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Protocadherins branch out: Multiple roles in dendrite development

, &
Pages 214-226 | Received 30 Oct 2014, Accepted 10 Dec 2014, Published online: 14 Apr 2015

References

  • Vaughn JE, Barber RP, Sims TJ. Dendritic development and preferential growth into synaptogenic fields: A quantitative study of Golgi-impregnated spinal motor neurons. Synapse 1988; 2:69-78; PMID:2458630; http://dx.doi.org/10.1002/syn.890020110
  • Vaughn J, Anonymous. Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 1989; 3:255; PMID:2655146; http://dx.doi.org/10.1002/syn.890030312
  • Cline H, Haas K. The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: a review of the synaptotrophic hypothesis. J Physiol 2008; 586:1509; PMID:18202093; http://dx.doi.org/10.1113/jphysiol.2007.150029
  • Jan YN, Jan LY. Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci 2010; 11:316; PMID:20404840; http://dx.doi.org/10.1038/nrn2836
  • Dierssen M, Ramakers GJ. Dendritic pathology in mental retardation: from molecular genetics to neurobiology. Genes, Brain, and Behav 2006; 5 Suppl 2):48; PMID:16681800; http://dx.doi.org/10.1111/j.1601-183X.2006.00224.x
  • Kishi N, Macklis JD. MeCP2 functions largely cell-autonomously, but also non-cell-autonomously, in neuronal maturation and dendritic arborization of cortical pyramidal neurons. Exp Neurol 2010; 222:51; PMID:20025874; http://dx.doi.org/10.1016/j.expneurol.2009.12.007
  • Kwon CH, Luikart BW, Powell CM, Zhou J, Matheny SA, Zhang W, Li Y, Baker SJ, Parada LF. Pten regulates neuronal arborization and social interaction in mice. Neuron 2006; 50:377; PMID:16675393; http://dx.doi.org/10.1016/j.neuron.2006.03.023
  • Hutsler JJ, Zhang H. Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res 2010; 1309:83; PMID:19896929; http://dx.doi.org/10.1016/j.brainres.2009.09.120
  • Redies C, Hertel N, Hubner CA. Cadherins and neuropsychiatric disorders. Brain Res 2012; 1470:130-44; PMID:22765916; http://dx.doi.org/10.1016/j.brainres.2012.06.020
  • Singh SK, Eroglu C. Neuroligins provide molecular links between syndromic and nonsyndromic autism. Sci Signal 2013; 6:re4.
  • Penagarikano O, Geschwind DH. What does CNTNAP2 reveal about autism spectrum disorder? Trends Mol Med 2012; 18:156-63; PMID:22365836; http://dx.doi.org/10.1016/j.molmed.2012.01.003
  • Kim S-Y, Yasuda S, Tanaka H, Yamagata K, Kim H. Non-clustered protocadherin. Cell Adhesion & Migration 2011; 5:97-105; PMID:21173574; http://dx.doi.org/10.4161/cam.5.2.14374
  • Yagi T. Molecular codes for neuronal individuality and cell assembly in the brain. Front Mole Neurosci 2012; 5:45; PMID:22518100; http://dx.doi.org/10.3389/fnmol.2012.00045
  • Weiner JA, Jontes JD. Protocadherins, not prototypical: a complex tale of their interactions, expression, and functions. Front Mole Neurosci 2013; 6:4; PMID:23515683
  • Kahr I, Vandepoele K, van Roy F. Delta-protocadherins in health and disease. Elsevier, 2013:169-92.
  • Sharma P, McNeill H. Fat and dachsous cadherins. Prog Mol Biol Transl Sci 2013; 116:215-35; PMID:23481197; http://dx.doi.org/10.1016/B978-0-12-394311-8.00010-8
  • Feng J, Han Q, Zhou L. Planar cell polarity genes, Celsr1-3, in neural development. Neurosci Bull 2012; 28:309-15; PMID:22622831; http://dx.doi.org/10.1007/s12264-012-1232-8
  • Berger-Muller S, Suzuki T. Seven-pass transmembrane cadherins: roles and emerging mechanisms in axonal and dendritic patterning. Mol Neurobiol 2011; 44:313-20; PMID:21909747; http://dx.doi.org/10.1007/s12035-011-8201-5
  • Nollet F, Kools P, van Roy F. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 2000; 299:551-72; PMID:10835267; http://dx.doi.org/10.1006/jmbi.2000.3777
  • Morishita H, Yagi T. Protocadherin family: diversity, structure, and function. Curr Opin Cell Biol 2007; 19:584; PMID:17936607; http://dx.doi.org/10.1016/j.ceb.2007.09.006
  • Hulpiau P, van Roy F. Molecular evolution of the cadherin superfamily. Int J Biochem Cell Biol 2009; 41:349-69; PMID:18848899; http://dx.doi.org/10.1016/j.biocel.2008.09.027
  • Takeichi M. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development (Cambridge, England) 1988; 102:639; PMID:3048970
  • Gumbiner BM. Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mole Cell Biol 2005; 6:622; PMID:16025097; http://dx.doi.org/10.1038/nrm1699
  • Halbleib JM, Nelson WJ. Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 2006; 20:3199; PMID:17158740; http://dx.doi.org/10.1101/gad.1486806
  • Leckband D, Prakasam A. Mechanism and dynamics of cadherin adhesion. Ann Rev Biomed Eng 2006; 8:259; PMID:16834557; http://dx.doi.org/10.1146/annurev.bioeng.8.061505.095753
  • Sano K, Tanihara H, Heimark RL, Obata S, Davidson M, St John T, Taketani S, Suzuki S. Protocadherins: a large family of cadherin-related molecules in central nervous system. Embo J 1993; 12:2249-56; PMID:8508762
  • Obata S, Sago H, Mori N, Rochelle JM, Seldin MF, Davidson M, St John T, Taketani S, Suzuki ST. Protocadherin Pcdh2 shows properties similar to, but distinct from, those of classical cadherins. J Cell Sci 1995; 108 (Pt 12):3765-73; PMID:8719883
  • Sago H, Kitagawa M, Obata S, Mori N, Taketani S, Rochelle JM, Seldin MF, Davidson M, St John T, Suzuki ST. Cloning, expression, and chromosomal localization of a novel cadherin-related protein, protocadherin-3. Genomics 1995; 29:631-40; PMID:8575755; http://dx.doi.org/10.1006/geno.1995.9956
  • Suzuki ST. Protocadherins and diversity of the cadherin superfamily. J Cell Sci 1996; 109 (Pt 11):2609-11; PMID:8937978
  • Wu Q, Maniatis T. A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 1999; 97:779-90; PMID:10380929; http://dx.doi.org/10.1016/S0092-8674(00)80789-8
  • Wu Q, Zhang T, Cheng JF, Kim Y, Grimwood J, Schmutz J, Dickson M, Noonan JP, Zhang MQ, Myers RM, et al. Comparative DNA sequence analysis of mouse and human protocadherin gene clusters. Genome Res 2001; 11:389-404; PMID:11230163; http://dx.doi.org/10.1101/gr.167301
  • Wu Q. Comparative Genomics and Diversifying Selection of the Clustered Vertebrate Protocadherin Genes. Genetics 2005; 169(4):2179-88; PMID: 15744052
  • Tada MN, Senzaki K, Tai Y, Morishita H, Tanaka YZ, Murata Y, Ishii Y, Asakawa S, Shimizu N, Sugino H, et al. Genomic organization and transcripts of the zebrafish Protocadherin genes. Gene 2004; 340:197-211; PMID:15475161; http://dx.doi.org/10.1016/j.gene.2004.07.014
  • Sugino H, Hamada S, Yasuda R, Tuji A, Matsuda Y, Fujita M, Yagi T. Genomic organization of the family of CNR cadherin genes in mice and humans. Genomics 2000; 63:75-87; PMID:10662547; http://dx.doi.org/10.1006/geno.1999.6066
  • Ribich S, Tasic B, Maniatis T. Identification of long-range regulatory elements in the protocadherin-alpha gene cluster. Proc Natl Acad Sci U S A 2006; 103:19719; PMID:17172445; http://dx.doi.org/10.1073/pnas.0609445104
  • Kehayova P, Monahan K, Chen W, Maniatis T. Regulatory elements required for the activation and repression of the protocadherin-alpha gene cluster. Proc Natl Acad Sci 2011; 108(41):17195-200; PMID: 21949399
  • Yokota S, Hirayama T, Hirano K, Kaneko R, Toyoda S, Kawamura Y, Hirabayashi M, Hirabayashi T, Yagi T. Identification of the Cluster Control Region for the Protocadherin-b Genes Located beyond the Protocadherin-g Cluster. J Biol Chem 2011; 286:31885-95; PMID:21771796; http://dx.doi.org/10.1074/jbc.M111.245605
  • Tasic B, Nabholz CE, Baldwin KK, Kim Y, Rueckert EH, Ribich SA, Cramer P, Wu Q, Axel R, Maniatis T. Promoter choice determines splice site selection in protocadherin alpha and gamma pre-mRNA splicing. Mol Cell 2002; 10:21-33; PMID:12150904; http://dx.doi.org/10.1016/S1097-2765(02)00578-6
  • Wang X, Su H, Bradley A. Molecular mechanisms governing Pcdh-gamma gene expression: evidence for a multiple promoter and cis-alternative splicing model. Genes Dev 2002; 16:1890-905; PMID:12154121; http://dx.doi.org/10.1101/gad.1004802
  • Esumi S, Kakazu N, Taguchi Y, Hirayama T, Sasaki A, Hirabayashi T, Koide T, Kitsukawa T, Hamada S, Yagi T. Monoallelic yet combinatorial expression of variable exons of the protocadherin-alpha gene cluster in single neurons. Nat Genet 2005; 37:171-6; PMID:15640798; http://dx.doi.org/10.1038/ng1500
  • Kaneko R, Kato H, Kawamura Y, Esumi S, Hirayama T, Hirabayashi T, Yagi T. Allelic gene regulation of Pcdh-alpha and Pcdh-gamma clusters involving both monoallelic and biallelic expression in single Purkinje cells. J Biol Chem 2006; 281:30551-60; PMID:16893882; http://dx.doi.org/10.1074/jbc.M605677200
  • Noguchi Y, Hirabayashi T, Katori S, Kawamura Y, Sanbo M, Hirabayashi M, Kiyonari H, Nakao K, Uchimura A, Yagi T. Total expression and dual gene-regulatory mechanisms maintained in deletions and duplications of the Pcdha cluster. J Biol Chem 2009; 284:32002-14; PMID:19797050; http://dx.doi.org/10.1074/jbc.M109.046938
  • Hirano K, Kaneko R, Izawa T, Kawaguchi M, Kitsukawa T, Yagi T. Single-neuron diversity generated by Protocadherin-b cluster in mouse central and peripheral nervous systems. Front Mole Neurosci 2012; 5:90; PMID:22969705
  • Schreiner D, Weiner JA. Combinatorial homophilic interaction between gamma-protocadherin multimers greatly expands the molecular diversity of cell adhesion. Proc Natl Acad Sci U S A 2010; 107:14893; PMID:20679223; http://dx.doi.org/10.1073/pnas.1004526107
  • Zipursky SL, Sanes JR. Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 2010; 143:343; PMID:21029858; http://dx.doi.org/10.1016/j.cell.2010.10.009
  • Murata Y, Hamada S, Morishita H, Mutoh T, Yagi T. Interaction with protocadherin-gamma regulates the cell surface expression of protocadherin-alpha. J Biol Chem 2004; 279:49508-16; PMID:15347688; http://dx.doi.org/10.1074/jbc.M408771200
  • Han MH, Lin C, Meng S, Wang X. Proteomics analysis reveals overlapping functions of clustered protocadherins. Mole Cell Proteomics 2010; 9:71; http://dx.doi.org/10.1074/mcp.M900343-MCP200
  • Thu CA, Chen WV, Rubinstein R, Chevee M, Wolcott HN, Felsovalyi KO, Tapia JC, Shapiro L, Honig B, Maniatis T. Single-cell identity generated by combinatorial homophilic interactions between alpha, beta, and gamma protocadherins. Cell 2014; 158:1045-59; PMID:25171406; http://dx.doi.org/10.1016/j.cell.2014.07.012
  • Kohmura N, Senzaki K, Hamada S, Kai N, Yasuda R, Watanabe M, Ishii H, Yasuda M, Mishina M, Yagi T. Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron 1998; 20:1137-51; PMID:9655502; http://dx.doi.org/10.1016/S0896-6273(00)80495-X
  • Blank M, Triana-Baltzer GB, Richards CS, Berg DK. Alpha-protocadherins are presynaptic and axonal in nicotinic pathways. Mol Cell Neurosci 2004; 26:530-43; PMID:15276155; http://dx.doi.org/10.1016/j.mcn.2004.04.008
  • Morishita H, Murata Y, Esumi S, Hamada S, Yagi T. CNR/Pcdhalpha family in subplate neurons, and developing cortical connectivity. Neuroreport 2004; 15:2595-9; PMID:15570159; http://dx.doi.org/10.1097/00001756-200412030-00007
  • Morishita H, Kawaguchi M, Murata Y, Seiwa C, Hamada S, Asou H, Yagi T. Myelination triggers local loss of axonal CNR/protocadherin alpha family protein expression. Eur J Neurosci 2004; 20:2843-7; PMID:15579137; http://dx.doi.org/10.1111/j.1460-9568.2004.03803.x
  • Wang X, Weiner JA, Levi S, Craig AM, Bradley A, Sanes JR. Gamma protocadherins are required for survival of spinal interneurons. Neuron 2002; 36:843-54; PMID:12467588; http://dx.doi.org/10.1016/S0896-6273(02)01090-5
  • Phillips GR, Huang JK, Wang Y, Tanaka H, Shapiro L, Zhang W, Shan WS, Arndt K, Frank M, Gordon RE, et al. The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron 2001; 32:63-77; PMID:11604139; http://dx.doi.org/10.1016/S0896-6273(01)00450-0
  • Phillips GR, Tanaka H, Frank M, Elste A, Fidler L, Benson DL, Colman DR. Gamma-protocadherins are targeted to subsets of synapses and intracellular organelles in neurons. J Neurosci 2003; 23:5096-104; PMID:12832533
  • Li Y, Serwanski DR, Miralles CP, Fiondella CG, Loturco JJ, Rubio ME, De Blas AL. Synaptic and nonsynaptic localization of protocadherin-gammaC5 in the rat brain. J Comp Neurol 2010; 518:3439-63; PMID:20589908; http://dx.doi.org/10.1002/cne.22390
  • Garrett AM, Weiner JA. Control of CNS synapse development by gamma-protocadherin-mediated astrocyte-neuron contact. J Neurosci 2009; 29:11723; PMID:19776259; http://dx.doi.org/10.1523/JNEUROSCI.2818-09.2009
  • Lefebvre JL, Zhang Y, Meister M, Wang X, Sanes JR. gamma-Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina. Development 2008; 135:4141-51; PMID:19029044; http://dx.doi.org/10.1242/dev.027912
  • Kallenbach S, Khantane S, Carroll P, Gayet O, Alonso S, Henderson CE, Dudley K. Changes in subcellular distribution of protocadherin gamma proteins accompany maturation of spinal neurons. J Neurosci Res 2003; 72:549-56; PMID:12749019; http://dx.doi.org/10.1002/jnr.10618
  • Fernandez-Monreal M, Kang S, Phillips GR. Gamma-protocadherin homophilic interaction and intracellular trafficking is controlled by the cytoplasmic domain in neurons. Mole Cell Neurosci 2009; 40:344; PMID:19136062; http://dx.doi.org/10.1016/j.mcn.2008.12.002
  • Fernández-Monreal M, Oung T, Hanson HH, O'Leary R, Janssen WG, Dolios G, Wang R, Phillips GR. g-protocadherins are enriched and transported in specialized vesicles associated with the secretory pathway in neurons. Eur J Neurosci 2010; 32:921-31; http://dx.doi.org/10.1111/j.1460-9568.2010.07386.x
  • Junghans D, Heidenreich M, Hack I, Taylor V, Frotscher M, Kemler R. Postsynaptic and differential localization to neuronal subtypes of protocadherin b16 in the mammalian central nervous system. Euro J Neurosci 2008; 27:559; PMID:18279309; http://dx.doi.org/10.1111/j.1460-9568.2008.06052.x
  • Puller C, Haverkamp S. Cell-type-specific localization of protocadherin b16 at AMPA and AMPA/kainate receptor-containing synapses in the primate retina. J Comp Neurol 2010; 519:467-79; http://dx.doi.org/10.1002/cne.22528
  • Prasad T, Wang X, Gray PA, Weiner JA. A differential developmental pattern of spinal interneuron apoptosis during synaptogenesis: insights from genetic analyses of the protocadherin-gamma gene cluster. Development (Cambridge, England) 2008; 135:4153; PMID:19029045; http://dx.doi.org/10.1242/dev.026807
  • Weiner JA, Wang X, Tapia JC, Sanes JR. Gamma protocadherins are required for synaptic development in the spinal cord. Proc Natl Acad Sci U S A 2005; 102:8-14; PMID:15574493; http://dx.doi.org/10.1073/pnas.0407931101
  • Su H, Marcheva B, Meng S, Liang FA, Kohsaka A, Kobayashi Y, Xu AW, Bass J, Wang X. Gamma-protocadherins regulate the functional integrity of hypothalamic feeding circuitry in mice. Dev Biol 2010; 339:38; PMID:20025866; http://dx.doi.org/10.1016/j.ydbio.2009.12.010
  • Lin YC, Koleske AJ. Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders. Annu Rev Neurosci 2010; 33:349-78; PMID:20367247; http://dx.doi.org/10.1146/annurev-neuro-060909-153204
  • Li Y, Xiao H, Chiou TT, Jin H, Bonhomme B, Miralles CP, Pinal N, Ali R, Chen WV, Maniatis T, et al. Molecular and functional interaction between protocadherin-gammaC5 and GABAA receptors. J Neurosci 2012; 32:11780-97; PMID:22915120; http://dx.doi.org/10.1523/JNEUROSCI.0969-12.2012
  • Garrett AM, Schreiner D, Lobas MA, Weiner JA. gamma-protocadherins control cortical dendrite arborization by regulating the activity of a FAK/PKC/MARCKS signaling pathway. Neuron 2012; 74:269; PMID:22542181; http://dx.doi.org/10.1016/j.neuron.2012.01.028
  • Chen J, Lu Y, Meng S, Han MH, Lin C, Wang X. alpha- and gamma-Protocadherins negatively regulate PYK2. J Biol Chem 2009; 284:2880; PMID:19047047; http://dx.doi.org/10.1074/jbc.M807417200
  • Beggs HE, Schahin-Reed D, Zang K, Goebbels S, Nave KA, Gorski J, Jones KR, Sretavan D, Reichardt LF. FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 2003; 40:501; PMID:14642275; http://dx.doi.org/10.1016/S0896-6273(03)00666-4
  • Rico B, Beggs HE, Schahin-Reed D, Kimes N, Schmidt A, Reichardt LF. Control of axonal branching and synapse formation by focal adhesion kinase. Nat Neurosci 2004; 7:1059; PMID:15378065; http://dx.doi.org/10.1038/nn1317
  • Gundlfinger A, Kapfhammer JP, Kruse F, Leitges M, Metzger F. Different regulation of Purkinje cell dendritic development in cerebellar slice cultures by protein kinase Calpha and -beta. JNeurobiol 2003; 57:95; http://dx.doi.org/10.1002/neu.10259
  • Metzger F, Kapfhammer JP. Protein kinase C activity modulates dendritic differentiation of rat Purkinje cells in cerebellar slice cultures. Euro J Neurosci 2000; 12:1993; PMID:10886339; http://dx.doi.org/10.1046/j.1460-9568.2000.00086.x
  • Schrenk K, Kapfhammer JP, Metzger F. Altered dendritic development of cerebellar Purkinje cells in slice cultures from protein kinase Cgamma-deficient mice. Neuroscience 2002; 110:675; PMID:11934475; http://dx.doi.org/10.1016/S0306-4522(01)00559-0
  • Li H, Chen G, Zhou B, Duan S. Actin Filament Assembly by Myristoylated, Alanine-rich C Kinase Substrate-Phosphatidylinositol-4,5-diphosphate Signaling Is Critical for Dendrite Branching. Mole Biol Cell 2008; 19:4804; PMID:18799624; http://dx.doi.org/10.1091/mbc.E08-03-0294
  • Suo L, Lu H, Ying G, Capecchi MR, Wu Q. Protocadherin clusters and cell adhesion kinase regulate dendrite complexity through Rho GTPase. J Mol Cell Biol 2012; 4:362; PMID:22730554; http://dx.doi.org/10.1093/jmcb/mjs034
  • Ledderose J, Dieter S, Schwarz MK. Maturation of postnatally generated olfactory bulb granule cells depends on functional gamma-protocadherin expression. SciRep 2013; 3:1514.
  • Millard SS, Zipursky SL. Dscam-mediated repulsion controls tiling and self-avoidance. Curr Opin Neurobiol 2008; 18:84; PMID:18538559; http://dx.doi.org/10.1016/j.conb.2008.05.005
  • Hattori D, Millard SS, Wojtowicz WM, Zipursky SL. Dscam-mediated cell recognition regulates neural circuit formation. Ann Rev Cell Dev Biol 2008; 24:597; PMID:18837673; http://dx.doi.org/10.1146/annurev.cellbio.24.110707.175250
  • Grueber WB, Sagasti A. Self-avoidance and Tiling: Mechanisms of Dendrite and Axon Spacing. Cold Spring Harbor Perspect Biol 2010; 2:a001750-a; PMID:20573716; http://dx.doi.org/10.1101/cshperspect.a001750
  • Garrett AM, Tadenev AL, Burgess RW. DSCAMs: restoring balance to developmental forces. Front Mol Neurosci 2012; 5:86; PMID:22912601; http://dx.doi.org/10.3389/fnmol.2012.00086
  • Fuerst PG, Bruce F, Tian M, Wei W, Elstrott J, Feller MB, Erskine L, Singer JH, Burgess RW. DSCAM and DSCAML1 function in self-avoidance in multiple cell types in the developing mouse retina. Neuron 2009; 64:484; PMID:19945391; http://dx.doi.org/10.1016/j.neuron.2009.09.027
  • Fuerst PG, Koizumi A, Masland RH, Burgess RW. Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 2008; 451:470-4; PMID:18216855; http://dx.doi.org/10.1038/nature06514
  • Hughes ME, Bortnick R, Tsubouchi A, Baumer P, Kondo M, Uemura T, Schmucker D. Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 2007; 54:417; PMID:17481395; http://dx.doi.org/10.1016/j.neuron.2007.04.013
  • Matthews BJ, Kim ME, Flanagan JJ, Hattori D, Clemens JC, Zipursky SL, Grueber WB. Dendrite self-avoidance is controlled by Dscam. Cell 2007; 129:593; PMID:17482551; http://dx.doi.org/10.1016/j.cell.2007.04.013
  • Soba P, Zhu S, Emoto K, Younger S, Yang SJ, Yu HH, Lee T, Jan LY, Jan YN. Drosophila sensory neurons require Dscam for dendritic self-avoidance and proper dendritic field organization. Neuron 2007; 54:403; PMID:17481394; http://dx.doi.org/10.1016/j.neuron.2007.03.029
  • Lefebvre JL, Kostadinov D, Chen WV, Maniatis T, Sanes JR. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 2012; 488:517; PMID:22842903; http://dx.doi.org/10.1038/nature11305
  • Prasad T, Weiner JA. Direct and indirect regulation of spinal cord Ia afferent terminal formation by the gamma-protocadherins. Front Mol Neurosci 2011; 4:54; PMID:22275881; http://dx.doi.org/10.3389/fnmol.2011.00054
  • Gibson DA, Tymanskyj S, Yuan RC, Leung HC, Lefebvre JL, Sanes JR, Chedotal A, Ma L. Dendrite self-avoidance requires cell-autonomous slit/robo signaling in cerebellar purkinje cells. Neuron 2014; 81:1040-56; PMID:24607227; http://dx.doi.org/10.1016/j.neuron.2014.01.009
  • Golan-Mashiach M, Grunspan M, Emmanuel R, Gibbs-Bar L, Dikstein R, Shapiro E. Identification of CTCF as a master regulator of the clustered protocadherin genes. Nucleic Acids Res 2012; 40(8):3378-91; PMID:22210889
  • Guo Y, Monahan K, Wu H, Gertz J, Varley KE, Li W, Myers RM, Maniatis T, Wu Q. CTCF/cohesin-mediated DNA looping is required for protocadherin alpha promoter choice. Proc Natl Acad Sci U S A 2012; 109:21081-6; PMID:23204437; http://dx.doi.org/10.1073/pnas.1219280110
  • Monahan K, Rudnick ND, Kehayova PD, Pauli F, Newberry KM, Myers RM, Maniatis T. Role of CCCTC binding factor (CTCF) and cohesin in the generation of single-cell diversity of protocadherin-alpha gene expression. Proc Natl Acad Sci U S A 2012; 109:9125-30; PMID:22550178; http://dx.doi.org/10.1073/pnas.1205074109
  • Hirayama T, Tarusawa E, Yoshimura Y, Galjart N, Yagi T. CTCF is required for neural development and stochastic expression of clustered Pcdh genes in neurons. Cell Reports 2012; 2:345; PMID:22854024; http://dx.doi.org/10.1016/j.celrep.2012.06.014
  • Toyoda S, Kawaguchi M, Kobayashi T, Tarusawa E, Toyama T, Okano M, Oda M, Nakauchi H, Yoshimura Y, Sanbo M, et al. Developmental epigenetic modification regulates stochastic expression of clustered protocadherin genes, generating single neuron diversity. Neuron 2014; 82:94-108; PMID:24698270; http://dx.doi.org/10.1016/j.neuron.2014.02.005
  • Wolverton T, Lalande M. Identification and characterization of three members of a novel subclass of protocadherins. Genomics 2001; 76:66-72; PMID:11549318; http://dx.doi.org/10.1006/geno.2001.6592
  • Redies C, Vanhalst K, Roy F. delta-Protocadherins: unique structures and functions. Cell Mol Life Sci 2005; 62:2840; PMID:16261259; http://dx.doi.org/10.1007/s00018-005-5320-z
  • Hirano S, Yan Q, Suzuki ST. Expression of a novel protocadherin, OL-protocadherin, in a subset of functional systems of the developing mouse brain. J Neurosci 1999; 19:995-1005; PMID:9920663
  • Yamagata K, Andreasson KI, Sugiura H, Maru E, Dominique M, Irie Y, Miki N, Hayashi Y, Yoshioka M, Kaneko K, et al. Arcadlin is a neural activity-regulated cadherin involved in long term potentiation. J Biol Chem 1999; 274:19473-1979; PMID:10383464; http://dx.doi.org/10.1074/jbc.274.27.19473
  • Hoshina N, Tanimura A, Yamasaki M, Inoue T, Fukabori R, Kuroda T, Yokoyama K, Tezuka T, Sagara H, Hirano S, et al. Protocadherin 17 regulates presynaptic assembly in topographic corticobasal Ganglia circuits. Neuron 2013; 78:839-54; PMID:23684785; http://dx.doi.org/10.1016/j.neuron.2013.03.031
  • Tai K, Kubota M, Shiono K, Tokutsu H, Suzuki ST. Adhesion Properties and Retinofugal Expression of Chicken Protocadherin-19. Brain Res 2010; 1344:13-24; PMID: 20438721
  • Chen X, Gumbiner BM. Paraxial protocadherin mediates cell sorting and tissue morphogenesis by regulating C-cadherin adhesion activity. J Cell Biol 2006; 174:301; PMID:16847104; http://dx.doi.org/10.1083/jcb.200602062
  • Yasuda S, Tanaka H, Sugiura H, Okamura K, Sakaguchi T, Tran U, Takemiya T, Mizoguchi A, Yagita Y, Sakurai T, et al. Activity-induced protocadherin arcadlin regulates dendritic spine number by triggering N-cadherin endocytosis via TAO2beta and p38 MAP kinases. Neuron 2007; 56:456; PMID:17988630; http://dx.doi.org/10.1016/j.neuron.2007.08.020
  • Biswas S, Emond MR, Jontes JD. Protocadherin-19 and N-cadherin interact to control cell movements during anterior neurulation. J Cell Biol 2010; 191:1029-41; PMID:21115806; http://dx.doi.org/10.1083/jcb.201007008
  • Emond MR, Biswas S, Blevins CJ, Jontes JD. A complex of Protocadherin-19 and N-cadherin mediates a novel mechanism of cell adhesion. J Cell Biol 2011; 195:1115-21; PMID:22184198; http://dx.doi.org/10.1083/jcb.201108115
  • Piper M, Dwivedy A, Leung L, Bradley RS, Holt CE. NF-protocadherin and TAF1 regulate retinal axon initiation and elongation in vivo. J Neurosci 2008; 28:100-5; PMID:18171927; http://dx.doi.org/10.1523/JNEUROSCI.4490-07.2008
  • International League Against Epilepsy Consortium on Complex Epilepsies. Electronic address e-auea. Genetic determinants of common epilepsies: a meta-analysis of genome-wide association studies. Lancet Neurol 2014; 13:893-903; PMID:25087078; http://dx.doi.org/10.1016/S1474-4422(14)70171-1
  • Tsai N-P, Wilkerson JR, Guo W, Maksimova MA, DeMartino GN, Cowan CW, Huber KM. Multiple Autism-Linked Genes Mediate Synapse Elimination via Proteasomal Degradation of a Synaptic Scaffold PSD-95. Cell 2012; 151:1581-94; PMID:23260144; http://dx.doi.org/10.1016/j.cell.2012.11.040
  • Morrow EM, Yoo SY, Flavell SW, Kim TK, Lin Y, Hill RS, Mukaddes NM, Balkhy S, Gascon G, Hashmi A, et al. Identifying autism loci and genes by tracing recent shared ancestry. Science (New York, NY) 2008; 321:218; http://dx.doi.org/10.1126/science.1157657
  • Schreiner D, Muller K, Hofer HW. The intracellular domain of the human protocadherin hFat1 interacts with Homer signalling scaffolding proteins. FEBS letters 2006; 580:5295; PMID:16979624; http://dx.doi.org/10.1016/j.febslet.2006.08.079
  • Ciani L, Patel A, Allen ND, ffrench-Constant C. Mice lacking the giant protocadherin mFAT1 exhibit renal slit junction abnormalities and a partially penetrant cyclopia and anophthalmia phenotype. Mol Cell Biol 2003; 23:3575-82; PMID:12724416; http://dx.doi.org/10.1128/MCB.23.10.3575-3582.2003
  • Saburi S, Hester I, Goodrich L, McNeill H. Functional interactions between Fat family cadherins in tissue morphogenesis and planar polarity. Development 2012; 139:1806-20; PMID:22510986; http://dx.doi.org/10.1242/dev.077461
  • Nakayama M, Nakajima D, Yoshimura R, Endo Y, Ohara O. MEGF1/fat2 proteins containing extraordinarily large extracellular domains are localized to thin parallel fibers of cerebellar granule cells. Mol Cell Neurosci 2002; 20:563; PMID:12213440; http://dx.doi.org/10.1006/mcne.2002.1146
  • Nagae S, Tanoue T, Takeichi M. Temporal and spatial expression profiles of the Fat3 protein, a giant cadherin molecule, during mouse development. Dev Dynamics 2007; 236:534; PMID:17131403; http://dx.doi.org/10.1002/dvdy.21030
  • Deans MR, Krol A, Abraira VE, Copley CO, Tucker AF, Goodrich LV. Control of neuronal morphology by the atypical cadherin fat3. Neuron 2011; 71:820; PMID:21903076; http://dx.doi.org/10.1016/j.neuron.2011.06.026
  • Probst B, Rock R, Gessler M, Vortkamp A, Puschel AW. The rodent Four-jointed ortholog Fjx1 regulates dendrite extension. Dev Biol 2007; 312:461-70; PMID:18028897; http://dx.doi.org/10.1016/j.ydbio.2007.09.054
  • Usui T, Shima Y, Shimada Y, Hirano S, Burgess RW, Schwarz TL, Takeichi M, Uemura T. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 1999; 98:585; PMID:10490098; http://dx.doi.org/10.1016/S0092-8674(00)80046-X
  • Chae J, Kim MJ, Goo JH, Collier S, Gubb D, Charlton J, Adler PN, Park WJ. The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development 1999; 126:5421-9; PMID:10556066
  • Shima Y, Kengaku M, Hirano T, Takeichi M, Uemura T. Regulation of dendritic maintenance and growth by a mammalian 7-pass transmembrane cadherin. Dev Cell 2004; 7:205-16; PMID:15296717; http://dx.doi.org/10.1016/j.devcel.2004.07.007
  • Kimura H, Usui T, Tsubouchi A, Uemura T. Potential dual molecular interaction of the Drosophila 7-pass transmembrane cadherin Flamingo in dendritic morphogenesis. J Cell Sci 2006; 119:1118; PMID:16507587; http://dx.doi.org/10.1242/jcs.02832
  • Shima Y, Kawaguchi SY, Kosaka K, Nakayama M, Hoshino M, Nabeshima Y, Hirano T, Uemura T. Opposing roles in neurite growth control by two seven-pass transmembrane cadherins. Nat Neurosci 2007; 10:963; PMID:17618280; http://dx.doi.org/10.1038/nn1933
  • Chen PL, Clandinin TR. The cadherin Flamingo mediates level-dependent interactions that guide photoreceptor target choice in Drosophila. Neuron 2008; 58:26; PMID:18400160; http://dx.doi.org/10.1016/j.neuron.2008.01.007
  • Bao H, Berlanga ML, Xue M, Hapip SM, Daniels RW, Mendenhall JM, Alcantara AA, Zhang B. The atypical cadherin flamingo regulates synaptogenesis and helps prevent axonal and synaptic degeneration in Drosophila. Mol Cell Neurosci 2007; 34:662; PMID:17321750; http://dx.doi.org/10.1016/j.mcn.2007.01.007
  • Tissir F, Bar I, Jossin Y, Goffinet AM. Protocadherin Celsr3 is crucial in axonal tract development. Nat Neurosci 2005; 8:451-7; PMID:15778712
  • Lee RC, Clandinin TR, Lee CH, Chen PL, Meinertzhagen IA, Zipursky SL. The protocadherin Flamingo is required for axon target selection in the Drosophila visual system. Nat Neurosci 2003; 6:557-63; PMID:12754514; http://dx.doi.org/10.1038/nn1063
  • Senti KA, Usui T, Boucke K, Greber U, Uemura T, Dickson BJ. Flamingo regulates R8 axon-axon and axon-target interactions in the Drosophila visual system. Curr Biol 2003; 13:828-32; PMID:12747830; http://dx.doi.org/10.1016/S0960-9822(03)00291-4
  • Gao FB, Brenman JE, Jan LY, Jan YN. Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Deve 1999; 13:2549; PMID:10521399; http://dx.doi.org/10.1101/gad.13.19.2549
  • Gao FB, Kohwi M, Brenman JE, Jan LY, Jan YN. Control of dendritic field formation in Drosophila: the roles of flamingo and competition between homologous neurons. Neuron 2000; 28:91; PMID:11086986; http://dx.doi.org/10.1016/S0896-6273(00)00088-X
  • Sweeney NT, Li W, Gao FB. Genetic manipulation of single neurons in vivo reveals specific roles of flamingo in neuronal morphogenesis. Dev Biol 2002; 247:76-88; PMID:12074553; http://dx.doi.org/10.1006/dbio.2002.0702
  • Grueber WB, Jan LY, Jan YN. Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development (Cambridge, England) 2002; 129:2867; PMID:12050135
  • Reuter JE, Nardine TM, Penton A, Billuart P, Scott EK, Usui T, Uemura T, Luo L. A mosaic genetic screen for genes necessary for Drosophila mushroom body neuronal morphogenesis. Development 2003; 130:1203-13; PMID:12571111; http://dx.doi.org/10.1242/dev.00319
  • Hakeda-Suzuki S, Berger-Muller S, Tomasi T, Usui T, Horiuchi SY, Uemura T, Suzuki T. Golden Goal collaborates with Flamingo in conferring synaptic-layer specificity in the visual system. Nat Neurosci 2011; 14:314-23; PMID:21317905; http://dx.doi.org/10.1038/nn.2756
  • Hakeda S, Suzuki T. Golden goal controls dendrite elongation and branching of multidendritic arborization neurons in Drosophila. Genes Cells 2013; 18:960-73; PMID:23919529; http://dx.doi.org/10.1111/gtc.12089
  • Matsubara D, Horiuchi S-Y, Shimono K, Usui T, Uemura T. The seven-pass transmembrane cadherin Flamingo controls dendritic self-avoidance via its binding to a LIM domain protein, Espinas, in Drosophila sensory neurons. Genes Dev 2011; 25:1982-96; PMID:21937715; http://dx.doi.org/10.1101/gad.16531611
  • Huarcaya Najarro E, Ackley BD. C. elegans fmi-1/flamingo and Wnt pathway components interact genetically to control the anteroposterior neurite growth of the VD GABAergic neurons. Dev Biol 2013; 377:224-235; PMID:23376536; http://dx.doi.org/10.1016/j.ydbio.2013.01.014
  • Dallosso, AR, Hancock, AL, Szemes, M, Moorwood, K, Chilukamarri, L, Tsai, HH, Sarkar, A, Barasch, J, Vuononvirta, R, Jones, C, et al. Frequent long-range epigenetic silencing of protocadherin gene clusters on chromosome 5q31 in Wilms' tumor. PLoS Genetics 2009; 5:e1000745; PMID:19956686; http://dx.doi.org/10.1371/journal.pgen.1000745
  • Dallosso AR, Oster B, Greenhough A, Thorsen K, Curry TJ, Owen C, Hancock AL, Szemes M, Paraskeva C, Frank M, et al. Long-range epigenetic silencing of chromosome 5q31 protocadherins is involved in early and late stages of colorectal tumorigenesis through modulation of oncogenic pathways. Oncogene 2012; 31:4409-4419; PMID:22249255; http://dx.doi.org/10.1038/onc.2011.609
  • Berndt JD, Aoyagi A, Yang P, Anastas JN, Tang L, Moon RT. Mindbomb 1, an E3 ubiquitin ligase, forms a complex with RYK to activate Wnt/b-catenin signaling. J Cell Biol 2011; 194:737-750; PMID:21875946; http://dx.doi.org/10.1083/jcb.201107021
  • Rosso SB, Sussman D, Wynshaw-Boris A, Salinas PC. Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 2005; 8: 34-42; PMID:15608632; http://dx.doi.org/10.1038/nn1374
  • Hiester BG, Galati DF, Salinas PC, Jones KR. Neurotrophin and Wnt signaling cooperatively regulate dendritic spine formation. Mol Cell Neurosci 2013; 56: 115-127; PMID:23639831; http://dx.doi.org/10.1016/j.mcn.2013.04.006
  • Ciani L, Salinas PC. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci 2005; 6:351-362; PMID:15832199; http://dx.doi.org/10.1038/nrn1665
  • Nakao S, Platek A, Hirano S, Takeichi M. Contact-dependent promotion of cell migration by the OL-protocadherin-Nap1 interaction. J Cell Biol 2008; 182:395-410; PMID:18644894; http://dx.doi.org/10.1083/jcb.200802069
  • Biswas S, Emond MR, Duy PQ, Hao le T, Beattie CE, Jontes JD. Protocadherin-18b interacts with Nap1 to control motor axon growth and arborization in zebrafish. Mol Biol Cell 2014; 25: 633-642; PMID:24371087; http://dx.doi.org/10.1091/mbc.E13-08-0475
  • Hayashi S, Inoue Y, Kiyonari H, Abe T, Misaki K, Moriguchi H, Tanaka Y, Takeichi M. Protocadherin-17 mediates collective axon extension by recruiting actin regulator complexes to interaxonal contacts. Dev Cell 2014; 30: 673-687; PMID:25199687; http://dx.doi.org/10.1016/j.devcel.2014.07.015

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