L1CAM Beneficially Inhibits Histone Deacetylase 2 Expression under Conditions of Alzheimer’s Disease

Author(s): Chengliang Hu, Junkai Hu, Xianghe Meng, Hongli Zhang, Huifan Shen, Peizhi Huang, Melitta Schachner*, Weijiang Zhao*

Journal Name: Current Alzheimer Research

Volume 17 , Issue 4 , 2020

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Background: Cognitive capacities in Alzheimer’s Disease (AD) are impaired by an epigenetic blockade mediated by histone deacetylase 2 (HDAC2), which prevents the transcription of genes that are important for synaptic plasticity.

Objective: Investigation of the functional relationship between cell adhesion molecule L1 and HDAC2 in AD.

Methods: Cultures of dissociated cortical and hippocampal neurons from wild-type or L1-deficient mice were treated with Aβ1-42 for 24 h. After removal of Aβ1-42 cells were treated with the recombinant L1 extracellular domain (rL1) for 24 h followed by immunohistochemistry, western blotting, and reverse transcription PCR to evaluate the interaction between L1 and HDAC2.

Results: Aβ and HDAC2 protein levels were increased in APPSWE/L1+/- mutant brains compared to APPSWE mutant brains. Administration of the recombinant extracellular domain of L1 to cultured cortical and hippocampal neurons reduced HDAC2 mRNA and protein levels. In parallel, reduced phosphorylation levels of glucocorticoid receptor 1 (GR1), which is implicated in regulating HDAC2 levels, was observed in response to L1 administration. Application of a glucocorticoid receptor inhibitor reduced Aβ-induced GR1 phosphorylation and prevented the increase in HDAC2 levels. HDAC2 protein levels were increased in cultured cortical neurons from L1-deficient mice. This change could be reversed by the administration of the recombinant extracellular domain of L1.

Conclusion: Our results suggest that some functionally interdependent activities of L1 and HDAC2 contribute to ameliorating the phenotype of AD by GR1 dephosphorylation, which leads to reduced HDAC2 expression. The combined findings encourage further investigations on the beneficial effects of L1 in the treatment of AD.

Keywords: Alzheimer's disease, cell adhesion molecule L1, histone deacetylase 2, glucocorticoid receptor 1, brain, neuron.

Schneider LS, Mangialasche F, Andreasen N, et al. Clinical trials and late-stage drug development for Alzheimer’s disease: an appraisal from 1984 to 2014. J Intern Med 2014; 275(3): 251-83.
[http://dx.doi.org/10.1111/joim.12191] [PMID: 24605808]
Cao J, Hou J, Ping J, Cai D. Advances in developing novel therapeutic strategies for Alzheimer’s disease. Mol Neurodegener 2018; 13(1): 64.
[http://dx.doi.org/10.1186/s13024-018-0299-8] [PMID: 30541602]
Henstridge CM, Hyman BT, Spires-Jones TL. Beyond the neuron-cellular interactions early in Alzheimer disease pathogenesis. Nat Rev Neurosci 2019; 20(2): 94-108.
[http://dx.doi.org/10.1038/s41583-018-0113-1] [PMID: 30643230]
Panza F, Lozupone M, Logroscino G, Imbimbo BP. A critical appraisal of amyloid-β-targeting therapies for Alzheimer disease. Nat Rev Neurol 2019; 15(2): 73-88.
[http://dx.doi.org/10.1038/s41582-018-0116-6] [PMID: 30610216]
Gräff J, Rei D, Guan JS, et al. An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature 2012; 483(7388): 222-6.
[http://dx.doi.org/10.1038/nature10849] [PMID: 22388814]
Gräff J, Tsai LH. Histone acetylation: molecular mnemonics on the chromatin. Nat Rev Neurosci 2013; 14(2): 97-111.
[http://dx.doi.org/10.1038/nrn3427] [PMID: 23324667]
Wang DB, Kinoshita C, Kinoshita Y, et al. Neuronal susceptibility to beta-amyloid toxicity and ischemic injury involves histone deacetylase-2 regulation of endophilin-B1. Brain Pathol 2019; 29(2): 164-75.
[http://dx.doi.org/10.1111/bpa.12647] [PMID: 30028551]
Jaworska J, Ziemka-Nalecz M, Zalewska T. Histone deacetylases 1 and 2 are required for brain development. Int J Dev Biol 2015; 59(4-6): 171-7.
[http://dx.doi.org/10.1387/ijdb.150071tz] [PMID: 26198144]
Penney J, Tsai LH. Histone deacetylases in memory and cognition. Sci Signal 2014; 7(355): re12.
[http://dx.doi.org/10.1126/scisignal.aaa0069] [PMID: 25492968]
Hagelkruys A, Lagger S, Krahmer J, et al. A single allele of Hdac2 but not Hdac1 is sufficient for normal mouse brain development in the absence of its paralog. Development 2014; 141(3): 604-16.
[http://dx.doi.org/10.1242/dev.100487] [PMID: 24449838]
Hou N, Gong M, Bi Y, et al. Spatiotemporal expression of HDAC2 during the postnatal development of the rat hippocampus. Int J Med Sci 2014; 11(8): 788-95.
[http://dx.doi.org/10.7150/ijms.8417] [PMID: 24936141]
Roth TL, Roth ED, Sweatt JD. Epigenetic regulation of genes in learning and memory. Essays Biochem 2010; 48(1): 263-74.
[PMID: 20822498]
Gonzalez-Zuñiga M, Contreras PS, Estrada LD, et al. c-Abl stabilizes HDAC2 levels by tyrosine phosphorylation repressing neuronal gene expression in Alzheimer’s disease. Mol Cell 2014; 56(1): 163-73.
[http://dx.doi.org/10.1016/j.molcel.2014.08.013] [PMID: 25219501]
Guan JS, Haggarty SJ, Giacometti E, et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 2009; 459(7243): 55-60.
[http://dx.doi.org/10.1038/nature07925] [PMID: 19424149]
Morris MJ, Mahgoub M, Na ES, Pranav H, Monteggia LM. Loss of histone deacetylase 2 improves working memory and accelerates extinction learning. J Neurosci 2013; 33(15): 6401-11.
[http://dx.doi.org/10.1523/JNEUROSCI.1001-12.2013] [PMID: 23575838]
Liu D, Tang H, Li XY, et al. Targeting the HDAC2/HNF-4A/miR-101b/AMPK pathway rescues tauopathy and dendritic abnormalities in Alzheimer’s disease. Mol Ther 2017; 25(3): 752-64.
[http://dx.doi.org/10.1016/j.ymthe.2017.01.018] [PMID: 28202389]
Hung TC, Lee WY, Chen KB, Chan YC, Lee CC, Chen CY. In silico investigation of traditional Chinese medicine compounds to inhibit human histone deacetylase 2 for patients with Alzheimer’s disease. BioMed Res Int 2014; 2014: 769867.
[http://dx.doi.org/10.1155/2014/769867] [PMID: 25045700]
Choong CJ, Sasaki T, Hayakawa H, et al. A novel histone deacetylase 1 and 2 isoform-specific inhibitor alleviates experimental Parkinson’s disease. Neurobiol Aging 2016; 37: 103-16.
[http://dx.doi.org/10.1016/j.neurobiolaging.2015.10.001] [PMID: 26545632]
Mielcarek M, Benn CL, Franklin SA, et al. SAHA decreases HDAC 2 and 4 levels in vivo and improves molecular phenotypes in the R6/2 mouse model of Huntington’s disease. PLoS One 2011; 6(11)e27746
[http://dx.doi.org/10.1371/journal.pone.0027746] [PMID: 22140466]
Panikker P, Xu SJ, Zhang H, et al. Restoring tip60 HAT/HDAC2 balance in the neurodegenerative brain relieves epigenetic transcriptional repression and reinstates cognition. J Neurosci 2018; 38(19): 4569-83.
[http://dx.doi.org/10.1523/JNEUROSCI.2840-17.2018] [PMID: 29654189]
Wagner FF, Zhang YL, Fass DM, et al. Kinetically selective inhibitors of histone deacetylase 2 (HDAC2) as cognition enhancers. Chem Sci (Camb) 2015; 6(1): 804-15.
[http://dx.doi.org/10.1039/C4SC02130D] [PMID: 25642316]
Gräff J, Joseph NF, Horn ME, et al. Epigenetic priming of memory updating during reconsolidation to attenuate remote fear memories. Cell 2014; 156(1-2): 261-76.
[http://dx.doi.org/10.1016/j.cell.2013.12.020] [PMID: 24439381]
Xu K, Dai XL, Huang HC, Jiang ZF. Targeting HDACs: A promising therapy for Alzheimer’s disease. Oxid Med Cell Longev 2011; 2011: 143269.
[http://dx.doi.org/10.1155/2011/143269] [PMID: 21941604]
Chuang DM, Leng Y, Marinova Z, Kim HJ, Chiu CT. Multiple roles of HDAC inhibition in neurodegenerative conditions. Trends Neurosci 2009; 32(11): 591-601.
[http://dx.doi.org/10.1016/j.tins.2009.06.002] [PMID: 19775759]
Singh P, Thakur MK. Histone deacetylase 2 inhibition attenuates downregulation of hippocampal plasticity gene expression during aging. Mol Neurobiol 2018; 55(3): 2432-42.
[http://dx.doi.org/10.1007/s12035-017-0490-x] [PMID: 28364391]
Choubey SK, Jeyakanthan J. Molecular dynamics and quantum chemistry-based approaches to identify isoform selective HDAC2 inhibitor - a novel target to prevent Alzheimer’s disease. J Recept Signal Transduct Res 2018; 38(3): 266-78.
[http://dx.doi.org/10.1080/10799893.2018.1476541] [PMID: 29932788]
Li X, Zhan Z, Zhang J, Zhou F, An L. Beta-Hydroxybutyrate Ameliorates abeta-induced downregulation of trka expression by inhibiting HDAC1/3 in SH-SY5Y cells. Am J Alzheimers Dis Other Demen 2020; 35:1533317519883496
Lindner J, Rathjen FG, Schachner M. L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 1983; 305(5933): 427-30.
[http://dx.doi.org/10.1038/305427a0] [PMID: 6621692]
Kruse J, Mailhammer R, Wernecke H, et al. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature 1984; 311(5982): 153-5.
[http://dx.doi.org/10.1038/311153a0] [PMID: 6206400]
Schachner M. Neural recognition molecules and synaptic plasticity. Curr Opin Cell Biol 1997; 9(5): 627-34.
[http://dx.doi.org/10.1016/S0955-0674(97)80115-9] [PMID: 9330865]
Maness PF, Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 2007; 10(1): 19-26.
[http://dx.doi.org/10.1038/nn1827] [PMID: 17189949]
Sytnyk V, Leshchyns’ka I, Schachner M. Neural cell adhesion molecules of the immunoglobulin superfamily regulate synapse formation, maintenance, and function. Trends Neurosci 2017; 40(5): 295-308.
[http://dx.doi.org/10.1016/j.tins.2017.03.003] [PMID: 28359630]
Xu J, Hu C, Jiang Q, Pan H, Shen H, Schachner M. Trimebutine, a small molecule mimetic agonist of adhesion molecule L1, contributes to functional recovery after spinal cord injury in mice. Dis Model Mech 2017; 10(9): 1117-28.
[http://dx.doi.org/10.1242/dmm.029801] [PMID: 28714852]
Kataria H, Lutz D, Chaudhary H, Schachner M, Loers G. Small molecule agonists of cell adhesion molecule L1 mimic L1 functions in vivo. Mol Neurobiol 2016; 53(7): 4461-83.
[http://dx.doi.org/10.1007/s12035-015-9352-6] [PMID: 26253722]
Bernreuther C, Dihné M, Johann V, et al. Neural cell adhesion molecule L1-transfected embryonic stem cells promote functional recovery after excitotoxic lesion of the mouse striatum. J Neurosci 2006; 26(45): 11532-9.
[http://dx.doi.org/10.1523/JNEUROSCI.2688-06.2006] [PMID: 17093074]
Cui YF, Hargus G, Xu JC, et al. Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery in Parkinsonian mice. Brain 2010; 133(Pt 1): 189-204.
[http://dx.doi.org/10.1093/brain/awp290] [PMID: 19995872]
Ourednik V, Ourednik J, Xu Y, et al. Cross-talk between stem cells and the dysfunctional brain is facilitated by manipulating the niche: evidence from an adhesion molecule. Stem Cells 2009; 27(11): 2846-56.
[http://dx.doi.org/10.1002/stem.227] [PMID: 19785036]
Strekalova H, Buhmann C, Kleene R, et al. Elevated levels of neural recognition molecule L1 in the cerebrospinal fluid of patients with Alzheimer disease and other dementia syndromes. Neurobiol Aging 2006; 27(1): 1-9.
[http://dx.doi.org/10.1016/j.neurobiolaging.2004.11.013] [PMID: 16298234]
Djogo N, Jakovcevski I, Müller C, et al. Adhesion molecule L1 binds to amyloid beta and reduces Alzheimer’s disease pathology in mice. Neurobiol Dis 2013; 56: 104-15.
[http://dx.doi.org/10.1016/j.nbd.2013.04.014] [PMID: 23639788]
Dahme M, Bartsch U, Martini R, Anliker B, Schachner M, Mantei N. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat Genet 1997; 17(3): 346-9.
[http://dx.doi.org/10.1038/ng1197-346] [PMID: 9354804]
Wang SL, Kutsche M, DiSciullo G, Schachner M, Bogen SA. Selective malformation of the splenic white pulp border in L1-deficient mice. J Immunol 2000; 165(5): 2465-73.
[http://dx.doi.org/10.4049/jimmunol.165.5.2465] [PMID: 10946272]
Schmid JS, Bernreuther C, Nikonenko AG, et al. Heterozygosity for the mutated X-chromosome-linked L1 cell adhesion molecule gene leads to increased numbers of neurons and enhanced metabolism in the forebrain of female carrier mice. Brain Struct Funct 2013; 218(6): 1375-90.
[http://dx.doi.org/10.1007/s00429-012-0463-9] [PMID: 23196656]
Liu Y, Yu Y, Schachner M, Zhao W. Neuregulin 1-β regulates cell adhesion molecule L1 expression in the cortex and hippocampus of mice. Biochem Biophys Res Commun 2013; 441(1): 7-12.
[http://dx.doi.org/10.1016/j.bbrc.2013.09.102] [PMID: 24140408]
Wu G, Nan C, Rollo JC, Huang X, Tian J. Sodium valproate-induced congenital cardiac abnormalities in mice are associated with the inhibition of histone deacetylase. J Biomed Sci 2010; 17: 16.
[http://dx.doi.org/10.1186/1423-0127-17-16] [PMID: 20219112]
Tu S, Okamoto S, Lipton SA, Xu H. Oligomeric Aβ-induced synaptic dysfunction in Alzheimer’s disease. Mol Neurodegener 2014; 9: 48.
[http://dx.doi.org/10.1186/1750-1326-9-48] [PMID: 25394486]
Chong FP, Ng KY, Koh RY, Chye SM. Tau proteins and tauopathies in Alzheimer’s disease. Cell Mol Neurobiol 2018; 38(5): 965-80.
[http://dx.doi.org/10.1007/s10571-017-0574-1] [PMID: 29299792]
Lane CA, Hardy J, Schott JM. Alzheimer’s disease. Eur J Neurol 2018; 25(1): 59-70.
[http://dx.doi.org/10.1111/ene.13439] [PMID: 28872215]
Chavoshinezhad S, Mohseni Kouchesfahani H, Ahmadiani A, Dargahi L. Interferon beta ameliorates cognitive dysfunction in a rat model of Alzheimer’s disease: Modulation of hippocampal neurogenesis and apoptosis as underlying mechanism. Prog Neuropsychopharmacol Biol Psychiatry 2019; 94: 109661
Peleg S, Sananbenesi F, Zovoilis A, et al. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 2010; 328(5979): 753-6.
[http://dx.doi.org/10.1126/science.1186088] [PMID: 20448184]
Siddiqui SA, Singh S, Ugale R, et al. Regulation of HDAC1 and HDAC2 during consolidation and extinction of fear memory. Brain Res Bull 2019; 150: 86-101.
[http://dx.doi.org/10.1016/j.brainresbull.2019.05.011] [PMID: 31108155]
Wei J, Xiong Z, Lee JB, et al. Histone modification of nedd4 ubiquitin ligase controls the loss of AMPA receptors and cognitive impairment induced by repeated stress. J Neurosci 2016; 36(7): 2119-30.
[http://dx.doi.org/10.1523/JNEUROSCI.3056-15.2016] [PMID: 26888924]
Kootar S, Frandemiche ML, Dhib G, et al. Identification of an acute functional cross-talk between amyloid-β and glucocorticoid receptors at hippocampal excitatory synapses. Neurobiol Dis 2018; 118: 117-28.
[http://dx.doi.org/10.1016/j.nbd.2018.07.001] [PMID: 30003950]
Lanté F, Chafai M, Raymond EF, et al. Subchronic glucocorticoid receptor inhibition rescues early episodic memory and synaptic plasticity deficits in a mouse model of Alzheimer’s disease. Neuropsychopharmacology 2015; 40(7): 1772-81.
[http://dx.doi.org/10.1038/npp.2015.25] [PMID: 25622751]
Pineau F, Canet G, Desrumaux C, et al. New selective glucocorticoid receptor modulators reverse amyloid-β peptide-induced hippocampus toxicity. Neurobiol Aging 2016; 45: 109-22.
[http://dx.doi.org/10.1016/j.neurobiolaging.2016.05.018] [PMID: 27459932]
Grant NJ, Claudepierre T, Aunis D, Langley K. Glucocorticoids and nerve growth factor differentially modulate cell adhesion molecule L1 expression in PC12 cells. J Neurochem 1996; 66(4): 1400-8.
[http://dx.doi.org/10.1046/j.1471-4159.1996.66041400.x] [PMID: 8627291]
Merino JJ, Cordero MI, Sandi C. Regulation of hippocampal cell adhesion molecules NCAM and L1 by contextual fear conditioning is dependent upon time and stressor intensity. Eur J Neurosci 2000; 12(9): 3283-90.
[http://dx.doi.org/10.1046/j.1460-9568.2000.00191.x] [PMID: 10998112]
Touyarot K, Sandi C. Chronic restraint stress induces an isoform-specific regulation on the neural cell adhesion molecule in the hippocampus. Neural Plast 2002; 9(3): 147-59.
[http://dx.doi.org/10.1155/NP.2002.147] [PMID: 12757368]
Wang Y, Jia A, Ma W. Dexmedetomidine attenuates the toxicity of β‑amyloid on neurons and astrocytes by increasing BDNF production under the regulation of HDAC2 and HDAC5. Mol Med Rep 2019; 19(1): 533-40.
[PMID: 30483749]
Dong Q, Li X, Wang CZ, et al. Roles of the CSE1L-mediated nuclear import pathway in epigenetic silencing. Proc Natl Acad Sci USA 2018; 115(17): E4013-22.
[http://dx.doi.org/10.1073/pnas.1800505115] [PMID: 29636421]
Singh P, Konar A, Kumar A, Srivas S, Thakur MK. Hippocampal chromatin-modifying enzymes are pivotal for scopolamine-induced synaptic plasticity gene expression changes and memory impairment. J Neurochem 2015; 134(4): 642-51.
[http://dx.doi.org/10.1111/jnc.13171] [PMID: 25982413]
Moonat S, Sakharkar AJ, Zhang H, Tang L, Pandey SC. Aberrant histone deacetylase2-mediated histone modifications and synaptic plasticity in the amygdala predisposes to anxiety and alcoholism. Biol Psychiatry 2013; 73(8): 763-73.
[http://dx.doi.org/10.1016/j.biopsych.2013.01.012] [PMID: 23485013]
Hendrickx A, Pierrot N, Tasiaux B, et al. Epigenetic regulations of immediate early genes expression involved in memory formation by the amyloid precursor protein of Alzheimer disease. PLoS One 2014; 9(6)e99467
[http://dx.doi.org/10.1371/journal.pone.0099467] [PMID: 24919190]
Hu XT, Zhu BL, Zhao LG, et al. Histone deacetylase inhibitor apicidin increases expression of the α-secretase ADAM10 through transcription factor USF1-mediated mechanisms. FASEB J 2017; 31(4): 1482-93.
[http://dx.doi.org/10.1096/fj.201600961RR] [PMID: 28003340]
Wang Y, Jia A, Ma W. Dexmedetomidine attenuates the toxicity of β‑amyloid on neurons and astrocytes by increasing BDNF production under the regulation of HDAC2 and HDAC5. Mol Med Rep 2019; 19(1): 533-40.
[PMID: 30483749]
Gaub P, Tedeschi A, Puttagunta R, Nguyen T, Schmandke A, Di Giovanni S. HDAC inhibition promotes neuronal outgrowth and counteracts growth cone collapse through CBP/p300 and P/CAF-dependent p53 acetylation. Cell Death Differ 2010; 17(9): 1392-408.
[http://dx.doi.org/10.1038/cdd.2009.216] [PMID: 20094059]
Yuan L, Liu C, Wan Y, Yan H, Li T. Effect of HDAC2/Inpp5f on neuropathic pain and cognitive function through regulating PI3K/Akt/GSK-3β signal pathway in rats with neuropathic pain. Exp Ther Med 2019; 18(1): 678-84.
Kalus I, Schnegelsberg B, Seidah NG, Kleene R, Schachner M. The proprotein convertase PC5A and a metalloprotease are involved in the proteolytic processing of the neural adhesion molecule L1. J Biol Chem 2003; 278(12): 10381-8.
[http://dx.doi.org/10.1074/jbc.M208351200] [PMID: 12529374]
Doberstein K, Pfeilschifter J, Gutwein P. The transcription factor PAX2 regulates ADAM10 expression in renal cell carcinoma. Carcinogenesis 2011; 32(11): 1713-23.
[http://dx.doi.org/10.1093/carcin/bgr195] [PMID: 21880579]
Zhou L, Barão S, Laga M, et al. The neural cell adhesion molecules L1 and CHL1 are cleaved by BACE1 protease in vivo. J Biol Chem 2012; 287(31): 25927-40.
[http://dx.doi.org/10.1074/jbc.M112.377465] [PMID: 22692213]
Kraus K, Kleene R, Henis M, et al. A fragment of adhesion molecule L1 binds to nuclear receptors to regulate synaptic plasticity and motor coordination. Mol Neurobiol 2018; 55(9): 7164-78.
[http://dx.doi.org/10.1007/s12035-018-0901-7] [PMID: 29383692]
Kraus K, Kleene R, Braren I, Loers G, Lutz D, Schachner M. A fragment of adhesion molecule L1 is imported into mitochondria, and regulates mitochondrial metabolism and trafficking. J Cell Sci 2018; 131(9)210500
[http://dx.doi.org/10.1242/jcs.210500] [PMID: 29632241]
Garver TD, Ren Q, Tuvia S, Bennett V. Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin. J Cell Biol 1997; 137(3): 703-14.
[http://dx.doi.org/10.1083/jcb.137.3.703] [PMID: 9151675]
Poplawski GH, Tranziska AK, Leshchyns’ka I, et al. L1CAM increases MAP2 expression via the MAPK pathway to promote neurite outgrowth. Mol Cell Neurosci 2012; 50(2): 169-78.
[http://dx.doi.org/10.1016/j.mcn.2012.03.010] [PMID: 22503709]
Corbett GT, Gonzalez FJ, Pahan K. Activation of peroxisome proliferator-activated receptor α stimulates ADAM10-mediated proteolysis of APP. Proc Natl Acad Sci USA 2015; 112(27): 8445-50.
[http://dx.doi.org/10.1073/pnas.1504890112] [PMID: 26080426]
Chami L, Checler F. BACE1 is at the crossroad of a toxic vicious cycle involving cellular stress and β-amyloid production in Alzheimer’s disease. Mol Neurodegener 2012; 7: 52.
[http://dx.doi.org/10.1186/1750-1326-7-52] [PMID: 23039869]
Thomas EA, D’Mello SR. Complex neuroprotective and neurotoxic effects of histone deacetylases. J Neurochem 2018; 145(2): 96-110.
[http://dx.doi.org/10.1111/jnc.14309] [PMID: 29355955]
De Simone A, Milelli A. Histone deacetylase inhibitors as multitarget ligands: new players in Alzheimer’s disease drug discovery? ChemMedChem 2019; 14(11): 1067-73.
[http://dx.doi.org/10.1002/cmdc.201900174] [PMID: 30958639]
Yang SS, Zhang R, Wang G, Zhang YF. The development prospection of HDAC inhibitors as a potential therapeutic direction in Alzheimer’s disease. Transl Neurodegener 2017; 6: 19.
[http://dx.doi.org/10.1186/s40035-017-0089-1] [PMID: 28702178]
Wei CH, Ryu SE. Homophilic interaction of the L1 family of cell adhesion molecules. Exp Mol Med 2012; 44(7): 413-23.
[http://dx.doi.org/10.3858/emm.2012.44.7.050] [PMID: 22573111]
Gouveia RM, Gomes CM, Sousa M, Alves PM, Costa J. Kinetic analysis of L1 homophilic interaction: role of the first four immunoglobulin domains and implications on binding mechanism. J Biol Chem 2008; 283(42): 28038-47.
[http://dx.doi.org/10.1074/jbc.M804991200] [PMID: 18701456]
Schulz F, Lutz D, Rusche N, et al. Gold nanoparticles functionalized with a fragment of the neural cell adhesion molecule L1 stimulate L1-mediated functions. Nanoscale 2013; 5(21): 10605-17.
[http://dx.doi.org/10.1039/c3nr02707d] [PMID: 24056775]
Tang DY, Yu Y, Zhao XJ, Schachner M, Zhao WJ. Single chain fragment variable antibodies developed by using as target the 3rd fibronectin type III homologous repeat fragment of human neural cell adhesion molecule L1 promote cell migration and neuritogenesis. Exp Cell Res 2015; 330(2): 336-45.
[http://dx.doi.org/10.1016/j.yexcr.2014.10.021] [PMID: 25447207]
Deussing JM, Jakovcevski M. Histone modifications in major depressive disorder and related rodent models. Adv Exp Med Biol 2017; 978: 169-83.
[http://dx.doi.org/10.1007/978-3-319-53889-1_9] [PMID: 28523546]

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Year: 2020
Published on: 22 April, 2020
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DOI: 10.2174/1567205017666200422155323
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