Neuroprotective effect of poly(lactic‑co‑glycolic acid) nanoparticle‑bound brain‑derived neurotrophic factor in a permanent middle cerebral artery occlusion model of ischemia in rats

• Autorzy: Kamarudin S.N. , Iezhitsa I. , Tripathy M. , Alyautdin R. , Ismail N.M.
• Języki publikacji: EN

Abstrakty

EN

Poly (lactide‑co‑glycolide) (PLGA) nanoparticles (NPs) are biodegradable carriers that participate in the transport of neuroprotective drugs across the blood brain barrier (BBB). Targeted brain‑derived neurotrophic factor (BDNF) delivery across the BBB could provide neuroprotection in brain injury. We tested the neuroprotective effect of PLGA nanoparticle‑bound BDNF in a permanent middle cerebral artery occlusion (pMCAO) model of ischemia in rats. Sprague‑Dawley rats were subjected to pMCAO. Four hours after pMCAO, two groups were intravenously treated with BDNF and NP‑BDNF, respectively. Functional outcome was assessed at 2 and 24 h after pMCAO, using the modified neurologic severity score (mNSS) and rotarod performance tests. Following functional assessments, rats were euthanized blood was taken to assess levels of the neurobiomarkers neuron‑specific enolase and S100 calcium‑binding protein β (S100β), and the brain was evaluated to measure the infarct volume. The NP‑BDNF‑treated group showed significant improvement in mNSS compared with pMCAO and BDNF‑treated groups and showed improved rotarod performance. The infarct volume in rats treated with NP‑BDNFs was also significantly smaller. These results were further corroborated by correlating differences in estimated NSE and S100β. NP‑BDNFs exhibit a significant neuroprotective effect in the pMCAO model of ischemia in rats.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2020
• Tom: 80
• Numer: 1
• Opis fizyczny: p.1-18,fig.,ref.

Twórcy

autor

Kamarudin S.N.

• Centre for Neuroscience Research, Faculty of Medicine, Universiti Teknologi MARA, Sungai Buloh Campus, Sungai Buloh, Selangor, Malaysia

autor

Iezhitsa I.

• Centre for Neuroscience Research, Faculty of Medicine, Universiti Teknologi MARA, Sungai Buloh Campus, Sungai Buloh, Selangor, Malaysia
• Laboratory and Forensic Medicine (I‑PPerForM), Institute for Pathology,Universiti Teknologi MARA, Sungai Buloh Campus, Sungai Buloh, Selangor, Malaysia
• Research Centre for Innovative Medicines, Volgograd State Medical University, Volgograd, Russian Federation

autor

Tripathy M.

• Centre for Molecular Pharmaceutics and Advanced Therapeutics, Adichunchanagiri College of Pharmacy, Adichunchanagiri University (ACU), B G Nagar, Karnattaka, India

autor

Alyautdin R.

• Scientific Centre for Expert Evaluation of Medicinal Products, Ministry of Health Russian Federation, Moscow, Russian Federation

autor

Ismail N.M.

• Faculty of Medicine, IMU Clinical School, International Medical University, Seremban, Malaysia

Bibliografia

• Albers GW, Bogousslavsky J, Bozik MA, Brass LM, Broderick JP, Fisher M, Goldstein LB, Salazar‑Grueso E, Zivin JA (2001) Recommendations for clinical trial evaluation of acute stroke therapies. Stroke 32: 1598–1606.
• Aziz ZA, Lee YY, Ngah BA, Sidek NN, Looi I, Hanip MR, Basri HB (2015) Acute stroke registry Malaysia, 2010–2014: results from the National Neurology Registry. J Stroke Cerebrovasc Dis 24: 2701–2709.
• Baron JC, Yamauchi H, Fujioka M, Endres M (2014) Selective neuronal loss in ischemic stroke and cerebrovascular disease. J Cereb Blood Flow Metab 34: 2–18.
• Barone FC, Feuerstein GZ (1999) Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 19: 819–834.
• Baydyuk M, Xu B (2014) BDNF signaling and survival of striatal neurons. Front Cell Neurosci 8: 254.
• Belayev L, Busto R, Zhao W, Fernandez G, Ginsberg MD (1999) Middle cerebral artery occlusion in the mouse by intraluminal suture coated with poly‑L‑lysine: neurological and histological validation. Brain Res 833: 181–190.
• Betz AL, Firth JA, Goldstein GW (1980) Polarity of the blood‑brain barrier: distribution of enzymes between the luminal and antiluminal mem‑ branes of brain capillary endothelial cells. Brain Res 192: 17–28.
• Betz AL, Goldstein GW (1978) Polarity of the blood‑brain barrier: neutral amino acid transport into isolated brain capillaries. Science 202: 225–227.
• Bharosay A, Bharosay VV, Saxena K, Varma M (2018) Role of brain biomarker in predicting clinical outcome in hypertensive cerebrovascular ischemic stroke. Indian J Clin Biochem 2017: 1–6.
• Boltze J, Schmidt UR, Reich DM, Kranz A, Reymann KG, Strassburger  M, Lobsien D, Wagner DC, Förschler A, Schäbitz WR (2012) Determination of the therapeutic time window for human umbilical cord blood mononuclear cell transplantation following experimental stroke in rats. Cell Transplant 21: 1199–1211.
• Çakmak VA, Gündüz A, Karaca Y, Alioğlu Z, Menteşe A, Topbaş M (2014) Diagnostic significance of ischemia‑modified albumin, S100b, and neuron‑specific enolase in acute ischemic stroke. Akademik Acil Tip Olgu Sunumlari Dergisi 13: 112–117.
• Carmichael ST (2005) Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2: 396–409.
• Casmiro M, Maitan S, De Pasquale F, Cova V, Scarpa E, Vignatelli L, NSE Study Group (2005) Cerebrospinal fluid and serum neuron-specific enolase concentrations in a normal population. Eur J Neuro 12: 369–374.
• Çeltik C, Acunaş B, Öner N, Pala Ö (2004) Neuron‑specific enolase as a marker of the severity and outcome of hypoxic ischemic encephalopathy. Brain Dev 26: 398–402.
• Chabok SY, Moghadam AD, Saneei Z, Amlashi FG, Leili EK, Amiri ZM (2012) Neuron‑specific enolase and S100BB as outcome predictors in severe diffuse axonal injury. J Trauma Acute Care Surg 72: 1654–1657.
• Chan DK, Levi C, Cordato D, O’Rourke F, Chen J, Redmond H, Xu YH, Middleton S, Pollack M, Hankey GJ (2014) Health service management study for stroke: a randomized controlled trial to evaluate two models of stroke care. Int J Stroke 9: 400–405.
• Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4: 299–309.
• Chao OY, Pum ME, Li JS, Huston JP (2012) The grid‑walking test: assessment of sensorimotor deficits after moderate or severe dopamine depletion by 6‑hydroxydopamine lesions in the dorsal striatum and medial fore‑ brain bundle. Neuroscience 202: 318–325.
• Chen A, Lin Z, Lan L, Xie G, Huang J, Lin J, Peng J, Tao J, Chen L (2012) Electroacupuncture at the Quchi and Zusanli acupoints exerts neuroprotec‑ tive role in cerebral ischemia‑reperfusion injured rats via activation of the PI3K/Akt pathway. Int J Mol Med 30: 791–796.
• Chen A, Xiong LJ, Tong Y, Mao M (2013a) Neuroprotective effect of brainde‑ rived neurotrophic factor mediated by autophagy through the PI3K/Akt/ mTOR pathway. Mol Med Rep 8: 1011–1016.
• Chen AI, Xiong LJ, Tong YU, Mao M (2013b) The neuroprotective roles of BDNF in hypoxic ischemic brain injury. Biomed Rep 1: 167–176.
• Chen J, Sanberg PR, Li Y, Wang L, Lu M, Willing AE, Sanchez‑Ramos J, Chopp M (2001) Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke 32: 2682–2688.
• Chen J, Zacharek A, Zhang C, Jiang H, Li Y, Roberts C, Lu  M, Kapke A, Chopp  M (2005) Endothelial nitric oxide synthase regulates brainde‑ rived neurotrophic factor expression and neurogenesis after stroke in mice. J Neurosci 25: 2366–2375.
• Chen J, Zhang C, Jiang H, Li Y, Zhang  L, Robin A, Katakowski  M, Lu  M, Chopp M (2005) Atorvastatin induction of VEGF and BDNF promotes brain plasticity after stroke in mice. J Cereb Blood Flow Metab 25: 281–290.
• Chiamulera C, Terron A, Reggiani A, Cristofori P (1993) Qualitative and quantitative analysis of the progressive cerebral damage after middle cerebral artery occlusion in mice. Brain Res 606: 251–258.
• Cunningham RT, Young IS, Winder J, O’Kane MJ, McKinstry S, Johnston CF, Dolan OM, Hawkins SA, Buchanan KD (1991) Serum neurone specific enolase (NSE) levels as an indicator of neuronal damage in patients with cerebral infarction. Eur J Clin Invest 21: 497–500.
• Ejaz S, Williamson DJ, Ahmed T, Sitnikov S, Hong YT, Sawiak SJ, Fryer TD, Aigbirhio FI, Baron JC (2013) Characterizing infarction and selective neuronal loss following temporary focal cerebral ischemia in the rat: a multi‑modality imaging study. Neurobiol Dis 51: 120–132.
• Elting JW, de Jager AE, Teelken AW, Schaaf MJ, Maurits NM, van der Naalt J, Sibinga CT, Sulter GA, De Keyser J (2000) Comparison of serum S‑100 protein levels following stroke and traumatic brain injury. J Neurol Sci 181: 104–110.
• Freret T, Bouet  V, Leconte C, Roussel S, Chazalviel  L, Divoux D, Schumann‑Bard P, Boulouard M (2009) Behavioral deficits after distal focal cerebral ischemia in mice: Usefulness of adhesive removal test. Behav Neurosci 123: 224–230.
• Fulle S, Pietrangelo T, Mariggio MA, Lorenzon P, Racanicchi L, Mozrzymas J, Guarnieri S, Zucconi‑Grassi G, Fano G (2000) Calcium and fos involvement in brain‑derived Ca2+‑binding protein (S100)‑dependent apoptosis in rat phaeochromocytoma cells. Exp Physiol 85: 243–253.
• Ga D, Fisher M, Macleod M, Davis SM (2008) Stroke. Lancet 371: 1612–1623.
• Garcia JH, Lassen NA, Weiller C, Sperling B, Nakagawara J (1996) Ischemic stroke and incomplete infarction. Stroke 27: 761–765.
• Garcia JH, Liu KF, Ye ZR, Gutierrez JA (1997) Incomplete infarct and delayed neuronal death after transient middle cerebral artery occlusion in rats. Stroke 28: 2303–2310.
• Garcia JH, Wagner S, Liu KF, Hu XJ (1995) Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats: statistical validation. Stroke 26: 627–635.
• Gelderblom  M, Daehn T, Schattling B, Ludewig P, Bernreuther C, Arunachalam P, Matschke J, Glatzel M, Gerloff C, Friese MA, Magnus T (2013) Plasma levels of neuron specific enolase quantify the extent of neuronal injury in murine models of ischemic stroke and multiple scle‑ rosis. Neurobiol Dis 59: 177–182.
• Gelperina S, Maksimenko O, Khalansky A, Vanchugova  L, Shipulo E, Abbasova K, Berdiev R, Wohlfart S, Chepurnova N, Kreuter J (2010) Drug delivery to the brain using surfactant‑coated poly (lactide‑co‑glycolide) nanoparticles: influence of the formulation parameters. Eur J Pharm Biopharm 74: 157–163.
• Goldlust EJ, Paczynski RP, He YY, Hsu CY, Goldberg MP (1996) Automated measurement of infarct size with scanned images of triphenyltetrazoli‑ um chloride‑stained rat brains. Stroke 27: 1657–1662.
• Goldstein GW, Betz AL (1986) The blood‑brain barrier. Sci Am 255: 74–83.
• Guo C, Zhu Y, Weng Y, Wang S, Guan Y, Wei G, Yin Y, Xi M, Wen A (2014) Therapeutic time window and underlying therapeutic mechanism of breviscapine injection against cerebral ischemia/reperfusion injury in rats. J Ethnopharmacol 151: 660–666.
• Guo ZV, Li N, Huber D, Ophir E, Gutnisky D, Ting JT, Feng G, Svoboda K (2014) Flow of cortical activity underlying a tactile decision in mice. Neuron 81: 179–194.
• Gupta S, Sharma U, Jagannathan NR, Gupta YK (2017) Neuroprotective effect of lercanidipine in middle cerebral artery occlusion model of stroke in rats. Exp Neurol 288: 25–37.
• Haley MJ, Lawrence CB (2017) The blood–brain barrier after stroke: struc‑ tural studies and the role of transcytotic vesicles. J Cereb Blood Flow Metab 37: 456–470.
• Han BH, D’Costa A, Back SA, Parsadanian M, Patel S, Shah AR, Gidday JM, Srinivasan A, Deshmukh M, Holtzman DM (2000) BDNF blocks caspase‑3 activation in neonatal hypoxia‑ischemia. Neurobiol Dis 7: 38–53.
• Han JC, Thurm A, Williams CG, Joseph LA, Zein WM, Brooks BP, Butman JA, Brady SM, Fuhr SR, Hicks MD, Huey AE (2013) Association of brainde‑ rived neurotrophic factor (BDNF) haploinsufficiency with lower adaptive behaviour and reduced cognitive functioning in WAGR/11p13 deletion syndrome. Cortex 49: 2700–2710.
• Hårdemark HG, Ericsson N, Kotwica Z, Rundström G, Mendel‑Hartvig I, Olsson Y, Påhlman S, Persson L (1989) S‑100 protein and neuron‑specific enolase in CSF after experimental traumatic or focal ischemic brain damage. J Neurosurgery 71: 727–731.
• Hatfield RH, Mendelow AD, Perry RH, Alvarezs LM, Modha P (1991) Triphenyltetrazolium chloride (TTC) as a  marker for ischaemic changes in rat brain following permanent middle cerebral artery occlusion Neuropathol Appl Neurobiol 17: 61–67.
• Hernandez TD, Schallert T (1988) Seizures and recovery from experimental brain damage. Exp Neurol 102: 318–324.
• Horn M, Seger F, Schlote W (1995) Neuron‑specific enolase in gerbil brain and serum after transient cerebral ischemia. Stroke 26: 290–297.
• Hu J, Ferreira A, Van Eldik LJ (1997) S100β induces neuronal cell death through nitric oxide release from astrocytes J Neurochem 69: 2294–2301.
• Jauch EC, Barreto AD, Broderick JP, Char DM, Cucchiara BL, Devlin TG, Haddock AJ, Hicks WJ, Hiestand BC, Jickling GC, June J (2017) Biomarkers of acute stroke etiology (BASE) study methodology. Transl Stroke Res 8: 424–428.
• Jiang Y, Wei N, Zhu J, Lu T, Chen Z, Xu G, Liu X (2010) Effects of brain‑derived neurotrophic factor on local inflammation in experimental stroke of rat. Mediators Inflamm 2010: 372423.
• Joshi CN, Jain SK, Murthy PS (2004) An optimized triphenyltetrazolium chloride method for identification of cerebral infarcts. Brain Res Brain Res Protoc 13: 11–17.
• Kanemitsu H, Nakagomi T, Tamura A, Tsuchiya T, Kono G, Sano K (2002) Differences in the extent of primary ischemic damage between middle cerebral artery coagulation and intraluminal occlusion models. J Cereb Blood Flow Metab 22: 1196–1204.
• Kim JY, Ho H, Kim N, Liu J, Tu CL, Yenari MA, Chang W (2014) Calcium-sensing receptor (CaSR) as a novel target for ischemic neuroprotection. Ann Clin Transl Neurol 1: 851–866.
• Koizumi JY, Yoshida Y, Nakazawa T, Ooneda G (1986) Experimental studies of ischemic brain edema. Jpn J Stroke 8: 1–8.
• Koppal T, Lam AG, Guo L, Van Eldik LJ (2001) S100B proteins that lack one or both cysteine residues can induce inflammatory responses in astrocytes and microglia. Neurochem Int 39: 401–407.
• Krueger  M, Härtig  W, Reichenbach A, Bechmann I, Michalski D (2013) Blood‑brain barrier breakdown after embolic stroke in rats occurs with‑ out ultrastructural evidence for disrupting tight junctions. PLoS One 8: e56419.
• Kulkarni SA, Feng SS (2011) Effects of surface modification on delivery efficiency of biodegradable nanoparticles across the blood–brain barrier. Nanomedicine 6: 377–394.
• Kume T, Kouchiyama H, Kaneko S, Maeda T, Kaneko S, Akaike A, Shimohama S, Kihara T, Kimura J, Wada K, Koizumi S (1997) BDNF prevents NO mediated glutamate cytotoxicity in cultured cortical neurons. Brain Res 756: 200–204.
• Lee S, Lee M, Hong Y, Won J, Lee Y, Kang SG, Chang KT, Hong Y (2014) Middle cerebral artery occlusion methods in rat versus mouse models of transient focal cerebral ischemic stroke. Neural Regen Res 9: 757.
• Lee S, Shin J, Lee M, Hong Y, Lee SK, Lee Y, Lkhagvasuren T, Kim DW, Yang YA, Chang KT, Hong Y (2012) Melatonin combined with exercise cannot alleviate cerebral injury in a rat model of focal cerebral ischemia/reper‑ fusion injury. Neural Regen Res 7: 993–999.
• Li K, Jia J, Wang Z, Zhang S (2015) Elevated serum levels of NSE and S‑100β correlate with increased risk of acute cerebral infarction in Asian populations. Med Sci Monit 21: 1879–1888.
• Li Y, Chopp M, Jiang N, Yao F, Zaloga C (1995) Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 15: 389–397.
• Li YI, Chen J, Zhang CL, Wang  L, Lu D, Katakowski  M, Gao Q, Shen LH, Zhang J, Lu M, Chopp M (2005) Gliosis and brain remodeling after treat‑ ment of stroke in rats with marrow stromal cells. Glia 49: 407–417.
• Liu F, Schafer DP, McCullough LD (2009) TTC, fluoro‑Jade B and NeuN staining confirm evolving phases of infarction induced by middle cerebral artery occlusion. J Neurosci Methods 179: 1–8.
• Liu S, Zhen G, Meloni BP, Campbell K, Winn HR (2009) Rodent stroke model guidelines for preclinical stroke trials. J Exp Stroke Transl Med 2: 2–27.
• Lo EH, Dalkara T, Moskowitz MA (2003) Neurological diseases: Mecha‑ nisms, challenges and opportunities in stroke.  Nat Rev Neurosci  4: 399–415.
• Lu B, Nagappan G, Guan X, Nathan PJ, Wren P (2013) BDNF‑based synaptic repair as a disease‑modifying strategy for neurodegenerative diseases. Nat Rev Neurosci 14: 401–416.
• Lu B, Nagappan G, Lu Y (2014) BDNF and synaptic plasticity, cognitive function, and dysfunction. Handb Exp Pharmacol 220: 223–250.
• Mabe H, Suzuki S, Mase M, Umemura A, Nagai H (1991) Serum neuron‑specific enolase levels after subarachnoid hemorrhage. Surg Neurol 36: 170–174.
• Martens P, Raabe A, Johnsson P (1998). Serum S‑100 and neuron‑specific enolase for prediction of regaining consciousness after global cerebral ischemia. Stroke 29: 2363–2366.
• Matsui T, Mori T, Tateishi N, Kagamiishi Y, Satoh S, Katsube N, Morikawa  E, Morimoto T, Ikuta F, Asano T (2002) Astrocytic activation and delayed infarct expansion after permanent focal ischemia in rats. Part I: enhanced astrocytic synthesis of S‑100β in the periinfarct area precedes delayed infarct expansion. J Cereb Blood Flow Metab 22: 711–722.
• Meng L, Liu B, Ji R, Jiang X, Yan X, Xin Y (2019) Targeting the BDNF/TrkB pathway for the treatment of tumors Oncol Lett 17: 2031–2039.
• Mergenthaler P, Meisel A (2012) Do stroke models model stroke? Dis Model Mech 5: 718–725. Missler U, Wiesmann  M, Friedrich C, Kaps  M (1997) S‑100 protein and neuron‑specific enolase concentrations in blood as indicators of infarction volume and prognosis in acute ischemic stroke. Stroke 28: 1956–1960.
• Moghimi SM, Hunter AC (2000) Poloxamers and poloxamines in nanoparticle engineering and experimental medicine. Trends Biotechnol 18: 412–420.
• Mori T, Koyama N, Arendash GW, Horikoshi-Sakuraba Y, Tan J, Town T (2010) Overexpression of human S100B exacerbates cerebral amyloidosis and gliosis in the Tg2576 mouse model of Alzheimer’s disease. Glia 58: 300–314.
• Mozafari MR, Pardakhty A, Azarmi S, Jazayeri JA, Nokhodchi A, Omri A (2009) Role of nanocarrier systems in cancer nanotherapy. J Liposome Res 19: 310–321.
• Murer MG, Yan Q, Raisman‑Vozari R (2001) Brain‑derived neurotrophic factor in the control human brain, and in Alzheimer’s disease and Parkinson’s disease. Prog Neurobiol 63: 71–124. Nagahara AH, Tuszynski MH (2011) Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nat Rev Drug Discov 10: 209–219.
• Nahirney PC, Reeson P, Brown CE (2016) Ultrastructural analysis of blood‑brain barrier breakdown in the periinfarct zone in young adult and aged mice. J Cereb Blood Flow Metab 36: 413–425.
• Nash DL, Bellolio MF, Stead LG (2008) S100 as a marker of acute brain ischemia: a systematic review. Neurocrit Care 8: 301–307.
• Ohira K, Hayashi M (2009) A new aspect of the TrkB signaling pathway in neural plasticity. Curr Neuropharmacol 7: 276–285.
• Olivecrona Z, Bobinski L, Koskinen LO (2015) Association of ICP, CPP, CT findings and S‑100B and NSE in severe traumatic head injury. Prognostic value of the biomarkers. Brain Inj 29: 446–454.
• Oron A, Oron U, Chen J, Eilam A, Zhang C, Sadeh M, Lampl Y, Streeter J, DeTaboada L, Chopp M (2006) Low‑level laser therapy applied transcra‑ nially to rats after induction of stroke significantly reduces long‑term neurological deficits. Stroke 37: 2620–2624.
• Park HS, Han KH, Shin JA, Park JH, Song KY, Kim DH (2014) The neuroprotective effects of carnosine in early stage of focal ischemia rodent model. J Korean Neurosurg Soc 55: 125–130.
• Park JS, Shin JA, Jung JS, Hyun JW, Van Le TK, Kim DH, Park EM, Kim HS (2012) Anti‑inflammatory mechanism of compound K in activated mi‑ croglia and its neuroprotective effect on experimental stroke in mice. J Pharmacol Exp Ther 341: 59–67.
• Patel RA, McMullen PW (2017) Neuroprotection in the treatment of acute ischemic stroke. Prog Cardiovasc Dis 59: 542–548.
• Persson L, Hårdemark HG, Gustafsson J, Rundström G, Mendel‑Hartvig IB, Esscher T, Påhlman S (1987) S‑100 protein and neuron‑specific enolase in cerebrospinal fluid and serum: markers of cell damage in human central nervous system. Stroke 18: 911–918.
• Poduslo JF, Curran GL (1996) Permeability at the blood‑brain and blood‑nerve barriers of the neurotrophic factors: NGF, CNTF, NT‑3, BDNF. Brain Res Mol Brain 36: 280–286.
• Popp A, Jaenisch N, Witte OW, Frahm C (2009) Identification of ischemic regions in a rat model of stroke. PloS One 4: e4764.
• Rogers DC, Campbell CA, Stretton JL, Mackay KB (1997a) Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat. Stroke 28: 2060–2066.
• Rogers DC, Fisher EM, Brown SD, Peters J, Hunter AJ, Martin JE (1997b) Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Ge‑ nome 8: 711–713.
• Sahu S, Nag DS, Swain A, Samaddar DP (2017) Biochemical changes in the injured brain. World J Biol Chem 8: 21. Sandoval KE, Witt KA (2008) Blood‑brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 32: 200–219.
• Saraiva C, Praça C, Ferreira R, Santos T, Ferreira  L, Bernardino  L (2016) Nanoparticle‑mediated brain drug delivery: overcoming blood‑brain barrier to treat neurodegenerative diseases. J Control Release 235: 34–47.
• Schaar KL, Brenneman MM, Savitz SI (2010) Functional assessments in the rodent stroke model. Exp Transl Stroke Med 2: 13. Schabitz WR, Berger C, Kollmar R, Seitz M, Tanay E, Kiessling M, Schwab S, Sommer C (2004) Effect of brain‑derived neurotrophic factor treatment and forced arm use on functional motor recovery after small cortical ischemia. Stroke 35: 992–997.
• Schäbitz WR, Schwab S, Spranger  M, Hacke  W (1997) Intraventricular brain‑derived neurotrophic factor reduces infarct size after focal cerebral ischemia in rats. J Cereb Blood Flow Metab 17: 500–506. Schabitz WR, Sommer C, Zoder W, Kiessling M, Schwaninger M, Schwab S (2000) Intravenous brain‑derived neurotrophic factor reduces infarct size and counterregulates Bax and Bcl‑2 expression after temporary fo‑ cal cerebral ischemia. Stroke 31: 2212–2216.
• Schwengel K, Namsolleck P, Lucht K, Clausen BH, Lambertsen KL, Valero‑Esquitino V, Thöne‑Reineke C, Müller S, Widdop RE, Denton KM, Horiuchi M (2016) Angiotensin AT2‑receptor stimulation improves survival and neurological outcome after experimental stroke in mice. J Mol Med 94: 957–966.
• Shukla PK, Khanna VK, Ali MM, Maurya R, Khan MY, Srimal RC (2006) Neuroprotective effect of Acorus calamus against middle cerebral artery occlusion–induced ischaemia in rat. Hum Exp Toxicol 25: 187–194.
• Skogseid IM, Nordby HK, Urdal P, Paus E, Lilleaas F (1992) Increased serum creatine kinase BB and neuron specific enolase following head injury indicates brain damage. Acta Neurochir 115: 106–111.
• Sorci G, Riuzzi F, Arcuri C, Tubaro C, Bianchi R, Giambanco I, Donato R (2013) S100B protein in tissue development, repair and regeneration. World J Biol Chem 4: 1–12.
• Steiner J, Bogerts B, Schroeter ML, Bernstein HG (2011) S100B protein in neurodegenerative disorders. Clin Chem Lab Med 49: 409–424.
• Stokum JA, Gerzanich V, Simard JM (2016) Molecular pathophysiology of cerebral edema. J Cereb Blood Flow Metab 36: 513–538.
• Sun J, Wang F, Li H, Zhang H, Jin J, Chen W, Pang M, Yu J, He Y, Liu J, Liu C (2015) Neuroprotective effect of sodium butyrate against cerebral ischemia/reperfusion injury in mice. Biomed Res Int 2015: 395895.
• Swanson RA, Morton MT, Tsao‑Wu G, Savalos RA, Davidson C, Sharp FR (1990) A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 10: 290–293.
• Taliyan R, Ramagiri S (2016) Delayed neuroprotection against cerebral ischemia reperfusion injury: putative role of BDNF and GSK‑3β. J Recept Signal Transduct Res 36: 402–410.
• Tanaka Y, Koizumi C, Marumo T, Omura T, Yoshida S (2007) Serum S100B is a useful surrogate marker for long‑term outcomes in photochemically‑induced thrombotic stroke rat models. Life Sci 81: 657–663.
• Tanaka Y, Marumo T, Omura T, Yoshida S (2007) Early increases in serum S100B are associated with cerebral hemorrhage in a rat model of focal cerebral ischemia. Brain Res 1227: 248–254.
• Tawk RG, Grewal SS, Heckman MG, Rawal B, Miller DA, Edmonston D, Ferguson JL, Navarro R, Ng  L, Brown BL, Meschia JF (2015) The relationship between serum neuron‑specific enolase levels and severity of bleeding and functional outcomes in patients with nontraumatic sub‑ arachnoid hemorrhage. Neurosurgery 78: 487–491.
• Thoenen H (1995) Neurotrophins and neuronal plasticity. Science 270: 593–598.
• Thorne RG, Frey WH (2001) Delivery of neurotrophic factors to the central nervous system. Clin Pharmacokinet 40: 907–946.
• Traudt CM, Juul SE (2013) Erythropoietin as a neuroprotectant for neonatal brain injury: animal models. Methods Mol Biol 982: 113–126.
• Tsivgoulis G, Katsanos AH, Alexandrov AV (2014) Reperfusion therapies of acute ischemic stroke: potentials and failures. Front Neurol 5: 215.
• Villa RF, Gorini A, Hoyer S (2009). Effect of ageing and ischemia on enzymatic activities linked to Krebs’ cycle, electron transfer chain, glutamate and aminoacids metabolism of free and intrasynaptic mitochondria of cerebral cortex. Neurochem Res 34: 2102.
• Wang CC, Chio CC, Chang CH, Kuo JR, Chang CP (2010) Beneficial effect of agmatine on brain apoptosis, astrogliosis, and edema after rat transient cerebral ischemia. BMC Pharmacol 10: 11. Williams AJ, Berti R, Dave JR, Elliot PJ, Adams J, Tortella FC (2004) Delayed treatment of ischemia/reperfusion brain injury: extended therapeutic window with the proteosome inhibitor MLN519. Stroke 35: 1186–1191.
• Wohlfart S, Khalansky AS, Gelperina S, Maksimenko O, Bernreuther C, Glatzel M, Kreuter J (2011) Efficient chemotherapy of rat glioblastoma using doxorubicin‑loaded PLGA nanoparticles with different stabilizers. PloS One 6: e19121.
• World Health Organization (2002) World Health Reports “Reducing risks, promoting healthy life”. Geneva. Yamashita K, Wiessner C, Lindholm D, Thoenen H, Hossmann KA (1997) Post‑occlusion treatment with BDNF reduces infarct size in a model of permanent occlusion of the middle cerebral artery in rat. Metab Brain Dis 12: 271–280.
• Yang Y, Rosenberg GA (2011) MMP‑mediated disruption of claudin‑5 in the blood–brain barrier of rat brain after cerebral ischemia. Methods Mol Biol 762: 333–345.
• Yi YH, Guo WC, Sun WW, Su T, Lin H, Chen SQ, Deng WY, Zhou  W, Liao WP (2008) Neuroprotection of lamotrigine on hypoxic‑ischemic brain damage in neonatal rats: Relations to administration time and doses. Biologics 2: 339–344.
• Yrjänheikki J, Tikka T, Keinänen R, Goldsteins G, Chan PH, Koistinaho J (1999) A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a  wide therapeutic window. Proc Natl Acad Sci 96: 13496–13500.
• Zaheer S, Beg M, Rizvi I, Islam N, Ullah E, Akhtar N (2013) Correlation between serum neuron specific enolase and functional neurological outcome in patients of acute ischemic stroke. Ann Indian Acad Neurol 16: 504–508.
• Zensi A, Begley D, Pontikis C, Legros C, Mihoreanu  L, Wagner S, Büchel C, Kreuter J (2009) Albumin nanoparticles targeted with Apo E enter the CNS by transcytosis and are delivered to neurones. J Control Release 137: 78–86.
• Zhang L, Zhang RL, Jiang Q, Ding G, Chopp M, Zhang ZG (2015) Focal embolic cerebral ischemia in the rat. Nat Protoc 10: 539–547.
• Zhang R, Zhang Z, Zhang C, Zhang  L, Robin A, Wang Y, Lu  M, Chopp  M (2004) Stroke transiently increases subventricular zone cell division from asymmetric to symmetric and increases neuronal differentiation in the adult rat. J Neurosci 24: 5810–5815

Identyfikatory

DOI

10.21307/ane‑2020‑001