Protein restriction during early life in rats alters pancreatic GABAA receptor subunit expression and glucagon secretion in adulthood

Canadian Journal of Diabetes

Volumn 36, Issue 3, 2012, Pages 100-107

  Durst, Michelle A ^a,c   Lux Lantos, Victoria A ^b   Hardy, Daniel B ^c   Hill, David J ^a,c   Arany, Edith J ^a,c  

^a LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^b INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Fetal programming; GABA; Low protein diet; Pancreatic development; Type 2 diabetes

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA4; 4 AMINOBUTYRIC ACID A RECEPTOR BETA1; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA3; 4 AMINOBUTYRIC ACID B RECEPTOR; ARGININE; ASPARTIC ACID; GLUCAGON; GLUCOSE; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 65; GLUTAMIC ACID; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; INSULIN; MESSENGER RNA; TAURINE;

ANIMAL EXPERIMENT; ANIMAL FOOD; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; FEMALE; GENE EXPRESSION; GESTATION PERIOD; GLUCAGON BLOOD LEVEL; GLUCAGON RELEASE; GLUCOSE HOMEOSTASIS; IN VIVO STUDY; INSULIN BLOOD LEVEL; INSULIN RELEASE; LACTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET; PROGENY; PROTEIN EXPRESSION; PROTEIN RESTRICTION; RAT; REAL TIME POLYMERASE CHAIN REACTION; WEANING; WESTERN BLOTTING;

EID: 84872389678     PISSN: 14992671     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jcjd.2012.06.002     Document Type: Article

References (41)

1. Barker DJ, Hales CN, Fall CH, et al. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 1993;36:62e7.
2. Desai M, Crowther NJ, Lucas A, et al. Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 1996;76:591e603.
3. Fernandez-Twinn DS, Wayman A, Ekizoglou S, et al. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol Regul Integr Comp Physiol 2005;288:R368e73.
4. Petrik J, Reusens B, Arany E, et al. A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor-II. Endocrinology 1999;140:4861e73.
5. Chamson-Reig A, Thyssen SM, Hill DJ, et al. Exposure of the pregnant rat to low protein diet causes impaired glucose homeostasis in the young adult offspring by different mechanisms in males and females. Exp Biol Med 2009;234:1425e36.
6. Petrik J, Arany E, McDonald TJ, et al. Apoptosis in the pancreatic islet cells of the neonatal rat is associated with a reduced expression of insulin-like growth factor II that may act as a survival factor. Endocrinology 1998;139:2994e3004.
7. Boujendar S, Arany E, Hill DJ, et al. Taurine supplementation of a low protein diet fed to rat dams normalizes the vascularization of the fetal endocrine pancreas. J Nutr 2003;133:2820e5.
8. Cherif H, Reusens B, Ahn MT, et al. Effects of taurine on the insulin secretion of rat fetal islets from dams fed a low-protein diet. J Endocrinol 1998;159:341e8.
9. Okada Y, Taniguchi H, Schimada C. High concentration of GABA and high glutamate decarboxylase activity in rat pancreatic islets and human insulinoma. Science 1976;194:620e2.
10. Wang C, Mao R, Van de Casteele M, et al. Glucagon-like peptide-1 stimulates GABA formation by pancreatic beta-cells at the level of glutamate decarboxylase. Am J Physiol Endocrinol Metab 2007;294:E1201e6.
11. Garry DJ, Coulter HD, McIntee TJ, et al. Immunoreactive GABA transaminase within the pancreatic islet is localized in mitochondria of the B-cell. J Histochem Cytochem 1987;35:831e6.
12. Satin LS, Kinard TA. Neurotransmitters and their receptors in the islets of Langerhans of the pancreas: what messages do acetylcholine, glutamate, and GABA transmit. Endocrine 1998;8:213e23.
13. Braun M, Wendt A, Buschard K, et al. GABAB receptor activation inhibits exocytosis in rat pancreatic beta-cells by G-protein-dependent activation of calcineurin. J Physiol 2001;559:397e409.
14. Brice NL, Varadi A, Ashcroft SJ, et al. Metabotropic glutamate and GABA(B) receptors contribute to the modulation of glucose-stimulated insulin secretion in pancreatic beta cells. Diabetologia 2002;45:242e52.
15. Gu XH, Kurose T, Kato S, et al. Suppressive effect of GABA on insulin secretion from the pancreatic beta-cells in the rat. Life Sci 1993;52:687e94.
16. Shi Y, Kanaani J, Menard-Rose V, et al. Increased expression of GAD65 and GABA in pancreatic beta-cells impairs first-phase insulin secretion. Am J Physiol Endocrinol Metab 2000;279:E684e94.
17. Braun M, Ramracheya R, Bengtsson M, et al. Gamma-aminobutyric acid (GABA) is an autocrine excitatory transmitter in human pancreatic beta-cells. Diabetes 2010;59:1694e701.
18. Braun M, Wendt A, Karanauskaite J, et al. Co-release and differential exit via the fusion pore of GABA, serotonin, and ATP from LDCV in rat pancreatic beta cells. J Gen Physiol 2007;129:221e31.
19. Soltani N, Qiu H, Aleksic M, et al. GABA exerts protective and regenerative effects on islet beta cells and reverse diabetes. Proc Natl Acad Sci USA 2011; 108:11692e7.
20. Nayeem N, Green TP, Martin IL, et al. Quaternary structure of the native GABAA receptor determined by electron microscopic image analysis. J Neurochem 1994;62:815e8.
21. Tretter V, Ehya N, Fuchs K, et al. Stoichiometry and assembly of a recombinant GABAA receptor subtype. J Neurosci 1997;17:2728e37.
22. Wendt A, Birnir B, Buschard K, et al. Glucose inhibition of glucagon secretion from rat alpha-cells is mediated by GABA released from neighboring beta-cells. Diabetes 2004;53:1038e45.
23. Xu E, Kumar M, Zhang Y, et al. Intra-islet insulin suppresses glucagon release via GABA-GABAA receptor system. Cell Metab 2006;3:47e58.
24. Wang Q, Liu L, Pei L, et al. Control of synaptic strength, a novel function of Akt. Neuron 2003;38:915e28.
25. Bettler B, Kaupmann K, Mosbacher J, et al. Molecular structure and physiological functions of GABA(B) receptors. Physiol Rev 2004;84:835e67.
26. Chebib M, Johnston GA. GABA-Activated ligand gated ion channels: medicinal chemistry and molecular biology. J Med Chem 2000;43:1427-47.
27. Marshall FH, Jones KA, Kaupmann K, et al. GABAB receptorsdthe first 7TM heterodimers. Trends Pharmacol Sci 1999;20:396e9.
28. Braun M, Wendt A, Birnir B, et al. Regulated exocytosis of GABA-containing synaptic-like microvesicles in pancreatic beta-cells. J Gen Physiol 2004;123: 191e204.
29. Bonaventura MM, Catalano PN, Chamson-Reig A, et al. GABA-B receptors and glucose homeostasis: evaluation in GABA-B receptor knock-out mice. Am J Physiol Endocrinol Metab 2008;294:E157e67.
30. Michalik M, Nelson J, Erecinska M. GABA production in rat islets of Langerhans. Diabetes 1993;42:1506e13.
31. Snoeck A, Remacle C, Reusens B, et al. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 1990;57:107e18.
32. Joseph JW, Koshkin V, Saleh MC, et al. Free fatty acid-induced beta-cell defects are dependent on uncoupling protein 2 expression. J Biol Chem 2004;279: 51049e56.
33. Dhanvantari S, Brubaker PL. Proglucagon processing in an islet cell line: effects of PC1 overexpression and PC2 depletion. Endocrinology 1998;139: 1630e7.
34. Saller CF, Czupryna MJ. Gamma-aminobutyric acid, glutamate, glycine and taurine analysis using reversed-phase high performance liquid chromatography and ultraviolet detection of dansyl chloride derivatives. J Chromatogr 1989;487:167e72.
35. Thellin O, Zorzi W, Lakaye B, et al. Housekeeping genes as internal standards: use and limits. J Biotechnol 1999;75:291e5.
36. Gillies MC, Mandel TE. The evolution of function and response to arginine challenge and pregnancy of portally and systemically placed islet cell grafts in streptozotocin diabetic mice. Metabolism 1990;39:1253e8.
37. Guenifi A, Ahren B, Abdel-Halim SM. Differential effects of glucagon-like peptide-1 (7-36)amide versus cholecystokinin on arginine-induced islet hormone release in vivo and in vitro. Pancreas 2001;22:58e64.
38. Franklin IK, Wollheim CB. GABA in the endocrine pancreas: its putative role as an islet cell paracrine-signaling molecule. J Gen Physiol 2004;123: 185e90.
39. Bailey SJ, Ravier MA, Rutter GA. Glucose-dependent regulation of gammaaminobutyric acid (GABA A) receptor expression in mouse pancreatic islet alpha-cells. Diabetes 2007;56:320e7.
40. Shah P, Vella A, Basu A, et al. Lack of suppression of glucagon contributes to postprandial hyperglycemia in subjects with type 2 diabetes mellitus. J Clin Endocrinol Metab 2000;85:4053e9.
41. Ishihara H, Maechler P, Gjinovci A, et al. Islet beta-cell secretion determines glucagon release from neighboring alpha-cells. Nat Cell Biol 2003;5: 330e5.