Semaphorin 3A is a chemoattractant for cortical apical dendrites

The apical dendrites of pyramidal neurons integrate inputs from various cortical layers and are central to information processing. Here we show that the growth of apical dendrites towards the pial surface is regulated by a diffusible chemoattractant present at high levels near the marginal zone. A major component of this signal is semaphorin 3A (Sema3A), which was previously characterized as a chemorepellant for cortical axons. Soluble guanylate cyclase is asymmetrically localized to the developing apical dendrite, and is required for the chemoattractive effect of Sema3A. Thus the asymmetric localization of soluble guanylate cyclase confers distinct Sema3A responses to axons and dendrites. These observations reveal a mechanism by which a single chemotropic signal can pattern both axons and dendrites during development.

[1]  A. Kolodkin Semaphorin-mediated neuronal growth cone guidance. , 1998, Progress in brain research.

[2]  C. Goodman,et al.  The Molecular Biology of Axon Guidance , 1996, Science.

[3]  M. Tessier-Lavigne,et al.  Neuropilin Is a Receptor for the Axonal Chemorepellent Semaphorin III , 1997, Cell.

[4]  W. Singer,et al.  Differential patterns of semaphorin expression in the developing rat brain , 1998, The European journal of neuroscience.

[5]  B. Sakmann,et al.  A new cellular mechanism for coupling inputs arriving at different cortical layers , 1999, Nature.

[6]  Alex L Kolodkin,et al.  Neuropilin Is a Semaphorin III Receptor , 1997, Cell.

[7]  C. Parent,et al.  A cell's sense of direction. , 1999, Science.

[8]  A. Ghosh,et al.  Patterning of cortical efferent projections by semaphorin-neuropilin interactions. , 1998, Science.

[9]  Mu-ming Poo,et al.  A Ligand-Gated Association between Cytoplasmic Domains of UNC5 and DCC Family Receptors Converts Netrin-Induced Growth Cone Attraction to Repulsion , 1999, Cell.

[10]  J. Bolz,et al.  Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. , 1998, Development.

[11]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[12]  M. Poo,et al.  Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. , 1998, Science.

[13]  Tomoko Nakanishi,et al.  ‘Green mice’ as a source of ubiquitous green cells , 1997, FEBS letters.

[14]  Alex L Kolodkin,et al.  Neuropilin-2 Is a Receptor for Semaphorin IV Insight into the Structural Basis of Receptor Function and Specificity , 1998, Neuron.

[15]  M. Miller,et al.  Development of Projection and Local Circuit Neurons in Neocortex , 1988 .

[16]  C. Goodman,et al.  Semaphorins III and IV repel hippocampal axons via two distinct receptors. , 1998, Development.

[17]  C. Shatz,et al.  Many Major CNS Axon Projections Develop Normally in the Absence of Semaphorin III , 1998, Molecular and Cellular Neuroscience.

[18]  M. Antonaccio,et al.  Inhibition of adenylate cyclase in human blood platelets by 9-substituted adenine derivatives. , 1979, Journal of cyclic nucleotide research.

[19]  D. Murphy,et al.  G Protein Signaling Events Are Activated at the Leading Edge of Chemotactic Cells , 1998, Cell.

[20]  J. Garthwaite,et al.  Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. , 1995, Molecular pharmacology.

[21]  P. Leder,et al.  The kit ligand: A cell surface molecule altered in steel mutant fibroblasts , 1990, Cell.

[22]  P. Baas Microtubules and Neuronal Polarity Lessons from Mitosis , 1999, Neuron.

[23]  C. Gilbert Microcircuitry of the visual cortex. , 1983, Annual review of neuroscience.

[24]  C. Goodman,et al.  Chimeric Axon Guidance Receptors The Cytoplasmic Domains of Slit and Netrin Receptors Specify Attraction versus Repulsion , 1999, Cell.

[25]  H. Genieser,et al.  (Rp)-8-pCPT-cGMPS, a novel cGMP-dependent protein kinase inhibitor. , 1994, European journal of pharmacology.

[26]  Jeffrey A. Golden,et al.  Semaphorin III is needed for normal patterning and growth of nerves, bones and heart , 1996, Nature.

[27]  G. Fishell,et al.  Striatal precursors adopt cortical identities in response to local cues. , 1995, Development.

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

[29]  K. Robinson,et al.  The coupling of cyclic GMP and photopolarization of Pelvetia zygotes. , 1997, Developmental biology.

[30]  H. Cline,et al.  Stabilization of dendritic arbor structure in vivo by CaMKII. , 1998, Science.