Neuroprotection following fluid percussion brain trauma: A pilot study using quercetin

Journal of Neurotrauma

Volumn 22, Issue 12, 2005, Pages 1475-1484

  Schültke, Elisabeth ^a   Kamencic, Huse ^a   Zhao, Min ^b   Tian, Guo Feng ^b   Baker, Andrew J ^b,c   Griebel, Robert W ^a   Juurlink, Bernhard H J ^d  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Brain trauma; Compound action potential; Electrophysiology; Fluid percussion model; Glutathione; Inflammation; Oxidative stress

Indexed keywords

FLAVONOID; GLUTATHIONE; MYELOPEROXIDASE; QUERCETIN; SODIUM CHLORIDE;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBROSPINAL FLUID; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; IMMUNOCYTOTOXICITY; INFLAMMATION; MALE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PERCUSSION; PILOT STUDY; RAT; SPINAL CORD INJURY; STATISTICAL SIGNIFICANCE; TRAUMATIC BRAIN INJURY; TREATMENT OUTCOME;

ACTION POTENTIALS; ANIMALS; BRAIN INJURIES; CORPUS CALLOSUM; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGY; GLUTATHIONE; IMMUNOHISTOCHEMISTRY; MALE; NEUROPROTECTIVE AGENTS; ORGAN CULTURE TECHNIQUES; PEROXIDASE; PILOT PROJECTS; QUERCETIN; RATS;

EID: 31044447792     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2005.22.1475     Document Type: Article

References (77)

1. ARABBI, P.R., GENOVESE, M.I., and LAJOLO, P.M. (2004). Flavonoids in vegetable foods commonly consumed in Brazil and estimated ingestion by the Brazilian population. J. Agric. Food Chem. 52, 1124-1131.
2. BAKER, A.J., PHAN, N., MOULTON, R.J., et al. (2002). Attenuation of the electrophysiological function of the corpus callosum after fluid percussion injury in the rat. J. Neurotrauma 19, 587-599.
3. BLACKBURN, W.D., JR., HECK, L.W., and WALLACE, R.W. (1987). The bioflavonoid quercetin inhibits neutrophil degranulation, superoxide production, and the phosphorylation of specific neutrophil proteins. Biochem. Biophys. Res. Commun. 144, 1229-1236.
4. BUSSE, W.W., KOPP, D.E., and MIDDLETON, E., JR. (1984). Flavonoid modulation of human neutrophil function. J. Allergy Clin. Immunol. 73, 801-809.
5. CARLOS, T.M., CLARK, R.S., FRANICOLA-HIGGINS, D., SCHIDING, J.K., and KOCHANEK, P.M. (1997). Expression of endothelial adhesion molecules and recruitment of neutrophils after traumatic brain injury in rats. J. Leukoc. Biol. 61, 279-285.
6. CARLSON, S.L., PARRISH, M.E., SPRINGER, J.E., DOTY, K., and DOSSETT, L. (1998). Acute inflammatory response in spinal cord following impact injury. Exp. Neurol. 151, 77-88.
7. CHEN, S., PICKARD, J.D., and HARRIS, N.G. (2003). Time course of cellular pathology after controlled cortical impact injury. Exp. Neurol. 182, 87-102.
8. CHENG, I.F., and BREEN, K. (2000). On the ability of four flavonoids, baicilein, luteolin, naringenin, and quercetin, to suppress the fenton reaction of the iron-ATP complex. Biometals 13, 77-83.
9. CHO, S.Y., PARK, S.J., KWON, M.J., et al. (2003). Quercetin suppresses proinflammatory cytokines production through MAP kinases and NF-kappaB pathway in lipopolysaccharide-stimulated macrophage. Mol. Cell. Biochem. 243, 153-160.
10. CHRISTMAN, J.W., BLACKWELL, T.S., and JUURLINK, B.H.J. (2000). Redox regulation of nuclear factor kappa B: therapeutic potential for attenuating inflammatory responses. Brain Pathol. 10, 153-162.
11. CLARK, R.A., and SZOT, S. (1981). The myeloperoxidase-hydrogen peroxide-halide system as effector of neutrophil-mediated tumor cell cytotoxicity. J. Immunol. 126, 1295-1301.
12. CLARK, R.S., SCHIDING, J.K., KACZOROWSKI, S.L., MARION, D.W., and KOCHANEK, P.M. (1994). Neutrophil accumulation after traumatic brain injury in rats: comparison of weight drop and controlled cortical impact models. J. Neurotrauma 11, 499-506.
13. CONQUER, J.A., MAIANI, G., AZZINI, E., RAGUZZINI, A., and HOLUB, B.J. (1998). Supplementation with quercetin markedly increases plasma quercetin concentration without effect on selected risk factors for heart disease in healthy subjects. J. Nutr. 128, 593-597.
14. CORTEZ, S.C., MCINTOSH, T.K., and NOBLE, L.J. (1989). Experimental fluid percussion brain injury: vascular disruption and neuronal and glial alterations. Brain Res. 482, 271-282.
15. DE VRIES, J.H., JANSSEN, P.L., HOLLMAN, P.C., VAN STAVEREN, W.A., and KATAN, M.B. (1997). Consumption of quercetin and kaempferol in free-living subjects eating a variety of diets. Cancer Lett. 114, 141-144.
16. DIXON, C.E., LYETH B.C., POVLISHOCK J.T., et al. (1987). A fluid percussion model of experimental brain injury in the rat. J. Neurosurg. 67, 110-119.
17. DOMIGAN, N.M., CHARLTON, T.S., DUNCAN, M.W., WINTERBOURN, C.C., and KETTLE, A.J. (1995). Chlorination of tyrosyl residues in peptides by myeloperoxidase and human neutrophils. J. Biol. Chem. 270, 16542-16548.
18. DONNELLY, L.E., NEWTON, R., KENNEDY, O.E., et al. (2004). Anti-inflammatory effects of resveratrol in lung epithelial cells: molecular mechanisms. Am. J. Physiol. Lung Cell Mol. Physiol. 287, L774-L783.
19. DUGAS, A.J., JR., CASTANEDA-ACOSTA, J., BONIN, G.C., PRICE, K.L., FISCHER, N.H., and WINSTON, G.W. (2000). Evaluation of the total peroxyl radical-scavenging capacity of flavonoids: structure-activity relationships. J. Nat. Prod. 63, 327-331.
20. ERLUND, I., MARNIEMI, J., HAKALA, P., ALFTHAN, G., MERIRINNE, E., and ARO, A. (2003). Consumption of black currants, lingonberries and bilberries increases serum quercetin concentrations. Eur. J. Clin. Nutr. 57, 37-42.
21. FERRALI, M., SIGNORINI, C., CACIOTTI, B., et al. (1997). Protection against oxidative damage of erythrocyte membrane by the flavonoid quercetin and its relation to iron chelating activity. FEBS Lett. 416, 123-129.
22. FURTMULLER, P.G., OBINGER, C., HSUANYU, Y., and DUNFORD, H.B. (2000). Mechanism of reaction of myeloperoxidase with hydrogen peroxide and chloride ion. Eur. J. Biochem. 267, 5858-5864.
23. GEODES, J.F., VOWLES, G.H., HACKSHAW, A.K., NICKOLS, C.D., SCOTT, I.S., and WHITWELL, H.L. (2001). Neuropathology of inflicted head injury in children. II. Microscopic brain injury in infants. Brain 124, 1299-1306.
24. GENTLEMAN, S.M., ROBERTS, G.W., GENNARELLI, T.A., et al. (1995). Axonal injury: a universal consequence of fatal closed head injury? Acta Neuropathol. 89, 537-543.
25. GRAHAM, D.I., MCINTOSH, T.K., MAXWELL, W.L., and NICOLL, J.A. (2000). Recent advances in neurotrauma. J. Neuropathol. Exp. Neurol. 59, 641-651.
26. GRAHAM, D.I., RAGHUPATHI, R., SAATMAN, K.E., MEANEY, D., and MCINTOSH, T.K. (2000). Tissue tears in the white matter after lateral fluid percussion brain injury in the rat: relevance to human brain injury. Acta Neuropathol. 99, 117-124.
27. HAKKINEN, S.H., KARENLAMPI, S.O., HEINONEN, I.M., MYKKANEN, H.M., and TORRONEN, A.R. (1999). Content of the flavonols quercetin, myricetin, and kaempferol in 25 edible berries. J. Agric. Food Chem. 47, 2274-2279.
28. HAYES, R.L., STALHAMMAR D., POVLISHOCK J.T., et al. (1987). A new model of concussive brain injury in the cat produced by extradural fluid volume loading: II. Physiological and neuropathological observations. Brain Inj. 1, 93-112.
29. HILL-FELBERG, S.J., MCINTOSH, T.K., OLIVER, D.L., RAGHUPATHI, R., and BARBARESE, E. (1999). Concurrent loss and proliferation of astrocytes following lateral fluid percussion brain injury in the adult rat. J. Neurosci. Res. 57, 271-279.
30. HOLLMAN, P.C., DE VRIES, J.H., VAN LEEUWEN, S.D., MENGELERS, M.J., and KATAN, M.B. (1995). Absorption of dietary quercetin glycosides and quercetin in healthy ileostomy volunteers. Am. J. Clin. Nutr. 62, 1276-1282.
31. HOLLMAN. P.C., and KATAN, M.B. (1999). Dietary flavonoids: intake, health effects and bioavailability. Food Chem. Toxicol. 37, 937-942.
32. HOLLMAN, P.C., V.D. GAAG, M., MENGELERS, M.J., VAN TRIJP, J.M., DE VRIES, J.H., and KATAN, M.B. (1996). Absorption and disposition kinetics of the dietary antioxidant quercetin in man. Free Radic. Biol. Med. 21, 703-707.
33. HOLLMAN, P.C., VAN TRIJP, J.M., BUYSMAN, M.N., et al. (1997). Relative bioavailability of the antioxidant flavonoid quercetin from various foods in man. FEBS Lett. 418, 152-156.
34. HOLMIN, S., SODERLUND, J., BIBERFELD, P., and MATHIESEN, T. (1998). Intracerebral inflammation after human brain contusion. Neurosurgery 42, 291-298.
35. HOVDA, D.A., LEE, S.M., SMITH, M.L., et al. (1995). The neurochemical and metabolic cascade following brain injury: moving from animal models to man. J. Neurotrauma 12, 903-906.
36. IARC. (1999). Quercetin. IARC monographs on the Evaluation of Carcinogenic Risks to Humans. IARC.
37. ISHIKAWA, Y., SUGIYAMA, H., STYLIANOU, E., and KITAMURA, M. (1999). Bioflavonoid quercetin inhibits interleukin-1-induced transcriptional expression of monocyte chemoattractant protein-1 in glomerular cells via suppression of nuclear factor-kappaB. J. Am. Soc. Nephrol. 10, 2290-2296.
38. JUURLINK, B.H.J. (1999). Management of oxidative stress in the CNS: the many roles of glutathione. Neurotox. Res. 1, 119-140.
39. JUURLINK, B.H.J., and PATERSON, P.C. (1998). Review of oxidative stress in brain and spinal cord injury: suggestions for pharmacological and nutritional management strategies. J. Spinal Cord Med. 21, 309-334.
40. KAMENCIC, H., LYON, A., PATERSON, P.C., and JUURLINK, B.H.J. (2000). Monocholorobimane method to measure tissue glutathione. Analyt. Biochem. 286, 35-37.
41. KEELING, K.L., HICKS, R.R., MAHESH, J., BILLINGS, B.B., and KOTWAL, G.J. (2000). Local neutrophil influx following lateral fluid-percussion brain injury in rats is associated with accumulation of complement activation fragments of the third component (C3) of the complement system. J. Neuroimmunol. 105, 20-30.
42. KOBUCHI, H., ROY, S., SEN, C.K., NGUYEN, H.G., and PACKER, L. (1999). Quercetin inhibits inducible ICAM-1 expression in human endothelial cells through the JNK pathway. Am. J. Physiol. 277, C403-411.
43. LUCISANO-VALIM, Y.M., KABEYA, L.M., KANASHIRO, A., et al. (2002). A simple method to study the activity of natural compounds on the chemiluminescence of neutrophils upon stimulation by immune complexes. J. Pharmacol. Toxicol. Methods 47, 53-58.
44. MAXWELL, W.L., POVLISHOCK, J.T., and GRAHAM, D.L. (1997). A mechanistic analysis of nondisruptive axonal injury: a review. J. Neurotrauma 14, 419-440.
45. McKENZIE, K.J., MCLELLAN, D.R., GENTLEMAN, S.M., MAXWELL, W.L., GENNARELLI, T.A., and GRAHAM, D.I. (1996). Is beta-APP a marker of axonal damage in short-surviving head injury? Acta Neuropathol. 92, 608-613.
46. MEYTHALER, J.M., PEDUZZI, J.D., ELEFTHERIOU, E., and NOVACK, T.A. (2001). Current concepts: diffuse axonal injury-associated traumatic brain injury. Arch. Phys. Med. Rehabil. 82, 1461-1471.
47. MOON, J.H., NAKATA, R., OSHIMA, S., INAKUMA, T., and TERAO, J. (2000). Accumulation of quercetin conjugates in blood plasma after the short-term ingestion of onion by women. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R461-R467.
48. MYHRSTAD, M.C., CARLSEN, H., NORDSTROM, O., BLOMHOFF, R., and MOSKAUG, J.J. (2002). Flavonoids increase the intracellular glutathione level by transactivation of the gamma-glutamylcysteine synthetase catalytical subunit promoter. Free Radic. Biol. Med. 32, 386-393.
49. NASHMI, R., and FEHLINGS, M.G. (2001). Changes in axonal physiology and morphology after chronic compressive injury of the rat thoracic spinal cord. Neuroscience 104, 235-251.
50. PAGONIS, C., TAUBER, A.I., PAVLOTSKY, N., and SIMONS, E.R. (1986). Flavonoid impairment of neutrophil response. Biochem. Pharmacol. 35, 237-245.
51. PEET, G.W., and LI, J. (1999). IkappaB kinases alpha and beta show a random sequential kinetic mechanism and are inhibited by staurosporine and quercetin. J. Biol. Chem. 274, 32655-32661.
52. PERRI, B.R., SMITH, D.H., MURAI, H., et al. (1997). Metabolic quantification of lesion volume following experimental traumatic brain injury in the rat. J. Neurotrauma 14, 15-22.
53. PINCEMAIL, J., DEBY, C., THIRION, A., DE BRUYN-DISTER, M., and GOUTIER, R. (1988). Human myeloperoxidase activity is inhibited in vitro by quercetin. Comparison with three related compounds. Experientia 44, 450-453.
54. RABY, C.A., MORGANTI-KOSSMANN, M.C., KOSSMANN, T., et al. (1998). Traumatic brain injury increases beta-amyloid peptide 1-42 in cerebrospinal fluid. J. Neurochem. 71, 2505-2509.
55. REITERER, G., TOBOREK, M., and HENNIG, B. (2004). Quercetin protects against linoleic acid-induced porcine endothelial cell dysfunction. J. Nutr. 134, 771-775.
56. RODRIGUES, M.R., RODRIGUEZ, D., RUSSO, M., and CAMPA, A. (2002). Macrophage activation includes high intracellular myeloperoxidase activity. Biochem. Biophys. Res. Commun. 292, 869-873.
57. ROYO, N.C., WAHL, F., and STUTZMANN, J.M. (1999). Kinetics of polymorphonuclear neutrophil infiltration after a traumatic brain injury in rat. Neuroreport 10, 1363-1367.
58. SCHOETTLE, R.J., KOCHANEK, P.M., MAGARGEE, M.J., UHL, M.W., and NEMOTO, E.M. (1990). Early polymorphonuclear leukocyte accumulation correlates with the development of posttraumatic cerebral edema in rats. J. Neurotrauma 7, 207-217.
59. SCHÜLTKE, E., KENDALL, E., KAMENCIC, H., GHONG, Z., GRIEBEL, R.W., and JUURLINK, B.H. (2003). Quercetin promotes functional recovery following acute spinal cord injury. J. Neurotrauma 20, 583-591.
60. SELLOUM, L., REICHL, S., MULLER, M., SEBIHI, L., and ARNHOLD, J. (2001). Effects of flavonols on the generation of superoxide anion radicals by xanthine oxidase and stimulated neutrophils. Arch. Biochem. Biophys. 395, 49-56.
61. SMITH, P.K., KROHN, R.I., HERMANSON, G.T., et al. (1985). Measurement of protein using bicinchoninic acid. Analyt. Biochem. 150, 76-85.
62. SOARES, H.D., HICKS, R.R., SMITH, D., and MCINTOSH, T.K. (1995). Inflammatory leukocytic recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury. J. Neurosci. 15, 8223-8233.
63. STAHEL, P.E., MORGANTI-KOSSMANN, M.C., and KOSSMANN, T. (1998). The role of the complement system in traumatic brain injury. Brain Res. Brain Res. Rev. 27, 243-256.
64. 'T HART, B., IP VIA CHING, T.R., VAN DIJK, H., and LABADIE, R.P. (1990). How flavonoids inhibit the generation of luminol-dependent chemiluminescence by activated human neutrophils. Chem. Biol. Interact. 73, 323-335.
65. TIAN, G.F., and BAKER, A.J. (2000). Glycolysis prevents anoxia-induced synaptic transmission damage in rat hippocampal slices. J. Neurophysiol. 83, 1830-1839.
66. TORDERA, M., FERRANDIZ, M.L., and ALCARAZ, M.J. (1994). Influence of anti-inflammatory flavonoids on degranulation and arachidonic acid release in rat neutrophils. Z. Naturforsch. C 49, 235-240.
67. UCHIDA, K., SHIRAISHI, M., NAITO, Y., TORII, Y., NAKAMURA, Y., and OSAWA, T. (1999). Activation of stress signaling pathways by the end product of lipid peroxidation. 4-hydroxy-2-nonenal is a potential inducer of intracellular peroxide production. J. Biol. Chem. 274, 2234-2242.
68. UDA, Y., PRICE, K.R., WILLIAMSON, G., and RHODES, M.J. (1997). Induction of the anticarcinogenic marker enzyme, quinone reductase, in murine hepatoma cells in vitro by flavonoids. Cancer Lett. 120, 213-216.
69. UHL, M.W., BIAGAS, K.V., GRUNDL, P.D., et al. (1994). Effects of neutropenia on edema, histology, and cerebral blood flow after traumatic brain injury in rats. J. Neurotrauma 11, 303-315.
70. VALERIO, L.G., JR., KEPA, J.K., PICKWELL, G.V., and QUATTROCHI, L.C. (2001). Induction of human NAD(P)H:quinone oxidoreductase (NQOI) gene expression by the flavonol quercetin. Toxicol. Lett. 119, 49-57.
71. WANG, L., MATSUSHITA, K., ARAKI, J., and TAKEDA, M. (2002). Inhibition of c-Jun N-terminal kinase ameliorates apoptosis induced by hydrogen peroxide in the kidney tubule epithelial cells (NRK-52E). Nephron 91, 142-147.
72. WILKINSON, A.E., BRIDGES, L.R., and SIVALOGANATHAN, S. (1999). Correlation of survival time with size of axonal swellings in diffuse axonal injury. Acta Neuropathol. 98, 197-202.
73. WILLIAMSON, G., PLUMB, G.W., UDA, Y., PRICE, K.R., and RHODES, M.J. (1996). Dietary quercetin glycosides: antioxidant activity and induction of the anticarcinogenic phase II marker enzyme quinone reductase in Hepalclc7 cells. Carcinogenesis 17, 2385-2387.
74. WINTERBOURN, C.C., and KETTLE, A.J. (2000). Biomarkers of myeloperoxidase-derived hypochlorous acid. Free Radic. Biol. Med. 29, 403-409.
75. YANNAI, S., DAY, A.J., WILLIAMSON, G., and RHODES, M.J. (1998). Characterization of flavonoids as monofunctional or bifunctional inducers of quinone reductase in murine hepatoma cell lines. Food Chem. Toxicol. 36, 623-630.
76. YOSHINO, M., and MURAKAMI, K. (1998). Interaction of iron with polyphenolic compounds: application to antioxidant characterization. Anal. Biochem. 257, 40-44.
77. YOSHIZUMI, M., TSUCHIYA, K., KIRIMA, K., KYAW, M., SUZAKI, Y., and TAMAKI, T. (2001). Quercetin inhibits She- and phosphatidylinositol 3-kinase-mediated c- Jun N-terminal kinase activation by angiotensin II in cultured rat aortic smooth muscle cells. Mol. Pharmacol. 60, 656-665.