDF]

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 Diabetes CareHome page
G. S. Meneilly, N. Greig, H. Tildesley, J. F. Habener, J. M. Egan, and D. Elahi
Effects of 3 Months of Continuous Subcutaneous Administration of Glucagon-Like Peptide 1 in Elderly Patients With Type 2 Diabetes
Diabetes Care, October 1, 2003; 26(10): 2835 - 2841.
[Abstract] [Full Text] [PDF]

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 Diabetes CareHome page
B. Ahren, J. J. Holst, and A. Mari
Characterization of GLP-1 Effects on {beta}-Cell Function After Meal Ingestion in Humans
Diabetes Care, October 1, 2003; 26(10): 2860 - 2864.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
M. Vincent, Y. Guz, M. Rozenberg, G. Webb, M. Furuta, D. Steiner, and G. Teitelman
Abrogation of Protein Convertase 2 Activity Results in Delayed Islet Cell Differentiation and Maturation, Increased {alpha}-Cell Proliferation, and Islet Neogenesis
Endocrinology, September 1, 2003; 144(9): 4061 - 4069.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
N. Vrang, C. B. Phifer, M. M. Corkern, and H.-R. Berthoud
Gastric distension induces c-Fos in medullary GLP-1/2-containing neurons
Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2003; 285(2): R470 - R478.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
R. H. Lustig, P. S. Hinds, K. Ringwald-Smith, R. K. Christensen, S. C. Kaste, R. E. Schreiber, S. N. Rai, S. Y. Lensing, S. Wu, and X. Xiong
Octreotide Therapy of Pediatric Hypothalamic Obesity: A Double-Blind, Placebo-Controlled Trial
J. Clin. Endocrinol. Metab., June 1, 2003; 88(6): 2586 - 2592.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
R. Gros, X. You, L. L. Baggio, M. G. Kabir, A. M. Sadi, I. N. Mungrue, T. G. Parker, Q. Huang, D. J. Drucker, and M. Husain
Cardiac Function in Mice Lacking the Glucagon-Like Peptide-1 Receptor
Endocrinology, June 1, 2003; 144(6): 2242 - 2252.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
S. L. Conarello, Z. Li, J. Ronan, R. S. Roy, L. Zhu, G. Jiang, F. Liu, J. Woods, E. Zycband, D. E. Moller, et al.
Mice lacking dipeptidyl peptidase IV are protected against obesity and insulin resistance
PNAS, May 27, 2003; 100(11): 6825 - 6830.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
X. Cao, G. Flock, C. Choi, D. M. Irwin, and D. J. Drucker
Aberrant Regulation of Human Intestinal Proglucagon Gene Expression in the NCI-H716 Cell Line
Endocrinology, May 1, 2003; 144(5): 2025 - 2033.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
E. V. Polyzogopoulou, F. Kalfarentzos, A. G. Vagenakis, and T. K. Alexandrides
Restoration of Euglycemia and Normal Acute Insulin Response to Glucose in Obese Subjects With Type 2 Diabetes Following Bariatric Surgery
Diabetes, May 1, 2003; 52(5): 1098 - 1103.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
F. M. Gribble, L. Williams, A. K. Simpson, and F. Reimann
A Novel Glucose-Sensing Mechanism Contributing to Glucagon-Like Peptide-1 Secretion From the GLUTag Cell Line
Diabetes, May 1, 2003; 52(5): 1147 - 1154.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
N. Pamir, F. C. Lynn, A. M. J. Buchan, J. Ehses, S. A. Hinke, J. A. Pospisilik, K. Miyawaki, Y. Yamada, Y. Seino, C. H. S. McIntosh, et al.
Glucose-dependent insulinotropic polypeptide receptor null mice exhibit compensatory changes in the enteroinsular axis
Am J Physiol Endocrinol Metab, May 1, 2003; 284(5): E931 - E939.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
M. Nishizawa, M. C. Moore, M. Shiota, S. M. Gustavson, W. L. Snead, D. W. Neal, and A. D. Cherrington
Effect of intraportal glucagon-like peptide-1 on glucose metabolism in conscious dogs
Am J Physiol Endocrinol Metab, May 1, 2003; 284(5): E1027 - E1036.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
T. P. Vahl, B. W. Paty, B. D. Fuller, R. L. Prigeon, and D. A. D'Alessio
Effects of GLP-1-(7-36)NH2, GLP-1-(7-37), and GLP-1- (9-36)NH2 on Intravenous Glucose Tolerance and Glucose-Induced Insulin Secretion in Healthy Humans
J. Clin. Endocrinol. Metab., April 1, 2003; 88(4): 1772 - 1779.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. Lopez de Maturana, A. Willshaw, A. Kuntzsch, R. Rudolph, and D. Donnelly
The Isolated N-terminal Domain of the Glucagon-like Peptide-1 (GLP-1) Receptor Binds Exendin Peptides with Much Higher Affinity than GLP-1
J. Biol. Chem., March 14, 2003; 278(12): 10195 - 10200.
[Abstract] [Full Text] [PDF]

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 Diabetes CareHome page
S. Quddusi, T. P. Vahl, K. Hanson, R. L. Prigeon, and D. A. D'Alessio
Differential Effects of Acute and Extended Infusions of Glucagon-Like Peptide-1 on First- and Second-Phase Insulin Secretion in Diabetic and Nondiabetic Humans
Diabetes Care, March 1, 2003; 26(3): 791 - 798.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
D. A. Stoffers, B. M. Desai, D. D. DeLeon, and R. A. Simmons
Neonatal Exendin-4 Prevents the Development of Diabetes in the Intrauterine Growth Retarded Rat
Diabetes, March 1, 2003; 52(3): 734 - 740.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
J. A. Pospisilik, J. Martin, T. Doty, J. A. Ehses, N. Pamir, F. C. Lynn, S. Piteau, H.-U. Demuth, C. H.S. McIntosh, and R. A. Pederson
Dipeptidyl Peptidase IV Inhibitor Treatment Stimulates {beta}-Cell Survival and Islet Neogenesis in Streptozotocin-Induced Diabetic Rats
Diabetes, March 1, 2003; 52(3): 741 - 750.
[Abstract] [Full Text] [PDF]

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 Pharmacol. Rev.Home page
K. E. Mayo, L. J. Miller, D. Bataille, S. Dalle, B. Goke, B. Thorens, and D. J. Drucker
International Union of Pharmacology. XXXV. The Glucagon Receptor Family
Pharmacol. Rev., March 1, 2003; 55(1): 167 - 194.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
G. Kang, J. W. Joseph, O. G. Chepurny, M. Monaco, M. B. Wheeler, J. L. Bos, F. Schwede, H.-G. Genieser, and G. G. Holz
Epac-selective cAMP Analog 8-pCPT-2'-O-Me-cAMP as a Stimulus for Ca2+-induced Ca2+ Release and Exocytosis in Pancreatic beta -Cells
J. Biol. Chem., February 28, 2003; 278(10): 8279 - 8285.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
R. W. Gelling, X. Q. Du, D. S. Dichmann, J. Romer, H. Huang, L. Cui, S. Obici, B. Tang, J. J. Holst, C. Fledelius, et al.
Lower blood glucose, hyperglucagonemia, and pancreatic alpha cell hyperplasia in glucagon receptor knockout mice
PNAS, February 4, 2003; 100(3): 1438 - 1443.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
D. D. De Leon, S. Deng, R. Madani, R. S. Ahima, D. J. Drucker, and D. A. Stoffers
Role of Endogenous Glucagon-Like Peptide-1 in Islet Regeneration After Partial Pancreatectomy
Diabetes, February 1, 2003; 52(2): 365 - 371.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Y. Li, T. Hansotia, B. Yusta, F. Ris, P. A. Halban, and D. J. Drucker
Glucagon-like Peptide-1 Receptor Signaling Modulates beta Cell Apoptosis
J. Biol. Chem., January 3, 2003; 278(1): 471 - 478.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z. Ni, Y. Anini, X. Fang, G. Mills, P. L Brubaker, and T. Jin
Transcriptional Activation of the Proglucagon Gene by Lithium and beta -Catenin in Intestinal Endocrine L Cells
J. Biol. Chem., January 3, 2003; 278(2): 1380 - 1387.
[Abstract] [Full Text] [PDF]

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 Exp. Biol. Med.Home page
M. Srinivasan, S. G. Laychock, D. J. Hill, and M. S. Patel
Neonatal Nutrition: Metabolic Programming of Pancreatic Islets and Obesity
Experimental Biology and Medicine, January 1, 2003; 228(1): 15 - 23.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
L. Rachdi, J.-C. Marie, and R. Scharfmann
Role for VPAC2 Receptor-Mediated Signals in Pancreas Development
Diabetes, January 1, 2003; 52(1): 85 - 92.
[Abstract] [Full Text] [PDF]


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