Kohmura, N. et al. Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron 20, 1137–1151. https://doi.org/10.1016/s0896-6273(00)80495-x (1998).
Google Scholar
Wu, Q. & Maniatis, T. A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97, 779–790. https://doi.org/10.1016/s0092-8674(00)80789-8 (1999).
Google Scholar
Esumi, S. et al. Monoallelic yet combinatorial expression of variable exons of the protocadherin-α gene cluster in single neurons. Nat. Genet. 37, 171–176. https://doi.org/10.1038/ng1500 (2005).
Google Scholar
Kaneko, R. et al. Allelic gene regulation of Pcdh-α and Pcdh-γ clusters involving both monoallelic and biallelic expression in single Purkinje cells. J. Biol. Chem. 281, 30551–30560. https://doi.org/10.1074/jbc.M605677200 (2006).
Google Scholar
Hirano, K. et al. Single-neuron diversity generated by protocadherin-β cluster in mouse central and peripheral nervous systems. Front. Mol. Neurosci. 5, 90. https://doi.org/10.3389/fnmol.2012.00090 (2012).
Google Scholar
Schreiner, D. & Weiner, J. A. Combinatorial homophilic interaction between gamma-protocadherin multimers greatly expands the molecular diversity of cell adhesion. Proc. Natl. Acad. Sci. USA 107, 14893–14898. https://doi.org/10.1073/pnas.1004526107 (2010).
Google Scholar
Thu, C. A. et al. Single-cell identity generated by combinatorial homophilic interactions between α, β, and γ protocadherins. Cell 158, 1045–1059. https://doi.org/10.1016/j.cell.2014.07.012 (2014).
Google Scholar
Rubinstein, R., Goodman, K. M., Maniatis, T., Shapiro, L. & Honig, B. Structural origins of clustered protocadherin-mediated neuronal barcoding. Semin. Cell Dev. Biol. 69, 140–150. https://doi.org/10.1016/j.semcdb.2017.07.023 (2017).
Google Scholar
Mountoufaris, G., Canzio, D., Nwakeze, C. L., Chen, W. V. & Maniatis, T. Writing, reading, and translating the clustered protocadherin cell surface recognition code for neural circuit assembly. Annu. Rev. Cell Dev. Biol. 34, 471–493. https://doi.org/10.1146/annurev-cellbio-100616-060701 (2018).
Google Scholar
Pancho, A., Aerts, T., Mitsogiannis, M. D. & Seuntjens, E. Protocadherins at the crossroad of signaling pathways. Front. Mol. Neurosci. 13, 117. https://doi.org/10.3389/fnmol.2020.00117 (2020).
Google Scholar
Lefebvre, J. L., Kostadinov, D., Chen, W. V., Maniatis, T. & Sanes, J. R. Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature 488, 517–521. https://doi.org/10.1038/nature11305 (2012).
Google Scholar
Kostadinov, D. & Sanes, J. R. Protocadherin-dependent dendritic self-avoidance regulates neural connectivity and circuit function. Elife 4, e08964. https://doi.org/10.7554/eLife.08964 (2015).
Google Scholar
Ing-Esteves, S. et al. Combinatorial effects of alpha- and gamma-protocadherins on neuronal survival and dendritic self-avoidance. J. Neurosci. 38, 2713–2729. https://doi.org/10.1523/JNEUROSCI.3035-17.2018 (2018).
Google Scholar
Hasegawa, S. et al. The protocadherin-α family is involved in axonal coalescence of olfactory sensory neurons into glomeruli of the olfactory bulb in mouse. Mol. Cell. Neurosci. 38, 66–79. https://doi.org/10.1016/j.mcn.2008.01.016 (2008).
Google Scholar
Mountoufaris, G. et al. Multicluster Pcdh diversity is required for mouse olfactory neural circuit assembly. Science 356, 411–414. https://doi.org/10.1126/science.aai8801 (2017).
Google Scholar
Katori, S. et al. Protocadherin-α family is required for serotonergic projections to appropriately innervate target brain areas. J. Neurosci. 29, 9137–9147. https://doi.org/10.1523/JNEUROSCI.5478-08.2009 (2009).
Google Scholar
Katori, S. et al. Protocadherin-αC2 is required for diffuse projections of serotonergic axons. Sci. Rep. 7, 15908. https://doi.org/10.1038/s41598-017-16120-y (2017).
Google Scholar
Chen, W. V. et al. PcdhαC2 is required for axonal tiling and assembly of serotonergic circuitries in mice. Science 356, 406–411. https://doi.org/10.1126/science.aal3231 (2017).
Google Scholar
Garrett, A. M., Schreiner, D., Lobas, M. A. & Weiner, J. A. γ-Protocadherins control cortical dendrite arborization by regulating the activity of a FAK/PKC/MARCKS signaling pathway. Neuron 74, 269–276. https://doi.org/10.1016/j.neuron.2012.01.028 (2012).
Google Scholar
Suo, L., Lu, H., Ying, G., Capecchi, M. R. & Wu, Q. Protocadherin clusters and cell adhesion kinase regulate dendrite complexity through Rho GTPase. J. Mol. Cell Biol. 4, 362–376. https://doi.org/10.1093/jmcb/mjs034 (2012).
Google Scholar
Molumby, M. J., Keeler, A. B. & Weiner, J. A. Homophilic protocadherin cell-cell interactions promote dendrite complexity. Cell Rep. 15, 1037–1050. https://doi.org/10.1016/j.celrep.2016.03.093 (2016).
Google Scholar
Molumby, M. J. et al. γ-Protocadherins interact with neuroligin-1 and negatively regulate dendritic spine morphogenesis. Cell Rep. 18, 2702–2714. https://doi.org/10.1016/j.celrep.2017.02.060 (2017).
Google Scholar
Steffen, D. M. et al. The γ-protocadherins interact physically and functionally with neuroligin-2 to negatively regulate inhibitory synapse density and are required for normal social interaction. Mol. Neurobiol. 58, 2574–2589. https://doi.org/10.1007/s12035-020-02263-z (2021).
Google Scholar
Reiss, K. et al. Regulated ADAM10-dependent ectodomain shedding of gamma-protocadherin C3 modulates cell-cell adhesion. J. Biol. Chem. 281, 21735–21744. https://doi.org/10.1074/jbc.M602663200 (2006).
Google Scholar
Rubinstein, R. et al. Molecular logic of neuronal self-recognition through protocadherin domain interactions. Cell 163, 629–642. https://doi.org/10.1016/j.cell.2015.09.026 (2015).
Google Scholar
Goodman, K. M. et al. Structural basis of diverse homophilic recognition by clustered α- and β-protocadherins. Neuron 90, 709–723. https://doi.org/10.1016/j.neuron.2016.04.004 (2016).
Google Scholar
Goodman, K. M. et al. γ-Protocadherin structural diversity and functional implications. Elife 5, e20930. https://doi.org/10.7554/eLife.20930 (2016).
Google Scholar
Goodman, K. M. et al. Protocadherin cis-dimer architecture and recognition unit diversity. Proc. Natl. Acad. Sci. USA 114, E9829–E9837. https://doi.org/10.1073/pnas.1713449114 (2017).
Google Scholar
Ozawa, M. & Kemler, R. Altered cell adhesion activity by pervanadate due to the dissociation of α-catenin from the E-cadherin catenin complex. J. Biol. Chem. 273, 6166–6170. https://doi.org/10.1074/jbc.273.11.6166 (1998).
Google Scholar
Stryer, L. & Haugland, R. P. Energy transfer: A spectroscopic ruler. Proc. Natl. Acad. Sci. USA 58, 719–726. https://doi.org/10.1073/pnas.58.2.719 (1967).
Google Scholar
Greenwald, E. C., Mehta, S. & Zhang, J. Genetically encoded fluorescent biosensors illuminate the spatiotemporal regulation of signaling networks. Chem. Rev. 118, 11707–11794. https://doi.org/10.1021/acs.chemrev.8b00333 (2018).
Google Scholar
Kim, S. A., Tai, C. Y., Mok, L. P., Mosser, E. A. & Schuman, E. M. Calcium-dependent dynamics of cadherin interactions at cell-cell junctions. Proc. Natl. Acad. Sci. USA 108, 9857–9862. https://doi.org/10.1073/pnas.1019003108 (2011).
Google Scholar
Fernàndez-Monreal, M., Kang, S. & Phillips, G. R. Gamma-protocadherin homophilic interaction and intracellular trafficking is controlled by the cytoplasmic domain in neurons. Mol. Cell. Neurosci. 40, 344–353. https://doi.org/10.1016/j.mcn.2008.12.002 (2009).
Google Scholar
Feinberg, E. H. et al. GFP reconstitution across synaptic partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57, 353–363. https://doi.org/10.1016/j.neuron.2007.11.030 (2008).
Google Scholar
Kim, J. et al. mGRASP enables mapping mammalian synaptic connectivity with light microscopy. Nat. Methods 9, 96–102. https://doi.org/10.1038/nmeth.1784 (2011).
Google Scholar
Tsetsenis, T., Boucard, A. A., Araç, D., Brunger, A. T. & Südhof, T. C. Direct visualization of trans-synaptic neurexin-neuroligin interactions during synapse formation. J. Neurosci. 34, 15083–15096. https://doi.org/10.1523/JNEUROSCI.0348-14.2014 (2014).
Google Scholar
Choi, J. H. et al. Interregional synaptic maps among engram cells underlie memory formation. Science 360, 430–435. https://doi.org/10.1126/science.aas9204 (2018).
Google Scholar
Kinoshita, N. et al. Genetically encoded fluorescent indicator GRAPHIC delineates intercellular connections. Science 15, 28–38. https://doi.org/10.1016/j.isci.2019.04.013 (2019).
Google Scholar
Kinoshita, N., Huang, A. J. Y., McHugh, T. J., Miyawaki, A. & Shimogori, T. Diffusible GRAPHIC to visualize morphology of cells after specific cell-cell contact. Sci. Rep. 10, 14437. https://doi.org/10.1038/s41598-020-71474-0 (2020).
Google Scholar
Hasegawa, S. et al. Clustered protocadherins are required for building functional neural circuits. Front. Mol. Neurosci. 10, 114. https://doi.org/10.3389/fnmol.2017.00114 (2017).
Google Scholar
Fujii, Y. et al. PA tag: A versatile protein tagging system using a super high affinity antibody against a dodecapeptide derived from human podoplanin. Protein Expr. Purif. 95, 240–247. https://doi.org/10.1016/j.pep.2014.01.009 (2014).
Google Scholar
Shibata, H. et al. A new role for annexin A11 in the early secretory pathway via stabilizing Sec31A protein at the endoplasmic reticulum exit sites (ERES). J. Biol. Chem. 290, 4981–4993. https://doi.org/10.1074/jbc.M114.592089 (2015).
Google Scholar
Kanadome, T., Shibata, H., Kuwata, K., Takahara, T. & Maki, M. The calcium-binding protein ALG-2 promotes endoplasmic reticulum exit site localization and polymerization of Trk-fused gene (TFG) protein. FEBS J. 284, 56–76. https://doi.org/10.1111/febs.13949 (2017).
Google Scholar
