Cerebral glycolysis: A century of persistent misunderstanding and misconception

Frontiers in Neuroscience

Volumn 8, Issue OCT, 2014, Pages

  Schurr, Avital ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT; CARBOHYDRATE; LACTATE DEHYDROGENASE; LACTIC ACID; TRICARBOXYLIC ACID;

ANAEROBIC GLYCOLYSIS; BRAIN METABOLISM; BRAIN TISSUE; CARBOHYDRATE METABOLISM; CEREBRAL GLYCOLYSIS; CITRIC ACID CYCLE; GLYCOLYSIS; HUMAN; MITOCHONDRION; MUSCLE FATIGUE; NONHUMAN; OXIDATION; OXYGEN SUPPLY; REVIEW; SCIENTIST;

EID: 84910090293     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00360     Document Type: Review

References (129)

1. Adam, N. K. (1921) Note of the oxygen consumption of amphibian muscle and nerve. Biochem. J. 15, 358-362.
2. Ashford, C. A. and Holmes E. G. (1929) Contributions to the study of brain metabolism. V. Role of phosphates in lactic acid production. Biochem. J. 23, 748-759.
3. Ashford, C. A. and Holmes, E. G. (1931) Further observations on the oxidation of lactic acid by brain tissue. Biochem. J. 25, 2028-2049.
4. Atlante, A., de Bari, L., Bobba, A., Marra, E., and Passarella, S. (2007) Transport and metabolism of l-lactate occur in mitochondria from cerebellar granule cells and are modified in cells undergoing low potassium dependent apoptosis. Biochim. Biophys. Acta, 1767, 1285-1299.
5. Bak, L. K., Schousboe, A., Sonnewald, U., and Waagepetersen, H. S. (2006) Glucose is necessary to maintain neurotransmitter homeostasis during synaptic activity in cultured glutamatergic neurons. J. Cereb. Blood Flow Metab. 26, 1285-1297
6. Barber, B. (1961) Resistance by scientists to scientific discovery. Science, 134, 596-602.
7. Barcroft, J. and Orbeli, L. (1910) The influence of lactic acid upon the dissociation curve of blood. J. Physiol. 41, 355-367.
8. Bartlett, G. R. (1959) Human red blood cell glycolytic intermediates. J. Biol. Chem. 234, 449-458.
9. Berg, J.M., Tymoczko, J.L., Stryer, L. and Gatto, G.J., Jr., Editors (2012) Biochemistry, Seventh Edition. W. H. Freeman and Company, New York.
10. Bliss, T. M., and Sapolsky, R. M. (2001) Interactions among glucose, lactate and adenosine regulate energy substrate utilization in hippocampal cultures. Brain Res. 899, 134-141.
11. Bouzier-Sore, A-K., Voisin, P., Canioni, P., Magistretti, P. J., and Pellerin, L. (2003) Lactate is the preferential energy substrate over glucose for neurons in culture. J. Cereb. Blood Flow Metab. 23, 1298-1306.
12. Brandt, R.B., Laux, J.E., Spainhour, S.E., and Kline, E.S. (1987) Lactate dehydrogenase in rat mitochondria. Arch. Biochem. Biophys. 259, 412-422.
13. Brooks, G. A. (1985) Lactate: glycolytic product and oxidative substrate during sustained exercise in mammals-'the lactate shuttle'. In: Comparative physiology and biochemistry - currecnt topics and trends Vol A. Respiration-Metabolism-Circulation, Ed. R. Gilles, (Berlin: Springer-Verlag) 208-218.
14. Brooks, G. A. (1998) Mammalian fuel utilization during sustained exercise. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 120, 89-107.
15. Brooks, G.A., Brown, M.A., Butz, C.E., Sicurello, J.P., and Dubouchaud, H. (1999) Cardiac and skeletal muscle mitochondria have a monocarboxylate transporter MCT1. J. Appl. Physiol. 87, 1713-1718.
16. Brooks, G. A. (2000) Intra- and extra-cellular lactate shuttles. Med. Sci. Sports. Exerc. 32, 790-799
17. Brooks, G. A. (2002a) Lactate shuttle-between but not within cells? J. Physiol. 541, 333
18. Brooks, G. A. (2002b) Lactate shuttles in nature. Biochem. Soc. Trans. 30, 258-264
19. Brooks, G. A., Dubouchaud, H., Brown, M., Sicurello, J. P., and Butz, C. E. (1999) Role of mitochondrial lactate dehydrogenase and lactate oxidation in the intracellular lactate shuttle. Proc. Natl. Acad. Sci. USA. 96:1129-1134
20. Burridge, W. (1910) An inquiry into some chemical factors of fatigue. J. Physiol. 41, 285-307.
21. Chih, C-P., Lipton, P., and Roberts, E. L. Jr. (2001) Do active cerebral neurons really use lactate than glucose? Trends Neurosci. 24, 573-578.
22. Chih, C-P., and Roberts, E. L. Jr. (2003) Energy substrates for neurons during neural activity: a critical review of the astrocyte-neuron lactate shuttle hypothesis. J. Cereb. Blood Flow Metab. 23, 1263-1281.
23. Cruz, N. F., Ball, K. K, and Dienel, G. A. (2007) Functional imaging of focal brain activation in conscious rats: impact of [(14)C]glucose metabolite spreading and release. J. Neurosci. Res. 85:3254-3266.
24. Dalsgaard, M. K., Quistorff, B., Danielsen, E. R., Selmer, C., Vogelsang, T., and Secher, N. H. (2004) A reduced cerebral metabolic ratio in exercise reflects metabolism and not accumulation of lactate within the human brain. J. Physiol. 554, 571-578.
25. Devlin, T.M., Editor (2011) Textbook of Biochemistry with Clinical Correlations. Seventh Edition, John Wiley & Sons, Inc., Hoboken, NJ.
26. Dienel, G.A., and Hertz, L. (2001) Glucose and lactate metabolism during brain activation. J. Neurosci. Res. 66:824-838.
27. Dienel, G.A., and Cruz, N.F. (2004) Nutrition during brain activation: does cell-to-cell lactate shuttling contribute significantly to sweet and sour food for thought? Neurochem. Int. 45:321-351.
28. Dienel, G. A., and Hertz, L. (2005) Astrocytic contributions to bioenergetics of cerebral ischemia. Glia 50, 362-88.
29. Dienel, G.A. (2012) Brain lactate metabolism: the discoveries and the controversies. J. Cereb. Blood Flow Metab. 32:1107-1138.
30. Dienel, G.A. (2012) Fueling and imaging brain activation. ASN NEURO 4(5):art:e00093.doi:10.1042/AN20120021
31. Dixon, K. C. (1935) The oxidative disappearance of lactic acid from brain and the pasture effect reaction. Bichem. J. 29, 973-977.
32. Elustondo, P.A., White, A.E., Hughes, M.E., Brebner, K., Pavlov, E., and Kane, D.A. (2013) Physical and functional association of lactate dehydrogenase (LDH) with skeletal muscle mitochondria. J. Biol Chem. 288, 25309-25317.
33. Evans, C.L. (1925) Studies on the physiology of plain muscle. IV. The lactate acid content of plain muscle under various conditions. Biochem. J. 19, 1115-1127
34. Feldman, I. and Hill, L. (1911) The influence of oxygen inhalation on the lactic acid produced during hard work. J. Physiol. 42, 439-443.
35. Fletcher, W.M. (1898) The survival respiration of muscle. J. Physiol. 23, 10-99.
36. Fletcher, W.M., and Hopkins, F.G. (1907) Lactic acid in amphibian muscle. J. Physiol. 35, 247-309.
37. Fletcher, W.M. (1911) On the alleged formation of lactic acid in muscle during autolysis and post-survival periods. J Physiol. 43, 286-312.
38. Fletcher, W.M. (1913) Lactic acid formation, survival respiration and rigor mortis in mammalian muscle. J. Physiol. 47, 361-380.
39. Fletcher, W.M. and Brown, G.M. (1914) The carbon dioxide production and hear rigor in muscle, and the theory of intra-molecular oxygen. J. Physiol. 48, 177-204.
40. Fillenz, M. (2005) The role of lactate in brain metabolism. Neurochem. Int. 47, 413-417.
41. Foster, D.L., and Moyle, D.M. (1921) A contribution to the study of the interconversion of carbohydrate and lactic acid in muscle. Biochem. J. 15, 672-680.
42. Fox P.T. and Raichle, M.E. (1986) Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proce. Natl. Acad. Sci. USA, 83, 1140-1144.
43. Fox, P.T., Raichle, M.E., Mintun, M.A., and Dence, C. (1988) Nonoxidative glucose consumption during focal physiologic neural activity. Science, 241, 462-464.
44. 13C-labelled microdialysis and high-resolution nuclear magnetic resonance study. Brain, 132, 2839-2849.
45. Gandhi, G.K., Cruz, N.F., Ball, K.K., and Dienel, G.A. (2009) Astrocytes are poised for lactate trafficking and release from activated brain and for supply of glucose to neurons. J. Neurochem. 111:522-536.
46. Gerard, R.A., Hill, A.V., and Zotterman, Y. (1927) The effect of frequency of stimulation on the heat production of nerve. J. Physiol. 63, 130-143.
47. th Anniversary of lactate research in muscle. Exerc. Sport Sci. Rev. 36, 109-115.
48. Hartree, W., and Hill, A. V. (1922) The recovery heat production in muscle. J. Physiol. 56, 367-381.
49. Hartree, W., and Hill, A.V. (1923) The anaerobic processs involved in muscular activity. J. Physiol. 58, 127-137.
50. Hashimoto, T., Hussien, R., and Brooks, G.A. (2006) Colocalization of MCT1, CD147, and LDH in mitochondrial inner membrane of L6 muscle cells: evidence of a mitochondrial lactate oxidation complex. Am J Physiol Endocrinol Metab 290, E1237-E1244.
51. Herrero-Mendez, A., Almeida, A., Fernandez, E., Maestre, C., Moncada, S., and Bolanos, J.P. (2009) Nature Cell Biol. 11, 747-752.
52. Hertz, L. (2004) The astrocyte-neuron lactate shuttle: a challenge of a challenge. J. Cereb Blood Flow Metab. 24, 1241-1248.
53. Hertz, L., Peng, L., and Dienel, G. A. (2007) Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J. Neurosci. Res. 27, 219-249.
54. Hill, A.V. (1910) The heat produced in contracture and muscular tone. J. Physiol. 40, 389-403.
55. Hill, A.V. (1911) The position occupied by the production of heat, in the chain of processes constituting a muscular contraction. J. Physiol. 42, 1-43.
56. Hill, A.V. (1913) The energy degraded in the recovery processes of stimulated muscles. J. Physiol. 46, 28-80.
57. Hill, A.V. (1914) The oxidative removal of lactic acid. J. Physiol. 48, (Suppl) x-xi.
58. Hill, L. and Nabarro, D. N. (1895) On the exchange of blood-gases in brain and muscle during states of rest and activity. J. Physiol. 18, 218-229.
59. Holden, H.F. (1924) Experiemnts on respiration and fermentation. Biochem. J. 18, 535-542.
60. Holmes, E.G. (1930) Oxidations in central and peripheral nervous tissue. Biochem. J. 24, 914-925.
61. Holmes, E.G. (1932) The metabolism of brain and nerve. Ann Rev. Biochem. 1, 487-506.
62. Holmes, B.E. and Holmes E.G. (1925a) Contributions to the study of brain metabolism. I. Carbohydrate metabolism. Preliminary paper. Biochem. J. 19, 492-499.
63. Holmes, E.G. and Holmes, B.E. (1925b) Contributions to the study of brain metabolism. II. Carbohydrate metabolism. Biochem. J. 19, 836-839.
64. Holmes, E.G. and Holmes, B.E. (1926) Contributions to the study of brain metabolism. III. Carbohydrate metabolism relationship of glycogen and lactic acid. Biochem. J. 20, 1196-1203.
65. Holmes, E.G. and Holmes, B.E. (1927) Contributions to the study of brain metabolism. IV. Carbohydrate metabolism of the brain tissue of depancreatised cats. Biochem. J. 21, 412-418.
66. Holmes, E.G. and Ashford C.A. (1930) Lactic acid oxidation in brain with reference to the "Meyerfof cycle." Biochem. J. 1119-1127.
67. Holmes, E.G. (1933) The relation between carbohydrate metabolism and the function of the grey matter of the central nervous system. Biochem. J. 27, 523-536.
68. Hu, Y., and Wilson, G.S. (1997a) Rapid changes in local extracellular rat brain glucose observed with an in vivo glucose sensor. J. Neurochem. 68, 1745-1752.
69. Hu, Y., and Wilson G.S. (1997b) A temporary local energy pool coupled to neuronal activity: fluctuations of extracellular lactate levels in rat brain monitored with rapidresponse enzyme-based sensor. J. Neurochem. 69, 1484-1490.
70. Ito, H. (1916) The formation of d-lactic acid by the autolysis of pus. J. Biol. Chem. 26, 173-176.
71. Izumi, Y, Benz, A.M., Zorumski, C. F., Olney, J.W. (1994) Effect of lactate and pyruvate on glucose utilization in rat hippocampal slices. Neuroreport 5, 617-620.
72. Jacobs, R.A., Meinild, A-K., Nordsborg, N.B., and Lundby, C. (2013) Lactate oxidation in human skeletal muscle mitochondria. Endocrin. Metabol. 304, E686-E694
73. Kalimo, H., Rehncrona, S., Soderfeldt, B., Olsson, Y., Siejö, B.K. (1981) Brain lactic acidosis and ischemic cell-damage. 2. Histopathology. J Cereb Blood flow Metab, 1, 313-327.
74. Kasischke, K.A., Vishwasrao, H.D., Fisher, P.J., Zipfel, W.R., and Webb, W.W. (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305, 99-103.
75. Koehler, A.E. (1924) The acidosis of operative anesthesia. J. Biol. Chem. 62, 435-451.
76. Koehler, A.E., Brunquist, E. H., and Loevenhart, A. S. (1925) The production of acidosis by anoxemia. J. Biol. Chem. 64, 313-323.
77. Krebs, H.A. and Johnson, W.A. (1937a) The role of citric acid in intermediary metabolism in animal tissue. Enzymologia 4, 148-156.
78. Krebs, H. A. and Johnson, W.A. (1937b) Metabolism of ketonic acids in animal tissues. Biochem. J. 31, 64-660.
79. Krebs, H. A. and Johnson, W.A. (1937c) Acetopyruvic acid (αγdiketovaleric acid) as an intermediate metabolite in animal tissues. Bichem. J. 31, 772-779.
80. Krebs, H.A., Salvin, E. and Johnson, W.A. (1938) The formation of citric and α-ketoglutaric acids in the mammalian body. Bichem. J. 32, 113-117.
81. rd Edn, (The University of Chicago Press, Ltd., London).
82. Larrabee, M.G. (1995) Lactate metabolism and its effects on glucose metabolism in the excised neural tissue. J. Neurochem. 64, 1734-41.
83. 2 production between glucose and lactate in excised sympathetic ganglia, with implications for brain. J. Neurochem. 67, 1726-1734.
84. Lemire, J., Mailloux, R.J., and Appanna, V.D. (2008) Mitochondrial lactate dehydrogenase is involved in oxidative-energy metabolism in human astrocytoma cells (CCF-STTG1). PLoS ONE 3(2): e1550. doi:10.1371/journal.pone.0001550
85. Lock, F.S., and Rosenheim, O. (1907) Contributions to the physiology of the isolated heart. The consumption of dextrose by mammalian cardiac muscle. J. Physiol. 36, 205-220.
86. Magistretti, P.J., and Pellerin, L. (1999) Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos. Tarns. R. Soc. Lond. B. Biol. Sc. 354, 1155-1163.
87. Magistretti, P.J., Pellerin, L., Rothman, D.L., Shulamn, R.G. (1999) Energy on demand. Science 283, 496-497.
88. Magistretti, P.J. (2000) Cellular bases of functional brain imaging: insights from neuronglia metabolic coupling. Brain Res. 886, 108-112.
89. Mangia, S., Garreffa, G., Bianciardi, M., Giove, F., Di Salle, F., and Maraviglia, B. (2003) The aerobic brain: lactate decrease at the onset of neural activity. Neuroscience 118, 7-10.
90. Margolis, H. (1993) Paradigms and barriers: how habits of mind govern scientific beliefs. (The University of Chicago Press, Ltd., London).
91. Marriott, W.M. (1914) The blood in acidosis from the quantitative standpoint. J Biol. Chem. 18, 507-517.
92. McKenna, M.C., Waagepetersen, H.S., Schousboe, A., Sonnewald, U. (2006) Neuronal and astrocytic shuttle mechanisms for cytosolic-mitochondrial transfer of reducing equivalents: current evidence and pharmacological tools. Biochem Pharmacol 71, 399-407.
93. Mowbray, J. (1975) A mitochondrial monocarboxylate transporter in rat liver and heart and its possible function in cell control. Biochem. J. 148, 41-47.
94. Pardo, B., Contreras, L., Serrano A., Ramos, M., Kobayashi, K., Iijima, M., Saheki, T., and Satrustegui, J. (2006) Essential role of aralar in the transduction of small Ca2+ signals to neuronal mitochondria. J Biol Chem 281,1039-1047.
95. Passarella, S., de Bari, L., Valenti, D., Pizzuto, R., Paventi, G., and Altane, A. (2008) Miochondria and l-lactate metabolism. FEBS Lett. 582, 3569-3576.
96. Pellerin, L., and Magistretti, P.J. (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. USA 91, 10625-10629.
97. Pellerin, L., and Magistretti, P.J. (2003) Food for thought: challenging the dogmas. J. Cereb. Blood Flow Metab. 23, 1282-1286.
98. Peters, R.A. (1913) The heat production of fatigue and its relation to the production of lactic acid in amphibian muscle. J. Physiol. 47, 243-271.
99. Ponsot, E., Zoll, J., N'Guessan, B., Ribera, F., Lampert, E., Richard, R., Veksler, V., Ventura-Clapier, R. and Mettauer, B. (2005). Mitochondrial tissue specificity of substrates utilization in rat cardiac and skeletal muscles. J. Cell Physiol. 203, 479-486.
100. Qu, H., Haberg, A., Haraldseth, O., Unsgard, G., and Sonnewald, U. (2000) (13)CMR spectroscopy study of lactate as substrate for rat brain. Dev Neurosci. 22, 429-436
101. Quastel, J.H. and Wheatley, A.H.M. (1932) Oxidations by the brain. Biochem. J. 26, 725-744.
102. Ransom, F. (1910) A contribution to the study of muscle-enzymes. J. Physiol. 40, 1-16.
103. Rasmussen, H.N., van Hall, G. and Rasmussen, U.F. (2002) Lactate dehydrogenase is not a mitochondrial enzyme in human and mouse vastus lateralis muscle. J. Physiol. 541, 575-580.
104. Rehncrona, S., Rosen, I., Seisö, B.K. (1981) Brain lactic acidosis and ischemic celldamage. Rehncrona, S., Rosen, I., Seisö, B.K. Biochemistry and neurophysiology. J Cereb Blood flow Metab, 1, 297-311.
105. Riegel, C. (1927a) Formation of lactic acid in the body after severe hemorrhage. J. Biol. Chem. 74, 123-134.
106. Riegel, C. (1927b) The rate of disappearance of sodium lactate injected intravenously and its effect upon sugar and inorganic phosphate of the blood.
107. Ringer, A.I. (1914) Studies in diabetes. I. Theory of diabetes, with consideration of the probable mechanism of antiketogenesis and the cause of acidosis. J. Biol Chem. 17, 107-119.
108. Roaf, H.E. (1914) The time relations of acid production in muscle during contraction. J. Physiol. 48, 380-391.
109. Ronzoni, E., Koechig, I., and Eaton, E. (1924) Ether Anesthesia. III. Role of lactic acid in the acidosis of ether anesthesia. J. Biol. Chem. 61, 465-492.
110. Sahlin, K., Fernstrom, M. and Tonkonogi, M. (2002) No evidence of an intracellular lactate shuttle in rat skeletal muscle. J. Physiol. 541, 569-574
111. Schurr, A. West C.A., and Rigor, B.M. (1988) Lactate-supported synaptic function in the rat hippocampal slice preparation. Science, 240, 1326-1328.
112. Schurr, A., Payne, R.S., Miller, J.J., and Rigor, B.M. (1997a) Brain lactate, not glucose, fuels the recovery of synaptic function from hypoxia upon reoxygenation: an in vitro study. Brain Res. 744, 105-111.
113. Schurr, A., Payne, R.S., Miller, J.J., and Rigor, B.M. (1997b) Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia: Further in vitro validation. J. Neurochem. 69, 423-426.
114. Schurr, A., and Rigor, B.M. (1998) Brain anaerobic lactate production: a suicide note or a survival kit? Dev. Neurosci. 20, 348-357.
115. Schurr, A., Miller J.J., Payne R.S., and Rigor, B.M. (1999a) An increase in lactate output by brain tissue serves to meet the energy needs of glutamate-activated neurons. J. Neurosci. 19, 34-39.
116. Schurr, A., Payne, R.S., Miller, J.J., and Rigor, B.M. (1999b) Study of cerebral energy metabolism using the rat hippocampal slice preparation. Methods: A Companion to Methods in Enzymology 18, 117-126.
117. Schurr, A., and Payne, R.S. (2007) Lactate, not pyruvate, is neuronal aerobic glycolysis end product: an in vitro electrophysiological study. Neuroscience, 147, 613-619.
118. Schurr, A., and Gozal, E. (2012) Aerobic production and utilization of lactate satisfy increased energy demands upon neuronal activation in hippocampal slices and provide neuroprotection against oxidative stress. Front. Pharmacol., 2011; 2: 96, doi: 10.3389/fphar.2011.00096
119. Shulman, R.G., and Rothman, D.L. (2001) The "glycogen shunt" in exercising muscle: A role for glycogen in muscle energetic and fatigue. Proc. Natl. Acad. Sci. USA 98, 457-461.
120. Siesjö, B.K. (1981) Cell-damage in the brain-a speculative synthesis. J Cereb Blood flow Metab, 1, 155-185.
121. Smith, D., Pernet, A., Hallett, W.A., Bingham, E., Marsden, P.K., and Amiel, S.A. (2003) Lactate: a preferred fuel for human brain metabolism in vivo. J. Cereb. Blood Flow Metab. 23, 658-664.
122. Stryer, L., Editor (1995) Biochemistry, Fourth Edition, Chap. 19, p 483. W. H. Freeman and Company, New York.
123. TASHIRO, S. (1913) Carbon dioxide production from nerve fibres when resting and when stimulated; a contribution to the chemical basis of irritability. Am. J. Physiol. 32, 107-136.
124. Tsacopoulos, M., and Magistretti, P.J. (1996) Metabolic coupling between glia and neurons. J. Neurosci. 16, 877-885
125. Tsuji, K. (1916) Lactic acid metabolism in the isolated heart (heart lung preparation). J. Physiol. 50, 312-321.
126. Underhill, F.P., and Black, C.L. (1912) The influence of cocaine upon metabolism with special reference to the elimination of lactic acid. J. Biol. Chem. 11, 235-252.
127. Van Hall, G. (2000) Lactate as a fuel for mitochondrial respiration. Acta Physiol. Scand. 168, 643-656.
128. Yoshida, Y., Holloway, G.P., Ljubicic, V., Hatta, H., Spriet, L.L., Hood, D.A. and Bonen, A. (2007) Negligible direct lactate oxidation in subsarcolemmal and intermyofibrillar mitochondria obtained from red and white rat skeletal muscle. J. Physiol. 582, 1317-1335
129. Zielke, H.R., Zielke, C.L., and Baab, P.J. (2009) Direct measurement of oxidative metabolism in the living brain by microdialysis: a review. J. Neurochem. 109 (Suppl. 1), 24-29.