Glucagon-like peptide-1 decreases intracerebral glucose content by activating hexokinase and changing glucose clearance during hyperglycemia

Journal of Cerebral Blood Flow and Metabolism

Volumn 32, Issue 12, 2012, Pages 2146-2152

  Gejl, Michael ^a,b   Egefjord, Lærke ^a   Lerche, Susanne ^a   Vang, Kim ^b   Bibby, Bo Martin ^c   Holst, Jens Juul ^b   Mengel, Annette ^b   Moller, Niels ^b   Rungby, Jorgen ^a,b   Brock, Birgitte ^a,c   Gjedde, Albert ^b  

^a AARHUS UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

2 deoxy glucose; blood brain barrier; diabetes; energy metabolism; GLP 1; glucagon like peptide 1; glucose; pharmacology

Indexed keywords

FLUORODEOXYGLUCOSE F 18; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; HEXOKINASE; NORADRENALIN;

ADULT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN REGION; CLINICAL ARTICLE; DIAGNOSTIC IMAGING EQUIPMENT; ENZYME ACTIVATION; FEMALE; GLUCOSE BRAIN LEVEL; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HUMAN; HYPERGLYCEMIA; MALE; METABOLIC RATE; PHOSPHORYLATION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ADULT; ALZHEIMER DISEASE; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN CHEMISTRY; BRAIN ISCHEMIA; CROSS-OVER STUDIES; DIABETES MELLITUS, TYPE 2; DOUBLE-BLIND METHOD; FLUORODEOXYGLUCOSE F18; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; GLUCOSE CLAMP TECHNIQUE; GLUCOSE TRANSPORTER TYPE 1; HEXOKINASE; HUMANS; HYPERGLYCEMIA; MALE; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; STROKE;

EID: 84870624506     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2012.118     Document Type: Article

References (38)

1. Morrish NJ, Wang SL, Stevens LK, Fuller JH, Keen H. Mortality and causes of death in the WHO Multinational Study of vascular disease in diabetes. Diabetologia 2001; 44 (Suppl 2): S14-S21.
2. Luchsinger JA, Reitz C, Honig LS, Tang MX, Shea S, Mayeux R. Aggregation of vascular risk factors and risk of incident Alzheimer disease. Neurology 2005; 65: 545-551.
3. Xu WL, von SE, Qiu CX, Winblad B, Fratiglioni L. Uncontrolled diabetes increases the risk of Alzheimer's disease: a population-based cohort study. Diabetologia 2009; 52: 1031-1039.
4. Bellolio MF, Gilmore RM, Stead LG. Insulin for glycaemic control in acute ischaemic stroke. Cochrane Database Syst Rev 2011; 9: CD005346.
5. Brubaker PL, Drucker DJ. Minireview: glucagon-like peptides regulate cell proliferation and apoptosis in the pancreas, gut, and central nervous system. Endocrinology 2004; 145: 2653-2659.
6. Drucker DJ, Nauck MA. The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 2006; 368: 1696-1705.
7. Holst JJ. On the physiology of GIP and GLP-1. Horm Metab Res 2004; 36: 747-754.
8. Hamilton A, Holscher C. Receptors for the incretin glucagon-like peptide-1 are expressed on neurons in the central nervous system. Neuroreport 2009; 20: 1161-1166.
9. Bak AM, Egefjord L, Gejl M, Steffensen C, Stecher CW, Smidt K, Brock B, Rungby J. Targeting amyloid-beta by glucagon-like peptide -1 (GLP-1) in Alzheimer's disease and diabetes. Expert Opin Ther Targets 2011; 15: 1153-1162.
10. Darsalia V, Mansouri S, Ortsater H, Olverling A, Nozadze N, Kappe C, Iverfeldt K, Tracy LM, Grankvist N, Sjoholm A, Patrone C. Glucagon-like peptide-1 receptor activation reduces ischaemic brain damage following stroke in Type 2 diabetic rats. Clin Sci (Lond) 2012; 122: 473-483.
11. Degn KB, Brock B, Juhl CB, Djurhuus CB, Grubert J, Kim D, Han J, Taylor K, Fineman M, Schmitz O. Effect of intravenous infusion of exenatide (synthetic exendin-4) on glucose-dependent insulin secretion and counterregulation during hypoglycemia. Diabetes 2004; 53: 2397-2403.
12. Lerche S, Brock B, Rungby J, Botker HE, Moller N, Rodell A, Bibby BM, Holst JJ, Schmitz O, Gjedde A. Glucagon-like peptide-1 inhibits blood-brain glucose transfer in humans. Diabetes 2008; 57: 325-331.
13. Toft-Nielsen MB, Madsbad S, Holst JJ. Continuous subcutaneous infusion of glucagon-like peptide 1 lowers plasma glucose and reduces appetite in type 2 diabetic patients. Diabetes Care 1999; 22: 1137-1143.
14. Sokoloff L, Reivich M, Kennedy C, Des Rosiers MH, Patlak CS, Pettigrew KD, Sakurada O, Shinohara M. The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem 1977; 28: 897-916.
15. Gjedde A. Calculation of cerebral glucose phosphorylation from brain uptake of glucose analogs in vivo: a re-examination. Brain Res 1982; 257: 237-274.
16. Gjedde A, Christensen O. Estimates of Michaelis-Menten constants for the two membranes of the brain endothelium. J Cereb Blood Flow Metab 1984; 4: 241-249.
17. Kuwabara H, Evans AC, Gjedde A. Michaelis-Menten constraints improved cerebral glucose metabolism and regional lumped constant measurements with [18F]fluorodeoxyglucose. J Cereb Blood Flow Metab 1990; 10: 180-189.
18. Hasselbalch SG, Madsen PL, Knudsen GM, Holm S, Paulson OB. Calculation of the FDG lumped constant by simultaneous measurements of global glucose and FDG metabolism in humans. J Cereb Blood Flow Metab 1998; 18: 154-160.
19. Gjedde A, Wienhard K, Heiss WD, Kloster G, Diemer NH, Herholz K, Pawlik G. Comparative regional analysis of 2-fluorodeoxyglucose and methylglucose uptake in brain of four stroke patients. With special reference to the regional estimation of the lumped constant. J Cereb Blood Flow Metab 1985; 5: 163-178.
20. Crone C. Facilitated transfer of glucose from blood into brain tissue. J Physiol 1965; 181: 103-113.
21. Hasselbalch SG, Knudsen GM, Videbaek C, Pinborg LH, Schmidt JF, Holm S, Paulson OB. No effect of insulin on glucose blood-brain barrier transport and cerebral metabolism in humans. Diabetes 1999; 48: 1915-1921.
22. Hom FG, Goodner CJ, Berrie MA. A [3H]2-deoxyglucose method for comparing rates of glucose metabolism and insulin responses among rat tissues in vivo. Validation of the model and the absence of an insulin effect on brain. Diabetes 1984; 33: 141-152.
23. McCall AL, Gould JB, Ruderman NB. Diabetes-induced alterations of glucose metabolism in rat cerebral microvessels. Am J Physiol 1984; 247: E462-E467.
24. Namba H, Lucignani G, Nehlig A, Patlak C, Pettigrew K, Kennedy C, Sokoloff L. Effects of insulin on hexose transport across blood-brain barrier in normoglycemia. Am J Physiol 1987; 252: E299-E303.
25. Seaquist ER, Damberg GS, Tkac I, Gruetter R. The effect of insulin on in vivo cerebral glucose concentrations and rates of glucose transport/metabolism in humans. Diabetes 2001; 50: 2203-2209.
26. Hertz MM, Paulson OB, Barry DI, Christiansen JS, Svendsen PA. Insulin increases glucose transfer across the blood-brain barrier in man. J Clin Invest 1981; 67: 597-604.
27. Shapiro ET, Cooper M, Chen CT, Given BD, Polonsky KS. Change in hexose distribution volume and fractional utilization of [18F]-2-deoxy-2-fluoro- Dglucose in brain during acute hypoglycemia in humans. Diabetes 1990; 39: 175-180.
28. Hirvonen J, Virtanen KA, Nummenmaa L, Hannukainen JC, Honka MJ, Bucci M, Nesterov SV, Parkkola R, Rinne J, Iozzo P, Nuutila P. Effects of insulin on brain glucose metabolism in impaired glucose tolerance. Diabetes 2011; 60: 443-447.
29. McCall AL. Cerebral glucose metabolism in diabetes mellitus. Eur J Pharmacol 2004; 490: 147-158.
30. Huitink JM, Visser FC, van Leeuwen GR, Van LA, Bax JJ, Heine RJ, Teule GJ, Visser CA. Influence of high and low plasma insulin levels on the uptake of fluorine-18 fluorodeoxyglucose in myocardium and femoral muscle, assessed by planar imaging. Eur J Nucl Med 1995; 22: 1141-1148.
31. Moller K, Qvist T, Tofteng F, Sahl C, Sonderkaer S, Dethloff T, Knudsen GM, Larsen FS. Cerebral blood flow and metabolism during infusion of norepinephrine and propofol in patients with bacterial meningitis. Stroke 2004; 35: 1333-1339.
32. Leybaert L. Neurobarrier coupling in the brain: a partner of neurovascular and neurometabolic coupling? J Cereb Blood Flow Metab 2005; 25: 2-16.
33. Gejl M, Sondergaard HM, Stecher C, Bibby BM, Moller N, Botker HE, Hansen SB, Gjedde A, Rungby J, Brock B. Exenatide alters myocardial glucose transport and uptake depending on insulin resistance and increases myocardial blood flow in patients with type 2 diabetes. J Clin Endocrinol Metab 2012; 97: E1165-E1169.
34. Morita K, Katoh C, Yoshinaga K, Noriyasu K, Mabuchi M, Tsukamoto T, Kageyama H, Shiga T, Kuge Y, Tamaki N. Quantitative analysis of myocardial glucose utilization in patients with left ventricular dysfunction by means of 18F-FDG dynamic positron tomography and three-compartment analysis. Eur J Nucl Med Mol Imaging 2005; 32: 806-812.
35. Johnson KA, Fox NC, Sperling RA, Klunk WE. Brain imaging in Alzheimer disease. Cold Spring Harb Perspect Med 2012; 2: a006213.
36. Brands AM, Kessels RP, de Haan EH, Kappelle LJ, Biessels GJ. Cerebral dysfunction in type 1 diabetes: effects of insulin, vascular risk factors and blood-glucose levels. Eur J Pharmacol 2004; 490: 159-168.
37. Humpel C. Chronic mild cerebrovascular dysfunction as a cause for Alzheimer's disease? Exp Gerontol 2011; 46: 225-232.
38. Bingham EM, Dunn JT, Smith D, Sutcliffe-Goulden J, Reed LJ, Marsden PK, Amiel SA. Differential changes in brain glucose metabolism during hypoglycaemia accompany loss of hypoglycaemia awareness in men with type 1 diabetes mellitus. An [11C]-3-O-methyl-D-glucose PET study. Diabetologia 2005; 48: 2080-2089.