Roles and regulation of ketogenesis in cultured astroglia and neurons under hypoxia and hypoglycemia

ASN Neuro

Volumn 6, Issue 5, 2014, Pages

  Takahashi, Shinichi ^a   Iizumi, Takuya ^a   Mashima, Kyoko ^a   Abe, Takato ^a   Suzuki, Norihiro ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Acetoacetate; AMP activated protein kinase; B hydroxybutyrate; Ketone bodies; Long chain fatty acids; Palmitic acid

Indexed keywords

CELL PROTEIN; CILOSTAZOL; LACTIC ACID; METFORMIN; PYRUVIC ACID; ROTENONE; 3 HYDROXYBUTYRIC ACID; ACETOACETIC ACID; ACETOACETIC ACID DERIVATIVE; CARBON; CARNITINE; KETONE BODY; PALMITIC ACID; PYRUVATE DEHYDROGENASE;

AEROBIC METABOLISM; ANIMAL CELL; ARTICLE; ASTROCYTE; GLUCOSE OXIDATION; HYPOGLYCEMIA; HYPOXIA; ISCHEMIA; KETOGENESIS; MACROGLIA; NERVE CELL; NONHUMAN; PROTEIN EXPRESSION; RAT; REPERFUSION; SPECTROPHOTOMETRY; ANIMAL; ANIMAL EMBRYO; ANOXIA; BRAIN CORTEX; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; METABOLISM; SPRAGUE DAWLEY RAT; TIME;

3-HYDROXYBUTYRIC ACID; ACETOACETATES; ANIMALS; ANOXIA; ASTROCYTES; CARBON ISOTOPES; CARNITINE; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; KETONE BODIES; NEURONS; PALMITIC ACID; PYRUVATE DEHYDROGENASE (LIPOAMIDE); RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 84930817386     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1177/1759091414550997     Document Type: Article

References (49)

1. Abe T., Takahashi S., & Suzuki N. (2006) Oxidative metabolism in cultured rat astroglia: Effects of reducing the glucose concentration in the culture medium and of D-aspartate or potassium stimulation. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism 26: 153–160.
2. Andres R., Cader G., & Zierler K. L. (1956) The quantitatively minor role of carbohydrate in oxidative metabolism by skeletal muscle in intact man in the basal state; measurements of oxygen and glucose uptake and carbon dioxide and lactate production in the forearm. The Journal of Clinical Investigation 35: 671–682.
3. Auestad N., Korsak R. A., Morrow J. W., & Edmond J. (1991) Fatty acid oxidation and ketogenesis by astrocytes in primary culture. Journal of Neurochemistry 56: 1376–1386.
4. Blazquez C., Sanchez C., Velasco G., & Guzman M. (1998) Role of carnitine palmitoyltransferase I in the control of ketogenesis in primary cultures of rat astrocytes. Journal of Neurochemistry 71: 1597–1606.
5. Blazquez C., Woods A., de Ceballos M. L., Carling D., & Guzman M. (1999) The AMP-activated protein kinase is involved in the regulation of ketone body production by astrocytes. Journal of Neurochemistry 73: 1674–1682.
6. Cardell M., Koide T., & Wieloch T. (1989) Pyruvate dehydrogenase activity in the rat cerebral cortex following cerebral ischemia. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism 9: 350–357.
7. Clarke D. D., & Sokoloff L (1999) Circulation and energy metabolism of the brain. In: Siegel G., Agranoff B., Albers R. W., & Fisher S. (eds) Basic neurochemistry: Molecular, cellular, and medical aspects, 6th ed. Philadelphia, PA: Lippincott-Raven, pp. 637–669.
8. Corton J. M., Gillespie J. G., Hawley S. A., & Hardie D. G. (1995) 5-aminoimidazole-4-carboxamide ribonucleoside A specific method for activating AMP-activated protein kinase in intact cells? European Journal of Biochemistry/FEBS 229: 558–565.
9. Dhopeshwarkar G. A., & Mead J. F. (1973) Uptake and transport of fatty acids into the brain and the role of the blood-brain barrier system. Advances in Lipid Research 11: 109–142.
10. Dienel G. A (2009) Energy metabolism in the brain. In: Byrne J. H., & Roberts J. L. (eds) From molecules to networks: An introduction to cellular and molecular neuroscience, 2nd ed. London, England: Academic Press, pp. 49–110.
11. Driscoll B. F., Deibler G. E., Law M. J., & Crane A. M. (1993) Damage to neurons in culture following medium change: Role of glutamine and extracellular generation of glutamate. Journal of Neurochemistry 61: 1795–1800.
12. Edmond J., Auestad N., Robbins R. A., & Bergstrom J. D. (1985) Ketone body metabolism in the neonate: Development and the effect of diet. Federation Proceedings 44: 2359–2364.
13. Edmond J., Robbins R. A., Bergstrom J. D., Cole R. A., & de Vellis J. (1987) Capacity for substrate utilization in oxidative metabolism by neurons, astrocytes, and oligodendrocytes from developing brain in primary culture. Journal of Neuroscience Research 18: 551–561.
14. Foretz M., Hebrard S., Leclerc J., Zarrinpashneh E., Soty M., Mithieux G., Viollet B. (2010) Metformin inhibits hepatic gluconeogenesis in mice independently of the LKB1/AMPK pathway via a decrease in hepatic energy state. The Journal of Clinical Investigation 120: 2355–2369.
15. Fukuchi T., Katayama Y., Kamiya T., McKee A., Kashiwagi F., Terashi A. (1998) The effect of duration of cerebral ischemia on brain pyruvate dehydrogenase activity, energy metabolites, and blood flow during reperfusion in gerbil brain. Brain Research 792: 59–65.
16. Fulgencio J. P., Kohl C., Girard J., & Pegorier J. P. (2001) Effect of metformin on fatty acid and glucose metabolism in freshly isolated hepatocytes and on specific gene expression in cultured hepatocytes. Biochemical Pharmacology 62: 439–446.
17. Guzman M., & Blazquez C. (2001) Is there an astrocyte-neuron ketone body shuttle? Trends in Endocrinology and Metabolism 12: 169–173.
18. Guzman M., & Blazquez C. (2004) Ketone body synthesis in the brain: Possible neuroprotective effects. Prostaglandins, Leukotrienes, and Essential Fatty Acids 70: 287–292.
19. Guzman M., & Geelen M. J. (1993) Regulation of fatty acid oxidation in mammalian liver. Biochimica et Biophysica Acta 1167: 227–241.
20. Izawa Y., Takahashi S., & Suzuki N. (2009) Pioglitazone enhances pyruvate and lactate oxidation in cultured neurons but not in cultured astroglia. Brain Research 1305: 64–73.
21. Kelley D. E., Reilly J. P., Veneman T., & Mandarino L. J. (1990) Effects of insulin on skeletal muscle glucose storage, oxidation, and glycolysis in humans. The American Journal of Physiology 258: E923–E929.
22. Laun R. A., Rapsch B., Abel W., Schroder O., Roher H. D., Ekkernkamp A., Schulte K. M. (2001) The determination of ketone bodies: Preanalytical, analytical and physiological considerations. Clinical and Experimental Medicine 1: 201–209.
23. Leary S. C., Hill B. C., Lyons C. N., Carlson C. G., Michaud D., Kraft C. S., Moyes C. D. (2002) Chronic treatment with azide in situ leads to an irreversible loss of cytochrome c oxidase activity via holoenzyme dissociation. The Journal of Biological Chemistry 277: 11321–11328.
24. Mathiisen T. M., Lehre K. P., Danbolt N. C., & Ottersen O. P. (2010) The perivascular astroglial sheath provides a complete covering of the brain microvessels: An electron microscopic 3D reconstruction. Glia 58: 1094–1103.
25. McKenna M. C. (2012) Substrate competition studies demonstrate oxidative metabolism of glucose, glutamate, glutamine, lactate and 3-hydroxybutyrate in cortical astrocytes from rat brain. Neurochemical Research 37: 2613–2626.
26. McKenna M. C., Tildon J. T., Stevenson J. H., Boatright R., & Huang S. (1993) Regulation of energy metabolism in synaptic terminals and cultured rat brain astrocytes: Differences revealed using aminooxyacetate. Developmental Neuroscience 15: 320–329.
27. Miller R. A., Chu Q., Xie J., Foretz M., Viollet B., Birnbaum M. J. (2013) Biguanides suppress hepatic glucagon signalling by decreasing production of cyclic AMP. Nature 494: 256–260.
28. Mitchell R. W., On N. H., Del Bigio M. R., Miller D. W., & Hatch G. M. (2011) Fatty acid transport protein expression in human brain and potential role in fatty acid transport across human brain microvessel endothelial cells. Journal of Neurochemistry 117: 735–746.
29. Nehlig A. (2004) Brain uptake and metabolism of ketone bodies in animal models. Prostaglandins, Leukotrienes, and Essential Fatty Acids 70: 265–275.
30. Nishizawa Y. (2001) Glutamate release and neuronal damage in ischemia. Life Sciences 69: 369–381.
31. Pan J. W., de Graaf R. A., Petersen K. F., Shulman G. I., Hetherington H. P., Rothman D. L. (2002) [2,4-13C2]-betahydroxybutyrate metabolism in human brain. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism 22: 890–898.
32. Pan J. W., Rothman T. L., Behar K. L., Stein D. T., & Hetherington H. P. (2000) Human brain beta-hydroxybutyrate and lactate increase in fasting-induced ketosis. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism 20: 1502–1507.
33. Pan J. W., Telang F. W., Lee J. H., de Graaf R. A., Rothman D. L., Stein D. T., Hetherington H. P. (2001) Measurement of betahydroxybutyrate in acute hyperketonemia in human brain. Journal of Neurochemistry 79: 539–544.
34. Pellerin L., & Magistretti P. J. (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: A mechanism coupling neuronal activity to glucose utilization. Proceedings of the National Academy of Sciences of the United States of America 91: 10625–10629.
35. Prins M. L. (2008) Cerebral metabolic adaptation and ketone metabolism after brain injury. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism 28: 1–16.
36. Puchowicz M. A., Zechel J. L., Valerio J., Emancipator D. S., Xu K., Pundik S., Lust W. D. (2008) Neuroprotection in dietinduced ketotic rat brain after focal ischemia. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism 28: 1907–1916.
37. Robinson A. M., & Williamson D. H. (1980) Physiological roles of ketone bodies as substrates and signals in mammalian tissues. Physiological Reviews 60: 143–187.
38. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Klenk D. C. (1985) Measurement of protein using bicinchoninic acid. Analytical Biochemistry 150: 76–85.
39. Smith Q. R., & Nagura H. (2001) Fatty acid uptake and incorporation in brain: Studies with the perfusion model. Journal of Molecular Neuroscience 16: 167–172.
40. Taıb B., Bouyakdan K., Hryhorczuk C., Rodaros D., Fulton S., Alquier T. (2013) Glucose regulates hypothalamic long-chain fatty acid metabolism via AMP-activated kinase (AMPK) in neurons and astrocytes. The Journal of Biological Chemistry 288: 37216–37229.
41. Takahashi S., Driscoll B. F., Law M. J., & Sokoloff L. (1995) Role of sodium and potassium ions in regulation of glucose metabolism in cultured astroglia. Proceedings of the National Academy of Sciences of the United States of America 92: 4616–4620.
42. Takahashi S., Izawa Y., & Suzuki N. (2011) Cilostazol enhances oxidative glucose metabolism in both neurons and astroglia without increasing ROS production. Pharmacology & Pharmacy 2: 315–321.
43. Takahashi S., Izawa Y., & Suzuki N. (2012a) Astroglial pentose phosphate pathway rates in response to high-glucose environments. ASN Neuro 4(2): e00078 doi:10.1042/AN20120002
44. Takahashi S., Izawa Y., & Suzuki N. (2012b) Astrogliopathy as a loss of astroglial protective function against glycoxidative stress under hyperglycemia. Clinical Neurology 52: 41–51.
45. Thompson P. E., Manganiello V., & Degerman E. (2007) Re-discovering PDE3 inhibitors—New opportunities for a long neglected target. Current Topics in Medicinal Chemistry 7: 421–436.
46. Vannucci S. J., & Simpson I. A. (2003) Developmental switch in brain nutrient transporter expression in the rat. American Journal of Physiology Endocrinology and Metabolism 285: E1127–E1134.
47. Veech R. L. (2004) 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, Leukotrienes, and Essential Fatty Acids 70: 309–319.
48. Waniewski R. A., & Martin D. L. (2004) Astrocytes and synaptosomes transport and metabolize lactate and acetate differently. Neurochemical Research 29: 209–217.
49. Zang Y., Yu L. F., Pang T., Fang L. P., Feng X., Wen T. Q., Li J. (2008) AICAR induces astroglial differentiation of neural stem cells via activating the JAK/STAT3 pathway independently of AMP-activated protein kinase. The Journal of Biological Chemistry 283: 6201–6208.