Regulation of dendrite morphogenesis by extrinsic cues

Dendrites play a central role in the integration and flow of information in the nervous system. The morphogenesis and maturation of dendrites is hence an essential step in the establishment of neuronal connectivity. Recent studies have uncovered crucial functions for extrinsic cues in the development of dendrites. We review the contribution of secreted polypeptide growth factors, contact-mediated proteins, and neuronal activity in distinct phases of dendrite development. We also highlight how extrinsic cues influence local and global intracellular mechanisms of dendrite morphogenesis. Finally, we discuss how these studies have advanced our understanding of neuronal connectivity and have shed light on the pathogenesis of neurodevelopmental disorders.

[1]  T. Tu,et al.  Generation and Behavior Characterization of CaMKIIβ Knockout Mice , 2014, PloS one.

[2]  Judit K. Makara,et al.  Compartmentalized dendritic plasticity and input feature storage in neurons , 2008, Nature.

[3]  Karl Deisseroth,et al.  Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology , 2001, Nature Neuroscience.

[4]  Li-Huei Tsai,et al.  Erratum: Autism spectrum disorder susceptibility gene TAOK2 affects basal dendrite formation in the neocortex (Nature Neuroscience (2012) 15 (1022-1031)) , 2014 .

[5]  John B. Thomas,et al.  Wnt-mediated axon guidance via the Drosophila Derailed receptor , 2003, Nature.

[6]  K. Shen,et al.  UNC-6 and UNC-40 promote dendritic growth through PAR-4 in Caenorhabditis elegans neurons , 2011, Nature Neuroscience.

[7]  Mu-ming Poo,et al.  Semaphorin3A Regulates Neuronal Polarization by Suppressing Axon Formation and Promoting Dendrite Growth , 2011, Neuron.

[8]  A. Bonni,et al.  Transcriptional Regulation of Neuronal Polarity and Morphogenesis in the Mammalian Brain , 2011, Neuron.

[9]  M. Sahin,et al.  EphA7 signaling guides cortical dendritic development and spine maturation , 2014, Proceedings of the National Academy of Sciences.

[10]  A. Chiba,et al.  Robo and Frazzled/DCC mediate dendritic guidance at the CNS midline , 2003, Nature Neuroscience.

[11]  Tudor C. Badea,et al.  Transmembrane semaphorin signaling controls laminar stratification in the mammalian retina , 2010, Nature.

[12]  Yu-Chih Lin,et al.  CaMKIIβ binding to stable F-actin in vivo regulates F-actin filament stability , 2008, Proceedings of the National Academy of Sciences.

[13]  V. Abraira,et al.  Control of Neuronal Morphology by the Atypical Cadherin Fat3 , 2011, Neuron.

[14]  Y. Sogawa,et al.  Investigation of the Ca(2+)-independent form of Ca(2+)/calmodulin-dependent protein kinase II in neurite outgrowth. , 2001, Brain research. Brain research protocols.

[15]  J. Hell,et al.  CaMKII: Claiming Center Stage in Postsynaptic Function and Organization , 2014, Neuron.

[16]  Y. Choe,et al.  Wnt5a controls neurite development in olfactory bulb interneurons , 2011, ASN neuro.

[17]  Suya Sun,et al.  A dual-shaping mechanism for postsynaptic ephrin-B3 as a receptor that sculpts dendrites and synapses , 2011, Nature Neuroscience.

[18]  R. Rodriguiz,et al.  Cerebellar Defects in Ca2+/Calmodulin Kinase IV-Deficient Mice , 2000, The Journal of Neuroscience.

[19]  A. Davies,et al.  Growth differentiation factor 5 is a key physiological regulator of dendrite growth during development , 2013, Development.

[20]  A. Bonni,et al.  Cell-intrinsic drivers of dendrite morphogenesis , 2013, Development.

[21]  Patrick R Hof,et al.  Changes in the structural complexity of the aged brain , 2007, Aging cell.

[22]  Tobias Meyer,et al.  Selective Regulation of Neurite Extension and Synapse Formation by the β but not the α Isoform of CaMKII , 2003, Neuron.

[23]  Yasunori Hayashi,et al.  The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure , 2007, Proceedings of the National Academy of Sciences.

[24]  J. Sanes,et al.  Dendrite Self-Avoidance Requires Cell-Autonomous Slit/Robo Signaling in Cerebellar Purkinje Cells , 2014, Neuron.

[25]  A. Bonni,et al.  Novel functions for the anaphase-promoting complex in neurobiology. , 2011, Seminars in cell & developmental biology.

[26]  Yasuyuki Shima,et al.  Opposing roles in neurite growth control by two seven-pass transmembrane cadherins , 2007, Nature Neuroscience.

[27]  E. Pasquale.  Developmental cell biology: Eph receptor signalling casts a wide net on cell behaviour , 2005, Nature Reviews Molecular Cell Biology.

[28]  S. Gygi,et al.  A Unique CaMKIIβ Signaling Pathway at the Centrosome Regulates Dendrite Patterning in the Brain , 2011, Nature Neuroscience.

[29]  J. C. Clemens,et al.  Alternative Splicing of Drosophila Dscam Generates Axon Guidance Receptors that Exhibit Isoform-Specific Homophilic Binding , 2004, Cell.

[30]  W. Cowan,et al.  The organization of certain afferents to the hippocampus and dentate gyrus in normal and reeler mice , 1979, The Journal of comparative neurology.

[31]  D. Hall,et al.  The Fusogen EFF-1 Controls Sculpting of Mechanosensory Dendrites , 2010, Science.

[32]  K. Shen,et al.  The transmembrane leucine-rich repeat protein DMA-1 promotes dendrite branching and growth in C. elegans , 2011, Nature Neuroscience.

[33]  Tom Maniatis,et al.  PROTOCADHERINS MEDIATE DENDRITIC SELF-AVOIDANCE IN THE MAMMALIAN NERVOUS SYSTEM , 2012, Nature.

[34]  G. Corfas,et al.  A TRPC5-regulated calcium signaling pathway controls dendrite patterning in the mammalian brain. , 2011, Genes & development.

[35]  L. Attisano,et al.  p21-Activated kinase (PAK) is required for Bone Morphogenetic Protein (BMP)-induced dendritogenesis in cortical neurons , 2013, Molecular and Cellular Neuroscience.

[36]  Michal Rivlin-Etzion,et al.  On and Off Retinal Circuit Assembly by Divergent Molecular Mechanisms , 2013, Science.

[37]  T. Yagi,et al.  Fyn and Cdk5 Mediate Semaphorin-3A Signaling, Which Is Involved in Regulation of Dendrite Orientation in Cerebral Cortex , 2002, Neuron.

[38]  R. Wong,et al.  Activity-dependent regulation of dendritic growth and patterning , 2002, Nature Reviews Neuroscience.

[39]  E. Huang,et al.  Trk receptors: roles in neuronal signal transduction. , 2003, Annual review of biochemistry.

[40]  Chih-Hao Hsu,et al.  Identification and characterization of three inherited genomic copy number variations associated with familial schizophrenia , 2012, Schizophrenia Research.

[41]  G. Ming,et al.  Class 3 Semaphorin Mediates Dendrite Growth in Adult Newborn Neurons through Cdk5/FAK Pathway , 2013, PloS one.

[42]  L. Luo,et al.  Dendrite morphogenesis depends on relative levels of NT-3/TrkC signaling , 2014, Science.

[43]  Julie H. Simpson,et al.  Ectopic Expression in the Giant Fiber System ofDrosophila Reveals Distinct Roles for Roundabout (Robo), Robo2, and Robo3 in Dendritic Guidance and Synaptic Connectivity , 2002, The Journal of Neuroscience.

[44]  Jeffrey L Goldberg,et al.  Intrinsic neuronal regulation of axon and dendrite growth , 2004, Current Opinion in Neurobiology.

[45]  L. Fradkin,et al.  Wnt5 and Drl/Ryk Gradients Pattern the Drosophila Olfactory Dendritic Map , 2014, The Journal of Neuroscience.

[46]  J. C. Clemens,et al.  Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe , 2006, Nature Neuroscience.

[47]  C. Quattrocchi,et al.  Reelin Promotes Hippocampal Dendrite Development through the VLDLR/ApoER2-Dab1 Pathway , 2004, Neuron.

[48]  B. Chait,et al.  Proteomic Studies of a Single CNS Synapse Type: The Parallel Fiber/Purkinje Cell Synapse , 2009, PLoS biology.

[49]  Alcino J. Silva,et al.  Calmodulin-Kinases: Modulators of Neuronal Development and Plasticity , 2008, Neuron.

[50]  E. Lasda,et al.  CaMKIIbeta association with the actin cytoskeleton is regulated by alternative splicing. , 2006, Molecular biology of the cell.

[51]  J. C. Clemens,et al.  Dendrite Self-Avoidance Is Controlled by Dscam , 2007, Cell.

[52]  C. Goodman,et al.  Regulation of Cortical Dendrite Development by Slit-Robo Interactions , 2002, Neuron.

[53]  Yasuyuki Shima,et al.  Regulation of dendritic maintenance and growth by a mammalian 7-pass transmembrane cadherin. , 2004, Developmental cell.

[54]  Azad Bonni,et al.  A CaMKII-NeuroD Signaling Pathway Specifies Dendritic Morphogenesis , 2004, Neuron.

[55]  C. Deng,et al.  Dendrite Complexity of Sympathetic Neurons Is Controlled during Postnatal Development by BMP Signaling , 2013, The Journal of Neuroscience.

[56]  M. McCarthy,et al.  A Survey of Genomic Studies Supports Association of Circadian Clock Genes with Bipolar Disorder Spectrum Illnesses and Lithium Response , 2012, PloS one.

[57]  Hannes E. Bülow,et al.  Skin-Derived Cues Control Arborization of Sensory Dendrites in Caenorhabditis elegans , 2013, Cell.

[58]  Anirvan Ghosh,et al.  Calcium Regulation of Dendritic Growth via CaM Kinase IV and CREB-Mediated Transcription , 2002, Neuron.

[59]  Y. Jan,et al.  Control of Dendritic Field Formation in Drosophila The Roles of Flamingo and Competition between Homologous Neurons , 2000, Neuron.

[60]  E. Huang,et al.  Neurotrophins: roles in neuronal development and function. , 2001, Annual review of neuroscience.

[61]  K. Shimono,et al.  The seven-pass transmembrane cadherin Flamingo controls dendritic self-avoidance via its binding to a LIM domain protein, Espinas, in Drosophila sensory neurons. , 2011, Genes & development.

[62]  Daniel A. Colón-Ramos,et al.  Netrin (UNC-6) mediates dendritic self-avoidance , 2012, Nature Neuroscience.

[63]  S. Grant,et al.  Molecular characterization and comparison of the components and multiprotein complexes in the postsynaptic proteome , 2006, Journal of neurochemistry.

[64]  M. Kondo,et al.  Homophilic Dscam Interactions Control Complex Dendrite Morphogenesis , 2007, Neuron.

[65]  E. Stein,et al.  DSCAM Contributes to Dendrite Arborization and Spine Formation in the Developing Cerebral Cortex , 2012, The Journal of Neuroscience.

[66]  B. Matthews,et al.  Dscam1-Mediated Self-Avoidance Counters Netrin-Dependent Targeting of Dendrites in Drosophila , 2011, Current Biology.

[67]  H. Bading,et al.  Nuclear Calcium-VEGFD Signaling Controls Maintenance of Dendrite Arborization Necessary for Memory Formation , 2011, Neuron.

[68]  Y. Jan,et al.  Integrins Regulate Repulsion-Mediated Dendritic Patterning of Drosophila Sensory Neurons by Restricting Dendrites in a 2D Space , 2012, Neuron.

[69]  A. Alonso,et al.  Signaling Mechanisms Underlying Reversible, Activity-Dependent Dendrite Formation , 2002, Neuron.

[70]  Michelle E. Kim,et al.  Integrins Establish Dendrite-Substrate Relationships that Promote Dendritic Self-Avoidance and Patterning in Drosophila Sensory Neurons , 2012, Neuron.

[71]  B. Chen,et al.  Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes. , 2009, Genes & development.

[72]  Yasuyuki Shima,et al.  Flamingo, a Seven-Pass Transmembrane Cadherin, Regulates Planar Cell Polarity under the Control of Frizzled , 1999, Cell.

[73]  Tzumin Lee,et al.  Drosophila Sensory Neurons Require Dscam for Dendritic Self-Avoidance and Proper Dendritic Field Organization , 2007, Neuron.

[74]  Xintong Dong,et al.  An Extracellular Adhesion Molecule Complex Patterns Dendritic Branching and Morphogenesis , 2013, Cell.

[75]  M. Marr,et al.  CaMKII-Dependent Phosphorylation of the GTPase Rem2 Is Required to Restrict Dendritic Complexity , 2013, The Journal of Neuroscience.

[76]  Masahito Yamagata,et al.  Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina , 2008, Nature.

[77]  L. Luo,et al.  Secreted Semaphorins from Degenerating Larval ORN Axons Direct Adult Projection Neuron Dendrite Targeting , 2011, Neuron.

[78]  Li-Huei Tsai,et al.  Autism spectrum disorder susceptibility gene TAOK2 affects basal dendrite formation in the neocortex , 2012, Nature Neuroscience.

[79]  S. Maeda,et al.  Semaphorin 3A induces CaV2.3 channel-dependent conversion of axons to dendrites , 2011, Nature Cell Biology.

[80]  D. Schreiner,et al.  γ-Protocadherins Control Cortical Dendrite Arborization by Regulating the Activity of a FAK/PKC/MARCKS Signaling Pathway , 2012, Neuron.

[81]  L. Luo,et al.  Graded Expression of Semaphorin-1a Cell-Autonomously Directs Dendritic Targeting of Olfactory Projection Neurons , 2007, Cell.

[82]  Kazuo Emoto,et al.  Compartmentalized Calcium Transients Trigger Dendrite Pruning in Drosophila Sensory Neurons , 2013, Science.

[83]  A. Wynshaw-Boris,et al.  Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development , 2005, Nature Neuroscience.

[84]  Y. Kohmura,et al.  Dendritic planarity of Purkinje cells is independent of Reelin signaling , 2014, Brain Structure and Function.

[85]  J. Massagué,et al.  Transcriptional control by the TGF‐β/Smad signaling system , 2000 .

[86]  D. Hwang,et al.  Altered branching patterns of Purkinje cells in mouse model for cortical development disorder , 2011, Scientific reports.

[87]  D. Lo,et al.  Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth , 2000, Nature Neuroscience.

[88]  Hugo W. Moser,et al.  Dendritic Anomalies in Disorders Associated with Mental Retardation , 2000 .

[89]  S. Siegelbaum,et al.  Reelin Signaling Specifies the Molecular Identity of the Pyramidal Neuron Distal Dendritic Compartment , 2014, Cell.

[90]  Lawrence C. Katz,et al.  Neurotrophins regulate dendritic growth in developing visual cortex , 1995, Neuron.

[91]  H. C. Hartzell,et al.  Activity-Dependent Regulation of Dendritic Growth and Maintenance by Glycogen Synthase Kinase 3β , 2013, Nature Communications.

[92]  J. C. Clemens,et al.  Drosophila Dscam Is an Axon Guidance Receptor Exhibiting Extraordinary Molecular Diversity , 2000, Cell.

[93]  M. Stryker,et al.  Cortical Degeneration in the Absence of Neurotrophin Signaling Dendritic Retraction and Neuronal Loss after Removal of the Receptor TrkB , 2000, Neuron.

[94]  Bing Zhou,et al.  Snapin recruits dynein to BDNF-TrkB signaling endosomes for retrograde axonal transport and is essential for dendrite growth of cortical neurons. , 2012, Cell reports.

[95]  A. Bonni,et al.  The ubiquitin receptor S5a/Rpn10 links centrosomal proteasomes with dendrite development in the mammalian brain. , 2013, Cell reports.

[96]  Y. Goshima,et al.  Increased proximal bifurcation of CA1 pyramidal apical dendrites in sema3A mutant mice , 2009, The Journal of comparative neurology.

[97]  Anirvan Ghosh,et al.  Semaphorin 3A is a chemoattractant for cortical apical dendrites , 2000, Nature.

[98]  R. Masland,et al.  Neurite arborization and mosaic spacing in the mouse retina require DSCAM , 2008, Nature.

[99]  N. Heintz,et al.  The adhesion-GPCR BAI3, a gene linked to psychiatric disorders, regulates dendrite morphogenesis in neurons , 2013, Molecular Psychiatry.

[100]  Aaron D. Milstein,et al.  GRIP1 controls dendrite morphogenesis by regulating EphB receptor trafficking , 2005, Nature Neuroscience.