Beneficial effects of sodium or ethyl pyruvate after traumatic brain injury in the rat

Experimental Neurology

Volumn 225, Issue 2, 2010, Pages 391-401

  Moro, Nobuhiro ^a   Sutton, Richard L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell Death; Cytochrome oxidase; Ethyl pyruvate; Functional recovery; Inflammation; Microglia; Neuroprotection; Rats; Sodium pyruvate; Traumatic brain injury

Indexed keywords

CD11B ANTIGEN; CYTOCHROME C OXIDASE; E 47808; ETHYLPYRUVIC ACID; P 2256; PYRUVATE SODIUM; PYRUVIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CONTUSION; BRAIN METABOLISM; CELL ACTIVATION; CELL DEATH; COGNITION; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; ENZYME ACTIVITY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MICROGLIA; NEUROPROTECTION; NONHUMAN; OPTICAL DENSITY; PRIORITY JOURNAL; RAT; REPEATED DRUG DOSE; SCORING SYSTEM; SINGLE DRUG DOSE; SPATIAL MEMORY; THERAPY DELAY; TRAUMATIC BRAIN INJURY; WALKING; WORKING MEMORY; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; BRAIN; BRAIN INJURIES; CELL COUNT; CONVALESCENCE; DRUG EFFECTS; MEMORY; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; BRAIN INJURIES; CELL COUNT; CELL DEATH; ELECTRON TRANSPORT COMPLEX IV; IMMUNOHISTOCHEMISTRY; MALE; MEMORY; MICROGLIA; MOTOR ACTIVITY; PYRUVATES; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION;

EID: 77956428420     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.07.013     Document Type: Article

References (68)

1. Alvarez G., Ramos M., Ruiz F., Satrustegui J., Bogonez E. Pyruvate protection against beta-amyloid-induced neuronal death: role of mitochondrial redox state. J. Neurosci. Res. 2003, 73:260-269.
2. Chen S., Pickard J.D., Harris N.G. Time course of cellular pathology after controlled cortical impact injury. Exp. Neurol. 2003, 182:87-102.
3. Chen T., Qian Y.Z., Di X., Rice A., Zhu J.P., Bullock R. Lactate/glucose dynamics after rat fluid percussion brain injury. J. Neurotrauma 2000, 17:135-142.
4. Chen W., Jia Z., Zhu H., Zhou K., Li Y., Misra H.P. Ethyl pyruvate inhibits peroxynitrite-induced DNA damage and hydroxyl radical generation: implications for neuroprotection. Neurochem. Res. 2010, 35:336-342.
5. Cho I.H., Kim S.W., Kim J.B., Kim T.K., Lee K.W., Han P.L., Lee J.K. Ethyl pyruvate attenuates kainic acid-induced neuronal cell death in the mouse hippocampus. J. Neurosci. Res. 2006, 84:1505-1511.
6. Choi J.S., Lee M.S., Jeong J.W. Ethyl pyruvate has a neuroprotective effect through activation of extracellular signal-regulated kinase in Parkinson's disease model. Biochem. Biophys. Res. Commun. 2010, 394:854-858.
7. Dai W., Cheng H.L., Huang R.Q., Zhuang Z., Shi J.X. Quantitative detection of the expression of mitochondrial cytochrome c oxidase subunits mRNA in the cerebral cortex after experimental traumatic brain injury. Brain Res. 2009, 1251:287-295.
8. Das U.N. Is pyruvate an endogenous anti-inflammatory molecule?. Nutrition 2006, 22:965-972.
9. Feeney D.M., Gonzalez A., Law W.A. Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury. Science 1982, 217:855-857.
10. Fink M.P. Ethyl pyruvate: a novel anti-inflammatory agent. J. Intern. Med. 2007, 261:349-362.
11. Fukushima M., Lee S.M., Moro N., Hovda D.A., Sutton R.L. Metabolic and histologic effects of sodium pyruvate treatment in the rat after cortical contusion injury. J. Neurotrauma 2009, 26:1095-1110.
12. Gonzalez S.V., Nguyen N.H., Rise F., Hassel B. Brain metabolism of exogenous pyruvate. J. Neurochem. 2005, 95:284-293.
13. Gonzalez-Falcon A., Candelario-Jalil E., Garcia-Cabrera M., Leon O.S. Effects of pyruvate administration on infarct volume and neurological deficits following permanent focal cerebral ischemia in rats. Brain Res. 2003, 990:1-7.
14. Harris L.K., Black R.T., Golden K.M., Reeves T.M., Povlishock J.T., Phillips L.L. Traumatic brain injury-induced changes in gene expression and functional activity of mitochondrial cytochrome C oxidase. J. Neurotrauma 2001, 18:993-1009.
15. Hollander M., Wolfe D.A. Nonparametric statistical methods 1999, Wiley, New York. 2nd ed.
16. Hovda D.A., Yoshino A., Kawamata T., Katayama Y., Becker D.P. Diffuse prolonged depression of cerebral oxidative metabolism following concussive brain injury in the rat: a cytochrome oxidase histochemistry study. Brain Res. 1991, 567:1-10.
17. Hurd R.E., Yen Y.F., Mayer D., Chen A., Wilson D., Kohler S., Bok R., Vigneron D., Kurhanewicz J., Tropp J., Spielman D., Pfefferbaum A. Metabolic imaging in the anesthetized rat brain using hyperpolarized [1-13C] pyruvate and [1-13C] ethyl pyruvate. Magn. Reson. Med. 2010, 63:1137-1143.
18. Huttemann M., Lee I., Kreipke C.W., Petrov T. Suppression of the inducible form of nitric oxide synthase prior to traumatic brain injury improves cytochrome c oxidase activity and normalizes cellular energy levels. Neuroscience 2008, 151:148-154.
19. Kao K.K., Fink M.P. The biochemical basis for the anti-inflammatory and cytoprotective actions of ethyl pyruvate and related compounds. Biochem. Pharmacol. 2010, 80:151-159.
20. Kashiwagi A., Nishio Y., Asahina T., Ikebuchi M., Harada N., Tanaka Y., Takahara N., Taki H., Obata T., Hidaka H., Saeki Y., Kikkawa R. Pyruvate improves deleterious effects of high glucose on activation of pentose phosphate pathway and glutathione redox cycle in endothelial cells. Diabetes 1997, 46:2088-2095.
21. Kelly D.F., Kozlowski D.A., Haddad E., Echiverri A., Hovda D.A., Lee S.M. Ethanol reduces metabolic uncoupling following experimental head injury. J. Neurotrauma 2000, 17:261-272.
22. Kelly D.F., Lee S.M., Pinanong P.A., Hovda D.A. Paradoxical effects of acute ethanolism in experimental brain injury. J. Neurosurg. 1997, 86:876-882.
23. Kim H.S., Cho I.H., Kim J.E., Shin Y.J., Jeon J.H., Kim Y., Yang Y.M., Lee K.H., Lee J.W., Lee W.J., Ye S.K., Chung M.H. Ethyl pyruvate has an anti-inflammatory effect by inhibiting ROS-dependent STAT signaling in activated microglia. Free Radic. Biol. Med. 2008, 45:950-963.
24. Kim J.B., Yu Y.M., Kim S.W., Lee J.K. Anti-inflammatory mechanism is involved in ethyl pyruvate-mediated efficacious neuroprotection in the postischemic brain. Brain Res. 2005, 1060:188-192.
25. Kim S.W., Jeong J.Y., Kim H.J., Seo J.S., Han P.L., Yoon S.H., Lee J.K. Combination treatment with ethyl pyruvate and aspirin enhances neuroprotection in the postischemic brain. Neurotox. Res. 2010, 17:39-49.
26. Kim T.Y., Yi J.S., Chung S.J., Kim D.K., Byun H.R., Lee J.Y., Koh J.Y. Pyruvate protects against kainate-induced epileptic brain damage in rats. Exp. Neurol. 2007, 208:159-167.
27. Krishnappa I.K., Contant C.F., Robertson C.S. Regional changes in cerebral extracellular glucose and lactate concentrations following severe cortical impact injury and secondary ischemia in rats. J. Neurotrauma 1999, 16:213-224.
28. Lee J.Y., Kim Y.H., Koh J.Y. Protection by pyruvate against transient forebrain ischemia in rats. J. Neurosci. 2001, 21:RC171.
29. Lee Y.J., Kang I.J., Bunger R., Kang Y.H. Enhanced survival effect of pyruvate correlates MAPK and NF-kappaB activation in hydrogen peroxide-treated human endothelial cells. J. Appl. Physiol. 2004, 96:793-801.
30. Lucas S.M., Rothwell N.J., Gibson R.M. The role of inflammation in CNS injury and disease. Br. J. Pharmacol. 2006, 147(Suppl 1):S232-S240.
31. McNay E.C., Fries T.M., Gold P.E. Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task. Proc. Natl Acad. Sci. USA 2000, 97:2881-2885.
32. Mizutani A., Maeda N., Toku S., Isohama Y., Sugahara K., Yamamoto H. Inhibition by ethyl pyruvate of the nuclear translocation of nuclear factor-kappaB in cultured lung epithelial cells. Pulm. Pharmacol. Ther. 2010, 23:308-315.
33. Mongan P.D., Capacchione J., Fontana J.L., West S., Bunger R. Pyruvate improves cerebral metabolism during hemorrhagic shock. Am. J. Physiol. Heart Circ. Physiol. 2001, 281:H854-H864.
34. Mongan P.D., Capacchione J., West S., Karaian J., Dubois D., Keneally R., Sharma P. Pyruvate improves redox status and decreases indicators of hepatic apoptosis during hemorrhagic shock in swine. Am. J. Physiol. Heart Circ. Physiol. 2002, 283:H1634-H1644.
35. Mongan P.D., Karaian J., Van Der Schuur B.M., Via D.K., Sharma P. Pyruvate prevents poly-ADP ribose polymerase (PARP) activation, oxidative damage, and pyruvate dehydrogenase deactivation during hemorrhagic shock in swine. J. Surg. Res. 2003, 112:180-188.
36. Montgomery C.M., Webb J.L. Metabolic studies on heart mitochondria. II. The inhibitory action of parapyruvate on the tricarboxylic acid cycle. J. Biol. Chem. 1956, 221:359-368.
37. Morganti-Kossmann M.C., Satgunaseelan L., Bye N., Kossmann T. Modulation of immune response by head injury. Injury 2007, 38:1392-1400.
38. O'Donnell-Tormey J., Nathan C.F., Lanks K., DeBoer C.J., de la Harpe J. Secretion of pyruvate. An antioxidant defense of mammalian cells. J. Exp. Med. 1987, 165:500-514.
39. Opii W.O., Nukala V.N., Sultana R., Pandya J.D., Day K.M., Merchant M.L., Klein J.B., Sullivan P.G., Butterfield D.A. Proteomic identification of oxidized mitochondrial proteins following experimental traumatic brain injury. J. Neurotrauma 2007, 24:772-789.
40. Park J.H., Hong Y.H., Kim H.J., Kim S.M., Kim M.J., Park K.S., Sung J.J., Lee K.W. Pyruvate slows disease progression in a G93A SOD1 mutant transgenic mouse model. Neurosci. Lett. 2007, 413:265-269.
41. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, Orlando. 2nd ed.
42. Phelan H., Stahls P., Hunt J., Bagby G.J., Molina P.E. Impact of alcohol intoxication on hemodynamic, metabolic, and cytokine responses to hemorrhagic shock. J. Trauma 2002, 52:675-682.
43. Ryu J.K., Choi H.B., McLarnon J.G. Combined minocycline plus pyruvate treatment enhances effects of each agent to inhibit inflammation, oxidative damage, and neuronal loss in an excitotoxic animal model of Huntington's disease. Neuroscience 2006, 141:1835-1848.
44. Ryu J.K., Kim S.U., McLarnon J.G. Neuroprotective effects of pyruvate in the quinolinic acid rat model of Huntington's disease. Exp. Neurol. 2003, 183:700-704.
45. Ryu J.K., Kim S.U., McLarnon J.G. Blockade of quinolinic acid-induced neurotoxicity by pyruvate is associated with inhibition of glial activation in a model of Huntington's disease. Exp. Neurol. 2004, 187:150-159.
46. Sappington P.L., Fink M.E., Yang R., Delude R.L., Fink M.P. Ethyl pyruvate provides durable protection against inflammation-induced intestinal epithelial barrier dysfunction. Shock 2003, 20:521-528.
47. Schmued L.C., Hopkins K.J. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 2000, 874:123-130.
48. Scholz T.D., Laughlin M.R., Balaban R.S., Kupriyanov V.V., Heineman F.W. Effect of substrate on mitochondrial NADH, cytosolic redox state, and phosphorylated compounds in isolated hearts. Am. J. Physiol. 1995, 268:H82-H91.
49. Sharma A.B., Barlow M.A., Yang S.H., Simpkins J.W., Mallet R.T. Pyruvate enhances neurological recovery following cardiopulmonary arrest and resuscitation. Resuscitation 2008, 76:108-119.
50. Sharma P., Benford B., Li Z.Z., Ling G.S. Role of pyruvate dehydrogenase complex in traumatic brain injury and measurement of pyruvate dehydrogenase enzyme by dipstick test. J. Emerg. Trauma Shock 2009, 2:67-72.
51. Sharma P., Karian J., Sharma S., Liu S., Mongan P.D. Pyruvate ameliorates post ischemic injury of rat astrocytes and protects them against PARP mediated cell death. Brain Res. 2003, 992:104-113.
52. Sharma P., Mongan P.D. Hypertonic sodium pyruvate solution is more effective than Ringer's ethyl pyruvate in the treatment of hemorrhagic shock. Shock 2010, 33:532-540.
53. Shen H., Hu X., Liu C., Wang S., Zhang W., Gao H., Stetler R.A., Gao Y., Chen J. Ethyl pyruvate protects against hypoxic-ischemic brain injury via anti-cell death and anti-inflammatory mechanisms. Neurobiol. Dis. 2010, 37:711-722.
54. Sims C.A., Wattanasirichaigoon S., Menconi M.J., Ajami A.M., Fink M.P. Ringer's ethyl pyruvate solution ameliorates ischemia/reperfusion-induced intestinal mucosal injury in rats. Crit. Care Med. 2001, 29:1513-1518.
55. Suh S.W., Aoyama K., Matsumori Y., Liu J., Swanson R.A. Pyruvate administered after severe hypoglycemia reduces neuronal death and cognitive impairment. Diabetes 2005, 54:1452-1458.
56. Sutton R.L., Feeney D.M. Alpha-noradrenergic agonists and antagonists affect recovery and maintenance of beam-walking ability after sensorimotor cortex ablation in the rat. Restor. Neurol. Neurosci. 1992, 4:1-11.
57. Sutton R.L., Lescaudron L., Stein D.G. Unilateral cortical contusion injury in the rat: vascular disruption and temporal development of cortical necrosis. J. Neurotrauma 1993, 10:135-149.
58. Taylor A.N., Rahman S.U., Sanders N.C., Tio D.L., Prolo P., Sutton R.L. Injury severity differentially affects short- and long-term neuroendocrine outcomes of traumatic brain injury. J. Neurotrauma 2008, 25:311-323.
59. Tokumaru O., Kuroki C., Yoshimura N., Sakamoto T., Takei H., Ogata K., Kitano T., Nisimaru N., Yokoi I. Neuroprotective effects of ethyl pyruvate on brain energy metabolism after ischemia-reperfusion injury: a (31)p-nuclear magnetic resonance study. Neurochem. Res. 2009, 34:775-785.
60. Varma S.D., Devamanoharan P.S., Ali A.H. Prevention of intracellular oxidative stress to lens by pyruvate and its ester. Free Radic. Res. 1998, 28:131-135.
61. Verwer R.W., Hermens W.T., Dijkhuizen P., ter Brake O., Baker R.E., Salehi A., Sluiter A.A., Kok M.J., Muller L.J., Verhaagen J., Swaab D.F. Cells in human postmortem brain tissue slices remain alive for several weeks in culture. FASEB J. 2002, 16:54-60.
62. Wang Q., Ding Q., Zhou Y., Gou X., Hou L., Chen S., Zhu Z., Xiong L. Ethyl pyruvate attenuates spinal cord ischemic injury with a wide therapeutic window through inhibiting high-mobility group box 1 release in rabbits. Anesthesiology 2009, 110:1279-1286.
63. Wang Q., van Hoecke M., Tang X.N., Lee H., Zheng Z., Swanson R.A., Yenari M.A. Pyruvate protects against experimental stroke via an anti-inflammatory mechanism. Neurobiol. Dis. 2009, 36:223-231.
64. Yi J.S., Kim T.Y., Kyu Kim D., Koh J.Y. Systemic pyruvate administration markedly reduces infarcts and motor deficits in rat models of transient and permanent focal cerebral ischemia. Neurobiol. Dis. 2007, 26:94-104.
65. Yoo M.H., Lee J.Y., Lee S.E., Koh J.Y., Yoon Y.H. Protection by pyruvate of rat retinal cells against zinc toxicity in vitro, and pressure-induced ischemia in vivo. Invest. Ophthalmol. Vis. Sci. 2004, 45:1523-1530.
66. Yu Y.M., Kim J.B., Lee K.W., Kim S.Y., Han P.L., Lee J.K. Inhibition of the cerebral ischemic injury by ethyl pyruvate with a wide therapeutic window. Stroke 2005, 36:2238-2243.
67. Zeng J., Liu J., Yang G.Y., Kelly M.J., James T.L., Litt L. Exogenous ethyl pyruvate versus pyruvate during metabolic recovery after oxidative stress in neonatal rat cerebrocortical slices. Anesthesiology 2007, 107:630-640.
68. Zlotnik A., Gurevich B., Cherniavsky E., Tkachov S., Matuzani-Ruban A., Leon A., Shapira Y., Teichberg V.I. The contribution of the blood glutamate scavenging activity of pyruvate to its neuroprotective properties in a rat model of closed head injury. Neurochem. Res. 2008, 33:1044-1050.