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Branching out: mechanisms of dendritic arborization
Open accessAbstract
Type-specific dendrite morphology is a hallmark of the neuron and has important functional implications in determining what signals a neuron receives and how these signals are integrated. During the past two decades, studies on dendritic arborization neurons in Drosophila melanogaster have started to identify mechanisms of dendrite morphogenesis that may have broad applicability to vertebrate species. Transcription factors, receptor-ligand interactions, various signalling pathways, local translational machinery, cytoskeletal elements, Golgi outposts and endosomes have been identified as contributors to the organization of dendrites of individual neurons and the placement of these dendrites in the neuronal circuitry. Further insight into these mechanisms will improve our understanding of how the nervous system functions and might help to identify the underlying causes of some neurological and neurodevelopmental disorders.
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“Dendritic morphogenesis, synaptogenesis and continued activity-dependent remodelling of synaptic connections are critical for the development and maintenance of functional neuronal networks.11, 12, 13, 14, 15”
From The autism and schizophrenia associated gene CYFIP1 is critical for the maintenance of dendritic complexity and the stabilization of mature spines (2014) · cites this paper as [11]
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“We refer the reader to other recent reviews in which individual mechanisms or topics are treated in greater depth (Baier 2013, Hong & Luo 2014, Jan & Jan 2010, Puram & Bonni 2013, Zipursky & Grueber 2013).”
InfluentialDevelopmental regulation of axon branching in the vertebrate nervous system
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“The secretory pathway in general and endosomal/lysosomal trafficking in particular are important for neurite outgrowth (Horton et al, 2005; Sann et al, 2009; Jan & Jan, 2010).”
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“Impoverished neuronal arborization is a structural correlate of several neurodevelopmental disorders, such as autism and Down syndrome (Jan and Jan, 2010).”
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Centrosomin represses dendrite branching by orienting microtubule nucleation
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“…Membrane Protein that Stabilizes Dendritic Branches Although transcription factors are well-established determinants of sensory neuron fate, the downstream pathways that they regulate are largely unknown (Jan and Jan, 2010; Jinushi-Nakao et al., 2007; Parrish et al., 2006; Sulkowski et al., 2011).”
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“In general, Rac1 regulates actin nucleation and polymerization, whereas the RhoA controls the contractibility of actin cytoskeleton through its downstream effector ROCK (Scott and Luo, 2001; Govek et al., 2005; Jan and Jan, 2010).”
BackgroundInfluentialTranscriptional Regulation of Neuronal Polarity and Morphogenesis in the Mammalian Brain
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Control of Neuronal Morphology by the Atypical Cadherin Fat3
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“Although pathways establishing axonal versus dendritic identity are being elucidated, the steps that determine how many neurites are retained to become primary dendrites are poorly understood (Jan and Jan, 2010).”
InfluentialBTBD3 Controls Dendrite Orientation Toward Active Axons in Mammalian Neocortex
Matsui, A., Tran, M., Yoshida, A., Kikuchi, S. S., Mami, U., Ogawa, M., & Shimogori, T. (2013) · Science · doi:10.1126/science.1244505 · Cited by 103
CLIP-170 and IQGAP1 Cooperatively Regulate Dendrite Morphology
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“Their development involves several cellular processes, among which both cytoskeletal rearrangement and stabilization play important roles (Urbanska et al., 2008; Jan and Jan, 2010).”
BackgroundLitterman, N. K., Ikeuchi, Y., Gallardo, G., O’Connell, B. C., Sowa, M. E., Gygi, S. P., Harper, J. W., & Bonni, A. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001060 · Cited by 106
“signaling is integrated with other cell-intrinsic regulators of dendrite morphogenesis, including transcription factors, that have been implicated in dendrite patterning”
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“Dendritic morphology varies greatly according to neuronal cell type, and specific morphological characteristics are linked with various functional implications (Jan and Jan, 2010).”
BackgroundMACF1 regulates the migration of pyramidal neurons via microtubule dynamics and GSK-3 signaling
Ka, M., Jung, E., Mueller, U. W., & Kim, W.-Y. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.09.009 · Cited by 103
“Accordingly, problems in neuron migration during development cause brain malformations and are associated with a variety of neurological diseases such as mental retardation, autism, and schizophrenia (Gleeson and Walsh, 2000; Jan and Jan, 2010; Kaufmann and Moser, 2000; Wegiel et al., 2010).”
BackgroundA scaling law derived from optimal dendritic wiring
Cuntz, H., Mathy, A., & Häusser, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200430109 · Cited by 104
Cell-intrinsic drivers of dendrite morphogenesis
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“Along with the secretory pathway, the endocytic pathway may regulate dendrite growth and branching by influencing the density of cell surface receptors involved in dendrite morphogenesis (Jan and Jan, 2010).”
BackgroundThe transmembrane LRR protein DMA-1 promotes dendrite branching and growth in C. elegans
Liu, O. W., & Shen, K. (2011) · Nature Neuroscience · doi:10.1038/nn.2978 · Cited by 100
“The study of the four classes of dendritic arborization neurons, which vary by the complexity of branching, has helped to illuminate important dendrite organizational principles, such as the ability to identify and avoid sister dendrites from the same neuron (self-avoidance) and the ability of dendrites from neurons o…”
BackgroundEarly Events in Axon/Dendrite Polarization
Cheng, P., & Poo, M. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113618 · Cited by 107
Molecular mechanisms of dendrite morphogenesis
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“While some of these mechanisms and pathways have also been implicated in dendrite morphogenesis in other types of neurons, discussing other types of neurons is beyond the scope of this review and we refer the readers to other excellent reviews (Jan and Jan, 2010; de la Torre-Ubieta and Bonni, 2011) on these topics.”
BackgroundZipcode Binding Protein 1 Regulates the Development of Dendritic Arbors in Hippocampal Neurons
Perycz, M., Urbanska, A. S., Krawczyk, P. S., Parobczak, K., & Jaworski, J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2387-10.2011 · Cited by 95
“Several cellular processes, including cytoskeleton dynamics and translation, are engaged to support proper dendritic development (Urbanska et al., 2008; Jan and Jan, 2010).”
BackgroundYamashita, N., Ohshima, T., Nakamura, F., Kolattukudy, P. E., Honnorat, J., Mikoshiba, K., & Goshima, Y. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5563-11.2012 · Cited by 95
“Recently, it has been well recognized that extracellular environments play important roles in regulating cell fate, proliferation, polarity and other cellular functions in non-neuronal as well as neuronal tissues (Craig and Banker, 1994; Breunig et al., 2007; Parrish et al., 2007; Jan and Jan, 2010).”
BackgroundWarre-Cornish, K. M., Perfect, L., Nagy, R., Duarte, R. R. R., Reid, M. J., Raval, P., Mueller, A., Evans, A., Couch, A. C. M., Ghevaert, C., et al. (2020) · Science Advances · doi:10.1126/sciadv.aay9506 · Cited by 90
“Furthermore, the macrocephaly present in some ASD cases has been attributed to increased dendrite number and size (46).”
BackgroundA RhoA Signaling Pathway Regulates Dendritic Golgi Outpost Formation
Quassollo, G., Wojnacki, J., Salas, D. A., Gastaldi, L., Marzolo, M., Conde, C. B., Bisbal, M., Couve, A., & Cáceres, A. (2015) · Current Biology · doi:10.1016/j.cub.2015.01.075 · Cited by 93
“Alternatively, dendritic GOP biogenesis may be explained by fragmentation of the somatic GA followed by dispersion and minus-end microtubule-based transport into dendrites [8, 9, 45].”
BackgroundLarval Defense against Attack from Parasitoid Wasps Requires Nociceptive Neurons
Robertson, J., Tsubouchi, A., & Tracey, W. D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078704 · Cited by 93
“The class IV neurons are the primary nociceptors of Drosophila larvae and have an elaborate dendritic field which tiles the larval body wall [23-28,31].”
BackgroundGunnewiek, T. M. K., van Hugte, E., Frega, M., Guardia, G. S., Foreman, K., Panneman, D. M., Mossink, B., Linda, K., Keller, J. M., Schubert, D., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107538 · Cited by 90
“Energy is required to fuel the formation and synchronized activity of neuronal circuits (Jan and Jan, 2010; Spruston, 2008).”
Dendrite Self-Avoidance Requires Cell-Autonomous Slit/Robo Signaling in Cerebellar Purkinje Cells
Gibson, D. A., Tymanskyj, S. R., Yuan, R., Leung, H. C., Lefebvre, J. L., Sanes, J. R., Chédotal, A., & Ma, L. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.009 · Cited by 89
“local molecular interactions during dendritic development (Jan and Jan, 2010).”
InfluentialNetrin (UNC-6) mediates dendritic self-avoidance
Smith, C. J., Watson, J. D., VanHoven, M. K., Colón‐Ramos, D. A., & Miller, D. M. (2012) · Nature Neuroscience · doi:10.1038/nn.3065 · Cited by 90
Weir, R. K., Bauman, M. D., Jacobs, B., & Schumann, C. M. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24332 · Cited by 87
Srivastava, D. P., Woolfrey, K. M., Jones, K. A., Anderson, C. T., Smith, K. R., Russell, T. A., Lee, H., Yasvoina, M. V., Wokosin, D. L., Özdinler, P. H., et al. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001350 · Cited by 85
“field [1].”
Copf, T. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.04.008 · Cited by 92
“One of the possible reasons behind macrocephaly has been proposed to include abnormal dendrites number and size, which might stem from either increased dendritic branching, and/or reduced dendritic pruning [4].”
InfluentialRAB-10 Regulates Dendritic Branching by Balancing Dendritic Transport
Taylor, C. A., Yan, J., Howell, A. S., Dong, X., & Shen, K. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005695 · Cited by 83
“Dendrites are more sensitive than axons in their reliance on the membrane supply from secretory pathways [2,6], and they have distinct transport needs.”
BackgroundMohammad, H., Marchisella, F., Ortega‐Martínez, S., Hollós, P., Eerola, K., Komulainen, E., Kulesskaya, N., Freemantle, E., Fagerholm, V., Savontous, E., et al. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.203 · Cited by 93
Light-Induced Structural and Functional Plasticity in Drosophila Larval Visual System
Yuan, Q., Xiang, Y., Yan, Z., Han, C., Jan, L. Y., & Jan, Y. N. (2011) · Science · doi:10.1126/science.1207121 · Cited by 83
Self-citationBlizinsky, K. D., Diaz-Castro, B., Forrest, M. P., Schürmann, B., Bach, A. P., Martin-de-Saavedra, M. D., Wang, L., Csernansky, J. G., Duan, J., & Penzes, P. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1607014113 · Cited by 76
“Dendrites constitute the receptive field of neurons, and alterations in dendritic morphology could contribute to abnormalities in cortical connectivity (26).”
BackgroundTranscription factors and effectors that regulate neuronal morphology
Santiago, C., & Bashaw, G. J. (2014) · Development · doi:10.1242/dev.110817 · Cited by 81
Dendritic structural plasticity
Tavosanis, G. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20951 · Cited by 89
“In most systems analyzed tiling could be achieved through homotypic repulsion of branches derived from neurons of the same type (recently reviewed by Jan and Jan (2010)).”
BackgroundFischer, R. S., Lam, P., Anna Huttenlocher, A., & Waterman, C. M. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.08.015 · Cited by 79
“Cells can stably maintain a branched architecture over time as in dendritic cells, neurons and melanocytes (Collin and Milne, 2016; Jan and Jan, 2010; Mort et al., 2015), or the branches can be dynamic and contribute to invasive migratory and pathfinding developmental programs such as elaboration…”
BackgroundPremutation CGG-repeat expansion of the Fmr1 gene impairs mouse neocortical development
Cunningham, C. L., Martínez‐Cerdeño, V., Porras, E. N., Prakash, A. N., Angelastro, J. M., Willemsen, R., Hagerman, P. J., Pessah, I. N., Berman, R. F., & Noctor, S. C. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq432 · Cited by 81
Yoshino, J., Morikawa, R. K., Hasegawa, E., & Emoto, K. (2017) · Current Biology · doi:10.1016/j.cub.2017.06.068 · Cited by 93
Shen, T., Ji, F., Wang, Y., Lei, X., Zhang, D., & Jiao, J. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1295 · Cited by 82
“Neuronal dendritic arborization is acquired soon after neurons have entered their destined cortical layer in the brain (50).”
BackgroundUltanir, S. K., Yadav, S., Hertz, N. T., Oses-Prieto, J. A., Claxton, S., Burlingame, A. L., Shokat, K. M., Jan, L. Y., & Jan, Y.-N. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.025 · Cited by 75
“Dendrite arborization and synapse formation are critical for wiring the neural circuitry (Jan and Jan, 2010; Parrish et al., 2006).”
Self-citationBustos, F. J., Varela‐Nallar, L., Campos, M., Henríquez, B., Phillips, M. A., Opazo, C., Aguayo, L. G., Montecino, M. A., Constantine‐Paton, M., Inestrosa, N. C., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094037 · Cited by 75
Development of larval motor circuits in Drosophila
Kohsaka, H., Okusawa, S., Itakura, Y., Fushiki, A., & Nose, A. (2012) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2012.01347.x · Cited by 85
“…available in this species, has enabled researchers to unravel basic principles underlying neural development across species, including molecular mechanisms of neural specification, axon guidance, dendrite formation and synaptogenesis (Doe 2008; Jan & Jan 2010; Kolodkin & Tessier-Lavigne 2011).”
BackgroundMethodZou, W., Dong, X., Broederdorf, T., Shen, A., Kramer, D. A., Shi, R., Liang, X., Miller, D. M., Xiang, Y. K., Yasuda, R., et al. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.04.008 · Cited by 69
“Genetic and cell biological studies showed that dendrite arborization requires both extrinsic and intrinsic mechanisms, including ligand-receptor signaling, transcription regulation, cytoskeleton remodeling, and membrane trafficking (Dong et al., 2015; Jan and Jan, 2010).”
BackgroundThe cellular basis of dendrite pathology in neurodegenerative diseases
Kweon, J. H., Kim, S., & Lee, S. B. (2017) · BMB Reports · doi:10.5483/bmbrep.2017.50.1.131 · Cited by 73
“very crucial roles in the control of their growth (14).”
BackgroundDendrite architecture organized by transcriptional control of the F-actin nucleator Spire
Ferreira, T., Ou, Y., Li, S. S. Y., Giniger, E., & van Meyel, D. J. (2014) · Development · doi:10.1242/dev.099655 · Cited by 73
“…expression of the MT-severing protein Spastin (Jinushi-Nakao et al., 2007; Ye et al., 2011), and Cut is thought to promote F-actin because high Cut levels coincide with class III morphology and the appearance of F-actin-rich spiked protrusions (Grueber et al., 2003; Jinushi-Nakao et al., 2007).”
BackgroundResultInfluentialCrescenzo, A. H. D., Panoutsopoulos, A. A., Tat, L., Schaaf, Z. A., Racherla, S., Henderson, L., Leung, K., Greene, N. D. E., Green, R., & Zarbalis, K. S. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa248 · Cited by 79
“These findings also fit in with studies that have reported dendritic abnormalities in several human neurodevelopmental syndromes associated with intellectual disability such as Down, Rett, and fragile-X syndromes (Kaufmann and Moser 2000).”
Principles of branch dynamics governing shape characteristics of cerebellar Purkinje cell dendrites
Fujishima, K., Horie, R., Mochizuki, A., & Kengaku, M. (2012) · Development · doi:10.1242/dev.081315 · Cited by 71
“Various molecular signals have been identified as regulators of dendritic arborization patterns (Jan and Jan, 2010).”
BackgroundMemo1-Mediated Tiling of Radial Glial Cells Facilitates Cerebral Cortical Development
Nakagawa, N., Plestant, C., Yabuno-Nakagawa, K., Li, J., Lee, J. C. L., Huang, C.-W., Lee, A., Krupa, O., Adhikari, A., Thompson, S., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.049 · Cited by 68
“The neuronal dendritic arborization is streamlined by a self-avoidance mechanism to achieve the non-overlapping growth of dendrites (Jan and Jan, 2010).”
Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons
Xie, Q., Brbić, M., Horns, F., Kolluru, S. S., Jones, R. C., Li, J., Reddy, A. R., Xie, A., Kohani, S., Li, Z., et al. (2021) · eLife · doi:10.7554/elife.63450 · Cited by 72
“During wiring, neurons extend their neurites to a coarse targeting region, elaborate their terminal structures, select pre- and post-synaptic partners, and finally form synaptic connections (Sanes & Yamagata, 2009; Jan & Jan, 2010; Kolodkin & Tessier-Lavigne, 2011; Sanes & Zipursky, 2020).”
BackgroundLocal endocytosis triggers dendritic thinning and pruning in Drosophila sensory neurons
Kanamori, T., Yoshino, J., Yasunaga, K.-I., Dairyo, Y., & Emoto, K. (2015) · Nature Communications · doi:10.1038/ncomms7515 · Cited by 74
“Mutants and transgenic lines used in this study are as follows: (1) pickpocket (ppk)-Gal4 (X), (2) UAS-mCherry-a-tubulin (second, Bloomington #25774), (3) UAS-GCaMP6s (second, Bloomington#42746), (4) UAS-mCD8-RFP (X), (5) UAS-mCD8-GFP (X, from a Bloomington LL4 line), (6) UAS-PA-TagRFP (third, this study), (7) UAS-pHl…”
Iyer, E. P. R., Iyer, S. C., Sullivan, L. F., Wang, D. Y. Q., Meduri, R., Graybeal, L. L., & Cox, D. N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072434 · Cited by 72
“Hence, not surprisingly, several TFs previously implicated in mediating da neuron dendrite morphogenesis including Knot, Cut, Spineless and Abrupt [4] were not uncovered due to their high expression in several non-da neuron tissue tissues including high expression in the ventral nerve chord [29].”
BackgroundResultStraub, J., Konrad, E. D. H., Grüner, J., Toutain, A., Bok, L. A., Cho, M. T., Crawford, H. P., Dubbs, H. A., Douglas, G., Jobling, R. K., et al. (2017) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2017.11.008 · Cited by 76
Zou, W., Shen, A., Dong, X., Tugizova, M. S., Xiang, Y. K., & Shen, K. (2016) · eLife · doi:10.7554/elife.18345 · Cited by 71
“Dendritic growth and branching is often cell-type specific and follows a stereotyped trajectory, suggestive of precise dendrite guidance mechanisms (Dong et al., 2015; Jan and Jan, 2010).”
BackgroundDesign principles and developmental mechanisms underlying retinal mosaics
Reese, B. E., & Keeley, P. W. (2014) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12139 · Cited by 71
“…comparable principles appear to be at work (Sanes & Zipursky, 2010), and the molecular and genetic underpinnings of some of those population dynamics are being revealed in exquisite detail (Jan & Jan, 2010), with attendant fascination in the elegance of their execution (Millard & Zipursky, 2008).”
Tanabe, K., Kani, S., Shimizu, T., Bae, Y., Abe, T., & Hibi, M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3352-10.2010 · Cited by 74
“Although a number of transcriptional, intracellular signaling, and extracellular molecules are known to regulate dendritic growth or branching (Parrish et al., 2007; Jan and Jan, 2010), how the number of primary dendrites is controlled is unknown.”
BackgroundIn situ cell-type-specific cell-surface proteomic profiling in mice
Shuster, S. A., Li, J., Chon, U., Sinantha-Hu, M. C., Luginbuhl, D. J., Udeshi, N. D., Carey, D. K., Takeo, Y. H., Xie, Q., Xu, C., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.09.025 · Cited by 70
“Neural circuit assembly comprises many interwoven processes, such as axon guidance and dendrite morphogenesis, each critically requiring CSPs (Jan and Jan, 2010; Kolodkin and Tessier-Lavigne, 2011; Sanes and Zipursky, 2020; Zipursky and Sanes, 2010).”
Protocadherins branch out: Multiple roles in dendrite development
Keeler, A. B., Molumby, M. J., & Weiner, J. A. (2015) · Cell Adhesion & Migration · doi:10.1080/19336918.2014.1000069 · Cited by 70
Development of the embryonic and larval peripheral nervous system of Drosophila
Singhania, A., & Grueber, W. B. (2014) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.135 · Cited by 69
Metadata
- Authors
- Jan, Y.-N., & Jan, L. Y.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Jan, Yuh-Nung
- Venue
- Nature Reviews Neuroscience
- Published
- 2010-05
- Volume
- 11
- Issue
- 5
- Pages
- 316-328
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- PMC
- PMC3079328
- OpenAlex
- W2065943966
- Cited by
- 693
- References
- 162
- Citations by year
- 2026: 15 · 2025: 41 · 2024: 24 · 2023: 29 · 2022: 33 · 2021: 41 · 2020: 71 · 2019: 41 · 2018: 45 · 2017: 49 · 2016: 52 · 2015: 38 · 2014: 58 · 2013: 53 · 2012: 53
- FWCI
- 4.49
- Type
- journal article
- Language
- en
- Update notices
- erratum (2010-06-01)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature reviews. Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health
- National Institute of Mental Health (R01MH084234)
- National Institute of Neurological Disorders and Stroke (R37NS040929)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- dendritic branching, dendrite morphogenesis, dendritic morphology, Drosophila melanogaster, transcription factors, ligand-receptor interactions, signaling pathways, local translation, cytoskeleton, endosomes, autism spectrum disorder, neurodevelopmental disorders, neural circuits
- MeSH terms
- Animals, Axons, Dendrites, Humans, Models, Neurological, Morphogenesis, Neurons, Signal Transduction
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