Cited by 485Wnt/β-catenin signaling in development and cancerNeuroscience and Neuropharmacology ResearchAxon Guidance and Neuronal Signaling

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Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development

Rosso, Silvana B, Sussman, Daniel, Wynshaw-Boris, Anthony, Salinas, Patricia C·2005·Nature Neuroscience

DOI 10.1038/nn1374

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Abstract

Dendritic arborization is required for proper neuronal connectivity. Rho GTPases have been implicated in the regulation of dendrite development. However, the signaling pathways that impinge on these molecular switches remain poorly understood. Here we show that Wnt7b, which is expressed in the mouse hippocampus, increases dendritic branching in cultured hippocampal neurons. This effect is mimicked by the expression of Dishevelled (Dvl) and is blocked by Sfrp1, a secreted Wnt antagonist. Consistent with these findings, hippocampal neurons from mice lacking Dvl1 show reduced dendritic arborization. Activation of the canonical Wnt-Gsk3beta pathway does not affect dendritic development. In contrast, Wnt7b and Dvl activate Rac and JNK in hippocampal neurons. Dominant-negative Rac, dominant-negative JNK or inhibition of JNK blocks Dvl-mediated dendritic growth. These findings demonstrate a new function for the non-canonical Wnt pathway in dendrite development and identify Dvl as a regulator of Rho GTPases and JNK during dendritic morphogenesis.

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Background
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Background
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Background
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Background
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BackgroundSelf-citation
mig-5/Dsh controls cell fate determination and cell migration in C. elegans
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Wnt5a Controls Neurite Development in Olfactory Bulb Interneurons
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“(c-Jun N-terminal kinase) Wnt pathway (Rosso et al., 2005).”
BackgroundMethodResultInfluential
Genetics of Bladder-Exstrophy-Epispadias Complex (BEEC): Systematic Elucidation of Mendelian and Multifactorial Phenotypes
Reutter, H. M., Keppler‐Noreuil, K. M., Keegan, C. E., Thiele, H., Yamada, G., & Ludwig, M. Z. (2015) · Current Genomics · doi:10.2174/1389202916666151014221806 · Cited by 31
“Among these genes, the authors discussed NOC2L, DVL1, the human homolog of the Drosophila dishevelled gene (dsh), encoding a cytoplasmic phosphoprotein that functions as a mediator of the WNT signaling pathway [66, 67], and MMP23B as possible candidate genes.”
Small GTPase protein Rac-1 is activated with maturation and regulates cell morphology and function in chondrocytes
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Altered expression of Autism-associated genes in the brain of Fragile X mouse model
Zhang, A., Shen, C.-H., Ma, S. Y., Ke, Y., & Idrissi, A. E. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.12.172 · Cited by 31
Wnt7b signalling through Frizzled-7 receptor promotes dendrite development by coactivating CaMKII and JNK
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“Wnt proteins, through their specific receptors modulate neuronal functioning by regulating axon guidance (Lyuksyutova et al., 2003), dendrite development (Rosso et al., 2005) and synapse assembly (Varela-Nallar et al., 2009; Sahores et al., 2010; Ciani et al., 2011).”
BackgroundInfluentialSelf-citation
Role of Wnt Signaling in the Control of Adult Hippocampal Functioning in Health and Disease: Therapeutic Implications
Ortiz‐Matamoros, A., Salcedo‐Tello, P., Ávila-Muñoz, E., Zepeda, A., & Arias, C. (2013) · Current Neuropharmacology · doi:10.2174/1570159x11311050001 · Cited by 30
“This effect is mimicked by Dvl1 overexpression and blocked by the Wnt antagonist sFRP, which is in line with the results from hippocampal neurons derived from a Dvl1 mutant mice [56].”
Result
Altered learning, memory, and social behavior in type 1 taste receptor subunit 3 knock-out mice are associated with neuronal dysfunction
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“With specific reference to the strongest scoring hippocampal bio-function prediction, i.e. “proliferation of neuronal cells,” the factors populating this group consisted of multiple transcripts linked to Alzheimer’s disease (AD) (K-Ras (58), Wnt7b (59), Rasgrf1 (60), and Tardbp (61, 62)), calcium-dependent hippocampal…”
Background
Wnt5a signaling controls cytokinesis by positioning ESCRT-III to the proper site at the midbody
Fumoto, K., Kikuchi, K., Gon, H., & Kikuchi, A. (2012) · Journal of Cell Science · doi:10.1242/jcs.108142 · Cited by 29
“Neurons from Dvl1 knockout mice developed a dendritic arbor of lesser complexity than neurons from wild-type mice (Rosso et al., 2005) and did not undergo growth cone remodeling to form synapses in response to Wnt probably through a failure of microtubule stabilization (Purro et al.”
Background
The transcriptional coactivator WBP2 primes triple-negative breast cancer cells for responses to Wnt signaling via the JNK/Jun kinase pathway
Li, Z., Lim, S. K., Xu, L., & Lim, Y. P. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.005796 · Cited by 28
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“To determine if Rac plays a role in oriented migration of PE cells, we inhibited JNK, a known downstream effector of Rac, using the pharmacological inhibitor SP600125 (Rosso et al., 2005).”
Influential
Potential cross-talk between (pro)renin receptors and Wnt/frizzled receptors in cardiovascular and renal disorders
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G-protein Coupled Receptors in Stem Cell Self-Renewal and Differentiation
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“Wnt signalling is implicated in a wide array of cellular processes in the developing nervous system including anterior-posterior neural tube specification [211, 212], regionalization of brain and spinal cord [213–217], axon guidance [218, 219], dendritic [220] and synapse formation and regulation [221–223] for review…”
Background
WNT‐3a modulates platelet function by regulating small GTPase activity
Steele, B. M., Harper, M. T., Smolenski, A., Alkazemi, N., Poole, A. W., Fitzgerald, D. J., & Maguire, P. B. (2012) · FEBS Letters · doi:10.1016/j.febslet.2012.05.060 · Cited by 27
“This inverse Rho/Rac relationship has been noted previously during platelet activation [28] and both RhoA and Rac1 play key roles during the WNT signalling response [29,30].”
Background
WNT10B Enhances Proliferation through β-Catenin and RAC1 GTPase in Human Corneal Endothelial Cells
Lee, J. G., & Heur, M. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.677245 · Cited by 26
Vertebrate Presynaptic Active Zone Assembly: a Role Accomplished by Diverse Molecular and Cellular Mechanisms
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System-based proteomic and metabonomic analysis of the Df(16)A+/− mouse identifies potential miR-185 targets and molecular pathway alterations
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Wnt5a Signals through DVL1 to Repress Ribosomal DNA Transcription by RNA Polymerase I
Dass, R. A., Sarshad, A. A., Carson, B. B., Feenstra, J. M., Kaur, A., Obrdlík, A., Parks, M., Prakash, V., Love, D. K., Pietras, K., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006217 · Cited by 26
“The roles of DVL proteins in Wnt signaling have mostly been associated with receptorproximal aspects, reversible assembly of multi-molecular complexes, and/or interactions with components of the cytoskeleton [20,21,40,41].”
Background
Effects of GSM 1800 MHz on dendritic development of cultured hippo-campal neurons
Wei, N., Xu, S., Chiang, H., Xu, Z., Zhou, S., Yang, W., & Luo, J. (2007) · Acta Pharmacologica Sinica · doi:10.1111/j.1745-7254.2007.00668.x · Cited by 26
Distinct functionality of dishevelled isoforms on Ca 2+ /calmodulin-dependent protein kinase 2 (CamKII) in Xenopus gastrulation
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“…small GTPases RhoA and Rac1 (Strutt et al., 1997; Habas et al., 2001, 2003) and their downstream effector kinases Rho-associated protein kinase (ROCK; Marlow et al., 2002; Simões et al., 2010) and c-jun N-terminal kinase (JNK; Boutros et al., 1998; Yamanaka et al., 2002; Rosso et al., 2005).”
Background
SFRP1 in Skin Tumor Initiation and Cancer Stem Cell Regulation with Potential Implications in Epithelial Cancers
Sunkara, R. R., Sarate, R. M., Setia, P., Shah, S. G., Gupta, S. K., Chaturvedi, P., Gera, P. B., & Waghmare, S. K. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.12.006 · Cited by 25
“It was previously reported that SFRP1 binds and inhibits WNT7B; therefore, knockout of SFRP1 would enhance the WNT7B-mediated noncanonical signaling pathway.”
BackgroundInfluential
Identification of shell-color-related microRNAs in the Manila clam Ruditapes philippinarum using high-throughput sequencing of small RNA transcriptomes
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“Wnt-7b regulates dendritic development in young neurons through the JNK cascade [Rosso et al., 2005].”
Background
Dendrite Complexity of Sympathetic Neurons Is Controlled during Postnatal Development by BMP Signaling
Majdazari, A., Stubbusch, J., Müller, C. M., Hennchen, M., Weber, M., Deng, C., Mishina, Y. M., Schütz, G., Deller, T., & Rohrer, H. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4748-12.2013 · Cited by 25
“, 1999) or interfere with the expression of growth stimulatory signals like Wnt/ -catenin (Yu and Malenka, 2003; Rosso et al., 2005).”
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The search for genetic determinants of human neural tube defects
Wolujewicz, P., & Ross, M. E. (2019) · Current Opinion in Pediatrics · doi:10.1097/mop.0000000000000817 · Cited by 25
“The WNT/PCP pathway has been implicated in axon guidance and regulating dendritic development among other functions [13,14].”
Background
Blockers of Wnt3a, Wnt10a, or β-Catenin Prevent Chemotherapy-Induced Neuropathic Pain In Vivo
Kim, H. K., Bae, J., Lee, S. H., Hwang, S.-H., Kim, M., Kim, M. J., Jun, S., Cervantes, C., Jung, Y., Back, S., et al. (2020) · Neurotherapeutics · doi:10.1007/s13311-020-00956-w · Cited by 27
Frizzled9 protein is regionally expressed in the developing medial cortical wall and the cells derived from this region
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Integrated analysis of multi‐omics data on epigenetic changes caused by combined exposure to environmental hazards
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Microglial WNT5A supports dendritic spines maturation and neuronal firing
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The role of glycogen synthase kinase-3 signaling in neurodevelopment and fragile X syndrome.
Portis, S. M., Giunta, B. N., Obregon, D. F., & Tan, J. (2012) · Europe PMC (PubMed Central) · Cited by 24
Impact of seizures on developing dendrites: Implications for intellectual developmental disabilities
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“Studies have implicated roles for both Wnt (Yu & Malenka, 2003; Rosso et al., 2005; Wayman et al., 2006) and mammalian target of rapamycin (mTOR) signaling (Wu et al., 2001; Dunah et al., 2005; Kumar et al., 2005; Chow et al., 2009) in the development of dendrites.”
Background
A novel function for Wnt signaling modulating neuronal firing activity and the temporal structure of spontaneous oscillation in the entorhinal–hippocampal circuit
Oliva, C. A., & Inestrosa, N. C. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.03.027 · Cited by 24
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All four zebrafish Wnt7 genes are expressed during early brain development
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Control of dendritic diversity
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The Exocyst Component Exo70 Modulates Dendrite Arbor Formation, Synapse Density, and Spine Maturation in Primary Hippocampal Neurons
Lira, M., Arancibia, D., Orrego, P. R., Montenegro‐Venegas, C., Cruz, Y., García, J., Leal‐Ortiz, S., Godoy, J. A., Gundelfinger, E. D., Inestrosa, N. C., et al. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1378-0 · Cited by 23
Canonical Wnt Signaling Modulates the Expression of Pre- and Postsynaptic Components in Different Temporal Patterns
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Small GTPase Rnd1 is involved in neuronal activity-dependent dendritic development in hippocampal neurons
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RETRACTED ARTICLE: Signaling network involved in the GPC3-induced inhibition of breast cancer progression: role of canonical Wnt pathway
Fernández, D., Guereño, M., Huvelle, M. A. L., Cercato, M. C., & Peters, M. G. (2018) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-018-2751-0 · Cited by 22
“While Dvl participates in the canonical Wnt pathway by inhibiting the GSK3β activity, it is also member of non-canonical PCP Wnt signaling and modulates the small GTPases RhoA, Rac as well as JNK (Rosso et al. 2005).”
Retracted
Transcription Factor 4 Safeguards Hippocampal Dentate Gyrus Development by Regulating Neural Progenitor Migration
Wang, Y., Lu, Z., Zhang, Y., Cai, Y., Yun, D., Tang, T., Cai, Z., Wang, C., Zhang, Y., Fang, F., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz297 · Cited by 23
Cell type-specific dendritic polarity in the absence of spatially organized external cues
Horton, A. C., Yi, J. J., & Ehlers, M. (2007) · Journal of Neurocytology · doi:10.1007/s11068-006-9003-y · Cited by 22
“Numerous cytoskeletal regulatory proteins have been identified as important both to initial dendrite outgrowth ( Rosso et al., 2005 ) and during the coupling of neuronal activity to structural plasticity (Buttery et al., 2006).”
Background

Authors: Rosso, S. B., Sussman, D., Wynshaw-Boris, A., & Salinas, P. C.
Affiliations: University of London (GB)
University of Maryland, Baltimore (US)
University of California San Diego (US)
Corresponding author: Salinas, Patricia C
ORCID: Rosso, Silvana B
Wynshaw-Boris, Anthony
Salinas, Patricia C
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2004-12-19
Volume: 8
Issue: 1
Pages: 34-42
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/nn1374
OpenAlex: W2087203385
Cited by: 485
References: 50
Citations by year: 2026: 3 · 2025: 11 · 2024: 21 · 2023: 9 · 2022: 11 · 2021: 17 · 2020: 15 · 2019: 14 · 2018: 23 · 2017: 18 · 2016: 19 · 2015: 27 · 2014: 29 · 2013: 32 · 2012: 43
FWCI: 9.64
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust
National Institute of Neurological Disorders and Stroke (R01NS073159)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
Keywords: Wnt signaling, Dishevelled, dendritic branching, Wnt7b, SFRP1, non-canonical Wnt pathway, Rac, JNK, Rho GTPases, hippocampal neurons, dendrite morphogenesis, Wnt antagonists
MeSH terms: Dishevelled Proteins, Acute-Phase Proteins, Animals, Cells, Cultured, Cytoskeleton, Dendrites, Embryo, Mammalian, Glycoproteins, Hippocampus, Mutation, Neurons, Phosphoproteins, Proteins, Proto-Oncogene Proteins, Tissue Distribution, Signal Transduction, Protein Structure, Tertiary, rac GTP-Binding Proteins, Intercellular Signaling Peptides and Proteins, JNK Mitogen-Activated Protein Kinases, Adaptor Proteins, Signal Transducing, Wnt Proteins, Mice

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Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development

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