Systemic pyruvate administration markedly reduces infarcts and motor deficits in rat models of transient and permanent focal cerebral ischemia

Neurobiology of Disease

Volumn 26, Issue 1, 2007, Pages 94-104

  Yi, Jung Sun ^a   Kim, Tae Youn ^a   Kyu Kim, Dong ^a   Koh, Jae Young ^a  

^a University of Ulsan College of Medicine   (South Korea)

Author keywords

Focal cerebral ischemia; Glycolysis; Lactate; Magnetic resonance; Neuronal death; Neuroprotection; Pyruvate; Rota rod; TUNEL

Indexed keywords

LACTIC ACID; PYRUVIC ACID; SODIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; DRUG MEGADOSE; GLYCOLYSIS; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR DYSFUNCTION; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; RAT; TRANSIENT ISCHEMIC ATTACK;

ANIMALS; BRAIN; BRAIN CHEMISTRY; BRAIN ISCHEMIA; CELL DEATH; CEREBRAL INFARCTION; DOSE-RESPONSE RELATIONSHIP, DRUG; IN SITU NICK-END LABELING; ISCHEMIC ATTACK, TRANSIENT; LASER-DOPPLER FLOWMETRY; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NAD; PSYCHOMOTOR PERFORMANCE; PYRUVIC ACID; RATS; RATS, SPRAGUE-DAWLEY;

EID: 33947321746     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2006.12.007     Document Type: Article

References (62)

1. Adams Jr. H.P., Brott T.G., Furlan A.J., Gomez C.R., Grotta J., Helgason C.M., Kwiatkowski T., Lyden P.D., Marler J.R., Torner J., Feinberg W., Mayberg M., and Thies W. Guidelines for thrombolytic therapy for acute stroke: a supplement to the guidelines for the management of patients with acute ischemic stroke. A statement for healthcare professionals from a Special Writing Group of the Stroke Council. American Heart Association. Stroke 27 (1996) 1711-1718
2. Alvarez G., Ramos M., Ruiz F., Satrustegui J., and Bogonez E. Pyruvate protection against beta-amyloid-induced neuronal death: role of mitochondrial redox state. J. Neurosci. Res. 73 (2003) 260-269
3. Aspey B.S., Cohen S., Patel Y., Terruli M., and Harrison M.J. Middle cerebral artery occlusion in the rat: consistent protocol for a model of stroke. Neuropathol. Appl. Neurobiol. 24 (1998) 487-497
4. Ayoub I.A., Lee E.J., Ogilvy C.S., Beal M.F., and Maynard K.I. Nicotinamide reduces infarction up to two hours after the onset of permanent focal cerebral ischemia in Wistar rats. Neurosci. Lett. 259 (1999) 21-24
5. Barber P.A., Zhang J., Demchuk A.M., Hill M.D., and Buchan A.M. Why are stroke patients excluded from TPA therapy? An analysis of patient eligibility. Neurology 56 (2001) 1015-1020
6. Bonanni L., Chachar M., Jover-Mengual T., Li H., Jones A., Yokota H., Ofengeim D., Flannery R.J., Miyawaki T., Cho C.H., Polster B.M., Pypaert M., Hardwick J.M., Sensi S.L., Zukin R.S., and Jonas E.A. Zinc-dependent multi-conductance channel activity in mitochondria isolated from ischemic brain. J. Neurosci. 26 (2006) 6851-6862
7. Calderone A., Jover T., Mashiko T., Noh K.M., Tanaka H., Bennett M.V., and Zukin R.S. Late calcium EDTA rescues hippocampal CA1 neurons from global ischemia-induced death. J. Neurosci. 24 (2004) 9903-9913
8. Chang I., Cho N., Koh J.Y., and Lee M.S. Pyruvate inhibits zinc-mediated pancreatic islet cell death and diabetes. Diabetologia 46 (2003) 1220-1227
9. Choi D.W. Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci. 18 (1995) 58-60
10. Chung S.J., Lee S.H., Lee Y.J., Park H.S., Bunger R., and Kang Y.H. Pyruvate protection against endothelial cytotoxicity induced by blockade of glucose uptake. J. Biochem. Mol. Biol. 37 (2004) 239-245
11. Clark W.M., Wissman S., Albers G.W., Jhamandas J.H., Madden K.P., and Hamilton S. Recombinant tissue-type plasminogen activator (Alteplase) for ischemic stroke 3 to 5 hours after symptom onset. The ATLANTIS Study: a randomized controlled trial. Alteplase Thrombolysis for Acute Noninterventional Therapy in Ischemic Stroke. JAMA 282 (1999) 2019-2026
12. Clark W.M., Albers G.W., Madden K.P., and Hamilton S. The rtPA (alteplase) 0- to 6-hour acute stroke trial, part A (A0276g): results of a double-blind, placebo-controlled, multicenter study. Thrombolytic therapy in acute ischemic stroke study investigators. Stroke 31 (2000) 811-816
13. Desagher S., Glowinski J., and Premont J. Pyruvate protects neurons against hydrogen peroxide-induced toxicity. J. Neurosci. 17 (1997) 9060-9067
14. Dirnagl U., Kaplan B., Jacewicz M., and Pulsinelli W. Continuous measurement of cerebral cortical blood flow by laser-Doppler flowmetry in a rat stroke model. J. Cereb. Blood Flow Metab. 9 (1989) 589-596
15. Dirnagl U., Iadecola C., and Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22 (1999) 391-397
16. Frederickson C.J., Koh J.Y., and Bush A.I. The neurobiology of zinc in health and disease. Nat. Rev., Neurosci. 6 (2005) 449-462
17. Frenzel J., Richter J., and Eschrich K. Pyruvate protects glucose-deprived Muller cells from nitric oxide-induced oxidative stress by radical scavenging. Glia 52 (2005) 276-288
18. Garcia J.H., Yoshida Y., Chen H., Li Y., Zhang Z.G., Lian J., Chen S., and Chopp M. Progression from ischemic injury to infarct following middle cerebral artery occlusion in the rat. Am. J. Pathol. 142 (1993) 623-635
19. Gonzalez-Falcon A., Candelario-Jalil E., Garcia-Cabrera M., and Leon O.S. Effects of pyruvate administration on infarct volume and neurological deficits following permanent focal cerebral ischemia in rats. Brain Res. 990 (2003) 1-7
20. Gyngell M.L., Busch E., Schmitz B., Kohno K., Back T., Hoehn-Berlage M., and Hossmann K.A. Evolution of acute focal cerebral ischaemia in rats observed by localized 1H MRS, diffusion-weighted MRI, and electrophysiological monitoring. NMR Biomed. 8 (1995) 206-214
21. Hacke W., Kaste M., Fieschi C., Toni D., Lesaffre E., von Kummer R., Boysen G., Bluhmki E., Hoxter G., Mahagne M.H., et al. Intravenous thrombolysis with recombinant tissue plasminogen activator for acute hemispheric stroke. The European Cooperative Acute Stroke Study (ECASS). JAMA 274 (1995) 1017-1025
22. Iadecola C., and Alexander M. Cerebral ischemia and inflammation. Curr. Opin. Neurol. 14 (2001) 89-94
23. Kalimo H., Rehncrona S., Soderfeldt B., Olsson Y., and Siesjo B.K. Brain lactic acidosis and ischemic cell damage: 2. Histopathology. J. Cereb. Blood Flow Metab. 1 (1981) 313-327
24. Kato H., and Kogure K. Biochemical and molecular characteristics of the brain with developing cerebral infarction. Cell. Mol. Neurobiol. 19 (1999) 93-108
25. Kim Y.H., and Koh J.Y. The role of NADPH oxidase and neuronal nitric oxide synthase in zinc-induced poly(ADP-ribose) polymerase activation and cell death in cortical culture. J. Neurochem. 177 (2002) 407-418
26. Koh J.Y., Suh S.W., Gwag B.J., He Y.Y., Hsu C.Y., and Choi D.W. The role of zinc in selective neuronal death after transient global cerebral ischemia. Science 272 (1996) 1013-1016
27. Kristian T., and Siesjo B.K. Calcium in ischemic cell death. Stroke 29 (1998) 705-718
28. Lee J.Y., Kim Y.H., and Koh J.Y. Protection by pyruvate against transient forebrain ischemia in rats. J. Neurosci. 21 (2001) RC171
29. Lee J.M., Zipfel G.J., Park K.H., He Y.Y., Hsu C.Y., and Choi D.W. Zinc translocation accelerates infarction after mild transient focal ischemia. Neuroscience 115 (2002) 871-878
30. Levy R.M., Berry I., Moseley M.E., and Weinstein P.R. Combined magnetic resonance imaging and bihemispheric magnetic resonance spectroscopy in acute experimental focal cerebral ischemia. Acta Radiol., Suppl. 369 (1986) 507-511
31. Lipton P. Ischemic cell death in brain neurons. Physiol. Rev. 79 (1999) 1431-1568
32. Longa E.Z., Weinstein P.R., Carlson S., and Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20 (1989) 84-91
33. Love S. Oxidative stress in brain ischemia. Brain Pathol. 9 (1999) 119-131
34. Mattson M.P., Culmsee C., and Yu Z.F. Apoptotic and antiapoptotic mechanisms in stroke. Cell Tissue Res. 301 (2000) 173-187
35. Mazzio E., and Soliman K.F. Pyruvic acid cytoprotection against 1-methyl-4-phenylpyridinium, 6-hydroxydopamine and hydrogen peroxide toxicities in vitro. Neurosci. Lett. 337 (2003) 77-80
36. Maynard K.I., Ayoub I.A., and Shen C.C. Delayed multidose treatment with nicotinamide extends the degree and duration of neuroprotection by reducing infarction and improving behavioral scores up to two weeks following transient focal cerebral ischemia in Wistar rats. Ann. N.Y. Acad. Sci. 939 (2001) 416-424
37. Memezawa H., Smith M.L., and Siesjo B.K. Penumbral tissues salvaged by reperfusion following middle cerebral artery occlusion in rats. Stroke 23 (1992) 552-559
38. Mongan P.D., Fontana J.L., Chen R., and Bunger R. Intravenous pyruvate prolongs survival during hemorrhagic shock in swine. Am. J. Physiol. 277 (1999) H2253-H2263
39. Nagamoto Y., Wick M., Prielmeier F., and Frahm J. Dynamic monitoring of cerebral metabolites during and after transient global ischemia in rats by quantitative proton NMR spectroscopy in vivo. NMR Biomed. 86 (1995) 265-270
40. Neumann-Haefelin T., Kastrup A., deCrespigny A., Yenari M.A., Ringer T., Sun G.H., and Moseley M.E. Serial MRI after transient focal cerebral ischemia in rats: dynamics of tissue injury, blood-brain barrier damage, and edema formation. Stroke 31 (2000) 1965-1972
41. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. N. Engl. J. Med. 333 (1995) 1581-1587
42. O'Donnell-Tormey J., Nathan C.F., Lanks K., DeBoer C.J., and de la Harpe J. Secretion of pyruvate. An antioxidant defense of mammalian cells. J. Exp. Med. 165 (1987) 500-514
43. Paschen W., Olah L., and Mies G. Effect of transient focal ischemia of mouse brain on energy state and NAD levels: no evidence that NAD depletion plays a major role in secondary disturbances of energy metabolism., 2000. J. Neurochem. 75 (2000) 1675-1680
44. Rehncrona S., Rosen I., and Siesjo B.K. Brain lactic acidosis and ischemic cell damage: 1. Biochemistry and neurophysiology. J. Cereb. Blood Flow Metab. 1 (1981) 297-311
45. Rehncrona S., Rosen I., and Smith M.L. Effect of different degrees of brain ischemia and tissue lactic acidosis on the short-term recovery of neurophysiologic and metabolic variables. Exp. Neurol. 87 (1985) 458-473
46. Rogers D.C., Campbell C.A., Stretton J.L., and Mackay K.B. Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat. Stroke 28 (1997) 2060-2065 discussion 2066
47. Sharma P., Karian J., Sharma S., Liu S., and Mongan P.D. Pyruvate ameliorates post ischemic injury of rat astrocytes and protects them against PARP mediated cell death. Brain Res. 992 (2003) 104-113
48. Sheline C.T., Behrens M.M., and Choi D.W. Zinc-induced cortical neuronal death: contribution of energy failure attributable to loss of NAD(+) and inhibition of glycolysis. J. Neurosci. 20 (2000) 3139-3146
49. Sheline C.T., Choi E.H., Kim-Han J.S., Dugan L.L., and Choi D.W. Cofactors of mitochondrial enzymes attenuate copper-induced death in vitro and in vivo. Ann. Neurol. 52 (2002) 195-204
50. Siemkowicz E. The effect of glucose upon restitution after transient cerebral ischemia: a summary. Acta Neurol. Scand. 71 (1985) 417-427
51. Siesjo B.K., and Siesjo P. Mechanisms of secondary brain injury. Eur. J. Anaesthesiol. 13 (1996) 247-268
52. Siesjo B.K., Katsura K.I., Kristian T., Li P.A., and Siesjo P. Molecular mechanisms of acidosis-mediated damage. Acta Neurochir., Suppl. 66 (1996) 8-14
53. Sorensen J.C., Mattsson B., Andreasen A., and Johansson B.B. Rapid disappearance of zinc positive terminals in focal brain ischemia. Brain Res. 812 (1998) 265-269
54. Swanson R.A., Morton M.T., Tsao-Wu G., Savalos R.A., Davidson C., and Sharp F.R. A semiautomated method for measuring brain infarct volume. J. Cereb. Blood Flow Metab. 10 (1990) 290-293
55. van der Toorn A., Dijkhuizen R.M., Tulleken C.A., and Nicolay K. Diffusion of metabolites in normal and ischemic rat brain measured by localized 1H MRS. Magn. Reson. Med. 36 (1996) 914-922
56. Vatankhah B., Dittmar M.S., Fehm N.P., Erban P., Ickenstein G.W., Jakob W., Bogdahn U., and Horn M. Thrombolysis for stroke in the elderly. J. Thromb. Thrombolysis 20 (2005) 5-10
57. Wagner K.R., Kleinholz M., de Courten-Myers G.M., and Myers R.E. Hyperglycemic versus normoglycemic stroke: topography of brain metabolites, intracellular pH, and infarct size. J. Cereb. Blood Flow Metab. 12 (1992) 213-222
58. Wang X.F., and Cynader M.S. Pyruvate released by astrocytes protects neurons from copper-catalyzed cysteine neurotoxicity. J. Neurosci. 21 (2001) 3322-3331
59. Yi J.S., Kim Y.H., and Koh J.Y. Infarct reduction in rats following intraventricular administration of either tissue plasminogen activator (tPA) or its non-protease mutant S478A-tPA. Exp. Neurol. 189 (2004) 354-360
60. Yoo M.H., Lee J.Y., Lee S.E., Koh J.Y., and 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. 45 (2004) 1523-1530
61. Zhang R.L., Chopp M., Chen H., and Garcia J.H. Temporal profile of ischemic tissue damage, neutrophil response, and vascular plugging following permanent and transient (2H) middle cerebral artery occlusion in the rat. J. Neurol. Sci. 125 (1994) 3-10
62. Zivin J.A. Neuroprotective therapies in stroke. Drugs 54 Suppl. 3 (1997) 83-88