Acta Neuropharmacologica ›› 2017, Vol. 7 ›› Issue (4): 53-64.DOI: 10.3969/j.issn.2095-1396.2017.04.008
TIAN You,WANG Xue,AI Jing
Online:
2017-08-26
Published:
2017-12-01
Contact:
艾静,女,博士,教授,博士生导师;研究方向:神经药理学;Tel:+86-0451-86671354,E-mail:azhrbmu@126.com
About author:
田由,女,硕士研究生;研究方向:神经药理学;E-mail:13225779116@163.com
Supported by:
国家自然科学基金资助项目(No.81271207,No.81471115,No.81671052)
CLC Number:
TIAN You,WANG Xue,AI Jing. Research Progress of Basal Forebrain Cholinergic Dysfunction in Alzheimer’s Disease[J]. Acta Neuropharmacologica, 2017, 7(4): 53-64.
Add to citation manager EndNote|Ris|BibTeX
URL: http://actanp.hebeinu.edu.cn/EN/10.3969/j.issn.2095-1396.2017.04.008
[1] Alzheimer's Association. 2015 Alzheimer's disease facts and figures [J]. Alzheimers Dement, 2015, 11(3): 332-384.[2] Bruno Dubois, Howard H Feldman, Claudia Jacova, et al. Revising the definition of Alzheimer's disease: a new lexicon [J]. Lancet Neurol, 2010, 9(11): 1118-1127.[3] Deborah E Barnes, Kristine Yaffe. The projected effect of risk factor reduction on Alzheimer's disease prevalence [J]. Lancet Neurol, 2011, 10(9): 819-828.[4] Matthew R Brier, Brian Gordon, Karl Friedrichsen, et al. Tau and Abeta imaging, CSF measures, and cognition in Alzheimer's disease [J]. Sci Transl Med, 2016, 8(338): 338ra66.[5] Karl Herrup. The case for rejecting the amyloid cascade hypothesis [J]. Nat Neurosci, 2015, 18(6): 794-799.[6] Elliott J Mufson, Scott E Counts, Sylvia E Perez, et al. Cholinergic system during the progression of Alzheimer's disease: therapeutic implications [J]. Expert Rev Neurother, 2008, 8(11): 1703-1718.[7] Hermona Soreq. Checks and balances on cholinergic signaling in brain and body function [J]. Trends Neurosci, 2015, 38(7): 448-458.[8] Haga Tatsuya. Molecular properties of the high-affinity choline transporter CHT1 [J]. J Biochem, 2014, 156(4): 181-194.[9] Takashi Okuda, Tatsuya Haga, Yoshikastu Kanai, et al. Identification and characterization of the high-affinity choline transporter [J]. Nat Neurosci, 2000, 3(2): 120-125.[10] Stefanie A G Black, R Jane Rylett. Choline transporter CHT regulation and function in cholinergic neurons [J]. Cent Nerv Syst Agents Med Chem, 2012, 12(2): 114-121.[11] Francesco Amenta, Seyed Khosrow Tayebati. Pathways of acetylcholine synthesis, transport and release as targets for treatment of adult-onset cognitive dysfunction [J]. Curr Med Chem, 2008, 15(5): 488-498.[12] Talita H Ferreira-Vieira, Isabella M Guimaraes, Flavia R Silva, et al. Alzheimer's disease: Targeting the Cholinergic System [J]. Curr Neuropharmacol, 2016, 14(1): 101-115.[13] Stanley M Parsons, Ben A Bahr, Lawrence M Gracz, et al. Acetylcholine transport: fundamental properties and effects of pharmacologic agents [J]. Ann N Y Acad Sci, 1987, 493220-493233.[14] Kota Banzai, Takeshi Adachi, Susumu Izumi. Comparative analyses of the cholinergic locus of ChAT and VAChT and its expression in the silkworm Bombyx mori [J]. Comp Biochem Physiol B Biochem Mol Biol, 2015, 1851-1859.[15] Brygdia Berse, Jan Krzysztof Blusztajn. Coordinated up-regulation of choline acetyltransferase and vesicular acetylcholine transporter gene expression by the retinoic acid receptor alpha, cAMP, and leukemia inhibitory factor/ciliary neurotrophic factor signaling pathways in a murine septal cell line [J]. J Biol Chem, 1995, 270(38): 22101-4.[16] Clarissa L Waites, Craig C Garner. Presynaptic function in health and disease [J]. Trends Neurosci, 2011, 34(6): 326-37.[17] Dragomir Milovanovic, Reinhard Jahn. Organization and dynamics of SNARE proteins in the presynaptic membrane [J]. Front Physiol, 2015, doi.org/10.3389/fphys.2015.00089.[18] Mitsuharu Midorikawa, Takeshi Sakaba. Imaging Exocytosis of Single Synaptic Vesicles at a Fast CNS Presynaptic Terminal [J]. Neuron, 2015, 88(3): 492-498.[19] Martijn C De Wilde, Cassia R Overk, Sijben J. W., et al. Meta-analysis of synaptic pathology in Alzheimer's disease reveals selective molecular vesicular machinery vulnerability [J]. Alzheimers Dement, 2016, 12(6): 633-44.[20] Benjamin H M Hunn, Stephanie J Cragg, J Paul Bolam, et al. Impaired intracellular trafficking defines early Parkinson's disease [J]. Trends Neurosci, 2015, 38(3): 178-88.[21] Elizabeth C Ballinger, Mala Ananth, Talmage D. A., et al. Basal Forebrain Cholinergic Circuits and Signaling in Cognition and Cognitive Decline [J]. Neuron, 2016, 91(6): 1199-1218.[22] Alexander Thiele. Muscarinic signaling in the brain [J]. Annu Rev Neurosci, 2013, 36(1):36271-94.[23] Agnes J Jasinska, Todd Zorick, Arthur L Brody, et al. Dual role of nicotine in addiction and cognition: a review of neuroimaging studies in humans [J]. Neuropharmacology, 2014, 84:111-22.[24] Katiuscia Martinello, Huang Zhuo, Rafael Lujan, et al. Cholinergic afferent stimulation induces axonal function plasticity in adult hippocampal granule cells [J]. Neuron, 2015, 85(2): 346-63.[25] John A Dani, Daniel Bertrand. Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system [J]. Annu Rev Pharmacol Toxicol, 2007, 47:699-729.[26] Leonor M Teles-Grilo Ruivo, Jack R Mellor. Cholinergic modulation of hippocampal network function [J]. Front Synaptic Neurosci, 2013, 5:2.[27] Ruth Fabian-Fine, Paul Skehel, Mick L Errington, et al. Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus [J]. J Neurosci, 2001, 21(20): 7993-8003.[28] Karen A Bell, Hoon Shim, Chen Ching-Kang, et al. Nicotinic excitatory postsynaptic potentials in hippocampal CA1 interneurons are predominantly mediated by nicotinic receptors that contain alpha4 and beta2 subunits [J]. Neuropharmacology, 2011, 61(8): 1379-88.[29] Hill J A, Zoli M, Bourgeois J P, et al. Immunocytochemical localization of a neuronal nicotinic receptor: the beta 2-subunit [J]. J Neurosci, 1993, 13(4): 1551-68.[30] Marina R Picciotto, Michael J Higley, Yann S Mineur, Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior [J]. Neuron, 2012, 76(1): 116-29.[31] Mcgehee D S, Heath M J, Gelber S, et al. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors [J]. Science, 1995, 269(5231): 1692-6.[32] Susan Wonnacott S. Presynaptic nicotinic ACh receptors [J]. Trends Neurosci, 1997, 20(2): 92-98.[33] Huibert D Mansvelder, J Russel Keath, Daniel S Mcgehee, Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas [J]. Neuron, 2002, 33(6): 905-19.[34] Vinay Parikh, Ji Jin-zhao, Michael W Decker, et al. Prefrontal beta2 subunit-containing and alpha7 nicotinic acetylcholine receptors differentially control glutamatergic and cholinergic signaling [J]. J Neurosci, 2010, 30(9): 3518-30.[35] Criscuolo C, Accorroni A, Domenici L, et al. Impaired synaptic plasticity in the visual cortex of mice lacking alpha7-nicotinic receptor subunit [J]. Neuroscience, 2015, 294:166-71.[36] Vesna Lazarevic, Sandra Fienko, Maria Andres-Alonso, et al. Physiological Concentrations of Amyloid Beta Regulate Recycling of Synaptic Vesicles via Alpha7 Acetylcholine Receptor and CDK5/Calcineurin Signaling [J]. Front Mol Neurosci, 2017, 10221.[37] Arendt T, Bigl V, Arendt A, et al. Loss of neurons in the nucleus basalis of Meynert in Alzheimer's disease, paralysis agitans and Korsakoff's Disease [J]. Acta Neuropathol, 1983, 61(2): 101-8.[38] Aquilonius S M, Eckernas S A, Sundwall A, Regional distribution of choline acetyltransferase in the human brain: changes in Huntington's chorea [J]. J Neurol Neurosurg Psychiatry, 1975, 38(7): 669-77.[39] Bruno Dubois, Merle Ruberg, France Javoy-Agid, et al. A subcortico-cortical cholinergic system is affected in Parkinson's disease [J]. Brain Res, 1983, 288(1-2): 213-218.[40] Elliott J Mufson, Stephen D Ginsberg, Milos D Ikonomovic, et al. Human cholinergic basal forebrain: chemoanatomy and neurologic dysfunction [J]. J Chem Neuroanat, 2003, 26(4): 233-42.[41] Giancarlo Pepeu, Maria Grazia Giovannini. The fate of the brain cholinergic neurons in neurodegenerative diseases [J]. Brain Res, 2017, 1670:173-184.[42] Wu Hao, John Williams, Jeremy Nathans, Complete morphologies of basal forebrain cholinergic neurons in the mouse [J]. Elife, 2014, 3:e02444.[43] Dayan Knox, Samantha M Keller. Cholinergic neuronal lesions in the medial septum and vertical limb of the diagonal bands of Broca induce contextual fear memory generalization and impair acquisition of fear extinction [J]. Hippocampus, 2016, 26(6): 718-26.[44] Patrick Dutar, Marie-Helene Bassant, Marie-Claude Senut, et al. The septohippocampal pathway: structure and function of a central cholinergic system [J]. Physiol Rev, 1995, 75(2): 393-427.[45] Amaral D G, Kurz J. An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat [J]. J Comp Neurol, 1985, 240(1): 37-59.[46] Nyakas C, Luiten P G, Spencer D G, et al. Detailed projection patterns of septal and diagonal band efferents to the hippocampus in the rat with emphasis on innervation of CA1 and dentate gyrus [J]. Brain Res Bull, 1987, 18(4): 533-45.[47] Ehren L Newman, Kishan Gupta, Jason R Climer, et al. Cholinergic modulation of cognitive processing: insights drawn from computational models [J]. Front Behav Neurosci, 2012, doi.org/10.3389/fnbeh.2012.00024.[48] Bernard Bloem, Luc Schoppink, Diana C Rotaru, et al. Topographic mapping between basal forebrain cholinergic neurons and the medial prefrontal cortex in mice [J]. J Neurosci, 2014, 34(49): 16234-16246.[49] Neven Henigsberg, Petra Kalember, Pero Hrabac, et al. 1-H MRS changes in dorsolateral prefrontal cortex after donepezil treatment in patients with mild to moderate Alzheimer's disease [J]. Coll Antropol, 2011, 35(Suppl): 1159-62.[50] Vanessa Krause, Shahid Bashir, Bettina Pollok, et al. 1 Hz rTMS of the left posterior parietal cortex (PPC) modifies sensorimotor timing [J]. Neuropsychologia, 2012, 50(14): 3729-35.[51] Michelle L Tomaszycki, Eldin Dzubur. 17beta-Hydroxysteroid dehydrogenase type IV, a Z-linked gene, is higher in females than in males in visual and auditory regions of developing zebra finches [J]. Brain Res, 2013, 1520: 95-106.[52] Patricia H Janak, Kay M Tye. From circuits to behaviour in the amygdala [J]. Nature, 2015, 517(7534): 284-92.[53] Dai Mitsushima, Akane Sano, Takuya Takahashi. A cholinergic trigger drives learning-induced plasticity at hippocampal synapses [J]. Nat Commun, 2013, 4: 2760.[54] Jessica J Roland, Amanda L Stewart, Kellie L Janke, et al. Medial septum-diagonal band of Broca (MSDB) GABAergic regulation of hippocampal acetylcholine efflux is dependent on cognitive demands [J]. J Neurosci, 2014, 34(2): 506-14.[55] Munir Gunes Kutlu, Thomas J Gould. Nicotinic modulation of hippocampal cell signaling and associated effects on learning and memory [J]. Physiol Behav, 2016, 155:162-171.[56] Siyoung Lee, Jisung Kim, Sang Gwon Seo, et al. Sulforaphane alleviates scopolamine-induced memory impairment in mice [J]. Pharmacol Res, 2014, 85: 23-32.[57] Saraswathi Subramaniyan, Seok Heo, Sudarshan Patil, et al. A hippocampal nicotinic acetylcholine alpha 7-containing receptor complex is linked to memory retrieval in the multiple-T-maze in C57BL/6j mice [J]. Behav Brain Res, 2014, 270: 137-45.[58] Gould R W, Dencker D, Grannan M, et al. Role for the M1 Muscarinic Acetylcholine Receptor in Top-Down Cognitive Processing Using a Touchscreen Visual Discrimination Task in Mice [J]. ACS Chem Neurosci, 2015, 6(10): 1683-1695.[59] Gu Zheng-lin, Jerrel L Yakel. Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity [J]. Neuron, 2011, 71(1): 155-165.[60] Andrew W Halff, David Gomez-Varela, Danielle John, et al. A novel mechanism for nicotinic potentiation of glutamatergic synapses [J]. J Neurosci, 2014, 34(6): 2051-64.[61] Paul T Francis, Alan M Palmer, Michael Snape, et al. The cholinergic hypothesis of Alzheimer's disease: a review of progress [J]. J Neurol Neurosurg Psychiatry, 1999, 66(2): 137-47.[62] Schliebs R, Arendt T. The significance of the cholinergic system in the brain during aging and in Alzheimer's disease [J]. J Neural Transm (Vienna), 2006, 113(11): 1625-44.[63] Marco Fuenzalida, Miguel Angel Perez, Hugo R Arias. Role of Nicotinic and Muscarinic Receptors on Synaptic Plasticity and Neurological Diseases [J]. Curr Pharm Des, 2016, 22(14): 2004-2014.[64] Kerbler G M, Fripp J, Rowe C C, et al. Alzheimer's Disease Neuroimaging Initiative, Basal forebrain atrophy correlates with amyloid beta burden in Alzheimer's disease [J]. Neuroimage Clin, 2015, 7:105-13.[65] Laura A Craig, Nancy S Hong, Robert J Mcdonald. Revisiting the cholinergic hypothesis in the development of Alzheimer's disease [J]. Neurosci Biobehav Rev, 2011, 35(6): 1397-409.[66] Linda M Bierer, Vahram Haroutunian, Steve Gabriel, et al. Neurochemical correlates of dementia severity in Alzheimer's disease: relative importance of the cholinergic deficits [J]. J Neurochem, 1995, 64(2): 749-60.[67] Milos D Ikonomovic, Elliott J Mufson, Joanne Wuu, et al. Reduction of choline acetyltransferase activity in primary visual cortex in mild to moderate Alzheimer's disease [J]. Arch Neurol, 2005, 62(3): 425-30.[68] Steven T Dekosky, Milos D Ikonomovic, Scot D Styren, et al. Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment [J]. Ann Neurol, 2002, 51(2): 145-55.[69] Fabiola M Ribeiro, Stefanie A G Black, Vania F Prado, et al. The "ins" and "outs" of the high-affinity choline transporter CHT1 [J]. J Neurochem, 2006, 97(1): 1-12.[70] Martin Sarter,Vinay Parikh. Choline transporters, cholinergic transmission and cognition [J]. Nat Rev Neurosci, 2005, 6(1): 48-56.[71] Daniel J Payette, Xie Jun, Guo Qing, Reduction in CHT1-mediated choline uptake in primary neurons from presenilin-1 M146V mutant knock-in mice [J]. Brain Res, 2007, 1135(1): 12-21.[72] Hideki Iwamoto, M Wade Calcutt, Randy D Blakely. Differential impact of genetically modulated choline transporter expression on the release of endogenous versus newly synthesized acetylcholine [J]. Neurochem Int, 2016, 98:138-145.[73] R J Rylett, M J Ball, E H Colhoun. Evidence for high affinity choline transport in synaptosomes prepared from hippocampus and neocortex of patients with Alzheimer's disease [J]. Brain Res, 1983, 289(1-2): 169-75.[74] Leah K Cuddy, Claudia Seah, Stephen H Pasternak, et al. Differential regulation of the high-affinity choline transporter by wild-type and Swedish mutant amyloid precursor protein [J]. J Neurochem, 2015, 134(4): 769-82.[75] Michael R Kilbourn. Small Molecule PET Tracers for Transporter Imaging [J]. Semin Nucl Med, 2017, 47(5): 536-552.[76] Counts S E, He B, Che S, et al. Alpha7 nicotinic receptor up-regulation in cholinergic basal forebrain neurons in Alzheimer disease [J]. Arch Neurol, 2007, 64(12): 1771-6.[77] Leung-Wing Chu, Ma E S K, Kam Yiu Lam, et al. Increased alpha 7 nicotinic acetylcholine receptor protein levels in Alzheimer's disease patients [J]. Dement Geriatr Cogn Disord, 2005, 19(2-3): 106-12.[78] Ewa Hellstrom-Lindahl, Malahat Mousavi, Zhang-ga Xiao, et al. Regional distribution of nicotinic receptor subunit mRNAs in human brain: comparison between Alzheimer and normal brain [J]. Brain Res Mol Brain Res, 1999, 66(1-2): 94-103.[79] Thanasak Teaktong, Alison Graham, Jennifer Court, et al. Alzheimer's disease is associated with a selective increase in alpha7 nicotinic acetylcholine receptor immunoreactivity in astrocytes [J]. Glia, 2003, 41(2): 207-11.[80] Robert G Nagele, Michael Robert D'andrea, William J Anderson, et al. Intracellular accumulation of beta-amyloid(1-42) in neurons is facilitated by the alpha 7 nicotinic acetylcholine receptor in Alzheimer's disease [J]. Neuroscience, 2002, 110(2): 199-211.[81] Daniela Puzzo, Lucia Privitera, Elena Leznik, et al. Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus [J]. J Neurosci, 2008, 28(53): 14537-45.[82] Scott E Counts, Bin He, Che Shao-li, et al. Galanin hyperinnervation upregulates choline acetyltransferase expression in cholinergic basal forebrain neurons in Alzheimer's disease [J]. Neurodegener Dis, 2008, 5(3-4): 228-31.[83] Gu Zheng-lin, Zhong Ping, Yan Zhen, Activation of muscarinic receptors inhibits beta-amyloid peptide-induced signaling in cortical slices [J]. J Biol Chem, 2003, 278(19): 17546-56.[84] Abraham Fisher, Zipora Pittel, Rachel Haring, et al. M1 muscarinic agonists can modulate some of the hallmarks in Alzheimer's disease: implications in future therapy [J]. J Mol Neurosci, 2003, 20(3): 349-56.[85] Ma Ke, Yang Zhi-hui, Yang Li-min, et al. Activation of M1 mAChRs by lesatropane rescues glutamate neurotoxicity in PC12 cells via PKC-mediated phosphorylation of ERK1/2 [J]. Bosn J Basic Med Sci, 2013, 13(3): 146-52.[86] Abraham Fisher, Rachel Brandeis, Rachel Haring Nira Bar-Ner, et al. AF150(S) and AF267B: M1 muscarinic agonists as innovative therapies for Alzheimer's disease [J]. J Mol Neurosci, 2002, 19(1-2): 145-53.[87] Antonella Caccamo, Salvatore Oddo, Lauren M Billings, et al. M1 receptors play a central role in modulating AD-like pathology in transgenic mice [J]. Neuron, 2006, 49(5): 671-82.[88] Stefan Teipel, Helmut Heinsen, Edson Amaro, et al. and Alzheimer's Disease Neuroimaging Initiative, Cholinergic basal forebrain atrophy predicts amyloid burden in Alzheimer's disease [J]. Neurobiol Aging, 2014, 35(3): 482-91.[89] Thomas Arendt, Martina K Bruckner, Markus Morawski, et al. Early neurone loss in Alzheimer's disease: cortical or subcortical? [J]. Acta Neuropathol Commun, 2015, 3:10.[90] Marsel Mesulam. The cholinergic lesion of Alzheimer's disease: pivotal factor or side show? [J]. Learn Mem, 2004, 11(1): 43-9.[91] Schmitz T W, Nathan Spreng R. Alzheimer's Disease Neuroimaging Initiative, Basal forebrain degeneration precedes and predicts the cortical spread of Alzheimer's pathology [J]. Nat Commun, 2016, 7:13249.[92] Aghourian M, Legault-Denis C, Soucy J P, et al. Quantification of brain cholinergic denervation in Alzheimer's disease using PET imaging with [18F]-FEOBV [J]. Mol Psychiatry, 2017, 22(11): 1531-1538.[93] Stephane Lehericy, Etienne C Hirsch, Pascale Cervera-Pierot, et al. Heterogeneity and selectivity of the degeneration of cholinergic neurons in the basal forebrain of patients with Alzheimer's disease [J]. J Comp Neurol, 1993, 330(1): 15-31.[94] Elliott J Mufson, Elizabeth Cochran, William Benzing, et al. Galaninergic innervation of the cholinergic vertical limb of the diagonal band (Ch2) and bed nucleus of the stria terminalis in aging, Alzheimer's disease and Down's syndrome [J]. Dementia, 1993, 4(5): 237-50.[95] Hiroshige Fujishiro, Hiroyuki Umegaki, Daisuke Isojima, et al. Depletion of cholinergic neurons in the nucleus of the medial septum and the vertical limb of the diagonal band in dementia with Lewy bodies [J]. Acta Neuropathol, 2006, 111(2): 109-14.[96] Maxime J Parent, Marc-Andre Bedard, Arturo Aliaga, et al. Cholinergic Depletion in Alzheimer's Disease Shown by [ (18) F]FEOBV Autoradiography [J]. Int J Mol Imaging, 2013, 2013: 205045.[97] Viviana Triaca, Pietro Calissano. Impairment of the nerve growth factor pathway driving amyloid accumulation in cholinergic neurons: the incipit of the Alzheimer's disease story? [J]. Neural Regen Res, 2016, 11(10): 1553-1556.[98] M Florencia Iulita, Augusto Claudio Cuello. The NGF Metabolic Pathway in the CNS and its Dysregulation in Down Syndrome and Alzheimer's Disease [J]. Curr Alzheimer Res, 2016, 13(1): 53-67.[99] M Florencia Iulita, A Claudio Cuello. Nerve growth factor metabolic dysfunction in Alzheimer's disease and Down syndrome [J]. Trends Pharmacol Sci, 2014, 35(7): 338-48.[100] Elliott J Mufson, He Bin, Muhammad Nadeem, et al. Hippocampal proNGF signaling pathways and beta-amyloid levels in mild cognitive impairment and Alzheimer disease [J]. J Neuropathol Exp Neurol, 2012, 71(11): 1018-29.[101] Alaina Baker-Nigh, Shahrooz Vahedi, Elena Goetz Davis, et al. Neuronal amyloid-beta accumulation within cholinergic basal forebrain in ageing and Alzheimer's disease [J]. Brain, 2015, 138(Pt 6): 1722-37.[102] Tomas Petrasek, Martina Skurlova, Kristyna Maleninska, et al. A Rat Model of Alzheimer's Disease Based on Abeta42 and Pro-oxidative Substances Exhibits Cognitive Deficit and Alterations in Glutamatergic and Cholinergic Neurotransmitter Systems [J]. Front Aging Neurosci, 2016, 8:83.[103] Maliheh Soodi, Soodabeh Saeidnia, Mohammad Sharifzadeh, et al. Satureja bachtiarica ameliorate beta-amyloid induced memory impairment, oxidative stress and cholinergic deficit in animal model of Alzheimer's disease [J]. Metab Brain Dis, 2016, 31(2): 395-404. |
[1] | YANG-Lin,AI-Jing. Research Progress of Brain-Derived Estrogen in Alzheimer’s Disease [J]. Acta Neuropharmacologica, 2019, 9(5): 50-64. |
[2] | ZHANG Shuai,AI Jing. Glutamate Dysfunction and Alzheimer’s Disease [J]. Acta Neuropharmacologica, 2018, 8(6): 9-20. |
[3] | ZHOU Wen-hua. Cognitive Enhancers as A Treatment for Heroin Relapse [J]. Acta Neuropharmacologica, 2018, 8(5): 66-67. |
[4] | 王奇. Bushen-Yizhi Formula Inhibits the NLRP3/NFκB Mediated Neuroinflammation and Improves the Motor Dysfunction in a Mouse Model of Parkinson's Disease [J]. Acta Neuropharmacologica, 2018, 8(5): 71-72. |
[5] | ZHU Chao,DU Ning-ning,ZHOU Yan-meng,WANG Hao,HOU Xue-qin,ZHANG Fang-fang,TAN Rui,GAO. Increased Blood Pressure Variability Impairs Memory in Rats [J]. Acta Neuropharmacologica, 2018, 8(5): 79-80. |
[6] | CUI Su-ying, SONG Jin-zhi, CUI Xiang-yu, HU Xiao, DING Hui, YE Hui, ZHANG Yong-he. Intracerebroventricular Streptozocin-induced Alzheimer’s Disease-like Sleep Disorders: Role of the GABAergic System in the Parabrachial Complex [J]. Acta Neuropharmacologica, 2018, 8(5): 96-97. |
[7] | YU Li-li1,2,XU Li1,WANG Yi-nuo1,XUE Lu-ning1,Gou Ji-wei1,LI Hong-bo1,HOU Xue-qin1*,ZHANG Han-ting1*. Effects of Osthole on Learning and Memory and the Estrogen Pathway in Ovariectomized Rats [J]. Acta Neuropharmacologica, 2018, 8(4): 7-8. |
[8] | SHEN li-xia1,LIU Liang-liang1,ZHANG Ming1,LIU Yang1,ZHANG Dan-shen 2*. Research of Quercetin’s Estrogen-Like Action on Central Nervous System and Its Mechanisms [J]. Acta Neuropharmacologica, 2018, 8(4): 23-25. |
[9] | WANG Hao1, ZHANG Fang-fang1, FU Hua-rong1, ZHOU Yan-meng1, LIU Xin1, HOU Xue-qin 1, HU Wei2, Rolf Hansen2, XU Ying3, James O’Donnell3, ZHANG Han-ting1,2. Targeting PDE4 for Alzheimer’s Disease and Alcoholism: An implication in Alcohol-Related Dementia? [J]. Acta Neuropharmacologica, 2018, 8(4): 39-41. |
[10] | YANG Wen-zhong1, ZHOU Xue-yan1, MA Tao1,2,3*. Impaired mRNA Translational Capacity is Correlated with Aging-Dependent Memory Deficits and Behavioral Inflexibility [J]. Acta Neuropharmacologica, 2018, 8(4): 50-52. |
[11] | WANG Jia-Yue,DUAN Yan-Hong,Wang Xin-He,Zhang Xu-Liang,Xu Mei-Chen, Cao Xiao-Hua *. The Effect of PHA-543613 on Memory Disorders in Presenilin1 and Presenilin2 Conditional Double Knockout Mice [J]. Acta Neuropharmacologica, 2018, 8(4): 52-53. |
[12] | ZHONG Jia-hong, WANG Hai-tao, XU Jiang-ping. Inhibition of Phosphodiesterase 4 by FCPR16 Protects SH-SY5Y Cells against MPP+-Induced Cell Death through Activating cAMP/PKA/CREB and Epac/Akt Signaling Pathways [J]. Acta Neuropharmacologica, 2018, 8(4): 54-55. |
[13] | LIN Zhi-bin. Pharmacological Progress of Ganoderma on Anti-aging and Anti-Alzheimer’s Disease [J]. Acta Neuropharmacologica, 2018, 8(1): 9-15. |
[14] | LIU Nuo,WANG Zhen-zhen,CHEN Nai-hong. The Role of Gut Flora in the Pathogenesis of Alzheimer’s Disease [J]. Acta Neuropharmacologica, 2017, 7(5): 28-. |
[15] | GAO Zhi-hong1,ZUO Ya-qi2,ZHANG Xiao-li1. A New Idea of Astragaloside-Induced Bone Marrow Mesenchymal Stem Cells in the Treatment of Parkinson’s Disease [J]. Acta Neuropharmacologica, 2017, 7(5): 39-44. |
Viewed | ||||||
Full text |
|
|||||
Abstract |
|
|||||