Abstract
The precise wiring of the nervous system is a combined outcome of progressive and regressive events during development. Axon guidance and synapse formation intertwined with cell death and neurite pruning sculpt the mature circuitry. It is now well recognized that pruning of dendrites and axons as means to refine neuronal networks, is a wide spread phenomena required for the normal development of vertebrate and invertebrate nervous systems. Here we will review the arising principles of cellular and molecular mechanisms of neurite pruning. We will discuss these principles in light of studies in multiple neuronal systems, and speculate on potential explanations for the emergence of neurite pruning as a mechanism to sculpt the nervous system.
Similar content being viewed by others
Abbreviations
- ALS:
-
Amyotrophic lateral sclerosis
- BDNF:
-
Brain derived neurotrophic factor
- CRMPs:
-
Collapsin response mediator proteins
- CST:
-
Corticospinal tract
- da:
-
Dendritic arborization
- dLGN:
-
Dorsal lateral geniculate nucleus
- DRG:
-
Dorsal root ganglia
- EcR:
-
Ecdysone receptor
- GAP:
-
GTPase activating protein
- GEF:
-
GTP exchange factor
- IPB:
-
Infrapyramidal bundle
- MARCM:
-
Mosaic analysis with a repressible cell marker
- MB:
-
Mushroom body
- MTs:
-
Microtubules
- NFs:
-
Neurofilaments
- NGF:
-
Nerve growth factor
- NMJ:
-
Neuromuscular junction
- PS:
-
Phosphatidylserine
- RGCs:
-
Retinal ganglion cells
- SC:
-
Superior colliculus
- SCG:
-
Superior cervical ganglion
- TGF-β:
-
Transforming growth factor-β
- UPS:
-
Ubituitin proteasome System
- WD:
-
Wallerian degeneration
References
Sperry RW (1963) Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc Natl Acad Sci USA 50:703–710
Raper JA, Bastiani M, Goodman CS (1983) Pathfinding by neuronal growth cones in grasshopper embryos. II. Selective fasciculation onto specific axonal pathways. J Neurosci Off J Soc Neurosci 3(1):31–41
Thomas JB, Bastiani MJ, Bate M, Goodman CS (1984) From grasshopper to Drosophila: a common plan for neuronal development. Nature 310(5974):203–207
Tessier-Lavigne M, Placzek M, Lumsden AG, Dodd J, Jessell TM (1988) Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 336(6201):775–778. doi:10.1038/336775a0
Dickson BJ (2002) Molecular mechanisms of axon guidance. Science 298(5600):1959–1964
Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274(5290):1123–1133
Luo L, O’Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127–156
Cowan WM, Fawcett JW, O’Leary DD, Stanfield BB (1984) Regressive events in neurogenesis. Science 225(4668):1258–1265
Innocenti GM, Price DJ (2005) Exuberance in the development of cortical networks. Nat Rev Neurosci 6(12):955–965. doi:10.1038/nrn1790
Thompson RA, Nelson CA (2001) Developmental science and the media. Early brain development. Am Psychol 56(1):5–15
Truman JW (1990) Metamorphosis of the central nervous system of Drosophila. J Neurobiol 21(7):1072–1084. doi:10.1002/neu.480210711
Ramon Y, Cajal S (1995) Histology of the nervous system. Oxford University Press, New-York
Chung WS, Barres BA (2009) Selective remodeling: refining neural connectivity at the neuromuscular junction. PLoS Biol 7(8):e1000185. doi:10.1371/journal.pbio.1000185
Sugihara I (2006) Organization and remodeling of the olivocerebellar climbing fiber projection. Cerebellum 5(1):15–22. doi:10.1080/14734220500527385
Hashimoto K, Kano M (2013) Synapse elimination in the developing cerebellum. Cell Mol Life Sci 70(24):4667–4680. doi:10.1007/s00018-013-1405-2
Davies AM (1996) The neurotrophic hypothesis: where does it stand? Philos Trans R Soc Lond B Biol Sci 351(1338):389–394
Stanfield BB, O’Leary DD, Fricks C (1982) Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones. Nature 298(5872):371–373
Hoopfer ED, McLaughlin T, Watts RJ, Schuldiner O, O’Leary DD, Luo L (2006) Wlds protection distinguishes axon degeneration following injury from naturally occurring developmental pruning. Neuron 50(6):883–895
O’Leary DD, Stanfield BB (1986) A transient pyramidal tract projection from the visual cortex in the hamster and its removal by selective collateral elimination. Brain Res 392(1–2):87–99
O’Leary DD, Koester SE (1993) Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron 10(6):991–1006
Nakamura H, O’Leary DD (1989) Inaccuracies in initial growth and arborization of chick retinotectal axons followed by course corrections and axon remodeling to develop topographic order. J Neurosci Off J Soc Neurosci 9(11):3776–3795
Feldheim DA, O’Leary DD (2010) Visual map development: bidirectional signaling, bifunctional guidance molecules, and competition. Cold Spring Harb Perspect Biol 2(11):a001768. doi:10.1101/cshperspect.a001768
Shatz CJ, Sretavan DW (1986) Interactions between retinal ganglion cells during the development of the mammalian visual system. Annu Rev Neurosci 9:171–207. doi:10.1146/annurev.ne.09.030186.001131
Josten NJ, Huberman AD (2010) Milestones and mechanisms for generating specific synaptic connections between the eyes and the brain. Curr Top Dev Biol 93:229–259. doi:10.1016/B978-0-12-385044-7.00008-4
Thummel CS (1996) Flies on steroids—Drosophila metamorphosis and the mechanisms of steroid hormone action. Trends Genet 12(8):306–310
Schubiger M, Wade AA, Carney GE, Truman JW, Bender M (1998) Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 125(11):2053–2062
Technau G, Heisenberg M (1982) Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295(5848):405–407
Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22(3):451–461
Lee T, Lee A, Luo L (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126(18):4065–4076
Watts RJ, Hoopfer ED, Luo L (2003) Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38(6):871–885
Yu F, Schuldiner O (2014) Axon and dendrite pruning in Drosophila. Curr Opin Neurobiol 27C:192–198. doi:10.1016/j.conb.2014.04.005
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(16):3631–3642. doi:10.1242/dev.01928
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
Jan YN, Jan LY (2010) Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci 11(5):316–328. doi:10.1038/nrn2836
Williams DW, Kondo S, Krzyzanowska A, Hiromi Y, Truman JW (2006) Local caspase activity directs engulfment of dendrites during pruning. Nat Neurosci 9(10):1234–1236
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(3):283–290
Han C, Jan LY, Jan YN (2011) Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron-glia interactions in Drosophila. Proc Natl Acad Sci USA 108(23):9673–9678. doi:10.1073/pnas.1106386108
Martin SM, O’Brien GS, Portera-Cailliau C, Sagasti A (2010) Wallerian degeneration of zebrafish trigeminal axons in the skin is required for regeneration and developmental pruning. Development 137(23):3985–3994. doi:10.1242/dev.053611
Rosenberg AF, Wolman MA, Franzini-Armstrong C, Granato M (2012) In vivo nerve-macrophage interactions following peripheral nerve injury. J Neurosci Off J Soc Neurosci 32(11):3898–3909. doi:10.1523/JNEUROSCI.5225-11.2012
Sagasti A, Guido MR, Raible DW, Schier AF (2005) Repulsive interactions shape the morphologies and functional arrangement of zebrafish peripheral sensory arbors. Curr Biol CB 15(9):804–814. doi:10.1016/j.cub.2005.03.048
Deckwerth TL, Johnson EM Jr (1993) Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J Cell Biol 123(5):1207–1222
Campenot RB (1982) Development of sympathetic neurons in compartmentalized cultures. II. Local control of neurite survival by nerve growth factor. Development Biol 93(1):13–21
Singh KK, Park KJ, Hong EJ, Kramer BM, Greenberg ME, Kaplan DR, Miller FD (2008) Developmental axon pruning mediated by BDNF-p75NTR-dependent axon degeneration. Nat Neurosci 11(6):649–658. doi:10.1038/nn.2114
Liu Y, Rutlin M, Huang S, Barrick CA, Wang F, Jones KR, Tessarollo L, Ginty DD (2012) Sexually dimorphic BDNF signaling directs sensory innervation of the mammary gland. Science 338(6112):1357–1360. doi:10.1126/science.1228258
Bagri A, Cheng HJ, Yaron A, Pleasure SJ, Tessier-Lavigne M (2003) Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 113(3):285–299
Portera-Cailliau C, Weimer RM, De Paola V, Caroni P, Svoboda K (2005) Diverse modes of axon elaboration in the developing neocortex. PLoS Biol 3(8):e272. doi:10.1371/journal.pbio.0030272
Tapia JC, Wylie JD, Kasthuri N, Hayworth KJ, Schalek R, Berger DR, Guatimosim C, Seung HS, Lichtman JW (2012) Pervasive synaptic branch removal in the mammalian neuromuscular system at birth. Neuron 74(5):816–829. doi:10.1016/j.neuron.2012.04.017
Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389–442. doi:10.1146/annurev.neuro.22.1.389
Bishop DL, Misgeld T, Walsh MK, Gan WB, Lichtman JW (2004) Axon branch removal at developing synapses by axosome shedding. Neuron 44(4):651–661. doi:10.1016/j.neuron.2004.10.026
Song JW, Misgeld T, Kang H, Knecht S, Lu J, Cao Y, Cotman SL, Bishop DL, Lichtman JW (2008) Lysosomal activity associated with developmental axon pruning. J Neurosci Off J Soc Neurosci 28(36):8993–9001. doi:10.1523/JNEUROSCI.0720-08.2008
Boulanger A, Farge M, Ramanoudjame C, Wharton K, Dura JM (2012) Drosophila motor neuron retraction during metamorphosis is mediated by inputs from TGF-beta/BMP signaling and orphan nuclear receptors. PLoS One 7(7):e40255. doi:10.1371/journal.pone.0040255
Liu Z, Chen Y, Wang D, Wang S, Zhang YQ (2010) Distinct presynaptic and postsynaptic dismantling processes of Drosophila neuromuscular junctions during metamorphosis. J Neurosci Off J Soc Neurosci 30(35):11624–11634. doi:10.1523/JNEUROSCI.0410-10.2010
Mack TG, Reiner M, Beirowski B, Mi W, Emanuelli M, Wagner D, Thomson D, Gillingwater T, Court F, Conforti L, Fernando FS, Tarlton A, Andressen C, Addicks K, Magni G, Ribchester RR, Perry VH, Coleman MP (2001) Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat Neurosci 4(12):1199–1206
Coleman MP, Freeman MR (2010) Wallerian degeneration, wld(s), and nmnat. Annu Rev Neurosci 33:245–267. doi:10.1146/annurev-neuro-060909-153248
Vargas ME, Barres BA (2007) Why is Wallerian degeneration in the CNS so slow? Annu Rev Neurosci 30:153–179. doi:10.1146/annurev.neuro.30.051606.094354
Bareyre FM, Kerschensteiner M, Misgeld T, Sanes JR (2005) Transgenic labeling of the corticospinal tract for monitoring axonal responses to spinal cord injury. Nat Med 11(12):1355–1360. doi:10.1038/nm1331
Beirowski B, Adalbert R, Wagner D, Grumme DS, Addicks K, Ribchester RR, Coleman MP (2005) The progressive nature of Wallerian degeneration in wild-type and slow Wallerian degeneration (WldS) nerves. BMC Neurosci 6:6. doi:10.1186/1471-2202-6-6
Xiong X, Collins CA (2012) A conditioning lesion protects axons from degeneration via the Wallenda/DLK MAP kinase signaling cascade. J Neurosci Off J Soc Neurosci 32(2):610–615. doi:10.1523/JNEUROSCI.3586-11.2012
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(6):869–881
Neukomm LJ, Burdett TC, Gonzalez MA, Zuchner S, Freeman MR (2014) Rapid in vivo forward genetic approach for identifying axon death genes in Drosophila. Proc Natl Acad Sci USA 111(27):9965–9970. doi:10.1073/pnas.1406230111
Fang Y, Soares L, Teng X, Geary M, Bonini NM (2012) A novel Drosophila model of nerve injury reveals an essential role of Nmnat in maintaining axonal integrity. Curr Biol CB 22(7):590–595. doi:10.1016/j.cub.2012.01.065
Deckwerth TL, Johnson EM Jr (1994) Neurites can remain viable after destruction of the neuronal soma by programmed cell death (apoptosis). Dev Biol 165(1):63–72
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(18):6375–6386
Tao J, Rolls MM (2011) Dendrites have a rapid program of injury-induced degeneration that is molecularly distinct from developmental pruning. J Neurosci Off J Soc Neurosci 31(14):5398–5405. doi:10.1523/JNEUROSCI.3826-10.2011
Osterloh JM, Yang J, Rooney TM, Fox AN, Adalbert R, Powell EH, Sheehan AE, Avery MA, Hackett R, Logan MA, MacDonald JM, Ziegenfuss JS, Milde S, Hou YJ, Nathan C, Ding A, Brown RH Jr, Conforti L, Coleman M, Tessier-Lavigne M, Zuchner S, Freeman MR (2012) dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 337(6093):481–484. doi:10.1126/science.1223899
Xiong X, Hao Y, Sun K, Li J, Li X, Mishra B, Soppina P, Wu C, Hume RI, Collins CA (2012) The Highwire ubiquitin ligase promotes axonal degeneration by tuning levels of Nmnat protein. PLoS Biol 10(12):e1001440. doi:10.1371/journal.pbio.1001440
Yu XM, Gutman I, Mosca TJ, Iram T, Ozkan E, Garcia KC, Luo L, Schuldiner O (2013) Plum, an immunoglobulin superfamily protein, regulates axon pruning by facilitating TGF-beta signaling. Neuron 78(3):456–468. doi:10.1016/j.neuron.2013.03.004
Awasaki T, Ito K (2004) Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr Biol CB 14(8):668–677. doi:10.1016/j.cub.2004.04.001
Watts RJ, Schuldiner O, Perrino J, Larsen C, Luo L (2004) Glia engulf degenerating axons during developmental axon pruning. Curr Biol CB 14(8):678–684. doi:10.1016/j.cub.2004.03.035
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(6):855–867
Awasaki T, Lai SL, Ito K, Lee T (2008) Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci Off J Soc Neurosci 28(51):13742–13753. doi:10.1523/JNEUROSCI.4844-08.2008
Stork T, Bernardos R (2012) Freeman MR (2012) Analysis of glial cell development and function in Drosophila. Cold Spring Harb Protoc 1:1–17. doi:10.1101/pdb.top067587
Doherty J, Logan MA, Tasdemir OE, Freeman MR (2009) Ensheathing glia function as phagocytes in the adult Drosophila brain. J Neurosci Off J Soc Neurosci 29(15):4768–4781. doi:10.1523/JNEUROSCI.5951-08.2009
Hakim Y, Yaniv SP, Schuldiner O (2014) Astrocytes play a key role in Drosophila mushroom body axon pruning. PLoS One 9(1):e86178. doi:10.1371/journal.pone.0086178
Tasdemir-Yilmaz OE, Freeman MR (2014) Astrocytes engage unique molecular programs to engulf pruned neuronal debris from distinct subsets of neurons. Genes Dev 28(1):20–33. doi:10.1101/gad.229518.113
Han C, Song Y, Xiao H, Wang D, Franc NC, Jan LY, Jan YN (2014) Epidermal cells are the primary phagocytes in the fragmentation and clearance of degenerating dendrites in Drosophila. Neuron 81(3):544–560. doi:10.1016/j.neuron.2013.11.021
Berbel P, Innocenti GM (1988) The development of the corpus callosum in cats: a light- and electron-microscopic study. J Comp Neurol 276(1):132–156. doi:10.1002/cne.902760109
Innocenti GM (1981) Growth and reshaping of axons in the establishment of visual callosal connections. Science 212(4496):824–827
Schafer DP, Stevens B (2013) Phagocytic glial cells: sculpting synaptic circuits in the developing nervous system. Curr Opin Neurobiol 23(6):1034–1040. doi:10.1016/j.conb.2013.09.012
Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333(6048):1456–1458. doi:10.1126/science.1202529
Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74(4):691–705. doi:10.1016/j.neuron.2012.03.026
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(7480):394–400. doi:10.1038/nature12776
Ravichandran KS, Lorenz U (2007) Engulfment of apoptotic cells: signals for a good meal. Nat Rev Immunol 7(12):964–974. doi:10.1038/nri2214
Tung TT, Nagaosa K, Fujita Y, Kita A, Mori H, Okada R, Nonaka S, Nakanishi Y (2013) Phosphatidylserine recognition and induction of apoptotic cell clearance by Drosophila engulfment receptor Draper. J Biochem 153(5):483–491. doi:10.1093/jb/mvt014
Burstyn-Cohen T, Lew ED, Traves PG, Burrola PG, Hash JC, Lemke G (2012) Genetic dissection of TAM receptor-ligand interaction in retinal pigment epithelial cell phagocytosis. Neuron 76(6):1123–1132. doi:10.1016/j.neuron.2012.10.015
Low LK, Liu XB, Faulkner RL, Coble J, Cheng HJ (2008) Plexin signaling selectively regulates the stereotyped pruning of corticospinal axons from visual cortex. Proc Natl Acad Sci US A 105(23):8136–8141
Liu XB, Low LK, Jones EG, Cheng HJ (2005) Stereotyped axon pruning via plexin signaling is associated with synaptic complex elimination in the hippocampus. J Neurosci Off J Soc Neurosci 25(40):9124–9134. doi:10.1523/JNEUROSCI.2648-05.2005
Low LK, Liu XB, Faulkner RL, Coble J, Cheng HJ (2008) Plexin signaling selectively regulates the stereotyped pruning of corticospinal axons from visual cortex. Proc Natl Acad Sci USA 105(23):8136–8141. doi:10.1073/pnas.0803849105
Xu NJ, Henkemeyer M (2009) Ephrin-B3 reverse signaling through Grb4 and cytoskeletal regulators mediates axon pruning. Nat Neurosci 12(3):268–276. doi:10.1038/nn.2254
Klein R (2004) Eph/ephrin signaling in morphogenesis, neural development and plasticity. Curr Opin Cell Biol 16(5):580–589
Zheng X, Wang J, Haerry TE, Wu AY, Martin J, O’Connor MB, Lee CH, Lee T (2003) TGF-beta signaling activates steroid hormone receptor expression during neuronal remodeling in the Drosophila brain. Cell 112(3):303–315
Awasaki T, Huang Y, O’Connor MB, Lee T (2011) Glia instruct developmental neuronal remodeling through TGF-beta signaling. Nat Neurosci 14(7):821–823. doi:10.1038/nn.2833
Maor-Nof M, Yaron A (2013) Neurite pruning and neuronal cell death: spatial regulation of shared destruction programs. Curr Opin Neurobiol 23(6):990–996. doi:10.1016/j.conb.2013.06.007
Nikolaev A, McLaughlin T, O’Leary DD, Tessier-Lavigne M (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457(7232):981–989
Schecterson LC, Bothwell M (2010) Neurotrophin receptors: old friends with new partners. Dev Neurobiol 70(5):332–338. doi:10.1002/dneu.20767
Ibanez CF, Simi A (2012) p75 neurotrophin receptor signaling in nervous system injury and degeneration: paradox and opportunity. Trends Neurosci 35(7):431–440. doi:10.1016/j.tins.2012.03.007
Cao L, Dhilla A, Mukai J, Blazeski R, Lodovichi C, Mason CA, Gogos JA (2007) Genetic modulation of BDNF signaling affects the outcome of axonal competition in vivo. Curr Biol CB 17(11):911–921. doi:10.1016/j.cub.2007.04.040
Park KJ, Grosso CA, Aubert I, Kaplan DR, Miller FD (2010) p75NTR-dependent, myelin-mediated axonal degeneration regulates neural connectivity in the adult brain. Nat Neurosci 13(5):559–566. doi:10.1038/nn.2513
Pan G, Bauer JH, Haridas V, Wang S, Liu D, Yu G, Vincenz C, Aggarwal BB, Ni J, Dixit VM (1998) Identification and functional characterization of DR6, a novel death domain-containing TNF receptor. FEBS Lett 431(3):351–356
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 USA 102(42):15230–15235
Wong JJ, Li S, Lim EK, Wang Y, Wang C, Zhang H, Kirilly D, Wu C, Liou YC, 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(9):e1001657. doi:10.1371/journal.pbio.1001657
Yaniv SP, Issman-Zecharya N, Oren-Suissa M, Podbilewicz B, Schuldiner O (2012) Axon regrowth during development and regeneration following injury share molecular mechanisms. Curr Biol CB 22(19):1774–1782. doi:10.1016/j.cub.2012.07.044
Zhai Q, Wang J, Kim A, Liu Q, Watts R, Hoopfer E, Mitchison T, Luo L, He Z (2003) Involvement of the ubiquitin-proteasome system in the early stages of wallerian degeneration. Neuron 39(2):217–225
Feinstein-Rotkopf Y, Arama E (2009) Can’t live without them, can live with them: roles of caspases during vital cellular processes. Apoptosis
Kuranaga E, Miura M (2007) Nonapoptotic functions of caspases: caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol 17(3):135–144. doi:10.1016/j.tcb.2007.01.001
Simon DJ, Weimer RM, McLaughlin T, Kallop D, Stanger K, Yang J, O’Leary DD, Hannoush RN, Tessier-Lavigne M (2012) A caspase cascade regulating developmental axon degeneration. J Neurosci Off J Soc Neurosci 32(49):17540–17553. doi:10.1523/JNEUROSCI.3012-12.2012
Cusack CL, Swahari V, Hampton Henley W, Michael Ramsey J, Deshmukh M (2013) Distinct pathways mediate axon degeneration during apoptosis and axon-specific pruning. Nat Commun 4:1876. doi:10.1038/ncomms2910
Unsain N, Higgins JM, Parker KN, Johnstone AD, Barker PA (2013) XIAP Regulates Caspase Activity in Degenerating Axons. Cell Rep 4(4):751–763. doi:10.1016/j.celrep.2013.07.015
Cosker KE, Pazyra-Murphy MF, Fenstermacher SJ, Segal RA (2013) Target-derived neurotrophins coordinate transcription and transport of bclw to prevent axonal degeneration. J Neurosci Off J Soc Neurosci 33(12):5195–5207. doi:10.1523/JNEUROSCI.3862-12.2013
Yang J, Weimer RM, Kallop D, Olsen O, Wu Z, Renier N, Uryu K, Tessier-Lavigne M (2013) Regulation of axon degeneration after injury and in development by the endogenous calpain inhibitor calpastatin. Neuron 80(5):1175–1189. doi:10.1016/j.neuron.2013.08.034
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(6139):1475–1478. doi:10.1126/science.1234879
George EB, Glass JD, Griffin JW (1995) Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels. J Neurosci Off J Soc Neurosci 15(10):6445–6452
Chen M, Maloney JA, Kallop DY, Atwal JK, Tam SJ, Baer K, Kissel H, Kaminker JS, Lewcock JW, Weimer RM, Watts RJ (2012) Spatially coordinated kinase signaling regulates local axon degeneration. J Neurosci Off J Soc Neurosci 32(39):13439–13453. doi:10.1523/JNEUROSCI.2039-12.2012
Ghosh AS, Wang B, Pozniak CD, Chen M, Watts RJ, Lewcock JW (2011) DLK induces developmental neuronal degeneration via selective regulation of proapoptotic JNK activity. J Cell Biol 194(5):751–764. doi:10.1083/jcb.201103153
Lee HH, Jan LY, Jan YN (2009) Drosophila IKK-related kinase Ik2 and Katanin p60-like 1 regulate dendrite pruning of sensory neuron during metamorphosis. Proc Natl Acad Sci U S A 106(15):6363–6368
Gerdts J, Sasaki Y, Vohra B, Marasa J, Milbrandt J (2011) Image-based screening identifies novel roles for IkappaB kinase and glycogen synthase kinase 3 in axonal degeneration. J Biol Chem 286(32):28011–28018. doi:10.1074/jbc.M111.250472
Shea TB, Lee S (2013) The discontinuous nature of neurofilament transport accommodates both establishment and repair of the axonal neurofilament array. Cytoskeleton (Hoboken) 70(2):67–73. doi:10.1002/cm.21087
Perrot R, Berges R, Bocquet A, Eyer J (2008) Review of the multiple aspects of neurofilament functions, and their possible contribution to neurodegeneration. Mol Neurobiol 38(1):27–65. doi:10.1007/s12035-008-8033-0
Letourneau PC (2009) Actin in axons: stable scaffolds and dynamic filaments. Results Probl Cell Differ 48:65–90. doi:10.1007/400_2009_15
Amos LA, Schlieper D (2005) Microtubules and maps. Adv Protein Chem 71:257–298. doi:10.1016/S0065-3233(04)71007-4
Weisenberg RC, Deery WJ (1976) Role of nucleotide hydrolysis in microtubule assembly. Nature 263(5580):792–793
Luduena RF, Anderson WH, Prasad V, Jordan MA, Ferrigni KC, Roach MC, Horowitz PM, Murphy DB, Fellous A (1986) Interactions of vinblastine and maytansine with tubulin. Ann N Y Acad Sci 466:718–732
Maor-Nof M, Homma N, Raanan C, Nof A, Hirokawa N, Yaron A (2013) Axonal pruning is actively regulated by the microtubule-destabilizing protein kinesin superfamily protein 2A. Cell Rep 3(4):971–977. doi:10.1016/j.celrep.2013.03.005
Walker KL, Yoo HK, Undamatla J, Szaro BG (2001) Loss of neurofilaments alters axonal growth dynamics. J Neurosci Off J Soc Neurosci 21(24):9655–9666
Wakatsuki S, Saitoh F, Araki T (2011) ZNRF1 promotes Wallerian degeneration by degrading AKT to induce GSK3B-dependent CRMP2 phosphorylation. Nat Cell Biol 13(12):1415–1423. doi:10.1038/ncb2373
Touma E, Kato S, Fukui K, Koike T (2007) Calpain-mediated cleavage of collapsin response mediator protein(CRMP)-2 during neurite degeneration in mice. Eur J Neurosci 26(12):3368–3381. doi:10.1111/j.1460-9568.2007.05943.x
Riccomagno MM, Hurtado A, Wang H, Macopson JG, Griner EM, Betz A, Brose N, Kazanietz MG, Kolodkin AL (2012) The RacGAP beta2-Chimaerin selectively mediates axonal pruning in the hippocampus. Cell 149(7):1594–1606. doi:10.1016/j.cell.2012.05.018
Turner LJ, Nicholls S, Hall A (2004) The activity of the plexin-A1 receptor is regulated by Rac. J Biol Chem 279(32):33199–33205
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(12):1497–1505. doi:10.1038/nn.2415
Loncle N, Williams DW (2012) An interaction screen identifies headcase as a regulator of large-scale pruning. J Neurosci Off J Soc Neurosci 32(48):17086–17096. doi:10.1523/JNEUROSCI.1391-12.2012
Marin EC, Watts RJ, Tanaka NK, Ito K, Luo L (2005) Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132(4):725–737. doi:10.1242/dev.01614
Schuldiner O, Berdnik D, Levy JM, Wu JS, Luginbuhl D, Gontang AC, Luo L (2008) piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Dev Cell 14(2):227–238. doi:10.1016/j.devcel.2007.11.001
Boulanger A, Clouet-Redt C, Farge M, Flandre A, Guignard T, Fernando C, Juge F, Dura JM (2011) ftz-f1 and Hr39 opposing roles on EcR expression during Drosophila mushroom body neuron remodeling. Nat Neurosci 14(1):37–44. doi:10.1038/nn.2700
Florentin A, Arama E (2012) Caspase levels and execution efficiencies determine the apoptotic potential of the cell. J Cell Biol 196(4):513–527. doi:10.1083/jcb.201107133
Erturk A, Wang Y, Sheng M (2014) Local pruning of dendrites and spines by caspase-3-dependent and proteasome-limited mechanisms. J Neurosci Off J Soc Neurosci 34(5):1672–1688. doi:10.1523/JNEUROSCI.3121-13.2014
Bialas AR, Stevens B (2013) TGF-beta signaling regulates neuronal C1q expression and developmental synaptic refinement. Nat Neurosci 16(12):1773–1782. doi:10.1038/nn.3560
Acknowledgments
We thank M. Maor-Nof and S. Yaniv for critical reading of the manuscript and Z. Schoenmann for assistance with the graphics. Research in our laboratories is currently supported by the Israeli Science Foundaton (ISF) and Minerva foundation (A.Y.) and the European Research Council (erc), Israeli Science Foundation (ISF) and Minerva foundation (O.S). O.S. is an incumbent of the Aser Rothstein Career Development Chair.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Schuldiner, O., Yaron, A. Mechanisms of developmental neurite pruning. Cell. Mol. Life Sci. 72, 101–119 (2015). https://doi.org/10.1007/s00018-014-1729-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00018-014-1729-6