Protocadherins mediate dendritic self-avoidance in the mammalian nervous system.

paper Cited Public

Authors: Lefebvre, Julie L; Kostadinov, Dimitar; Chen, Weisheng V; Maniatis, Tom; Sanes, Joshua R
Year: 2012
Journal: Nature
PMID: 22842903
DOI: 10.1038/nature11305
PMCID: PMC3427422

Dendritic arborizations of many neurons are patterned by a process called self-avoidance, in which branches arising from a single neuron repel each other. By minimizing gaps and overlaps within the arborization, self-avoidance facilitates complete coverage of a neuron’s territory by its neurites. Remarkably, some neurons that display self-avoidance interact freely with other neurons of the same subtype, implying that they discriminate self from non-self. Here we demonstrate roles for the clustered protocadherins (Pcdhs) in dendritic self-avoidance and self/non-self discrimination. The Pcdh locus encodes 58 related cadherin-like transmembrane proteins, at least some of which exhibit isoform-specific homophilic adhesion in heterologous cells and are expressed stochastically and combinatorially in single neurons. Deletion of all 22 Pcdh genes in the mouse γ-subcluster (Pcdhg genes) disrupts self-avoidance of dendrites in retinal starburst amacrine cells (SACs) and cerebellar Purkinje cells. Further genetic analysis of SACs showed that Pcdhg proteins act cell-autonomously during development, and that replacement of the 22 Pcdhg proteins with a single isoform restores self-avoidance. Moreover, expression of the same single isoform in all SACs decreases interactions among dendrites of neighbouring SACs (heteroneuronal interactions). These results suggest that homophilic Pcdhg interactions between sibling neurites (isoneuronal interactions) generate a repulsive signal that leads to self-avoidance. In this model, heteroneuronal interactions are normally permitted because dendrites seldom encounter a matched set of Pcdhg proteins unless they emanate from the same soma. In many respects, our results mirror those reported for Dscam1 (Down syndrome cell adhesion molecule) in Drosophila: this complex gene encodes thousands of recognition molecules that exhibit stochastic expression and isoform-specific interactions, and mediate both self-avoidance and self/non-self discrimination. Thus, although insect Dscam and vertebrate Pcdh proteins share no sequence homology, they seem to underlie similar strategies for endowing neurons with distinct molecular identities and patterning their arborizations.

Figure 1

Pcdhgs are required for self-avoidance of SAC dendritesa. Pcdh locus comprises Pcdha, Pcdhb and Pcdhg subclusters. Pcdha and Pcdhg isoforms are assembled by splicing of 1 variable exon to 3 constant exons.b. SACs are present in both inner nuclear and ganglion cell layers (INL, GCL) and extend dendrites that form radially symmetrical arbors confined to thin sublaminae in the inner plexiform layer (IPL).c. SAC dendrites avoid isoneuronal dendrites but form synapses with dendrites of other SACs.d-i. Morphology of single SAC, labeled with membrane-Cherry, in the GCL in wild-type and Pcdhg mutant retinas. Wild-type SAC dendrites self-avoid. In Pcdhg mutants, self-avoidance defects include self-crossing and bundling of dendrites. Crossings are detected at 0.2 μm x-y resolution in single 0.8 μm optical sections (g,i magnified inset in f,h). Images with 0.2 μm z resolution are shown in Supplementary Fig. 1.j. SAC dendritic self-crossings in 1st-5th order branches per SAC. Graph underestimates difference between genotypes because the most severely affected mutant SACs could not be scored. ** P<0.01k,l. Number of terminal branches (i) and dendritic field diameter (j) do not differ between wild-type and mutant SACs. i-l show means ±s.e.m; n=8 cells from 5-6 animals per genotype.Scale bars, 50 μm (d,f) or 10 μm (e,g).

Figure 2

Pcdhgs pattern developing SAC dendrites in a cell-autonomous mannera-h. SACs in developing wild-type and Pcdhg mutant retinas. Wild-type SACs extend fine, exuberant branches (P3, P5) that make transient intradendritic contacts (P5, P8); by P12, excess branches and isoneuronal contacts are eliminated. Dendrites of mutant SACs display excessive self-crossing and bundling by P3; by P12, excess branches are eliminated, but crossing dendrites remain.i,j. Cultured Pcdhg mutant SACs exhibit loss of symmetric growth and uneven distribution of neurites.k. Histogram of fractal dimensions (Df, metric for space-filling) for 47 wild-type (black) and 47 mutant (grey) SACs. Wild-type SAC in i has Df of 1.61 and mutant SAC in j has Df of 1.53.l. Mean Df for cultured SACs (n=47 cells), SACs in vivo at P5 (n=6) and adult (n=9). *** P<0.001. Error bars, s.e.m. Scale bars, 50 μm except 20 μm in i,j.

Figure 3

No single Pcdhg isoform is necessary and any isoform is sufficient for dendrite self-avoidancea. SACs lacking Pcdhgc3-c5 (pcdhgtcko/fcon3;retina-cre) exhibit self-avoidance.b. Replacement of all 22 Pcdhgs by the PcdhgC3 isoform rescues SAC dendrite self-avoidance.c. SACs lacking Pcdhga1-a3 (pcdhgtako/tako) exhibit self-avoidance.d. Replacement of all 22 Pcdhgs by the PcdhgA1 isoform rescues SAC dendrite self-avoidance.e. Compared to mutants lacking all 22 isoforms, self-crossings in SACs expressing 19 or 1 isoform are restored to control levels. *** P<0.001; n.s., not significant. Bars are mean ± s.e.m, from 7 SACs from pcdhgtcko/fcon3;retina-cre retinas, 3 SACs from pcdhgtako/tako, and 9 from remaining genotypes. Scale bars, 50 μm.

Figure 4

Reducing Pcdhg diversity disrupts heteroneuronal SAC interactionsa. Two nearby SACs from a wild-type mouse injected with contrasting fluorescent dyes. Right panel shows image of the green SAC flipped vertically.b. Overlap between red and green cells in a. First two bars are derived from the two panels in a. The green cell was rotated in 45° steps or flipped and then rotated; third and fourth bars show mean overlap ± s.e.m. derived from these images (n=7). All inversions and rotations decrease overlap, indicating that overlap in the real image is non-random.c-e. Tracings of SAC pairs, and versions flipped as in a, from wild-type, Pcdhgrko/rko and cA1;Pcdhgrko/rko mice. Overlap shown in black.f. Overlap between neighboring cells, expressed as ratio between overlap measured in real and flipped images. Bars show mean ± s.e.m. for 11, 9 and 8 pairs from wild-type, Pcdhgrko/rko and single isoform-expressing (cA1;Pcdhgrko/rko and cC3;Pcdhgrko/rko) animals. Expression of a single isoform in neighboring SACs decreases their interaction.g. Mean length of overlapping segments between SAC pairs. R, real image; F, flipped image. *P=0.05; **P<0.05; ***P<0.01. Error bars, s.e.m. N as in f. Scale bar, 50 μm.

Figure 5

Purkinje cell dendrite self-avoidance requires Pcdhgsa-c. Control Purkinje cells labeled with Cre-dependent AAV-XFP in L7-cre transgenic mouse. Self-avoidance is clear in high magnification view in c (inset in b).d-f. Purkinje cells lacking Pcdhgs and labeled as in a-c have disorganized arbors marked by frequent self-crossing defects. f shows area boxed in e. g. Self-crossings detected in single confocal z-sections of 7225 μm2 unit area. *** P <0.001; n=8, 15 and 15 cells at P15, P21 and P35 respectively from ≥ 3 mice per genotype. h,i. Area of dendritic arbors (n=20 cells) and cell density (>40 regions) do not differ between control and mutant Purkinje cells. Bars show mean ±s.e.m. Scale bars, 50 μm in a, b, d, e; 10 μm in c, f.

#	Section	Preview
0	METHODS SUMMARY	Transgenic, knock-out and knock-in mouse lines used for this study, as well as methods for marking…
1	METHODS — Mouse strains	The Pcdhg fcon3 conditional mutant allele, in which the third constant exon is flanked by loxP…
2	METHODS — Mouse strains	the site of transgene integration rather than expression of fstl4. Thy1-OFP3 transgenic mice, in…
3	METHODS — Generation of single Pcdhg isoform conditional knock-in mice	Pcdhga1 and pcdhgc3 full-length cDNAs were amplified from RNA isolated from P21 C57/BL6 mouse brain,…
4	METHODS — Labeling of neurons	Plasmid encoding pAAV2/2-CAG-palmitoylation tag-mCherry-WPRE was used to generate recombinant AAV2/2…
5	METHODS — Labeling of neurons	To inject virus into eyes, adult mice were anesthetized with ketamine/xylazine by intraperitoneal…
6	METHODS — Labeling of neurons	For biolistic transfection of SACs, gold particles (1.0 μm diameter, Bio-Rad), were coated with…
7	METHODS — Labeling of neurons	To assess interactions between dendrites of neighboring SACs, we injected pairs of cells with…
8	METHODS — Tissue preparation and immunohistochemistry	Mice were euthanized with intraperitoneal injection of Nembutal, and either enucleated immediately…
9	METHODS — Tissue preparation and immunohistochemistry	Wholemount preparations and cryosections of retinas were performed as described22,42. Briefly, whole…
10	METHODS — SAC purification and culture	To isolate and culture wild-type and Pcdhg mutant SACs in vitro, we crossed the Thy1-OFP3 transgene,…
11	METHODS — Image Analysis	For best reproduction and clarity of SAC arbors, maximized projections of confocal images were…
12	METHODS — Image Analysis	For analysis of SAC density and mosaic regularity, confocal z-stacks of ChAT-labeled SACs through…
13	METHODS — Image Analysis	To compare the space-filling and complexity of control and mutant SAC arbors, we computed fractal…
14	METHODS — Image Analysis	For analysis of dendrite overlap between arbors of neighboring SACs, pairs with somata separated by…
15	METHODS — Image Analysis	Purkinje cell dendrite self-crossings detected in single confocal planes were counted in a 7,225…
16	METHODS — Image Analysis	Means were compared using two-tailed Student’s t test on condition of equivalent variances…
17	METHODS — RT-PCR of dissociated retina cells	We used FACS to sort live cells from dissociated P7 whole retina, VC1.1+ amacrine cells, and…

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In this knowledge base

Title	Year	PMID
A protocadherin gene cluster regulatory variant is associated with nicotine withdrawal and the urge to smoke.	2017	27067016
Functional significance of isoform diversification in the protocadherin gamma gene cluster.	2012	22884324

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Molecular mechanisms regulating the spatial configuration of neurites.	Hasegawa K et al.	—	2022	→
Mouse models for the study of clustered protocadherins.	McLeod CM et al.	—	2022	→
Neurons Induce Tiled Astrocytes with Branches That Avoid Each Other.	Hayashi MK et al.	—	2022	→
Patterned cPCDH expression regulates the fine organization of the neocortex.	Lv X et al.	—	2022	→
Pyk2 suppresses contextual fear memory in an autophosphorylation-independent manner.	Zheng J et al.	—	2022	→
Retinal cadherins and the retinal cadherinopathies: Current concepts and future directions.	Yusuf IH et al.	—	2022	→
Self-avoidance alone does not explain the function of Dscam1 in mushroom body axonal wiring.	Dong H et al.	—	2022	→
The Conserved Serine Transporter SdaC Moonlights To Enable Self Recognition.	Chittor A et al.	—	2022	→
The HUSH complex controls brain architecture and protocadherin fidelity.	Hagelkruys A et al.	—	2022	→
The m<sup>6</sup>A reader YTHDF2 is a negative regulator for dendrite development and maintenance of retinal ganglion cells.	Niu F et al.	—	2022	→
To Stick or Not to Stick: The Multiple Roles of Cell Adhesion Molecules in Neural Circuit Assembly.	Moreland T et al.	—	2022	→
Trans-splicing facilitated by RNA pairing greatly expands sDscam isoform diversity but not homophilic binding specificity.	Hou S et al.	—	2022	→
Whole-Exome Sequencing Identified Rare Variants in PCDHGB1 in Patients with Adult-Onset Dystonia.	Li LX et al.	—	2022	→
A loss-of-function variant in SUV39H2 identified in autism-spectrum disorder causes altered H3K9 trimethylation and dysregulation of protocadherin β-cluster genes in the developing brain.	Balan S et al.	—	2021	→
Biallelic variants in PCDHGC4 cause a novel neurodevelopmental syndrome with progressive microcephaly, seizures, and joint anomalies.	Iqbal M et al.	—	2021	→
Connecting the Neurobiology of Developmental Brain Injury: Neuronal Arborisation as a Regulator of Dysfunction and Potential Therapeutic Target.	Goikolea-Vives A et al.	—	2021	→
Converging genetic and epigenetic drivers of paediatric acute lymphoblastic leukaemia identified by an information-theoretic analysis.	Koldobskiy MA et al.	—	2021	→
Development of FRET-based indicators for visualizing homophilic trans interaction of a clustered protocadherin.	Kanadome T et al.	—	2021	→
Development of the vertebrate retinal direction-selective circuit.	Hamilton NR et al.	—	2021	→
Expression of an alternatively spliced variant of SORL1 in neuronal dendrites is decreased in patients with Alzheimer's disease.	Monti G et al.	—	2021	→
Gamma-protocadherin localization at the synapse is associated with parameters of synaptic maturation.	LaMassa N et al.	—	2021	→
Genomic Intelligence as Über Bio-Cybersecurity: The Gödel Sentence in Immuno-Cognitive Systems.	Markose SM	—	2021	→
Histone lysine methyltransferase SETDB1 as a novel target for central nervous system diseases.	Markouli M et al.	—	2021	→
Human-modified canids in human-modified landscapes: The evolutionary consequences of hybridization for grey wolves and free-ranging domestic dogs.	Pilot M et al.	—	2021	→
Little cells of the little brain: microglia in cerebellar development and function.	Stoessel MB et al.	—	2021	→
Long-Term Enhancement of NMDA Receptor Function in Inhibitory Neurons Preferentially Modulates Potassium Channels and Cell Adhesion Molecules.	Xia D et al.	—	2021	→
May the Odds Be Ever in Your Favor: Non-deterministic Mechanisms Diversifying Cell Surface Molecule Expression.	Williams DL et al.	—	2021	→
Molecular mechanisms regulating synaptic specificity and retinal circuit formation.	Graham HK et al.	—	2021	→
Molecular mechanisms that mediate dendrite morphogenesis.	Lefebvre JL	—	2021	→
Pharmacological and Therapeutic Approaches in the Treatment of Epilepsy.	Ghosh S et al.	—	2021	→
Role of DSCAM in the Development of Neural Control of Movement and Locomotion.	Lemieux M et al.	—	2021	→
Tetris in the Nervous System: What Principles of Neuronal Tiling Can Tell Us About How Glia Play the Game.	DeSantis DF et al.	—	2021	→
The angiopoietin-Tie2 pathway regulates Purkinje cell dendritic morphogenesis in a cell-autonomous manner.	Luck R et al.	—	2021	→
Theory of branching morphogenesis by local interactions and global guidance.	Uçar MC et al.	—	2021	→
The γ-Protocadherins Interact Physically and Functionally with Neuroligin-2 to Negatively Regulate Inhibitory Synapse Density and Are Required for Normal Social Interaction.	Steffen DM et al.	—	2021	→
An epigenome-wide association study of early-onset major depression in monozygotic twins.	Roberson-Nay R et al.	—	2020	→
Antagonistic regulation by insulin-like peptide and activin ensures the elaboration of appropriate dendritic field sizes of amacrine neurons.	Luo J et al.	—	2020	→
Chelicerata sDscam isoforms combine homophilic specificities to define unique cell recognition.	Zhou F et al.	—	2020	→
Clustered gamma-protocadherins regulate cortical interneuron programmed cell death.	Mancia Leon WR et al.	—	2020	→
Clustered Protocadherins Emerge as Novel Susceptibility Loci for Mental Disorders.	Jia Z et al.	—	2020	→
Dendritic Spine Density is Increased in Arcadlin-deleted Mouse Hippocampus.	Takeuchi C et al.	—	2020	→
Extrinsic Factors Regulating Dendritic Patterning.	Lin TY et al.	—	2020	→
Family-wide Structural and Biophysical Analysis of Binding Interactions among Non-clustered δ-Protocadherins.	Harrison OJ et al.	—	2020	→
<i>Caenorhabditis elegans</i> Flamingo FMI-1 controls dendrite self-avoidance through F-actin assembly.	Hsu HW et al.	—	2020	→
[Intrinsic and extrinsic mechanisms regulating neuronal dendrite morphogenesis].	Zhao W et al.	—	2020	→
Loss of Clustered Protocadherin Diversity Alters the Spatial Distribution of Cortical Interneurons in Mice.	Gallerani N et al.	—	2020	→
Neuronal strategies for meeting the right partner during brain wiring.	Agi E et al.	—	2020	→
New Optical Tools to Study Neural Circuit Assembly in the Retina.	Rangel Olguin AG et al.	—	2020	→
Origins and Proliferative States of Human Oligodendrocyte Precursor Cells.	Huang W et al.	—	2020	→
Pcdhβ deficiency affects hippocampal CA1 ensemble activity and contextual fear discrimination.	Asai H et al.	—	2020	→
Protocadherins at the Crossroad of Signaling Pathways.	Pancho A et al.	—	2020	→
Right Place at the Right Time: How Changes in Protocadherins Affect Synaptic Connections Contributing to the Etiology of Neurodevelopmental Disorders.	Mancini M et al.	—	2020	→
Synaptic Specificity, Recognition Molecules, and Assembly of Neural Circuits.	Sanes JR et al.	—	2020	→
Tandem CTCF sites function as insulators to balance spatial chromatin contacts and topological enhancer-promoter selection.	Jia Z et al.	—	2020	→
The role of clustered protocadherins in neurodevelopment and neuropsychiatric diseases.	Flaherty E et al.	—	2020	→
The γ-Protocadherins Regulate the Survival of GABAergic Interneurons during Developmental Cell Death.	Carriere CH et al.	—	2020	→
Visual Experience Influences Dendritic Orientation but Is Not Required for Asymmetric Wiring of the Retinal Direction Selective Circuit.	El-Quessny M et al.	—	2020	→
βIII spectrin controls the planarity of Purkinje cell dendrites by modulating perpendicular axon-dendrite interactions.	Fujishima K et al.	—	2020	→
Actin assembly and non-muscle myosin activity drive dendrite retraction in an UNC-6/Netrin dependent self-avoidance response.	Sundararajan L et al.	—	2019	→
Beyond being innervated: the epidermis actively shapes sensory dendritic patterning.	Yang WK et al.	—	2019	→
Branching mechanisms shaping dendrite architecture.	Lanoue V et al.	—	2019	→
Chromatin establishes an immature version of neuronal protocadherin selection during the naive-to-primed conversion of pluripotent stem cells.	Almenar-Queralt A et al.	—	2019	→
CRISPR/Cas9 interrogation of the mouse Pcdhg gene cluster reveals a crucial isoform-specific role for Pcdhgc4.	Garrett AM et al.	—	2019	→
Deep Survey of GABAergic Interneurons: Emerging Insights From Gene-Isoform Transcriptomics.	Que L et al.	—	2019	→
DNA Microscopy: Optics-free Spatio-genetic Imaging by a Stand-Alone Chemical Reaction.	Weinstein JA et al.	—	2019	→
Epigenetic Regulations in Neuropsychiatric Disorders.	Kuehner JN et al.	—	2019	→
Evolutionarily conserved and divergent functions for cell adhesion molecules in neural circuit assembly.	Kim B	—	2019	→
Germline Structural Variations Are Preferential Sites of DNA Replication Timing Plasticity during Development.	Hulke ML et al.	—	2019	→
Identification of an adhesive interface for the non-clustered δ1 protocadherin-1 involved in respiratory diseases.	Modak D et al.	—	2019	→
Interaction specificity of clustered protocadherins inferred from sequence covariation and structural analysis.	Nicoludis JM et al.	—	2019	→
MEA6 Deficiency Impairs Cerebellar Development and Motor Performance by Tethering Protein Trafficking.	Wang XT et al.	—	2019	→
Mechanisms that regulate morphogenesis of a highly branched neuron in C. elegans.	Sundararajan L et al.	—	2019	→
Microglia exit the CNS in spinal root avulsion.	Green LA et al.	—	2019	→
Revisiting Dscam diversity: lessons from clustered protocadherins.	Jin Y et al.	—	2019	→
Segregated neural explants exhibit co-oriented, asymmetric, neurite outgrowth.	Pettigrew DB et al.	—	2019	→
Snf2h Drives Chromatin Remodeling to Prime Upper Layer Cortical Neuron Development.	Alvarez-Saavedra M et al.	—	2019	→
Stages and transitions in dendrite arbor differentiation.	Yoong LF et al.	—	2019	→
Tandem Directional CTCF Sites Balance Protocadherin Promoter Usage	Wu Q et al.	—	2019	—
The generation of a protocadherin cell-surface recognition code for neural circuit assembly.	Canzio D et al.	—	2019	→
Tiling and somatotopic alignment of mammalian low-threshold mechanoreceptors.	Kuehn ED et al.	—	2019	→
Visualization of clustered protocadherin neuronal self-recognition complexes.	Brasch J et al.	—	2019	→
A chelicerate-specific burst of nonclassical Dscam diversity.	Cao G et al.	—	2018	→
A copy number variation generated by complicated organization of PCDHA gene cluster is associated with egg performance traits in Xinhua E-strain.	Huang T et al.	—	2018	→
A Dendritic Guidance Receptor Complex Brings Together Distinct Actin Regulators to Drive Efficient F-Actin Assembly and Branching.	Zou W et al.	—	2018	→
A Dense Starburst Plexus Is Critical for Generating Direction Selectivity.	Morrie RD et al.	—	2018	→
Alpha protocadherins and Pyk2 kinase regulate cortical neuron migration and cytoskeletal dynamics via Rac1 GTPase and WAVE complex in mice.	Fan L et al.	—	2018	→
Assembly and maintenance of GABAergic and Glycinergic circuits in the mammalian nervous system.	Gamlin CR et al.	—	2018	→
Bistratified starburst amacrine cells in Sox2 conditional knockout mouse retina display ON and OFF responses.	Stincic TL et al.	—	2018	→
Cadherin Combinations Recruit Dendrites of Distinct Retinal Neurons to a Shared Interneuronal Scaffold.	Duan X et al.	—	2018	→
Combinatorial Effects of Alpha- and Gamma-Protocadherins on Neuronal Survival and Dendritic Self-Avoidance.	Ing-Esteves S et al.	—	2018	→
Dendritic Self-Avoidance and Morphological Development of Cerebellar Purkinje Cells.	Fujishima K et al.	—	2018	→
DL-3-n-butylphthalide promotes dendrite development in cortical neurons subjected to oxygen-glucose deprivation/reperfusion.	Zhang P et al.	—	2018	→
DSCAM promotes self-avoidance in the developing mouse retina by masking the functions of cadherin superfamily members.	Garrett AM et al.	—	2018	→
Expression and Roles of the Immunoglobulin Superfamily Recognition Molecule Sidekick1 in Mouse Retina.	Yamagata M et al.	—	2018	→
Functional analysis of cell-free RNA using mid-trimester amniotic fluid supernatant in pregnancy with the fetal growth restriction.	Cho HY et al.	—	2018	→
Gene expression profile analysis of aortic vascular smooth muscle cells reveals upregulation of cadherin genes in myocardial infarction patients.	Derda AA et al.	—	2018	→
Genomic responses to selection for tame/aggressive behaviors in the silver fox (<i>Vulpes vulpes</i>).	Wang X et al.	—	2018	→
<i>Drosophila</i> Sidekick is required in developing photoreceptors to enable visual motion detection.	Astigarraga S et al.	—	2018	→
Interactions between the Ig-Superfamily Proteins DIP-α and Dpr6/10 Regulate Assembly of Neural Circuits.	Xu S et al.	—	2018	→
Molecular diversity of clustered protocadherin-α required for sensory integration and short-term memory in mice.	Yamagishi T et al.	—	2018	→
Molecular mechanisms underlying monosynaptic sensory-motor circuit development in the spinal cord.	Imai F et al.	—	2018	→
MTSS1 Regulation of Actin-Nucleating Formin DAAM1 in Dendritic Filopodia Determines Final Dendritic Configuration of Purkinje Cells.	Kawabata Galbraith K et al.	—	2018	→
Neural architecture: from cells to circuits.	Richards SEV et al.	—	2018	→
Overexpression of protocadherin 7 inhibits neuronal survival by downregulating BIRC5 in vitro.	Xiao H et al.	—	2018	→
Recent advances in branching mechanisms underlying neuronal morphogenesis.	Menon S et al.	—	2018	→
Regulated Alternative Splicing of <i>Drosophila Dscam2</i> Is Necessary for Attaining the Appropriate Number of Photoreceptor Synapses.	Kerwin SK et al.	—	2018	→
Ret and Substrate-Derived TGF-β Maverick Regulate Space-Filling Dendrite Growth in Drosophila Sensory Neurons.	Hoyer N et al.	—	2018	→
Tissue-specific activities of the Fat1 cadherin cooperate to control neuromuscular morphogenesis.	Helmbacher F	—	2018	→
Tuning of delta-protocadherin adhesion through combinatorial diversity.	Bisogni AJ et al.	—	2018	→
Writing, Reading, and Translating the Clustered Protocadherin Cell Surface Recognition Code for Neural Circuit Assembly.	Mountoufaris G et al.	—	2018	→
A crossroad of neuronal diversity to build circuitry.	Yoshinaga S et al.	—	2017	→
A protocadherin gene cluster regulatory variant is associated with nicotine withdrawal and the urge to smoke.	Jensen KP et al.	—	2017	→
Cellular and Molecular Analysis of Dendritic Morphogenesis in a Retinal Cell Type That Senses Color Contrast and Ventral Motion.	Liu J et al.	—	2017	→
Clustered Protocadherins Are Required for Building Functional Neural Circuits.	Hasegawa S et al.	—	2017	→
Clustered protocadherin trafficking.	Phillips GR et al.	—	2017	→
Dendro-dendritic cholinergic excitation controls dendritic spike initiation in retinal ganglion cells.	Brombas A et al.	—	2017	→
DSCAM-mediated control of dendritic and axonal arbor outgrowth enforces tiling and inhibits synaptic plasticity.	Simmons AB et al.	—	2017	→
Establishing Wiring Specificity in Visual System Circuits: From the Retina to the Brain.	Zhang C et al.	—	2017	→
HIDE Probes: A New Toolkit for Visualizing Organelle Dynamics, Longer and at Super-Resolution.	Thompson AD et al.	—	2017	→
Long-term alterations to DNA methylation as a biomarker of prenatal alcohol exposure: From mouse models to human children with fetal alcohol spectrum disorders.	Laufer BI et al.	—	2017	→
Long-Term Live-Cell STED Nanoscopy of Primary and Cultured Cells with the Plasma Membrane HIDE Probe DiI-SiR.	Thompson AD et al.	—	2017	→
Mechanisms regulating dendritic arbor patterning.	Ledda F et al.	—	2017	→
Multicluster Pcdh diversity is required for mouse olfactory neural circuit assembly.	Mountoufaris G et al.	—	2017	→
Neuronal territory formation by the atypical cadherins and clustered protocadherins.	Lefebvre JL	—	2017	→
Pcdhαc2 is required for axonal tiling and assembly of serotonergic circuitries in mice.	Chen WV et al.	—	2017	→
Programmable disorder in random DNA tilings.	Tikhomirov G et al.	—	2017	→
Protocadherin <i>cis</i>-dimer architecture and recognition unit diversity.	Goodman KM et al.	—	2017	→
Protocadherin-αC2 is required for diffuse projections of serotonergic axons.	Katori S et al.	—	2017	→
Regulation of neural circuit formation by protocadherins.	Peek SL et al.	—	2017	→
Regulatory Features for Odorant Receptor Genes in the Mouse Genome.	Degl'Innocenti A et al.	—	2017	→
Replicable Expansion and Differentiation of Neural Precursors from Adult Canine Skin.	Duncan T et al.	—	2017	→
Structural origins of clustered protocadherin-mediated neuronal barcoding.	Rubinstein R et al.	—	2017	→
Wiring visual systems: common and divergent mechanisms and principles.	Kolodkin AL et al.	—	2017	→
γ-Protocadherins Interact with Neuroligin-1 and Negatively Regulate Dendritic Spine Morphogenesis.	Molumby MJ et al.	—	2017	→
δ-Protocadherins: Organizers of neural circuit assembly.	Light SEW et al.	—	2017	→
Aberrant expression and functions of protocadherins in human malignant tumors.	Shan M et al.	—	2016	→
A large family of Dscam genes with tandemly arrayed 5' cassettes in Chelicerata.	Yue Y et al.	—	2016	→
Alteration of Gene Expression, DNA Methylation, and Histone Methylation in Free Radical Scavenging Networks in Adult Mouse Hippocampus following Fetal Alcohol Exposure.	Chater-Diehl EJ et al.	—	2016	→
A multi-protein receptor-ligand complex underlies combinatorial dendrite guidance choices in <i>C. elegans</i>.	Zou W et al.	—	2016	→
Antiparallel protocadherin homodimers use distinct affinity- and specificity-mediating regions in cadherin repeats 1-4.	Nicoludis JM et al.	—	2016	→
A transducible nuclear/nucleolar protein, mLLP, regulates neuronal morphogenesis and synaptic transmission.	Yu NK et al.	—	2016	→
Consensus Paper: Cerebellar Development.	Leto K et al.	—	2016	→
CRISPR Double Cutting through the Labyrinthine Architecture of 3D Genomes.	Huang H et al.	—	2016	→
Development of synaptic connectivity in the retinal direction selective circuit.	Morrie RD et al.	—	2016	→
Distinct and Cooperative Functions for the <i>Protocadherin</i>-α, -β and -γ Clusters in Neuronal Survival and Axon Targeting.	Hasegawa S et al.	—	2016	→
Duplication of a Single Neuron in C. elegans Reveals a Pathway for Dendrite Tiling by Mutual Repulsion.	Yip ZC et al.	—	2016	→
Emerging Roles of Filopodia and Dendritic Spines in Motoneuron Plasticity during Development and Disease.	Kanjhan R et al.	—	2016	→
Epidermis-Derived Semaphorin Promotes Dendrite Self-Avoidance by Regulating Dendrite-Substrate Adhesion in Drosophila Sensory Neurons.	Meltzer S et al.	—	2016	→
Epigenetic dysregulation in the developing Down syndrome cortex.	El Hajj N et al.	—	2016	→
Establishment of high reciprocal connectivity between clonal cortical neurons is regulated by the Dnmt3b DNA methyltransferase and clustered protocadherins.	Tarusawa E et al.	—	2016	→
Functional impact of splice isoform diversity in individual cells.	Yap K et al.	—	2016	→
Functional test of PCDHB11, the most human-specific neuronal surface protein.	de Freitas GB et al.	—	2016	→
High-specificity bioinformatics framework for epigenomic profiling of discordant twins reveals specific and shared markers for ACPA and ACPA-positive rheumatoid arthritis.	Gomez-Cabrero D et al.	—	2016	→
Histone and DNA Modifications as Regulators of Neuronal Development and Function.	Lomvardas S et al.	—	2016	→
Homophilic Protocadherin Cell-Cell Interactions Promote Dendrite Complexity.	Molumby MJ et al.	—	2016	→
Replacing the PDZ-interacting C-termini of DSCAM and DSCAML1 with epitope tags causes different phenotypic severity in different cell populations.	Garrett AM et al.	—	2016	→
Specification of synaptic connectivity by cell surface interactions.	de Wit J et al.	—	2016	→
Structural Basis of Diverse Homophilic Recognition by Clustered α- and β-Protocadherins.	Goodman KM et al.	—	2016	→
Structural basis of Dscam1 homodimerization: Insights into context constraint for protein recognition.	Li SA et al.	—	2016	→
Structural determinants of adhesion by Protocadherin-19 and implications for its role in epilepsy.	Cooper SR et al.	—	2016	→
The γ-Protocadherin-C3 isoform inhibits canonical Wnt signalling by binding to and stabilizing Axin1 at the membrane.	Mah KM et al.	—	2016	→
What's Luck Got to Do with It: Single Cells, Multiple Fates, and Biological Nondeterminism.	Symmons O et al.	—	2016	→
γ-Protocadherin structural diversity and functional implications.	Goodman KM et al.	—	2016	→
Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5-Drl signaling pathway.	Yasunaga K et al.	—	2015	→
Alternative Splicing in the Mammalian Nervous System: Recent Insights into Mechanisms and Functional Roles.	Raj B et al.	—	2015	→
Associative DNA methylation changes in children with prenatal alcohol exposure.	Laufer BI et al.	—	2015	→
Beyond Molecular Codes: Simple Rules to Wire Complex Brains.	Hassan BA et al.	—	2015	→
Cadherin-8 expression, synaptic localization, and molecular control of neuronal form in prefrontal corticostriatal circuits.	Friedman LG et al.	—	2015	→
Cadherin-based transsynaptic networks in establishing and modifying neural connectivity.	Friedman LG et al.	—	2015	→
CRISPR Inversion of CTCF Sites Alters Genome Topology and Enhancer/Promoter Function.	Guo Y et al.	—	2015	→
Design principles and developmental mechanisms underlying retinal mosaics.	Reese BE et al.	—	2015	→
Development of dendritic form and function.	Lefebvre JL et al.	—	2015	→
DSCAM promotes refinement in the mouse retina through cell death and restriction of exploring dendrites.	Li S et al.	—	2015	→
Emerging roles of protocadherins: from self-avoidance to enhancement of motility.	Hayashi S et al.	—	2015	→
Epigenetic events regulating monoallelic gene expression.	Massah S et al.	—	2015	→
Genetic Mapping in Mice Reveals the Involvement of Pcdh9 in Long-Term Social and Object Recognition and Sensorimotor Development.	Bruining H et al.	—	2015	→
Ig Superfamily Ligand and Receptor Pairs Expressed in Synaptic Partners in Drosophila.	Tan L et al.	—	2015	→
Impaired clustered protocadherin-α leads to aggregated retinogeniculate terminals and impaired visual acuity in mice.	Meguro R et al.	—	2015	→
Intrinsic and extrinsic mechanisms of dendritic morphogenesis.	Dong X et al.	—	2015	→
Molecular logic of neuronal self-recognition through protocadherin domain interactions.	Rubinstein R et al.	—	2015	→
Monoallelic expression of the human FOXP2 speech gene.	Adegbola AA et al.	—	2015	→
mTORC1 and mTORC2 have largely distinct functions in Purkinje cells.	Angliker N et al.	—	2015	→
Multicolor analysis of oligodendrocyte morphology, interactions, and development with Brainbow.	Dumas L et al.	—	2015	→
Neuronal cell-type-specific alternative splicing: A mechanism for specifying connections in the brain?	Li JS et al.	—	2015	→
Protein Kinase C Phosphorylation of a γ-Protocadherin C-terminal Lipid Binding Domain Regulates Focal Adhesion Kinase Inhibition and Dendrite Arborization.	Keeler AB et al.	—	2015	→
Protocadherin-9 involvement in retinal development in Xenopus laevis.	Izuta Y et al.	—	2015	→
Protocadherin-dependent dendritic self-avoidance regulates neural connectivity and circuit function.	Kostadinov D et al.	—	2015	→
Protocadherins and hypothalamic development: do they play an unappreciated role?	Coughlin GM et al.	—	2015	→
Protocadherins branch out: Multiple roles in dendrite development.	Keeler AB et al.	—	2015	→
Quantitative comparison of a human cancer cell surface proteome between interphase and mitosis.	Özlü N et al.	—	2015	→
Regulation of dendrite morphogenesis by extrinsic cues.	Valnegri P et al.	—	2015	→
Self-awareness in the retina.	Garrett AM et al.	—	2015	→
Sidekick 2 directs formation of a retinal circuit that detects differential motion.	Krishnaswamy A et al.	—	2015	→
Structure and Sequence Analyses of Clustered Protocadherins Reveal Antiparallel Interactions that Mediate Homophilic Specificity.	Nicoludis JM et al.	—	2015	→
The classic cadherins in synaptic specificity.	Basu R et al.	—	2015	→
The clustered protocadherin endolysosomal trafficking motif mediates cytoplasmic association.	Shonubi A et al.	—	2015	→
The Dendritic Differentiation of Purkinje Neurons: Unsolved Mystery in Formation of Unique Dendrites.	Tanaka M	—	2015	→
The Independent Probabilistic Firing of Transcription Factors: A Paradigm for Clonal Variability in the Zebrafish Retina.	Boije H et al.	—	2015	→
The Ret receptor regulates sensory neuron dendrite growth and integrin mediated adhesion.	Soba P et al.	—	2015	→
The role of cell adhesion molecules in visual circuit formation: from neurite outgrowth to maps and synaptic specificity.	Missaire M et al.	—	2015	→
The unfolded protein response is required for dendrite morphogenesis.	Wei X et al.	—	2015	→
A critical period defined by axon-targeting mechanisms in the murine olfactory bulb.	Tsai L et al.	—	2014	→
Adhesion networks of cnidarians: a postgenomic view.	Tucker RP et al.	—	2014	→
Cell-intrinsic requirement of Dscam1 isoform diversity for axon collateral formation.	He H et al.	—	2014	→
Dendrite self-avoidance requires cell-autonomous slit/robo signaling in cerebellar purkinje cells.	Gibson DA et al.	—	2014	→
Developmental epigenetic modification regulates stochastic expression of clustered protocadherin genes, generating single neuron diversity.	Toyoda S et al.	—	2014	→
Developmental localization of adhesion and scaffolding proteins at the cone synapse.	Nuhn JS et al.	—	2014	→
Development of retinal layers.	Nguyen-Ba-Charvet KT et al.	—	2014	→
Development of the embryonic and larval peripheral nervous system of Drosophila.	Singhania A et al.	—	2014	→
Expansion of stochastic expression repertoire by tandem duplication in mouse Protocadherin-α cluster.	Kaneko R et al.	—	2014	→
Functional architecture of the retina: development and disease.	Hoon M et al.	—	2014	→
Heterochromatin-mediated gene silencing facilitates the diversification of olfactory neurons.	Lyons DB et al.	—	2014	→
Heterogeneity in immune responses: from populations to single cells.	Satija R et al.	—	2014	→
High frequency of rare variants with a moderate-to-high predicted biological effect in protocadherin genes of extremely obese.	Mariman EC et al.	—	2014	→
LKB1 and AMPK regulate synaptic remodeling in old age.	Samuel MA et al.	—	2014	→
Loop formation and self-fasciculation of cortical axon using photonic guidance at long working distance.	Mondal A et al.	—	2014	→
Neuronal cell types and connectivity: lessons from the retina.	Seung HS et al.	—	2014	→
Nuclear architecture as an epigenetic regulator of neural development and function.	Alexander JM et al.	—	2014	→
Photoreceptor-derived activin promotes dendritic termination and restricts the receptive fields of first-order interneurons in Drosophila.	Ting CY et al.	—	2014	→
Polymorphic receptors: neuronal functions and molecular mechanisms of diversification.	Schreiner D et al.	—	2014	→
proBDNF negatively regulates neuronal remodeling, synaptic transmission, and synaptic plasticity in hippocampus.	Yang J et al.	—	2014	→
Protocadherin-17 mediates collective axon extension by recruiting actin regulator complexes to interaxonal contacts.	Hayashi S et al.	—	2014	→
Regulation of cadherin expression in nervous system development.	Paulson AF et al.	—	2014	→
Regulation of the protocadherin Celsr3 gene and its role in globus pallidus development and connectivity.	Jia Z et al.	—	2014	→
Roles for DSCAM and DSCAML1 in central nervous system development and disease.	Montesinos ML	—	2014	→
Single-cell identity generated by combinatorial homophilic interactions between α, β, and γ protocadherins.	Thu CA et al.	—	2014	→
So many pieces, one puzzle: cell type specification and visual circuitry in flies and mice.	Wernet MF et al.	—	2014	→
Sorting out a promiscuous superfamily: towards cadherin connectomics.	Sotomayor M et al.	—	2014	→
Sox2 regulates cholinergic amacrine cell positioning and dendritic stratification in the retina.	Whitney IE et al.	—	2014	→
Spatio-temporally restricted expression of cell adhesion molecules during chicken embryonic development.	Roy P et al.	—	2014	→
The biology of boundary conditions: cellular reconstitution in one, two, and three dimensions.	Vahey MD et al.	—	2014	→
Type II cadherins guide assembly of a direction-selective retinal circuit.	Duan X et al.	—	2014	→
An epigenetic trap involved in olfactory receptor gene choice.	Reinsborough C et al.	—	2013	→
An extracellular adhesion molecule complex patterns dendritic branching and morphogenesis.	Dong X et al.	—	2013	→
Cell-specific cre recombinase expression allows selective ablation of glutamate receptors from mouse horizontal cells.	Ströh S et al.	—	2013	→
Clustered protocadherins.	Chen WV et al.	—	2013	→
Contributions of VLDLR and LRP8 in the establishment of retinogeniculate projections.	Su J et al.	—	2013	→
Coupling of NF-protocadherin signaling to axon guidance by cue-induced translation.	Leung LC et al.	—	2013	→
Dendritic self-avoidance: protocadherins have it covered.	Hoang P et al.	—	2013	→
Gap junction-dependent homolog avoidance in the developing CNS.	Baker MW et al.	—	2013	→
Genetic basis of neuronal individuality in the mammalian brain.	Yagi T	—	2013	→
IGSF9 family proteins.	Hansen M et al.	—	2013	→
Maturation of postnatally generated olfactory bulb granule cells depends on functional γ-protocadherin expression.	Ledderose J et al.	—	2013	→
Motor axon regeneration and muscle reinnervation in young adult and aged animals.	Kang H et al.	—	2013	→
Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain.	Hughes EG et al.	—	2013	→
On and off retinal circuit assembly by divergent molecular mechanisms.	Sun LO et al.	—	2013	→
On eukaryotic intelligence: signaling system's guidance in the evolution of multicellular organization.	Marijuán PC et al.	—	2013	→
Probabilistic splicing of Dscam1 establishes identity at the level of single neurons.	Miura SK et al.	—	2013	→
Protocadherins, not prototypical: a complex tale of their interactions, expression, and functions.	Weiner JA et al.	—	2013	→
Regulation of dendritic filopodial interactions by ZO-1 and implications for dendrite morphogenesis.	Komaki R et al.	—	2013	→
Role of self-avoidance in neuronal wiring.	Kise Y et al.	—	2013	→
Self-contact elimination by membrane fusion.	Sumida GM et al.	—	2013	→
Self-referential forces are sufficient to explain different dendritic morphologies.	Memelli H et al.	—	2013	→
Stochastic gene expression in mammals: lessons from olfaction.	Magklara A et al.	—	2013	→
Structural and molecular interrogation of intact biological systems.	Chung K et al.	—	2013	→
Synaptic laminae in the visual system: molecular mechanisms forming layers of perception.	Baier H	—	2013	→
The molecular basis of self-avoidance.	Zipursky SL et al.	—	2013	→
The neuron identity problem: form meets function.	Fishell G et al.	—	2013	→
Turning single cells into microarrays by super-resolution barcoding.	Cai L	—	2013	→
Ultra-deep profiling of alternatively spliced Drosophila Dscam isoforms by circularization-assisted multi-segment sequencing.	Sun W et al.	—	2013	→
Visual circuit assembly requires fine tuning of the novel Ig transmembrane protein Borderless.	Cameron S et al.	—	2013	→
A novel mouse Dscam mutation inhibits localization and shedding of DSCAM.	Schramm RD et al.	—	2012	→
CTCF/cohesin-mediated DNA looping is required for protocadherin α promoter choice.	Guo Y et al.	—	2012	→
Functional significance of isoform diversification in the protocadherin gamma gene cluster.	Chen WV et al.	—	2012	→
Gene pioneers: Donald Brown and Thomas Maniatis win the 2012 Lasker~Koshland Special Achievement Award in Medical Science.	Claiborn K	—	2012	→
High-resolution in vivo imaging of regenerating dendrites of Drosophila sensory neurons during metamorphosis: local filopodial degeneration and heterotypic dendrite-dendrite contacts.	Satoh D et al.	—	2012	→
Molecular and functional interaction between protocadherin-γC5 and GABAA receptors.	Li Y et al.	—	2012	→