Serotonin 5-HT
Actin Cytoskeleton
/ metabolism
Actins
/ metabolism
Animals
Animals, Newborn
Cells, Cultured
Dendritic Spines
/ physiology
Female
Long-Term Potentiation
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Neurons
/ metabolism
Rats
Rats, Sprague-Dawley
Receptors, Serotonin, 5-HT4
/ genetics
Signal Transduction
/ genetics
Synapses
/ physiology
Synaptic Transmission
/ physiology
rhoA GTP-Binding Protein
/ physiology
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
14 02 2020
14 02 2020
Historique:
received:
15
11
2018
accepted:
23
01
2020
entrez:
16
2
2020
pubmed:
16
2
2020
medline:
22
6
2021
Statut:
epublish
Résumé
Activity-dependent remodeling of excitatory connections underpins memory formation in the brain. Serotonin receptors are known to contribute to such remodeling, yet the underlying molecular machinery remains poorly understood. Here, we employ high-resolution time-lapse FRET imaging in neuroblastoma cells and neuronal dendrites to establish that activation of serotonin receptor 5-HT
Identifiants
pubmed: 32060357
doi: 10.1038/s42003-020-0791-x
pii: 10.1038/s42003-020-0791-x
pmc: PMC7021812
doi:
Substances chimiques
Actins
0
Receptors, Serotonin, 5-HT4
158165-40-3
RhoA protein, mouse
EC 3.6.5.2
rhoA GTP-Binding Protein
EC 3.6.5.2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
76Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 101896/Z/13/Z
Pays : United Kingdom
Références
Ethell, I. M. & Pasquale, E. B. Molecular mechanisms of dendritic spine development and remodeling. Prog. Neurobiol. 75, 161–205 (2005).
pubmed: 15882774
doi: 10.1016/j.pneurobio.2005.02.003
pmcid: 15882774
Sekino, Y., Kojima, N. & Shirao, T. Role of actin cytoskeleton in dendritic spine morphogenesis. Neurochem. Int. 51, 92–104 (2007).
pubmed: 17590478
doi: 10.1016/j.neuint.2007.04.029
pmcid: 17590478
Honkura, N., Matsuzaki, M., Noguchi, J., Ellis-Davies, G. C. R. & Kasai, H. The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 57, 719–729 (2008).
pubmed: 18341992
doi: 10.1016/j.neuron.2008.01.013
pmcid: 18341992
Nakayama, A. Y., Harms, M. B. & Luo, L. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J. Neurosci. 20, 5329–5338 (2000).
pubmed: 10884317
pmcid: 6772334
doi: 10.1523/JNEUROSCI.20-14-05329.2000
Tashiro, A., Minden, A. & Yuste, R. Regulation of dendritic spine morphology by the Rho family of small GTPases: antagonistic roles of Rac and Rho. Cereb. Cortex 10, 927–938 (2000).
pubmed: 11007543
doi: 10.1093/cercor/10.10.927
pmcid: 11007543
Jalink, K. et al. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126, 801–810 (1994).
pubmed: 8045941
doi: 10.1083/jcb.126.3.801
pmcid: 8045941
Kozma, R., Sarner, S., Ahmed, S. & Lim, L. Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 17, 1201–1211 (1997).
pubmed: 9032247
pmcid: 231845
doi: 10.1128/MCB.17.3.1201
Luo, L., Liao, Y. J., Jan, L. Y. & Jan, Y. N. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787–1802 (1994).
pubmed: 7958857
doi: 10.1101/gad.8.15.1787
pmcid: 7958857
Bijata, M., Wlodarczyk, J. & Figiel, I. Dystroglycan controls dendritic morphogenesis of hippocampal neurons in vitro. Front. Cell. Neurosci. https://doi.org/10.3389/fncel.2015.00199 (2015).
Rosário, M. et al. Neocortical dendritic complexity is controlled during development by NOMA-GAP-dependent inhibition of Cdc42 and activation of cofilin. Genes Dev. 26, 1743–1757 (2012).
pubmed: 22810622
pmcid: 3418591
doi: 10.1101/gad.191593.112
Ma, Q.-L. et al. p21-activated kinase-aberrant activation and translocation in Alzheimer disease pathogenesis. J. Biol. Chem. 283, 14132–14143 (2008).
pubmed: 18347024
pmcid: 2376243
doi: 10.1074/jbc.M708034200
Ide, M. & Lewis, D. A. Altered cortical CDC42 signaling pathways in schizophrenia: implications for dendritic spine deficits. Biol. Psychiatry 68, 25–32 (2010).
pubmed: 20385374
pmcid: 2900524
doi: 10.1016/j.biopsych.2010.02.016
Xiao, F. et al. Overexpression of N-WASP in the brain of human epilepsy. Brain Res. 1233, 168–175 (2008).
pubmed: 18708039
doi: 10.1016/j.brainres.2008.07.101
pmcid: 18708039
Yuan, J. et al. Altered expression of the small guanosine triphosphatase RhoA in human temporal lobe epilepsy. J. Mol. Neurosci. 42, 53–58 (2010).
pubmed: 20140537
doi: 10.1007/s12031-010-9330-4
pmcid: 20140537
Carlier, M. F. et al. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J. Cell Biol. 136, 1307–1322 (1997).
pubmed: 9087445
pmcid: 2132522
doi: 10.1083/jcb.136.6.1307
Chan, A. Y., Bailly, M., Zebda, N., Segall, J. E. & Condeelis, J. S. Role of cofilin in epidermal growth factor-stimulated actin polymerization and lamellipod protrusion. J. Cell Biol. 148, 531–542 (2000).
pubmed: 10662778
pmcid: 2174812
doi: 10.1083/jcb.148.3.531
DesMarais, V., Ghosh, M., Eddy, R. & Condeelis, J. Cofilin takes the lead. J. Cell Sci. 118, 19–26 (2005).
pubmed: 15615780
doi: 10.1242/jcs.01631
pmcid: 15615780
Bamburg, J. R. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15, 185–230 (1999).
pubmed: 10611961
doi: 10.1146/annurev.cellbio.15.1.185
pmcid: 10611961
Bernstein, B. W. & Bamburg, J. R. ADF/Cofilin: a functional node in cell biology. Trends Cell Biol. 20, 187–195 (2010).
pubmed: 20133134
pmcid: 2849908
doi: 10.1016/j.tcb.2010.01.001
Noguchi, J. et al. State-dependent diffusion of actin-depolymerizing factor/cofilin underlies the enlargement and shrinkage of dendritic spines. Sci. Rep. 6, 32897 (2016).
pubmed: 27595610
pmcid: 5011767
doi: 10.1038/srep32897
Ponimaskin, E. G., Profirovic, J., Vaiskunaite, R., Richter, D. W. & Voyno-Yasenetskaya, T. A. 5-Hydroxytryptamine 4(a) receptor is coupled to the Gα subunit of heterotrimeric G13 protein. J. Biol. Chem. 277, 20812–20819 (2002).
pubmed: 11923294
doi: 10.1074/jbc.M112216200
pmcid: 11923294
Cavaccini, A. et al. Serotonergic signaling controls input-specific synaptic plasticity at striatal circuits. Neuron 98, 801–816.e7 (2018).
pubmed: 29706583
doi: 10.1016/j.neuron.2018.04.008
pmcid: 29706583
Eglen, R. M., Wong, E. H. F., Dumuis, A. & Bockaert, J. Central 5-HT4 receptors. Trends Pharmacol. Sci. 16, 391–398 (1995).
pubmed: 8578609
doi: 10.1016/S0165-6147(00)89081-1
pmcid: 8578609
Marchetti, E. et al. Enhancement of reference memory in aged rats by specific activation of 5-HT(4) receptors using an olfactory associative discrimination task. Brain Res. 1405, 49–56 (2011).
pubmed: 21745655
doi: 10.1016/j.brainres.2011.06.020
pmcid: 21745655
Marchetti-Gauthier, E., Roman, F. S., Dumuis, A., Bockaert, J. & Soumireu-Mourat, B. BIMU1 increases associative memory in rats by activating 5-HT4 receptors. Neuropharmacology 36, 697–706 (1997).
pubmed: 9225296
doi: 10.1016/S0028-3908(97)00058-0
pmcid: 9225296
Wong, E. H., Reynolds, G. P., Bonhaus, D. W., Hsu, S. & Eglen, R. M. Characterization of [3H]GR 113808 binding to 5-HT4 receptors in brain tissues from patients with neurodegenerative disorders. Behav. Brain Res. 73, 249–252 (1996).
pubmed: 8788512
doi: 10.1016/0166-4328(96)00106-4
pmcid: 8788512
Kvachnina, E. et al. 5-HT7 receptor is coupled to Gα subunits of heterotrimeric G12-protein to regulate gene transcription and neuronal morphology. J. Neurosci. 25, 7821–7830 (2005).
pubmed: 16120784
pmcid: 6725246
doi: 10.1523/JNEUROSCI.1790-05.2005
Komatsu, N. et al. Development of an optimized backbone of FRET biosensors for kinases and GTPases. Mol. Biol. Cell 22, 4647–4656 (2011).
pubmed: 21976697
pmcid: 3226481
doi: 10.1091/mbc.e11-01-0072
Kranenburg, O., Poland, M., Gebbink, M., Oomen, L. & Moolenaar, W. H. Dissociation of LPA-induced cytoskeletal contraction from stress fiber formation by differential localization of RhoA. J. Cell Sci. 110, 2417–2427 (1997).
pubmed: 9410880
pmcid: 9410880
Kranenburg, O. et al. Activation of RhoA by lysophosphatidic acid and Gα12/13 subunits in neuronal cells: induction of neurite retraction. Mol. Biol. Cell 10, 1851–1857 (1999).
pubmed: 10359601
pmcid: 25381
doi: 10.1091/mbc.10.6.1851
Endo, M. et al. Control of Growth Cone Motility and Morphology by LIM Kinase and Slingshot via Phosphorylation and Dephosphorylation of Cofilin. J. Neurosci. 23, 2527–2537 (2003).
pubmed: 12684437
pmcid: 6742113
doi: 10.1523/JNEUROSCI.23-07-02527.2003
Flynn, K. C. et al. ADF/Cofilin-mediated actin retrograde flow directs neurite formation in the developing brain. Neuron 76, 1091–1107 (2012).
pubmed: 23259946
doi: 10.1016/j.neuron.2012.09.038
pmcid: 23259946
Bijata, M. et al. Synaptic remodeling depends on signaling between serotonin receptors and the extracellular matrix. Cell Rep. 19, 1767–1782 (2017).
pubmed: 28564597
doi: 10.1016/j.celrep.2017.05.023
pmcid: 28564597
Riedl, J. et al. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5, 605–607 (2008).
pubmed: 18536722
pmcid: 2814344
doi: 10.1038/nmeth.1220
Gähwiler, B. H., Capogna, M., Debanne, D., McKinney, R. A. & Thompson, S. M. Organotypic slice cultures: a technique has come of age. Trends Neurosci. 20, 471–477 (1997).
pubmed: 9347615
doi: 10.1016/S0166-2236(97)01122-3
Gogolla, N., Galimberti, I., DePaola, V. & Caroni, P. Preparation of organotypic hippocampal slice cultures for long-term live imaging. Nat. Protoc. 1, 1165–1171 (2006).
pubmed: 17406399
doi: 10.1038/nprot.2006.168
Mlinar, B., Pugliese, A. M. & Corradetti, R. Selective inhibition of local excitatory synaptic transmission by serotonin through an unconventional receptor in the CA1 region of rat hippocampus. J. Physiol. 534, 141–158 (2001).
pubmed: 11432998
pmcid: 2278682
doi: 10.1111/j.1469-7793.2001.t01-2-00141.x
Mlinar, B., Mascalchi, S., Mannaioni, G., Morini, R. & Corradetti, R. 5-HT4 receptor activation induces long-lasting EPSP-spike potentiation in CA1 pyramidal neurons. Eur. J. Neurosci. 24, 719–731 (2006).
pubmed: 16930402
doi: 10.1111/j.1460-9568.2006.04949.x
pmcid: 16930402
Kobe, F. et al. 5-HT7R/G12 Signaling regulates neuronal morphology and function in an age-dependent manner. J. Neurosci. 32, 2915–2930 (2012).
pubmed: 22378867
pmcid: 3369253
doi: 10.1523/JNEUROSCI.2765-11.2012
Luo, L. Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity. Annu. Rev. Cell Dev. Biol. 18, 601–635 (2002).
pubmed: 12142283
doi: 10.1146/annurev.cellbio.18.031802.150501
pmcid: 12142283
Hotulainen, P. & Hoogenraad, C. C. Actin in dendritic spines: connecting dynamics to function. J. Cell Biol. 189, 619–629 (2010).
pubmed: 20457765
pmcid: 2872912
doi: 10.1083/jcb.201003008
Lappalainen, P. & Drubin, D. G. Cofilin promotes rapid actin filament turnover in vivo. Nature 388, 78–82 (1997).
pubmed: 9214506
doi: 10.1038/40418
pmcid: 9214506
Maekawa, M. et al. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285, 895–898 (1999).
pubmed: 10436159
doi: 10.1126/science.285.5429.895
pmcid: 10436159
Moriyama, K., Iida, K. & Yahara, I. Phosphorylation of Ser-3 of cofilin regulates its essential function on actin. Genes Cells Devoted Mol. Cell. Mech. 1, 73–86 (1996).
doi: 10.1046/j.1365-2443.1996.05005.x
Niwa, R., Nagata-Ohashi, K., Takeichi, M., Mizuno, K. & Uemura, T. Control of actin reorganization by Slingshot, a family of phosphatases that dephosphorylate ADF/cofilin. Cell 108, 233–246 (2002).
pubmed: 11832213
doi: 10.1016/S0092-8674(01)00638-9
pmcid: 11832213
Ponimaskin, E. G. et al. The 5-hydroxytryptamine(4a) receptor is palmitoylated at two different sites, and acylation is critically involved in regulation of receptor constitutive activity. J. Biol. Chem. 277, 2534–2546 (2002).
pubmed: 11706023
doi: 10.1074/jbc.M106529200
pmcid: 11706023
Corset, V. et al. Netrin-1-mediated axon outgrowth and cAMP production requires interaction with adenosine A2b receptor. Nature 407, 747–750 (2000).
pubmed: 11048721
doi: 10.1038/35037600
pmcid: 11048721
Couvillon, A. D. & Exton, J. H. Role of heterotrimeric G-proteins in lysophosphatidic acid-mediated neurite retraction by RhoA-dependent and -independent mechanisms in N1E-115 cells. Cell. Signal. 18, 715–728 (2006).
pubmed: 16122906
doi: 10.1016/j.cellsig.2005.06.012
pmcid: 16122906
Iyengar, R. Gating by cyclic AMP: expanded role for an old signaling pathway. Science 271, 461–463 (1996).
pubmed: 8560257
doi: 10.1126/science.271.5248.461
pmcid: 8560257
Yu, J.-Z., Dave, R. H., Allen, J. A., Sarma, T. & Rasenick, M. M. Cytosolic G s Acts as an intracellular messenger to increase microtubule dynamics and promote neurite outgrowth. J. Biol. Chem. 284, 10462–10472 (2009).
pubmed: 19237344
pmcid: 2667733
doi: 10.1074/jbc.M809166200
Vázquez-Victorio, G., González-Espinosa, C., Espinosa-Riquer, Z. P. & Macías-Silva, M. in Methods in Cell Biology (ed K. Shukla, A.) vol. 132 165–188 (Academic Press, 2016).
Schmidt, M., Dekker, F. J. & Maarsingh, H. Exchange protein directly activated by cAMP (epac): a multidomain cAMP mediator in the regulation of diverse biological functions. Pharmacol. Rev. 65, 670–709 (2013).
pubmed: 23447132
doi: 10.1124/pr.110.003707
pmcid: 23447132
Racz, B. & Weinberg, R. J. Spatial organization of cofilin in dendritic spines. Neuroscience 138, 447–456 (2006).
pubmed: 16388910
doi: 10.1016/j.neuroscience.2005.11.025
pmcid: 16388910
Shi, Y., Pontrello, C. G., DeFea, K. A., Reichardt, L. F. & Ethell, I. M. Focal adhesion kinase acts downstream of EphB receptors to maintain mature dendritic spines by regulating cofilin activity. J. Neurosci. 29, 8129–8142 (2009).
pubmed: 19553453
pmcid: 2819391
doi: 10.1523/JNEUROSCI.4681-08.2009
Gu, J. et al. ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat. Neurosci. 13, 1208–1215 (2010).
pubmed: 20835250
pmcid: 2947576
doi: 10.1038/nn.2634
Zhou, Q., Homma, K. J. & Poo, M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44, 749–757 (2004).
pubmed: 15572107
doi: 10.1016/j.neuron.2004.11.011
pmcid: 15572107
Da Silva, J. S. & Dotti, C. G. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat. Rev. Neurosci. 3, 694–704 (2002).
pubmed: 12209118
doi: 10.1038/nrn918
pmcid: 12209118
Moon, S. Y. & Zheng, Y. Rho GTPase-activating proteins in cell regulation. Trends Cell Biol. 13, 13–22 (2003).
pubmed: 12480336
doi: 10.1016/S0962-8924(02)00004-1
pmcid: 12480336
Pertz, O. Spatio-temporal Rho GTPase signaling—where are we now? J. Cell Sci. 123, 1841–1850 (2010).
pubmed: 20484664
doi: 10.1242/jcs.064345
pmcid: 20484664
Rossman, K. L., Der, C. J. & Sondek, J. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6, 167–180 (2005).
pubmed: 15688002
doi: 10.1038/nrm1587
pmcid: 15688002
Fusco, L. et al. Computer vision profiling of neurite outgrowth dynamics reveals spatiotemporal modularity of Rho GTPase signaling. J. Cell Biol. 212, 91–111 (2016).
pubmed: 26728857
pmcid: 4700477
doi: 10.1083/jcb.201506018
Speranza, L. et al. Serotonin 5-HT7 receptor increases the density of dendritic spines and facilitates synaptogenesis in forebrain neurons. J. Neurochem. 141, 647–661 (2017).
pubmed: 28122114
doi: 10.1111/jnc.13962
pmcid: 28122114
Mlinar, B., Mascalchi, S., Mannaioni, G., Morini, R. & Corradetti, R. 5-HT4 receptor activation induces long-lasting EPSP-spike potentiation in CA1 pyramidal neurons. Eur. J. Neurosci. 24, 719–731 (2006).
pubmed: 16930402
doi: 10.1111/j.1460-9568.2006.04949.x
pmcid: 16930402
Matsumoto, M. et al. Evidence for involvement of central 5-HT(4) receptors in cholinergic function associated with cognitive processes: behavioral, electrophysiological, and neurochemical studies. J. Pharmacol. Exp. Ther. 296, 676–682 (2001).
pubmed: 11181892
pmcid: 11181892
Kemp, A. & Manahan-Vaughan, D. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc. Natl Acad. Sci. USA 101, 8192–8197 (2004).
pubmed: 15150407
doi: 10.1073/pnas.0402650101
pmcid: 15150407
Kemp, A. & Manahan-Vaughan, D. The 5-hydroxytryptamine4 receptor exhibits frequency-dependent properties in synaptic plasticity and behavioural metaplasticity in the hippocampal CA1 region in vivo. Cereb. Cortex 15, 1037–1043 (2005).
pubmed: 15537670
doi: 10.1093/cercor/bhh204
pmcid: 15537670
Kulla, A. & Manahan-Vaughan, D. Modulation by serotonin 5-HT(4) receptors of long-term potentiation and depotentiation in the dentate gyrus of freely moving rats. Cereb. Cortex N. Y. N. 1991 12, 150–162 (2002).
Restivo, L. et al. The promnesic effect of G-protein-coupled 5-HT4 receptors activation is mediated by a potentiation of learning-induced spine growth in the mouse hippocampus. Neuropsychopharmacology 33, 2427–2434 (2008).
pubmed: 18075492
doi: 10.1038/sj.npp.1301644
pmcid: 18075492
King, M. V., Marsden, C. A. & Fone, K. C. F. A role for the 5-HT(1A), 5-HT4 and 5-HT6 receptors in learning and memory. Trends Pharmacol. Sci. 29, 482–492 (2008).
pubmed: 19086256
doi: 10.1016/j.tips.2008.07.001
pmcid: 19086256
Lamirault, L. & Simon, H. Enhancement of place and object recognition memory in young adult and old rats by RS 67333, a partial agonist of 5-HT4 receptors. Neuropharmacology 41, 844–853 (2001).
pubmed: 11684148
doi: 10.1016/S0028-3908(01)00123-X
pmcid: 11684148
Lelong, V., Dauphin, F. & Boulouard, M. RS 67333 and D-cycloserine accelerate learning acquisition in the rat. Neuropharmacology 41, 517–522 (2001).
pubmed: 11543772
doi: 10.1016/S0028-3908(01)00085-5
pmcid: 11543772
Marchetti, E. et al. Modulation of memory processes and cellular excitability in the dentate gyrus of freely moving rats by a 5-HT4 receptors partial agonist, and an antagonist. Neuropharmacology 47, 1021–1035 (2004).
pubmed: 15555636
doi: 10.1016/j.neuropharm.2004.06.033
pmcid: 15555636
Terry, A. V. et al. Enhanced delayed matching performance in younger and older macaques administered the 5-HT4 receptor agonist, RS 17017. Psychopharmacol. (Berl.) 135, 407–415 (1998).
doi: 10.1007/s002130050529
Compan, V. et al. Attenuated Response to Stress and Novelty and Hypersensitivity to Seizures in 5-HT4 Receptor Knock-Out Mice. J. Neurosci. 24, 412–419 (2004).
pubmed: 14724239
pmcid: 6729986
doi: 10.1523/JNEUROSCI.2806-03.2004
Stoppini, L., Buchs, P. A. & Muller, D. A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37, 173–182 (1991).
pubmed: 1715499
doi: 10.1016/0165-0270(91)90128-M
pmcid: 1715499
Bergeijk, J., van, Rydel-Könecke, K., Grothe, C. & Claus, P. The spinal muscular atrophy gene product regulates neurite outgrowth: importance of the C terminus. FASEB J. 21, 1492–1502 (2007).
pubmed: 17317728
doi: 10.1096/fj.06-7136com
pmcid: 17317728
Lee, C. W. et al. Dynamic localization of g-actin during membrane protrusion in neuronal motility. Curr. Biol. 23, 1046–1056 (2013).
pubmed: 23746641
pmcid: 3712510
doi: 10.1016/j.cub.2013.04.057
Ruszczycki, B. et al. Sampling issues in quantitative analysis of dendritic spines morphology. BMC Bioinforma. 13, 213 (2012).
doi: 10.1186/1471-2105-13-213
Oray, S., Majewska, A. & Sur, M. Effects of synaptic activity on dendritic spine motility of developing cortical layer v pyramidal neurons. Cereb. Cortex 16, 730–741 (2006).
pubmed: 16120796
doi: 10.1093/cercor/bhj019
Harris, K. M., Jensen, F. E. & Tsao, B. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation [published erratum appears in J Neurosci 1992 Aug;12(8):following table of contents]. J. Neurosci. 12, 2685–2705 (1992).
pubmed: 1613552
pmcid: 6575840
doi: 10.1523/JNEUROSCI.12-07-02685.1992
Hotulainen, P. et al. Defining mechanisms of actin polymerization and depolymerization during dendritic spine morphogenesis. J. Cell Biol. 185, 323–339 (2009).
pubmed: 19380880
pmcid: 2700375
doi: 10.1083/jcb.200809046
Basu, S. et al. Quantitative 3-D morphometric analysis of individual dendritic spines. Sci. Rep. 8, 3545 (2018).
Degasperi, A. et al. Evaluating Strategies to Normalise Biological Replicates of Western Blot Data. PLoS ONE 9, e87293 (2014).
pubmed: 24475266
pmcid: 3903630
doi: 10.1371/journal.pone.0087293