Xuefu Zhuyu decoction improves neurological dysfunction by increasing synapsin expression after traumatic brain injury
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摘要
Xuefu Zhuyu decoction has been used for treating traumatic brain injury and improving post-traumatic dysfunction, but its mechanism of action needs further investigation. This study established rat models of traumatic brain injury by controlled cortical impact. Rat models were intragastrically administered 9 and 18 g/kg Xuefu Zhuyu decoction once a day for 14 or 21 days. Changes in neurological function were assessed by modified neurological severity scores and the Morris water maze. Immunohistochemistry, western blot assay, and reverse-transcription polymerase chain reaction were used to analyze synapsin protein and m RNA expression at the injury site of rats. Our results showed that Xuefu Zhuyu decoction visibly improved neurological function of rats with traumatic brain injury. These changes were accompanied by increased expression of synaptophysin, synapsin Ⅰ, and postsynaptic density protein-95 protein and m RNA in a dose-dependent manner. These findings indicate that Xuefu Zhuyu decoction increases synapsin expression and improves neurological deficits after traumatic brain injury.
Xuefu Zhuyu decoction has been used for treating traumatic brain injury and improving post-traumatic dysfunction, but its mechanism of action needs further investigation. This study established rat models of traumatic brain injury by controlled cortical impact. Rat models were intragastrically administered 9 and 18 g/kg Xuefu Zhuyu decoction once a day for 14 or 21 days. Changes in neurological function were assessed by modified neurological severity scores and the Morris water maze. Immunohistochemistry, western blot assay, and reverse-transcription polymerase chain reaction were used to analyze synapsin protein and m RNA expression at the injury site of rats. Our results showed that Xuefu Zhuyu decoction visibly improved neurological function of rats with traumatic brain injury. These changes were accompanied by increased expression of synaptophysin, synapsin Ⅰ, and postsynaptic density protein-95 protein and m RNA in a dose-dependent manner. These findings indicate that Xuefu Zhuyu decoction increases synapsin expression and improves neurological deficits after traumatic brain injury.
Xuefu Zhuyu decoction has been used for treating traumatic brain injury and improving post-traumatic dysfunction, but its mechanism of action needs further investigation. This study established rat models of traumatic brain injury by controlled cortical impact. Rat models were intragastrically administered 9 and 18 g/kg Xuefu Zhuyu decoction once a day for 14 or 21 days. Changes in neurological function were assessed by modified neurological severity scores and the Morris water maze. Immunohistochemistry, western blot assay, and reverse-transcription polymerase chain reaction were used to analyze synapsin protein and m RNA expression at the injury site of rats. Our results showed that Xuefu Zhuyu decoction visibly improved neurological function of rats with traumatic brain injury. These changes were accompanied by increased expression of synaptophysin, synapsin Ⅰ, and postsynaptic density protein-95 protein and m RNA in a dose-dependent manner. These findings indicate that Xuefu Zhuyu decoction increases synapsin expression and improves neurological deficits after traumatic brain injury.
引文
Ansari MA,Roberts KN,Scheff SW(2008a)Oxidative stress and modification of synaptic proteins in hippocampus after traumatic brain injury.Free Radic Biol Med 45:443-452.
Ansari MA,Roberts KN,Scheff SW(2008b)A time course of contusion-induced oxidative stress and synaptic proteins in cortex in a rat model of TBI.J Neurotrauma 25:513-526.
Atkins CM(2011)Decoding hippocampal signaling deficits after traumatic brain injury.Transl Stroke Res 2:546-555.
Aungst SL,Kabadi SV,Thompson SM,Stoica BA,Faden AI(2014)Repeated mild traumatic brain injury causes chronic neuroinflammation,changes in hippocampal synaptic plasticity,and associated cognitive deficits.J Cereb Blood Flow Metab 34:1223-1232.
Ayton S,Zhang M,Roberts BR,Lam LQ,Lind M,Mc Lean C,Bush AI,Frugier T,Crack PJ,Duce JA(2014)Ceruloplasmin and beta-amyloid precursor protein confer neuroprotection in traumatic brain injury and lower neuronal iron.Free Radic Biol Med 69:331-337.
Barman A,Chatterjee A,Bhide R(2016)Cognitive impairment and rehabilitation strategies after traumatic brain injury.Indian J Psychol Med 38:172-181.
Bonanomi D,Rusconi L,Colombo CA,Benfenati F,Valtorta F(2007)Synaptophysin I selectively specifies the exocytic pathway of synaptobrevin 2/VAMP2.Biochem J 404:525-534.
Bruns J,Jr.,Hauser WA(2003)The epidemiology of traumatic brain injury:a review.Epilepsia 44 Suppl 10:2-10.
Cesca F,Baldelli P,Valtorta F,Benfenati F(2010)The synapsins:key actors of synapse function and plasticity.Prog Neurobiol 91:313-348.
El-Husseini AE,Schnell E,Chetkovich DM,Nicoll RA,Bredt DS(2000)PSD-95involvement in maturation of excitatory synapses.Science 290:1364-1368.
Ferrer I(1999)Neurons and their dendrites in frontotemporal dementia.Dement Geriatr Cogn Disord 10 Suppl 1:55-60.
Fornasiero EF,Bonanomi D,Benfenati F,Valtorta F(2010)The role of synapsins in neuronal development.Cell Mol Life Sci 67:1383-1396.
Fu C,Xia Z,Liu Y,Lu H,Zhang Z,Wang Y,Fan X(2016)Qualitative analysis of major constituents from Xue Fu Zhu Yu Decoction using ultra high performance liquid chromatography with hybrid ion trap time-of-flight mass spectrometry.J Sep Sci 39:3457-3468.
Futai K,Kim MJ,Hashikawa T,Scheiffele P,Sheng M,Hayashi Y(2007)Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin.Nat Neurosci 10:186-195.
Gardoni F,Schrama LH,Kamal A,Gispen WH,Cattabeni F,Di Luca M(2001)Hippocampal synaptic plasticity involves competition between Ca2+/calmodulin-dependent protein kinase II and postsynaptic density95 for binding to the NR2A subunit of the NMDA receptor.J Neurosci21:1501-1509.
Gorczyca D,Ashley J,Speese S,Gherbesi N,Thomas U,Gundelfinger E,Gramates LS,Budnik V(2007)Postsynaptic membrane addition depends on the Discs-Large-interacting t-SNARE Gtaxin.J Neurosci 27:1033-1044.
Gulino R,Perciavalle V,Gulisano M(2010)Expression of cell fate determinants and plastic changes after neurotoxic lesion of adult mice spinal cord by cholera toxin-B saporin.Eur J Neurosci 31:1423-1434.
Gulino R,Dimartino M,Casabona A,Lombardo SA,Perciavalle V(2007)Synaptic plasticity modulates the spontaneous recovery of locomotion after spinal cord hemisection.Neurosci Res 57:148-156.
Haring RS,Narang K,Canner JK,Asemota AO,George BP,Selvarajah S,Haider AH,Schneider EB(2015)Traumatic brain injury in the elderly:morbidity and mortality trends and risk factors.J Surg Res 195:1-9.
Hu Q,Manaenko A,Xu T,Guo Z,Tang J,Zhang JH(2016)Hyperbaric oxygen therapy for traumatic brain injury:bench-to-bedside.Med Gas Res6:102-110.
Khan M,Khan H,Singh I,Singh AK(2017)Hypoxia inducible factor-1 alpha stabilization for regenerative therapy in traumatic brain injury.Neural Regen Res 12:696-701.
Kondo A,Shahpasand K,Mannix R,Qiu J,Moncaster J,Chen CH,Yao Y,Lin YM,Driver JA,Sun Y,Wei S,Luo ML,Albayram O,Huang P,Rotenberg A,Ryo A,Goldstein LE,Pascual-Leone A,Mc Kee AC,Meehan W,et al.(2015)Antibody against early driver of neurodegeneration cis P-tau blocks brain injury and tauopathy.Nature 523:431-436.
Lang SB,Stein V,Bonhoeffer T,Lohmann C(2007)Endogenous brain-derived neurotrophic factor triggers fast calcium transients at synapses in developing dendrites.J Neurosci 27:1097-1105.
Li SX,Wang JC,Cui J,Jia J,Qiao BL,Wang QH(2015)Effect of Xuefu Zhuyu decoction on the neural functional recovery and living ability in patients with craniocerebral injury.Xiandai Zhongxiyi Jiehe Zazhi 24:350-352.
Lin W,Yang LK,Cai S,Zhu J,Feng Y,Yang LX,Feng ZZ,Li PP,Chen JH,Wang YH(2016)Cognitive function and biomarkers after traumatic brain injury:protocol for a prospective inception cohort study.Asia Pac J Clin Trials Nerv Syst Dis 1:170-176.
Liu X,Wang H(2017)Effect of Danshen injection with neural stem cells transplantation in rats with craniocerebral injury.Zhongguo Zuzhi Gongcheng Yanjiu 21:4709-4715.
Livak KJ,Schmittgen TD(2001)Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T))Method.Methods 25:402-408.
Lou YL,Chen P,Jiang Y,Zhang H,Min YH(2016)Neural stem cell transplantation for sequela of traumatic brain injury:the best timing for treatment.Zhongguo Zuzhi Gongcheng Yanjiu 20:1474-1480.
Oliveira TG,Chan RB,Tian H,Laredo M,Shui G,Staniszewski A,Zhang H,Wang L,Kim TW,Duff KE,Wenk MR,Arancio O,Di Paolo G(2010)Phospholipase d2 ablation ameliorates Alzheimer’s disease-linked synaptic dysfunction and cognitive deficits.J Neurosci 30:16419-16428.
Oshima T,Lee S,Sato A,Oda S,Hirasawa H,Yamashita T(2009)TNF-alpha contributes to axonal sprouting and functional recovery following traumatic brain injury.Brain Res 1290:102-110.
Pan W,Han S,Kang L,Li S,Du J,Cui H(2016)Effects of dihydrotestosterone on synaptic plasticity of the hippocampus in mild cognitive impairment male SAMP8 mice.Exp Ther Med 12:1455-1463.
Paoletti I,De Gregorio V,Baroni A,Tufano MA,Donnarumma G,Perez JJ(2013)Amygdalin analogues inhibit IFN-gamma signalling and reduce the inflammatory response in human epidermal keratinocytes.Inflammation36:1316-1326.
Perez EJ,Cepero ML,Perez SU,Coyle JT,Sick TJ,Liebl DJ(2016)Eph B3signaling propagates synaptic dysfunction in the traumatic injured brain.Neurobiol Dis 94:73-84.
Popescu C,Anghelescu A,Daia C,Onose G(2015)Actual data on epidemiological evolution and prevention endeavours regarding traumatic brain injury.J Med Life 8:272-277.
Saito S,Kobayashi T,Osawa T,Kato S(2010)Effectiveness of Japanese herbal medicine yokukansan for alleviating psychiatric symptoms after traumatic brain injury.Psychogeriatrics 10:45-48.
Shi WL,Zhang JS,Hu YQ(2013)Prevention and treatment of blood vessels related diseases by xuefu zhuyu decoction(see text):its clinical application and progress in researches of mechanisms.Zhongguo Zhong Xi Yi Jie He Za Zhi 33:712-716.
Steiner P,Higley MJ,Xu W,Czervionke BL,Malenka RC,Sabatini BL(2008)Destabilization of the postsynaptic density by PSD-95 serine 73 phosphorylation inhibits spine growth and synaptic plasticity.Neuron 60:788-802.
Sucher NJ(2013)The application of Chinese medicine to novel drug discovery.Expert opinion on drug discovery 8:21-34.
Sun X,Wei X,Qu S,Zhao Y,Zhang X(2010)Hydroxysafflor Yellow A suppresses thrombin generation and inflammatory responses following focal cerebral ischemia-reperfusion in rats.Bioorg Med Chem Lett 20:4120-4124.
Thickbroom GW,Mastaglia FL(2009)Plasticity in neurological disorders and challenges for noninvasive brain stimulation(NBS).J Neuroeng Rehabil 6:4.
Villapol S,Balarezo MG,Affram K,Saavedra JM,Symes AJ(2015)Neurorestoration after traumatic brain injury through angiotensin II receptor blockage.Brain 138:3299-3315.
Wada T,Asano Y,Shinoda J(2012)Decreased fractional anisotropy evaluated using tract-based spatial statistics and correlated with cognitive dysfunction in patients with mild traumatic brain injury in the chronic stage.AJNR Am J Neuroradiol 33:2117-2122.
Wang H,Peng RY(2016)Basic roles of key molecules connected with NMDAR signaling pathway on regulating learning and memory and synaptic plasticity.Mil Med Res 3:26.
Wang S,Cesca F,Loers G,Schweizer M,Buck F,Benfenati F,Schachner M,Kleene R(2011)Synapsin I is an oligomannose-carrying glycoprotein,acts as an oligomannose-binding lectin,and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes.J Neurosci31:7275-7290.
Wang W,Li H,Yu J,Hong M,Zhou J,Zhu L,Wang Y,Luo M,Xia Z,Yang ZJ,Tang T,Ren P,Huang X,Wang J(2016)Protective effects of chinese herbal medicine rhizoma drynariae in rats after traumatic brain injury and identification of active compound.Mol Neurobiol 53:4809-4820.
Wu A,Ying Z,Gomez-Pinilla F(2004)Dietary omega-3 fatty acids normalize BDNF levels,reduce oxidative damage,and counteract learning disability after traumatic brain injury in rats.J Neurotrauma 21:1457-1467.
Wu A,Ying Z,Gomez-Pinilla F(2006)Dietary curcumin counteracts the outcome of traumatic brain injury on oxidative stress,synaptic plasticity,and cognition.Exp Neurol 197:309-317.
Wu A,Ying Z,Gomez-Pinilla F(2007)Omega-3 fatty acids supplementation restores mechanisms that maintain brain homeostasis in traumatic brain injury.J Neurotrauma 24:1587-1595.
Yang Y,Rosenberg GA(2011)Blood-brain barrier breakdown in acute and chronic cerebrovascular disease.Stroke 42:3323-3328.
Yorke AM,Littleton S,Alsalaheen BA(2016)Concussion attitudes and beliefs,knowledge,and clinical practice:survey of physical therapists.Phys Ther96:1018-1028.
Zhao J,Tu EJ,Mc Murray C,Sleigh A(2012)Rising mortality from injury in urban China:demographic burden,underlying causes and policy implications.Bull World Health Organ 90:461-467.
Zhao W,Wang C,Li Z,Chen L,Li J,Cui W,Ding S,Xi Q,Wang F,Jia F,Xiao S,Guo Y,Zhao Y(2015)Efficacy and safety of transcutaneous electrical acupoint stimulation to treat muscle spasticity following brain injury:a double-blinded,multicenter,randomized controlled trial.PLo S One10:e0116976.
Zhou ZW,Li YD,Gao WW,Chen JL,Yue SY,Zhang JN(2017)Cold water swimming pretreatment reduces cognitive deficits in a rat model of traumatic brain injury.Neural Regen Res 12:1322-1328.
Zhu X,Park J,Golinski J,Qiu J,Khuman J,Lee CC,Lo EH,Degterev A,Whalen MJ(2014)Role of Akt and mammalian target of rapamycin in functional outcome after concussive brain injury in mice.J Cereb Blood Flow Metab34:1531-1539.
Ansari MA,Roberts KN,Scheff SW(2008b)A time course of contusion-induced oxidative stress and synaptic proteins in cortex in a rat model of TBI.J Neurotrauma 25:513-526.
Atkins CM(2011)Decoding hippocampal signaling deficits after traumatic brain injury.Transl Stroke Res 2:546-555.
Aungst SL,Kabadi SV,Thompson SM,Stoica BA,Faden AI(2014)Repeated mild traumatic brain injury causes chronic neuroinflammation,changes in hippocampal synaptic plasticity,and associated cognitive deficits.J Cereb Blood Flow Metab 34:1223-1232.
Ayton S,Zhang M,Roberts BR,Lam LQ,Lind M,Mc Lean C,Bush AI,Frugier T,Crack PJ,Duce JA(2014)Ceruloplasmin and beta-amyloid precursor protein confer neuroprotection in traumatic brain injury and lower neuronal iron.Free Radic Biol Med 69:331-337.
Barman A,Chatterjee A,Bhide R(2016)Cognitive impairment and rehabilitation strategies after traumatic brain injury.Indian J Psychol Med 38:172-181.
Bonanomi D,Rusconi L,Colombo CA,Benfenati F,Valtorta F(2007)Synaptophysin I selectively specifies the exocytic pathway of synaptobrevin 2/VAMP2.Biochem J 404:525-534.
Bruns J,Jr.,Hauser WA(2003)The epidemiology of traumatic brain injury:a review.Epilepsia 44 Suppl 10:2-10.
Cesca F,Baldelli P,Valtorta F,Benfenati F(2010)The synapsins:key actors of synapse function and plasticity.Prog Neurobiol 91:313-348.
El-Husseini AE,Schnell E,Chetkovich DM,Nicoll RA,Bredt DS(2000)PSD-95involvement in maturation of excitatory synapses.Science 290:1364-1368.
Ferrer I(1999)Neurons and their dendrites in frontotemporal dementia.Dement Geriatr Cogn Disord 10 Suppl 1:55-60.
Fornasiero EF,Bonanomi D,Benfenati F,Valtorta F(2010)The role of synapsins in neuronal development.Cell Mol Life Sci 67:1383-1396.
Fu C,Xia Z,Liu Y,Lu H,Zhang Z,Wang Y,Fan X(2016)Qualitative analysis of major constituents from Xue Fu Zhu Yu Decoction using ultra high performance liquid chromatography with hybrid ion trap time-of-flight mass spectrometry.J Sep Sci 39:3457-3468.
Futai K,Kim MJ,Hashikawa T,Scheiffele P,Sheng M,Hayashi Y(2007)Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin.Nat Neurosci 10:186-195.
Gardoni F,Schrama LH,Kamal A,Gispen WH,Cattabeni F,Di Luca M(2001)Hippocampal synaptic plasticity involves competition between Ca2+/calmodulin-dependent protein kinase II and postsynaptic density95 for binding to the NR2A subunit of the NMDA receptor.J Neurosci21:1501-1509.
Gorczyca D,Ashley J,Speese S,Gherbesi N,Thomas U,Gundelfinger E,Gramates LS,Budnik V(2007)Postsynaptic membrane addition depends on the Discs-Large-interacting t-SNARE Gtaxin.J Neurosci 27:1033-1044.
Gulino R,Perciavalle V,Gulisano M(2010)Expression of cell fate determinants and plastic changes after neurotoxic lesion of adult mice spinal cord by cholera toxin-B saporin.Eur J Neurosci 31:1423-1434.
Gulino R,Dimartino M,Casabona A,Lombardo SA,Perciavalle V(2007)Synaptic plasticity modulates the spontaneous recovery of locomotion after spinal cord hemisection.Neurosci Res 57:148-156.
Haring RS,Narang K,Canner JK,Asemota AO,George BP,Selvarajah S,Haider AH,Schneider EB(2015)Traumatic brain injury in the elderly:morbidity and mortality trends and risk factors.J Surg Res 195:1-9.
Hu Q,Manaenko A,Xu T,Guo Z,Tang J,Zhang JH(2016)Hyperbaric oxygen therapy for traumatic brain injury:bench-to-bedside.Med Gas Res6:102-110.
Khan M,Khan H,Singh I,Singh AK(2017)Hypoxia inducible factor-1 alpha stabilization for regenerative therapy in traumatic brain injury.Neural Regen Res 12:696-701.
Kondo A,Shahpasand K,Mannix R,Qiu J,Moncaster J,Chen CH,Yao Y,Lin YM,Driver JA,Sun Y,Wei S,Luo ML,Albayram O,Huang P,Rotenberg A,Ryo A,Goldstein LE,Pascual-Leone A,Mc Kee AC,Meehan W,et al.(2015)Antibody against early driver of neurodegeneration cis P-tau blocks brain injury and tauopathy.Nature 523:431-436.
Lang SB,Stein V,Bonhoeffer T,Lohmann C(2007)Endogenous brain-derived neurotrophic factor triggers fast calcium transients at synapses in developing dendrites.J Neurosci 27:1097-1105.
Li SX,Wang JC,Cui J,Jia J,Qiao BL,Wang QH(2015)Effect of Xuefu Zhuyu decoction on the neural functional recovery and living ability in patients with craniocerebral injury.Xiandai Zhongxiyi Jiehe Zazhi 24:350-352.
Lin W,Yang LK,Cai S,Zhu J,Feng Y,Yang LX,Feng ZZ,Li PP,Chen JH,Wang YH(2016)Cognitive function and biomarkers after traumatic brain injury:protocol for a prospective inception cohort study.Asia Pac J Clin Trials Nerv Syst Dis 1:170-176.
Liu X,Wang H(2017)Effect of Danshen injection with neural stem cells transplantation in rats with craniocerebral injury.Zhongguo Zuzhi Gongcheng Yanjiu 21:4709-4715.
Livak KJ,Schmittgen TD(2001)Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T))Method.Methods 25:402-408.
Lou YL,Chen P,Jiang Y,Zhang H,Min YH(2016)Neural stem cell transplantation for sequela of traumatic brain injury:the best timing for treatment.Zhongguo Zuzhi Gongcheng Yanjiu 20:1474-1480.
Oliveira TG,Chan RB,Tian H,Laredo M,Shui G,Staniszewski A,Zhang H,Wang L,Kim TW,Duff KE,Wenk MR,Arancio O,Di Paolo G(2010)Phospholipase d2 ablation ameliorates Alzheimer’s disease-linked synaptic dysfunction and cognitive deficits.J Neurosci 30:16419-16428.
Oshima T,Lee S,Sato A,Oda S,Hirasawa H,Yamashita T(2009)TNF-alpha contributes to axonal sprouting and functional recovery following traumatic brain injury.Brain Res 1290:102-110.
Pan W,Han S,Kang L,Li S,Du J,Cui H(2016)Effects of dihydrotestosterone on synaptic plasticity of the hippocampus in mild cognitive impairment male SAMP8 mice.Exp Ther Med 12:1455-1463.
Paoletti I,De Gregorio V,Baroni A,Tufano MA,Donnarumma G,Perez JJ(2013)Amygdalin analogues inhibit IFN-gamma signalling and reduce the inflammatory response in human epidermal keratinocytes.Inflammation36:1316-1326.
Perez EJ,Cepero ML,Perez SU,Coyle JT,Sick TJ,Liebl DJ(2016)Eph B3signaling propagates synaptic dysfunction in the traumatic injured brain.Neurobiol Dis 94:73-84.
Popescu C,Anghelescu A,Daia C,Onose G(2015)Actual data on epidemiological evolution and prevention endeavours regarding traumatic brain injury.J Med Life 8:272-277.
Saito S,Kobayashi T,Osawa T,Kato S(2010)Effectiveness of Japanese herbal medicine yokukansan for alleviating psychiatric symptoms after traumatic brain injury.Psychogeriatrics 10:45-48.
Shi WL,Zhang JS,Hu YQ(2013)Prevention and treatment of blood vessels related diseases by xuefu zhuyu decoction(see text):its clinical application and progress in researches of mechanisms.Zhongguo Zhong Xi Yi Jie He Za Zhi 33:712-716.
Steiner P,Higley MJ,Xu W,Czervionke BL,Malenka RC,Sabatini BL(2008)Destabilization of the postsynaptic density by PSD-95 serine 73 phosphorylation inhibits spine growth and synaptic plasticity.Neuron 60:788-802.
Sucher NJ(2013)The application of Chinese medicine to novel drug discovery.Expert opinion on drug discovery 8:21-34.
Sun X,Wei X,Qu S,Zhao Y,Zhang X(2010)Hydroxysafflor Yellow A suppresses thrombin generation and inflammatory responses following focal cerebral ischemia-reperfusion in rats.Bioorg Med Chem Lett 20:4120-4124.
Thickbroom GW,Mastaglia FL(2009)Plasticity in neurological disorders and challenges for noninvasive brain stimulation(NBS).J Neuroeng Rehabil 6:4.
Villapol S,Balarezo MG,Affram K,Saavedra JM,Symes AJ(2015)Neurorestoration after traumatic brain injury through angiotensin II receptor blockage.Brain 138:3299-3315.
Wada T,Asano Y,Shinoda J(2012)Decreased fractional anisotropy evaluated using tract-based spatial statistics and correlated with cognitive dysfunction in patients with mild traumatic brain injury in the chronic stage.AJNR Am J Neuroradiol 33:2117-2122.
Wang H,Peng RY(2016)Basic roles of key molecules connected with NMDAR signaling pathway on regulating learning and memory and synaptic plasticity.Mil Med Res 3:26.
Wang S,Cesca F,Loers G,Schweizer M,Buck F,Benfenati F,Schachner M,Kleene R(2011)Synapsin I is an oligomannose-carrying glycoprotein,acts as an oligomannose-binding lectin,and promotes neurite outgrowth and neuronal survival when released via glia-derived exosomes.J Neurosci31:7275-7290.
Wang W,Li H,Yu J,Hong M,Zhou J,Zhu L,Wang Y,Luo M,Xia Z,Yang ZJ,Tang T,Ren P,Huang X,Wang J(2016)Protective effects of chinese herbal medicine rhizoma drynariae in rats after traumatic brain injury and identification of active compound.Mol Neurobiol 53:4809-4820.
Wu A,Ying Z,Gomez-Pinilla F(2004)Dietary omega-3 fatty acids normalize BDNF levels,reduce oxidative damage,and counteract learning disability after traumatic brain injury in rats.J Neurotrauma 21:1457-1467.
Wu A,Ying Z,Gomez-Pinilla F(2006)Dietary curcumin counteracts the outcome of traumatic brain injury on oxidative stress,synaptic plasticity,and cognition.Exp Neurol 197:309-317.
Wu A,Ying Z,Gomez-Pinilla F(2007)Omega-3 fatty acids supplementation restores mechanisms that maintain brain homeostasis in traumatic brain injury.J Neurotrauma 24:1587-1595.
Yang Y,Rosenberg GA(2011)Blood-brain barrier breakdown in acute and chronic cerebrovascular disease.Stroke 42:3323-3328.
Yorke AM,Littleton S,Alsalaheen BA(2016)Concussion attitudes and beliefs,knowledge,and clinical practice:survey of physical therapists.Phys Ther96:1018-1028.
Zhao J,Tu EJ,Mc Murray C,Sleigh A(2012)Rising mortality from injury in urban China:demographic burden,underlying causes and policy implications.Bull World Health Organ 90:461-467.
Zhao W,Wang C,Li Z,Chen L,Li J,Cui W,Ding S,Xi Q,Wang F,Jia F,Xiao S,Guo Y,Zhao Y(2015)Efficacy and safety of transcutaneous electrical acupoint stimulation to treat muscle spasticity following brain injury:a double-blinded,multicenter,randomized controlled trial.PLo S One10:e0116976.
Zhou ZW,Li YD,Gao WW,Chen JL,Yue SY,Zhang JN(2017)Cold water swimming pretreatment reduces cognitive deficits in a rat model of traumatic brain injury.Neural Regen Res 12:1322-1328.
Zhu X,Park J,Golinski J,Qiu J,Khuman J,Lee CC,Lo EH,Degterev A,Whalen MJ(2014)Role of Akt and mammalian target of rapamycin in functional outcome after concussive brain injury in mice.J Cereb Blood Flow Metab34:1531-1539.
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