Structural origins of clustered protocadherin-mediated neuronal barcoding

Seminars in Cell & Developmental Biology - Tập 69 - Trang 140-150 - 2017
Rotem Rubinstein1,2, Kerry Marie Goodman1, Tom Maniatis1,3, Lawrence Shapiro1,3, Barry Honig1,2,3,4,5
1Department of Biochemistry and Molecular Biophysics, New York, NY 10032, USA
2Department of Systems Biology, New York, NY 10032, USA
3Zuckerman Mind Brain and Behavior Institute, New York, NY 10032, USA
4Howard Hughes Medical Institute, New York, NY 10032, USA
5Department of Medicine, Columbia University, New York, NY 10032, USA

Tài liệu tham khảo

Azevedo, 2009, Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain, J. Comp. Neurol., 513, 532, 10.1002/cne.21974 Lefebvre, 2012, Protocadherins mediate dendritic self-avoidance in the mammalian nervous system, Nature, 488, 517, 10.1038/nature11305 Kostadinov, 2015, Protocadherin-dependent dendritic self-avoidance regulates neural connectivity and circuit function, Elife, 4, 10.7554/eLife.08964 Mountoufaris, 2017, Multicluster Pcdh diversity is required for mouse olfactory neural circuit assembly, Science, 356, 411, 10.1126/science.aai8801 Chen, 2012, Functional significance of isoform diversification in the protocadherin gamma gene cluster, Neuron, 75, 402, 10.1016/j.neuron.2012.06.039 Lefebvre, 2008, gamma-Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina, Development, 135, 4141, 10.1242/dev.027912 Prasad, 2011, Direct and indirect regulation of spinal cord la afferent terminal formation by the gamma-protocadherins, Front. Mol. Neurosci., 2011 Prasad, 2008, A differential developmental pattern of spinal interneuron apoptosis during synaptogenesis: insights from genetic analyses of the protocadherin-gamma gene cluster, Development, 135, 4153, 10.1242/dev.026807 Lin, 2010, PDCD10/CCM3 acts downstream of {gamma}-protocadherins to regulate neuronal survival, J. Biol. Chem., 285, 41675, 10.1074/jbc.M110.179895 Garrett, 2009, Control of CNS synapse development by {gamma}-protocadherin-mediated astrocyte-neuron contact, J. Neurosci., 29, 11723, 10.1523/JNEUROSCI.2818-09.2009 Weiner, 2005, Gamma protocadherins are required for synaptic development in the spinal cord, Proc. Natl. Acad. Sci. U. S. A., 102, 8, 10.1073/pnas.0407931101 Hasegawa, 2008, The protocadherin-alpha family is involved in axonal coalescence of olfactory sensory neurons into glomeruli of the olfactory bulb in mouse, Mol. Cell. Neurosci., 38, 66, 10.1016/j.mcn.2008.01.016 Hasegawa, 2012, Constitutively expressed Protocadherin-alpha regulates the coalescence and elimination of homotypic olfactory axons through its cytoplasmic region, Front. Mol. Neurosci., 5, 97, 10.3389/fnmol.2012.00097 Fukuda, 2008, Down-regulation of protocadherin-alpha A isoforms in mice changes contextual fear conditioning and spatial working memory, Eur. J. Neurosci., 28, 1362, 10.1111/j.1460-9568.2008.06428.x Wang, 2002, Gamma protocadherins are required for survival of spinal interneurons, Neuron, 36, 843, 10.1016/S0896-6273(02)01090-5 Chen, 2017, Pcdhalphac2 is required for axonal tiling and assembly of serotonergic circuitries in mice, Science, 356, 406, 10.1126/science.aal3231 Hasegawa, 2016, Distinct and cooperative functions for the protocadherin-α, -β and-γ clusters in neuronal survival and axon targeting, Front. Mol. Neurosci., 9, 155, 10.3389/fnmol.2016.00155 Kohmura, 1998, Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex, Neuron, 20, 1137, 10.1016/S0896-6273(00)80495-X Wu, 1999, A striking organization of a large family of human neural cadherin-like cell adhesion genes, Cell, 97, 779, 10.1016/S0092-8674(00)80789-8 Yu, 2008, Elephant shark sequence reveals unique insights into the evolutionary history of vertebrate genes: a comparative analysis of the protocadherin cluster, Proc. Natl. Acad. Sci. U. S. A., 105, 3819, 10.1073/pnas.0800398105 Yu, 2007, Sequencing and comparative analysis of fugu protocadherin clusters reveal diversity of protocadherin genes among teleosts, BMC Evol. Biol., 7, 49, 10.1186/1471-2148-7-49 Esumi, 2005, Monoallelic yet combinatorial expression of variable exons of the protocadherin-alpha gene cluster in single neurons, Nat. Genet., 37, 171, 10.1038/ng1500 Hirano, 2012, Single-neuron diversity generated by protocadherin-beta cluster in mouse central and peripheral nervous systems, Front. Mol. Neurosci., 5 Kaneko, 2006, Allelic gene regulation of Pcdh-alpha and Pcdh-gamma clusters involving both monoallelic and biallelic expression in single Purkinje cells, J. Biol. Chem., 281, 30551, 10.1074/jbc.M605677200 Tasic, 2002, Promoter choice determines splice site selection in protocadherin alpha and −gamma pre-mRNA splicing, Mol. Cell, 10, 21, 10.1016/S1097-2765(02)00578-6 Wang, 2002, Molecular mechanisms governing Pcdh-gamma gene expression: evidence for a multiple promoter and cis-alternative splicing model, Genes. Dev., 16, 1890, 10.1101/gad.1004802 Zipursky, 2017, The molecular basis of self-Avoidance, vol 362013, 547 Zipursky, 2010, Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly, Cell, 143, 343, 10.1016/j.cell.2010.10.009 Hattori, 2009, Robust discrimination between self and non-self neurites requires thousands of Dscam1 isoforms, Nature, 461, 644-U87, 10.1038/nature08431 Hattori, 2008, Dscam-mediated cell recognition regulates neural circuit formation, Annu. Rev. Cell Dev. Biol., 597, 10.1146/annurev.cellbio.24.110707.175250 Neves, 2004, Stochastic yet biased expression of multiple Dscam splice variants by individual cells, Nat. Genet., 36, 240, 10.1038/ng1299 Sun, 2013, Ultra-deep profiling of alternatively spliced Drosophila Dscam isoforms by circularization-assisted multi-segment sequencing, EMBO J., 32, 2029, 10.1038/emboj.2013.144 Zhan, 2004, Analysis of Dscam diversity in regulating axon guidance in Drosophila mushroom bodies, Neuron, 43, 673, 10.1016/j.neuron.2004.07.020 Miura, 2013, Probabilistic splicing of Dscam1 establishes identity at the level of single neurons, Cell, 155, 1166, 10.1016/j.cell.2013.10.018 Wojtowicz, 2004, Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding, Cell, 118, 619, 10.1016/j.cell.2004.08.021 Wojtowicz, 2007, A vast repertoire of Dscam binding specificities arises from modular interactions of variable ig domains, Cell, 130, 1134, 10.1016/j.cell.2007.08.026 Thu, 2014, Single-cell identity generated by combinatorial homophilic interactions between alpha, beta, and gamma protocadherins, Cell, 158, 1045, 10.1016/j.cell.2014.07.012 Schreiner, 2010, Combinatorial homophilic interaction between gamma-protocadherin multimers greatly expands the molecular diversity of cell adhesion, Proc. Natl. Acad. Sci. U. S. A., 107, 14893, 10.1073/pnas.1004526107 Schmucker, 2000, Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity, Cell, 101, 671, 10.1016/S0092-8674(00)80878-8 Matthews, 2007, Dendrite self-avoidance is controlled by Dscam, Cell, 129, 593, 10.1016/j.cell.2007.04.013 Hulpiau, 2009, Molecular evolution of the cadherin superfamily, Int. J. Biochem. Cell Biol., 41, 349, 10.1016/j.biocel.2008.09.027 Fernandez-Monreal, 2009, Gamma-protocadherin homophilic interaction and intracellular trafficking is controlled by the cytoplasmic domain in neurons, Mol. Cell. Neurosci., 40, 344, 10.1016/j.mcn.2008.12.002 Frank, 2005, Differential expression of individual gamma-protocadherins during mouse brain development, Mol. Cell. Neurosci., 29, 603, 10.1016/j.mcn.2005.05.001 Molumby, 2016, Homophilic protocadherin cell-cell interactions promote dendrite complexity, Cell Rep., 15, 1037, 10.1016/j.celrep.2016.03.093 Bonn, 2007, Combinatorial expression of alpha- and gamma-protocadherins alters their presenilin-dependent processing, Mol. Cell. Biol., 27, 4121, 10.1128/MCB.01708-06 Murata, 2004, Interaction with protocadherin-gamma regulates the cell surface expression of protocadherin-alpha, J. Biol. Chem., 279, 49508, 10.1074/jbc.M408771200 Morishita, 2006, Structure of the cadherin-related neuronal receptor/protocadherin-alpha first extracellular cadherin domain reveals diversity across cadherin families, J. Biol. Chem., 281, 33650, 10.1074/jbc.M603298200 Nicoludis, 2015, Sequence analyses of clustered protocadherins reveal antiparallel interactions that mediate homophilic specificity, Structure, 23, 2087, 10.1016/j.str.2015.09.005 Rubinstein, 2015, Molecular logic of neuronal self-recognition through protocadherin domain interactions, Cell, 163, 629, 10.1016/j.cell.2015.09.026 Harrison, 2016, Structural basis of adhesive binding by desmocollins and desmogleins, Proc. Natl. Acad. Sci. U. S. A., 113, 7160, 10.1073/pnas.1606272113 Boggon, 2002, C-cadherin ectodomain structure and implications for cell adhesion mechanisms, Science, 296, 1308, 10.1126/science.1071559 Goodman, 2016, Structural basis of diverse homophilic recognition by clustered alpha- and beta-protocadherins, Neuron, 90, 709, 10.1016/j.neuron.2016.04.004 Goodman, 2016, γ-Protocadherin structural diversity and functional implications, eLife, 5, e20930, 10.7554/eLife.20930 Nicoludis, 2016, Antiparallel protocadherin homodimers use distinct affinity- and specificity-mediating regions in cadherin repeats 1–4, eLife, 5 Brasch, 2012, Thinking outside the cell: how cadherins drive adhesion, Trends Cell Biol., 22, 299, 10.1016/j.tcb.2012.03.004 Ciatto, 2010, T-cadherin structures reveal a novel adhesive binding mechanism, Nat. Struct. Mol. Biol., 17, 339-U110, 10.1038/nsmb.1781 Harrison, 2010, Two-step adhesive binding by classical cadherins, Nat. Struct. Mol. Biol., 17, 348, 10.1038/nsmb.1784 Sotomayor, 2012, Structure of a force-conveying cadherin bond essential for inner-ear mechanotransduction, Nature, 492, 128, 10.1038/nature11590 Cooper, 2016, Structural determinants of adhesion by protocadherin-19 and implications for its role in epilepsy, Elife, 5, 10.7554/eLife.18529 Yagi, 2012, Molecular codes for neuronal individuality and cell assembly in the brain, Front. Mol. Neurosci., 5, 45, 10.3389/fnmol.2012.00045 Wu, 2011, Transforming binding affinities from three dimensions to two with application to cadherin clustering, Nature, 475, 510-U107, 10.1038/nature10183 Wu, 2013, Simulations of adhesion receptor dimerization on membrane surfaces, Biophys. J ., 104, 1221, 10.1016/j.bpj.2013.02.009 Buchanan, 2010, Proteolytic processing of protocadherin proteins requires endocytosis, Proc. Natl. Acad. Sci. U. S. A., 107, 17774, 10.1073/pnas.1013105107 Haas, 2005, Presenilin-dependent processing and nuclear function of gamma-protocadherins, J. Biol. Chem., 280, 9313, 10.1074/jbc.M412909200 Hambsch, 2005, {gamma}-Protocadherins, presenilin-mediated release of C-terminal fragment promotes locus expression, J. Biol. Chem., 280, 15888, 10.1074/jbc.M414359200 Han, 2010, Proteomics analysis reveals overlapping functions of clustered protocadherins, Mol. Cell. Proteomics, 9, 71, 10.1074/mcp.M900343-MCP200 Molumby, 2017, Gamma-protocadherins interact with neuroligin-1 and negatively regulate dendritic spine morphogenesis, Cell Rep., 18, 2702, 10.1016/j.celrep.2017.02.060 Schalm, 2010, Phosphorylation of protocadherin proteins by the receptor tyrosine kinase Ret, Proc. Natl. Acad. Sci. U. S. A., 107, 13894, 10.1073/pnas.1007182107 Zhang, 2012, Structure-based prediction of protein–protein interactions on a genome-wide scale, Nature, 490, 556, 10.1038/nature11503 Mah, 2016, The gamma-protocadherin-C3 isoform inhibits canonical Wnt signalling by binding to and stabilizing Axin1 at the membrane, Sci. Rep., 6