A centronuclear myopathy-causing mutation in dynamin-2 disrupts neuronal morphology and excitatory synaptic transmission in a murine model of the disease.
centronuclear myopathy
dendritic arborisation
dendritic spines
dynamin-2
neuronal morphology
synaptic transmission
Journal
Neuropathology and applied neurobiology
ISSN: 1365-2990
Titre abrégé: Neuropathol Appl Neurobiol
Pays: England
ID NLM: 7609829
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
revised:
30
04
2023
received:
12
09
2022
accepted:
02
06
2023
medline:
31
8
2023
pubmed:
15
6
2023
entrez:
15
6
2023
Statut:
ppublish
Résumé
Dynamin-2 is a large GTPase, a member of the dynamin superfamily that regulates membrane remodelling and cytoskeleton dynamics. Mutations in the dynamin-2 gene (DNM2) cause autosomal dominant centronuclear myopathy (CNM), a congenital neuromuscular disorder characterised by progressive weakness and atrophy of the skeletal muscles. Cognitive defects have been reported in some DNM2-linked CNM patients suggesting that these mutations can also affect the central nervous system (CNS). Here we studied how a dynamin-2 CNM-causing mutation influences the CNS function. Heterozygous mice harbouring the p.R465W mutation in the dynamin-2 gene (HTZ), the most common causing autosomal dominant CNM, were used as disease model. We evaluated dendritic arborisation and spine density in hippocampal cultured neurons, analysed excitatory synaptic transmission by electrophysiological field recordings in hippocampal slices, and evaluated cognitive function by performing behavioural tests. HTZ hippocampal neurons exhibited reduced dendritic arborisation and lower spine density than WT neurons, which was reversed by transfecting an interference RNA against the dynamin-2 mutant allele. Additionally, HTZ mice showed defective hippocampal excitatory synaptic transmission and reduced recognition memory compared to the WT condition. Our findings suggest that the dynamin-2 p.R465W mutation perturbs the synaptic and cognitive function in a CNM mouse model and support the idea that this GTPase plays a key role in regulating neuronal morphology and excitatory synaptic transmission in the hippocampus.
Substances chimiques
Dynamin II
EC 3.6.5.5
DNM2 protein, mouse
EC 3.6.5.5
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12918Informations de copyright
© 2023 British Neuropathological Society.
Références
Arriagada-Diaz J, Prado-Vega L, Cárdenas Díaz AM, Ardiles AO, Gonzalez-Jamett AM. Dynamin superfamily at pre- and postsynapses: master regulators of synaptic transmission and plasticity in health and disease. Neuroscientist. 0:1073858420974313.
Ferguson SM, De Camilli P. Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol. 2012;13(2):75-88. doi:10.1038/nrm3266
Gonzalez-Jamett AM, Momboisse F, Guerra MJ, et al. Dynamin-2 regulates fusion pore expansion and quantal release through a mechanism that involves actin dynamics in neuroendocrine chromaffin cells. PLoS ONE. 2013;8(8):e70638. doi:10.1371/journal.pone.0070638
Lomash RM, Gu X, Youle RJ, Lu W, Roche KW. Neurolastin, a dynamin family GTPase, regulates excitatory synapses and spine density. Cell Rep. 2015;12(5):743-751. doi:10.1016/j.celrep.2015.06.064
Newman-Smith ED, Shurland DL, van der Bliek AM. Assignment of the dynamin-1 gene (DNM1) to human chromosome 9q34 by fluorescence in situ hybridization and somatic cell hybrid analysis. Genomics. 1997;41(2):286-289. doi:10.1006/geno.1996.4596
Noakes PG, Chin D, Kim SS, Liang S, Phillips WD. Expression and localisation of dynamin and syntaxin during neural development and neuromuscular synapse formation. J Comp Neurol. 1999;410(4):531-540. doi:10.1002/(SICI)1096-9861(19990809)410:4<531::AID-CNE2>3.0.CO;2-C
Zuchner S, Noureddine M, Kennerson M, et al. Mutations in the pleckstrin homology domain of dynamin 2 cause dominant intermediate Charcot-Marie-tooth disease. Nat Genet. 2005;37(3):289-294. doi:10.1038/ng1514
Antonny B, Burd C, De Camilli P, et al. Membrane fission by dynamin: what we know and what we need to know. EMBO J. 2016;35(21):2270-2284. doi:10.15252/embj.201694613
Praefcke GJ, McMahon HT. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol. 2004;5(2):133-147. doi:10.1038/nrm1313
Singh M, Jadhav HR, Bhatt T. Dynamin functions and ligands: classical mechanisms behind. Mol Pharmacol. 2017;91(2):123-134. doi:10.1124/mol.116.105064
Chappie JS, Acharya S, Liu YW, Leonard M, Pucadyil TJ, Schmid SL. An intramolecular signaling element that modulates dynamin function in vitro and in vivo. Mol Biol Cell. 2009;20(15):3561-3571. doi:10.1091/mbc.e09-04-0318
Faelber K, Posor Y, Gao S, et al. Crystal structure of nucleotide-free dynamin. Nature. 2011;477(7366):556-560. doi:10.1038/nature10369
Ford MG, Jenni S, Nunnari J. The crystal structure of dynamin. Nature. 2011;477(7366):561-566. doi:10.1038/nature10441
Kong L, Sochacki KA, Wang H, et al. Cryo-EM of the dynamin polymer assembled on lipid membrane. Nature. 2018;560(7717):258-262. doi:10.1038/s41586-018-0378-6
Hinshaw JE, Schmid SL. Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature. 1995;374(6518):190-192. doi:10.1038/374190a0
Warnock DE, Baba T, Schmid SL. Ubiquitously expressed dynamin-II has a higher intrinsic GTPase activity and a greater propensity for self-assembly than neuronal dynamin-I. Mol Biol Cell. 1997;8(12):2553-2562. doi:10.1091/mbc.8.12.2553
Gu C, Yaddanapudi S, Weins A, et al. Direct dynamin-actin interactions regulate the actin cytoskeleton. EMBO J. 2010;29(21):3593-3606. doi:10.1038/emboj.2010.249
Lin SS, Hsieh TL, Liou GG, et al. Dynamin-2 regulates postsynaptic cytoskeleton organization and neuromuscular junction development. Cell Rep. 2020;33(4):108310. doi:10.1016/j.celrep.2020.108310
Schiffer M, Teng B, Gu C, et al. Pharmacological targeting of actin-dependent dynamin oligomerization ameliorates chronic kidney disease in diverse animal models. Nat Med. 2015;21(6):601-609. doi:10.1038/nm.3843
Zhang R, Lee DM, Jimah JR, et al. Dynamin regulates the dynamics and mechanical strength of the actin cytoskeleton as a multifilament actin-bundling protein. Nat Cell Biol. 2020;22(6):674-688. doi:10.1038/s41556-020-0519-7
Tanifuji S, Funakoshi-Tago M, Ueda F, Kasahara T, Mochida S. Dynamin isoforms decode action potential firing for synaptic vesicle recycling. J Biol Chem. 2013;288(26):19050-19059. doi:10.1074/jbc.M112.445874
Bhatnagar A, Willins DL, Gray JA, Woods J, Benovic JL, Roth BL. The dynamin-dependent, arrestin-independent internalization of 5-hydroxytryptamine 2A (5-HT2A) serotonin receptors reveals differential sorting of arrestins and 5-HT2A receptors during endocytosis. J Biol Chem. 2001;276(11):8269-8277. doi:10.1074/jbc.M006968200
Carroll RC, Beattie EC, Xia H, et al. Dynamin-dependent endocytosis of ionotropic glutamate receptors. Proc Natl Acad Sci U S A. 1999;96(24):14112-14117. doi:10.1073/pnas.96.24.14112
Kabbani N, Jeromin A, Levenson R. Dynamin-2 associates with the dopamine receptor signalplex and regulates internalization of activated D2 receptors. Cell Signal. 2004;16(4):497-503. doi:10.1016/j.cellsig.2003.09.011
Wang W, Ju YY, Zhou QX, et al. The small GTPase Rac1 contributes to extinction of aversive memories of drug withdrawal by facilitating GABAA receptor endocytosis in the vmPFC. J Neurosci. 2017;37(30):7096-7110. doi:10.1523/JNEUROSCI.3859-16.2017
Jaskolski F, Mayo-Martin B, Jane D, Henley JM. Dynamin-dependent membrane drift recruits AMPA receptors to dendritic spines. J Biol Chem. 2009;284(18):12491-12503. doi:10.1074/jbc.M808401200
Chowdhury S, Shepherd JD, Okuno H, et al. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron. 2006;52(3):445-459. doi:10.1016/j.neuron.2006.08.033
Lu J, Helton TD, Blanpied TA, et al. Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer. Neuron. 2007;55(6):874-889. doi:10.1016/j.neuron.2007.06.041
Zheng N, Jeyifous O, Munro C, Montgomery JM, Green WN. Synaptic activity regulates AMPA receptor trafficking through different recycling pathways. Elife. 2015;4:4. doi:10.7554/eLife.06878
Okamoto PM, Gamby C, Wells D, Fallon J, Vallee RB. Dynamin isoform-specific interaction with the shank/ProSAP scaffolding proteins of the postsynaptic density and actin cytoskeleton. J Biol Chem. 2001;276(51):48458-48465. doi:10.1074/jbc.M104927200
Ferguson SM, Raimondi A, Paradise S, et al. Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev Cell. 2009;17(6):811-822. doi:10.1016/j.devcel.2009.11.005
Ferguson SM, Brasnjo G, Hayashi M, et al. A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science. 2007;316(5824):570-574. doi:10.1126/science.1140621
Raimondi A, Ferguson SM, Lou X, et al. Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron. 2011;70(6):1100-1114. doi:10.1016/j.neuron.2011.04.031
Ali T, Bednarska J, Vassilopoulos S, et al. Correlative SICM-FCM reveals changes in morphology and kinetics of endocytic pits induced by disease-associated mutations in dynamin. FASEB J. 2019;33(7):8504-8518. doi:10.1096/fj.201802635R
Bitoun M, Maugenre S, Jeannet PY, et al. Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat Genet. 2005;37(11):1207-1209. doi:10.1038/ng1657
Bohm J, Biancalana V, Dechene ET, et al. Mutation spectrum in the large GTPase dynamin 2, and genotype-phenotype correlation in autosomal dominant centronuclear myopathy. Hum Mutat. 2012;33(6):949-959. doi:10.1002/humu.22067
Koutsopoulos OS, Koch C, Tosch V, Bohm J, North KN, Laporte J. Mild functional differences of dynamin 2 mutations associated to centronuclear myopathy and Charcot-Marie tooth peripheral neuropathy. PLoS ONE. 2011;6(11):e27498. doi:10.1371/journal.pone.0027498
Liu YW, Lukiyanchuk V, Schmid SL. Common membrane trafficking defects of disease-associated dynamin 2 mutations. Traffic. 2011;12(11):1620-1633. doi:10.1111/j.1600-0854.2011.01250.x
Sambuughin N, Goldfarb LG, Sivtseva TM, et al. Adult-onset autosomal dominant spastic paraplegia linked to a GTPase-effector domain mutation of dynamin 2. BMC Neurol. 2015;15(1):223. doi:10.1186/s12883-015-0481-3
Tanabe K, Takei K. Dynamic instability of microtubules requires dynamin 2 and is impaired in a Charcot-Marie-tooth mutant. J Cell Biol. 2009;185(6):939-948. doi:10.1083/jcb.200803153
Fischer D, Herasse M, Bitoun M, et al. Characterization of the muscle involvement in dynamin 2-related centronuclear myopathy. Brain. 2006;129(6):1463-1469. doi:10.1093/brain/awl071
Jeannet PY, Bassez G, Eymard B, et al. Clinical and histologic findings in autosomal centronuclear myopathy. Neurology. 2004;62(9):1484-1490. doi:10.1212/01.WNL.0000124388.67003.56
Echaniz-Laguna A, Nicot AS, Carre S, et al. Subtle central and peripheral nervous system abnormalities in a family with centronuclear myopathy and a novel dynamin 2 gene mutation. Neuromuscul Disord. 2007;17(11-12):955-959. doi:10.1016/j.nmd.2007.06.467
Durieux AC, Vassilopoulos S, Laine J, et al. A centronuclear myopathy-dynamin 2 mutation impairs autophagy in mice. Traffic. 2012;13(6):869-879. doi:10.1111/j.1600-0854.2012.01348.x
Durieux AC, Vignaud A, Prudhon B, et al. A centronuclear myopathy-dynamin 2 mutation impairs skeletal muscle structure and function in mice. Hum Mol Genet. 2010;19(24):4820-4836. doi:10.1093/hmg/ddq413
Ardiles AO, Flores-Munoz C, Toro-Ayala G, et al. Pannexin 1 regulates bidirectional hippocampal synaptic plasticity in adult mice. Front Cell Neurosci. 2014;8:326. doi:10.3389/fncel.2014.00326
Ardiles AO, Tapia-Rojas CC, Mandal M, et al. Postsynaptic dysfunction is associated with spatial and object recognition memory loss in a natural model of Alzheimer's disease. Proc Natl Acad Sci U S A. 2012;109(34):13835-13840. doi:10.1073/pnas.1201209109
Flores-Munoz C, Gomez B, Mery E, et al. Acute Pannexin 1 blockade mitigates early synaptic plasticity defects in a mouse model of Alzheimer's disease. Front Cell Neurosci. 2020;14:46. doi:10.3389/fncel.2020.00046
Gajardo I, Salazar CS, Lopez-Espindola D, et al. Lack of Pannexin 1 alters synaptic GluN2 subunit composition and spatial reversal learning in mice. Front Mol Neurosci. 2018;11:114. doi:10.3389/fnmol.2018.00114
Zhang XY, Ji F, Wang N, Chen LL, Tian T, Lu W. Glycine induces bidirectional modifications in N-methyl-D-aspartate receptor-mediated synaptic responses in hippocampal CA1 neurons. J Biol Chem. 2014;289(45):31200-31211. doi:10.1074/jbc.M114.570630
Beaudoin GM 3rd, Lee SH, Singh D, et al. Culturing pyramidal neurons from the early postnatal mouse hippocampus and cortex. Nat Protoc. 2012;7(9):1741-1754. doi:10.1038/nprot.2012.099
Trochet D, Prudhon B, Beuvin M, et al. Allele-specific silencing therapy for dynamin 2-related dominant centronuclear myopathy. EMBO Mol Med. 2018;10(2):239-253. doi:10.15252/emmm.201707988
Flores-Munoz C, Garcia-Rojas F, Perez MA, et al. The long-term Pannexin 1 ablation produces structural and functional modifications in hippocampal neurons. Cell. 2022;11(22):11. doi:10.3390/cells11223646
Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol. 1993;234(3):779-815. doi:10.1006/jmbi.1993.1626
Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, de Vries AH. The MARTINI force field: coarse grained model for biomolecular simulations. J Phys Chem B. 2007;111(27):7812-7824. doi:10.1021/jp071097f
Monticelli L, Kandasamy SK, Periole X, Larson RG, Tieleman DP, Marrink SJ. The MARTINI coarse-grained force field: extension to proteins. J Chem Theory Comput. 2008;4(5):819-834. doi:10.1021/ct700324x
Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph. 1996;14:33-38, 27-8. doi:10.1016/0263-7855(96)00018-5
Jo S, Kim T, Iyer VG, Im W. CHARMM-GUI: a web-based graphical user interface for CHARMM. J Comput Chem. 2008;29(11):1859-1865. doi:10.1002/jcc.20945
Qi Y, Cheng X, Han W, Jo S, Schulten K, Im W. CHARMM-GUI PACE CG builder for solution, micelle, and bilayer coarse-grained simulations. J Chem Inf Model. 2014;54(3):1003-1009. doi:10.1021/ci500007n
Lee J, Cheng X, Swails JM, et al. CHARMM-GUI input generator for NAMD, GROMACS, AMBER, OpenMM, and CHARMM/OpenMM simulations using the CHARMM36 additive force field. J Chem Theory Comput. 2016;12(1):405-413. doi:10.1021/acs.jctc.5b00935
Lee J, Hitzenberger M, Rieger M, Kern NR, Zacharias M, Im W. CHARMM-GUI supports the amber force fields. J Chem Phys. 2020;153(3):035103. doi:10.1063/5.0012280
Tian C, Kasavajhala K, Belfon KAA, et al. ff19SB: amino-acid-specific protein backbone parameters trained against quantum mechanics energy surfaces in solution. J Chem Theory Comput. 2020;16(1):528-552. doi:10.1021/acs.jctc.9b00591
Hinostroza F, Neely A, Araya-Duran I, et al. Dynamin-2 R465W mutation induces long range perturbation in highly ordered oligomeric structures. Sci Rep. 2020;10(1):18151. doi:10.1038/s41598-020-75216-0
Gray NW, Kruchten AE, Chen J, McNiven MA. A dynamin-3 spliced variant modulates the actin/cortactin-dependent morphogenesis of dendritic spines. J Cell Sci. 2005;118(6):1279-1290. doi:10.1242/jcs.01711
Itoh K, Murata D, Kato T, et al. Brain-specific Drp1 regulates postsynaptic endocytosis and dendrite formation independently of mitochondrial division. Elife. 2019;8:8. doi:10.7554/eLife.44739
Kurklinsky S, Chen J, McNiven MA. Growth cone morphology and spreading are regulated by a dynamin-cortactin complex at point contacts in hippocampal neurons. J Neurochem. 2011;117(1):48-60. doi:10.1111/j.1471-4159.2011.07169.x
Bayonés L, Alfonso-Bueno S, Montenegro M, et al. Membrane retrieval after immediately releasable pool (IRP) exocytosis is produced by dynamin-dependent and dynamin-independent/protein kinase C-dependent mechanisms. J Neurochem. 2022;163(5):391-405. doi:10.1111/jnc.15710
Gonzalez-Jamett AM, Baez-Matus X, Olivares MJ, et al. Dynamin-2 mutations linked to centronuclear myopathy impair actin-dependent trafficking in muscle cells. Sci Rep. 2017;7(1):4580. doi:10.1038/s41598-017-04418-w
Koleske AJ. Molecular mechanisms of dendrite stability. Nat Rev Neurosci. 2013;14(8):536-550. doi:10.1038/nrn3486
Nicoll RA, Schmitz D. Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci. 2005;6(11):863-876. doi:10.1038/nrn1786
Zhang J, Xia J, Xiong H. Techniques for extracellular recordings. In: Xiong H, Gendelman HE, eds. Current Laboratory Methods in Neuroscience Research. Springer New York; 2014:325-345.
Shors TJ, Matzel LD. Long-term potentiation: what's learning got to do with it? Behav Brain Sci. 1997;20(4):597-614; discussion -55. doi:10.1017/S0140525X97001593
Lüscher CaM RC. NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol. 2012;4(6):a005710. doi:10.1101/cshperspect.a005710
Bayazitov IT, Richardson RJ, Fricke RG, Zakharenko SS. Slow presynaptic and fast postsynaptic components of compound long-term potentiation. J Neurosci. 2007;27(43):11510-11521. doi:10.1523/JNEUROSCI.3077-07.2007
Citri AaM RC. Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology. 2008;33(1):18-41. doi:10.1038/sj.npp.1301559
Anggono V, Huganir RL. Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol. 2012;22(3):461-469. doi:10.1016/j.conb.2011.12.006
Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol. 2002;64(1):355-405. doi:10.1146/annurev.physiol.64.092501.114547
Lu W, Man H, Ju W, Trimble WS, MacDonald JF, Wang YT. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron. 2001;29(1):243-254. doi:10.1016/S0896-6273(01)00194-5
Collingridge GL, Peineau S, Howland JG, Wang YT. Long term depression in the CNS. Nat Rev Neurosci. 2010;11(7):459-473. doi:10.1038/nrn2867
Ge Y, Dong Z, Bagot RC, et al. Hippocampal long-term depression is required for the consolidation of spatial memory. Proc Natl Acad Sci U S A. 2010;107(38):16697-16702. doi:10.1073/pnas.1008200107
Martin SJ, Grimwood PD, Morris RG. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci. 2000;23(1):649-711. doi:10.1146/annurev.neuro.23.1.649
Ennaceur A, Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data. Behav Brain Res. 1988;31(1):47-59. doi:10.1016/0166-4328(88)90157-X
Barnes CA. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol. 1979;93(1):74-104. doi:10.1037/h0077579
Negron-Oyarzo I, Neira D, Espinosa N, Fuentealba P, Aboitiz F. Prenatal stress produces persistence of remote memory and disrupts functional connectivity in the hippocampal-prefrontal cortex axis. Cereb Cortex. 2015;25(9):3132-3143. doi:10.1093/cercor/bhu108
Pitts MW. Barnes maze procedure for spatial learning and memory in mice. Bio Protoc. 2018;8(5):8. doi:10.21769/BioProtoc.2744
Shin W, Ge L, Arpino G, et al. Visualization of membrane pore in live cells reveals a dynamic-pore theory governing fusion and endocytosis. Cell. 2018;173:934-45.e12. doi:10.1016/j.cell.2018.02.062
Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol. 1994;127(4):915-934. doi:10.1083/jcb.127.4.915
Loerke D, Mettlen M, Yarar D, et al. Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol. 2009;7(3):e57. doi:10.1371/journal.pbio.1000057
van der Bliek AM, Redelmeier TE, Damke H, Tisdale EJ, Meyerowitz EM, Schmid SL. Mutations in human dynamin block an intermediate stage in coated vesicle formation. J Cell Biol. 1993;122(3):553-563. doi:10.1083/jcb.122.3.553
Nicoziani P, Vilhardt F, Llorente A, et al. Role for dynamin in late endosome dynamics and trafficking of the cation-independent mannose 6-phosphate receptor. Mol Biol Cell. 2000;11(2):481-495. doi:10.1091/mbc.11.2.481
Mooren OL, Kotova TI, Moore AJ, Schafer DA. Dynamin2 GTPase and cortactin remodel actin filaments. J Biol Chem. 2009;284(36):23995-24005. doi:10.1074/jbc.M109.024398
Yamada H, Takeda T, Michiue H, Abe T, Takei K. Actin bundling by dynamin 2 and cortactin is implicated in cell migration by stabilizing filopodia in human non-small cell lung carcinoma cells. Int J Oncol. 2016;49(3):877-886. doi:10.3892/ijo.2016.3592
Gu C, Chang J, Shchedrina VA, et al. Regulation of dynamin oligomerization in cells: the role of dynamin-actin interactions and its GTPase activity. Traffic. 2014;15(8):819-838. doi:10.1111/tra.12178
Bosch M, Castro J, Saneyoshi T, Matsuno H, Sur M, Hayashi Y. Structural and molecular remodeling of dendritic spine substructures during long-term potentiation. Neuron. 2014;82(2):444-459. doi:10.1016/j.neuron.2014.03.021
Okamoto K, Nagai T, Miyawaki A, Hayashi Y. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci. 2004;7(10):1104-1112. doi:10.1038/nn1311
Kevenaar JT, Hoogenraad CC. The axonal cytoskeleton: from organization to function. Front Mol Neurosci. 2015;8:44.
Konietzny A, Bar J, Mikhaylova M. Dendritic actin cytoskeleton: structure, functions, and regulations. Front Cell Neurosci. 2017;11:147. doi:10.3389/fncel.2017.00147
Gordon-Weeks PR, Fournier AE. Neuronal cytoskeleton in synaptic plasticity and regeneration. J Neurochem. 2014;129(2):206-212. doi:10.1111/jnc.12502
Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD. Recycling endosomes supply AMPA receptors for LTP. Science. 2004;305(5692):1972-1975. doi:10.1126/science.1102026
Man HY, Lin JW, Ju WH, et al. Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron. 2000;25(3):649-662. doi:10.1016/S0896-6273(00)81067-3
Castillo PE. Presynaptic LTP and LTD of excitatory and inhibitory synapses. Cold Spring Harb Perspect Biol. 2012;4(2):4. doi:10.1101/cshperspect.a005728
Cheung G, Cousin MA. Synaptic vesicle generation from activity-dependent bulk endosomes requires a dephosphorylation-dependent dynamin-syndapin interaction. J Neurochem. 2019;151(5):570-583. doi:10.1111/jnc.14862
Watanabe S, Liu Q, Davis MW, et al. Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions. Elife. 2013;2:e00723. doi:10.7554/eLife.00723
Moya-Diaz J, Alvarez YD, Montenegro M, et al. Sustained exocytosis after action potential-like stimulation at Low frequencies in mouse chromaffin cells depends on a dynamin-dependent fast endocytotic process. Front Cell Neurosci. 2016;10:184. doi:10.3389/fncel.2016.00184
Moro A, van Nifterick A, Toonen RF, Verhage M. Dynamin controls neuropeptide secretion by organizing dense-core vesicle fusion sites. Sci Adv. 2021;7(21):7. doi:10.1126/sciadv.abf0659
Lee HK, Kameyama K, Huganir RL, Bear MF. NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron. 1998;21(5):1151-1162. doi:10.1016/S0896-6273(00)80632-7
Bach ME, Hawkins RD, Osman M, Kandel ER, Mayford M. Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell. 1995;81(6):905-915. doi:10.1016/0092-8674(95)90010-1
Lynch MA. Long-term potentiation and memory. Physiol Rev. 2004;84(1):87-136. doi:10.1152/physrev.00014.2003
Dong Z, Bai Y, Wu X, et al. Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze. Neuropharmacology. 2013;64:65-73. doi:10.1016/j.neuropharm.2012.06.027
Manahan-Vaughan D, Braunewell KH. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci U S A. 1999;96(15):8739-8744. doi:10.1073/pnas.96.15.8739
Mills F, Bartlett TE, Dissing-Olesen L, et al. Cognitive flexibility and long-term depression (LTD) are impaired following beta-catenin stabilization in vivo. Proc Natl Acad Sci U S A. 2014;111(23):8631-8636. doi:10.1073/pnas.1404670111
Nicholls RE, Alarcon JM, Malleret G, et al. Transgenic mice lacking NMDAR-dependent LTD exhibit deficits in behavioral flexibility. Neuron. 2008;58(1):104-117. doi:10.1016/j.neuron.2008.01.039
Kemp A, Manahan-Vaughan D. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci U S A. 2004;101(21):8192-8197. doi:10.1073/pnas.0402650101
Romero NB, Bitoun M. Centronuclear myopathies. Semin Pediatr Neurol. 2011;18(4):250-256. doi:10.1016/j.spen.2011.10.006
Hayes LH, Perdomini M, Aykanat A, et al. Phenotypic spectrum of DNM2-related centronuclear myopathy. Neurol Genet. 2022;8(6):e200027. doi:10.1212/NXG.0000000000200027
Reumers SFI, Erasmus CE, Bouman K, et al. Clinical, genetic, and histological features of centronuclear myopathy in the Netherlands. Clin Genet. 2021;100(6):692-702. doi:10.1111/cge.14054
Verma S, Balasubramanian SB. Clinical, electrophysiology, and pathology features of dynamin centronuclear myopathy: a case report and review of literature. J Clin Neuromuscul Dis. 2016;18(2):84-88. doi:10.1097/CND.0000000000000141
Brown MW, Aggleton JP. Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci. 2001;2(1):51-61. doi:10.1038/35049064
Burgess N, Maguire EA, O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron. 2002;35(4):625-641. doi:10.1016/S0896-6273(02)00830-9
Negron-Oyarzo I, Espinosa N, Aguilar-Rivera M, Fuenzalida M, Aboitiz F, Fuentealba P. Coordinated prefrontal-hippocampal activity and navigation strategy-related prefrontal firing during spatial memory formation. Proc Natl Acad Sci U S A. 2018;115(27):7123-7128. doi:10.1073/pnas.1720117115
Jo YS, Park EH, Kim IH, et al. The medial prefrontal cortex is involved in spatial memory retrieval under partial-cue conditions. J Neurosci. 2007;27(49):13567-13578. doi:10.1523/JNEUROSCI.3589-07.2007
Winters BD, Bussey TJ. Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. J Neurosci. 2005;25(1):52-61. doi:10.1523/JNEUROSCI.3827-04.2005
Warburton EC, Brown MW. Findings from animals concerning when interactions between perirhinal cortex, hippocampus and medial prefrontal cortex are necessary for recognition memory. Neuropsychologia. 2010;48(8):2262-2272. doi:10.1016/j.neuropsychologia.2009.12.022
Haskins AL, Yonelinas AP, Quamme JR, Ranganath C. Perirhinal cortex supports encoding and familiarity-based recognition of novel associations. Neuron. 2008;59(4):554-560. doi:10.1016/j.neuron.2008.07.035
Chawla A, Cordner ZA, Boersma G, Moran TH. Cognitive impairment and gene expression alterations in a rodent model of binge eating disorder. Physiol Behav. 2017;180:78-90. doi:10.1016/j.physbeh.2017.08.004
Crews FT, Boettiger CA. Impulsivity, frontal lobes and risk for addiction. Pharmacol Biochem Behav. 2009;93(3):237-247. doi:10.1016/j.pbb.2009.04.018