Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2

Wayman, Gary A.; Impey, Soren; Marks, Daniel; Saneyoshi, Takeo; Grant, Wilmon F.; Derkach, Victor; Soderling, Thomas R.

doi:10.1016/j.neuron.2006.05.008

Cited by 466Neuroscience and Neuropharmacology ResearchWnt/β-catenin signaling in development and cancerGenetics and Neurodevelopmental Disorders

Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2

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Wayman, Gary A., Impey, Soren, Marks, Daniel, Saneyoshi, Takeo, Grant, Wilmon F., Derkach, Victor, Soderling, Thomas R.·2006·Neuron

DOI 10.1016/j.neuron.2006.05.008

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Abstract

Members of the Wnt signaling family are important mediators of numerous developmental events, including activity-dependent dendrite development, but the pathways regulating expression and secretion of Wnt in response to neuronal activity are poorly defined. Here, we identify an NMDA receptor-mediated, Ca2+-dependent signaling pathway that couples neuronal activity to dendritic arborization through enhanced Wnt synthesis and secretion. Activity-dependent dendritic outgrowth and branching in cultured hippocampal neurons and slices is mediated through activation by CaM-dependent protein kinase kinase (CaMKK) of the membrane-associated gamma isoform of CaMKI. Downstream effectors of CaMKI include the MAP-kinase pathway of Ras/MEK/ERK and the transcription factor CREB. A serial analysis of chromatin occupancy screen identified Wnt-2 as an activity-dependent CREB-responsive gene. Neuronal activity enhances CREB-dependent transcription of Wnt-2, and expression of Wnt-2 stimulates dendritic arborization. This novel signaling pathway contributes to dynamic remodeling of the dendritic architecture in response to neuronal activity during development.

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Knockdown of CREB expression by shCREB reduces the density of all spine types below control levels in the absence or presence of PCB 95.
“Similarly, knockdown of CREB expression by shCREB (Wayman et al., 2006) reduces the density of all spine types below control levels in the absence or presence of PCB 95 (Fig. 3B).”
From The Environmental Neurotoxicant PCB 95 Promotes Synaptogenesis via Ryanodine Receptor-Dependent miR132 Upregulation (2014) · cites this paper as Wayman et al., 2006
Wnt2 and other proteins usually linked to neural development might also play significant roles in regulating neuronal function after critical periods.
“nonetheless, Wnt2 and other proteins traditionally associated with neural development may have important roles in post-critical period regulation of neuronal function (Farias et al., 2007; Moon et al., 2004; Wayman et al., 2006).”
From Unifying Views of Autism Spectrum Disorders: A Consideration of Autoregulatory Feedback Loops (2016) · cites this paper as Wayman et al., 2006

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BackgroundResultInfluentialSelf-citation
Neuronal Activity-Regulated Gene Transcription in Synapse Development and Cognitive Function
West, A. E., & Greenberg, M. E. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005744 · Cited by 532 · see citing works
“In hippocampal neurons, activation of CaMKI or CaMKIV-dependent phosphorylation of CREB is required for the ability of membrane depolarization or NMDAreceptor activation to promote dendritic arborization (Redmond et al. 2002; Wayman et al. 2006, 2008a).”
Background
Communication Between the Synapse and the Nucleus in Neuronal Development, Plasticity, and Disease
Cohen, S., & Greenberg, M. E. (2008) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.24.110707.175235 · Cited by 400 · see citing works
“N IH -PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript (Redmond et al. 2002, Wayman et al. 2006).”
Background
Mef2‐mediated transcription of the miR379–410 cluster regulates activity‐dependent dendritogenesis by fine‐tuning Pumilio2 protein levels
Fiore, R., Khudayberdiev, S., Christensen, M., Siegel, G., Flavell, S. W., Kim, T.-K., Greenberg, M. E., & Schratt, G. M. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.10 · Cited by 376 · see citing works
“To mimic activity-dependent dendritogenesis in vitro , cultured hippocampal neurons (DIV7) were treated for 6 h with KCl or BDNF and analysed by Sholl analysis (see Materials and methods) at DIV10 (Wayman et al , 2006).”
Method
Wnt signaling in the nervous system and in Alzheimer's disease
Inestrosa, N. C., & Varela-Nallar, L. (2014) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjt051 · Cited by 324 · see citing works
“Wnt-2 expression was increased by activation of NMDAR in hippocampal neurons (Wayman et al., 2006), and an NMDAR-dependent release of Wnt-3a was shown to be induced by tetanic stimulation (Chen et al.”
Background
Synaptic plasticity in depression: Molecular, cellular and functional correlates
Marsden, W. N. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.12.012 · Cited by 315 · see citing works
Rapid Activity-Dependent Modifications in Synaptic Structure and Function Require Bidirectional Wnt Signaling
Ataman, B., Ashley, J., Gorczyca, M. G., Ramachandran, P., Fouquet, W., Sigrist, S. J., & Budnik, V. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.026 · Cited by 285 · see citing works
“Potential scenarios include an activity-dependent increase in wg mRNA or Wg protein synthesis as observed in the mammalian brain (Wayman et al., 2006).”
BackgroundInfluential
Restoring Wnt/β-catenin signaling is a promising therapeutic strategy for Alzheimer’s disease
Jia, L., Piña-Crespo, J., & Li, Y. (2019) · Molecular Brain · doi:10.1186/s13041-019-0525-5 · Cited by 288 · see citing works
Wnt signaling in neural circuit assembly
Salinas, P. C., & Zou, Y. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125649 · Cited by 274 · see citing works
“The discovery that electrical activity can regulate Wnt expression and/or release (Wayman et al. 2006, Yu & Malenka 2003) and that Wnts might regulate neurotransmitter release suggests that Wnts could contribute to a positive feedback mechanism for synaptic modulation.”
BackgroundInfluential
WNT signaling in neuronal maturation and synaptogenesis
Rosso, S. B., & Inestrosa, N. C. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00103 · Cited by 272 · see citing works
The Growing Role of mTOR in Neuronal Development and Plasticity
Jaworski, J., & Sheng, M. (2006) · Molecular Neurobiology · doi:10.1385/mn:34:3:205 · Cited by 268 · see citing works
“Protein kinases such as CaMKs (7,10,11), MAP kinases (70,71), Rhoassociated coiled-coil-forming protein kinase (72) and Pak1 (73) are important regulators of dendritogenesis.”
Background
Wnt signaling during synaptic development and plasticity
Budnik, V., & Salinas, P. C. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.12.002 · Cited by 264 · see citing works
Mechanisms that Regulate Establishment, Maintenance, and Remodeling of Dendritic Fields
Parrish, J. Z., Emoto, K., Kim, M. D., & Jan, Y. N. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112907 · Cited by 257 · see citing works
NMDA and AMPA receptors: old channels, new tricks
Rao, V. R., & Finkbeiner, S. M. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.03.012 · Cited by 250 · see citing works
“Working through the MAPK pathway, NMDA receptorsenhanceCREB-dependenttranscriptionofWnt-2, a secreted glycoprotein that stimulates dendritic arborization [ 52 ].”
Calcium Signaling in Neuronal Motility
Zheng, J. Q., & Poo, M.-M. (2007) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.23.090506.123221 · Cited by 292 · see citing works
“For example, activity-dependent Ca2+ elevation activates CaMKI, which phosphorylates MAPK Ras/MEK/ERK and the transcription factor CREB to enhance Wnt-2 production; this in turn promotes dendritic arborization (Wayman et al. 2006).”
Background
Minding the calcium store: Ryanodine receptor activation as a convergent mechanism of PCB toxicity
Pessah, I. N., Cherednichenko, G., & Lein, P. J. (2010) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.10.009 · Cited by 231 · see citing works
“Activation of a CaMK-CREB-Wnt signaling pathway has recently been demonstrated to link neuronal activity to transcription of gene products that regulate dendritic growth (Wayman et al., 2006) (Fig.”
Activity-Dependent Synaptogenesis: Regulation by a CaM-Kinase Kinase/CaM-Kinase I/βPIX Signaling Complex
Saneyoshi, T., Wayman, G. A., Fortin, D. A., Davare, M. A., Hoshi, N., Nozaki, N., Natsume, T., & Soderling, T. R. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.016 · Cited by 228 · see citing works
Self-citation
An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling
Impey, S., Davare, M., Lasiek, A., Fortin, D., Ando, H., Varlamova, O., Obrietan, K., Soderling, T. R., Goodman, R. H., & Wayman, G. A. (2010) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2009.10.005 · Cited by 270 · see citing works
“The transcription factor CREB regulates dendritic growth (Redmond et al., 2002; Wayman et al., 2006) and spine formation in hippocampal neurons (Marie et al.”
BackgroundMethodInfluentialSelf-citation
Single-Cell Optogenetic Excitation Drives Homeostatic Synaptic Depression
Goold, C. P., & Nicoll, R. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.020 · Cited by 244 · see citing works
Wnt signaling in development and disease
Freese, J. L., Pino, D., & Pleasure, S. J. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.09.003 · Cited by 219 · see citing works
Wnt7a signaling promotes dendritic spine growth and synaptic strength through Ca 2+ /Calmodulin-dependent protein kinase II
Ciani, L., Boyle, K. A., Dickins, E. M., Sahores, M., Anane, D., Lopes, D. M., Gibb, A. J., & Salinas, P. C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018132108 · Cited by 209 · see citing works
“In sharp contrast to other Wnts, like Wnt5a (23, 25), Wnt7a specifically promotes the formation and function of excitatory synapses, whereas inhibitory synapses are unaffected.”
BackgroundInfluential
Cell atrophy and loss in depression: reversal by antidepressant treatment
Banasr, M., Dwyer, J. M., & Duman, R. S. (2011) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2011.09.002 · Cited by 201 · see citing works
Developmental neurotoxicity of succeeding generations of insecticides
Abreu‐Villaça, Y., & Levin, E. D. (2016) · Environment International · doi:10.1016/j.envint.2016.11.019 · Cited by 202 · see citing works
“…those that delay sodium channel inactivation and affect sodium current, alters spontaneous synchronized calcium oscillations that are essential for normal neuronal development (Dolmetsch et al., 1998; Wayman et al., 2006) and increases phosphorylated CREB and activity-dependent dendritic growth.”
Background
Mechanisms of specificity in neuronal activity-regulated gene transcription
Lyons, M. R., & West, A. E. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.05.003 · Cited by 199 · see citing works
“Importantly, it has been demonstrated by a myriad of studies that one critical way in which NMDARs are capable of exerting their effects on a neuron’s life and metabolism is via regulation of gene transcription (Hardingham and Bading, 2003; Wayman et al., 2006; West et al., 2002).”
Background
Dynamic O-GlcNAc modification regulates CREB-mediated gene expression and memory formation
Rexach, J. E., Clark, P. M., Mason, D. E., Neve, R. L., Peters, E. C., & Hsieh‐Wilson, L. C. (2012) · Nature Chemical Biology · doi:10.1038/nchembio.770 · Cited by 199 · see citing works
WNT-β Catenin Signaling as a Potential Therapeutic Target for Neurodegenerative Diseases: Current Status and Future Perspective
Ramakrishna, K., Nalla, L. V., Dumala, N., Venkateswarlu, K., Viswanadh, M. K., Nalluri, B. N., Chakravarthy, G., Duguluri, S., Singh, P., Nand, S., et al. (2023) · Diseases · doi:10.3390/diseases11030089 · Cited by 203 · see citing works
“ment-binding protein (CREB) mediated transcription process [19]—owing to multiple physiological and pathological roles, particularly cell proliferation, survival, and migration.”
Background
Wnt signaling in the regulation of adult hippocampal neurogenesis
Varela‐Nallar, L., & Inestrosa, N. C. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00100 · Cited by 197 · see citing works
“Importantly, the release and expression of Wnt ligands is modulated by neuronal activity (Chen et al., 2006; Wayman et al., 2006; Tabatadze et al., 2012), and incubation of adult hippocampal slices with secreted Wnt inhibitors affects glutamatergic neurotransmission (Chen et al., 2006;…”
Background
Wnt Signaling in the Vertebrate Central Nervous System: From Axon Guidance to Synaptic FunctionPreprint
Salinas, P. C. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008003 · Cited by 189 · see citing works
“Importantly, blockade of Wnt2 compromised dendritic development (Wayman et al. 2006).”
Background
Long-Term Potentiation-Dependent Spine Enlargement Requires Synaptic Ca 2+ -Permeable AMPA Receptors Recruited by CaM-Kinase I
Fortin, D. A., Davare, M. A., Srivastava, T., Brady, J. D., Nygaard, S. C., Derkach, V. A., & Soderling, T. R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1746-10.2010 · Cited by 188 · see citing works
“, 2004), dendritic arborization (Wayman et al., 2006), and spine/synapses formation (Saneyoshi et al.”
BackgroundMethodInfluentialSelf-citation
Unifying Views of Autism Spectrum Disorders: A Consideration of Autoregulatory Feedback Loops
Mullins, C., Fishell, G., & Tsien, R. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.017 · Cited by 167 · see citing works
“However, as clearly summarized by Kalkman (2012), onemust recognize themultiple roles ofWnt signaling not only in cell adhesion and dendritic remodeling but also in early brain development (Rosso et al., 2005; Salinas and Zou, 2008; Ueda et al., 2008; Wayman et al., 2006; Yu and Malenka, 2003).”
Membrane lipid rafts and neurobiology: age‐related changes in membrane lipids and loss of neuronal function
Egawa, J., Pearn, M. L., Lemkuil, B. P., Patel, P. M., & Head, B. P. (2015) · The Journal of Physiology · doi:10.1113/jp270590 · Cited by 174 · see citing works
“…exists several pro-growth pathways that converge upon cAMP: NMDAR, AMPAR, TrkB and GPCRs such as dopamine 1 receptor (D1R) and serotonin receptors (5-HT6 and 5-HT7) (Gao et al. 2003; Schmitt et al. 2004; Wayman et al. 2004, 2006; Kong et al. 2007; Chytrova et al. 2008; Fantini & Barrantes, 2009).”
Background
Curcumin Enhances Neurogenesis and Cognition in Aged Rats: Implications for Transcriptional Interactions Related to Growth and Synaptic Plasticity
Dong, S., Zeng, Q., Mitchell, E. S., Xiu, J., Duan, Y., Li, C., Tiwari, J. K., Hu, Y., Cao, X., & Zhao, Z. Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031211 · Cited by 179 · see citing works
TRPC6 channels promote dendritic growth via the CaMKIV-CREB pathway
Tai, Y., Feng, S., Ge, R., Du, W., Zhang, X., He, Z., & Wang, Y. (2008) · Journal of Cell Science · doi:10.1242/jcs.026906 · Cited by 174 · see citing works
Molecular mechanisms of autism: a possible role for Ca2+ signaling
Krey, J. F., & Dolmetsch, R. E. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.01.010 · Cited by 169 · see citing works
Calmodulin kinases: essential regulators in health and disease
Takemoto‐Kimura, S., Suzuki, K., Horigane, S., Kamijo, S., Inoue, M., Sakamoto, M., Fujii, H., & Bito, H. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14020 · Cited by 171 · see citing works
Developmental Exposure to Polychlorinated Biphenyls Interferes with Experience-Dependent Dendritic Plasticity and Ryanodine Receptor Expression in Weanling Rats
Yang, D., Kim, K. H., Phimister, A., Bachstetter, A. D., Ward, T. R., Stackman, R. W., Mervis, R. F., Wisniewski, A. B., Klein, S. L., Kodavanti, P. R. S., et al. (2009) · Environmental Health Perspectives · doi:10.1289/ehp.11771 · Cited by 166 · see citing works
“On day 6 in vitro (6DIV) cultures were transfected with plasmid encoding a microtubuleassociated protein2 (MAP2)enhanced green fluorescent protein (GFP) fusion construct (Wayman et al. 2006) using Lipofectamine2000 (Invitrogen) according to the manufacturer’s protocol.”
InfluentialSelf-citation
Wnt Signaling in Vertebrate Neural Development and Function
Mulligan, K. A., & Cheyette, B. N. R. (2012) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-012-9404-x · Cited by 165 · see citing works
“2006) and Wnt2, in turn, increases dendrite arborization in these cells (Wayman et al. 2006).”
Influential
Wnts in adult brain: from synaptic plasticity to cognitive deficiencies
Oliva, C. A., Vargas, J. Y., & Inestrosa, N. C. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00224 · Cited by 162 · see citing works
“Neuronal activity induced by high K+ sequentially activates NMDARs, CaMKK, CaMKI, Ras, MEK/ERK, and CREB-dependent transcription of Wnt2 (Wayman et al., 2006), indicating that Wnt2 could be a CREB-responsive gene.”
BackgroundInfluential
Wnt signalling in neuronal differentiation and development
Inestrosa, N. C., & Varela‐Nallar, L. (2014) · Cell and Tissue Research · doi:10.1007/s00441-014-1996-4 · Cited by 162 · see citing works
“activity (Chen et al. 2006; Wayman et al. 2006), supporting the notion that these ligands may play a role during neuronal”
BackgroundInfluential
Progenitor Hyperpolarization Regulates the Sequential Generation of Neuronal Subtypes in the Developing Neocortex
Vitali, I., Fièvre, S., Telley, L., Oberst, P., Bariselli, S., Frangeul, L., Baumann, N., McMahon, J. J., Klingler, E., Bocchi, R., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.036 · Cited by 152 · see citing works
“Activity-dependent modulation of canonical WNT signaling has previously been reported to occur at later stages of differentiation, during dendritic arborization and synaptic plasticity (Ataman et al., 2008; Wayman et al., 2006; Chen et al., 2006; Yu and Malenka, 2003).”
Canonical and noncanonical Wnt signaling in neural stem/progenitor cells
Bengoa‐Vergniory, N., & Kypta, R. M. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2028-6 · Cited by 161 · see citing works
“Wnt-2 overexpression Induced dendritic arborization in hippocampal progenitors [61]”
Recruitment of Calcium-Permeable AMPA Receptors during Synaptic Potentiation Is Regulated by CaM-Kinase I
Guire, E. S., Oh, M. C., Soderling, T. R., & Derkach, V. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0384-08.2008 · Cited by 151 · see citing works
“…incorporation of CP-AMPARs The CaMKK/CaMKI cascade is involved in multiple aspects of activity-dependent neuronal development and plasticity (Wayman et al., 2004, 2006; Saneyoshi et al., 2008), including TBS-LTP (Schmitt et al., 2005), in part because of regulation of actin dynamics (Wayman…”
BackgroundSelf-citation
Nanoporous Gold as a Neural Interface Coating: Effects of Topography, Surface Chemistry, and Feature Size
Chapman, C. A. R., Chen, H., Stamou, M., Biener, J., Biener, M. M., Lein, P. J., & Şeker, E. (2015) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.5b00410 · Cited by 150 · see citing works
Regulation of NMDA-Receptor Synaptic Transmission by Wnt Signaling
Cerpa, W. F., Gambrill, A. C., Inestrosa, N. C., & Barría, A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6311-10.2011 · Cited by 147 · see citing works
“A canonical Wnt ligand, Wnt-3a, has been reported to modify a major form of synaptic plasticity, long term potentiation (LTP) (Chen et al., 2006), and Wnt-2 has been shown to induce dendritic arborization (Wayman et al., 2006).”
Background
CaMKII in cerebral ischemia
Coultrap, S. J., Vest, R. S., Ashpole, N. M., Hudmon, A., & Bayer, K. U. (2011) · Acta Pharmacologica Sinica · doi:10.1038/aps.2011.68 · Cited by 145 · see citing works
Derepression of a Neuronal Inhibitor due to miRNA Dysregulation in a Schizophrenia-Related Microdeletion
Xu, B., Hsu, P.-K., Stark, K. L., Karayiorgou, M., & Gogos, J. A. (2013) · Cell · doi:10.1016/j.cell.2012.11.052 · Cited by 145 · see citing works
Synaptic Wnt signaling—a contributor to major psychiatric disorders?
Okerlund, N. D., & Cheyette, B. N. R. (2011) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-011-9083-6 · Cited by 143 · see citing works
“Studies in cultured hippocampal neurons (HCNs) have shown that an increase in Wnt7b (Rosso et al. 2005) or in Wnt2 are both associated with increases in complexity of dendritic arbors and that Wnt2 transcription is upregulated by neuronal activity in this system (Wayman et al. 2006).”
Background
Intracellular Metabotropic Glutamate Receptor 5 (mGluR5) Activates Signaling Cascades Distinct from Cell Surface Counterparts
Jong, Y.-J. I., Kumar, V., & O’Malley, K. L. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.046276 · Cited by 145 · see citing works
PCB-95 Promotes Dendritic Growth via Ryanodine Receptor–Dependent Mechanisms
Wayman, G. A., Yang, D., Bose, D. D., Lesiak, A., Ledoux, V., Bruun, D., Pessah, I. N., & Lein, P. J. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104832 · Cited by 136 · see citing works
“Dendritic arbors of individual neurons in highdensity neuron glia cocultures were visualized by expressing a MAP2BEGFP construct under the control of the CAG promoter, which exhibits neuron specific expression (Wayman et al. 2006).”
BackgroundMethodInfluentialSelf-citation
Snapin Recruits Dynein to BDNF-TrkB Signaling Endosomes for Retrograde Axonal Transport and Is Essential for Dendrite Growth of Cortical Neurons
Zhou, B., Cai, Q., Xie, Y., & Sheng, Z. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.06.010 · Cited by 141 · see citing works
“pCREB-dependent transcription is necessary for regulation of dendritic morphology and development (Redmond et al., 2002; Wayman et al., 2006).”
Background
Molecular Mechanisms Underlying Ca2+/Calmodulin-Dependent Protein Kinase Kinase Signal Transduction
Tokumitsu, H., & Sakagami, H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911025 · Cited by 134 · see citing works
Small mouse cholangiocytes proliferate in response to H1 histamine receptor stimulation by activation of the IP 3 /CaMK I/CREB pathway
Francis, H., Glaser, S. S., DeMorrow, S., Gaudio, E., Ueno, Y., Venter, J. K., Dostal, D. E., Onori, P., Franchitto, A., Marzioni, M., et al. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00369.2007 · Cited by 136 · see citing works
PCB-95 Modulates the Calcium-Dependent Signaling Pathway Responsible for Activity-Dependent Dendritic Growth
Wayman, G. A., Bose, D. D., Yang, D., Lesiak, A. J., Bruun, D. A., Impey, S., Ledoux, V. A., Pessah, I. N., & Lein, P. J. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104833 · Cited by 136 · see citing works
“To determine which CaMKI isoforms may be involved in PCB-95–induced dendritic growth, previously characterized small hairpin RNA (shRNA) constructs that suppress individual CaMKI isoforms (Wayman et al. 2006) were expressed in hippo campal neurons.”
BackgroundMethodResultInfluentialSelf-citation
Evidence Implicating Non-Dioxin-Like Congeners as the Key Mediators of Polychlorinated Biphenyl (PCB) Developmental Neurotoxicity
Klocke, C. R., & Lein, P. J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21031013 · Cited by 135 · see citing works
Analysis of CaM-kinase signaling in cells
Wayman, G. A., Tokumitsu, H., Davare, M. A., & Soderling, T. R. (2011) · Cell Calcium · doi:10.1016/j.ceca.2011.02.007 · Cited by 128 · see citing works
“Table 1 lists the sequence we have successfully used to inhibit the expression of CaMKs in rat neurons [23, 38, 50, 73].”
BackgroundMethodInfluentialSelf-citation
Frizzled-5, a receptor for the synaptic organizer Wnt7a, regulates activity-mediated synaptogenesis
Sahores, M., Gibb, A. J., & Salinas, P. C. (2010) · Development · doi:10.1242/dev.046722 · Cited by 128 · see citing works
“Wnts contribute to HFS-induced synapse formation and synaptic localization of Fz5 Neuronal activity regulates the expression of Wnts in hippocampal neurons (Wayman et al., 2006; Yu and Malenka, 2003; Gogolla et al., 2009).”
Background
Differential expression of microRNA in peripheral blood mononuclear cells as specific biomarker for major depressive disorder patients
Fan, H., Sun, X., Guo, W., Zhong, A., Niu, W., Zhao, L., Dai, Y.-H., Guo, Z.-M., Zhang, L.-Y., & Lu, J. Z. (2014) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2014.08.007 · Cited by 129 · see citing works
Wnts in action: from synapse formation to synaptic maintenance
Dickins, E. M., & Salinas, P. C. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00162 · Cited by 121 · see citing works
“Wnt2 is also regulated by activity through a mechanism that requires NMDAR activation and cAMP response element-binding protein (CREB)-mediated transcription to promote dendritic arborization of cultured hippocampal neurons (Wayman et al., 2006).”
BackgroundInfluential
TORC1 Regulates Activity-Dependent CREB-Target Gene Transcription and Dendritic Growth of Developing Cortical Neurons
Li, S., Zhang, C., Takemori, H., Zhou, Y., & Xiong, Z. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2296-08.2009 · Cited by 126 · see citing works
“TORC1 is required for dendritic growth of developing cortical neurons in vitro Ca 2 -mediated gene expression is involved in activitydependent regulation of dendritic development (Redmond et al., 2002; Wayman et al., 2006).”
Background
Molecular basis of dendritic arborization [Review]
Urbańska, M., Błażejczyk, M., & Jaworski, J. (2008) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-2008-1695 · Cited by 125 · see citing works
“…TDL, TDBTN, complexity hippocampus, cortex, cerebellum/rat, mouse Redmond et al. 2002, Yu and Malenka 2003, Gaudilliere et al. 2004, Chen et al. 2005, Wayman et al. 2006, Wu et al. 2007 GABAR GABA application – increased TDL and number of primary dendrites Inh – decreased TDL and number of…”
BackgroundInfluential
Neuronal connectivity as a convergent target of gene × environment interactions that confer risk for Autism Spectrum Disorders
Stamou, M., Streifel, K. M., Goines, P. E., & Lein, P. J. (2013) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2012.12.001 · Cited by 128 · see citing works
“…mutation exhibited increased neuronal complexity and upregulated expression of genes linked to Ca2+-dependent regulation of CREB, including CaMK, which is consistent with studies demonstrating that CaMK signaling through CREB links activity to increased dendritic growth (Wayman et al., 2006).”
BackgroundResultInfluential
Physiological Roles Of The Ca2+/Cam-Dependent Protein kinase Cascade In Health and Disease
COLOMER, J., & Means, A. R. (2007) · Springer eBooks · doi:10.1007/978-1-4020-6191-2_7 · Cited by 124 · see citing works
CREB mediates brain serotonin regulation of bone mass through its expression in ventromedial hypothalamic neuronsPreprint
Oury, F., Yadav, V. K., Wang, Y., Zhou, B., Liu, X. S., Guo, X.-D. E., Tecott, L. H., Schütz, G., Means, A. R., & Karsenty, G. (2010) · Genes & Development · doi:10.1101/gad.1977210 · Cited by 124 · see citing works
“Although it acts in many different cellular contexts, CREB is a major regulator of multiple aspects of neurobiology, such as neuron survival, axon growth, and synaptic transmission (Ribar et al. 2000; Wayman et al. 2004, 2006; Mizuno et al. 2006).”
Background
Brain-derived neurotrophic factor activation of CaM-kinase kinase via transient receptor potential canonical channels induces the translation and synaptic incorporation of GluA1-containing calcium-permeable AMPA receptors
Fortin, D. A., Srivastava, T., Dwarakanath, D., Pierre, P., Nygaard, S., Derkach, V. A., & Soderling, T. R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6034-11.2012 · Cited by 120 · see citing works
“The construction, validation, and specificity of the plasmid-based shRNA constructs for knockdown of CaMKK have been described previously (Wayman et al., 2006; Saneyoshi et al., 2008).”
MethodInfluentialSelf-citation
BDNF-Promoted Increases in Proximal Dendrites Occur via CREB-Dependent Transcriptional Regulation of Cypin
Kwon, M., Fernandez, J. R., Zegarek, G. F., Lo, S. B., & Firestein, B. L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6785-10.2011 · Cited by 115 · see citing works
Raphe-mediated signals control the hippocampal response to SRI antidepressants via miR-16
Launay, J., Mouillet‐Richard, S., Baudry, A., Pietri, M., & Kellermann, O. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.54 · Cited by 118 · see citing works
Regulation of Dendritogenesis via a Lipid-Raft-Associated Ca2+/Calmodulin-Dependent Protein Kinase CLICK-III/CaMKIγ
Takemoto‐Kimura, S., Ageta‐Ishihara, N., Nonaka, M., Adachi-Morishima, A., Mano, T., Okamura, M., Fujii, H., Fuse, T., Hoshino, M., Suzuki, S., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.021 · Cited by 118 · see citing works
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Authors: Wayman, G. A., Impey, S., Marks, D., Saneyoshi, T., Grant, W. F., Derkach, V., & Soderling, T. R.
Affiliations: Oregon Health & Science University (US)
Corresponding author: Soderling, Thomas R.
ORCID: Wayman, Gary A.
Marks, Daniel
Saneyoshi, Takeo
Venue: Neuron
Publisher: Elsevier BV
Published: 2006-06
Volume: 50
Issue: 6
Pages: 897-909
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2006.05.008
OpenAlex: W1998977808
Cited by: 466
References: 76
Citations by year: 2026: 11 · 2025: 7 · 2024: 12 · 2023: 18 · 2022: 15 · 2021: 11 · 2020: 21 · 2019: 19 · 2018: 22 · 2017: 34 · 2016: 19 · 2015: 20 · 2014: 33 · 2013: 37 · 2012: 35
FWCI: 10.74
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 2639 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
Tokyo Tech Research Repository (Tokyo Institute of Technology) (submittedVersion)
Funders: National Institutes of Health (R01 GM041292)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords: dendritic branching, CaMKI, CaMKK, CREB, NMDA receptor signaling, calcium signaling, hippocampal neurons, Wnt secretion, Ras/MEK/ERK pathway, dendritic remodeling, chromatin occupancy
MeSH terms: Animals, Animals, Newborn, Cells, Cultured, Dendrites, Enzyme Activation, Hippocampus, Organ Culture Techniques, Transcription, Genetic, Rats, Sprague-Dawley, Cyclic AMP Response Element-Binding Protein, Calcium-Calmodulin-Dependent Protein Kinases, Wnt2 Protein, Rats, Calcium-Calmodulin-Dependent Protein Kinase Type 1

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Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2

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