Caffeic acid phenethyl ester protects blood-brain barrier integrity and reduces contusion volume in rodent models of traumatic brain injury

Journal of Neurotrauma

Volumn 29, Issue 6, 2012, Pages 1209-1218

  Zhao, Jing ^a   Pati, Shibani ^a   Redell, John B ^a   Zhang, Min ^a   Moore, Anthony N ^a   Dash, Pramod K ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

claudin 5; neurovascular function; reactive oxygen species; tight junction; vascular permeability

Indexed keywords

CAFFEIC ACID PHENETHYL ESTER; CLAUDIN 5; EVANS BLUE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CONTUSION; BRAIN CORTEX; BRAIN DYSFUNCTION; CONTRAST MEDIUM EXTRAVASATION; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING; MALE; MEMBRANE PERMEABILITY; MEMORY; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RAT; TASK PERFORMANCE; TRAUMATIC BRAIN INJURY; VESTIBULAR FUNCTION;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN INJURIES; CAFFEIC ACIDS; DISEASE MODELS, ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; PHENYLETHYL ALCOHOL; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION;

EID: 84859906185     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.1858     Document Type: Article

References (84)

1. Adelson, P.D., Whalen, M.J., Kochanek, P.M., Robichaud, P., and Carlos, T.M. (1998). Blood-brain barrier permeability and acute inflammation in two models of traumatic brain injury in the immature rat: a preliminary report. Acta Neurochir. Suppl. 71, 104-106. (Pubitemid 128444370)
2. Babikian, T., Prins, M.L., Cai, Y., Barkhoudarian, G., Hartonian, I., Hovda, D.A., and Giza, C.C. (2010). Molecular and physiological responses to juvenile traumatic brain injury: focus on growth and metabolism. Dev. Neurosci. 32, 431-441.
3. Baldwin, S.A., Fugaccia, I., Brown, D.R., Brown, L.V., and Scheff, S.W. (1996). Blood-brain barrier breach following cortical contusion in the rat. J. Neurosurg. 85, 476-481. (Pubitemid 26278031)
4. Baskaya, M.K., Rao, A.M., Dogan, A., Donaldson, D., and Dempsey, R.J. (1997). The biphasic opening of the blood-brain barrier in the cortex and hippocampus after traumatic brain injury in rats. Neurosci. Lett. 226, 33-36. (Pubitemid 27190398)
5. Beauchamp, K., Mutlak, H., Smith, W.R., Shohami, E., and Stahel, P.F. (2008). Pharmacology of traumatic brain injury: where is the ''golden bullet''? Mol. Med. 14, 731-740.
6. Bramlett, H.M., and Dietrich, W.D. (2007). Progressive damage after brain and spinal cord injury: pathomechanisms and treatment strategies. Prog. Brain Res. 161, 125-141. (Pubitemid 47017402)
7. Celik, S., and Erdogan, S. (2008). Caffeic acid phenethyl ester (CAPE) protects brain against oxidative stress and inflammation induced by diabetes in rats. Mol. Cell Biochem. 312, 39-46.
8. Chan, W.S., Wen, P.C., and Chiang, H.C. (1995). Structureactivity relationship of caffeic acid analogues on xanthine oxidase inhibition. Anticancer Res. 15, 703-707.
9. Colicos, M.A., Dixon, C.E., and Dash, P.K. (1996). Delayed, selective neuronal death following experimental cortical impact injury in rats: possible role in memory deficits. Brain Res. 739, 111-119. (Pubitemid 26387369)
10. Dash, P.K., Mach, S.A., and Moore, A.N. (2002). The role of extracellular signal-regulated kinase in cognitive and motor deficits following experimental traumatic brain injury. Neuroscience 114, 755-767. (Pubitemid 35247661)
11. Dash, P.K., Moore, A.N., and Dixon, C.E. (1995). Spatial memory deficits, increased phosphorylation of the transcription factor CREB, and induction of the AP-1 complex following experimental brain injury. J. Neurosci. 15, 2030-2039.
12. Dash, P.K., Moore, A.N., Moody, M.R., Treadwell, R., Felix, J.L., and Clifton, G.L. (2004). Post-trauma administration of caffeine plus ethanol reduces contusion volume and improves working memory in rats. J. Neurotrauma 21, 1573-1583. (Pubitemid 39525167)
13. DeWitt, D.S., and Prough, D.S. (2003). Traumatic cerebral vascular injury: the effects of concussive brain injury on the cerebral vasculature. J. Neurotrauma 20, 795-825. (Pubitemid 37159064)
14. Dixon, C.E., Clifton, G.L., Lighthall, J.W., Yaghmai, A.A., and Hayes, R.L. (1991). A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39, 253-262.
15. Dixon, C.E., Kochanek, P.M., Yan, H.Q., Schiding, J.K., Griffith, R.G., Baum, E., Marion, D.W., and DeKosky, S.T. (1999). One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J. Neurotrauma 16, 109-122. (Pubitemid 29113822)
16. Fan, P., Yamauchi, T., Noble, L.J., and Ferriero, D.M. (2003). Age-dependent differences in glutathione peroxidase activity after traumatic brain injury. J. Neurotrauma 20, 437-445. (Pubitemid 36617947)
17. Fedor, M., Berman, R.F., Muizelaar, J.P., and Lyeth, B.G. (2010). Hippocampal theta dysfunction after lateral fluid percussion injury. J. Neurotrauma 27, 1605-1615.
18. Fesen, M.R., Kohn, K.W., Leteurtre, F., and Pommier, Y. (1993). Inhibitors of human immunodeficiency virus integrase. Proc. Natl. Acad. Sci. USA 90, 2399-2403. (Pubitemid 23078634)
19. Floyd, C.L., and Lyeth, B.G. (2007). Astroglia: important mediators of traumatic brain injury. Prog. Brain Res. 161, 61-79. (Pubitemid 47017399)
20. Giri, B.K., Krishnappa, I.K., Bryan, R.M., Jr., Robertson, C., and Watson, J. (2000). Regional cerebral blood flow after cortical impact injury complicated by a secondary insult in rats. Stroke 31, 961-967. (Pubitemid 30198446)
21. Giza, C.C., Prins, M.L., Hovda, D.A., Herschman, H.R., and Feldman, J.D. (2002). Genes preferentially induced by depolarization after concussive brain injury: effects of age and injury severity. J. Neurotrauma 19, 387-402. (Pubitemid 34412048)
22. Golding, E.M., Robertson, C.S., and Bryan, R.M., Jr. (1999). The consequences of traumatic brain injury on cerebral blood flow and autoregulation: a review. Clin. Exp. Hypertens. 21, 299-332. (Pubitemid 29239414)
23. Hall, E.D. (1993). The role of oxygen radicals in traumatic injury: clinical implications. J. Emerg. Med. 11 Suppl. 1, 31-36. (Pubitemid 23054996)
24. Hall, E.D., Vaishnav, R.A., and Mustafa, A.G. (2010). Antioxidant therapies for traumatic brain injury. Neurotherapeutics. 7, 51-61.
25. Hamm, R.J., Dixon, C.E., Gbadebo, D.M., Singha, A.K., Jenkins, L.W., Lyeth, B.G., and Hayes, R.L. (1992). Cognitive deficits following traumatic brain injury produced by controlled cortical impact. J. Neurotrauma 9, 11-20.
26. Hayes, R.L., and Dixon, C.E. (1994). Neurochemical changes in mild head injury. Semin. Neurol. 14, 25-31. (Pubitemid 24113259)
27. Hayes, R.L., Robinson, G., Muller, U., and Wang, K.K. (2009). Translation of neurological biomarkers to clinically relevant platforms. Methods Mol. Biol. 566, 303-313.
28. Hicks, R.R., Fertig, S.J., Desrocher, R.E., Koroshetz, W.J., and Pancrazio, J.J. (2010). Neurological effects of blast injury. J. Trauma 68, 1257-1263.
29. Hishikawa, K., Nakaki, T., and Fujita, T. (2005). Oral flavonoid supplementation attenuates atherosclerosis development in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 25, 442-446. (Pubitemid 40189171)
30. Honda, M., Nakagawa, S., Hayashi, K., Kitagawa, N., Tsutsumi, K., Nagata, I., and Niwa, M. (2006). Adrenomedullin improves the blood-brain barrier function through the expression of claudin-5. Cell Mol. Neurobiol. 26, 109-118. (Pubitemid 43881818)
31. Huh, J.W., and Raghupathi, R. (2009). New concepts in treatment of pediatric traumatic brain injury. Anesthesiol. Clin. 27, 213-240.
32. Igarashi, T., Huang, T.T., and Noble, L.J. (2001). Regional vulnerability after traumatic brain injury: gender differences in mice that overexpress human copper, zinc superoxide dismutase. Exp. Neurol. 172, 332-341. (Pubitemid 34075082)
33. Ilhan, A., Akyol, O., Gurel, A., Armutcu, F., Iraz, M., and Oztas, E. (2004). Protective effects of caffeic acid phenethyl ester against experimental allergic encephalomyelitis-induced oxidative stress in rats. Free Radic. Biol. Med. 37, 386-394. (Pubitemid 38834004)
34. Irmak, M.K., Fadillioglu, E., Sogut, S., Erdogan, H., Gulec, M., Ozer, M., Yagmurca, M., and Gozukara, M.E. (2003). Effects of caffeic acid phenethyl ester and alpha-tocopherol on reperfusion injury in rat brain. Cell Biochem. Funct. 21, 283-289. (Pubitemid 36988383)
35. Kalonia, H., Kumar, P., Kumar, A., and Nehru, B. (2009). Effect of caffeic acid and rofecoxib and their combination against intrastriatal quinolinic acid induced oxidative damage, mitochondrial and histological alterations in rats. Inflammopharmacology 17, 211-219.
36. Kelley, B.J., Lifshitz, J., and Povlishock, J.T. (2007). Neuroinflammatory responses after experimental diffuse traumatic brain injury. J. Neuropathol. Exp. Neurol. 66, 989-1001. (Pubitemid 350060367)
37. Khan, M., Elango, C., Ansari, M.A., Singh, I., and Singh, A.K. (2007). Caffeic acid phenethyl ester reduces neurovascular inflammation and protects rat brain following transient focal cerebral ischemia. J. Neurochem. 102, 365-377. (Pubitemid 47000595)
38. Khan, M., Im, Y.B., Shunmugavel, A., Gilg, A.G., Dhindsa, R.K., Singh, A.K., and Singh, I. (2009). Administration of Snitrosoglutathione after traumatic brain injury protects the neurovascular unit and reduces secondary injury in a rat model of controlled cortical impact. J. Neuroinflammation 6, 32.
39. Kochanek, A.R., Kline, A.E., Gao, W.M., Chadha, M., Lai, Y., Clark, R.S., Dixon, C.E., and Jenkins, L.W. (2006). Gel-based hippocampal proteomic analysis 2 weeks following traumatic brain injury to immature rats using controlled cortical impact. Dev. Neurosci. 28, 410-419. (Pubitemid 44310507)
40. Kolb, B., Sutherland, R.J., and Whishaw, I.Q. (1983). A comparison of the contributions of the frontal and parietal association cortex to spatial localization in rats. Behav. Neurosci. 97, 13-27. (Pubitemid 13046637)
41. Kono, Y., Kobayashi, K., Tagawa, S., Adachi, K., Ueda, A., Sawa, Y., and Shibata, H. (1997). Antioxidant activity of polyphenolics in diets. Rate constants of reactions of chlorogenic acid and caffeic acid with reactive species of oxygen and nitrogen. Biochim. Biophys. Acta 1335, 335-342. (Pubitemid 27274041)
42. Koshihara, Y., Neichi, T., Murota, S., Lao, A., Fujimoto, Y., and Tatsuno, T. (1984). Caffeic acid is a selective inhibitor for leukotriene biosynthesis. Biochim. Biophys. Acta 792, 92-97. (Pubitemid 14180908)
43. Liao, H.F., Chen, Y.Y., Liu, J.J., Hsu, M.L., Shieh, H.J., Liao, H.J., Shieh, C.J., Shiao, M.S., and Chen, Y.J. (2003). Inhibitory effect of caffeic acid phenethyl ester on angiogenesis, tumor invasion, and metastasis. J. Agric. Food Chem. 51, 7907-7912.
44. Lifshitz, J., Friberg, H., Neumar, R.W., Raghupathi, R., Welsh, F.A., Janmey, P., Saatman, K.E., Wieloch, T., Grady, M.S., and McIntosh, T.K. (2003). Structural and functional damage sustained by mitochondria after traumatic brain injury in the rat: evidence for differentially sensitive populations in the cortex and hippocampus. J. Cereb. Blood Flow Metab. 23, 219-231. (Pubitemid 36188460)
45. Loane, D.J., and Faden, A.I. (2010). Neuroprotection for traumatic brain injury: translational challenges and emerging therapeutic strategies. Trends Pharmacol. Sci. 31, 596-604.
46. Lotocki, G., Vaccari, J.P., Perez, E.R., Sanchez-Molano, J., Furones- Alonso, O., Bramlett, H.M., and Dietrich, W.D. (2009). Alterations in blood-brain barrier permeability to large and small molecules and leukocyte accumulation after traumatic brain injury: effects of post-traumatic hypothermia. J. Neurotrauma 26, 1123-1134.
47. Lyeth, B.G., Jenkins, L.W., Hamm, R.J., Dixon, C.E., Phillips, L.L., Clifton, G.L., Young, H.F., and Hayes, R.L. (1990). Prolonged memory impairment in the absence of hippocampal cell death following traumatic brain injury in the rat. Brain Res. 526, 249-258. (Pubitemid 20307884)
48. Margulies, S., and Hicks, R. (2009). Combination therapies for traumatic brain injury: prospective considerations. J. Neurotrauma 26, 925-939.
49. Meaney, D.F., and Smith, D.H. (2011). Biomechanics of concussion. Clin. Sports Med. 30, 19-31, vii.
50. Mechoulam, R., and Shohami, E. (2007). Endocannabinoids and traumatic brain injury. Mol. Neurobiol. 36, 68-74. (Pubitemid 351360359)
51. Michaluart, P., Masferrer, J.L., Carothers, A.M., Subbaramaiah, K., Zweifel, B.S., Koboldt, C., Mestre, J.R., Grunberger, D., Sacks, P.G., Tanabe, T., and Dannenberg, A.J. (1999). Inhibitory effects of caffeic acid phenethyl ester on the activity and expression of cyclooxygenase-2 in human oral epithelial cells and in a rat model of inflammation. Cancer Res. 59, 2347-2352. (Pubitemid 29242281)
52. Mirzoeva, O.K., and Calder, P.C. (1996). The effect of propolis and its components on eicosanoid production during the inflammatory response. Prostaglandins Leukot. Essent. Fatty Acids 55, 441-449. (Pubitemid 27014134)
53. Natarajan, K., Singh, S., Burke, T.R., Jr., Grunberger, D., and Aggarwal, B.B. (1996). Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc. Natl. Acad. Sci. USA 93, 9090-9095. (Pubitemid 26282023)
54. Orban, Z., Mitsiades, N., Burke, T.R., Jr., Tsokos, M., and Chrousos, G.P. (2000). Caffeic acid phenethyl ester induces leukocyte apoptosis, modulates nuclear factor-kappa B and suppresses acute inflammation. Neuroimmunomodulation 7, 99-105. (Pubitemid 30117304)
55. Orsolic, N., Terzic, S., Mihaljevic, Z., Sver, L., and Basic, I. (2005). Effects of local administration of propolis and its polyphenolic compounds on tumor formation and growth. Biol. Pharm. Bull. 28, 1928-1933. (Pubitemid 41437083)
56. Ottens, A.K., Bustamante, L., Golden, E.C., Yao, C., Hayes, R.L., Wang, K.K., Tortella, F.C., and Dave, J.R. (2010). Neuroproteomics: a biochemical means to discriminate the extent and modality of brain injury. J. Neurotrauma 27, 1837-1852.
57. Park, E.H., and Kahng, J.H. (1999). Suppressive effects of propolis in rat adjuvant arthritis. Arch. Pharm. Res. 22, 554-558.
58. Phillips, L.L., and Reeves, T.M. (2001). Interactive pathology following traumatic brain injury modifies hippocampal plasticity. Restor. Neurol. Neurosci 19, 213-235. (Pubitemid 33753776)
59. Povlishock, J.T., and Kontos, H.A. (1992). The role of oxygen radicals in the pathobiology of traumatic brain injury. Hum. Cell 5, 345-353.
60. Raghupathi, R. (2004). Cell death mechanisms following traumatic brain injury. Brain Pathol. 14, 215-222. (Pubitemid 38656395)
61. Ray, S.K., Dixon, C.E., and Banik, N.L. (2002). Molecular mechanisms in the pathogenesis of traumatic brain injury. Histol. Histopathol. 17, 1137-1152.
62. Reeves, T.M., Kao, C.Q., Phillips, L.L., Bullock, M.R., and Povlishock, J.T. (2000). Presynaptic excitability changes following traumatic brain injury in the rat. J. Neurosci. Res. 60, 370-379. (Pubitemid 30253601)
63. Royo, N.C., LeBold, D., Magge, S.N., Chen, I., Hauspurg, A., Cohen, A.S., and Watson, D.J. (2007). Neurotrophin-mediated neuroprotection of hippocampal neurons following traumatic brain injury is not associated with acute recovery of hippocampal function. Neuroscience 148, 359-370. (Pubitemid 47362511)
64. Saatman, K.E., Creed, J., and Raghupathi, R. (2010). Calpain as a therapeutic target in traumatic brain injury. Neurotherapeutics 7, 31-42.
65. Sayeed, I., and Stein, D.G. (2009). Progesterone as a neuroprotective factor in traumatic and ischemic brain injury. Prog. Brain Res. 175, 219-237.
66. Shear, D.A., Lu, X.C., Bombard, M.C., Pedersen, R., Chen, Z., Davis, A., and Tortella, F.C. (2010). Longitudinal characterization of motor and cognitive deficits in a model of penetrating ballistic-like brain injury. J. Neurotrauma 27, 1911-1923.
67. Shellington, D.K., Du, L., Wu, X., Exo, J., Vagni, V., Ma, L., Janesko-Feldman, K., Clark, R.S., Bayir, H., Dixon, C.E., Jenkins, L.W., Hsia, C.J., and Kochanek, P.M. (2011). Polynitroxylated pegylated hemoglobin: A novel neuroprotective hemoglobin for acute volume-limited fluid resuscitation after combined traumatic brain injury and hemorrhagic hypotension in mice. Crit. Care Med. 39, 494-505.
68. Smith, C.M., Chen, Y., Sullivan, M.L., Kochanek, P.M., and Clark, R.S. (2010). Autophagy in acute brain injury: feast, famine, or folly? Neurobiol.
69. Dis. Smith, S.L., Andrus, P.K., Zhang, J.R., and Hall, E.D. (1994). Direct measurement of hydroxyl radicals, lipid peroxidation, and blood-brain barrier disruption following unilateral cortical impact head injury in the rat. J. Neurotrauma 11, 393-404. (Pubitemid 24304691)
70. Sondheimer, E. (1958). On the distribution of caffeic acid and the chlorogenic acid isomers in plants. Arch. Biochem. Biophys. 74, 131-138.
71. Stewart, L.R., White, A.R., Jobling, M.F., Needham, B.E., Maher, F., Thyer, J., Beyreuther, K., Masters, C.L., Collins, S.J., and Cappai, R. (2001). Involvement of the 5-lipoxygenase pathway in the neurotoxicity of the prion peptide PrP106-126. J. Neurosci. Res. 65, 565-572. (Pubitemid 32847149)
72. Stoica, B.A., and Faden, A.I. (2010). Cell death mechanisms and modulation in traumatic brain injury.Neurotherapeutics 7, 3-12.
73. Sud'ina, G.F., Mirzoeva, O.K., Pushkareva, M.A., Korshunova, G.A., Sumbatyan, N.V., and Varfolomeev, S.D. (1993). Caffeic acid phenethyl ester as a lipoxygenase inhibitor with antioxidant properties. FEBS Lett. 329, 21-24. (Pubitemid 23248240)
74. Sullivan, P.G., Sebastian, A.H., and Hall, E.D. (2011). Therapeutic window analysis of the neuroprotective effects of cyclosporine a after traumatic brain injury. J. Neurotrauma 28, 311-318.
75. Uz, T., Pesold, C., Longone, P., and Manev, H. (1998). Agingassociated up-regulation of neuronal 5-lipoxygenase expression: putative role in neuronal vulnerability. FASEB J. 12, 439-449. (Pubitemid 28146523)
76. Vink, R., and Bullock, M.R. (2010). Traumatic brain injury: therapeutic challenges and new directions. Neurotherapeutics 7, 1-2.
77. Wei, X., Zhao, L., Ma, Z., Holtzman, D.M., Yan, C., Dodel, R.C., Hampel, H., Oertel, W., Farlow, M.R., and Du, Y. (2004). Caffeic acid phenethyl ester prevents neonatal hypoxicischaemic brain injury. Brain 127, 2629-2635. (Pubitemid 39627372)
78. Werner, C., and Engelhard, K. (2007). Pathophysiology of traumatic brain injury. Br. J. Anaesth. 99, 4-9. (Pubitemid 47072553)
79. Whalen, M.J., Carlos, T.M., Kochanek, P.M., and Heineman, S. (1998). Blood-brain barrier permeability, neutrophil accumulation and vascular adhesion molecule expression after controlled cortical impact in rats: a preliminary study. Acta Neurochir. Suppl. 71, 212-214. (Pubitemid 128444400)
80. Yakovlev, A.G., and Faden, A.I. (2001). Caspase-dependent apoptotic pathways in CNS injury. Mol. Neurobiol. 24, 131-144. (Pubitemid 34066682)
81. Yang, J.Q., Zhou, Q.X., Liu, B.Z., and He, B.C. (2008). Protection of mouse brain from aluminum-induced damage by caffeic acid. CNS Neurosci. Ther. 14, 10-16.
82. Zhang, L., Zhang, W.P., Chen, K.D., Qian, X.D., Fang, S.H., and Wei, E.Q. (2007). Caffeic acid attenuates neuronal damage, astrogliosis and glial scar formation in mouse brain with cryoinjury. Life Sci. 80, 530-537. (Pubitemid 46038325)
83. Zhao, J., Moore, A.N., Redell, J.B., and Dash, P.K. (2007). Enhancing expression of Nrf2-driven genes protects the bloodbrain barrier after brain injury. J. Neurosci. 27, 10240-10248. (Pubitemid 47450456)
84. Zhou, Y., Fang, S.H., Ye, Y.L., Chu, L.S., Zhang, W.P., Wang, M.L., and Wei, E.Q. (2006). Caffeic acid ameliorates early and delayed brain injuries after focal cerebral ischemia in rats. Acta Pharmacol. Sin. 27, 1103-1110. (Pubitemid 44410989)