Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development
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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Wnt signaling has multiple roles, including in cell adhesion, dendritic remodeling, and early brain development.
“However, as clearly summarized by Kalkman (Kalkman, 2012), one must recognize the multiple roles of Wnt 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).”
From Unifying Views of Autism Spectrum Disorders: A Consideration of Autoregulatory Feedback Loops (2016) · cites this paper as Rosso et al., 2005
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Wnt-5a/JNK Signaling Promotes the Clustering of PSD-95 in Hippocampal Neurons
Farı́as, G. G., Alfaro, I. E., Cerpa, W. F., Grabowski, C. P., Godoy, J. A., Bonansco, C., & Inestrosa, N. C. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m808986200 · Cited by 200 · see citing works
The regulation and function of mammalian AMPK‐related kinases
Bright, N. J., Thornton, C., & Carling, D. (2009) · Acta Physiologica · doi:10.1111/j.1748-1716.2009.01971.x · Cited by 200 · see citing works
“There is increasing evidence to suggest that Wnt signalling is important in dendrite development following axon specification (Rosso et al. 2005).”
BackgroundA role for primary cilia in glutamatergic synaptic integration of adult-born neurons
Kumamoto, N., Gu, Y., Wang, J., Janoschka, S., Takemaru, K.-I., Levine, J., & Ge, S. (2012) · Nature Neuroscience · doi:10.1038/nn.3042 · Cited by 196 · see citing works
“Indeed, dendritic development is regulated in other types of neurons by several different Wnt and β-catenin signaling pathway”
Varela-Nallar, L., Alfaro, I. E., Serrano, F. G., Parodi, J., & Inestrosa, N. C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010011107 · Cited by 197 · see citing works
“It has been reported that Wnt signaling plays a key role in diverse aspects of neuronal development and connectivity (2), regulating axon guidance and remodeling (3), dendrite development (4), synapse formation, (5) and synaptic plasticity (6, 7).”
BackgroundBell, K. F. S., Al-Mubarak, B., Martel, M.-A., McKay, S., Wheelan, N., Hasel, P., Márkus, N. M., Baxter, P., Deighton, R. F., Serio, A., et al. (2015) · Nature Communications · doi:10.1038/ncomms8066 · Cited by 191 · see citing works
“Thus, cortical neuronal development is impaired by inhibition of Rac and JNK, mediators of non-canonical Wnt signaling, as well as via the interference of canonical Wnt signaling via inhibition of β -catenin, consistent with previous findings in hippocampal neurons 23, 24, 25 .”
Wnt Signaling: Role in Alzheimer Disease and Schizophrenia
Inestrosa, N. C., Montecinos-Oliva, C., & Fuenzalida, M. (2012) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-012-9417-5 · Cited by 186 · see citing works
“…of the Wnt ligand (right side), β-catenin accumulated in the cytoplasm goes to the nucleus and activates the transcription factor TCF/LEF initiating the transcription of target genes (see Table 1 ) number and length of dendritic branching in immature hippocampal neurons (Rosso et al. 2005 ).”
BackgroundUnifying 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
“Thus, abnormal physiological feedback would affect different circuits in varying ways depending on their cellular and synaptic makeup (Rothwell et al., 2014).”
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“…signaling of JNKs and phosphoinositide3-kinase or extracellular signal-regulated kinase 1/2 (Kita et al. 1998; Waetzig and Herdegen 2003), new evidence suggests crosstalks, e.g., between Wnt signaling and JNKs, whereby JNKs stabilize microtubules (Rosso et al. 2005; Ciani and Salinas 2007).”
BackgroundTRPC6 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
“Overexpression of TRPC6 increased phosphorylation of CaMKIV at Thr196, a site known to be critical for its kinase activity (Selbert et al., 1995), (1.592±0.323, n=3, P=0.042, normalized to total CaMKIV) (Fig.”
BackgroundInfluentialThe Role of Wnt Signalling in Angiogenesis.
Olsen, J. J., Pohl, S., Deshmukh, A. P., Visweswaran, M., Ward, N. C., Arfuso, F., Agostino, M., & Dharmarajan, A. (2017) · Europe PMC (PubMed Central) · Cited by 170 · see citing works
The Wnt signaling pathway: Aging gracefully as a protectionist?
Maiese, K., Li, F., Chong, Z. Z., & Shang, Y. (2008) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2008.01.004 · Cited by 170 · see citing works
“…and DVL can activate Rac and JNK signaling pathways to promote dendritic branching in cultured hippocampal neurons, since application of dominant-negative Rac, administration of dominant-negative JNK, or inhibition of JNK activity can inhibit DVL -mediated dendritic growth (Rosso et al., 2005).”
BackgroundWnt signaling in eye organogenesis
Fuhrmann, S. (2008) · Organogenesis · doi:10.4161/org.4.2.5850 · Cited by 165 · see citing works
Autism spectrum disorder susceptibility gene TAOK2 affects basal dendrite formation in the neocortex
de Anda, F. C., Rosário, A. L., Durak, O., Tran, T. S., Gräff, J., Meletis, K., Rei, D., Soda, T., Madabhushi, R., Ginty, D. D., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3141 · Cited by 171 · see citing works
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
“…in axon guidance, dendrite maturation, potentiation of NMDAR currents, accumulation of the Postsynaptic Density-95 (PSD95) protein, and Acetylcholine neurotransmitter receptor clustering (Cerpa et al. 2011; Farias et al. 2009; Henriquez et al. 2008; Rosso et al. 2005; Shafer et al. 2011).”
InfluentialWnts 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
“On the other hand, it has been shown that the ligand Wnt7b and Dvl, independently of Wnt/GSK-3β, can activate Rac and downstream JNK to increase dendritic length and branching in immature hippocampal neurons (Rosso et al., 2005).”
BackgroundInfluentialPhysiological roles of MKK4 and MKK7: Insights from animal models
Wang, X., Destrument, A., & Tournier, C. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2006.10.016 · Cited by 165 · see citing works
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
“Wnt-7b also regulates dendritic arborization, and this effect is mediated by a non-canonical Wnt signalling cascade that involves JNK activation (Rosso et al. 2005).”
BackgroundWnt/Fz signaling and the cytoskeleton: potential roles in tumorigenesis
Lai, S.-L., Chien, A. J., & Moon, R. T. (2009) · Cell Research · doi:10.1038/cr.2009.41 · Cited by 158 · see citing works
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
“noncanonical Wnt signaling [49], and Wnt-7a is frequently found to play both canonical and noncanonical roles [50, 51].”
WNT secretion and signalling in human disease
Herr, P., Hausmann, G., & Basler, K. (2012) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2012.06.008 · Cited by 158 · see citing works
Redundant expression of canonical Wnt ligands in human breast cancer cell lines
Benhaj, K., Akçalı, K. C., & Öztürk, M. (2006) · Oncology Reports · doi:10.3892/or.15.3.701 · Cited by 157 · see citing works
“WNT7B Maintained Yes/no No Canonical and non-canonical (22,23,35,39,42,43)”
Wnt7a Regulates Multiple Steps of Neurogenesis
Qu, Q., Sun, G., Murai, K., Ye, P., Li, W., Asuelime, G. E., Cheung, Y.-T., & Shi, Y. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.00325-13 · Cited by 150 · see citing works
“Exposure of cultured hippocampal neurons to Wnt7b-conditioned medium increases neurite length and branching of these neurons (45).”
BackgroundInfluentialOpposing roles in neurite growth control by two seven-pass transmembrane cadherins
Shima, Y., Kawaguchi, S., Kosaka, K., Nakayama, M., Hoshino, M., Nabeshima, Y., Hirano, T., & Uemura, T. (2007) · Nature Neuroscience · doi:10.1038/nn1933 · Cited by 154 · see citing works
“To test this hypothesis, we applied JNK inhibitor SP600125, which suppresses dendrite growth by Dvl-mediated noncanonical Wnt signalin”
MethodMultiple functions of the noncanonical Wnt pathway
Gómez‐Orte, E., Sáenz‐Narciso, B., Moreno, S., & Cabello, J. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.06.003 · Cited by 153 · see citing works
A review of the evidence for the canonical Wnt pathway in autism spectrum disorders
Kalkman, H. (2012) · Molecular Autism · doi:10.1186/2040-2392-3-10 · Cited by 142 · see citing works
“The canonical Wnt pathway plays an important role in brain development [30-35] and synaptic function [36-38].”
BackgroundWinding through the WNT pathway during cellular development and demise.
Li, F., Chong, Z. Z., & Maiese, K. (2006) · PubMed · doi:10.14670/hh-21.103 · Cited by 154 · see citing works
What is bad in cancer is good in the embryo: Importance of EMT in neural crest development
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“Interestingly the results with another member of the Rho family, Rac that has been associated with non-canonical Wnt signaling in dendrite morphogenesis [52], were the opposite as its overexpression induced the NC markers [53].”
Klotho protects against mouse renal fibrosis by inhibiting Wnt signaling
Satoh, M., Nagasu, H., Morita, Y., Yamaguchi, T. P., Kanwar, Y. S., & Kashihara, N. (2012) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00460.2012 · Cited by 149 · see citing works
“Wnt activates JNK and rac1 through noncanonical pathway, and these signaling pathways are widely conserved in both vertebrate and invertebrate (24).”
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
“For example, Dvl1 has been shown to bind Rac directly and promote its activity (Rosso et al. 2005).”
BackgroundInfluentialHirai, S.-I., Cui, D. F., Miyata, T., Ogawa, M., Kiyonari, H., Suda, Y., Aizawa, S., Banba, Y., & Ohno, S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2272-06.2006 · Cited by 143 · see citing works
“The Wnt (winglesstype MMTV integration site family) pathway is also a candidate as a DLK regulator because it has been shown to regulate process formation in neural cells via JNK (Rosso et al., 2004; Tissir et al., 2005).”
BackgroundSatoh, W., Gotoh, T., Tsunematsu, Y., Aizawa, S., & Shimono, A. (2006) · Development · doi:10.1242/dev.02274 · Cited by 142 · see citing works
“Furthermore, Sfrp1 also interacts with Wnt7b, and is capable of attenuating the noncanonical Wnt signaling pathway, leading to inhibition of axon guidance (Rosso et al., 2005).”
BackgroundWnt Signaling in Skeletal Muscle Dynamics: Myogenesis, Neuromuscular Synapse and Fibrosis
Cisternas, P., Henríquez, J. P., Brandan, E., & Inestrosa, N. C. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8540-5 · Cited by 139 · see citing works
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
“1008 volume 120 | number 7 | July 2012 • Environmental Health Perspectives activate the scaffold protein Dishevelled, which in turn stimulates dendritic growth via effects on the actin and microtubule cytoskeleton mediated by β-catenin and/or activation of the RhoGTPases Rac and/or JNK [members of the rho family of gu…”
BackgroundMouse models of autism spectrum disorders: The challenge for behavioral genetics
Moy, S. S., Nadler, J. J., Magnuson, T., & Crawley, J. N. (2006) · American Journal of Medical Genetics Part C Seminars in Medical Genetics · doi:10.1002/ajmg.c.30081 · Cited by 135 · see citing works
A chromatin-modifying function of JNK during stem cell differentiation
Tiwari, V. K., Stadler, M. B., Wirbelauer, C., Paro, R., Schübeler, D., & Beisel, C. (2011) · Nature Genetics · doi:10.1038/ng.1036 · Cited by 133 · see citing works
“Our data also agree with observations that activated JNK is required for axon formation and dendritic growt”
ResultWaetzig, V., Zhao, Y., & Herdegen, T. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.08.002 · Cited by 129 · see citing works
The complex world of oligodendroglial differentiation inhibitors
Kremer, D., Aktaş, O., Hartung, H., & Küry, P. (2011) · Annals of Neurology · doi:10.1002/ana.22415 · Cited by 129 · see citing works
Chen, C.-Y., Lin, C.-W., Chang, C.-Y., Jiang, S., & Hsueh, Y. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201008050 · Cited by 130 · see citing works
“In addition to phosphorylating transcription factors, JNK can phosphorylate microtubule-associated proteins and affect microtubule stability and dendrite morphology in mammals (Chang et al., 2003; Björkblom et al., 2005; Rosso et al., 2005; Tararuk et al., 2006; Podkowa et al., 2010).”
Wnt signaling promotes AChR aggregation at the neuromuscular synapse in collaboration with agrin
Henríquez, J. P., Webb, A., Bence, M., Bildsoe, H., Sahores, M., Hughes, S. M., & Salinas, P. C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806300105 · Cited by 129 · see citing works
“To examine the role of Wnt signaling at vertebrate peripheral synapses, we analyzed the Dvl1 mutant mouse, which exhibits a subtle behavioral phenotype (16) as well as defects in dendrite development and in central synaptogenesis (17, 18).”
BackgroundSelf-citationFrizzled-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
“Sprague-Dawley rat embryos and cultured as described previously (Rosso et al., 2005).”
BackgroundMethodSelf-citationMammalian cadherins and protocadherins: about cell death, synapses and processing
Junghans, D., Haas, I. G., & Kemler, R. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.08.008 · Cited by 126 · see citing works
“However, activation of Wnt signaling by depolarization and consequential effects on dendrite branching do not require LEF/TCF-mediated gene activation ([27 ]; see also [29]).”
BackgroundWnts 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
“In addition, Wnts modulate dendritogenesis, axon guidance and synaptogenesis (Ciani and Salinas, 2005; Ille and Sommer, 2005; Rosso et al., 2005; Salinas and Zou, 2008; Budnik and Salinas, 2011; Park and Shen, 2012; Salinas, 2012).”
BackgroundSelf-citationMolecular 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
“In addition to electrical and neurotransmitter stimuli, other extracellular signals such as BDNF, Wnt-7 and EphrinB-EphB interaction, control dendritic growth employing the Rho GTPases (Penzes et al. 2003, Rosso et al. 2005, Takemoto-Kimura et al. 2007).”
BackgroundModulation of GSK-3 as a Therapeutic Strategy on Tau Pathologies
Medina, M., Garrido, J. J., & Wandosell, F. G. (2011) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2011.00024 · Cited by 124 · see citing works
“An alternative system of GSK-3 regulation is represented by the Wnt signaling pathway in which, in the absence of ligand, GSK3β phosphorylates β-catenin, as a part of a degradation signal (for review see, i.e., Moon et al., 2004; Rosso et al., 2005).”
Ataman, B., Ashley, J., Gorczyca, D., Gorczyca, M. G., Mathew, D., Wichmann, C., Sigrist, S. J., & Budnik, V. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600387103 · Cited by 123 · see citing works
Wnts: up-and-coming at the synapse
Speese, S. D., & Budnik, V. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.04.003 · Cited by 123 · see citing works
“More recently, it has been demonstrated that Wnt-7b is expressed in the mouse hippocampus during dendrite maturation, and when transfected into hippocampal cultures,itincreaseddendritecomplexity[19].Asimilareffect was observed by transfecting Dvl-1, indicating that WNT- 7b might signal through DVL-1 [ 19 ].”
BackgroundInfluentialArenas, E. (2014) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mju001 · Cited by 122 · see citing works
The Pattern of Cortical Dysfunction in a Mouse Model of a Schizophrenia-Related Microdeletion
Fénelon, K., Xu, B., Lai, C. S., Mukai, J., Markx, S., Stark, K. L., Hsu, P.-K., Gan, W.-B., Fischbach, G. D., MacDermott, A. B., et al. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1611-13.2013 · Cited by 116 · see citing works
“2 deletions on dendrite and spine formation (Rosso et al., 2005; Evans et al., 2011).”
BackgroundWnt-5aoccludes Aβ oligomer-induced depression of glutamatergic transmission in hippocampal neurons
Cerpa, W. F., Farı́as, G. G., Godoy, J. A., Fuenzalida, M., Bonansco, C., & Inestrosa, N. C. (2010) · Molecular Neurodegeneration · doi:10.1186/1750-1326-5-3 · Cited by 118 · see citing works
“Also the activation of JNK could modulate the actin cytoskeleton and produce a remodeling in the dendritic spines structures [46].”
BackgroundRole of Wnt Signaling in Central Nervous System Injury
Lambert, C., Cisternas, P., & Inestrosa, N. C. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9138-x · Cited by 118 · see citing works
“1b, left) [38].”
Loss- and gain-of-function analyses reveal targets of Pax6 in the developing mouse telencephalon
Holm, P. C., Mader, M. T., Haubst, N., Wizenmann, A., Sigvardsson, M., & Götz, M. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2006.10.008 · Cited by 117 · see citing works
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
“, 2004), Dishevelled (Rosso et al., 2005), some novel genes in Drosophila (Gao et al.”
BackgroundWnt2 Expression and Signaling Is Increased by Different Classes of Antidepressant Treatments
Okamoto, H., Voleti, B., Banasr, M., Sarhan, M., Đurić, V., Girgenti, M. J., Dileone, R., Newton, S. S., & Duman, R. S. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.04.023 · Cited by 116 · see citing works
En1 and Wnt signaling in midbrain dopaminergic neuronal development
dos Santos, M. T. A., & Smidt, M. P. (2011) · Neural Development · doi:10.1186/1749-8104-6-23 · Cited by 111 · see citing works
“Indeed, Wnt signaling seems to take part in most of the processes needed to generate a fully functional neuron (Figure 4A) from a neuronal stem cell, participating in early events, such as neuronal induction [163], anteriorposterior patterning and morphogenesis [164-167] and neuronal precursor proliferation [168-174],…”
BackgroundNucleoredoxin, a Novel Thioredoxin Family Member Involved in Cell Growth and Differentiation
Funato, Y., & Miki, H. (2007) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1550 · Cited by 114 · see citing works
“Indeed, hippocampal neurons obtained from Dvl1 -knockout mice show defective dendrite development (153).”
Farías, G. G., Vallés, A. S., Colombres, M., Godoy, J. A., Toledo, E. M., Lukas, R. J., Barrantes, F. J., & Inestrosa, N. C. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3934-06.2007 · Cited by 108 · see citing works
“, 2006) were prepared as described previously (Hall et al., 2000; Rosso et al., 2004; Quintanilla et al., 2005; Seto and Bellen, 2006).”
MethodHe, C., Gomes, I., Nguyen, T., Jayaram, G., Ram, P. T., Devi, L. A., & Iyengar, R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502812200 · Cited by 107 · see citing works
Li, Y.-C., Li, B., Wan, X.-Z., Zhang, W., Zhong, L., & Tang, S.-J. (2012) · Molecular Brain · doi:10.1186/1756-6606-5-1 · Cited by 91 · see citing works
“More recent studies have revealed that Wnt signaling is critically involved in key processes of the formation and plasticity of the nervous system, including neurogenesis [3], axon guidance [4], dendritic development [5], synaptic differentiation [6] and plasticity [7,8].”
BackgroundTargeting WNT Signaling for Multifaceted Glioblastoma Therapy
McCord, M., Mukouyama, Y., Gilbert, M. R., & Jackson, S. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00318 · Cited by 104 · see citing works
“In addition, DSV1 (a specific isoform of DSV) regulates the development of hippocampal dendrites in mice (Rosso et al., 2005).”
BackgroundModulating Wnt signaling at the root: Porcupine and Wnt acylation
Torres, V. I., Godoy, J. A., & Inestrosa, N. C. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.02.009 · Cited by 104 · see citing works
- 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
- Venue
- Nature Neuroscience
- Published
- 2004-12-19
- Volume
- 8
- Issue
- 1
- Pages
- 34-42
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- 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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