Glycolysis and the significance of lactate in traumatic brain injury

Frontiers in Neuroscience

Volumn 9, Issue APR, 2015, Pages

  Carpenter, Keri L H ^a   Jalloh, Ibrahim ^a   Hutchinson, Peter J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cerebral energy metabolism; Glucose; Glycolysis; Lactate; Microdialysis; Pyruvate; Traumatic brain injury (human)

Indexed keywords

LACTIC ACID;

ASTROCYTE; BRAIN LEVEL; CARBON NUCLEAR MAGNETIC RESONANCE; CITRIC ACID CYCLE; GLIA; GLYCOLYSIS; HUMAN; LACTATE BLOOD LEVEL; MICRODIALYSIS; NONHUMAN; OUTCOME ASSESSMENT; REVIEW; TRAUMATIC BRAIN INJURY;

EID: 84928664214     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00112     Document Type: Review

References (77)

1. Alessandri, B., Schwandt, E., Kamada, Y., Nagata, M., Heimann, A., and Kempski, O. (2012). The neuroprotective effect of lactate is not due to improved glutamate uptake after controlled cortical impact in rats. J. Neurotrauma 29, 2181-2191. doi: 10.1089/neu.2011.2067
2. Bak, L. K., Walls, A. B., Schousboe, A., Ring, A., Sonnewald, U., and Waagepetersen, H. S. (2009). Neuronal glucose but not lactate utilization is positively correlated with NMDA-induced neurotransmission and fluctuations in cytosolic Ca2+ levels. J. Neurochem. 109 (Suppl. 1), 87-93. doi: 10.1111/j.1471-4159.2009.05943.x
3. Bartnik, B. L., Lee, S. M., Hovda, D. A., and Sutton, R. L. (2007). The fate of glucose during the period of decreased metabolism after fluid percussion injury: a 13C NMR study. J. Neurotrauma 24, 1079-1092. doi: 10.1089/neu.2006.0210
4. Bartnik, B. L., Sutton, R. L., Fukushima, M., Harris, N. G., Hovda, D. A., and Lee, S. M. (2005). Upregulation of pentose phosphate pathway and preservation of tricarboxylic acid cycle flux after experimental brain injury. J. Neurotrauma 22, 1052-1065. doi: 10.1089/neu.2005.22.1052
5. Befroy, D. E., Rothman, D. L., Petersen, K. F., and Shulman, G. I. (2012). (31)P-magnetization transfer magnetic resonance spectroscopy measurements of in vivo metabolism. Diabetes 61, 2669-2678. doi: 10.2337/db12-0558
6. Bensinger, S. J., and Christofk, H. R. (2012). New aspects of the Warburg effect in cancer cell biology. Semin. Cell Dev. Biol. 23, 352-361. doi: 10.1016/j.semcdb.2012.02.003
7. Ben-Yoseph, O., Boxer, P. A., and Ross, B. D. (1996). Assessment of the role of the glutathione and pentose phosphate pathways in the protection of primary cerebrocortical cultures from oxidative stress. J. Neurochem. 66, 2329-2337. doi: 10.1046/j.1471-4159.1996.66062329.x
8. Beutler, E., Yeh, M., and Fairbanks, V. F. (1962). The normal human female as a mosaic of X-chromosome activity: studies using the gene for C-6-PD-deficiency as a marker. Proc. Natl. Acad. Sci. U.S.A. 48, 9-16. doi: 10.1073/pnas.48.1.9
9. Bittar, P. G., Charnay, Y., Pellerin, L., Bouras, C., and Magistretti, P. J. (1996). Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J. Cereb. Blood Flow Metab. 16, 1079-1089. doi: 10.1097/00004647-199611000-00001
10. Boumezbeur, F., Petersen, K. F., Cline, G. W., Mason, G. F., Behar, K. L., Shulman, G. I., et al. (2010). The contribution of blood lactate to brain energy metabolism in humans measured by dynamic 13C nuclear magnetic resonance spectroscopy. J. Neurosci. 30, 13983-13991. doi: 10.1523/JNEUROSCI.2040-10.2010
11. Bouzat, P., Sala, N., Suys, T., Zerlauth, J. B., Marques-Vidal, P., Feihl, F., et al. (2014). Cerebral metabolic effects of exogenous lactate supplementation on the injured human brain. Intensive Care Med. 40, 412-421. doi: 10.1007/s00134-013-3203-6
12. Brekke, E. M., Morken, T. S., Wideroe, M., Haberg, A. K., Brubakk, A. M., and Sonnewald, U. (2014). The pentose phosphate pathway and pyruvate carboxylation after neonatal hypoxic-ischemic brain injury. J. Cereb. Blood Flow Metab. 34, 724-734. doi: 10.1038/jcbfm.2014.8
13. Cappellini, M. D., and Fiorelli, G. (2008). Glucose-6-phosphate dehydrogenase deficiency. Lancet 371, 64-74. doi: 10.1016/S0140-6736(08)60073-2
14. Carpenter, K. L., Jalloh, I., Gallagher, C. N., Grice, P., Howe, D. J., Mason, A., et al. (2014). (13)C-labelled microdialysis studies of cerebral metabolism in TBI patients. Eur. J. Pharm. Sci. 57, 87-97. doi: 10.1016/j.ejps.2013.12.012
15. Chesnut, R. M., Marshall, L. F., Klauber, M. R., Blunt, B. A., Baldwin, N., Eisenberg, H. M., et al. (1993). The role of secondary brain injury in determining outcome from severe head injury. J. Trauma 34, 216-222. doi: 10.1097/00005373-199302000-00006
16. 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. doi: 10.1097/01.WCB.0000081369.51727.6F
17. Cruz, F., and Cerdan, S. (1999). Quantitative 13C NMR studies of metabolic compartmentation in the adult mammalian brain. NMR Biomed. 12, 451-462.
18. De Bock, K., Georgiadou, M., Schoors, S., Kuchnio, A., Wong, B. W., Cantelmo, A. R., et al. (2013). Role of PFKFB3-driven glycolysis in vessel sprouting. Cell 154, 651-663. doi: 10.1016/j.cell.2013.06.037
19. Dienel, G. A. (2014). Lactate shuttling and lactate use as fuel after traumatic brain injury: metabolic considerations. J. Cereb. Blood Flow Metab. 34, 1736-1748. doi: 10.1038/jcbfm.2014.153
20. Domanska-Janik, K. (1988). Hexose monophosphate pathway activity in normal and hypoxic rat brain. Resuscitation 16, 79-90. doi: 10.1016/0300-9572(88)90073-1
21. Dusick, J. R., Glenn, T. C., Lee, W. N., Vespa, P. M., Kelly, D. F., Lee, S. M., et al. (2007). Increased pentose phosphate pathway flux after clinical traumatic brain injury: a [1,2-13C2]glucose labeling study in humans. J. Cereb. Blood Flow Metab. 27, 1593-1602. doi: 10.1038/sj.jcbfm.9600458
22. Fink, M. P. (2007). Ethyl pyruvate: a novel anti-inflammatory agent. J. Intern. Med. 261, 349-362. doi: 10.1111/j.1365-2796.2007.01789.x
23. Gallagher, C. N., Carpenter, K. L., Grice, P., Howe, D. J., Mason, A., Timofeev, I., et al. (2009). The human brain utilizes lactate via the tricarboxylic acid cycle: a 13C-labelled microdialysis and high-resolution nuclear magnetic resonance study. Brain 132(Pt 10), 2839-2849. doi: 10.1093/brain/awp202
24. Galow, L. V., Schneider, J., Lewen, A., Ta, T. T., Papageorgiou, I. E., and Kann, O. (2014). Energy substrates that fuel fast neuronal network oscillations. Front. Neurosci. 8:398. doi: 10.3389/fnins.2014.00398
25. Garnett, M. R., Corkill, R. G., Blamire, A. M., Rajagopalan, B., Manners, D. N., Young, J. D., et al. (2001). Altered cellular metabolism following traumatic brain injury: a magnetic resonance spectroscopy study. J. Neurotrauma 18, 231-240. doi: 10.1089/08977150151070838
26. Gendrel, A. V., and Heard, E. (2011). Fifty years of X-inactivation research. Development 138, 5049-5055. doi: 10.1242/dev.068320
27. Harper, P. S. (2011). Mary Lyon and the hypothesis of random X chromosome inactivation. Hum. Genet. 130, 169-174. doi: 10.1007/s00439-011-1013-x
28. Holloway, R., Zhou, Z., Harvey, H. B., Levasseur, J. E., Rice, A. C., Sun, D., et al. (2007). Effect of lactate therapy upon cognitive deficits after traumatic brain injury in the rat. Acta Neurochir. (Wien) 149, 919-927; discussion 927. doi: 10.1007/s00701-007-1241-y
29. Hutchinson, P. J., O'Connell, M. T., Seal, A., Nortje, J., Timofeev, I., Al-Rawi, P. G., et al. (2009). A combined microdialysis and FDG-PET study of glucose metabolism in head injury. Acta Neurochir. (Wien) 151, 51-61; discussion 61. doi: 10.1007/s00701-008-0169-1
30. Ichai, C., Armando, G., Orban, J. C., Berthier, F., Rami, L., Samat-Long, C., et al. (2009). Sodium lactate versus mannitol in the treatment of intracranial hypertensive episodes in severe traumatic brain-injured patients. Intensive Care Med. 35, 471-479. doi: 10.1007/s00134-008-1283-5
31. Ichai, C., Payen, J. F., Orban, J. C., Quintard, H., Roth, H., Legrand, R., et al. (2013). Half-molar sodium lactate infusion to prevent intracranial hypertensive episodes in severe traumatic brain injured patients: a randomized controlled trial. Intensive Care Med. 39, 1413-1422. doi: 10.1007/s00134-013-2978-9
32. Ide, K., Schmalbruch, I. K., Quistorff, B., Horn, A., and Secher, N. H. (2000). Lactate, glucose and O2 uptake in human brain during recovery from maximal exercise. J. Physiol. 522(Pt 1), 159-164. doi: 10.1111/j.1469-7793.2000.t01-2-00159.xm
33. Ivanov, A. I., Malkov, A. E., Waseem, T., Mukhtarov, M., Buldakova, S., Gubkina, O., et al. (2014). Glycolysis and oxidative phosphorylation in neurons and astrocytes during network activity in hippocampal slices. J. Cereb. Blood Flow Metab. 34, 397-407. doi: 10.1038/jcbfm.2013.222
34. Jalloh, I., Carpenter, K. L., Grice, P., Howe, D. J., Mason, A., Gallagher, C. N., et al. (2015). Glycolysis and the pentose phosphate pathway after human traumatic brain injury: microdialysis studies using 1,2-(13)C2 glucose. J. Cereb. Blood Flow Metab. 35, 111-120. doi: 10.1038/jcbfm.2014.177
35. Jalloh, I., Carpenter, K. L., Helmy, A., Carpenter, T. A., Menon, D. K., and Hutchinson, P. J. (2014). Glucose metabolism following human traumatic brain injury: methods of assessment and pathophysiological findings. Metab. Brain Dis. doi: 10.1007/s11011-014-9628-y. [Epub ahead of print].
36. Jalloh, I., Helmy, A., Shannon, R. J., Gallagher, C. N., Menon, D. K., Carpenter, K. L., et al. (2013). Lactate uptake by the injured human brain: evidence from an arteriovenous gradient and cerebral microdialysis study. J. Neurotrauma 30, 2031-2037. doi: 10.1089/neu.2013.2947
37. John, S., Weiss, J. N., and Ribalet, B. (2011). Subcellular localization of hexokinases I and II directs the metabolic fate of glucose. PLoS ONE 6:e17674. doi: 10.1371/journal.pone.0017674
38. Katayama, Y., Becker, D. P., Tamura, T., and Hovda, D. A. (1990). Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J. Neurosurg. 73, 889-900. doi: 10.3171/jns.1990.73.6.0889
39. Kawamata, T., Katayama, Y., Hovda, D. A., Yoshino, A., and Becker, D. P. (1992). Administration of excitatory amino acid antagonists via microdialysis attenuates the increase in glucose utilization seen following concussive brain injury. J. Cereb. Blood Flow Metab. 12, 12-24. doi: 10.1038/jcbfm.1992.3
40. Kramer, A. H., Roberts, D. J., and Zygun, D. A. (2012). Optimal glycemic control in neurocritical care patients: a systematic review and meta-analysis. Crit. Care 16, R203. doi: 10.1186/cc11812
41. Lebon, V., Petersen, K. F., Cline, G. W., Shen, J., Mason, G. F., Dufour, S., et al. (2002). Astroglial contribution to brain energy metabolism in humans revealed by 13C nuclear magnetic resonance spectroscopy: elucidation of the dominant pathway for neurotransmitter glutamate repletion and measurement of astrocytic oxidative metabolism. J. Neurosci. 22, 1523-1531.
42. Lewen, A., Fujimura, M., Sugawara, T., Matz, P., Copin, J. C., and Chan, P. H. (2001). Oxidative stress-dependent release of mitochondrial cytochrome c after traumatic brain injury. J. Cereb. Blood Flow Metab. 21, 914-920. doi: 10.1097/00004647-200108000-00003
43. Lyon, M. F. (1961). Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190, 372-373. doi: 10.1038/190372a0
44. Maddock, R. J., and Buonocore, M. H. (2012). MR spectroscopic studies of the brain in psychiatric disorders. Curr. Top. Behav. Neurosci. 11, 199-251. doi: 10.1007/7854_2011_197
45. Margolis, S. A., and Coxon, B. (1986). Identification and quantitation of the impurities in sodium pyruvate. Anal. Chem. 58, 2504-2510. doi: 10.1021/ac00125a033
46. Marino, S., Zei, E., Battaglini, M., Vittori, C., Buscalferri, A., Bramanti, P., et al. (2007). Acute metabolic brain changes following traumatic brain injury and their relevance to clinical severity and outcome. J. Neurol. Neurosurg. Psychiatry 78, 501-507. doi: 10.1136/jnnp.2006.099796
47. Neely, J. R., Denton, R. M., England, P. J., and Randle, P. J. (1972). The effects of increased heart work on the tricarboxylate cycle and its interactions with glycolysis in the perfused rat heart. Biochem. J. 128, 147-159.
48. Newcombe, V. F., Williams, G. B., Outtrim, J. G., Chatfield, D., Gulia Abate, M., Geeraerts, T., et al. (2013). Microstructural basis of contusion expansion in traumatic brain injury: insights from diffusion tensor imaging. J. Cereb. Blood Flow Metab. 33, 855-862. doi: 10.1038/jcbfm.2013.11
49. Notaro, R., Afolayan, A., and Luzzatto, L. (2000). Human mutations in glucose 6-phosphate dehydrogenase reflect evolutionary history. FASEB J. 14, 485-494.
50. Overgaard, M., Rasmussen, P., Bohm, A. M., Seifert, T., Brassard, P., Zaar, M., et al. (2012). Hypoxia and exercise provoke both lactate release and lactate oxidation by the human brain. FASEB J. 26, 3012-3020. doi: 10.1096/fj.11-191999
51. Pandolfi, P. P., Sonati, F., Rivi, R., Mason, P., Grosveld, F., and Luzzatto, L. (1995). Targeted disruption of the housekeeping gene encoding glucose 6-phosphate dehydrogenase (G6PD): G6PD is dispensable for pentose synthesis but essential for defense against oxidative stress. EMBO J. 14, 5209-5215.
52. Patel, A. B., Lai, J. C., Chowdhury, G. M., Hyder, F., Rothman, D. L., Shulman, R. G., et al. (2014). Direct evidence for activity-dependent glucose phosphorylation in neurons with implications for the astrocyte-to-neuron lactate shuttle. Proc. Natl. Acad. Sci. U.S.A. 111, 5385-5390. doi: 10.1073/pnas.1403576111
53. 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. U.S.A. 91, 10625-10629. doi: 10.1073/pnas.91.22.10625
54. Pellerin, L., and Magistretti, P. J. (2012). Sweet sixteen for ANLS. J. Cereb. Blood Flow Metab. 32, 1152-1166. doi: 10.1038/jcbfm.2011.149
55. Rice, A. C., Zsoldos, R., Chen, T., Wilson, M. S., Alessandri, B., Hamm, R. J., et al. (2002). Lactate administration attenuates cognitive deficits following traumatic brain injury. Brain Res. 928, 156-159. doi: 10.1016/S0006-8993(01)03299-1
56. Riganti, C., Gazzano, E., Polimeni, M., Aldieri, E., and Ghigo, D. (2012). The pentose phosphate pathway: an antioxidant defense and a crossroad in tumor cell fate. Free Radic. Biol. Med. 53, 421-436. doi: 10.1016/j.freeradbiomed.2012.05.006
57. Rodriguez-Rodriguez, P., Fernandez, E., and Bolanos, J. P. (2013). Underestimation of the pentose-phosphate pathway in intact primary neurons as revealed by metabolic flux analysis. J. Cereb. Blood Flow Metab. 33, 1843-1845. doi: 10.1038/jcbfm.2013.168
58. Roozenbeek, B., Maas, A. I., and Menon, D. K. (2013). Changing patterns in the epidemiology of traumatic brain injury. Nat. Rev. Neurol. 9, 231-236. doi: 10.1038/nrneurol.2013.22
59. Rothman, D. L., De Feyter, H. M., de Graaf, R. A., Mason, G. F., and Behar, K. L. (2011). 13C MRS studies of neuroenergetics and neurotransmitter cycling in humans. NMR Biomed. 24, 943-957. doi: 10.1002/nbm.1772
60. Sala, N., Suys, T., Zerlauth, J. B., Bouzat, P., Messerer, M., Bloch, J., et al. (2013). Cerebral extracellular lactate increase is predominantly nonischemic in patients with severe traumatic brain injury. J. Cereb. Blood Flow Metab. 33, 1815-1822. doi: 10.1038/jcbfm.2013.142
61. Samaras, N., Samaras, D., Frangos, E., Forster, A., and Philippe, J. (2013). A review of age-related dehydroepiandrosterone decline and its association with well-known geriatric syndromes: is treatment beneficial? Rejuvenation Res. 16, 285-294. doi: 10.1089/rej.2013.1425
62. Schumacher, M., Weill-Engerer, S., Liere, P., Robert, F., Franklin, R. J., Garcia-Segura, L. M., et al. (2003). Steroid hormones and neurosteroids in normal and pathological aging of the nervous system. Prog. Neurobiol. 71, 3-29. doi: 10.1016/j.pneurobio.2003.09.004
63. Schurr, A. (2006). Lactate: the ultimate cerebral oxidative energy substrate? J. Cereb. Blood Flow Metab. 26, 142-152. doi: 10.1038/sj.jcbfm.9600174
64. Shannon, R. J., Carpenter, K. L., Guilfoyle, M. R., Helmy, A., and Hutchinson, P. J. (2013). Cerebral microdialysis in clinical studies of drugs: pharmacokinetic applications. J. Pharmacokinet. Pharmacodyn. 40, 343-358. doi: 10.1007/s10928-013-9306-4
65. Sonnewald, U. (2014). Glutamate synthesis has to be matched by its degradation - where do all the carbons go? J. Neurochem. 131, 399-406. doi: 10.1111/jnc.12812
66. Stocchetti, N., Furlan, A., and Volta, F. (1996). Hypoxemia and arterial hypotension at the accident scene in head injury. J. Trauma 40, 764-767. doi: 10.1097/00005373-199605000-00014
67. Suzuki, A., Stern, S. A., Bozdagi, O., Huntley, G. W., Walker, R. H., Magistretti, P. J., et al. (2011). Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144, 810-823. doi: 10.1016/j.cell.2011.02.018
68. TeSlaa, T., and Teitell, M. A. (2014). Techniques to monitor glycolysis. Methods Enzymol. 542, 91-114. doi: 10.1016/B978-0-12-416618-9.00005-4
69. Timofeev, I., Carpenter, K. L., Nortje, J., Al-Rawi, P. G., O'Connell, M. T., Czosnyka, M., et al. (2011a). Cerebral extracellular chemistry and outcome following traumatic brain injury: a microdialysis study of 223 patients. Brain 134(Pt 2), 484-494. doi: 10.1093/brain/awq353
70. Timofeev, I., Czosnyka, M., Carpenter, K. L., Nortje, J., Kirkpatrick, P. J., Al-Rawi, P. G., et al. (2011b). Interaction between brain chemistry and physiology after traumatic brain injury: impact of autoregulation and microdialysis catheter location. J. Neurotrauma 28, 849-860. doi: 10.1089/neu.2010.1656
71. Timofeev, I., Nortje, J., Al-Rawi, P. G., Hutchinson, P. J., and Gupta, A. K. (2013). Extracellular brain pH with or without hypoxia is a marker of profound metabolic derangement and increased mortality after traumatic brain injury. J. Cereb. Blood Flow Metab. 33, 422-427. doi: 10.1038/jcbfm.2012.186
72. Tyson, R. L., Gallagher, C., and Sutherland, G. R. (2003). 13C-Labeled substrates and the cerebral metabolic compartmentalization of acetate and lactate. Brain Res. 992, 43-52. doi: 10.1016/j.brainres.2003.08.027
73. Unterberg, A. W., Stover, J., Kress, B., and Kiening, K. L. (2004). Edema and brain trauma. Neuroscience 129, 1021-1029. doi: 10.1016/j.neuroscience.2004.06.046
74. van Hall, G., Stromstad, M., Rasmussen, P., Jans, O., Zaar, M., Gam, C., et al. (2009). Blood lactate is an important energy source for the human brain. J. Cereb. Blood Flow Metab. 29, 1121-1129. doi: 10.1038/jcbfm.2009.35
75. Vespa, P., Bergsneider, M., Hattori, N., Wu, H. M., Huang, S. C., Martin, N. A., et al. (2005). Metabolic crisis without brain ischemia is common after traumatic brain injury: a combined microdialysis and positron emission tomography study. J. Cereb. Blood Flow Metab. 25, 763-774. doi: 10.1038/sj.jcbfm.9600073
76. Warburg, O. (1956). On the origin of cancer cells. Science 123, 309-314. doi: 10.1126/science.123.3191.309
77. Xiong, Y., Gu, Q., Peterson, P. L., Muizelaar, J. P., and Lee, C. P. (1997). Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury. J. Neurotrauma 14, 23-34. doi: 10.1089/neu.1997.14.23