Adaptive mechanisms regulate preferred utilization of ketones in the heart and brain of a hibernating mammal during arousal from torpor

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 296, Issue 2, 2009, Pages

  Andrews, Matthew T ^a   Russeth, Kevin P ^b   Drewes, Lester R ^b   Henry, Pierre Gilles ^b  

^a UNIVERSITY OF MINNESOTA DULUTH   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

hydroxybutyrate; 13C magnetic resonance spectroscopy; Blood brain barrier; Glucose; Hibernation

Indexed keywords

3 HYDROXYBUTYRIC ACID; 4 AMINOBUTYRIC ACID; ASPARTIC ACID; CARBON 13; CREATININE; GLUCOSE; GLUTAMIC ACID; GLYCINE; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 1; CARBON; COTRANSPORTER; GLUCOSE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORT PROTEIN 1; MONOCARBOXYLATE TRANSPORTER; SLC2A1 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AROUSAL; ARTICLE; BLOOD BRAIN BARRIER; BODY TEMPERATURE; BRAIN METABOLISM; CITRIC ACID CYCLE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HEART MUSCLE METABOLISM; HEART RATE; HIBERNATION; ISOTOPE LABELING; LOW TEMPERATURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; SQUIRREL; UPREGULATION; ANIMAL; BLOOD; BRAIN; ENERGY METABOLISM; GLUCOSE BLOOD LEVEL; HEART MUSCLE; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; RAT; SCIURIDAE; SEASON;

3-HYDROXYBUTYRIC ACID; ANIMALS; AROUSAL; BLOOD GLUCOSE; BLOOD-BRAIN BARRIER; BODY TEMPERATURE; BRAIN; CARBON ISOTOPES; CITRIC ACID CYCLE; ENERGY METABOLISM; GLUCOSE TRANSPORTER TYPE 1; HEART RATE; HIBERNATION; MAGNETIC RESONANCE SPECTROSCOPY; MONOCARBOXYLIC ACID TRANSPORTERS; MYOCARDIUM; RATS; SCIURIDAE; SEASONS; SYMPORTERS;

EID: 61949363966     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.90795.2008     Document Type: Article

References (35)

1. Andrews MT. Advances in molecular biology of hibernation in mammals. Bioessays 29: 431-440, 2007.
2. Andrews MT, Squire TL, Bowen CM, Rollins MB. Low-temperature carbon utilization is regulated by novel gene activity in the heart of a hibernating mammal. Proc Natl Acad Sci USA 95: 8392-8397, 1998.
3. Buck MJ, Squire TL, Andrews MT. Coordinate expression of the PDK4 gene: a means of regulating fuel selection in a hibernating mammal. Physiol Genomics 8: 5-13, 2002.
4. Cruz NF, Dienel GA. High glycogen levels in brains of rats with minimal environmental stimuli: implications for metabolic contributions of working astrocytes. J Cereb Blood Flow Metab 22: 1476-1489, 2002.
5. Grey NJ, Karl I, Kipnis DM. Physiologic mechanisms in the development of starvation ketosis in man. Diabetes 24: 10-16, 1975.
6. Epperson LE, Dahl TA, Martin SL. Quantitative analysis of liver protein expression during hibernation in the golden-mantled ground squirrel. Mol Cell Proteomics 3: 920-933, 2004.
7. Galster W, Morrison PR. Gluconeogenesis in arctic ground squirrels between periods of hibernation. Am J Physiol 228: 325-330, 1975.
8. Gerhart DZ, Enerson BE, Zhdankina OY, Leino RL, Drewes LR. Expression of monocarboxylate transporter MCT1 by brain endothelium and glia in adult and suckling rats. Am J Physiol Endocrinol Metab 273: E207-E213, 1997.
9. Henry PG, Oz G, Provencher S, Gruetter R. Toward dynamic isotopomer analysis in the rat brain in vivo: automatic quantitation of 13C NMR spectra using LC Model. NMR Biomed 16: 400-412, 2003.
10. Henry PG, Russeth KP, Tkac I, Drewes LR, Andrews MT, Gruetter R. Brain energy metabolism and neurotransmission at near-freezing temperatures: in vivo (1)H MRS study of a hibernating mammal. J Neurochem 101: 1505-1515, 2007.
11. Henry PG, Tkac I, Gruetter R. 1H-localized broadband 13C NMR spectroscopy of the rat brain in vivo at 9.4 T. Magn Reson Med 50: 684-692, 2003.
12. Inagaki T, Dutchak P, Zhao G, Ding X, Gautron L, Parameswara V, Li Y, Goetz R, Mohammadi M, Esser V, Elmquist JK, Gerard RD, Burgess SC, Hammer RE, Mangelsdorf DJ, Kliewer SA. Endocrine regulation of the fasting response by PPARα-mediated induction of fibroblast growth factor 21. Cell Metab 5: 415-425, 2007.
13. Krilowicz BL. Ketone body metabolism in a ground squirrel during hibernation and fasting. Am J Physiol Regul Integr Comp Physiol 249: R462-R470, 1985.
14. Lavau M, Fornari V, Hashim SA. Ketone metabolism in brain slices from rats with diet induced hyperketonemia. J Nutr 108: 621-639, 1978.
15. Leino RL, Gerhart DZ, Drewes LR. Monocarboxylate transporter (MCT1) abundance in brains of suckling and adult rats: a quantitative electron microscopic immunogold study. Brain Res Dev Brain Res 113: 47-54, 1999.
16. Leino RL, Gerhart DZ, Duelli R, Enerson BE, Drewes LR. Diet-induced ketosis increases monocarboxylate transporter (MCT1) levels in rat brain. Neurochem Int 38: 519-527, 2001.
17. Malloy CR, Sherry AD, Jeffrey FM. Analysis of tricarboxylic acid cycle of the heart using 13C isotope isomers. Am J Physiol Heart Circ Physiol 259: H987-H995, 1990.
18. Martin SL, Epperson LE, Rose JC, Kurtz CC, Ane C, Carey HV. Proteomic analysis of the winter-protected phenotype of hibernating ground squirrel intestine. Am J Physiol Regul Integr Comp Physiol 295: R316-R328, 2008.
19. Musacchia XJ, Ackerman PD, Entenman C. In vitro oxidation of [3-14C]acetoacetate in brain cortex from hibernating hamsters and ground squirrels. Comp Biochem Physiol B 55: 359-362, 1976.
20. Nehlig A, Pereira de Vasconcelos A. Glucose and ketone body utilization by the brain of neonatal rats. Prog Neurobiol 40: 163-221, 1993.
21. Page MA, Krebs HA, Williamson DH. Activities of enzymes of ketone-body utilization in brain and other tissues of suckling rats. Biochem J 121: 49-53, 1971.
22. Pengelley ET, Fisher KC. Rhythmical arousal from hibernation in the gold-mantled ground squirrel, Citellus lateralis tescorum. Can J Zool 39: 105-120, 1961.
23. Ponten U, Ratcheson RA, Salford LG, Siesjo BK. Optimal freezing conditions for cerebral metabolites in rats. J Neurochem 21: 1127-1138, 1973.
24. Pull I, McIlwain H. 3-Hydroxybutyrate dehydrogenase of rat brain on dietary change and during maturation. J Neurochem 18: 1163-1165, 1971.
25. Rauch JC, Behrisch HW. Ketone bodies: a source of energy during hibernation. Can J Zool 59: 754-760, 1981.
26. Robinson AM, Williamson DH. Physiological roles of ketone bodies as substrates and signals in mammalian tissues. Physiol Rev 60: 143-187, 1980.
27. Russeth KP, Higgins L, Andrews MT. Identification of proteins from non-model organisms using mass spectrometry: application to a hibernating mammal. J Proteome Res 5: 829-839, 2006.
28. Serkova NJ, Rose JC, Epperson LE, Carey HV, Martin SL. Quantitative analysis of liver metabolites in three stages of the circannual hibernation cycle in 13-lined ground squirrels by NMR. Physiol Genomics 31: 15-24, 2007.
29. Squire TL, Lowe ME, Bauer VW, Andrews MT. Pancreatic triacylglycerol lipase in a hibernating mammal. II Cold-adapted function and differential expression. Physiol Genomics 16: 131-140, 2003.
30. Staples JF, Hochachka PW. The effect of hibernation status and cold-acclimation on hepatocyte gluconeogenesis in the golden-mantled ground squirrel (Spermophilus lateralis). Can J Zool 76: 1734-1740, 1998.
31. VanItallie TB, Nufert TH. Ketones: metabolism's ugly duckling. Nutr Rev 61: 327-341, 2003.
32. Veech RL. The therapeutic implications of ketone bodies: the effects of ketone bodies in pathological conditions: ketosis, ketogenic diet, redox states, insulin resistance, and mitochondrial metabolism. Prostaglandins Leukot Essent Fatty Acids 70: 309-319, 2004.
33. Veech RL, Chance B, Kashiwaya Y, Lardy HA, Cahill GF Jr. Ketone bodies, potential therapeutic uses. IUBMB Life 51: 241-247, 2001.
34. Zhang WW, Churchill S, Churchill P. Developmental regulation of D-beta-hydroxybutyrate dehydrogenase in rat liver and brain. FEBS Lett 256: 71-74, 1989.
35. Ziegler A, Zaugg CE, Buser PT, Seelig J, Kunnecke B. Non-invasive measurements of myocardial carbon metabolism using in vivo 13C NMR spectroscopy. NMR Biomed 15: 222-234, 2002.