Changes in human brain glutamate concentration during hypoglycemia: Insights into cerebral adaptations in hypoglycemia-associated autonomic failure in type 1 diabetes

Journal of Cerebral Blood Flow and Metabolism

Volumn 34, Issue 5, 2014, Pages 876-882

  Terpstra, Melissa ^a   Moheet, Amir ^a   Kumar, Anjali ^a   Eberly, Lynn E ^b   Seaquist, Elizabeth ^a   Öz, Gülin ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

brain; diabetes; glutamate; hypoglycemia; unawareness

Indexed keywords

ADRENALIN; GLUCOSE; GLUTAMIC ACID;

ADULT; AMINO ACID BRAIN LEVEL; ARTICLE; AUTONOMIC DYSFUNCTION; BODY MASS; CLINICAL ARTICLE; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FEMALE; GLUCOSE BLOOD LEVEL; HUMAN; HYPOGLYCEMIA; HYPOGLYCEMIA ASSOCIATED AUTONOMIC FAILURE; INSULIN DEPENDENT DIABETES MELLITUS; MALE; OCCIPITAL CORTEX; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; QUALITY CONTROL;

ADULT; BLOOD GLUCOSE; BRAIN; DIABETES MELLITUS, TYPE 1; FEMALE; GLUTAMIC ACID; HUMANS; HYPOGLYCEMIA; MALE; MIDDLE AGED;

EID: 84899928323     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.32     Document Type: Article

References (40)

1. The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of longterm complications in insulin-dependent diabetes mellitus. New Engl J Med 1993; 329: 977-986.
2. Cryer PE. Mechanisms of hypoglycemia-associated autonomic failure and its component syndromes in diabetes. Diabetes 2005; 54: 3592-3601.
3. McCrimmon RJ, Oz G. Cerebral adaptation to recurrent hypoglycemia. Transl Endocrinol Metab 2013; 3: 1-25.
4. Mangia S, Tesfaye N, De Martino F, Kumar AF, Kollasch P, Moheet AA et al. Hypoglycemia-induced increases in thalamic cerebral blood flow are blunted in subjects with type 1 diabetes and hypoglycemia unawareness. J Cereb Blood Flow Metab 2012; 32: 2084-2090.
5. Kennan RP, Takahashi K, Pan C, Shamoon H, Pan JW. Human cerebral blood flow and metabolism in acute insulin-induced hypoglycemia. J Cereb Blood Flow Metab 2005; 25: 527-534.
6. Abdul-Rahman A, Siesjo BK. Local cerebral glucose consumption during insulininduced hypoglycemia, and in the recovery period following glucose administration. Acta Physiol Scand 1980; 110: 149-159.
7. Ghajar JB, Plum F, Duffy TE. Cerebral oxidative metabolism and blood flow during acute hypoglycemia and recovery in unanesthetized rats. J Neurochem 1982; 38: 397-409.
8. Van de Ven KCC, De Galan BE, Van der Graaf M, Shestov AA, Henry P-G, Tack CJ et al. Effect of acute hypoglycemia in on human cerebral glucose metabolism measured by 13C magnetic resonance spectroscopy. Diabetes 2011; 60: 1467-1473.
9. Lubow JM, Pinon IG, Avogaro A, Cobelli C, Treeson DM, Mandeville KA et al. Brain oxygen utilization is unchanged by hypoglycemia in normal humans: lactate, alanine, and leucine uptake are not sufficient to offset energy deficit. Am J Physiol Endocrinol Metab 2006; 290: E149-E153.
10. Oz G, Kumar A, Rao JP, Kodl CT, Chow L, Eberly LE et al. Human brain glycogen metabolism during and after hypoglycemia. Diabetes 2009; 58: 1978-1985.
11. Horinaka N, Artz N, Jehle J, Takahashi S, Kennedy C, Sokoloff L. Examination of potential mechanisms in the enhancement of cerebral blood flow by hypoglycemia and pharmacological doses of deoxyglucose. J Cereb Blood Flow Metab 1997; 17: 54-63.
12. Choi I-Y. In vivo measurements of brain glucose transport using the reversible Michaelis-Menten model and simultaneouls measurements of cerebral blood flow changes during hyupoglycemia. J Cereb Blood Flow Metab 2001; 21: 653-663.
13. Brondsted HE, Gjedde A. Glucose phosphorylation rate in rat parietal cortex during normoglycemia, hypoglycemia, acute hyperglycemia, and in diabetesprone rats. Acta Neurol Scand 1990; 81: 233-236.
14. Suda S, Shinohara M, Miyaoka M, Lucignani G, Kennedy C, Sokoloff L. The lumped constant of the deoxyglucose method in hypoglycemia: effects of moderate hypoglycemia on local cerebral glucose utilization in the rat. J Cereb Blood Flow Metab 1990; 10: 499-509.
15. Norberg K, Siesio BK. Oxidative metabolism of the cerebral cortex of the rat in severe insulin-induced hypoglycaemia. J Neurochem 1976; 26: 345-352.
16. Choi IY, Seaquist ER, Gruetter R. Effect of hypoglycemia on brain glycogen metabolism in vivo. J Neurosci Res 2003; 72: 25-32.
17. Dawson RM. Studies on the glutamine and glutamic acid content of the rat brain during insulin hypoglycaemia. Biochem J 1950; 47: 386-391.
18. Lewis LD, Ljunggren B, Norberg K, Siesjo BK. Changes in carbohydrate substrates, amino acids and ammonia in the brain during insulin-induced hypoglycemia. J Neurochem 1974; 23: 659-671.
19. Behar KL, den Hollander JA, Petroff OA, Hetherington HP, Prichard JW, Shulman RG. Effect of hypoglycemic encephalopathy upon amino acids, high-energy phosphates, and pHi in the rat brain in vivo: detection by sequential 1H and 31P NMR spectroscopy. J Neurochem 1985; 44: 1045-1055.
20. Sutherland GR, Tyson RL, Auer RN. Truncation of the krebs cycle during hypoglycemic coma. Med Chem 2008; 4: 379-385.
21. Rao R, Ennis K, Long JD, Ugurbil K, Gruetter R, Tkac I. Neurochemical changes in the developing rat hippocampus during prolonged hypoglycemia. J Neurochem 2010; 114: 728-738.
22. Bischof MG, Brehm A, Bernroider E, Krssak M, Mlynarik V, Krebs M et al. Cerebral glutamate metabolism during hypoglycaemia in healthy and type 1 diabetic humans. Eur J Clin Invest 2006; 36: 164-169.
23. Criego AB, Tkac I, Kumar A, Thomas W, Gruetter R, Seaquist ER. Brain glucose concentrations in patients with type 1 diabetes and hypoglycemia unawareness. J Neurosci Res 2005; 79: 42-47.
24. Clarke WL, Cox DJ, Gonder-Frederick LA, Julian D, Schlundt D, Polonsky W. Reduced awareness of hypoglycemia in adults with IDDM. A prospective study of hypoglycemic frequency and associated symptoms. Diabetes Care 1995; 18: 517-522.
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. Towler DA, Havlin CE, Craft S, Cryer P. Mechanism of awareness of hypoglycemia. Perception of neurogenic (predominantly cholinergic) rather than neuroglycopenic symptoms. Diabetes 1993; 42: 1791-1798.
27. Tkac I, Oz G, Adriany G, Ugurbil K, Gruetter R. In vivo 1H NMR spectroscopy of the human brain at high magnetic fields: metabolite quantification at 4T vs. 7T. Magn Reson Med 2009; 62: 868-879.
28. Gruetter R, Tkac I. Field mapping without reference scan using asymmetric echoplanar techniques. Magn Reson Med 2000; 43: 319-323.
29. Provencher SW. Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 2001; 14: 260-264.
30. Govindaraju V, Young K, Maudsley AA. Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed 2000; 13: 129-153.
31. Provencher SW. LCModel and LCMgui User's Manual http://s-provencher.com/.
32. Moheet A, Emir UE, Terpstra M, Kumar A, Eberly LE, Seaquist ER et al. Initial experience with seven tesla magnetic resonance spectroscopy of hypothalamic GABA during hyperinsulinemic euglycemia and hypoglycemia in healthy humans. Magn Reson Med 2013; 71: 12-18.
33. Henry PG, Criego AB, Kumar A, Seaquist ER. Measurement of cerebral oxidative glucose consumption in patients with type 1 diabetes mellitus and hypoglycemia unawareness using (13)C nuclear magnetic resonance spectroscopy. Metabolism 2010; 59: 100-106.
34. Van de Ven KCC, Van der Graaf M, Tack CJ, Heerchap A, De Galan BE. Steady-state brain glucose concentrations during hypoglycemia in healthy humans and patients with type 1 diabetes. Diabetes 2012; 61: 1974-1977.
35. Mason GF, Petersen KF, Lebon V, Rothman DL, Shulman GI. Increased brain monocarboxylic acid transport and utilization in type 1 diabetes. Diabetes 2006; 55: 929-934.
36. Herzog RI, Jiang L, Herman P, Zhao C, Sanganahalli BG, Mason GF et al. Lactate preserves neuronal metabolism and function following antecedent recurrent hypoglycemia. J Clin Invest 2013; 123: 1988-1998.
37. Kreis R, Ross BD. Cerebral metabolic disturbances in patients with subacute and chronic diabetes mellitus: detection with proton MR spectroscopy. Radiology 1992; 184: 123-130.
38. Geissler A, Frund R, Scholmerich J, Feuerbach S, Zietz B. Alterations of cerebral metabolism in patients with diabetes mellitus studied by proton magnetic resonance spectroscopy. Exp Clin Endocrinol Diabetes 2003; 111: 421-427.
39. Duarte JM, Carvalho RA, Cunha RA, Gruetter R. Caffeine consumption attenuates neurochemical modifications in the hippocampus of streptozotocin-induced diabetic rats. J Neurochem 2009; 111: 368-379.
40. Stevens MJ, Lattimer SA, Kamijo M, Van Huysen C, Sima AA, Greene DA. Osmotically-induced nerve taurine depletion and the compatible osmolyte hypothesis in experimental diabetic neuropathy in the rat. Diabetologia 1993; 36: 608-614.