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Neurological Research
A Journal of Progress in Neurosurgery, Neurology and Neurosciences
Volume 42, 2020 - Issue 3
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ORIGINAL RESEARCH PAPER

Neuroprotection by trans-resveratrol against collagenase-induced neurological and neurobehavioural deficits in rats involves adenosine A1 receptors

, ORCID Icon, ORCID Icon, ORCID Icon, &
Pages 189-208 | Received 28 Aug 2019, Accepted 29 Dec 2019, Published online: 04 Feb 2020

References

  • Sacco RL, Kasner SE, Broderick JP, et al. An updated definition of stroke for the 21st century: A statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2013;44:2064–2089. DOI:10.1161/STR.0b013e318296aeca
  • Niu M, Dai X, Zou W, et al. Autophagy, endoplasmic reticulum stress and the unfolded protein response in intracerebral hemorrhage. Transl Neurosci. 2017;8:37–48. DOI:10.1515/tnsci-2017-0008
  • Go AS, Mozaffarian D, Roger VL, et al. Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation. 2013;127:e6-e245. DOI:10.1161/CIR.0b013e31828124ad
  • Feigin VL, Lawes CM, Bennett DA, et al. Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review. Lancet Neurol. 2009;8:355–369. DOI:10.1016/S1474-4422(09)70025-0
  • Jones SB, Sen S, Lakshminarayan K, et al. Poststroke outcomes vary by pathogenic stroke subtype in the atherosclerosis risk in communities study. Stroke. 2013;44:2307–2310. DOI:10.1161/STROKEAHA.113.000830
  • Aronowski J, Zhao X. Molecular pathophysiology of cerebral hemorrhage: secondary brain injury. Stroke. 2011;42:1781–1786. DOI:10.1161/STROKEAHA.110.596718
  • Cai JC, Liu W, Lu F, et al. Resveratrol attenuates neurological deficit and neuroinflammation following intracerebral hemorrhage. Exp Ther Med. 2018;4131–4138. DOI:10.3892/etm.2018.5938
  • Wang Y, Zeigler MM, Lam GK, et al. The role of the NADPH oxidase complex, p38 MAPK, and Akt in regulating human monocyte/macrophage survival. Am J Respir Cell Mol Biol. 2007;36:68–77. DOI:10.1165/rcmb.2006-0165OC
  • Wang T, Nowrangi D, Yu L, et al. Activation of dopamine D1 receptor decreased NLRP3-mediated inflammation in intracerebral hemorrhage mice. J Neuroinflammation. 2018;15:2. DOI:10.1186/s12974-017-1039-7
  • Lan X, Han X, Li Q, et al. Pinocembrin protects hemorrhagic brain primarily by inhibiting toll-like receptor 4 and reducing M1 phenotype microglia. Brain Behav Immun. 2017;61:326–339. DOI:10.1016/j.bbi.2016.12.012
  • Percie Du Sert N, Alfieri A, Allan SM, et al. The IMPROVE guidelines (Ischaemia models: procedural refinements of in vivo experiments). J Cereb Blood Flow Metab. 2017;37:3488–3517. DOI:10.1177/0271678X17709185
  • Shi J, Wu G, Zou X, et al. Oleuropein protects intracerebral hemorrhage-induced disruption of blood-brain barrier through alleviation of oxidative stress. Pharmacol Reports. 2017;69:1206–1212. DOI:10.1016/j.pharep.2017.05.004
  • Wang JP, Zhang MY. Role for Target of Rapamycin (mTOR) signal pathway in regulating neuronal injury after intracerebral hemorrhage. Cell Physiol Biochem. 2017;41:145–153. DOI:10.1159/000455983
  • Yuan R, Fan H, Cheng S, et al. Silymarin prevents NLRP3 inflammasome activation and protects against intracerebral hemorrhage. Biomed Pharmacother. 2017;93:308–315. DOI:10.1016/j.biopha.2017.06.018
  • Zeng J, Chen Y, Ding R, et al. Isoliquiritigenin alleviates early brain injury after experimental intracerebral hemorrhage via suppressing ROS- and/or NF- κ B-mediated NLRP3 inflammasome activation by promoting Nrf2 antioxidant pathway. J Neuroinflammation. 2017;14:119. DOI:10.1186/s12974-017-0895-5
  • Rorato R, Borges BDC, Uchoa ET. LPS-induced low-grade inflammation increases hypothalamic JNK expression and causes central insulin resistance irrespective of body weight changes. Int J Mol Sci. 2017;18:1431. DOI:10.3390/ijms18071431
  • Lei C, Wu B, Cao T, et al. Activation of the high-mobility group box 1 protein-receptor for advanced glycation end-products signaling pathway in rats during neurogenesis after intracerebral hemorrhage. Stroke. 2015;46:500–506. DOI:10.1161/STROKEAHA.114.006825
  • Lei C, Zhang S, Cao T, et al. HMGB1 may act via RAGE to promote angiogenesis in the later phase after intracerebral hemorrhage. Neuroscience. 2015;295:39–47. DOI:10.1016/j.neuroscience.2015.03.032
  • Shen X, Ma L, Dong W, et al. Autophagy regulates intracerebral hemorrhage induced neural damage via apoptosis and NF-κB pathway. Neurochem Int. 2016;96:100–112. DOI:10.1016/j.neuint.2016.03.004
  • Kim CK, Ryu WS, Choi IY, et al. Detrimental effects of leptin on intracerebral hemorrhage via the STAT3 signal pathway. J Cereb Blood Flow Metab. 2013;33:944–953. DOI:10.1038/jcbfm.2013.35
  • King MD, Whitaker-Lea WA, Campbell JM, et al. Necrostatin-1 reduces neurovascular injury after intracerebral hemorrhage. Int J Cell Biol. 2014;2014:15–17. DOI:10.1155/2014/495817
  • Sperlágh B, Vizi ES. The role of extracellular adenosine in chemical neurotransmission in the hippocampus and basal ganglia: pharmacological and clinical aspects. Curr Top Med Chem. 2011;11:1034–1046. DOI:10.2174/156802611795347564
  • Boison D, Chen J-F, Fredholm BB. Adenosine signalling and function in glial cells. Cell Death Differ. 2010;17:1071-1082. DOI:10.1038/cdd.2009.131
  • Gomes CV, Kaster MP, Tomé AR, et al. Adenosine receptors and brain diseases: neuroprotection and neurodegeneration. Biochim Biophys Acta - Biomembr. 2011;1808:1380–1399. DOI:10.1016/j.bbamem.2010.12.001
  • Cipriani R, Villa P, Chece G, et al. CX3CL1 is neuroprotective in permanent focal cerebral ischemia in rodents. J Neurosci. 2011;31:16327–16335. DOI:10.1523/JNEUROSCI.3611-11.2011
  • Higashi H, Meno JR, Marwaha AS, et al. Hippocampal injury and neurobehavioral deficits following hyperglycemic cerebral ischemia: effect of theophylline and ZM 241385. J Neurosurg. 2002;96:117–126. DOI:10.3171/jns.2002.96.1.0117
  • Yang ZJ, Wang B, Kwansa H, et al. Adenosine A2A receptor contributes to ischemic brain damage in newborn piglet. J Cereb Blood Flow Metab. 2013;33:1612–1620. DOI:10.1038/jcbfm.2013.117
  • Gui L, Duan W, Tian H, et al. Adenosine A2A receptor deficiency reduces striatal glutamate outflow and attenuates brain injury induced by transient focal cerebral ischemia in mice. Brain Res. 2009;1297:185–193. DOI:10.1016/J.BRAINRES.2009.08.050
  • Sehba FA, Flores R, Muller A, et al. Adenosine A2A receptors in early ischemic vascular injury after subarachnoid hemorrhage. J Neurosurg. 2010;113:826–834. DOI:10.3171/2009.9.JNS09802.Adenosine
  • Higdon J, Steward VJDWP. In: resveratrol. Micronutr. Inf. Center. Linus Pauling Institute, Oregon, United States. 2016.  [cited 2019 Jan 7]. Available from: http://lpi.oregonstate.edu/mic/dietary-factors/phytochemicals/resveratrol
  • Sajish M, Schimmel P. A human tRNA synthetase is a potent PARP1-activating effector target for resveratrol. Nature. 2015;519:370–373. DOi:10.1038/nature14028
  • Bonsack F, Alleyne CH, Sukumari-Ramesh S. Resveratrol attenuates neurodegeneration and improves neurological outcomes after intracerebral hemorrhage in mice. Front Cell Neurosci. 2017;11:1–9. DOI:10.3389/fncel.2017.00228
  • Dragone T, Cianciulli A, Calvello R, et al. Resveratrol counteracts lipopolysaccharide-mediated microglial inflammation by modulating a SOCS-1 dependent signaling pathway. Toxicol Vitr. 2014;28:1126–1135. DOI:10.3389/fncel.2017.00228
  • Kumar V, Pandey A, Jahan S, et al. Differential responses of trans-resveratrol on proliferation of neural progenitor cells and aged rat hippocampal neurogenesis. Sci Rep. 2016;6:28142. DOI:10.1038/srep28142
  • Bellaver B, Bobermin LD, Souza DG, et al. Signaling mechanisms underlying the glioprotective effects of resveratrol against mitochondrial dysfunction. Biochim Biophys Acta - Mol Basis Dis. 2016;1862:1827–1838. DOI:10.1016/j.bbadis.2016.06.018
  • Li D, Liu N, Zhao L, et al. Protective effect of resveratrol against nigrostriatal pathway injury in striatum via JNK pathway. Brain Res. 2017;1654:1–8. DOI:10.1016/j.brainres.2016.10.013
  • Zhou XM, Zhou ML, Zhang XS, et al. Resveratrol prevents neuronal apoptosis in an early brain injury model. J Surg Res. 2014;189:159–165. DOI:10.1016/j.jss.2014.01.062
  • Patel KR, Scott E, Brown VA, et al. Clinical trials of resveratrol. Ann N Y Acad Sci. 2011;1215:161–169. DOI:10.1111/j.1749-6632.2010.05853.x
  • Walle T, Hsieh F, DeLegge MH, et al. High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab Dispos. 2004;32:1377–1382. DOI:10.1124/dmd.104.000885
  • Goldberg DM, Yan J, Soleas GJ. Absorption of three wine-related polyphenols in three different matrices by healthy subjects. Clin Biochem. 2003;36:79–87. DOI:10.1016/S0009-9120(02)00397-1
  • Johnson JJ, Nihal M, Siddiqui IA, et al. Enhancing the bioavailability of resveratrol by combining it with piperine. Mol Nutr Food Res. 2011;55:1169–1176. DOI:10.1002/mnfr.201100117
  • Mattarei A, Azzolini M, La Spina M, et al. Amino acid carbamates as prodrugs of resveratrol. Sci Rep. 2015;5:1–11. DOI:10.1038/srep15216
  • Peñalva R, Morales J, González-Navarro CJ, et al. Increased oral bioavailability of resveratrol by its encapsulation in casein nanoparticles. Int J Mol Sci. 2018;19. DOI:10.3390/ijms19092816
  • Singh N, Bansal Y, Bhandari R, et al. Resveratrol protects against ICV collagenase-induced neurobehavioral and biochemical deficits. J Inflamm. 2017;14:14. DOI:10.1186/s12950-017-0158-3
  • Razali N, Agarwal R, Agarwal P, et al. Role of adenosine receptors in resveratrol-induced intraocular pressure lowering in rats with steroid-induced ocular hypertension. Clin Exp Ophthalmol. 2015;43:54–66. DOI:10.1111/ceo.12375
  • Schiffmann SN, Fisone G, Moresco R, et al. Adenosine A2A receptors and basal ganglia physiology. Prog Neurobiol. 2007;83:277–292. DOi:10.1016/j.pneurobio.2007.05.001
  • Ferre S, Quiroz C, Woods AS, et al. An update on adenosine A2A-dopamine D2 receptor interactions: implications for the function of G protein-coupled receptors. Curr Pharm Des. 2008;14:1468–1474. DOI:10.2174/138161208784480108
  • Zhai W, Chen D, Shen H, et al. A1 adenosine receptor attenuates intracerebral hemorrhage-induced secondary brain injury in rats by activating the P38-MAPKAP2-Hsp27 pathway. Mol Brain. 2016;9:66. DOI:10.1186/s13041-016-0247-x
  • National Research Council. Guidelines for the care and use of mammals in neuroscience and behavioral research. Washington, DC: The National Academies Press. 2003. DOI:10.17226/10732
  • Charan J, Kantharia N. How to calculate sample size in animal studies? J Pharmacol Pharmacother. 2013;4:303. DOI:10.4103/0976-500X.119726
  • Paxinos G, Watson C. The rat brain in stereotaxic coordinates. Vol. 439. Acad Press Inc; 2007. DOI:10.1016/0166-2236(87)90017-8
  • Lamprea MR, Cardenas FP, Setem J, et al. Thigmotactic responses in an open-field. Braz J Med Biol Res. 2008;41:135–140. DOI:10.1590/S0100-879X2008000200010
  • Doeppner TR, Kaltwasser B, Bähr M, et al. Effects of neural progenitor cells on post-stroke neurological impairment—a detailed and comprehensive analysis of behavioral tests. Front Cell Neurosci. 2014;8:1–15. DOI:10.3389/fncel.2014.00338
  • Deacon RMJ. Measuring motor coordination in mice. J Vis Exp. 2013;1–8. DOI:10.3791/2609
  • Spasov AA, Iezhitsa IN, Kharitonova MV, et al. Depression-like and anxiety-related behaviour of rats fed with magnesium-deficient diet. Zh Vyssh Nerv Deiat Im I P Pavlova. 2008;58:476–485.
  • Iezhitsa IN, Spasov AA, Kharitonova MV, et al. Effect of magnesium chloride on psychomotor activity, emotional status, and acute behavioural responses to clonidine, d -amphetamine, arecoline, nicotine, apomorphine, and L-5-hydroxytryptophan. Nutr Neurosci. 2011;14:10–24. DOI:10.1179/174313211X12966635733277
  • Neuroscience Physiology Research Equipment Psychological Assessment Stoelting Co. [cited 2019 Jan 7]. Available from: https://www.stoeltingco.com/anymaze/video-tracking.html
  • Med Associates Inc. Single Lane Rota-Rod for Rat. Med Associates Inc. [cited 2019 Jan 7]. Available from: https://www.med-associates.com/product/env-574r/
  • Instruction manual. Instr Man GSM Grip Strength M Cat No 47200; 2011. p. 1–194. DOI:10.1016/j.colsurfa.2005.08.013
  • Niu J, Hu R. Role of flunarizine hydrochloride in secondary brain injury following intracerebral hemorrhage in rats. Int J Immunopathol Pharmacol. 2017;30:413-419. DOI:10.1177/0394632017742224
  • Park J, Youl J, Choi S, et al. Thermo-sensitive assembly of the biomaterial REP reduces hematoma volume following collagenase-induced intracerebral hemorrhage in rats. Nanomedicine Nanotechnology, Biol Med. 2017;13:1853–1862. DOI:10.1016/j.nano.2017.04.001
  • Gage GJ, Kipke DR, Shain W. Whole animal perfusion fixation for rodents. J Vis Exp. 2012;1–9. DOI:10.3791/3564
  • Altumbabic M, Peeling J, Del Bigio MR. Intracerebral hemorrhage in the rat: effects of hematoma aspiration. Stroke. 1998;29:1917-1923. Available from: http://stroke.ahajournals.org/content/strokeaha/29/9/1917.full.pdf
  • Rosenberg GA, Mun-bryce S, Wesley M, et al. Collagenase-induced intracerebral hemorrhage in rats. Stroke 1990;21:801-807.
  • Huang L-C. Collagenase-induced rat intra-striatal hemorrhage mimicking severe human intra-striatal hemorrhage. Chin J Physiol. 2017;60:259–266. DOI:10.4077/cjp.2017.baf478
  • Borroto-escuela DO, Mora D La PM, Manger P. Brain dopamine transmission in health and parkinson ’ s disease : modulation of synaptic transmission and plasticity through volume transmission and dopamine heteroreceptors. Front Synaptic Neurosci. 2018;10:1–24. DOI:10.3389/fnsyn.2018.00020
  • Nazario LR, Silva RS, Bonan CD. Targeting adenosine signaling in parkinson ’ s disease : from pharmacological to non-pharmacological approaches. Front Neurosci. 2017;11:658. DOI:10.3389/fnins.2017.00658
  • Sichardt K, Nieber K. Adenosine A 1 receptor : functional receptor-receptor interactions in the brain. Purinergic Signal. 2007;3:285–298. DOI:10.1007/s11302-007-9065-z
  • Benarroch EE. Adenosine and its receptors: multiple modulatory functions and potential therapeutic targets for neurologic disease. Neurology. 2008;70:231–236. DOI:10.1212/01.wnl.0000297939.18236.ec
  • Sunderland A, Tinson D, Bradley L, et al. Arm function after stroke. An evaluation of grip strength as a measure of recovery and a prognostic indicator. J Neurol Neurosurg Psychiatry. 1989;52:1267–1272. DOI:10.1136/jnnp.52.11.1267
  • Ekstrand E, Lexell J, Brogårdh C. Grip strength is a representative measure of muscle weakness in the upper extremity after stroke. Top Stroke Rehabil. 2016;23:400–405. DOI:10.1080/10749357.2016.1168591
  • Pankratov Y, Lalo U, Verkhratsky A, et al. Vesicular release of ATP at central synapses. Pflügers Arch Eur J Physiol. 2006;452:589–597. DOI:10.1007/s00424-006-0061-x
  • Chung YC, Bok E, Huh SH, et al. Cannabinoid receptor type 1 protects nigrostriatal dopaminergic neurons against mptp neurotoxicity by inhibiting microglial activation. J Immunol. 2011;187:6508-6517. DOI:10.4049/jimmunol.1102435
  • Zou S, Kumar U. Cannabinoid receptors and the endocannabinoid system : signaling and function in the central nervous system. Int J Mol Sci. 2018;19:833. DOI:10.3390/ijms19030833
  • Martire A, Tebano MT, Chiodi V, et al. Pre-synaptic adenosine A2A receptors control cannabinoid CB 1 receptor-mediated inhibition of striatal glutamatergic neurotransmission. J Neurochem. 2011;116:273–280.DOI:10.1111/j.1471-4159.2010.07101.x
  • Sousa VC, Assaife-Lopes N, Ribeiro JA, et al. Regulation of hippocampal cannabinoid CB1receptor actions by adenosine A1receptors and chronic caffeine administration: implications for the effects of Δ 9-tetrahydrocannabinol on spatial memory. Neuropsychopharmacology. 2011;36:472–487. DOI:10.1038/npp.2010.179
  • DeSanty K, Dar MS. Cannabinoid-induced motor incoordination through the cerebellar CB1 receptor in mice. Pharmacol Biochem Behav. 2001;69:251–259. DOI:10.1016/S0091-3057(01)00539-1
  • Vlachou S, Stamatopoulou F, Nomikos GG, et al. Enhancement of endocannabinoid neurotransmission through CB 1 cannabinoid receptors counteracts the reinforcing and psychostimulant effects of cocaine. Int J Neuropsychopharmacol. 2008;11:905–923. DOI:10.1017/S1461145708008717
  • Vizi ES, Fekete A, Karoly R, et al. Non-synaptic receptors and transporters involved in brain functions and targets of drug treatment. Br J Pharmacol. 2010;160:785–809. DOI:10.1111/j.1476-5381.2009.00624.x
  • Cunha RA. Neuroprotection by adenosine in the brain: from A1receptor activation to A2Areceptor blockade. Purinergic Signal. 2005;1:111–134. DOI:10.1007/s11302-005-0649-1
  • Park S, Ahmad F, Philp A, et al. Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell. 2012;148:421–433. DOI:10.1016/j.cell.2012.01.017.Park
  • Duncan RS, Goad DL, Grillo MA, et al. molecules control of intracellular calcium signaling as a neuroprotective strategy. Molecules. 2010;15:1168–1195. DOI:10.3390/molecules15031168
  • Blank T, Nijholt I, Teichert U, et al. The phosphoprotein DARPP-32 mediates cAMP-dependent potentiation of striatal N-methyl-D-aspartate responses. PNAS. 1997;94:14859-14864.
  • Hwang BY, Appelboom G, Ayer A, et al. Advances in neuroprotective strategies: potential therapies for intracerebral hemorrhage. Cerebrovasc Dis. 2011;31:211–222. DOI:10.1159/000321870
  • Ohnishi M, Monda A, Takemoto R, et al. Sesamin supresses activation of microglia and P44/42 MAPK pathway, which confers neuroprotection in rat intracerebral hemorrhage. Neuroscience. 2013;232:45–52. DOI:10.1016/j.neuroscience.2012.11.057
  • Mohar DS, Malik S. The sirtuin system: the holy grail of resveratrol? J Clin Exp Cardiolog. 2012;3:216.
  • Calleri E, Pochetti G, Dossouc KSS, et al. Resveratrol and its metabolites bind to PPARs. Chembiochem. 2014;15:1154-1160.
  • Zhou Y, Wang S, Li Y, et al. SIRT1/PGC-1α signaling promotes mitochondrial functional recovery and reduces apoptosis after intracerebral hemorrhage in rats. Front Mol Neurosci. 2018;10:1–14. DOI:10.3389/fnmol.2017.00443
  • Chang CF, Wan J, Li Q, et al. Alternative activation-skewed microglia/macrophages promote hematoma resolution in experimental intracerebral hemorrhage. Neurobiol Dis. 2017;103:54–69. DOI:10.1016/j.nbd.2017.03.016
  • Sakata Y, Zhuang H, Kwansa H, et al. Resveratrol protects against experimental stroke: putative neuroprotective role of heme oxygenase 1. Exp Neurol. 2010;224:325–329. DOI:10.1016/j.expneurol.2010.03.032
  • Ohata H, Cao S, Koehler RC. Contribution of adenosine A 2A and A 2B receptors and heme oxygenase to AMPA-induced dilation of pial arterioles in rats. Am J Physiol Regul Integr Comp Physiol. 2006;291:R728-735.
  • Mracsko E, Veltkamp R. Neuroinflammation after intracerebral hemorrhage. Front Cell Neurosci. 2014;8:1–13. DOI:10.3389/fncel.2014.00388
  • Baur JA. Resveratrol, sirtuins, and the promise of a DR mimetic. Mech Ageing Dev. 2010;131:261–269. DOI:10.1016/j.mad.2010.02.007
  • Giménez-Llort L, Fernández-Teruel A, Escorihuela RM, et al. Mice lacking the adenosine A 1 receptor are anxious and aggressive, but are normal learners with reduced muscle strength and survival rate. Eur J Neurosci. 2002;16:547–550.DOI:10.1046/j.1460-9568.2002.02122.x
  • Gomez G, Sitkovsky MV. Differential requirement for A2a and A3 adenosine receptors for the protective effect of inosine in vivo. Blood. 2003;102:4472-4478.DOI:10.1182/blood-2002-11-3624

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