Increased brain lactate concentrations without increased lactate oxidation during hypoglycemia in type 1 diabetic individuals

Diabetes

Volumn 62, Issue 9, 2013, Pages 3075-3080

  De Feyter, Henk M ^a   Mason, Graeme F ^a   Shulman, Gerald I ^a   Rothman, Douglas L ^a   Petersen, Kitt Falk ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 13; CARBOXYLIC ACID; GLUTAMIC ACID; GLUTAMINE; INSULIN; LACTIC ACID; LACTIC ACID C 13; RADIOISOTOPE; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN; BRAIN METABOLISM; CARBON NUCLEAR MAGNETIC RESONANCE; CLINICAL ARTICLE; CONTINUOUS INFUSION; CONTROLLED STUDY; DIABETIC PATIENT; ENERGY TRANSFER; GLUCOSE OXIDATION; GLYCEMIC CONTROL; HUMAN; HYPOGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN TREATMENT; LACTATE BLOOD LEVEL; METABOLIC PARAMETERS; PLASMA; PRIORITY JOURNAL; YOUNG ADULT; METABOLISM; OXIDATION REDUCTION REACTION;

ADULT; BRAIN; DIABETES MELLITUS, TYPE 1; HUMANS; HYPOGLYCEMIA; LACTIC ACID; OXIDATION-REDUCTION;

EID: 84880709881     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-0313     Document Type: Article

References (40)

1. Shalitin S, Phillip M. Hypoglycemia in type 1 diabetes: a still unresolved problem in the era of insulin analogs and pump therapy. Diabetes Care 2008;31(Suppl. 2):S121-S124
2. Davis SN, Mann S, Briscoe VJ, Ertl AC, Tate DB. Effects of intensive therapy and antecedent hypoglycemia on counterregulatory responses to hypoglycemia in type 2 diabetes. Diabetes 2009;58:701-709
3. Dagogo-Jack SE, Craft S, Cryer PE. Hypoglycemia-associated autonomic failure in insulin-dependent diabetes mellitus. Recent antecedent hypo-glycemia reduces autonomic responses to, symptoms of, and defense against subsequent hypoglycemia. J Clin Invest 1993;91:819-828
4. Cryer PE. Diverse causes of hypoglycemia-associated autonomic failure in diabetes. N Engl J Med 2004;350:2272-2279
5. Segel SA, Fanelli CG, Dence CS, et al. Blood-to-brain glucose transport, cerebral glucose metabolism, and cerebral blood flow are not increased after hypoglycemia. Diabetes 2001;50:1911-1917
6. van de Ven KC, de Galan BE, van der Graaf M, et al. Effect of acute hy-poglycemia on human cerebral glucose metabolism measured by C magnetic resonance spectroscopy. Diabetes 2011;60:1467-1473
7. van de Ven KCC, van der Graaf M, Tack CJ, Heerschap 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
8. Criego AB, Tkác I, Kumar A, Thomas W, Gruetter R, Seaquist ER. Brain glucose concentrations in healthy humans subjected to recurrent hypo-glycemia. J Neurosci Res 2005;82:525-530
9. 11C]glucose uptake and metabolism in the brain of insulin-dependent diabetic subjects. Am J Physiol 1990;258:E805-E812
10. Boyle PJ, Kempers SF, O'Connor AM, Nagy RJ. Brain glucose uptake and unawareness of hypoglycemia in patients with insulin-dependent diabetes mellitus. N Engl J Med 1995;333:1726-1731
11. Öz G, Tesfaye N, Kumar A, Deelchand DK, Eberly LE, Seaquist ER. Brain glycogen content and metabolism in subjects with type 1 diabetes and hypoglycemia unawareness. J Cereb Blood Flow Metab 2012;32:256-263
12. Oz G, Seaquist ER, Kumar A, et al. Human brain glycogen content and metabolism: implications on its role in brain energy metabolism. Am J Physiol Endocrinol Metab 2007;292:E946-E951
13. Oz G, Kumar A, Rao JP, et al. Human brain glycogen metabolism during and after hypoglycemia. Diabetes 2009;58:1978-1985
14. 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
15. Halestrap AP, Meredith D. The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch 2004;447:619-628
16. Simpson IA, Carruthers A, Vannucci SJ. Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 2007;27:1766-1791
17. King P, Kong MF, Parkin H, MacDonald IA, Barber C, Tattersall RB. Intravenous lactate prevents cerebral dysfunction during hypoglycaemia in insulin-dependent diabetes mellitus. Clin Sci (Lond) 1998;94:157-163
18. Maran A, Crepaldi C, Trupiani S, et al. Brain function rescue effect of lactate following hypoglycaemia is not an adaptation process in both normal and type I diabetic subjects. Diabetologia 2000;43:733-741
19. Maran A, Cranston I, Lomas J, Macdonald I, Amiel SA. Protection by lac-tate of cerebral function during hypoglycaemia. Lancet 1994;343:16-20
20. Smith D, Pernet A, Hallett WA, Bingham E, Marsden PK, Amiel SA. Lactate: a preferred fuel for human brain metabolism in vivo. J Cereb Blood Flow Metab 2003;23:658-664
21. van Hall G, Strømstad M, Rasmussen P, et al. Blood lactate is an important energy source for the human brain. J Cereb Blood Flow Metab 2009;29: 1121-1129
22. Pellerin L, Magistretti PJ. Sweet sixteen for ANLS. J Cereb Blood Flow Metab 2012;32:1152-1166
23. Brooks GA. The lactate shuttle during exercise and recovery. Med Sci Sports Exerc 1986;18:360-368
24. 13C nuclear magnetic resonance spectroscopy. J Neurosci 2010;30:13983-13991
25. 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
26. Shen J, Rycyna RE, Rothman DL. Improvements on an in vivo automatic shimming method [FASTERMAP]. Magn Reson Med 1997;38:834-839
27. 13C NMR. Proc Natl Acad Sci USA 1999;96:8235-8240
28. 1H spectra with LCModel. NMR Biomed 2001;14:260-264
29. 1H-MRS in investigating the metabolism of the activated human visual cortex at 7 T. Magn Reson Imaging 2006;24:343-348
30. Michaelis T, Merboldt KD, Bruhn H, Hänicke W, Frahm J. Absolute concentrations of metabolites in the adult human brain in vivo: quantification of localized proton MR spectra. Radiology 1993;187:219-227
31. 13C] glucose. J Neu-rochem 2007;100:73-86
32. Mason GF, Gruetter R, Rothman DL, Behar KL, Shulman RG, Novotny EJ. Simultaneous determination of the rates of the TCA cycle, glucose utilization, alpha-ketoglutarate/glutamate exchange, and glutamine synthesis in human brain by NMR. J Cereb Blood Flow Metab 1995;15:12-25
33. Leenders KL, Perani D, Lammertsma AA, et al. Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. Brain 1990;113:27-47
34. van de Ven KCC, Tack CJ, Heerschap A, van der Graaf M, de Galan BE. Patients with type 1 diabetes exhibit altered cerebral metabolism during hypoglycemia. J Clin Invest 2013;123:623-629
35. Simpson IA, Appel NM, Hokari M, et al. Blood-brain barrier glucose transporter: effects of hypo-and hyperglycemia revisited. J Neurochem 1999;72:238-247
36. 13C NMR study. J Neurochem 2006;99:260-268
37. 11C]-3-O-methyl- D-glucose PET study. Diabetologia 2005;48:2080-2089
38. Criego AB, Tkác 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
39. Bergersen LH, Gjedde A. Is lactate a volume transmitter of metabolic states of the brain? Front Neuroenergetics 2012;4:5
40. Brooks GA. Cell-cell and intracellular lactate shuttles. J Physiol 2009;587: 5591-5600