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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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“…the stereotyped organization of identified dendritic arborization (da) neurons in 6 Drosophila, which have contributed much to the physiological functions of nociception and proprioception (Corty et al., 2009; Grueber et al., 2002; Im and Galko, 2012; Jan and Jan, 2010; Landgraf and Evers, 2005).”
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“The number of primary dendrites arising from the cell body, higher-order dendrites emerging from primary dendrites, and dendritic branching patterns appear to be critical for neuronal function (Jan and Jan, 2010).”
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“Lastly, MFs are constituted by actin filaments, and their polymerization dynamic is closely associated with the activity of actin-binding proteins (ABPs) like drebrin and ADF/cofilin.”
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Dendrite remodeling in development and disease
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InfluentialAchieving functional neuronal dendrite structure through sequential stochastic growth and retraction
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BackgroundSarcomeres Pattern Proprioceptive Sensory Dendritic Endings through UNC-52/Perlecan in C. elegans
Liang, X., Dong, X., Moerman, D. G., Shen, K., & Wang, X. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.03.010 · Cited by 54
“Most of our understanding of the molecular mechanisms regulating dendritic branching comes from studies of the dendritic arborization neurons in Drosophila melanogaster (Corty et al., 2009; Jan and Jan, 2010).”
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Qi, C., Liu, S., Qin, R., Zhang, Y., Wang, G., Shang, Y., Wang, Y., & Liang, J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3647-13.2014 · Cited by 58
“BDNF has been characterized as a critical factor in promoting dendritic morphogenesis in various types of neurons (Jan and Jan, 2010; Park and Poo, 2013).”
BackgroundInfluentialLrig1 is a cell‐intrinsic modulator of hippocampal dendrite complexity and BDNF signaling
Alsina, F. C., Hita, F. J., Fontanet, P., Irala, D., Hedman, H., Ledda, F., & Paratcha, G. (2016) · EMBO Reports · doi:10.15252/embr.201541218 · Cited by 53
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APC/C Cdh1 -Rock2 pathway controls dendritic integrity and memory
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“Whereas neurogenesis is the main determinant of embryonic brain growth (12, 15), dendrite length and dendritic arbor complexity are key determinants of adult brain size (16).”
Reviewing the Role of the Efferent Vestibular System in Motor and Vestibular Circuits
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“This information is useful though, because dendritic patterns and arbor could reflect specific transcription factors, cell surface receptors, various cytoskeletal elements and pathways, as well as interactions between synaptically connected neurons (reviewed in Jan and Jan, 2010).”
BackgroundThe many disguises of the signalling endosome
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Transcription factor Acj6 controls dendrite targeting via a combinatorial cell-surface code
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Activity-Dependent Regulation of Dendritic Complexity by Semaphorin 3A through Farp1
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“Mechanisms that regulate the development of dendritic trees include soluble cues, adhesive interactions, and neuronal activity (Wong and Ghosh, 2002; Polleux and Ghosh, 2008; Jan and Jan, 2010).”
BackgroundMao, C., Xiong, Y., Xiong, Z., Wang, Q., Zhang, Y., & Jin, S. (2014) · Development · doi:10.1242/dev.097774 · Cited by 54
“arbors to class IV neurons with the most highly branched dendritic trees (Grueber et al., 2002; Jan and Jan, 2010).”
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“It is known that distinct molecules regulate outgrowth and branching (Jan and Jan 2010).”
BackgroundRosário, M., Schuster, S., Jüttner, R., Parthasarathy, S., Tarabykin, V. S., & Birchmeier, W. (2012) · Genes & Development · doi:10.1101/gad.191593.112 · Cited by 53
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“Research in the past decades has elucidatedmechanisms underlying dendrite morphogenesis (Jan and Jan, 2010) and synapse formation (S€udhof, 2018; Yogev and Shen, 2014).”
BackgroundHomotypic Regulation of Neuronal Morphology and Connectivity in the Mouse Retina
Lee, S., Cowgill, E. J., Al-Nabulsi, A., Quinn, E. J., Evans, S. Μ., & Reese, B. E. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2844-11.2011 · Cited by 49
“Multiple processes coordinate the assembly of this precise circuitry, including cell-intrinsic instructions that direct and constrain morphogenesis (Jan and Jan, 2010), and activity-dependent mechanisms that establish the synaptic contacts underlying these neural circuits (Holtmaat and Svoboda, 2009).”
BackgroundMeltzer, S., Yadav, S., Lee, J., Soba, P., Younger, S. H., Jin, P., Zhang, W., Parrish, J. Z., Jan, L. Y., & Jan, Y. N. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.020 · Cited by 51
Self-citationKeeler, A. B., Schreiner, D., & Weiner, J. A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.642306 · Cited by 50
The role of MACF1 in nervous system development and maintenance
Moffat, J. J., Ka, M., Jung, E., Smith, A. L., & Kim, W.-Y. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.05.020 · Cited by 49
Tang, L. T. H., Díaz-Balzac, C. A., Rahman, M., Ramírez-Suárez, N. J., Salzberg, Y., Lázaro‐Peña, M. I., & Bülow, H. E. (2019) · eLife · doi:10.7554/elife.38949 · Cited by 47
“Both genes that act within the developing neurons and in surrounding tissues are crucial to establish distict dendritic structures during development (JAN AND JAN 2010; DONG et al. 2015; LEFEBVRE et al. 2015).”
BackgroundNmnat exerts neuroprotective effects in dendrites and axons
Wen, Y., Parrish, J. Z., He, R., Zhai, R. G., & Kim, M. D. (2011) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2011.05.002 · Cited by 49
“…suggestive of a widespread neuroprotective role for Nmnat in the CNS. Nmnat is neuroprotective in dendrites Although our understanding of the molecular mechanisms that regulate the growth and patterning of dendritic arbors has significantly progressed (Jan and Jan, 2010), the Mol Cell Neurosci.”
BackgroundTransient localization of the Arp2/3 complex initiates neuronal dendrite branching in vivo
Stürner, T., Tatarnikova, A., Mueller, J. O., Schaffran, B., Cuntz, H., Zhang, Y., Némethová, M., Bogdan, S., Small, V., & Tavosanis, G. (2019) · Development · doi:10.1242/dev.171397 · Cited by 50
“To address the specific regulatory events at the core of the process of initial dendrite branch formation, we concentrated on the Drosophila larval sensory da neurons (Gao et al., 1999; Jan and Jan, 2010; Singhania and Grueber, 2014).”
BackgroundCentella asiatica attenuates Aβ-induced neurodegenerative spine loss and dendritic simplification
Gray, N. E., Zweig, J. A., Murchison, C., Caruso, M., Matthews, D. G., Kawamoto, C., Harris, C. J., Quinn, J. F., & Soumyanath, A. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.02.072 · Cited by 49
“The complex regulation of spine formation and arborization potentially implicates a variety of biological pathways and processes including histone modification, transcription factors, microRNAs, kinases, hormones and cell surface receptors [37, 38].”
BackgroundSalzberg, Y., Ramírez-Suárez, N. J., & Bülow, H. E. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004657 · Cited by 49
“The understanding of sensory dendrite morphogenesis has been greatly advanced through studies in the fly Drosophila melanogaster (reviewed in [3]).”
BackgroundLee, S. B., Bagley, J. A., Lee, H. Y., Jan, L. Y., & Jan, Y. N. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113573108 · Cited by 49
“In summary, our study reveals that a subset of polyQ proteins cause neuronal type-specific dendrite defects closely associated with specific alterations in the actin cytoskeleton, which play critical roles in neuronal morphogenesis (13).”
BackgroundInfluentialSelf-citationThe Ret receptor regulates sensory neuron dendrite growth and integrin mediated adhesion
Soba, P., Han, C., Zheng, Y., Perea, D., Miguel‐Aliaga, I., Jan, L. Y., & Jan, Y. N. (2015) · eLife · doi:10.7554/elife.05491 · Cited by 48
“Two of the organizing principles in dendrite 41 development are self-avoidance and tiling (Jan and Jan, 2010; Grueber and Sagasti, 42 2010; Zipursky and Sanes, 2010).”
BackgroundSelf-citationTerada, S.-I., Matsubara, D., Onodera, K., Matsuzaki, M., Uemura, T., & Usui, T. (2016) · eLife · doi:10.7554/elife.12959 · Cited by 58
Kalirin-9 and Kalirin-12 Play Essential Roles in Dendritic Outgrowth and Branching
Yan, Y., Eipper, B. A., & Mains, R. E. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu182 · Cited by 49
Lrrk regulates the dynamic profile of dendritic Golgi outposts through the golgin Lava lamp
Lin, C., Li, H., Lee, Y., Cheng, Y.-J., Wu, R., & Chien, C. (2015) · The Journal of Cell Biology · doi:10.1083/jcb.201411033 · Cited by 48
Cellular Bases of Olfactory Circuit Assembly Revealed by Systematic Time-Lapse Imaging
Li, T., Tian-ming Fu, B., Wong, K. K. L., Li, H., Xie, Q., Luginbuhl, D. J., Wagner, M. J., Betzig, E., & Luo, L. (2021) · Cell · doi:10.1016/j.cell.2021.08.030 · Cited by 48
How does morphology relate to function in sensory arbors?
Hall, D. H., & Treinin, M. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.07.004 · Cited by 50
Bleckert, A., & Wong, R. (2010) · BioEssays · doi:10.1002/bies.201000095 · Cited by 53
Skupien, A., Konopka, A., Trzaskoma, P., Labus, J., Gorlewicz, A., Swiech, L. J., Babraj, M., Doleżyczek, H., Figiel, I., Ponimaskin, E. G., et al. (2014) · Journal of Cell Science · doi:10.1242/jcs.154542 · Cited by 46
“…trees and their functional capabilities are altered in various psychiatric and neurodevelopmental disorders, such as schizophrenia, Down’s syndrome, fragile X syndrome, Angelman’s syndrome, Rett’s syndrome and autism (Kaufmann and Moser, 2000; Jan and Jan, 2010; Kulkarni and Firestein, 2012).”
BackgroundInfluentialAmpuero, E., Jury, N., Härtel, S., Marzolo, M., & van Zundert, B. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25605 · Cited by 47
Glycerophospholipids – Emerging players in neuronal dendrite branching and outgrowth
Ziegler, A. B., & Tavosanis, G. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.12.009 · Cited by 47
Wietek, J., Rodriguez-Rozada, S., Tutas, J., Tenedini, F. M., Grimm, C., Oertner, T. G., Soba, P., Hegemann, P., & Wiegert, J. S. (2017) · Scientific Reports · doi:10.1038/s41598-017-14330-y · Cited by 49
In vivo dendrite regeneration after injury is different from dendrite developmentPreprint
Thompson-Peer, K. L., DeVault, L., Li, T., Jan, L. Y., & Jan, Y. N. (2016) · Genes & Development · doi:10.1101/gad.282848.116 · Cited by 45
“Dendrite arborization (da) neurons are sensory neurons in the Drosophila larval peripheral nervous system (PNS) that can be grouped into four classes based on the class-specific expression of genes and the complexity of their dendrite arbors (Jan and Jan 2010).”
Self-citationThe unfolded protein response is required for dendrite morphogenesis
Wei, X., Howell, A. S., Dong, X., Taylor, C. A., Cooper, R. C., Zhang, J., Zou, W., Sherwood, D. R., & Shen, K. (2015) · eLife · doi:10.7554/elife.06963 · Cited by 46
Iyer, S. C., Iyer, E. P. R., Meduri, R., Rubaharan, M., Kuntimaddi, A., Karamsetty, M., & Cox, D. N. (2013) · Journal of Cell Science · doi:10.1242/jcs.131144 · Cited by 47
“Several studies have focused on the identification and characterization of transcription factors that function to specify and control dendritic growth, branching and cytoskeletal rearrangements (Jan and Jan, 2010; Corty et al., 2009; Ye et al., 2011; Iyer et al., 2012; Nagel et al., 2012).”
BackgroundCyr61, a Matricellular Protein, Is Needed for Dendritic Arborization of Hippocampal Neurons
Malik, A. R., Urbańska, M., Góźdź, A., Swiech, L. J., Nagalski, A., Perycz, M., Błażejczyk, M., & Jaworski, J. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.411629 · Cited by 45
“First, these processes are crucial for dendritic growth (3, 4).”
BackgroundMechanisms that regulate morphogenesis of a highly branched neuron in C. elegans
Sundararajan, L., Stern, J. L., & Miller, D. M. (2019) · Developmental Biology · doi:10.1016/j.ydbio.2019.04.002 · Cited by 43
“The crucial role of the cytoskeleton in dendrite outgrowth is well-established and thus would also be expected to drive PVD morphogenesis (Delandre et al., 2016; Y. N. Jan and L. Y. Jan 2010; Luo, 2002).”
BackgroundDeterministic and Stochastic Rules of Branching Govern Dendrite Morphogenesis of Sensory Neurons
Palavalli, A., Tizón-Escamilla, N., Rupprecht, J.-F., & Lecuit, T. (2020) · Current Biology · doi:10.1016/j.cub.2020.10.054 · Cited by 45
Bimodal Control of Dendritic and Axonal Growth by the Dual Leucine Zipper Kinase Pathway
Wang, X., Kim, J. H., Bazzi, M., Robinson, S. D., Collins, C. A., & Ye, B. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001572 · Cited by 44
“The dendrites and axons of these neurons are distinguishable from each other at both molecular and organelle levels in a way that resembles mammalian neurons [33].”
BackgroundContext-aware modeling of neuronal morphologies
Torben-Nielsen, B., & Schutter, E. D. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00092 · Cited by 49
“Sensation of these molecules then influences when a growth cone branches or terminates as well as the direction of elongation (Itoh al., 1993; 2010).”
BackgroundAFF-1 fusogen can rejuvenate the regenerative potential of adult dendritic trees via self-fusion
Kravtsov, V., Oren‐Suissa, M., & Podbilewicz, B. (2017) · Development · doi:10.1242/dev.150037 · Cited by 44
Krieger, M., Both, M., Kranig, S. A., Pitzer, C., Klugmann, M., Vogt, G., Draguhn, A., & Schneider, A. (2012) · Scientific Reports · doi:10.1038/srep00697 · Cited by 42
Developmental Plasticity of the Dendritic Compartment: Focus on the Cytoskeleton
Urbańska, M., Swiech, L. J., & Jaworski, J. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-3-7091-0932-8_12 · Cited by 42
Koichiro, Tsujimura, K., Nakashima, H., & Nakashima, K. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.705749 · Cited by 43
“The Wnt-dishevelled pathway regulates dendrite morphogenesis in mammalian neurons, whereas Rab5, a component of the early endocytic pathway, promotes dendritic branching of fly dendritic arborization neurons (6).”
BackgroundPhospholipid Homeostasis Regulates Dendrite Morphogenesis in Drosophila Sensory Neurons
Meltzer, S., Bagley, J. A., Perez, G. L., O’Brien, C. E., DeVault, L., Guo, Y., Jan, L. Y., & Jan, Y. N. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.09.089 · Cited by 40
Self-citationClayton, E. L., Milioto, C., Muralidharan, B., Norona, F. E., Edgar, J. R., Soriano, A., Jafar‐Nejad, P., Rigo, F., Collinge, J., & Isaacs, A. M. (2018) · Brain · doi:10.1093/brain/awy284 · Cited by 45
“Numerous Drosophila mutant models have shown a link between altered dendritic branching and (i) motor proteins; (ii) endocytic pathways; and (iii) local translation (for a comprehensive review see Jan and Jan, 2010).”
BackgroundAtypical age-related changes in cortical thickness in autism spectrum disorder
Nunes, A. S., Vakorin, V. A., Kozhemiako, N., Peatfield, N. A., Ribary, U., & Doesburg, S. M. (2020) · Scientific Reports · doi:10.1038/s41598-020-67507-3 · Cited by 51
Single-neuron criticality optimizes analog dendritic computation
Gollo, L. L., Kinouchi, O., & Copelli, M. (2013) · Scientific Reports · doi:10.1038/srep03222 · Cited by 41
The GTPase Rem2 regulates synapse development and dendritic morphology
Ghiretti, A. E., & Paradis, S. (2010) · Developmental Neurobiology · doi:10.1002/dneu.20868 · Cited by 40
Avery, A. W., Thomas, D. D., & Hays, T. S. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707108114 · Cited by 40
“For example, the molecular and cell biological mechanisms that control branch stability and remodeling within a dendritic field remain largely elusive (44, 45).”
BackgroundConserved regulation of neurodevelopmental processes and behavior by FoxP in Drosophila
Castells‐Nobau, A., Eidhof, I., Fencková, M., Brenman‐Suttner, D. B., Gooyert, J. M. S.-D., Christine, S., Schellevis, R. L., van der Laan, K. J., Quentin, C., van Ninhuijs, L., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0211652 · Cited by 43
“Class IV da neurons present extensively branched dendritic arbors that cover the larval body wall [44].”
Background
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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