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Extracellular Signals Controlling Neuroblast Migration in the Postnatal Brain

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Cellular and Molecular Control of Neuronal Migration

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 800))

Abstract

The most prominent example of long-distance migration in the postnatal brain is the rostral migratory stream (RMS) formed by neuroblasts originating in the subventricular zone (SVZ), one of the main neurogenic niches. Stem cell-derived neuroblasts leave the SVZ and migrate rostrally towards the olfactory bulb (OB), where they ultimately differentiate into inhibitory interneurons. This migration is essential for the proper integration of new neurons into the synaptic network and for the regulation of synaptic plasticity and olfactory memory. SVZ-derived postnatal neuroblasts undergo tangential migration independent of radial glia. They slide along each other in chains, which become progressively encased by an astrocytic tunnel throughout adulthood, while keeping in close contact with surrounding blood vessels. Once in the OB, neuroblasts switch to radial migration before differentiating. While the existence of an RMS is still controversial in the adult human brain, prominent migration of SVZ-derived neuroblasts towards the OB is observed in human infants, where it may play an important role in plasticity in a crucial period for the formation of synaptic networks. Moreover, SVZ neuroblasts are able to deviate from their migratory path to reach areas of injury and neurodegeneration. Identifying the extracellular factors and the intracellular mechanisms regulating neuroblast migration can therefore not only clarify a fundamental aspect of postnatal neurogenesis, but can also become relevant for therapeutic strategies exploiting the recruitment of endogenous stem cell-derived neural progenitors. This chapter presents an overview of the wide range of extracellular factors guiding neuroblast migration that have emerged over the last two decades.

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References

  • Aguado T, Palazuelos J, Monory K, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzman M, Galve-Roperh I (2006) The endocannabinoid system promotes astroglial differentiation by acting on neural progenitor cells. J Neurosci 26(5):1551–1561. doi:10.1523/JNEUROSCI.3101-05.2006

    PubMed  CAS  Google Scholar 

  • Andrade N, Komnenovic V, Blake SM, Jossin Y, Howell B, Goffinet A, Schneider WJ, Nimpf J (2007) ApoER2/VLDL receptor and Dab1 in the rostral migratory stream function in postnatal neuronal migration independently of Reelin. Proc Natl Acad Sci U S A 104(20):8508–8513. doi:10.1073/pnas.0611391104

    PubMed  CAS  Google Scholar 

  • Angot E, Loulier K, Nguyen-Ba-Charvet KT, Gadeau AP, Ruat M, Traiffort E (2008) Chemoattractive activity of sonic hedgehog in the adult subventricular zone modulates the number of neural precursors reaching the olfactory bulb. Stem Cells 26(9):2311–2320. doi:10.1634/stemcells.2008-0297

    PubMed  CAS  Google Scholar 

  • Anilkumar N, Parsons M, Monk R, Ng T, Adams JC (2003) Interaction of fascin and protein kinase Calpha: a novel intersection in cell adhesion and motility. EMBO J 22(20):5390–5402. doi:10.1093/emboj/cdg521

    PubMed  CAS  Google Scholar 

  • Anton ES, Marchionni MA, Lee KF, Rakic P (1997) Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124(18):3501–3510

    PubMed  CAS  Google Scholar 

  • Anton ES, Ghashghaei HT, Weber JL, McCann C, Fischer TM, Cheung ID, Gassmann M, Messing A, Klein R, Schwab MH, Lloyd KC, Lai C (2004) Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nat Neurosci 7(12):1319–1328. doi:10.1038/nn1345

    PubMed  CAS  Google Scholar 

  • Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8(9):963–970. doi:10.1038/nm747

    PubMed  CAS  Google Scholar 

  • Balenci L, Saoudi Y, Grunwald D, Deloulme JC, Bouron A, Bernards A, Baudier J (2007) IQGAP1 regulates adult neural progenitors in vivo and vascular endothelial growth factor-triggered neural progenitor migration in vitro. J Neurosci 27(17):4716–4724. doi:10.1523/JNEUROSCI.0830-07.2007

    PubMed  CAS  Google Scholar 

  • Bath KG, Mandairon N, Jing D, Rajagopal R, Kapoor R, Chen ZY, Khan T, Proenca CC, Kraemer R, Cleland TA, Hempstead BL, Chao MV, Lee FS (2008) Variant brain-derived neurotrophic factor (Val66Met) alters adult olfactory bulb neurogenesis and spontaneous olfactory discrimination. J Neurosci 28(10):2383–2393. doi:10.1523/JNEUROSCI.4387-07.2008

    PubMed  CAS  Google Scholar 

  • Battista D, Rutishauser U (2010) Removal of polysialic acid triggers dispersion of subventricularly derived neuroblasts into surrounding CNS tissues. J Neurosci 30(11):3995–4003. doi:10.1523/JNEUROSCI.4382-09.2010

    PubMed  CAS  Google Scholar 

  • Belmadani A, Tran PB, Ren D, Miller RJ (2006) Chemokines regulate the migration of neural progenitors to sites of neuroinflammation. J Neurosci 26(12):3182–3191. doi:10.1523/JNEUROSCI.0156-06.2006

    PubMed  CAS  Google Scholar 

  • Belvindrah R, Hankel S, Walker J, Patton BL, Muller U (2007) Beta1 integrins control the formation of cell chains in the adult rostral migratory stream. J Neurosci 27(10):2704–2717. doi:10.1523/JNEUROSCI.2991-06.2007

    PubMed  CAS  Google Scholar 

  • Belvindrah R, Nissant A, Lledo PM (2011) Abnormal neuronal migration changes the fate of developing neurons in the postnatal olfactory bulb. J Neurosci 31(20):7551–7562. doi:10.1523/JNEUROSCI.6716-10.2011

    PubMed  CAS  Google Scholar 

  • Bergmann O, Liebl J, Bernard S, Alkass K, Yeung MS, Steier P, Kutschera W, Johnson L, Landen M, Druid H, Spalding KL, Frisen J (2012) The age of olfactory bulb neurons in humans. Neuron 74(4):634–639. doi:10.1016/j.neuron.2012.03.030

    PubMed  CAS  Google Scholar 

  • Birchmeier C, Gherardi E (1998) Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol 8(10):404–410

    PubMed  CAS  Google Scholar 

  • Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A, Matias I, Schiano-Moriello A, Paul P, Williams EJ, Gangadharan U, Hobbs C, Di Marzo V, Doherty P (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 163(3):463–468. doi:10.1083/jcb.200305129

    PubMed  CAS  Google Scholar 

  • Blake SM, Strasser V, Andrade N, Duit S, Hofbauer R, Schneider WJ, Nimpf J (2008) Thrombospondin-1 binds to ApoER2 and VLDL receptor and functions in postnatal neuronal migration. EMBO J 27(22):3069–3080. doi:10.1038/emboj.2008.223

    PubMed  CAS  Google Scholar 

  • Bolteus AJ, Bordey A (2004) GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci 24(35):7623–7631. doi:10.1523/JNEUROSCI.1999-04.2004

    PubMed  CAS  Google Scholar 

  • Bovetti S, Hsieh YC, Bovolin P, Perroteau I, Kazunori T, Puche AC (2007) Blood vessels form a scaffold for neuroblast migration in the adult olfactory bulb. J Neurosci 27(22):5976–5980. doi:10.1523/JNEUROSCI.0678-07.2007

    PubMed  CAS  Google Scholar 

  • Bozoyan L, Khlghatyan J, Saghatelyan A (2012) Astrocytes control the development of the migration-promoting vasculature scaffold in the postnatal brain via VEGF signaling. J Neurosci 32(5):1687–1704. doi:10.1523/JNEUROSCI.5531-11.2012

    PubMed  CAS  Google Scholar 

  • Bribian A, Barallobre MJ, Soussi-Yanicostas N, de Castro F (2006) Anosmin-1 modulates the FGF-2-dependent migration of oligodendrocyte precursors in the developing optic nerve. Mol Cell Neurosci 33(1):2–14. doi:10.1016/j.mcn.2006.05.009

    PubMed  CAS  Google Scholar 

  • Buonanno A (2010) The neuregulin signaling pathway and schizophrenia: from genes to synapses and neural circuits. Brain Res Bull 83(3–4):122–131. doi:10.1016/j.brainresbull.2010.07.012

    PubMed  CAS  Google Scholar 

  • Cariboni A, Pimpinelli F, Colamarino S, Zaninetti R, Piccolella M, Rumio C, Piva F, Rugarli EI, Maggi R (2004) The product of X-linked Kallmann’s syndrome gene (KAL1) affects the migratory activity of gonadotropin-releasing hormone (GnRH)-producing neurons. Hum Mol Genet 13(22):2781–2791. doi:10.1093/hmg/ddh309

    PubMed  CAS  Google Scholar 

  • Cayre M, Canoll P, Goldman JE (2009) Cell migration in the normal and pathological postnatal mammalian brain. Prog Neurobiol 88(1):41–63. doi:10.1016/j.pneurobio.2009.02.001

    PubMed  CAS  Google Scholar 

  • Chazal G, Durbec P, Jankovski A, Rougon G, Cremer H (2000) Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci 20(4):1446–1457

    PubMed  CAS  Google Scholar 

  • Chiaramello S, Dalmasso G, Bezin L, Marcel D, Jourdan F, Peretto P, Fasolo A, De Marchis S (2007) BDNF/ TrkB interaction regulates migration of SVZ precursor cells via PI3-K and MAP-K signalling pathways. Eur J Neurosci 26(7):1780–1790. doi:10.1111/j.1460-9568.2007.05818.x

    PubMed  CAS  Google Scholar 

  • Comte I, Kim Y, Young CC, van der Harg JM, Hockberger P, Bolam PJ, Poirier F, Szele FG (2011) Galectin-3 maintains cell motility from the subventricular zone to the olfactory bulb. J Cell Sci 124(Pt 14):2438–2447. doi:10.1242/jcs.079954

    PubMed  CAS  Google Scholar 

  • Conover JC, Doetsch F, Garcia-Verdugo JM, Gale NW, Yancopoulos GD, Alvarez-Buylla A (2000) Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci 3(11):1091–1097. doi:10.1038/80606

    PubMed  CAS  Google Scholar 

  • Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D (1996) In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16(8):2649–2658

    PubMed  CAS  Google Scholar 

  • Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S et al (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367(6462):455–459. doi:10.1038/367455a0

    PubMed  CAS  Google Scholar 

  • Curtis MA, Faull RL, Eriksson PS (2007a) The effect of neurodegenerative diseases on the subventricular zone. Nat Rev Neurosci 8(9):712–723. doi:10.1038/nrn2216

    PubMed  CAS  Google Scholar 

  • Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS (2007b) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315(5816):1243–1249. doi:1136281 [pii] 10.1126/science.1136281

    PubMed  CAS  Google Scholar 

  • Dode C, Levilliers J, Dupont JM, De Paepe A, Le Du N, Soussi-Yanicostas N, Coimbra RS, Delmaghani S, Compain-Nouaille S, Baverel F, Pecheux C, Le Tessier D, Cruaud C, Delpech M, Speleman F, Vermeulen S, Amalfitano A, Bachelot Y, Bouchard P, Cabrol S, Carel JC, Delemarre-van de Waal H, Goulet-Salmon B, Kottler ML, Richard O, Sanchez-Franco F, Saura R, Young J, Petit C, Hardelin JP (2003) Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat Genet 33(4):463–465. doi:10.1038/ng1122

    PubMed  CAS  Google Scholar 

  • Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17(13):5046–5061

    PubMed  CAS  Google Scholar 

  • Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36(6):1021–1034

    PubMed  CAS  Google Scholar 

  • Ekonomou A, Ballard CG, Pathmanaban ON, Perry RH, Perry EK, Kalaria RN, Minger SL (2011) Increased neural progenitors in vascular dementia. Neurobiol Aging 32(12):2152–2161. doi:10.1016/j.neurobiolaging.2010.01.007

    PubMed  Google Scholar 

  • Elola MT, Wolfenstein-Todel C, Troncoso MF, Vasta GR, Rabinovich GA (2007) Galectins: matricellular glycan-binding proteins linking cell adhesion, migration, and survival. Cell Mol Life Sci 64(13):1679–1700. doi:10.1007/s00018-007-7044-8

    PubMed  CAS  Google Scholar 

  • Emsley JG, Hagg T (2003) alpha6beta1 integrin directs migration of neuronal precursors in adult mouse forebrain. Exp Neurol 183(2):273–285

    PubMed  CAS  Google Scholar 

  • Gao Y, Vasilyev DV, Goncalves MB, Howell FV, Hobbs C, Reisenberg M, Shen R, Zhang MY, Strassle BW, Lu P, Mark L, Piesla MJ, Deng K, Kouranova EV, Ring RH, Whiteside GT, Bates B, Walsh FS, Williams G, Pangalos MN, Samad TA, Doherty P (2010) Loss of retrograde endocannabinoid signaling and reduced adult neurogenesis in diacylglycerol lipase knock-out mice. J Neurosci 30(6):2017–2024. doi:10.1523/JNEUROSCI.5693-09.2010

    PubMed  CAS  Google Scholar 

  • Garcia-Gonzalez D, Clemente D, Coelho M, Esteban PF, Soussi-Yanicostas N, de Castro F (2010) Dynamic roles of FGF-2 and Anosmin-1 in the migration of neuronal precursors from the subventricular zone during pre- and postnatal development. Exp Neurol 222(2):285–295. doi:10.1016/j.expneurol.2010.01.006

    PubMed  CAS  Google Scholar 

  • Garratt AN, Britsch S, Birchmeier C (2000) Neuregulin, a factor with many functions in the life of a schwann cell. Bioessays 22(11):987–996. doi:10.1002/1521-1878(200011)22:11<987::AID-BIES5>3.0.CO;2-5

    PubMed  CAS  Google Scholar 

  • Garzotto D, Giacobini P, Crepaldi T, Fasolo A, De Marchis S (2008) Hepatocyte growth factor regulates migration of olfactory interneuron precursors in the rostral migratory stream through Met-Grb2 coupling. J Neurosci 28(23):5901–5909. doi:10.1523/JNEUROSCI.1083-08.2008

    PubMed  CAS  Google Scholar 

  • Ghashghaei HT, Weber J, Pevny L, Schmid R, Schwab MH, Lloyd KC, Eisenstat DD, Lai C, Anton ES (2006) The role of neuregulin-ErbB4 interactions on the proliferation and organization of cells in the subventricular zone. Proc Natl Acad Sci U S A 103(6):1930–1935. doi:10.1073/pnas.0510410103

    PubMed  CAS  Google Scholar 

  • Godin JD, Thomas N, Laguesse S, Malinouskaya L, Close P, Malaise O, Purnelle A, Raineteau O, Campbell K, Fero M, Moonen G, Malgrange B, Chariot A, Metin C, Besson A, Nguyen L (2012) p27(Kip1) is a microtubule-associated protein that promotes microtubule polymerization during neuron migration. Dev Cell 23(4):729–744. doi:10.1016/j.devcel.2012.08.006

    PubMed  CAS  Google Scholar 

  • Goldstein B, Macara IG (2007) The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13(5):609–622. doi:10.1016/j.devcel.2007.10.007

    PubMed  CAS  Google Scholar 

  • Goncalves MB, Suetterlin P, Yip P, Molina-Holgado F, Walker DJ, Oudin MJ, Zentar MP, Pollard S, Yanez-Munoz RJ, Williams G, Walsh FS, Pangalos MN, Doherty P (2008) A diacylglycerol lipase-CB2 cannabinoid pathway regulates adult subventricular zone neurogenesis in an age-dependent manner. Mol Cell Neurosci 38(4):526–536. doi:10.1016/j.mcn.2008.05.001

    PubMed  CAS  Google Scholar 

  • Gonzalez-Martinez D, Kim SH, Hu Y, Guimond S, Schofield J, Winyard P, Vannelli GB, Turnbull J, Bouloux PM (2004) Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism. J Neurosci 24(46):10384–10392. doi:10.1523/JNEUROSCI.3400-04.2004

    PubMed  CAS  Google Scholar 

  • Goritz C, Frisen J (2012) Neural stem cells and neurogenesis in the adult. Cell Stem Cell 10(6):657–659. doi:10.1016/j.stem.2012.04.005

    PubMed  Google Scholar 

  • Grade S, Weng YC, Snapyan M, Kriz J, Malva JO, Saghatelyan A (2013) Brain-derived neurotrophic factor promotes vasculature-associated migration of neuronal precursors toward the ischemic striatum. PLoS One 8(1):e55039. doi:10.1371/journal.pone.0055039

    PubMed  CAS  Google Scholar 

  • Hack I, Bancila M, Loulier K, Carroll P, Cremer H (2002) Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat Neurosci 5(10):939–945. doi:10.1038/nn923

    PubMed  CAS  Google Scholar 

  • Hall A, Lalli G (2010) Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harb Perspect Biol 2(2):a001818. doi:10.1101/cshperspect.a001818

    PubMed  Google Scholar 

  • Herz J, Chen Y (2006) Reelin, lipoprotein receptors and synaptic plasticity. Nat Rev Neurosci 7(11):850–859. doi:10.1038/nrn2009

    PubMed  CAS  Google Scholar 

  • Higginbotham H, Tanaka T, Brinkman BC, Gleeson JG (2006) GSK3beta and PKCzeta function in centrosome localization and process stabilization during Slit-mediated neuronal repolarization. Mol Cell Neurosci 32(1–2):118–132. doi:10.1016/j.mcn.2006.03.003

    PubMed  CAS  Google Scholar 

  • Hippenmeyer S, Shneider NA, Birchmeier C, Burden SJ, Jessell TM, Arber S (2002) A role for neuregulin1 signaling in muscle spindle differentiation. Neuron 36(6):1035–1049

    PubMed  CAS  Google Scholar 

  • Hirota Y, Ohshima T, Kaneko N, Ikeda M, Iwasato T, Kulkarni AB, Mikoshiba K, Okano H, Sawamoto K (2007) Cyclin-dependent kinase 5 is required for control of neuroblast migration in the postnatal subventricular zone. J Neurosci 27(47):12829–12838. doi:10.1523/JNEUROSCI.1014-07.2007

    PubMed  CAS  Google Scholar 

  • Holland SJ, Gale NW, Mbamalu G, Yancopoulos GD, Henkemeyer M, Pawson T (1996) Bidirectional signalling through the EPH-family receptor Nuk and its transmembrane ligands. Nature 383(6602):722–725. doi:10.1038/383722a0

    PubMed  CAS  Google Scholar 

  • Hu H (1999) Chemorepulsion of neuronal migration by Slit2 in the developing mammalian forebrain. Neuron 23(4):703–711

    PubMed  CAS  Google Scholar 

  • Hurtado-Chong A, Yusta-Boyo MJ, Vergano-Vera E, Bulfone A, de Pablo F, Vicario-Abejon C (2009) IGF-I promotes neuronal migration and positioning in the olfactory bulb and the exit of neuroblasts from the subventricular zone. Eur J Neurosci 30(5):742–755. doi:10.1111/j.1460-9568.2009.06870.x

    PubMed  Google Scholar 

  • Imitola J, Raddassi K, Park KI, Mueller FJ, Nieto M, Teng YD, Frenkel D, Li J, Sidman RL, Walsh CA, Snyder EY, Khoury SJ (2004) Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A 101(52):18117–18122. doi:10.1073/pnas.0408258102

    PubMed  CAS  Google Scholar 

  • Itoh N, Ornitz DM (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet 20(11):563–569. doi:10.1016/j.tig.2004.08.007

    PubMed  CAS  Google Scholar 

  • James R, Kim Y, Hockberger PE, Szele FG (2011) Subventricular zone cell migration: lessons from quantitative two-photon microscopy. Front Neurosci 5:30. doi:10.3389/fnins.2011.00030

    PubMed  Google Scholar 

  • Jankovski A, Sotelo C (1996) Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J Comp Neurol 371(3):376–396. doi:10.1002/(SICI)1096-9861(19960729)371:3<376::AID-CNE3>3.0.CO;2-#

    PubMed  CAS  Google Scholar 

  • Jarov A, Williams KP, Ling LE, Koteliansky VE, Duband JL, Fournier-Thibault C (2003) A dual role for Sonic hedgehog in regulating adhesion and differentiation of neuroepithelial cells. Dev Biol 261(2):520–536

    PubMed  CAS  Google Scholar 

  • Jin K, Xie L, Kim SH, Parmentier-Batteur S, Sun Y, Mao XO, Childs J, Greenberg DA (2004) Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol Pharmacol 66(2):204–208. doi:10.1124/mol.66.2.204

    PubMed  CAS  Google Scholar 

  • Jones FS, Jones PL (2000) The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev Dyn 218(2):235–259. doi:10.1002/(SICI)1097-0177(200006)218:2<235::AID-DVDY2>3.0.CO;2-G

    PubMed  CAS  Google Scholar 

  • Jorgensen JR, Fransson A, Fjord-Larsen L, Thompson LH, Houchins JP, Andrade N, Torp M, Kalkkinen N, Andersson E, Lindvall O, Ulfendahl M, Brunak S, Johansen TE, Wahlberg LU (2012) Cometin is a novel neurotrophic factor that promotes neurite outgrowth and neuroblast migration in vitro and supports survival of spiral ganglion neurons in vivo. Exp Neurol 233(1):172–181. doi:10.1016/j.expneurol.2011.09.027

    PubMed  CAS  Google Scholar 

  • Kaneko N, Marin O, Koike M, Hirota Y, Uchiyama Y, Wu JY, Lu Q, Tessier-Lavigne M, Alvarez-Buylla A, Okano H, Rubenstein JL, Sawamoto K (2010) New neurons clear the path of astrocytic processes for their rapid migration in the adult brain. Neuron 67(2):213–223. doi:10.1016/j.neuron.2010.06.018

    PubMed  CAS  Google Scholar 

  • Kawauchi T, Sekine K, Shikanai M, Chihama K, Tomita K, Kubo K, Nakajima K, Nabeshima Y, Hoshino M (2010) Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron 67(4):588–602. doi:10.1016/j.neuron.2010.07.007

    PubMed  CAS  Google Scholar 

  • Kazanis I, Lathia JD, Vadakkan TJ, Raborn E, Wan R, Mughal MR, Eckley DM, Sasaki T, Patton B, Mattson MP, Hirschi KK, Dickinson ME, ffrench-Constant C (2010) Quiescence and activation of stem and precursor cell populations in the subependymal zone of the mammalian brain are associated with distinct cellular and extracellular matrix signals. J Neurosci 30(29):9771–9781. doi:10.1523/JNEUROSCI.0700-10.2010

    PubMed  CAS  Google Scholar 

  • Keimpema E, Barabas K, Morozov YM, Tortoriello G, Torii M, Cameron G, Yanagawa Y, Watanabe M, Mackie K, Harkany T (2010) Differential subcellular recruitment of monoacylglycerol lipase generates spatial specificity of 2-arachidonoyl glycerol signaling during axonal pathfinding. J Neurosci 30(42):13992–14007. doi:10.1523/JNEUROSCI.2126-10.2010

    PubMed  CAS  Google Scholar 

  • Kerjan G, Dolan J, Haumaitre C, Schneider-Maunoury S, Fujisawa H, Mitchell KJ, Chedotal A (2005) The transmembrane semaphorin Sema6A controls cerebellar granule cell migration. Nat Neurosci 8(11):1516–1524. doi:10.1038/nn1555

    PubMed  CAS  Google Scholar 

  • Keynes R, Tannahill D, Morgenstern DA, Johnson AR, Cook GM, Pini A (1997) Surround repulsion of spinal sensory axons in higher vertebrate embryos. Neuron 18(6):889–897

    PubMed  CAS  Google Scholar 

  • Kim HM, Qu T, Kriho V, Lacor P, Smalheiser N, Pappas GD, Guidotti A, Costa E, Sugaya K (2002) Reelin function in neural stem cell biology. Proc Natl Acad Sci U S A 99(6):4020–4025. doi:10.1073/pnas.062698299

    PubMed  CAS  Google Scholar 

  • Kim Y, Comte I, Szabo G, Hockberger P, Szele FG (2009) Adult mouse subventricular zone stem and progenitor cells are sessile and epidermal growth factor receptor negatively regulates neuroblast migration. PLoS One 4(12):e8122. doi:10.1371/journal.pone.0008122

    PubMed  Google Scholar 

  • Kirschenbaum B, Doetsch F, Lois C, Alvarez-Buylla A (1999) Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J Neurosci 19(6):2171–2180

    PubMed  CAS  Google Scholar 

  • Klein R (2012) Eph/ephrin signalling during development. Development 139(22):4105–4109. doi:10.1242/dev.074997

    PubMed  CAS  Google Scholar 

  • Koizumi H, Higginbotham H, Poon T, Tanaka T, Brinkman BC, Gleeson JG (2006) Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nat Neurosci 9(6):779–786. doi:10.1038/nn1704

    PubMed  CAS  Google Scholar 

  • Kokovay E, Goderie S, Wang Y, Lotz S, Lin G, Sun Y, Roysam B, Shen Q, Temple S (2010) Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell 7(2):163–173. doi:10.1016/j.stem.2010.05.019

    PubMed  CAS  Google Scholar 

  • Lacar B, Young SZ, Platel JC, Bordey A (2012) Preparation of acute subventricular zone slices for calcium imaging. J Vis Exp (67):e4071. doi:10.3791/4071

  • Lawler J (2000) The functions of thrombospondin-1 and-2. Curr Opin Cell Biol 12(5):634–640

    PubMed  CAS  Google Scholar 

  • Lazarini F, Lledo PM (2011) Is adult neurogenesis essential for olfaction? Trends Neurosci 34(1):20–30. doi:10.1016/j.tins.2010.09.006

    PubMed  CAS  Google Scholar 

  • Lee SR, Kim HY, Rogowska J, Zhao BQ, Bhide P, Parent JM, Lo EH (2006) Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J Neurosci 26(13):3491–3495. doi:10.1523/JNEUROSCI.4085-05.2006

    PubMed  CAS  Google Scholar 

  • Lee HS, Han J, Lee SH, Park JA, Kim KW (2010) Meteorin promotes the formation of GFAP-positive glia via activation of the Jak-STAT3 pathway. J Cell Sci 123(Pt 11):1959–1968. doi:10.1242/jcs.063784

    PubMed  CAS  Google Scholar 

  • Lepousez G, Valley MT, Lledo PM (2013) The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu Rev Physiol 75:339–363. doi:10.1146/annurev-physiol-030212-183731

    PubMed  CAS  Google Scholar 

  • Li X, Su H, Fu QL, Guo J, Lee DH, So KF, Wu W (2011) Soluble NgR fusion protein modulates the proliferation of neural progenitor cells via the Notch pathway. Neurochem Res 36(12):2363–2372. doi:10.1007/s11064-011-0562-7

    PubMed  CAS  Google Scholar 

  • Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7(3):179–193. doi:10.1038/nrn1867

    PubMed  CAS  Google Scholar 

  • Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271(5251):978–981

    PubMed  CAS  Google Scholar 

  • Macas J, Nern C, Plate KH, Momma S (2006) Increased generation of neuronal progenitors after ischemic injury in the aged adult human forebrain. J Neurosci 26(50):13114–13119. doi:10.1523/JNEUROSCI.4667-06.2006

    PubMed  CAS  Google Scholar 

  • Mason I (2007) Initiation to end point: the multiple roles of fibroblast growth factors in neural development. Nat Rev Neurosci 8(8):583–596. doi:10.1038/nrn2189

    PubMed  CAS  Google Scholar 

  • McCaffrey LM, Macara IG (2009) Widely conserved signaling pathways in the establishment of cell polarity. Cold Spring Harb Perspect Biol 1(2):a001370. doi:10.1101/cshperspect.a001370

    PubMed  Google Scholar 

  • Mejia-Gervacio S, Murray K, Sapir T, Belvindrah R, Reiner O, Lledo PM (2012) MARK2/Par-1 guides the directionality of neuroblasts migrating to the olfactory bulb. Mol Cell Neurosci 49(2):97–103. doi:10.1016/j.mcn.2011.10.006

    PubMed  CAS  Google Scholar 

  • Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2008) Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3(3):265–278. doi:10.1016/j.stem.2008.07.004

    PubMed  CAS  Google Scholar 

  • Miyakoshi LM, Todeschini AR, Mendez-Otero R, Hedin-Pereira C (2012) Role of the 9-O-acetyl GD3 in subventricular zone neuroblast migration. Mol Cell Neurosci 49(2):240–249. doi:10.1016/j.mcn.2011.08.010

    PubMed  CAS  Google Scholar 

  • Mobley AK, McCarty JH (2011) beta8 integrin is essential for neuroblast migration in the rostral migratory stream. Glia 59(11):1579–1587. doi:10.1002/glia.21199

    PubMed  Google Scholar 

  • Molina-Holgado F, Rubio-Araiz A, Garcia-Ovejero D, Williams RJ, Moore JD, Arevalo-Martin A, Gomez-Torres O, Molina-Holgado E (2007) CB2 cannabinoid receptors promote mouse neural stem cell proliferation. Eur J Neurosci 25(3):629–634. doi:10.1111/j.1460-9568.2007.05322.x

    PubMed  Google Scholar 

  • Murase S, Horwitz AF (2002) Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J Neurosci 22(9):3568–3579. doi:20026349

    PubMed  CAS  Google Scholar 

  • Nam SC, Kim Y, Dryanovski D, Walker A, Goings G, Woolfrey K, Kang SS, Chu C, Chenn A, Erdelyi F, Szabo G, Hockberger P, Szele FG (2007) Dynamic features of postnatal subventricular zone cell motility: a two-photon time-lapse study. J Comp Neurol 505(2):190–208. doi:10.1002/cne.21473

    PubMed  Google Scholar 

  • Ng KL, Li JD, Cheng MY, Leslie FM, Lee AG, Zhou QY (2005) Dependence of olfactory bulb neurogenesis on prokineticin 2 signaling. Science 308(5730):1923–1927. doi:10.1126/science.1112103

    PubMed  CAS  Google Scholar 

  • Nguyen-Ba-Charvet KT, Picard-Riera N, Tessier-Lavigne M, Baron-Van Evercooren A, Sotelo C, Chedotal A (2004) Multiple roles for slits in the control of cell migration in the rostral migratory stream. J Neurosci 24(6):1497–1506. doi:10.1523/JNEUROSCI.4729-03.2004

    PubMed  CAS  Google Scholar 

  • Ohab JJ, Fleming S, Blesch A, Carmichael ST (2006) A neurovascular niche for neurogenesis after stroke. J Neurosci 26(50):13007–13016. doi:10.1523/JNEUROSCI.4323-06.2006

    PubMed  CAS  Google Scholar 

  • Oudin MJ, Gajendra S, Williams G, Hobbs C, Lalli G, Doherty P (2011a) Endocannabinoids regulate the migration of subventricular zone-derived neuroblasts in the postnatal brain. J Neurosci 31(11):4000–4011. doi:10.1523/JNEUROSCI.5483-10.2011

    PubMed  CAS  Google Scholar 

  • Oudin MJ, Hobbs C, Doherty P (2011b) DAGL-dependent endocannabinoid signalling: roles in axonal pathfinding, synaptic plasticity and adult neurogenesis. Eur J Neurosci 34(10):1634–1646. doi:10.1111/j.1460-9568.2011.07831.x

    PubMed  Google Scholar 

  • Palazuelos J, Aguado T, Egia A, Mechoulam R, Guzman M, Galve-Roperh I (2006) Non-psychoactive CB2 cannabinoid agonists stimulate neural progenitor proliferation. FASEB J 20(13):2405–2407. doi:10.1096/fj.06-6164fje

    PubMed  CAS  Google Scholar 

  • Paratcha G, Ibanez CF, Ledda F (2006) GDNF is a chemoattractant factor for neuronal precursor cells in the rostral migratory stream. Mol Cell Neurosci 31(3):505–514. doi:10.1016/j.mcn.2005.11.007

    PubMed  CAS  Google Scholar 

  • Pencea V, Luskin MB (2003) Prenatal development of the rodent rostral migratory stream. J Comp Neurol 463(4):402–418. doi:10.1002/cne.10746

    PubMed  Google Scholar 

  • Peretto P, Giachino C, Aimar P, Fasolo A, Bonfanti L (2005) Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J Comp Neurol 487(4):407–427. doi:10.1002/cne.20576

    PubMed  Google Scholar 

  • Pernet V, Schwab ME (2012) The role of Nogo-A in axonal plasticity, regrowth and repair. Cell Tissue Res 349(1):97–104. doi:10.1007/s00441-012-1432-6

    PubMed  CAS  Google Scholar 

  • Pesheva P, Gennarini G, Goridis C, Schachner M (1993) The F3/11 cell adhesion molecule mediates the repulsion of neurons by the extracellular matrix glycoprotein J1-160/180. Neuron 10(1):69–82

    PubMed  CAS  Google Scholar 

  • Platel JC, Lacar B, Bordey A (2007) GABA and glutamate signaling: homeostatic control of adult forebrain neurogenesis. J Mol Histol 38(6):602–610

    PubMed  Google Scholar 

  • Platel JC, Dave KA, Bordey A (2008a) Control of neuroblast production and migration by converging GABA and glutamate signals in the postnatal forebrain. J Physiol 586(16):3739–3743. doi:10.1113/jphysiol.2008.155325

    PubMed  CAS  Google Scholar 

  • Platel JC, Heintz T, Young S, Gordon V, Bordey A (2008b) Tonic activation of GLUK5 kainate receptors decreases neuroblast migration in whole-mounts of the subventricular zone. J Physiol 586(16):3783–3793. doi:10.1113/jphysiol.2008.155879

    PubMed  CAS  Google Scholar 

  • Platel JC, Dave KA, Gordon V, Lacar B, Rubio ME, Bordey A (2010) NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron 65(6):859–872. doi:10.1016/j.neuron.2010.03.009

    PubMed  CAS  Google Scholar 

  • Ponzetto C, Zhen Z, Audero E, Maina F, Bardelli A, Basile ML, Giordano S, Narsimhan R, Comoglio P (1996) Specific uncoupling of GRB2 from the Met receptor. Differential effects on transformation and motility. J Biol Chem 271(24):14119–14123

    PubMed  CAS  Google Scholar 

  • Probstmeier R, Michels M, Franz T, Chan BM, Pesheva P (1999) Tenascin-R interferes with integrin-dependent oligodendrocyte precursor cell adhesion by a ganglioside-mediated signalling mechanism. Eur J Neurosci 11(7):2474–2488

    PubMed  CAS  Google Scholar 

  • Prosser HM, Bradley A, Caldwell MA (2007) Olfactory bulb hypoplasia in Prokr2 null mice stems from defective neuronal progenitor migration and differentiation. Eur J Neurosci 26(12):3339–3344. doi:10.1111/j.1460-9568.2007.05958.x

    PubMed  Google Scholar 

  • Puverel S, Nakatani H, Parras C, Soussi-Yanicostas N (2009) Prokineticin receptor 2 expression identifies migrating neuroblasts and their subventricular zone transient-amplifying progenitors in adult mice. J Comp Neurol 512(2):232–242. doi:10.1002/cne.21888

    PubMed  CAS  Google Scholar 

  • Reisenberg M, Singh PK, Williams G, Doherty P (2012) The diacylglycerol lipases: structure, regulation and roles in and beyond endocannabinoid signalling. Philos Trans R Soc Lond B Biol Sci 367(1607):3264–3275. doi:10.1098/rstb.2011.0387

    PubMed  CAS  Google Scholar 

  • Renaud J, Kerjan G, Sumita I, Zagar Y, Georget V, Kim D, Fouquet C, Suda K, Sanbo M, Suto F, Ackerman SL, Mitchell KJ, Fujisawa H, Chedotal A (2008) Plexin-A2 and its ligand, Sema6A, control nucleus-centrosome coupling in migrating granule cells. Nat Neurosci 11(4):440–449. doi:10.1038/nn2064

    PubMed  CAS  Google Scholar 

  • Rio C, Rieff HI, Qi P, Khurana TS, Corfas G (1997) Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19(1):39–50

    PubMed  CAS  Google Scholar 

  • Robin AM, Zhang ZG, Wang L, Zhang RL, Katakowski M, Zhang L, Wang Y, Zhang C, Chopp M (2006) Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. J Cereb Blood Flow Metab 26(1):125–134. doi:10.1038/sj.jcbfm.9600172

    PubMed  CAS  Google Scholar 

  • Rolando C, Parolisi R, Boda E, Schwab ME, Rossi F, Buffo A (2012) Distinct roles of Nogo-a and Nogo receptor 1 in the homeostatic regulation of adult neural stem cell function and neuroblast migration. J Neurosci 32(49):17788–17799. doi:10.1523/JNEUROSCI.3142-12.2012

    PubMed  CAS  Google Scholar 

  • Rousselot P, Lois C, Alvarez-Buylla A (1995) Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J Comp Neurol 351(1):51–61. doi:10.1002/cne.903510106

    PubMed  CAS  Google Scholar 

  • Rouzer CA, Ghebreselasie K, Marnett LJ (2002) Chemical stability of 2-arachidonylglycerol under biological conditions. Chem Phys Lipids 119(1–2):69–82

    PubMed  CAS  Google Scholar 

  • Saghatelyan A, de Chevigny A, Schachner M, Lledo PM (2004) Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nat Neurosci 7(4):347–356. doi:10.1038/nn1211

    PubMed  CAS  Google Scholar 

  • Saha B, Ypsilanti AR, Boutin C, Cremer H, Chedotal A (2012) Plexin-B2 regulates the proliferation and migration of neuroblasts in the postnatal and adult subventricular zone. J Neurosci 32(47):16892–16905. doi:10.1523/JNEUROSCI.0344-12.2012

    PubMed  CAS  Google Scholar 

  • Sanai N, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A (2007) Comment on “Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension”. Science 318(5849):393; author reply 393. doi:10.1126/science.1145011

    Google Scholar 

  • Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478(7369):382–386. doi:10.1038/nature10487

    PubMed  CAS  Google Scholar 

  • Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N, Murcia NS, Garcia-Verdugo JM, Marin O, Rubenstein JL, Tessier-Lavigne M, Okano H, Alvarez-Buylla A (2006) New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311(5761):629–632. doi:10.1126/science.1119133

    PubMed  CAS  Google Scholar 

  • Schaar BT, McConnell SK (2005) Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci U S A 102(38):13652–13657. doi:10.1073/pnas.0506008102

    PubMed  CAS  Google Scholar 

  • Shieh JC, Schaar BT, Srinivasan K, Brodsky FM, McConnell SK (2011) Endocytosis regulates cell soma translocation and the distribution of adhesion proteins in migrating neurons. PLoS One 6(3):e17802. doi:10.1371/journal.pone.0017802

    PubMed  CAS  Google Scholar 

  • Shinohara R, Thumkeo D, Kamijo H, Kaneko N, Sawamoto K, Watanabe K, Takebayashi H, Kiyonari H, Ishizaki T, Furuyashiki T, Narumiya S (2012) A role for mDia, a Rho-regulated actin nucleator, in tangential migration of interneuron precursors. Nat Neurosci 15(3):373–380. doi:10.1038/nn.3020, S371-372

    PubMed  CAS  Google Scholar 

  • Shu T, Ayala R, Nguyen MD, Xie Z, Gleeson JG, Tsai LH (2004) Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning. Neuron 44(2):263–277. doi:10.1016/j.neuron.2004.09.030

    PubMed  CAS  Google Scholar 

  • Simo S, Pujadas L, Segura MF, La Torre A, Del Rio JA, Urena JM, Comella JX, Soriano E (2007) Reelin induces the detachment of postnatal subventricular zone cells and the expression of the Egr-1 through Erk1/2 activation. Cereb Cortex 17(2):294–303. doi:10.1093/cercor/bhj147

    PubMed  Google Scholar 

  • Snapyan M, Lemasson M, Brill MS, Blais M, Massouh M, Ninkovic J, Gravel C, Berthod F, Gotz M, Barker PA, Parent A, Saghatelyan A (2009) Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J Neurosci 29(13):4172–4188. doi:10.1523/JNEUROSCI.4956-08.2009

    PubMed  CAS  Google Scholar 

  • Sonego M, Gajendra S, Parsons M, Ma Y, Hobbs C, Zentar MP, Williams G, Machesky LM, Doherty P, Lalli G (2013) Fascin regulates the migration of subventricular zone-derived neuroblasts in the postnatal brain. J Neurosci 33(30):12171–12185. doi:10.1523/JNEUROSCI.0653-13.2013

    Google Scholar 

  • Sonego M, Ya Z, Oudin MJ, Doherty P, Lalli G (in press-b) In vivo postnatal electroporation and time-lapse imaging of neuroblast migration in mouse acute brain slices. J Vis Exp

    Google Scholar 

  • Soussi-Yanicostas N, de Castro F, Julliard AK, Perfettini I, Chedotal A, Petit C (2002) Anosmin-1, defective in the X-linked form of Kallmann syndrome, promotes axonal branch formation from olfactory bulb output neurons. Cell 109(2):217–228

    PubMed  CAS  Google Scholar 

  • Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Bostrom E, Westerlund I, Vial C, Buchholz BA, Possnert G, Mash DC, Druid H, Frisen J (2013) Dynamics of hippocampal neurogenesis in adult humans. Cell 153(6):1219–1227. doi:10.1016/j.cell.2013.05.002

    PubMed  CAS  Google Scholar 

  • Staquicini FI, Dias-Neto E, Li J, Snyder EY, Sidman RL, Pasqualini R, Arap W (2009) Discovery of a functional protein complex of netrin-4, laminin gamma1 chain, and integrin alpha6beta1 in mouse neural stem cells. Proc Natl Acad Sci U S A 106(8):2903–2908. doi:10.1073/pnas.0813286106

    PubMed  CAS  Google Scholar 

  • Stewart RR, Hoge GJ, Zigova T, Luskin MB (2002) Neural progenitor cells of the neonatal rat anterior subventricular zone express functional GABA(A) receptors. J Neurobiol 50(4):305–322

    PubMed  CAS  Google Scholar 

  • Sundholm-Peters NL, Yang HK, Goings GE, Walker AS, Szele FG (2005) Subventricular zone neuroblasts emigrate toward cortical lesions. J Neuropathol Exp Neurol 64(12):1089–1100

    PubMed  Google Scholar 

  • Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG (2004) Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 165(5):709–721. doi:10.1083/jcb.200309025

    PubMed  CAS  Google Scholar 

  • Tissir F, Goffinet AM (2003) Reelin and brain development. Nat Rev Neurosci 4(6):496–505. doi:10.1038/nrn1113

    PubMed  CAS  Google Scholar 

  • Tomasiewicz H, Ono K, Yee D, Thompson C, Goridis C, Rutishauser U, Magnuson T (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11(6):1163–1174

    PubMed  CAS  Google Scholar 

  • Tran TS, Kolodkin AL, Bharadwaj R (2007) Semaphorin regulation of cellular morphology. Annu Rev Cell Dev Biol 23:263–292. doi:10.1146/annurev.cellbio.22.010605.093554

    PubMed  CAS  Google Scholar 

  • Wang DD, Krueger DD, Bordey A (2003) GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. J Physiol 550 (Pt 3):785–800. doi:10.1113/jphysiol.2003.042572

    PubMed  CAS  Google Scholar 

  • Wang Z, Andrade N, Torp M, Wattananit S, Arvidsson A, Kokaia Z, Jorgensen JR, Lindvall O (2012) Meteorin is a chemokinetic factor in neuroblast migration and promotes stroke-induced striatal neurogenesis. J Cereb Blood Flow Metab 32(2):387–398. doi:10.1038/jcbfm.2011.156

    PubMed  CAS  Google Scholar 

  • Wells A (1999) EGF receptor. Int J Biochem Cell Biol 31(6):637–643

    PubMed  CAS  Google Scholar 

  • Wichterle H, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Direct evidence for homotypic, glia-independent neuronal migration. Neuron 18(5):779–791

    PubMed  CAS  Google Scholar 

  • Williams EJ, Walsh FS, Doherty P (2003) The FGF receptor uses the endocannabinoid signaling system to couple to an axonal growth response. J Cell Biol 160(4):481–486. doi:10.1083/jcb.200210164

    PubMed  CAS  Google Scholar 

  • Wittko IM, Schanzer A, Kuzmichev A, Schneider FT, Shibuya M, Raab S, Plate KH (2009) VEGFR-1 regulates adult olfactory bulb neurogenesis and migration of neural progenitors in the rostral migratory stream in vivo. J Neurosci 29(27):8704–8714. doi:10.1523/JNEUROSCI.5527-08.2009

    PubMed  CAS  Google Scholar 

  • Wu W, Wong K, Chen J, Jiang Z, Dupuis S, Wu JY, Rao Y (1999) Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 400(6742):331–336. doi:10.1038/22477

    PubMed  CAS  Google Scholar 

  • Xiao ZC, Bartsch U, Margolis RK, Rougon G, Montag D, Schachner M (1997) Isolation of a tenascin-R binding protein from mouse brain membranes. A phosphacan-related chondroitin sulfate proteoglycan. J Biol Chem 272(51):32092–32101

    PubMed  CAS  Google Scholar 

  • Yagita Y, Sakurai T, Tanaka H, Kitagawa K, Colman DR, Shan W (2009) N-cadherin mediates interaction between precursor cells in the subventricular zone and regulates further differentiation. J Neurosci Res 87(15):3331–3342. doi:10.1002/jnr.22044

    PubMed  CAS  Google Scholar 

  • Yan YP, Sailor KA, Lang BT, Park SW, Vemuganti R, Dempsey RJ (2007) Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia. J Cereb Blood Flow Metab 27(6):1213–1224. doi:10.1038/sj.jcbfm.9600432

    PubMed  CAS  Google Scholar 

  • Yancopoulos GD, Klagsbrun M, Folkman J (1998) Vasculogenesis, angiogenesis, and growth factors: ephrins enter the fray at the border. Cell 93(5):661–664

    PubMed  CAS  Google Scholar 

  • Young SZ, Taylor MM, Bordey A (2011) Neurotransmitters couple brain activity to subventricular zone neurogenesis. Eur J Neurosci 33(6):1123–1132. doi:10.1111/j.1460-9568.2011.07611.x

    PubMed  Google Scholar 

  • Ypsilanti AR, Zagar Y, Chedotal A (2010) Moving away from the midline: new developments for Slit and Robo. Development 137(12):1939–1952. doi:10.1242/dev.044511

    PubMed  CAS  Google Scholar 

  • Zhang H, Vutskits L, Pepper MS, Kiss JZ (2003) VEGF is a chemoattractant for FGF-2-stimulated neural progenitors. J Cell Biol 163(6):1375–1384. doi:10.1083/jcb.200308040

    PubMed  CAS  Google Scholar 

  • Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132(4):645–660. doi:10.1016/j.cell.2008.01.033

    PubMed  CAS  Google Scholar 

  • Zigova T, Pencea V, Wiegand SJ, Luskin MB (1998) Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci 11(4):234–245. doi:10.1006/mcne.1998.0684

    PubMed  CAS  Google Scholar 

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Acknowledgments

 Work in the Lalli lab is funded by the Wellcome Trust. I thank Patrick Doherty and Giovanni Lesa for valuable comments on this chapter, Madeleine Oudin and members of the Lalli and Doherty labs for providing neuroblast images.

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Lalli, G. (2014). Extracellular Signals Controlling Neuroblast Migration in the Postnatal Brain. In: Nguyen, L., Hippenmeyer, S. (eds) Cellular and Molecular Control of Neuronal Migration. Advances in Experimental Medicine and Biology, vol 800. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7687-6_9

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