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Published in: Metabolic Brain Disease 3/2018

01-06-2018 | Original Article

Vanillic acid attenuates cerebral hyperemia, blood-brain barrier disruption and anxiety-like behaviors in rats following transient bilateral common carotid occlusion and reperfusion

Authors: Seyed Esmaeil Khoshnam, Yaghoob Farbood, Hadi Fathi Moghaddam, Alireza Sarkaki, Mohammad Badavi, Layasadat Khorsandi

Published in: Metabolic Brain Disease | Issue 3/2018

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Abstract

Transient bilateral common carotid artery occlusion (tBCCAO), followed by reperfusion, is a model of transient global hypoperfusion. In the present study we aimed to investigate the probable effects of Vanillic acid (VA) on some physiological parameters including cerebral hyperemia, blood-brain barrier (BBB) disruption, anxiety behaviors and neurological deficits induced by bilateral occlusion of the common carotid arteries and reperfusion (BCCAO/R) in rats. Rats were randomly divided into four groups; Sham, BCCAO/R, VA and VA+ BCCAO/R. Chronic cerebral hypoperfusion was induced after 2 weeks of pretreatment by VA. Subsequently, sensorimotor scores, elevated plus maze tests, cerebral hyperemia, and BBB disruption were evaluated 72 h after 30 min of BCCAO. Pretreatment of rats by VA improved sensory motor signs, anxiolytic behavior in BCCAO/R rats compared with untreated rats (p < 0.05). Further, VA attenuated reactive hyperemia and BBB disruption in BCCAO/R rats compared with untreated rats (p < 0.01). To our knowledge, this study is the first to reveal VA could attenuate reactive hyperemia and improve BBB disruption following BCCAO/R, and could improve neurological scores and anxiety like behaviors in this model of cerebral hypoperfusion. These results suggest that VA could be a promising pretreatment agent in cerebral hypoperfusion.
Literature
go back to reference Aronsson ÅF, Spulber S, Popescu LM, Winblad B, Post C, Oprica M, Schultzberg M (2006) α-Melanocyte-stimulating hormone is neuroprotective in rat global cerebral ischemia. Neuropeptides 40:65–75CrossRef Aronsson ÅF, Spulber S, Popescu LM, Winblad B, Post C, Oprica M, Schultzberg M (2006) α-Melanocyte-stimulating hormone is neuroprotective in rat global cerebral ischemia. Neuropeptides 40:65–75CrossRef
go back to reference Badavi M, Khoshbaten A, Hajizadeh S (2000) Decreased response of rat knee joint blood vessels to phenylephrine in chronic inflammation: involvement of nitric oxide. Exp Physiol 85:49–55CrossRefPubMed Badavi M, Khoshbaten A, Hajizadeh S (2000) Decreased response of rat knee joint blood vessels to phenylephrine in chronic inflammation: involvement of nitric oxide. Exp Physiol 85:49–55CrossRefPubMed
go back to reference Belayev L, Busto R, Ikeda M, Rubin LL, Kajiwara A, Morgan L, Ginsberg MD (1998) Protection against blood–brain barrier disruption in focal cerebral ischemia by the type IV phosphodiesterase inhibitor BBB022: a quantitative study. Brain Res 787:277–285CrossRefPubMed Belayev L, Busto R, Ikeda M, Rubin LL, Kajiwara A, Morgan L, Ginsberg MD (1998) Protection against blood–brain barrier disruption in focal cerebral ischemia by the type IV phosphodiesterase inhibitor BBB022: a quantitative study. Brain Res 787:277–285CrossRefPubMed
go back to reference Calixto-Campos C s, Carvalho TT, Hohmann MS, Pinho-Ribeiro FA, Fattori V, Manchope MF, Zarpelon AC, Baracat MM, Georgetti SR, Casagrande R (2015) Vanillic acid inhibits inflammatory pain by inhibiting neutrophil recruitment, oxidative stress, cytokine production, and NFκB activation in mice. J Nat Prod 78:1799–1808CrossRefPubMed Calixto-Campos C s, Carvalho TT, Hohmann MS, Pinho-Ribeiro FA, Fattori V, Manchope MF, Zarpelon AC, Baracat MM, Georgetti SR, Casagrande R (2015) Vanillic acid inhibits inflammatory pain by inhibiting neutrophil recruitment, oxidative stress, cytokine production, and NFκB activation in mice. J Nat Prod 78:1799–1808CrossRefPubMed
go back to reference Chandler MJ, DeLeo J, Carney JM (1985) An unanesthetized-gerbil model of cerebral ischemia-induced behavioral changes. J Pharmacol Methods 14:137–146CrossRefPubMed Chandler MJ, DeLeo J, Carney JM (1985) An unanesthetized-gerbil model of cerebral ischemia-induced behavioral changes. J Pharmacol Methods 14:137–146CrossRefPubMed
go back to reference Chen D, Tang J, Khatibi NH, Zhu M, Li Y, Wang C, Jiang R, Tu L, Wang S (2011) Treatment with Z-ligustilide, a component of Angelica sinensis, reduces brain injury after a subarachnoid hemorrhage in rats. J Pharmacol Exp Ther 337:663–672CrossRefPubMed Chen D, Tang J, Khatibi NH, Zhu M, Li Y, Wang C, Jiang R, Tu L, Wang S (2011) Treatment with Z-ligustilide, a component of Angelica sinensis, reduces brain injury after a subarachnoid hemorrhage in rats. J Pharmacol Exp Ther 337:663–672CrossRefPubMed
go back to reference Cheng C-Y, Su S-Y, Tang N-Y, Ho T-Y, Chiang S-Y, Hsieh C-L (2008) Ferulic acid provides neuroprotection against oxidative stress-related apoptosis after cerebral ischemia/reperfusion injury by inhibiting ICAM-1 mRNA expression in rats. Brain Res 1209:136–150CrossRefPubMed Cheng C-Y, Su S-Y, Tang N-Y, Ho T-Y, Chiang S-Y, Hsieh C-L (2008) Ferulic acid provides neuroprotection against oxidative stress-related apoptosis after cerebral ischemia/reperfusion injury by inhibiting ICAM-1 mRNA expression in rats. Brain Res 1209:136–150CrossRefPubMed
go back to reference Cho J-Y, Kim I-S, Jang Y-H, Kim A-R, Lee S-R (2006) Protective effect of quercetin, a natural flavonoid against neuronal damage after transient global cerebral ischemia. Neurosci Lett 404:330–335CrossRefPubMed Cho J-Y, Kim I-S, Jang Y-H, Kim A-R, Lee S-R (2006) Protective effect of quercetin, a natural flavonoid against neuronal damage after transient global cerebral ischemia. Neurosci Lett 404:330–335CrossRefPubMed
go back to reference Coyle P, Panzenbeck MJ (1990) Collateral development after carotid artery occlusion in Fischer 344 rats. Stroke 21:316–321CrossRefPubMed Coyle P, Panzenbeck MJ (1990) Collateral development after carotid artery occlusion in Fischer 344 rats. Stroke 21:316–321CrossRefPubMed
go back to reference Delaquis P, Stanich K, Toivonen P (2005) Effect of pH on the inhibition of Listeria spp. by vanillin and vanillic acid. J. Food Prot 68:1472–1476CrossRef Delaquis P, Stanich K, Toivonen P (2005) Effect of pH on the inhibition of Listeria spp. by vanillin and vanillic acid. J. Food Prot 68:1472–1476CrossRef
go back to reference Dianat, M., G. R. Hamzavi, M. Badavi and A. Samarbaf-zadeh (2015) Effect of vanillic acid on ischemia-reperfusion of isolated rat heart: Hemodynamic parameters and infarct size assays Dianat, M., G. R. Hamzavi, M. Badavi and A. Samarbaf-zadeh (2015) Effect of vanillic acid on ischemia-reperfusion of isolated rat heart: Hemodynamic parameters and infarct size assays
go back to reference Dianat M, Radmanesh E, Badavi M, Mard SA, Goudarzi G (2016) Disturbance effects of PM10 on iNOS and eNOS mRNA expression levels and antioxidant activity induced by ischemia–reperfusion injury in isolated rat heart: protective role of vanillic acid. Environ Sci Pollut Res 23:5154–5165CrossRef Dianat M, Radmanesh E, Badavi M, Mard SA, Goudarzi G (2016) Disturbance effects of PM10 on iNOS and eNOS mRNA expression levels and antioxidant activity induced by ischemia–reperfusion injury in isolated rat heart: protective role of vanillic acid. Environ Sci Pollut Res 23:5154–5165CrossRef
go back to reference Farbood Y, Sarkaki A, Khalaj L, Khodagholi F, Badavi M, Ashabi G (2015) Targeting Adenosine Monophosphate-Activated Protein Kinase by Metformin Adjusts Post-Ischemic Hyperemia and Extracellular Neuronal Discharge in Transient Global Cerebral Ischemia. Microcirculation 22:534–541CrossRefPubMed Farbood Y, Sarkaki A, Khalaj L, Khodagholi F, Badavi M, Ashabi G (2015) Targeting Adenosine Monophosphate-Activated Protein Kinase by Metformin Adjusts Post-Ischemic Hyperemia and Extracellular Neuronal Discharge in Transient Global Cerebral Ischemia. Microcirculation 22:534–541CrossRefPubMed
go back to reference Farkas E, Luiten PG, Bari F (2007) Permanent, bilateral common carotid artery occlusion in the rat: a model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Res Rev 54:162–180CrossRefPubMed Farkas E, Luiten PG, Bari F (2007) Permanent, bilateral common carotid artery occlusion in the rat: a model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Res Rev 54:162–180CrossRefPubMed
go back to reference Garcia JH, Wagner S, Liu K-F, Hu X-j (1995) Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Stroke 26:627–635CrossRefPubMed Garcia JH, Wagner S, Liu K-F, Hu X-j (1995) Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Stroke 26:627–635CrossRefPubMed
go back to reference Hori E, Uwano T, Tamura R, Miyake N, Nishijo H, Ono T (2002) Effects of a novel arginine-vasopressin derivative, NC-1900, on the spatial memory impairment of rats with transient forebrain ischemia. Cogn Brain Res 13:1–15CrossRef Hori E, Uwano T, Tamura R, Miyake N, Nishijo H, Ono T (2002) Effects of a novel arginine-vasopressin derivative, NC-1900, on the spatial memory impairment of rats with transient forebrain ischemia. Cogn Brain Res 13:1–15CrossRef
go back to reference Hori M, Kitakaze M (1991) Adenosine, the heart, and coronary circulation. Hypertension 18:565–574CrossRefPubMed Hori M, Kitakaze M (1991) Adenosine, the heart, and coronary circulation. Hypertension 18:565–574CrossRefPubMed
go back to reference Iwasaki Y, Ito S, Suzuki M, Nagahori T, Yamamoto T, Konno H (1989) Forebrain ischemia induced by temporary bilateral common carotid occlusion in normotensive rats. J Neurol Sci 90:155–165CrossRefPubMed Iwasaki Y, Ito S, Suzuki M, Nagahori T, Yamamoto T, Konno H (1989) Forebrain ischemia induced by temporary bilateral common carotid occlusion in normotensive rats. J Neurol Sci 90:155–165CrossRefPubMed
go back to reference Jian H, Yi-Fang W, Qi L, Xiao-Song H, Gui-Yun Z (2013) Cerebral blood flow and metabolic changes in hippocampal regions of a modified rat model with chronic cerebral hypoperfusion. Acta Neurol Belg 113:313–317CrossRefPubMed Jian H, Yi-Fang W, Qi L, Xiao-Song H, Gui-Yun Z (2013) Cerebral blood flow and metabolic changes in hippocampal regions of a modified rat model with chronic cerebral hypoperfusion. Acta Neurol Belg 113:313–317CrossRefPubMed
go back to reference Jiang J, Wang W, Sun YJ, Hu M, Li F, Zhu DY (2007) Neuroprotective effect of curcumin on focal cerebral ischemic rats by preventing blood–brain barrier damage. Eur J Pharmacol 561:54–62CrossRefPubMed Jiang J, Wang W, Sun YJ, Hu M, Li F, Zhu DY (2007) Neuroprotective effect of curcumin on focal cerebral ischemic rats by preventing blood–brain barrier damage. Eur J Pharmacol 561:54–62CrossRefPubMed
go back to reference Kam A, Li KM, Razmovski-Naumovski V, Nammi S, Chan K, Li Y, Li GQ (2012) The protective effects of natural products on blood-brain barrier breakdown. Curr Med Chem 19:1830–1845CrossRefPubMed Kam A, Li KM, Razmovski-Naumovski V, Nammi S, Chan K, Li Y, Li GQ (2012) The protective effects of natural products on blood-brain barrier breakdown. Curr Med Chem 19:1830–1845CrossRefPubMed
go back to reference Khaksari M, Mahmmodi R, Shahrokhi N, Shabani M, Joukar S, Aqapour M (2013) The effects of shilajit on brain edema, intracranial pressure and neurologic outcomes following the traumatic brain injury in rat. Iranian J Basic Med Scie 16:858–864 Khaksari M, Mahmmodi R, Shahrokhi N, Shabani M, Joukar S, Aqapour M (2013) The effects of shilajit on brain edema, intracranial pressure and neurologic outcomes following the traumatic brain injury in rat. Iranian J Basic Med Scie 16:858–864
go back to reference Khoshnam S, Sarkaki A, Khorsandi L, Winlow W, Badavi M, Moghaddam H, Farbooda Y (2017a) Vanillic acid attenuates effects of transient bilateral common carotid occlusion and reperfusion in rats. Biomed Pharmacotherapy = Biomed Pharmacotherapie 96:667CrossRef Khoshnam S, Sarkaki A, Khorsandi L, Winlow W, Badavi M, Moghaddam H, Farbooda Y (2017a) Vanillic acid attenuates effects of transient bilateral common carotid occlusion and reperfusion in rats. Biomed Pharmacotherapy = Biomed Pharmacotherapie 96:667CrossRef
go back to reference Khoshnam SE, Winlow W, Farbood Y, Moghaddam HF, Farzaneh M (2017b) Emerging Roles of microRNAs in Ischemic Stroke: As Possible Therapeutic Agents. J Stroke 19:166CrossRefPubMedPubMedCentral Khoshnam SE, Winlow W, Farbood Y, Moghaddam HF, Farzaneh M (2017b) Emerging Roles of microRNAs in Ischemic Stroke: As Possible Therapeutic Agents. J Stroke 19:166CrossRefPubMedPubMedCentral
go back to reference Khoshnam, S. E., W. Winlow and M. Farzaneh (2017c) The Interplay of MicroRNAs in the Inflammatory Mechanisms Following Ischemic Stroke. Journal of Neuropathology & Experimental Neurology:nlx036 Khoshnam, S. E., W. Winlow and M. Farzaneh (2017c) The Interplay of MicroRNAs in the Inflammatory Mechanisms Following Ischemic Stroke. Journal of Neuropathology & Experimental Neurology:nlx036
go back to reference Khoshnam, S. E., W. Winlow, M. Farzaneh, Y. Farbood and H. F. Moghaddam (2017d) Pathogenic mechanisms following ischemic stroke. Neurological Sciences:1–20 Khoshnam, S. E., W. Winlow, M. Farzaneh, Y. Farbood and H. F. Moghaddam (2017d) Pathogenic mechanisms following ischemic stroke. Neurological Sciences:1–20
go back to reference Kim M-C, Kim S-J, Kim D-S, Jeon Y-D, Park SJ, Lee HS, Um J-Y, Hong S-H (2011) Vanillic acid inhibits inflammatory mediators by suppressing NF-κB in lipopolysaccharide-stimulated mouse peritoneal macrophages. Immunopharmacol Immunotoxicol 33:525–532CrossRefPubMed Kim M-C, Kim S-J, Kim D-S, Jeon Y-D, Park SJ, Lee HS, Um J-Y, Hong S-H (2011) Vanillic acid inhibits inflammatory mediators by suppressing NF-κB in lipopolysaccharide-stimulated mouse peritoneal macrophages. Immunopharmacol Immunotoxicol 33:525–532CrossRefPubMed
go back to reference Kim S-J, Kim M-C, Um J-Y, Hong S-H (2010) The beneficial effect of vanillic acid on ulcerative colitis. Molecules 15:7208–7217CrossRefPubMed Kim S-J, Kim M-C, Um J-Y, Hong S-H (2010) The beneficial effect of vanillic acid on ulcerative colitis. Molecules 15:7208–7217CrossRefPubMed
go back to reference Koh P-O (2012) Ferulic acid modulates nitric oxide synthase expression in focal cerebral ischemia. Lab Animal Res 28:273–278CrossRef Koh P-O (2012) Ferulic acid modulates nitric oxide synthase expression in focal cerebral ischemia. Lab Animal Res 28:273–278CrossRef
go back to reference Lapi D, Marchiafava P, Colantuoni A (2008) Pial microvascular responses to transient bilateral common carotid artery occlusion: effects of hypertonic glycerol. J Vasc Res 45:89–102CrossRefPubMed Lapi D, Marchiafava P, Colantuoni A (2008) Pial microvascular responses to transient bilateral common carotid artery occlusion: effects of hypertonic glycerol. J Vasc Res 45:89–102CrossRefPubMed
go back to reference Lapi, D., S. Vagnani, G. Pignataro, E. Esposito, M. Paterni and A. Colantuoni (2012a) Protective effects of quercetin on rat pial microvascular changes during transient bilateral common carotid artery occlusion and reperfusion. Front. Physiol 3 Lapi, D., S. Vagnani, G. Pignataro, E. Esposito, M. Paterni and A. Colantuoni (2012a) Protective effects of quercetin on rat pial microvascular changes during transient bilateral common carotid artery occlusion and reperfusion. Front. Physiol 3
go back to reference Lapi, D., S. Vagnani, G. Pignataro, E. Esposito, M. Paterni and A. Colantuoni (2012b) Rat pial microvascular responses to transient bilateral common carotid artery occlusion and reperfusion: quercetin’s mechanism of action. Front. Physiol 3 Lapi, D., S. Vagnani, G. Pignataro, E. Esposito, M. Paterni and A. Colantuoni (2012b) Rat pial microvascular responses to transient bilateral common carotid artery occlusion and reperfusion: quercetin’s mechanism of action. Front. Physiol 3
go back to reference Latour LL, Kang DW, Ezzeddine MA, Chalela JA, Warach S (2004) Early blood–brain barrier disruption in human focal brain ischemia. Ann Neurol 56:468–477CrossRefPubMed Latour LL, Kang DW, Ezzeddine MA, Chalela JA, Warach S (2004) Early blood–brain barrier disruption in human focal brain ischemia. Ann Neurol 56:468–477CrossRefPubMed
go back to reference Leal L, Pierdoná T, Góes J, Fonsêca K, Canuto K, Silveira E, Bezerra A, Viana G (2011) A comparative chemical and pharmacological study of standardized extracts and vanillic acid from wild and cultivated Amburana cearensis AC Smith. Phytomedicine 18:230–233CrossRefPubMed Leal L, Pierdoná T, Góes J, Fonsêca K, Canuto K, Silveira E, Bezerra A, Viana G (2011) A comparative chemical and pharmacological study of standardized extracts and vanillic acid from wild and cultivated Amburana cearensis AC Smith. Phytomedicine 18:230–233CrossRefPubMed
go back to reference Li H, Wang J, Wang P, Rao Y, Chen L (2016) Resveratrol reverses the synaptic plasticity deficits in a chronic cerebral hypoperfusion rat model. J Stroke Cerebrovasc Dis 25:122–128CrossRefPubMed Li H, Wang J, Wang P, Rao Y, Chen L (2016) Resveratrol reverses the synaptic plasticity deficits in a chronic cerebral hypoperfusion rat model. J Stroke Cerebrovasc Dis 25:122–128CrossRefPubMed
go back to reference Liu Y, Tang G, Li Y, Wang Y, Chen X, Gu X, Zhang Z, Wang Y, Yang G-Y (2014) Metformin attenuates blood-brain barrier disruption in mice following middle cerebral artery occlusion. J Neuroinflammation 11:177CrossRefPubMedPubMedCentral Liu Y, Tang G, Li Y, Wang Y, Chen X, Gu X, Zhang Z, Wang Y, Yang G-Y (2014) Metformin attenuates blood-brain barrier disruption in mice following middle cerebral artery occlusion. J Neuroinflammation 11:177CrossRefPubMedPubMedCentral
go back to reference Menard J, Treit D (1998) The septum and the hippocampus differentially mediate anxiolytic effects of R (+)-8-OH-DPAT. Behav Pharmacol 9:93–101PubMed Menard J, Treit D (1998) The septum and the hippocampus differentially mediate anxiolytic effects of R (+)-8-OH-DPAT. Behav Pharmacol 9:93–101PubMed
go back to reference Milot MR, Plamondon H (2009) Time-dependent effects of global cerebral ischemia on anxiety, locomotion, and habituation in rats. Behav Brain Res 200:173–180CrossRefPubMed Milot MR, Plamondon H (2009) Time-dependent effects of global cerebral ischemia on anxiety, locomotion, and habituation in rats. Behav Brain Res 200:173–180CrossRefPubMed
go back to reference O'Connor CA, Cernak I, Vink R (2005) Both estrogen and progesterone attenuate edema formation following diffuse traumatic brain injury in rats. Brain Res 1062:171–174CrossRefPubMed O'Connor CA, Cernak I, Vink R (2005) Both estrogen and progesterone attenuate edema formation following diffuse traumatic brain injury in rats. Brain Res 1062:171–174CrossRefPubMed
go back to reference Onetti Y, Dantas AP, Pérez B, Cugota R, Chamorro A, Planas AM, Vila E, Jiménez-Altayó F (2015) Middle cerebral artery remodeling following transient brain ischemia is linked to early postischemic hyperemia: a target of uric acid treatment. Am J Phys Heart Circ Phys 308:H862–H874 Onetti Y, Dantas AP, Pérez B, Cugota R, Chamorro A, Planas AM, Vila E, Jiménez-Altayó F (2015) Middle cerebral artery remodeling following transient brain ischemia is linked to early postischemic hyperemia: a target of uric acid treatment. Am J Phys Heart Circ Phys 308:H862–H874
go back to reference Pérez-Asensio FJ, De la Rosa X, Jiménez-Altayó F, Gorina R, Martínez E, Messeguer À, Vila E, Chamorro À, Planas AM (2010) Antioxidant CR-6 protects against reperfusion injury after a transient episode of focal brain ischemia in rats. J Cereb Blood Flow Metab 30:638–652CrossRefPubMed Pérez-Asensio FJ, De la Rosa X, Jiménez-Altayó F, Gorina R, Martínez E, Messeguer À, Vila E, Chamorro À, Planas AM (2010) Antioxidant CR-6 protects against reperfusion injury after a transient episode of focal brain ischemia in rats. J Cereb Blood Flow Metab 30:638–652CrossRefPubMed
go back to reference Pietrelli A, Lopez-Costa J, Goni R, Brusco A, Basso N (2012) Aerobic exercise prevents age-dependent cognitive decline and reduces anxiety-related behaviors in middle-aged and old rats. Neuroscience 202:252–266CrossRefPubMed Pietrelli A, Lopez-Costa J, Goni R, Brusco A, Basso N (2012) Aerobic exercise prevents age-dependent cognitive decline and reduces anxiety-related behaviors in middle-aged and old rats. Neuroscience 202:252–266CrossRefPubMed
go back to reference Pillow, B. H. and J. H. Flavell (1985) Intellectual realism: The role of children's interpretations of pictures and perceptual verbs. Child Dev :664–670 Pillow, B. H. and J. H. Flavell (1985) Intellectual realism: The role of children's interpretations of pictures and perceptual verbs. Child Dev :664–670
go back to reference Preitner F, Muzzin P, Revelli JP, Seydoux J, Galitzky J, Berlan M, Lafontan M, Giacobino JP (1998) Metabolic response to various β-adrenoceptor agonists in β3-adrenoceptor knockout mice: Evidence for a new β-adrenergic receptor in brown adipose tissue. Br J Pharmacol 124:1684–1688CrossRefPubMedPubMedCentral Preitner F, Muzzin P, Revelli JP, Seydoux J, Galitzky J, Berlan M, Lafontan M, Giacobino JP (1998) Metabolic response to various β-adrenoceptor agonists in β3-adrenoceptor knockout mice: Evidence for a new β-adrenergic receptor in brown adipose tissue. Br J Pharmacol 124:1684–1688CrossRefPubMedPubMedCentral
go back to reference Prince PSM, Rajakumar S, Dhanasekar K (2011) Protective effects of vanillic acid on electrocardiogram, lipid peroxidation, antioxidants, proinflammatory markers and histopathology in isoproterenol induced cardiotoxic rats. Eur J Pharmacol 668:233–240CrossRef Prince PSM, Rajakumar S, Dhanasekar K (2011) Protective effects of vanillic acid on electrocardiogram, lipid peroxidation, antioxidants, proinflammatory markers and histopathology in isoproterenol induced cardiotoxic rats. Eur J Pharmacol 668:233–240CrossRef
go back to reference Pun PB, Lu J, Moochhala S (2009) Involvement of ROS in BBB dysfunction. Free Radic Res 43:348–364CrossRefPubMed Pun PB, Lu J, Moochhala S (2009) Involvement of ROS in BBB dysfunction. Free Radic Res 43:348–364CrossRefPubMed
go back to reference Quartu M, Serra MP, Boi M, Pillolla G, Melis T, Poddighe L, Del Fiacco M, Falconieri D, Carta G, Murru E (2012) Effect of acute administration of Pistacia lentiscus L. essential oil on rat cerebral cortex following transient bilateral common carotid artery occlusion. Lipids Health Dis 11:8CrossRefPubMedPubMedCentral Quartu M, Serra MP, Boi M, Pillolla G, Melis T, Poddighe L, Del Fiacco M, Falconieri D, Carta G, Murru E (2012) Effect of acute administration of Pistacia lentiscus L. essential oil on rat cerebral cortex following transient bilateral common carotid artery occlusion. Lipids Health Dis 11:8CrossRefPubMedPubMedCentral
go back to reference Sarti C, Pantoni L, Bartolini L, Inzitari D (2002a) Cognitive impairment and chronic cerebral hypoperfusion: what can be learned from experimental models. J Neurol Sci 203:263–266CrossRefPubMed Sarti C, Pantoni L, Bartolini L, Inzitari D (2002a) Cognitive impairment and chronic cerebral hypoperfusion: what can be learned from experimental models. J Neurol Sci 203:263–266CrossRefPubMed
go back to reference Sarti C, Pantoni L, Bartolini L, Inzitari D (2002b) Persistent impairment of gait performances and working memory after bilateral common carotid artery occlusion in the adult Wistar rat. Behav Brain Res 136:13–20CrossRefPubMed Sarti C, Pantoni L, Bartolini L, Inzitari D (2002b) Persistent impairment of gait performances and working memory after bilateral common carotid artery occlusion in the adult Wistar rat. Behav Brain Res 136:13–20CrossRefPubMed
go back to reference Shlosberg D, Benifla M, Kaufer D, Friedman A (2010) Blood–brain barrier breakdown as a therapeutic target in traumatic brain injury. Nat Rev Neurol 6:393–403CrossRefPubMedPubMedCentral Shlosberg D, Benifla M, Kaufer D, Friedman A (2010) Blood–brain barrier breakdown as a therapeutic target in traumatic brain injury. Nat Rev Neurol 6:393–403CrossRefPubMedPubMedCentral
go back to reference Singh JCH, Kakalij RM, Kshirsagar RP, Kumar BH, Komakula SSB, Diwan PV (2015) Cognitive effects of vanillic acid against streptozotocin-induced neurodegeneration in mice. Pharm Biol 53:630–636CrossRefPubMed Singh JCH, Kakalij RM, Kshirsagar RP, Kumar BH, Komakula SSB, Diwan PV (2015) Cognitive effects of vanillic acid against streptozotocin-induced neurodegeneration in mice. Pharm Biol 53:630–636CrossRefPubMed
go back to reference Takata F, Dohgu S, Matsumoto J, Machida T, Kaneshima S, Matsuo M, Sakaguchi S, Takeshige Y, Yamauchi A, Kataoka Y (2013) Metformin induces up-regulation of blood–brain barrier functions by activating AMP-activated protein kinase in rat brain microvascular endothelial cells. Biochem Biophys Res Commun 433:586–590CrossRefPubMed Takata F, Dohgu S, Matsumoto J, Machida T, Kaneshima S, Matsuo M, Sakaguchi S, Takeshige Y, Yamauchi A, Kataoka Y (2013) Metformin induces up-regulation of blood–brain barrier functions by activating AMP-activated protein kinase in rat brain microvascular endothelial cells. Biochem Biophys Res Commun 433:586–590CrossRefPubMed
go back to reference Tsapenko, M., M. Weber, A. Moser, M. Keupp, W. Timmermann, S. Debus, A. Thiede and H. Henrich (2001) Restoration of blood circulation in reperfusion of ischemic tissues. Klin Khir :45–47 Tsapenko, M., M. Weber, A. Moser, M. Keupp, W. Timmermann, S. Debus, A. Thiede and H. Henrich (2001) Restoration of blood circulation in reperfusion of ischemic tissues. Klin Khir :45–47
go back to reference Ulrich PT, Kroppenstedt S, Heimann A, Kempski O (1998) Laser-Doppler scanning of local cerebral blood flow and reserve capacity and testing of motor and memory functions in a chronic 2-vessel occlusion model in rats. Stroke 29:2412–2420CrossRefPubMed Ulrich PT, Kroppenstedt S, Heimann A, Kempski O (1998) Laser-Doppler scanning of local cerebral blood flow and reserve capacity and testing of motor and memory functions in a chronic 2-vessel occlusion model in rats. Stroke 29:2412–2420CrossRefPubMed
go back to reference Urquiaga I, Leighton F (2000) Plant polyphenol antioxidants and oxidative stress. Biol Res 33:55–64CrossRefPubMed Urquiaga I, Leighton F (2000) Plant polyphenol antioxidants and oxidative stress. Biol Res 33:55–64CrossRefPubMed
go back to reference Winter B, Juckel G, Viktorov I, Katchanov J, Gietz A, Sohr R, Balkaya M, Hörtnagl H, Endres M (2005) Anxious and hyperactive phenotype following brief ischemic episodes in mice. Biol Psychiatry 57:1166–1175CrossRefPubMed Winter B, Juckel G, Viktorov I, Katchanov J, Gietz A, Sohr R, Balkaya M, Hörtnagl H, Endres M (2005) Anxious and hyperactive phenotype following brief ischemic episodes in mice. Biol Psychiatry 57:1166–1175CrossRefPubMed
go back to reference Xu X, Li Z, Yang Z, Zhang T (2012) Decrease of synaptic plasticity associated with alteration of information flow in a rat model of vascular dementia. Neuroscience 206:136–143CrossRefPubMed Xu X, Li Z, Yang Z, Zhang T (2012) Decrease of synaptic plasticity associated with alteration of information flow in a rat model of vascular dementia. Neuroscience 206:136–143CrossRefPubMed
go back to reference Yanpallewar S, Hota D, Rai S, Kumar M, Acharya S (2004) Nimodipine attenuates biochemical, behavioral and histopathological alterations induced by acute transient and long-term bilateral common carotid occlusion in rats. Pharmacol Res 49:143–150CrossRefPubMed Yanpallewar S, Hota D, Rai S, Kumar M, Acharya S (2004) Nimodipine attenuates biochemical, behavioral and histopathological alterations induced by acute transient and long-term bilateral common carotid occlusion in rats. Pharmacol Res 49:143–150CrossRefPubMed
go back to reference Zhao H, Steinberg GK, Sapolsky RM (2007) General versus specific actions of mild-moderate hypothermia in attenuating cerebral ischemic damage. J Cereb Blood Flow Metab 27:1879–1894CrossRefPubMed Zhao H, Steinberg GK, Sapolsky RM (2007) General versus specific actions of mild-moderate hypothermia in attenuating cerebral ischemic damage. J Cereb Blood Flow Metab 27:1879–1894CrossRefPubMed
Metadata
Title
Vanillic acid attenuates cerebral hyperemia, blood-brain barrier disruption and anxiety-like behaviors in rats following transient bilateral common carotid occlusion and reperfusion
Authors
Seyed Esmaeil Khoshnam
Yaghoob Farbood
Hadi Fathi Moghaddam
Alireza Sarkaki
Mohammad Badavi
Layasadat Khorsandi
Publication date
01-06-2018
Publisher
Springer US
Published in
Metabolic Brain Disease / Issue 3/2018
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-018-0187-5

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