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Cadherins in Neural Development

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The Cadherin Superfamily

Abstract

Cadherins play many diverse roles in the development of the nervous system of vertebrates. Far from being simple adhesion molecules, they also orchestrate cell generation, cell movements, and cell morphogenesis. Cadherins also regulate specificity of cell-to-cell interactions during neuronal circuit formation and function. Cadherin expression during neural development is also dynamic and highly regulated. At each phase of embryo development, cadherins emerge as key molecular determinants of neural function through their many diverse binding partners. Additionally, they play important roles in the plasticity of the nervous system, a key feature believed to underpin the ability of the brain to function. Many neurodevelopmental disorders also have cadherin disfunction at their heart indicating that cadherin-based therapies may emerge as future treatments for these devastating conditions.

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References

  • Abe K, Chisaka O, Van Roy F, Takeichi M (2004) Stability of dendritic spines and synaptic contacts is controlled by alpha N-catenin. Nat Neurosci 7:357–363

    Article  CAS  PubMed  Google Scholar 

  • Ahrens T, Pertz O, Haussinger D et al (2002) Analysis of heterophilic and homophilic interactions of cadherins using the c-Jun/c-Fos dimerization domains. J Biol Chem 277:19455–19460

    Article  CAS  PubMed  Google Scholar 

  • Aiga M, Levinson JN, Bamji SX (2011) N-cadherin and neuroligins cooperate to regulate synapse formation in hippocampal cultures. J Biol Chem 286:851–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alberini CM (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89:121–145

    Article  CAS  PubMed  Google Scholar 

  • Andrews GL, Mastick GS (2003) R-cadherin is a Pax6-regulated, growth-promoting cue for pioneer axons. J Neurosci 23:9873–9880

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arikkath J, Reichardt LF (2008) Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity. Trends Neurosci 31:487–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Astick M, Tubby K, Mubarak WM et al (2014) Central topography of cranial motor nuclei controlled by differential cadherin expression. Curr Biol 24:2541–2547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babb SG, Marrs J (2004) E-cadherin regulates cell movements and tissue formation in early zebrafish embryos. Dev Dyn 230:263–277

    Article  CAS  PubMed  Google Scholar 

  • Barnes SH, Price SR, Wentzel C, Guthrie SC (2010) Cadherin-7 and cadherin-6B differentially regulate the growth, branching and guidance of cranial motor axons. Development 137:805–814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bekirov IH, Nagy V, Svoronos A et al (2008) Cadherin-8 and N cadherin differentially regulate pre- and postsynaptic development of the hippocampal mossy fiber pathway. Hippocampus 18:349–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bellion A, Baudoin J-P, Alvarez C (2005) Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J Neurosci 25:5691–5699

    Article  CAS  PubMed  Google Scholar 

  • Bello SM, Millo H, Rajebhosale M, Price SR (2012) Catenin-dependent cadherin function drives divisional segregation of spinal motor neurons. J Neurosci 32:490–505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhalla K, LuoY BT et al (2008) Alterations in CDH15 and KIRREL3 in patients with mild to severe intellectual disability. Am J Hum Genet 83:703–713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bixby JL, Lilien J, Reichardt LF (1988) Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J Cell Biol 107:353–361

    Article  CAS  PubMed  Google Scholar 

  • Bixby JL, Grunwald GB, Bookman RJ (1994) Ca2+ influx and neurite growth in response to purified N-cadherin and laminin. J Cell Biol 127:1461–1475

    Article  CAS  PubMed  Google Scholar 

  • Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borchers A, David R, Wedlich D (2001) Xenopus cadherin-11 restrains cranial neural crest migration and influences neural crest specification. Development 128:3049–3060

    CAS  PubMed  Google Scholar 

  • Børglum AD, Demontis D, Grove J et al (2014) Genome-wide study of association and interaction with maternal cytomegalovirus infection suggests new schizophrenia loci. Mol Psychiatry 19:325–333

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bozdagi O, Valcin M, Poskanzer K et al (2004) Temporally distinct demands for classic cadherins in synapse formation and maturation. Mol Cell Neurosci 27:509–521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bozdagi O, Wang XB, Nikitczuk JS et al (2010) Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin. J Neurosci 30:9984–9989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradke F, Dotti CG (2000) Establishment of neuronal polarity: lessons from cultured hippocampal neurons. Curr Opin Neurobiol 10:574–581

    Article  CAS  PubMed  Google Scholar 

  • Brigidi GS, Bamji SX (2011) Cadherin-catenin adhesion complexes at the synapse. Curr Opin Neurobiol 21:208–214

    Article  CAS  PubMed  Google Scholar 

  • Cappello S, Attardo A, Wu X et al (2006) The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci 9:1099–1107. doi:10.1038/nn1744

    Article  CAS  PubMed  Google Scholar 

  • Carver EA, Jiang R, Lan Y et al (2001) The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition the mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol Cell Biol 21:8184–8188. doi:10.1128/MCB.21.23.8184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chadborn N, Eickholt B, Doherty P, Bolsover S (2002) Direct measurement of local raised subplasmalemmal calcium concentrations in growth cones advancing on an N-cadherin substrate. Eur J Neurosci 15:1891–1898

    Article  PubMed  Google Scholar 

  • Chang L, Blain D, Bertuzzi S, Brooks BP (2006) Uveal coloboma: clinical and basic science update. Curr Opin Ophthalmol 17:447–470. doi:10.1097/01.icu.0000243020.82380.f6

    Article  PubMed  Google Scholar 

  • Chapman NH, Estes A, Munson J et al (2011) Genome-scan for IQ discrepancy in au- tism: evidence for loci on chromosomes 10 and 16. Hum Genet 129:59–70

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen S, Lewis B, Moran A, Xie T (2012) Cadherin-mediated cell adhesion is critical for the closing of the mouse optic fissure. PloS One 7:1–8. doi:10.1371/journal.pone.0051705

    CAS  Google Scholar 

  • Chenn A, Walsh C (2003) Increased neuronal production, enlarged forebrains and cytoarchitectural distortions in beta-catenin overexpressing transgenic mice. Cereb Cortex 13:599–606. doi:10.1093/cercor/13.6.599

    Article  PubMed  Google Scholar 

  • Chenn A, Zhang YA, Chang BT, McConnell SK (1998) Intrinsic polarity of mammalian neuroepithelial cells. Mol Cell Neurosci 11:183–193. doi:10.1006/mcne.1998.0680

    Article  CAS  PubMed  Google Scholar 

  • Chow RL, Lang RA (2001) Early eye development in vertebrates. Annu Rev Cell Dev Biol 17:255–296

    Article  CAS  PubMed  Google Scholar 

  • Chu TT, Liu Y (2010) An integrated genomic analysis of gene function correlation on schizophrenia susceptibility genes. J Hum Genet 55:285–292

    Article  CAS  PubMed  Google Scholar 

  • Ciruna B, Rossant J (2001) FGF signalling regulates mesoderm cell Fate specification and morphogenetic movement at the primitive streak. Dev Cell 1:37–49. doi:10.1016/S1534-5807(01)00017-X

    Article  CAS  PubMed  Google Scholar 

  • Clay MR, Halloran MC (2014) Cadherin 6 promotes neural crest cell detachment via F-actin regulation and influences active Rho distribution during epithelial-to-mesenchymal transition. Development 141:2506–2515. doi:10.1242/dev.105551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coles EG, Taneyhill LA, Bronner-Fraser M (2007) A critical role for Cadherin6B in regulating avian neural crest emigration. Dev Biol 312:533–544. doi:10.1016/j.ydbio.2007.09.056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costa MR, Wen G, Lepier A et al (2008) Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development 135:11–22. doi:10.1242/dev.009951

    Article  CAS  PubMed  Google Scholar 

  • Crepel A, De Wolf V, Brison N et al (2014) Association of CDH11 with non-syndromic ASD. Am J Med Genet B Neuropsychiatr Genet 165:391–398

    Article  CAS  Google Scholar 

  • Dady A, Blavet C, Duband JL (2012) Timing and kinetics of E- to N-cadherin switch during neurulation in the avian embryo. Dev Dyn 241:1333–1349. doi:10.1002/dvdy.23813

    Article  CAS  PubMed  Google Scholar 

  • Das RM, Storey KG (2014) Apical abscission alters cell polarity and dismantles the primary cilium during neurogenesis. Science 343:200–204. doi:10.1126/science.1247521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Anda FC, Pollarolo G, Da Silva JS et al (2005) Centrosome localization determines neuronal polarity. Nature 436:704–708

    Article  PubMed  CAS  Google Scholar 

  • de Anda F, Gartner A, Tsai LH, Dotti CG (2008) Pyramidal neuron polarity axis is defined at the bipolar stage. J Cell Sci 121:178–185

    Article  CAS  Google Scholar 

  • de Anda FC, Meletis K, Ge X et al (2010) Centrosome motility is essential for initial axon formation in the neocortex. J Neurosci 30:10391–10406

    Article  PubMed  CAS  Google Scholar 

  • Demireva EY, Shapiro LS, Jessell TM, Zampieri N (2011) Motor neuron position and topographic order imposed by β - and γ-catenin activities. Cell 147:641–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doe CQ (2008) Neural stem cells: balancing self-renewal with differentiation. Development 135:1575–1587. doi:10.1242/dev.014977

    Article  CAS  PubMed  Google Scholar 

  • Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454–1468

    CAS  PubMed  Google Scholar 

  • Duan X, Krishnaswamy A, De la Huerta I, Sanes JR (2014) Type II cadherins guide assembly of a direction-selective retinal circuit. Cell 158:793–807

    Article  CAS  PubMed  Google Scholar 

  • Dunah AW, Hueske E, Wyszynski M (2005) LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat Neurosci 8:458–467

    CAS  PubMed  Google Scholar 

  • Dupin E, Creuzet S, Le Douarin NM (2006) The contribution of the neural crest to the vertebrate body. Adv Exp Med Biol 589:96–119

    Article  CAS  PubMed  Google Scholar 

  • Elia LP, Yamamoto M, Zang K, Reichardt LF (2006) p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron 51:43–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fannon AM, Colman DR (1996) A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 17:423–434

    Article  CAS  PubMed  Google Scholar 

  • Farkas LM, Huttner WB (2008) The cell biology of neural stem and progenitor cells and its significance for their proliferation versus differentiation during mammalian brain development. Curr Opin Cell Biol 20:707–715. doi:10.1016/j.ceb.2008.09.008

    Article  CAS  PubMed  Google Scholar 

  • Gartner A, Fornasiero EF, Dotti CG (2012a) N-cadherin: a new player in neuronal polarity. Cell Cycle 11:2223–2224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gartner A, Fornasiero EF, Munck S et al (2012b) N-cadherin specifies first asymmetry in developing neurons. EMBO J 31:1893–1903

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gärtner A, Fornasiero EF, Dotti CG (2014a) Cadherins as regulators of neuronal polarity. Cell Adh Migr 14:1–8

    Google Scholar 

  • Gärtner A, Fornasiero EF, Valtorta F, Dotti CG (2014b) Distinct temporal hierarchies in membrane and cytoskeleton dynamics precede the morphological polarization of developing neurons. J Cell Sci 127:4409–4419

    Article  PubMed  CAS  Google Scholar 

  • Gilmore EC, Walsh CA (2013) Genetic causes of microcephaly and lessons for neuronal development. Wiley Interdiscp Rev Dev Biol 2:461–478. doi:10.1002/wdev.89

    Article  CAS  Google Scholar 

  • Gleeson JG (2001) Neuronal migration disorders. Ment Retard Dev Disabil Res Rev 7:167–171

    Article  CAS  PubMed  Google Scholar 

  • Götz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777–788. doi:10.1038/nrm1739

    Article  PubMed  CAS  Google Scholar 

  • Gregory W, Edmondson J (1988) Cytology and neuron-glial apposition of migrating cerebellar granule cells in vitro. J Neurosci 8:1728–1738

    CAS  PubMed  Google Scholar 

  • Haase G, Dessaud E, Garcès A (2002) GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools. Neuron 35:893–905

    Article  CAS  PubMed  Google Scholar 

  • Halbleib JM, Nelson WJ (2006) Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20:3199–3214. doi:10.1101/gad.1486806

    Article  CAS  PubMed  Google Scholar 

  • Hall BK (2008) The neural crest and neural crest cells in vertebrate development and evolution. TripleC. doi:10.1007/128

    Google Scholar 

  • Hall R, Erickson C (2003) ADAM 10: an active metalloprotease expressed during avian epithelial morphogenesis. Dev Biol 256:146–159

    Article  CAS  PubMed  Google Scholar 

  • Hatakeyama J, Bessho Y, Katoh K et al (2004) Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131:5539–5550. doi:10.1242/dev.01436

    Article  CAS  PubMed  Google Scholar 

  • Hatakeyama J, Wakamatsu Y, Nagafuchi A et al (2014) Cadherin-based adhesions in the apical endfoot are required for active Notch signaling to control neurogenesis in vertebrates. Development 141:1671–1682. doi:10.1242/dev.102988

    Article  CAS  PubMed  Google Scholar 

  • Hatta K, Takeichi M (1986) Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature 320:447–449. doi:10.1038/320447a0

    Article  CAS  PubMed  Google Scholar 

  • Hazan RB, Qiao R, Keren R et al (2004) Cadherin switch in tumor progression. Ann N Y Acad Sci 1014:155–163. doi:10.1196/annals.1294.016

    Article  CAS  PubMed  Google Scholar 

  • Higginbotham HR, Gleeson JG (2007) The centrosome in neuronal development. Trends Neurosci 30:276–283

    Article  CAS  PubMed  Google Scholar 

  • Hirano S, Takeichi M (2012) Cadherins in brain morphogenesis and wiring. Physiol Rev 92:597–634

    Article  CAS  PubMed  Google Scholar 

  • Hirano M, Hashimoto S, Yonemura S et al (2008) EPB41L5 functions to post-transcriptionally regulate cadherin and integrin during epithelial-mesenchymal transition. J Cell Biol 182:1217–1230. doi:10.1083/jcb.200712086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong E, Brewster R (2006) N-cadherin is required for the polarized cell behaviours that drive neurulation in the zebrafish. Development 133:3895–3905. doi:10.1242/dev.02560

    Article  CAS  PubMed  Google Scholar 

  • Inuzuka H, Redies C, Takeichi M (1991) Differential expression of R- and N-cadherin in neural and mesodermal tissues during early chicken development. Development 113:959–967

    CAS  PubMed  Google Scholar 

  • Johnson C, Drgon T, Liu QR et al (2006) Pooled association genome scanning for alcohol dependence using 104,268 SNPs: validation and use to identify alcoholism vulnerability loci in unrelated individuals from the collaborative study on the genetics of alcoholism. Am J Med Genet B Neuropsychiatr Genet 141:844–853

    Article  Google Scholar 

  • Junghans D, Hack I, Frotscher M et al (2005) Beta-catenin-mediated cell-adhesion is vital for embryonic forebrain development. Dev Dyn 233:528–539. doi:10.1002/dvdy.20365

    Article  CAS  PubMed  Google Scholar 

  • Kadowaki M, Nakamura S, Machon O et al (2007) N-cadherin mediates cortical organization in the mouse brain. Dev Biol 304:22–33

    Article  CAS  PubMed  Google Scholar 

  • Katsamba P, Carroll K, Ahlsen G et al (2009) Linking molecular affinity and cellular specificity in cadherin-mediated adhesion. Proc Natl Acad Sci U S A 106:11594–11599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kay JN, De la Huerta I, Kim IJ (2011) Retinal ganglion cells with distinct directional preferences differ in molecular identity, structure, and central projections. J Neurosci 31:7753–7762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kostetskii I, Moore R, Kemler R, Radice GL (2001) Differential adhesion leads to segregation and exclusion of N-cadherin-deficient cells in chimeric embryos. Dev Biol 234:72–79. doi:10.1006/dbio.2001.0250

    Article  CAS  PubMed  Google Scholar 

  • Lasky-Su J, Neale BM, Franke B et al (2008) Genome-wide association scan of quantitative traits for attention deficit hyperactivity disorder identifies novel associations and confirms candidate gene associations. Am J Med Genet B Neuropsychiatr Genet 147:1345–1354

    Article  CAS  Google Scholar 

  • Lee CH, Gumbiner BM (1995) Disruption of gastrulation movements in Xenopus by a dominant-negative mutant for C-cadherin. Dev Biol 171:363–373. doi:10.1006/dbio.1995.1288

    Article  CAS  PubMed  Google Scholar 

  • Lein W-H, Klezovitch O, Fernandez TE, et al (2006) αE-catenin controls cerebral cortical size by regulating hedgehog signalling pathway. 311:1609–1612. doi:10.1126/science.1121449.

    Google Scholar 

  • Lepage SE, Bruce AEE (2010) Zebrafish epiboly: mechanics and mechanisms. Int J Dev Biol 54:1213–1228. doi:10.1387/ijdb.093028sl

    Article  CAS  PubMed  Google Scholar 

  • Lesch KP, Timmesfeld N, Renner TJ et al (2008) Molecular genetics of adult ADHD: converging evidence from genome-wide association and extended pedigree linkage studies. J Neural Transm 115:1573–1585

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Marrs JA, Azodi E et al (2004) Differential expression of cadherins in the developing and adult zebrafish olfactory system. J Comp Neurol 478:269–281

    Article  CAS  PubMed  Google Scholar 

  • Livet J, Sigrist M, Stroebel S et al (2002) ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron 35:877–892

    Article  CAS  PubMed  Google Scholar 

  • Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605–623

    Article  CAS  PubMed  Google Scholar 

  • Malinverno M, Carta M, Epis R et al (2010) Synaptic localization and activity of ADAM10 regulate excit- atory synapses through N-cadherin cleavage. J Neurosci 30:16343–16355

    Article  CAS  PubMed  Google Scholar 

  • Marambaud P, Wen PH, Dutt A et al (2003) A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 114:635–645

    Article  CAS  PubMed  Google Scholar 

  • Marín O, Valiente M, Ge X, Tsai L-H (2010) Guiding neuronal cell migrations. Cold Spring Harb Perspect Biol 2:1–21. doi:10.1101/cshperspect.a001834

    Article  CAS  Google Scholar 

  • Marrs GS, Theisen CS, Bruses JL (2009) N-cadherin modulates voltage activated calcium influx via RhoA, p120-catenin, and myosin-actin interaction. Mol Cell Neurosci 40:390–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin-Belmonte F, Perez-Moreno M (2011) Epithelial cell polarity, stem cells and cancer. Nat Rev Cancer 12:23–38. doi:10.1038/nrc3169

    PubMed  Google Scholar 

  • Masai I, Lele Z, Yamaguchi M (2003) N-cadherin mediates retinal lamination, maintenance of forebrain compartments and patterning of retinal neurites. Development 130:2479–2494

    Article  PubMed  CAS  Google Scholar 

  • Matsunaga M, Hatta K, Nagafuchi A, Takeichi M (1988a) Guidance of optic nerve fibres by N-cadherin adhesion molecules. Nature 334:62–64

    Article  CAS  PubMed  Google Scholar 

  • Matsunaga M, Hatta K, Takeichi M (1988b) Role of N-cadherin cell adhesion molecules in the histogenesis of neural retina. Neuron 1:289–295. doi:10.1016/0896-6273(88)90077-3

    Article  CAS  PubMed  Google Scholar 

  • Matsunaga E, Nambu S, Oka M, Iriki A (2013) Differential cadherin expression in the developing postnatal telencephalon of a New World monkey. J Comp Neurol 521:4027–4060

    CAS  PubMed  Google Scholar 

  • Mayor R, Theveneau E (2013) The neural crest. Development 140:2247–2251. doi:10.1242/dev.091751

    Article  CAS  PubMed  Google Scholar 

  • Medina M, Marinescu RC, Overhauser J, Kosik KS (2000) Hemizygosity of delta-catenin (CTNND2) is associated with severe mental retardation in cri-du-chat syndrome. Genomics 63:157–164

    Article  CAS  PubMed  Google Scholar 

  • Monea S, Jordan BA, Srivastava S et al (2006) Membrane localization of membrane type 5 matrix metalloproteinase by AMPA receptor binding protein and cleavage of cadherins. J Neurosci 26:2300–2312

    Article  CAS  PubMed  Google Scholar 

  • Mysore SP, Tai CY, Schuman EM (2007) Effects of N-cadherin disruption on spine morphological dynamics. Front Cell Neurosci 1:1. doi:10.3389/neuro.03.001.2007

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakagawa S, Takeichi M (1995) Neural crest cell-cell adhesion controlled by sequential and subpopulation-specific expression of novel cadherins. Development 121:1321–1332. doi:10.1016/0168-9525(95)90550-2

    CAS  PubMed  Google Scholar 

  • Nakaya Y, Sheng G (2008) Epithelial to mesenchymal transition during gastrulation: an embryological view. Dev Growth Differ 50:755–766. doi:10.1111/j.1440-169X.2008.01070.x

    Article  CAS  PubMed  Google Scholar 

  • Nelson J, Nusse R (2004) Convergence of Wnt, β-Catenin, and Cadherin pathways. Science (80–) 303:1483–1487. doi:10.1126/science.1094291

    Google Scholar 

  • Nishimura T, Takeichi M (2009) Remodeling of the Adherens Junctions During Morphogenesis. In: Lecuit T (ed) Tissue remodeling and epithelial morphogenesis, 1st edn. Elsevier, San Diego, pp 33–49

    Google Scholar 

  • Noles SR, Chenn A (2007) Cadherin inhibition of β -catenin signaling regulates the proliferation and differentiation of neural precursor cells. Mol Cell Neurosci 35:549–558. doi:10.1016/j.mcn.2007.04.012

    Google Scholar 

  • Nuriya M, Huganir RL (2006) Regulation of AMPA receptor trafficking by N-cadherin. J Neurochem 97:652–661

    Article  CAS  PubMed  Google Scholar 

  • Oblander SA, Brady-Kalnay SM (2010) Distinct PTPmu-associated signaling molecules dif- ferentially regulate neurite outgrowth on E-, N-, and R-cadherin. Mol Cell Neurosci 44:78–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oblander SA, Ensslen-Craig SE, Longo FM, Brady-Kalnay SM (2007) E-cadherin promotes retinal ganglion cell neurite outgrowth in a protein tyrosine phosphatase mu dependent manner. Mol Cell Neurosci 34:481–492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ozair MZ, Kintner C, Brivanlou AH (2013) Neural induction and early patterning in vertebrates. Wiley Interdiscip Rev Dev Biol 2:479–498. doi:10.1002/wdev.90

    Article  CAS  PubMed  Google Scholar 

  • Paradis S, Harrar DB, Lin Y et al (2007) An RNAi-based approach identifies molecules required for gluta- matergic and GABAergic synapse development. Neuron 53:217–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park K-S, Gumbiner BM (2010) Cadherin 6B induces BMP signaling and de-epithelialization during the epithelial mesenchymal transition of the neural crest. Development 137:2691–2701. doi:10.1242/dev.050096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park K-S, Gumbiner BM (2012) Cadherin-6B stimulates an epithelial mesenchymal transition and the delamination of cells from the neural ectoderm via LIMK/ cofilin mediated non-canonical BMP receptor signaling. Dev Biol 366:232–243. doi:10.1016/j.biotechadv.2011.08.021.Secreted

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perego C, Vanoni C, Massari S et al (2002) Invasive behaviour of glioblastoma cell lines is associated with altered organisation of the cadherin-catenin adhesion system. J Cell Sci 115:3331–3340

    CAS  PubMed  Google Scholar 

  • Pollarolo G, Schulz JG, Munck S, Dotti CG (2011) Cytokinesis remnants define first neuronal asymmetry in vivo. Nat Neurosci 14:1525–1533

    Article  CAS  PubMed  Google Scholar 

  • Powell SK, Rivas RJ, Rodriguez-Boulan E, Hatten ME (1997) Development of polarity in cerebellar granule neurons. J Neurobiol 32:223–236

    Article  CAS  PubMed  Google Scholar 

  • Price SR, De Marco GNV, Ranscht B, Jessell TM (2002) Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109:205–16

    Article  CAS  PubMed  Google Scholar 

  • Radice GL, Rayburn H, Matsunami H et al (1997) Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181:64–78. doi:10.1006/dbio.1996.8443

    Article  CAS  PubMed  Google Scholar 

  • Rakic P (2003) Developmental and evolutionary adaptations of cortical radial glia. Cereb Cortex 13:541–549. doi:10.1093/cercor/13.6.541

    Article  PubMed  Google Scholar 

  • Rasin M-R, Gazula V-R, Breunig JJ et al (2007) Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat Neurosci 10:819–827. doi:10.1038/nn1924

    Article  CAS  PubMed  Google Scholar 

  • Redies C, Takeichi M (1993) N-and R-cadherin expression in the optic nerve of the chicken embryo. Glia 8:161–171

    Article  CAS  PubMed  Google Scholar 

  • Redies C, Engelhart K, Takeichi M (1993) Differential expression of N- and R-cadherin in functional neuronal systems and other structures of the developing chicken brain. J Comp Neurol 333:398–416

    Article  CAS  PubMed  Google Scholar 

  • Reiss K, Maretzky T, Ludwig A et al (2005) ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and beta-catenin nuclear signalling. EMBO J 24:742–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riehl R, Johnson K, Bradley R et al (1996) Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17:837–848

    Article  CAS  PubMed  Google Scholar 

  • Rose O, Grund C, Reinhardt S et al (1995) Contactus adherens, a special type of plaque-bearing adhering junction containing M-cadherin, in the granule cell layer of the cerebellar glomerulus. Proc Natl Acad Sci U S A 92:6022–6026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rousso DL, Pearson CA, Gaber ZB et al (2013) Foxp-mediated suppression of N-cadherin regulates neuroepithelial character and progenitor maintenance in the CNS. Neuron 74:314–330. doi:10.1038/nature11130.Reduced

    Article  CAS  Google Scholar 

  • Rungger-Brändle E, Ripperger JA, Steiner K et al (2010) Retinal patterning by Pax6-dependent cell adhesion molecules. Dev Neurobiol 70:764–780. doi:10.1002/dneu.20816

    Article  PubMed  CAS  Google Scholar 

  • Saglietti L, Dequidt C, Kamieniarz K et al (2007) Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron 54:461–477

    Article  CAS  PubMed  Google Scholar 

  • Schiffmacher AT, Padmanabhan R, Jhingory S, Taneyhill LA (2014) Cadherin-6B is proteolytically processed during epithelial-to-mesenchymal transitions of the cranial neural crest. Mol Biol Cell 25:41–54. doi:10.1091/mbc.E13-08-0459

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmid RS, McGrath B, Berechid BE et al (2003) Neuregulin 1-erbB2 signaling is required for the establishment of radial glia and their transformation into astrocytes in cerebral cortex. Proc Natl Acad Sci U S A 100:4251–4256. doi:10.1073/pnas.0630496100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheng L, Leshchyns’ka I, Sytnyk V (2013) Cell adhesion and intracellular calcium signaling in neurons. Cell Commun Signal 11:94. doi:10.1186/1478-811X-11-94

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shikanai M, Nakajima K, Kawauchi T (2011) N-Cadherin regulates radial glial fiber-dependent migration of cortical locomoting neurons. Commun Integr Biol 4:326–330. doi:10.4161/cib.4.3.14886

    Article  PubMed  PubMed Central  Google Scholar 

  • Shimizu T, Yabe T, Muraoka O et al (2005) E-cadherin is required for gastrulation cell movements in zebrafish. Mech Dev 122:747–763. doi:10.1016/j.mod.2005.03.008

    Article  CAS  PubMed  Google Scholar 

  • Shimoyama Y, Tsujimoto G, Kitajima M, Natori M (2000) Identification of three human type-II classic cadherins and frequent heterophilic interactions between different subclasses of type-II classic cadherins. Biochem J 349:159–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shoval I, Ludwig A, Kalcheim C (2007) Antagonistic roles of full-length N-cadherin and its soluble BMP cleavage product in neural crest delamination. Development 134:491–501. doi:10.1242/dev.02742

    Article  CAS  PubMed  Google Scholar 

  • Singh SM, Castellani C, O’Reilly R (2010) Autism meets schizophrenia via cadherin pathway. Schizophr Res 116:293–294

    Article  PubMed  Google Scholar 

  • Solecki DJ, Model L, Gaetz J (2004) Par6alpha signaling controls glial-guided neuronal migration. Nat Neurosci 7:1195–1203

    Article  CAS  PubMed  Google Scholar 

  • Solnica-Krezel L, Sepich DS (2012) Gastrulation: making and shaping germ layers. Annu Rev Cell Dev Biol 28:687–717

    Article  CAS  PubMed  Google Scholar 

  • Suzuki SC, Takeichi M (2008) Cadherins in neuronal morphogenesis and function. Dev Growth Differ 1:S119–S130

    Article  CAS  Google Scholar 

  • Swartling FJ, Savov V, Persson AI et al (2012) Distinct neural stem cell populations give rise to disparate brain tumors in response to N-MYC. Cancer Cell 21:601–613. doi:10.1016/j.ccr.2012.04.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tai CY, Mysore SP, Chiu C, Schuman EM (2007) Activity-regulated N-cadherin endocytosis. Neuron 54:771–785

    Article  CAS  PubMed  Google Scholar 

  • Tai CY, Kim SA, Schuman EM (2008) Cadherins and synaptic plasticity. Curr Opin Cell Biol 20:567–575

    Article  CAS  PubMed  Google Scholar 

  • Takahashi T, Nowakowski RS, Caviness VS (1993) Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci 13:820–833

    CAS  PubMed  Google Scholar 

  • Takeichi M (2007) The cadherin superfamily in neuronal connections and interactions. Nat Rev Neurosci 8:11–20

    Article  CAS  PubMed  Google Scholar 

  • Takeichi M, Inuzuka H, Shimamura K et al (1990) Cadherin subclasses: differential expression and their roles in neural morphogenesis. Cold Spring Harb Symp Quant Biol 55:319–325

    Article  CAS  PubMed  Google Scholar 

  • Tanabe K, Takahashi Y, Sato Y et al (2006) Cadherin is required for dendritic morphogenesis and synaptic terminal organization of retinal horizontal cells. Development 133:4085–4096

    Article  CAS  PubMed  Google Scholar 

  • Tanaka T, Serneo FF, Higgins C et al (2004) Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 165:709–721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taneyhill LA, Schiffmacher AT (2013) Chapter 3: The Cell Biology of Neural Crest Cell Delamination and EMT. In: Trainor P (ed) Neural Crest Cells: Evolution, Development and Disease. Elsevier Inc, Taramani, pp 1–22

    Google Scholar 

  • Taneyhill LA, Coles EG, Bronner-Fraser M (2007) Snail2 directly represses cadherin6B during epithelial-to-mesenchymal transitions of the neural crest. Development 134:1481–1490. doi:10.1242/dev.02834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Temple S (2001) The development of neural stem cells. Nature 414:112–117. doi:10.1038/35102174

    Article  CAS  PubMed  Google Scholar 

  • Teng J, Rai T, Tanaka Y et al (2005) The KIF3 motor transports N-cadherin and organizes the developing neuroepithelium. Nat Cell Biol 7:474–482. doi:10.1038/ncb1249

    Article  CAS  PubMed  Google Scholar 

  • Tepass U, Truong K, Godt D et al (2000) Cadherins in embryonic and neural morphogenesis. Nat Rev Mol Cell Biol 1:91–100. doi:10.1038/35040042

    Article  CAS  PubMed  Google Scholar 

  • Thalhammer A, Cingolani LA (2014) Cell adhesion and homeostatic synaptic plasticity. Neuropharmacology 78:23–30

    Article  CAS  PubMed  Google Scholar 

  • Theveneau E, Mayor R (2012) Neural crest delamination and migration: from epithelium-to-mesenchyme transition to collective cell migration. Dev Biol 366:34–54. doi:10.1016/j.ydbio.2011.12.041

    Article  CAS  PubMed  Google Scholar 

  • Thiery JP, Acloque H, Huang RYJ, Nieto MA (2009) Epithelial-Mesenchymal Transitions in Development and Disease. Cell 139:871–890. doi:10.1016/j.cell.2009.11.007

    Article  CAS  PubMed  Google Scholar 

  • Togashi H, Abe K, Mizoguchi A et al (2002) Cadherin regulates dendritic spine morphogenesis. Neuron 35:77–89

    Article  CAS  PubMed  Google Scholar 

  • Tomaselli KJ, Neugebauer KM, Bixby JL et al (1988) N-cadherin and integrins: two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron 1:33–43

    Article  CAS  PubMed  Google Scholar 

  • Treutlein J, Cichon S, Ridinger M et al (2009) Genome-wide association study of alcohol dependence. Arch Gen Psychiatry 66:773–784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuchiya B, Sato Y, Kameya T et al (2006) Differential expression of N-cadherin and E-cadherin in normal human tissues. Arch Histol Cytol 69:135–145

    Article  CAS  PubMed  Google Scholar 

  • Uchida N, Honjo Y, Johnson KR et al (1996) The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J Cell Biol 135:767–779

    Article  CAS  PubMed  Google Scholar 

  • Uemura K, Kihara T, Kuzuya A et al (2006) Characterization of sequential N-cadherin cleavage by ADAM10 and PS1. Neurosci Lett 402:278–283

    Article  CAS  PubMed  Google Scholar 

  • Vallin J, Girault JM, Thiery JP, Broders F (1998) Xenopus cadherin-11 is expressed in different populations of migrating neural crest cells. Mech Dev 75:171–174. doi:10.1016/S0925-4773(98)00099-9

    Article  CAS  PubMed  Google Scholar 

  • Wang K, Zhang H, Ma D et al (2009) Common genetic variants on 5p14.1 associate with autism spectrum dis- orders. Nature 459:528–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhadanov AB, Provance DW, Speer CA et al (1999) Absence of the tight junctional protein AF-6 disrupts epithelial cell-cell junctions and cell polarity during mouse development. Curr Biol 9:880–888. doi:10.1016/S0960-9822(99)80392-3

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Woodhead GJ, Swaminathan SK et al (2010) Cortical neural precursors inhibit their own differentiation via N- cadherin maintenance of beta-catenin signaling. Dev Cell 18:472–479. doi:10.1016/j.devcel.2009.12.025.Cortical

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Shemezis JR, Mcquinn ER et al (2013) AKT activation by N-cadherin regulates beta-catenin signaling and neuronal differentiation during cortical development. Neural Dev 8:1. doi:10.1186/1749-8104-8-7

    Article  CAS  Google Scholar 

  • Zhong Y, Brieher WM, Gumbiner BM (1999) Analysis of C-cadherin regulation during tissue morphogenesis with an activating antibody. J Cell Biol 144:351–359. doi:10.1083/jcb.144.2.351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu X, Zhang J, Tollkuhn J et al (2006) Sustained Notch signaling in progenitors is required for sequential emergence of distinct cell lineages during organogenesis. Genes Dev 20:2739–2753. doi:10.1101/gad.1444706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zmuda JF, Rivas RJ (1998) The Golgi apparatus and the centrosome are localized to the sites of newly emerging axons in cerebellar granule neurons in vitro. Cell Motil Cytoskel 41:18–38

    Article  CAS  Google Scholar 

  • Zohn IE, Li Y, Skolnik EY et al (2006) p38 and a p38-Interacting Protein Are Critical for Downregulation of E-Cadherin during Mouse Gastrulation. Cell 125:957–969. doi:10.1016/j.cell.2006.03.048

    Article  CAS  PubMed  Google Scholar 

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Brayshaw, L.L., Price, S.R. (2016). Cadherins in Neural Development. In: Suzuki, S., Hirano, S. (eds) The Cadherin Superfamily. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56033-3_12

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