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Published in: BMC Complementary Medicine and Therapies 1/2014

Open Access 01-12-2014 | Research article

Electroacupuncture decreases cognitive impairment and promotes neurogenesis in the APP/PS1 transgenic mice

Authors: Xuying Li, Fan Guo, Qiaomei Zhang, Tingting Huo, Lixin Liu, Haidong Wei, Lize Xiong, Qiang Wang

Published in: BMC Complementary Medicine and Therapies | Issue 1/2014

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Abstract

Background

Alzheimer’s disease (AD) is a severe neurodegenerative disease for which there is currently no effective treatment. The purpose of this study was to investigate whether repeated electroacupuncture (EA) stimulation would improve cognitive function and the pathological features of AD in amyloid precursor protein (APP)/presenilin 1 (PS1) double transgenic mice.

Methods

Cognitive function of APP/PS1 double transgenic mice was assessed using the Morris water maze test before and after EA treatment. Levels of amyloid β-peptide (Aβ) deposits in the hippocampus and cortex were evaluated by immunofluorescence, western blot and enzyme-linked immunosorbent assay. Expression of brain-derived neurotrophic factor (BDNF) was also examined by immunofluorescence and western blot. The neurogenesis was labeled by the DNA marker bromodeoxyuridine.

Results

EA stimulation significantly ameliorated the learning and memory deficits of AD mice by shortening escape latency and increasing the time spent in the target zone during the probe test. Additionally, decreased Aβ deposits and increased BDNF expression and neurogenesis in the hippocampus and cortex of EA-treated AD mice were detected. The same change was detected in wild-type mice after EA treatment compared with wild-type mice without EA treatment.

Conclusions

Repeated EA stimulation may improve cognitive function, attenuate Aβ deposits, up-regulate the expression of BDNF and promote neurogenesis in the APP/PS1 double transgenic mice. This suggests that EA may be a promising treatment for AD.
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Literature
2.
go back to reference Hampel H, Prvulovic D, Teipel S, Jessen F, Luckhaus C, Frölich L, Riepe MW, Dodel R, Leyhe T, Bertram L, Hoffmann W, Faltraco F, German Task Force on Alzheimer’s Disease (GTF-AD): The future of Alzheimer’s disease: the next 10 years. Prog Neurobiol. 2011, 95: 718-728. 10.1016/j.pneurobio.2011.11.008.CrossRefPubMed Hampel H, Prvulovic D, Teipel S, Jessen F, Luckhaus C, Frölich L, Riepe MW, Dodel R, Leyhe T, Bertram L, Hoffmann W, Faltraco F, German Task Force on Alzheimer’s Disease (GTF-AD): The future of Alzheimer’s disease: the next 10 years. Prog Neurobiol. 2011, 95: 718-728. 10.1016/j.pneurobio.2011.11.008.CrossRefPubMed
3.
go back to reference Selkoe DJ: Images in neuroscience. Alzheimer’s disease: from genes to pathogenesis. Am J Psychiatry. 1997, 154: 1198-CrossRefPubMed Selkoe DJ: Images in neuroscience. Alzheimer’s disease: from genes to pathogenesis. Am J Psychiatry. 1997, 154: 1198-CrossRefPubMed
4.
go back to reference Chuang TT: Neurogenesis in mouse models of Alzheimer’s disease. Biochim Biophys Acta. 1802, 2010: 872-880. Chuang TT: Neurogenesis in mouse models of Alzheimer’s disease. Biochim Biophys Acta. 1802, 2010: 872-880.
5.
go back to reference Henry RA, Hughes SM, Connor B: AAV-mediated delivery of BDNF augments neurogenesis in the normal and quinolinic acid-lesioned adult rat brain. Eur J Neurosci. 2007, 25: 3513-3525. 10.1111/j.1460-9568.2007.05625.x.CrossRefPubMed Henry RA, Hughes SM, Connor B: AAV-mediated delivery of BDNF augments neurogenesis in the normal and quinolinic acid-lesioned adult rat brain. Eur J Neurosci. 2007, 25: 3513-3525. 10.1111/j.1460-9568.2007.05625.x.CrossRefPubMed
6.
go back to reference Larsen MH, Rosenbrock H, Sams-Dodd F, Mikkelsen JD: Expression of brain derived neurotrophic factor, activity-regulated cytoskeleton protein mRNA, and enhancement of adult hippocampal neurogenesis in rats after sub-chronic and chronic treatment with the triple monoamine re-uptake inhibitor tesofensine. Eur J Pharmacol. 2007, 555: 115-121. 10.1016/j.ejphar.2006.10.029.CrossRefPubMed Larsen MH, Rosenbrock H, Sams-Dodd F, Mikkelsen JD: Expression of brain derived neurotrophic factor, activity-regulated cytoskeleton protein mRNA, and enhancement of adult hippocampal neurogenesis in rats after sub-chronic and chronic treatment with the triple monoamine re-uptake inhibitor tesofensine. Eur J Pharmacol. 2007, 555: 115-121. 10.1016/j.ejphar.2006.10.029.CrossRefPubMed
7.
go back to reference Connor B, Young D, Yan Q, Faull RL, Synek B, Dragunow M: Brain-derived neurotrophic factor is reduced in Alzheimer’s disease. Brain Res Mol Brain Res. 1997, 49: 71-81. 10.1016/S0169-328X(97)00125-3.CrossRefPubMed Connor B, Young D, Yan Q, Faull RL, Synek B, Dragunow M: Brain-derived neurotrophic factor is reduced in Alzheimer’s disease. Brain Res Mol Brain Res. 1997, 49: 71-81. 10.1016/S0169-328X(97)00125-3.CrossRefPubMed
8.
go back to reference Siegel GJ, Chauhan NB: Neurotrophic factors in Alzheimer’s and Parkinson’s disease brain. Brain Res Brain Res Rev. 2000, 33: 199-227. 10.1016/S0165-0173(00)00030-8.CrossRefPubMed Siegel GJ, Chauhan NB: Neurotrophic factors in Alzheimer’s and Parkinson’s disease brain. Brain Res Brain Res Rev. 2000, 33: 199-227. 10.1016/S0165-0173(00)00030-8.CrossRefPubMed
9.
go back to reference Feng S, Wang Q, Wang H, Peng Y, Wang L, Lu Y, Shi T, Xiong L: Electroacupuncture pretreatment ameliorates hypergravity-induced impairment of learning and memory and apoptosis of hippocampal neurons in rats. Neurosci Lett. 2010, 478: 150-155. 10.1016/j.neulet.2010.05.006.CrossRefPubMed Feng S, Wang Q, Wang H, Peng Y, Wang L, Lu Y, Shi T, Xiong L: Electroacupuncture pretreatment ameliorates hypergravity-induced impairment of learning and memory and apoptosis of hippocampal neurons in rats. Neurosci Lett. 2010, 478: 150-155. 10.1016/j.neulet.2010.05.006.CrossRefPubMed
10.
go back to reference Wang Q, Peng Y, Chen S, Gou X, Hu B, Du J, Lu Y, Xiong L: Pretreatment with electroacupuncture induces rapid tolerance to focal cerebral ischemia through regulation of endocannabinoid system. Stroke. 2009, 40: 2157-2164. 10.1161/STROKEAHA.108.541490.CrossRefPubMed Wang Q, Peng Y, Chen S, Gou X, Hu B, Du J, Lu Y, Xiong L: Pretreatment with electroacupuncture induces rapid tolerance to focal cerebral ischemia through regulation of endocannabinoid system. Stroke. 2009, 40: 2157-2164. 10.1161/STROKEAHA.108.541490.CrossRefPubMed
11.
go back to reference Wang Q, Li X, Chen Y, Wang F, Yang Q, Chen S, Min Y, Li X, Xiong L: Activation of epsilon protein kinase C-mediated anti-apoptosis is involved in rapid tolerance induced by electroacupuncture pretreatment through cannabinoid receptor type 1. Stroke. 2011, 42: 389-396. 10.1161/STROKEAHA.110.597336.CrossRefPubMed Wang Q, Li X, Chen Y, Wang F, Yang Q, Chen S, Min Y, Li X, Xiong L: Activation of epsilon protein kinase C-mediated anti-apoptosis is involved in rapid tolerance induced by electroacupuncture pretreatment through cannabinoid receptor type 1. Stroke. 2011, 42: 389-396. 10.1161/STROKEAHA.110.597336.CrossRefPubMed
12.
go back to reference Tao J, Xue XH, Chen LD, Yang SL, Jiang M, Gao YL, Wang XB: Electroacupuncture improves neurological deficits and enhances proliferation and differentiation of endogenous nerve stem cells in rats with focal cerebral ischemia. Neurol Res. 2010, 32: 198-204. 10.1179/174313209X414506.CrossRefPubMed Tao J, Xue XH, Chen LD, Yang SL, Jiang M, Gao YL, Wang XB: Electroacupuncture improves neurological deficits and enhances proliferation and differentiation of endogenous nerve stem cells in rats with focal cerebral ischemia. Neurol Res. 2010, 32: 198-204. 10.1179/174313209X414506.CrossRefPubMed
13.
go back to reference Hwang IK, Chung JY, Yoo DY, Yi SS, Youn HY, Seong JK, Yoon YS: Effects of electroacupuncture at Zusanli and Baihui on brain-derived neurotrophic factor and cyclic AMP response element-binding protein in the hippocampal dentate gyrus. J Vet Med Sci. 2010, 72: 1431-1436. 10.1292/jvms.09-0527.CrossRefPubMed Hwang IK, Chung JY, Yoo DY, Yi SS, Youn HY, Seong JK, Yoon YS: Effects of electroacupuncture at Zusanli and Baihui on brain-derived neurotrophic factor and cyclic AMP response element-binding protein in the hippocampal dentate gyrus. J Vet Med Sci. 2010, 72: 1431-1436. 10.1292/jvms.09-0527.CrossRefPubMed
14.
go back to reference Lu Z, Xiong L, Zhu Z, Wang Q, Chen M: Acupoint specificity of electroacupuncture preconditioning effect on cerebral ischemia injury in rats. Chin Acupunct Moxib. 2002, 22: 671-673. Lu Z, Xiong L, Zhu Z, Wang Q, Chen M: Acupoint specificity of electroacupuncture preconditioning effect on cerebral ischemia injury in rats. Chin Acupunct Moxib. 2002, 22: 671-673.
15.
go back to reference Wimo A, Jönsson L, Gustavsson A, McDaid D, Ersek K, Georges J, Gulácsi L, Karpati K, Kenigsberg P, Valtonen H: The economic impact of dementia in Europe in 2008-cost estimates from the Eurocode project. Int J Geriatr Psychiatry. 2011, 26: 825-832. 10.1002/gps.2610.CrossRefPubMed Wimo A, Jönsson L, Gustavsson A, McDaid D, Ersek K, Georges J, Gulácsi L, Karpati K, Kenigsberg P, Valtonen H: The economic impact of dementia in Europe in 2008-cost estimates from the Eurocode project. Int J Geriatr Psychiatry. 2011, 26: 825-832. 10.1002/gps.2610.CrossRefPubMed
16.
go back to reference McGowan E, Eriksen J, Hutton M: A decade of modeling Alzheimer’s disease in transgenic mice. Trends Genet. 2006, 22: 281-289. 10.1016/j.tig.2006.03.007.CrossRefPubMed McGowan E, Eriksen J, Hutton M: A decade of modeling Alzheimer’s disease in transgenic mice. Trends Genet. 2006, 22: 281-289. 10.1016/j.tig.2006.03.007.CrossRefPubMed
17.
go back to reference Masliah E, Sisk A, Mallory M, Mucke L, Schenk D, Games D: Comparison of neurodegenerative pathology in transgenic mice overexpressing V717F beta-amyloid precursor protein and Alzheimer’s disease. J Neurosci. 1996, 16: 5795-5811.PubMed Masliah E, Sisk A, Mallory M, Mucke L, Schenk D, Games D: Comparison of neurodegenerative pathology in transgenic mice overexpressing V717F beta-amyloid precursor protein and Alzheimer’s disease. J Neurosci. 1996, 16: 5795-5811.PubMed
18.
go back to reference Shi J, Perry G, Aliev G, Smith MA, Ashe KH, Friedland RP: Serum amyloid P is not present in amyloid beta deposits of a transgenic animal model. Neuroreport. 1999, 10: 3229-3232. 10.1097/00001756-199910190-00019.CrossRefPubMed Shi J, Perry G, Aliev G, Smith MA, Ashe KH, Friedland RP: Serum amyloid P is not present in amyloid beta deposits of a transgenic animal model. Neuroreport. 1999, 10: 3229-3232. 10.1097/00001756-199910190-00019.CrossRefPubMed
19.
go back to reference Aucoin JS, Jiang P, Aznavour N, Tong XK, Buttini M, Descarries L, Hamel E: Selective cholinergic denervation, independent from oxidative stress, in a mouse model of Alzheimer’s disease. Neuroscience. 2005, 132: 73-86. 10.1016/j.neuroscience.2004.11.047.CrossRefPubMed Aucoin JS, Jiang P, Aznavour N, Tong XK, Buttini M, Descarries L, Hamel E: Selective cholinergic denervation, independent from oxidative stress, in a mouse model of Alzheimer’s disease. Neuroscience. 2005, 132: 73-86. 10.1016/j.neuroscience.2004.11.047.CrossRefPubMed
20.
go back to reference Bronfman FC, Moechars D, Van Leuven F: Acetylcholinesterase-positive fiber deafferentation and cell shrinkage in the septohippocampal pathway of aged amyloid precursor protein london mutant transgenic mice. Neurobiol Dis. 2000, 7: 152-168. 10.1006/nbdi.2000.0283.CrossRefPubMed Bronfman FC, Moechars D, Van Leuven F: Acetylcholinesterase-positive fiber deafferentation and cell shrinkage in the septohippocampal pathway of aged amyloid precursor protein london mutant transgenic mice. Neurobiol Dis. 2000, 7: 152-168. 10.1006/nbdi.2000.0283.CrossRefPubMed
21.
go back to reference Jing XH, Chen SL, Shi H, Cai H, Jin ZG: Electroacupuncture restores learning and memory impairment induced by both diabetes mellitus and cerebral ischemia in rats. Neurosci Lett. 2008, 443: 193-198. 10.1016/j.neulet.2008.07.086.CrossRefPubMed Jing XH, Chen SL, Shi H, Cai H, Jin ZG: Electroacupuncture restores learning and memory impairment induced by both diabetes mellitus and cerebral ischemia in rats. Neurosci Lett. 2008, 443: 193-198. 10.1016/j.neulet.2008.07.086.CrossRefPubMed
22.
go back to reference Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, Fidani L, Giuffra L, Haynes A, Irving N, James L: Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer’s disease. Nature. 1991, 349: 704-706. 10.1038/349704a0.CrossRefPubMed Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, Fidani L, Giuffra L, Haynes A, Irving N, James L: Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer’s disease. Nature. 1991, 349: 704-706. 10.1038/349704a0.CrossRefPubMed
23.
go back to reference Cai XD, Golde TE, Younkin SG: Release of excess amyloid beta protein from a mutant amyloid beta protein precursor. Science. 1993, 259: 514-516. 10.1126/science.8424174.CrossRefPubMed Cai XD, Golde TE, Younkin SG: Release of excess amyloid beta protein from a mutant amyloid beta protein precursor. Science. 1993, 259: 514-516. 10.1126/science.8424174.CrossRefPubMed
24.
go back to reference Lopera F, Ardilla A, Martínez A, Madrigal L, Arango-Viana JC, Lemere CA, Arango-Lasprilla JC, Hincapíe L, Arcos-Burgos M, Ossa JE, Behrens IM, Norton J, Lendon C, Goate AM, Ruiz-Linares A, Rosselli M, Kosik KS: Clinical features of early-onset Alzheimer disease in a large kindred with an E280A presenilin-1 mutation. JAMA. 1997, 277: 793-799. 10.1001/jama.1997.03540340027028.CrossRefPubMed Lopera F, Ardilla A, Martínez A, Madrigal L, Arango-Viana JC, Lemere CA, Arango-Lasprilla JC, Hincapíe L, Arcos-Burgos M, Ossa JE, Behrens IM, Norton J, Lendon C, Goate AM, Ruiz-Linares A, Rosselli M, Kosik KS: Clinical features of early-onset Alzheimer disease in a large kindred with an E280A presenilin-1 mutation. JAMA. 1997, 277: 793-799. 10.1001/jama.1997.03540340027028.CrossRefPubMed
25.
go back to reference Di Carlo M, Giacomazza D, San Biaqio PL: Alzheimer’s disease: biological aspects, therapeutic perspectives and diagnostic tools. J Phys Condens Matter. 2012, 24: 244102-10.1088/0953-8984/24/24/244102.CrossRefPubMed Di Carlo M, Giacomazza D, San Biaqio PL: Alzheimer’s disease: biological aspects, therapeutic perspectives and diagnostic tools. J Phys Condens Matter. 2012, 24: 244102-10.1088/0953-8984/24/24/244102.CrossRefPubMed
26.
go back to reference Donovan MH, Yazdani U, Norris RD, Games D, German DC, Eisch AJ: Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer’s disease. J Comp Neurol. 2006, 495: 70-83. 10.1002/cne.20840.CrossRefPubMed Donovan MH, Yazdani U, Norris RD, Games D, German DC, Eisch AJ: Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer’s disease. J Comp Neurol. 2006, 495: 70-83. 10.1002/cne.20840.CrossRefPubMed
27.
go back to reference Gan L, Qiao S, Lan X, Chi L, Luo C, Lien L, Yan Liu Q, Liu R: Neurogenic responses to amyloid-beta plaques in the brain of Alzheimer’s disease-like transgenic (pPDGF-APPSw, Ind) mice. Neurobiol Dis. 2008, 29: 71-80. 10.1016/j.nbd.2007.08.002.CrossRefPubMed Gan L, Qiao S, Lan X, Chi L, Luo C, Lien L, Yan Liu Q, Liu R: Neurogenic responses to amyloid-beta plaques in the brain of Alzheimer’s disease-like transgenic (pPDGF-APPSw, Ind) mice. Neurobiol Dis. 2008, 29: 71-80. 10.1016/j.nbd.2007.08.002.CrossRefPubMed
28.
go back to reference Choi SH, Veeraraghavalu K, Lazarov O, Marler S, Ransohoff RM, Ramirez JM, Sisodia SS: Non-cell-autonomous effects of presenilin 1 variants on enrichment-mediated hippocampal progenitor cell proliferation and differentiation. Neuron. 2008, 59: 568-580. 10.1016/j.neuron.2008.07.033.CrossRefPubMedPubMedCentral Choi SH, Veeraraghavalu K, Lazarov O, Marler S, Ransohoff RM, Ramirez JM, Sisodia SS: Non-cell-autonomous effects of presenilin 1 variants on enrichment-mediated hippocampal progenitor cell proliferation and differentiation. Neuron. 2008, 59: 568-580. 10.1016/j.neuron.2008.07.033.CrossRefPubMedPubMedCentral
29.
go back to reference Ma QH, Futagawa T, Yang WL, Jiang XD, Zeng L, Takeda Y, Xu RX, Bagnard D, Schachner M, Furley AJ, Karagogeos D, Watanabe K, Dawe GS, Xiao ZC: A TAG1-APP signalling pathway through Fe65 negatively modulates neurogenesis. Nat Cell Biol. 2008, 10: 283-294. 10.1038/ncb1690.CrossRefPubMed Ma QH, Futagawa T, Yang WL, Jiang XD, Zeng L, Takeda Y, Xu RX, Bagnard D, Schachner M, Furley AJ, Karagogeos D, Watanabe K, Dawe GS, Xiao ZC: A TAG1-APP signalling pathway through Fe65 negatively modulates neurogenesis. Nat Cell Biol. 2008, 10: 283-294. 10.1038/ncb1690.CrossRefPubMed
30.
go back to reference Yu H, Saura CA, Choi SY, Sun LD, Yang X, Handler M, Kawarabayashi T, Younkin L, Fedeles B, Wilson MA, Younkin S, Kandel ER, Kirkwood A, Shen J: APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron. 2001, 31: 713-726. 10.1016/S0896-6273(01)00417-2.CrossRefPubMed Yu H, Saura CA, Choi SY, Sun LD, Yang X, Handler M, Kawarabayashi T, Younkin L, Fedeles B, Wilson MA, Younkin S, Kandel ER, Kirkwood A, Shen J: APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron. 2001, 31: 713-726. 10.1016/S0896-6273(01)00417-2.CrossRefPubMed
31.
go back to reference Thoenen H: Neurotrophins and neuronal plasticity. Science. 1995, 270: 593-598. 10.1126/science.270.5236.593.CrossRefPubMed Thoenen H: Neurotrophins and neuronal plasticity. Science. 1995, 270: 593-598. 10.1126/science.270.5236.593.CrossRefPubMed
32.
go back to reference Durany N, Michel T, Kurt J, Cruz-Sánchez FF, Cervós-Navarro J, Riederer P: Brain-derived neurotrophic factor and neurotrophin-3 levels in Alzheimer’s disease brains. Int J Dev Neurosci. 2000, 18: 807-813. 10.1016/S0736-5748(00)00046-0.CrossRef Durany N, Michel T, Kurt J, Cruz-Sánchez FF, Cervós-Navarro J, Riederer P: Brain-derived neurotrophic factor and neurotrophin-3 levels in Alzheimer’s disease brains. Int J Dev Neurosci. 2000, 18: 807-813. 10.1016/S0736-5748(00)00046-0.CrossRef
33.
go back to reference Holsinger RM, Schnarr J, Henry P, Castelo VT, Fahnestock M: Quantitation of BDNF mRNA in human parietal cortex by competitive reverse transcription-polymerase chain reaction: decreased levels in Alzheimer’s disease. Brain Res Mol Brain Res. 2000, 76: 347-354. 10.1016/S0169-328X(00)00023-1.CrossRefPubMed Holsinger RM, Schnarr J, Henry P, Castelo VT, Fahnestock M: Quantitation of BDNF mRNA in human parietal cortex by competitive reverse transcription-polymerase chain reaction: decreased levels in Alzheimer’s disease. Brain Res Mol Brain Res. 2000, 76: 347-354. 10.1016/S0169-328X(00)00023-1.CrossRefPubMed
34.
go back to reference Arancibia S, Silhol M, Moulière F, Meffre J, Höllinger I, Maurice T, Tapia-Arancibia L: Protective effect of BDNF against beta-amyloid induced neurotoxicity in vitro and in vivo in rats. Neurobiol Dis. 2008, 31: 316-326. 10.1016/j.nbd.2008.05.012.CrossRefPubMed Arancibia S, Silhol M, Moulière F, Meffre J, Höllinger I, Maurice T, Tapia-Arancibia L: Protective effect of BDNF against beta-amyloid induced neurotoxicity in vitro and in vivo in rats. Neurobiol Dis. 2008, 31: 316-326. 10.1016/j.nbd.2008.05.012.CrossRefPubMed
35.
go back to reference Tong L, Balazs R, Thornton PL, Cotman CW: Beta-amyloid peptide at sublethal concentrations downregulates brain-derived neurotrophic factor functions in cultured cortical neurons. J Neurosci. 2004, 24: 6799-6809. 10.1523/JNEUROSCI.5463-03.2004.CrossRefPubMed Tong L, Balazs R, Thornton PL, Cotman CW: Beta-amyloid peptide at sublethal concentrations downregulates brain-derived neurotrophic factor functions in cultured cortical neurons. J Neurosci. 2004, 24: 6799-6809. 10.1523/JNEUROSCI.5463-03.2004.CrossRefPubMed
36.
go back to reference Vitolo OV, Sant’Angelo A, Costanzo V, Battaglia F, Arancio O, Shelanski M: Amyloid beta -peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc Natl Acad Sci U S A. 2002, 99: 13217-13221. 10.1073/pnas.172504199.CrossRefPubMedPubMedCentral Vitolo OV, Sant’Angelo A, Costanzo V, Battaglia F, Arancio O, Shelanski M: Amyloid beta -peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc Natl Acad Sci U S A. 2002, 99: 13217-13221. 10.1073/pnas.172504199.CrossRefPubMedPubMedCentral
37.
go back to reference Sairanen M, Lucas G, Ernfors P, Castren M, Castren E: Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J Neurosci. 2005, 25: 1089-1094. 10.1523/JNEUROSCI.3741-04.2005.CrossRefPubMed Sairanen M, Lucas G, Ernfors P, Castren M, Castren E: Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J Neurosci. 2005, 25: 1089-1094. 10.1523/JNEUROSCI.3741-04.2005.CrossRefPubMed
38.
go back to reference Wang Q, Xiong L, Chen S, Liu Y, Zhu X: Rapid tolerance to focal cerebral ischemia in rats is induced by preconditioning with electroacupuncture: window of protection and the role of adenosine. Neurosci Lett. 2005, 381: 158-162. 10.1016/j.neulet.2005.02.019.CrossRefPubMed Wang Q, Xiong L, Chen S, Liu Y, Zhu X: Rapid tolerance to focal cerebral ischemia in rats is induced by preconditioning with electroacupuncture: window of protection and the role of adenosine. Neurosci Lett. 2005, 381: 158-162. 10.1016/j.neulet.2005.02.019.CrossRefPubMed
Metadata
Title
Electroacupuncture decreases cognitive impairment and promotes neurogenesis in the APP/PS1 transgenic mice
Authors
Xuying Li
Fan Guo
Qiaomei Zhang
Tingting Huo
Lixin Liu
Haidong Wei
Lize Xiong
Qiang Wang
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2014
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/1472-6882-14-37

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