Abstract
Dendrites are the entry site of neural signals into neurons. Once formed, dendrites do not maintain their structure, rather are dynamically remodeled in vivo: some dendrites are pruned away, while others lengthen and branch out. Dendritic remodeling occurs not only during neural development but also in mature dendrites under both physiological and pathological conditions, suggesting its contribution to neural plasticity. The underlying cellular and molecular mechanisms remain poorly understood; however, they are just beginning to be elucidated from studies in vertebrate and invertebrate model systems. Here, we review recent advances in our understanding of dendritic remodeling by focusing particularly on insights obtained from layer IV spiny stellate neurons in the rodent somatosensory cortex and Drosophila sensory neurons.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Awasaki T, Ito K (2004) Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr Biol 14:668–677. doi:10.1016/j
Awasaki T, Tatsumi R, Takahashi K, Arai K, Nakanishi Y, Ueda R, Ito K (2006) Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during Drosophila metamorphosis. Neuron 50:855–867. doi:10.1016/j.neuron.2006.04.027
Beuchle D, Schwarz H, Langegger M, Koch I, Aberle H (2007) Drosophila MICAL regulates myofilament organization and synaptic structure. Mech Dev 124:390–406. doi:10.1016/j.mod.2007.01.006
Buszczak M, Segraves WA (2000) Insect metamorphosis: out with the old, in with the new. Curr Biol 10:R830–R833. doi:10.1016/S0960-9822(00)00792-2
Cajal R (1911) Histology of the nervous system of man and vertebrates translated from the French. Oxford University Press, Oxford
Chen JL, Lin WC, Cha JW, So PT, Kubota Y, Nedivi E (2011) Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat Neurosci 14:587–594. doi:10.1038/nn.2799
Chung WS, Clarke LE, Wang GX, Stafford BK, Sher A, Chakraborty C, Joung J, Foo LC, Thompson A, Chen C, Smith SJ, Barres BA (2013) Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature 504:394–400. doi:10.1038/nature12776
Coleman MP, Freeman MR (2010) Wallerian degeneration, Wld(S), and nmnat. Annu Rev Neurosci 33:245–267. doi:10.1146/annurev-neuro-060909-153248
Consoulas C (2002) Dendritic remodeling and growth of motoneurons during metamorphosis of Drosophila melanogaster. J Neurosci 22:4906–4917
Datwani A, Iwasato T, Itohara S, Erzurumlu RS (2002) Lesion-induced thalamocortical axonal plasticity in the S1 cortex is independent of NMDA receptor function in excitatory cortical neurons. J Neurosci 22:9171–9175
Ehlinger DG, Bergstrom HC, McDonald CG, Smith RF (2012) Nicotine-induced dendritic remodeling in the insular cortex. Neurosci Lett 516:89–93. doi:10.1016/j.neulet.2012.03.064
Emoto K (2012) Signaling mechanisms that coordinate the development and maintenance of dendritic fields. Curr Opin Neurobiol 22:805–811. doi:10.1016/j.conb.2012.04.005
Espinosa JS, Wheeler DG, Tsien RW, Luo L (2009) Uncoupling dendrite growth and patterning: single-cell knockout analysis of NMDA receptor 2B. Neuron 62:205–217. doi:10.1016/j.neuron
Gourley SL, Swanson AM, Koleske AJ (2013) Corticosteroid-induced neural remodeling predicts behavioral vulnerability and resilience. J Neurosci 33:3107–3112. doi:10.1523/JNEUROSCI.2138-12.2013
Hakim Y, Yaniv SP, Schuldiner O (2014) Astrocytes play a key role in Drosophila mushroom body axon pruning. PLoS One 9:e86178. doi:10.1371/journal.pone.0086178
Han C, Jan LY, Jan Y-N (2011) Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proc Natl Acad Sci U S A 108:9673–9678. doi:10.1073/pnas.1106386108
Han C, Song Y, Xiao H, Wang D, Franc NC, Jan LY, Jan Y-N (2014) Epidermal cells are the primary phagocytes in the fragmentation and clearance of degenerating dendrites in Drosophila. Neuron 81:544–560. doi:10.1016/j.neuron.2013.11.021
Harris RM, Woolsey TA (1979) Morphology of Golgi-impregnated neurons in mouse cortical barrels following vibrissae damage at different postnatal ages. Brain Res 161:1177–1184
Hoopfer ED, McLaughlin T, Watts RJ, Schuldiner O, O’Leary DDM, Luo L (2006) Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron 50:883–895. doi:10.1016/j.neuron.2006.05.013
Hoopfer ED, Penton A, Watts RJ, Luo L (2008) Genomic analysis of Drosophila neuronal remodeling: a role for the RNA-binding protein Boule as a negative regulator of axon pruning. J Neurosci 28:6092–6103. doi:10.1523/JNEUROSCI.0677-08.2008
Hung R-J, Yazdani U, Yoon J, Wu H, Yang T, Gupta N, Huang Z, van Berkel WJH, Terman JR (2010) Mical links semaphorins to F-actin disassembly. Nature 463:823–827. doi:10.1038/nature08724
Kanamori T, Kanai MI, Dairyo Y, Yasunaga K, Morikawa RK, Emoto K (2013) Compartmentalized calcium transients trigger dendrite pruning in Drosophila sensory neurons. Science 340:1475–1478. doi:10.1126/science.1234879
Kanamori T, Yoshino J, Yasunaga K, Dairyo Y, Emoto K (2015) Local endocytosis triggers dendrite thinning and pruning in Drosophila sensory neurons. Nat Commun (in press)
Kaneko M, Yamaguchi K, Eiraku M, Sato M, Takata N, Kiyohara Y, Mishina M, Hirase H, Hashikawa T, Kengaku M (2011) Remodeling of monoplanar Purkinje cell dendrites during cerebellar circuit formation. PLoS One 6:e20108. doi:10.1371/journal.pone.0020108
Kim SE, Coste B, Chadha A, Cook B, Patapoutian A (2012) The role of Drosophila Piezo in mechanical nociception. Nature 483:209–212. doi:10.1038/nature10801
Kirilly D, Gu Y, Huang Y, Wu Z, Bashirullah A, Low BC, Kolodkin AL, Wang H, Yu F (2009) A genetic pathway composed of Sox14 and Mical governs severing of dendrites during pruning. Nat Neurosci 12:1497–1505. doi:10.1038/nn.2415
Kirilly D, Wong JJL, Lim EKH, Wang Y, Zhang H, Wang C, Liao Q, Wang H, Liou Y-C, Wang H, Yu F (2011) Intrinsic epigenetic factors cooperate with the steroid hormone ecdysone to govern dendrite pruning in Drosophila. Neuron 72:86–100. doi:10.1016/j.neuron.2011.08.003
Kuo CT, Jan LY, Jan YN (2005) Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling. Proc Natl Acad Sci U S A 102:15230–15235. doi:10.1073/pnas.0507393102
Kuo CT, Zhu S, Younger S, Jan LY, Jan YN (2006) Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51:283–290. doi:10.1016/j.neuron.2006.07.014
Kuraishi T, Nakagawa Y, Nagaosa K, Hashimoto Y, Ishimoto T, Moki T, Fujita Y, Nakayama H, Dohmae N, Shiratsuchi A, Yamamoto N, Ueda K, Yamaguchi M, Awasaki T, Nakanishi Y (2009) Pretaporter, a Drosophila protein serving as a ligand for Draper in the phagocytosis of apoptotic cells. EMBO J 28:3868–3878. doi:10.1038/emboj.2009.343
Kuranaga E, Kanuka H, Tonoki A, Takemoto K, Tomioka T, Kobayashi M, Hayashi S, Miura M (2006) Drosophila IKK-related kinase regulates nonapoptotic function of caspases via degradation of IAPs. Cell 126:583–596. doi:10.1016/j.cell.2006.05.048
Kurant E, Axelrod S, Leaman D, Gaul U (2008) Six-microns-under acts upstream of Draper in the glial phagocytosis of apoptotic neurons. Cell 133:498–509. doi:10.1016/j.cell.2008.02.052
Lee W-CA, Huang H, Feng G, Sanes JR, Brown EN, So PT, Nedivi E (2006) Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biol 4:e29. doi:10.1371/journal.pbio.0040029
Lee H, Jan LY, Jan Y (2009) p60-like 1 regulate dendrite pruning of sensory neuron during metamorphosis. Proc Natl Acad Sci U S A 106:6363–6368
Li J, Liu N, Lu K, Zhang L, Gu J, Guo F, An S, Zhang L, Zhang L (2012) Cocaine-induced dendritic remodeling occurs in both D1 and D2 dopamine receptor-expressing neurons in the nucleus accumbens. Neurosci Lett 517:118–122. doi:10.1016/j.neulet.2012.04.040
Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, Morrison JH, McEwen BS (2006) Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26:7870–7874. doi:10.1523/JNEUROSCI.1184-06.2006
Liu OW, Shen K (2011) The transmembrane LRR protein DMA-1 promotes dendrite branching and growth in C. elegans. Nat Neurosci 15:57–63. doi:10.1038/nn.2978
Loncle N, Williams DW (2012) An interaction screen identifies headcase as a regulator of large-scale pruning. J Neurosci 32:17086–17096. doi:10.1523/JNEUROSCI.1391-12.2012
Lunn ER, Perry VH, Brown MC, Rosen H, Gordon S (1989) Absence of Wallerian degeneration does not hinder regeneration in peripheral nerve. Eur J Neurosci 1:27–33
Lyons GR, Andersen RO, Abdi K, Song W-S, Kuo CT (2014) Cysteine proteinase-1 and cut protein isoform control dendritic innervation of two distinct sensory fields by a single neuron. Cell Rep 6:783–791. doi:10.1016/j.celrep.2014.02.003
MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR (2006) The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50:869–881. doi:10.1016/j.neuron.2006.04.028
Malun D, Brunjes PC (1996) Development of olfactory glomeruli: temporal and spatial interactions between olfactory receptor axons and mitral cells in opossums and rats. J Comp Neurol 368:1–16
Manaka J, Kuraishi T, Shiratsuchi A, Nakai Y, Higashida H, Henson P, Nakanishi Y (2004) Draper-mediated and phosphatidylserine-independent phagocytosis of apoptotic cells by Drosophila hemocytes/macrophages. J Biol Chem 279:48466–48476. doi:10.1074/jbc.M408597200
Matsui A, Tran M, Yoshida AC, Kikuchi SS, U M, Ogawa M, Shimogori T (2013) BTBD3 controls dendrite orientation toward active axons in mammalian neocortex. Science 342:114–118. doi:10.1126/science.1244505
Mizuno H, Luo W, Tarusawa E, Saito YM, Sato T, Yoshimura Y, Itohara S, Iwasato T (2014) NMDAR-regulated dynamics of layer 4 neuronal dendrites during thalamocortical reorganization in neonates. Neuron 82:365–379. doi:10.1016/j.neuron.2014.02.026
Oren-Suissa M, Hall DH, Treinin M, Shemer G, Podbilewicz B (2010) The fusogen EFF-1 controls sculpting of mechanosensory dendrites. Science 328:1285–1288. doi:10.1126/science.1189095
Oshima K, Takeda M, Kuranaga E, Ueda R, Aigaki T, Miura M, Hayashi S (2006) IKK epsilon regulates F actin assembly and interacts with Drosophila IAP1 in cellular morphogenesis. Curr Biol 16:1531–1537. doi:10.1016/j.cub.2006.06.032
Parrish JZ, Emoto K, Kim MD, Jan YN (2007) Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu Rev Neurosci 30:399–423. doi:10.1146/annurev.neuro.29.051605.112907
Rumpf S, Lee SB, Jan LY, Jan YN (2011) Neuronal remodeling and apoptosis require VCP-dependent degradation of the apoptosis inhibitor DIAP1. Development 138:1153–1160. doi:10.1242/dev.062703
Rumpf S, Bagley JA, Thompson-Peer KL, Zhu S, Gorczyca D, Beckstead RB, Jan LY, Jan YN (2014) Drosophila valosin-containing protein is required for dendrite pruning through a regulatory role in mRNA metabolism. Proc Natl Acad Sci U S A 111:7331–7336. doi:10.1073/pnas.1406898111
Salzberg Y, Ramirez-Suarez NJ, Bülow HE (2014) The proprotein convertase KPC-1/furin controls branching and self-avoidance of sensory dendrites in Caenorhabditis elegans. PLoS Genet 10:e1004657. doi:10.1371/journal.pgen.1004657
Satoh D, Suyama R, Kimura K, Uemura T (2012) High-resolution in vivo imaging of regenerating dendrites of Drosophila sensory neurons during metamorphosis: local filopodial degeneration and heterotypic dendrite-dendrite contacts. Genes Cells 17:939–951. doi:10.1111/gtc.12008
Schoenmann Z, Assa-Kunik E, Tiomny S, Minis A, Haklai-Topper L, Arama E, Yaron A (2010) Axonal degeneration is regulated by the apoptotic machinery or a NAD+-sensitive pathway in insects and mammals. J Neurosci 30:6375–6386. doi:10.1523/JNEUROSCI.0922-10.2010
Schroeder NE, Androwski RJ, Rashid A, Lee H, Lee J, Barr MM (2013) Dauer-specific dendrite arborization in C. elegans is regulated by KPC-1/Furin. Curr Biol 23:1527–1535. doi:10.1016/j.cub.2013.06.058
Scott JA, Williams DW, Truman JW (2011) The BTB/POZ zinc finger protein Broad-Z3 promotes dendritic outgrowth during metamorphic remodeling of the peripheral stretch receptor dbd. Neural Dev 6:39. doi:10.1186/1749-8104-6-39
Shimono K, Fujimoto A, Tsuyama T, Yamamoto-Kochi M, Sato M, Hattori Y, Sugimura K, Usui T, Kimura K, Uemura T (2009) Multidendritic sensory neurons in the adult Drosophila abdomen: origins, dendritic morphology, and segment- and age-dependent programmed cell death. Neural Dev 4:37. doi:10.1186/1749-8104-4-37
Shimono K, Fujishima K, Nomura T, Ohashi M, Usui T, Kengaku M, Toyoda A, Uemura T (2014) An evolutionarily conserved protein CHORD regulates scaling of dendritic arbors with body size. Sci Rep 4:4415. doi:10.1038/srep04415
Smith CJ, Watson JD, VanHoven MK, Colón-Ramos DA, Miller DM 3rd (2012) Netrin (UNC-6) mediates dendritic self-avoidance. Nat Neurosci 15:731–737. doi:10.1038/nn.3065
Smith CJ, O’Brien T, Chatzigeorgiou M, Spencer WG, Feingold-Link E, Husson SJ, Hori S, Mitani S, Gottschalk A, Schafer WR, Miller DM 3rd (2013) Sensory neuron fates are distinguished by a transcriptional switch that regulates dendrite branch stabilization. Neuron 79:266–280. doi:10.1016/j.neuron.2013.05.009
Steffen H, Van der Loos H (1980) Early lesions of mouse vibrissal follicles: their influence on dendritic orientation in the cortical barrelfield. Exp Brain Res 40:410–431
Tao J, Rolls MM (2011) Dendrites have a rapid program of injury-induced degeneration that is molecularly distinct from developmental pruning. J Neurosci 31:5398–5405. doi:10.1523/JNEUROSCI.3826-10.2011
Tasdemir-Yilmaz OE, Freeman MR (2014) Astrocytes engage unique molecular programs to engulf pruned neuronal debris from distinct subsets of neurons. Genes Dev 28:20–33. doi:10.1101/gad.229518.113
Thummel C (1996) Flies on steroids—Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet 12:306–310
Wang G, Liets L, Chalupa L (2001) Unique functional properties of on and off pathways in the developing mammalian retina. J Neurosci 21:4310–4317
Watts R, Hoopfer E, Luo L (2003) Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38:871–885
Watts RJ, Schuldiner O, Perrino J, Larsen C, Luo L (2004) Glia engulf degenerating axons during developmental axon pruning. Curr Biol 14:678–684. doi:10.1016/j.cub.2004.03.035
Williams DW, Truman JW (2004) Mechanisms of dendritic elaboration of sensory neurons in Drosophila: insights from in vivo time lapse. J Neurosci 24:1541–1550. doi:10.1523/JNEUROSCI.4521-03.2004
Williams DW, Truman JW (2005) Cellular mechanisms of dendrite pruning in Drosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons. Development 132:3631–3642. doi:10.1242/dev.01928
Williams DW, Kondo S, Krzyzanowska A, Hiromi Y, Truman JW (2006) Local caspase activity directs engulfment of dendrites during pruning. Nat Neurosci 9:1234–1236. doi:10.1038/nn1774
Wong JJL, Li S, Lim EKH, Wang Y, Wang C, Zhang H, Kirilly D, Wu C, Liou Y-C, Wang H, Yu F (2013) A Cullin1-based SCF E3 ubiquitin ligase targets the InR/PI3K/TOR pathway to regulate neuronal pruning. PLoS Biol 11:e1001657. doi:10.1371/journal.pbio.1001657
Yan Z, Zhang W, He Y, Gorczyca D, Xiang Y, Cheng LE, Meltzer S, Jan LY, Jan YN (2013) Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature 493:221–225. doi:10.1038/nature11685
Yasunaga K, Kanamori T, Morikawa R, Suzuki E, Emoto K (2010) Dendrite reshaping of adult Drosophila sensory neurons requires matrix metalloproteinase-mediated modification of the basement membranes. Dev Cell 18:621–632. doi:10.1016/j.devcel.2010.02.010
Yu X, Odera S, Chuang C-H, Lu N, Zhou Z (2006) C. elegans Dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells. Dev. Cell 10:743–757. doi:10.1016/j.devcel.2006.04.007
Zhang H, Wang Y, Wong JJL, Lim K-L, Liou Y-C, Wang H, Yu F (2014) Endocytic pathways downregulate the L1-type cell adhesion molecule neuroglian to promote dendrite pruning in Drosophila. Dev Cell 30:463–478. doi:10.1016/j.devcel.2014.06.014
Zhong L, Hwang RY, Tracey WD (2010) Pickpocket is a DEG/ENaC protein required for mechanical nociception in Drosophila larvae. Curr Biol 20:429–434. doi:10.1016/j.cub.2009.12.057
Zhong L, Bellemer A, Yan H, Honjo K, Robertson J, Hwang RY, Pitt GS, Tracey WD (2012) Thermosensory and non-thermosensory isoforms of Drosophila melanogaster TRPA1 reveal heat sensor domains of a thermoTRP channel. Cell Rep 1:43–55. doi:10.1016/j.celrep.2011.11.002
Zhou Z, Hartwieg E, Horvitz HR (2001) CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104:43–56. doi:10.1016/S0092-8674(01)00190-8
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer Japan
About this chapter
Cite this chapter
Togashi, K., Koizumi, H., Kanamori, T., Emoto, K. (2016). Molecular Control of Dendritic Remodeling. In: Emoto, K., Wong, R., Huang, E., Hoogenraad, C. (eds) Dendrites. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56050-0_12
Download citation
DOI: https://doi.org/10.1007/978-4-431-56050-0_12
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-56048-7
Online ISBN: 978-4-431-56050-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)