Semaphorin3A/PlexinA3 association with the Scribble scaffold for cGMP increase is required for apical dendrite development

The development of the apical dendrite from the leading process of the bipolar pyramidal neuron might be directed by spatially organized extrinsic cues acting on localized intrinsic determinants. The extracellular cues regulating apical dendrite polarization remain elusive. We show that leading proc...

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Published in	Cell reports (Cambridge) Vol. 38; no. 11; p. 110483
Main Authors	Szczurkowska, Joanna, Guo, Alan, Martin, Jacqueline, Lee, Seong-Il, Martinez, Edward, Chien, Chia Te, Khan, Tamor A., Singh, Ravnit, Dadson, Doreen, Tran, Tracy S., Pautot, Sophie, Shelly, Maya
Format	Journal Article
Language	English
Published	United States Elsevier Inc 15.03.2022
Subjects	apical dendrite development Cells, Cultured cGMP Cyclic GMP Cyclic GMP - metabolism Dendrites Dendrites - metabolism hippocampal CA1 Life Sciences Neurogenesis neuron polarization PlexinA3 protein scaffold Scribble Semaphorin-3A Semaphorin-3A - metabolism Semaphorin-3A - pharmacology Semaphorin3A Semaphorins Semaphorins - metabolism apical dendrite development protein scaffold PlexinA3 Semaphorin3A Scribble hippocampal CA1 cGMP neuron polarization
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ISSN	2211-1247 2211-1247
DOI	10.1016/j.celrep.2022.110483

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Abstract	The development of the apical dendrite from the leading process of the bipolar pyramidal neuron might be directed by spatially organized extrinsic cues acting on localized intrinsic determinants. The extracellular cues regulating apical dendrite polarization remain elusive. We show that leading process and apical dendrite development are directed by class III Semaphorins and mediated by a localized cGMP-synthesizing complex. The scaffolding protein Scribble that associates with the cGMP-synthesizing enzyme soluble guanylate cyclase (sGC) also associates with the Semaphorin3A (Sema3A) co-receptor PlexinA3. Deletion or knockdown of PlexinA3 and Sema3A or disruption of PlexinA3-Scribble association prevents Sema3A-mediated cGMP increase and causes defects in apical dendrite development. These manipulations also impair bipolar polarity and leading process establishment. Local cGMP elevation or sGC expression rescues the effects of PlexinA3 knockdown or PlexinA3-Scribble complex disruption. During neuronal polarization, leading process and apical dendrite development are directed by a scaffold that links Semaphorin cue to cGMP increase. [Display omitted] •Sema3A co-receptor PlexinA3 interacts with the Scribble scaffold for cGMP synthesis•Sema3A/PlexinA3 association with Scribble mediates cGMP increase in dendrites•Sema3A/PlexinA3 mediate bipolar polarity and apical dendrite development via cGMP•Sema3A/PlexinA3-mediated localized cGMP increase may direct leading-edge polarity Szczurkowska et al. show that spatially directed Sema3A may promote development of the leading process and the apical dendrite via the co-receptor PlexinA3 by orchestrating localized cGMP increase on the scaffold protein, Scribble, at the leading edge of developing pyramidal neurons.
AbstractList	The development of the apical dendrite from the leading process of the bipolar pyramidal neuron might be directed by spatially organized extrinsic cues acting on localized intrinsic determinants. The extracellular cues regulating apical dendrite polarization remain elusive. We show that leading process and apical dendrite development are directed by class III Semaphorins and mediated by a localized cGMP-synthesizing complex. The scaffolding protein Scribble that associates with the cGMP-synthesizing enzyme soluble guanylate cyclase (sGC) also associates with the Semaphorin3A (Sema3A) co-receptor PlexinA3. Deletion or knockdown of PlexinA3 and Sema3A or disruption of PlexinA3-Scribble association prevents Sema3A-mediated cGMP increase and causes defects in apical dendrite development. These manipulations also impair bipolar polarity and leading process establishment. Local cGMP elevation or sGC expression rescues the effects of PlexinA3 knockdown or PlexinA3-Scribble complex disruption. During neuronal polarization, leading process and apical dendrite development are directed by a scaffold that links Semaphorin cue to cGMP increase. [Display omitted] •Sema3A co-receptor PlexinA3 interacts with the Scribble scaffold for cGMP synthesis•Sema3A/PlexinA3 association with Scribble mediates cGMP increase in dendrites•Sema3A/PlexinA3 mediate bipolar polarity and apical dendrite development via cGMP•Sema3A/PlexinA3-mediated localized cGMP increase may direct leading-edge polarity Szczurkowska et al. show that spatially directed Sema3A may promote development of the leading process and the apical dendrite via the co-receptor PlexinA3 by orchestrating localized cGMP increase on the scaffold protein, Scribble, at the leading edge of developing pyramidal neurons. The development of the apical dendrite from the leading process of the bipolar pyramidal neuron might be directed by spatially organized extrinsic cues acting on localized intrinsic determinants. The extracellular cues regulating apical dendrite polarization remain elusive. We show that leading process and apical dendrite development are directed by class III Semaphorins and mediated by a localized cGMP-synthesizing complex. The scaffolding protein Scribble that associates with the cGMP-synthesizing enzyme soluble guanylate cyclase (sGC) also associates with the Semaphorin3A (Sema3A) co-receptor PlexinA3. Deletion or knockdown of PlexinA3 and Sema3A or disruption of PlexinA3-Scribble association prevents Sema3A-mediated cGMP increase and causes defects in apical dendrite development. These manipulations also impair bipolar polarity and leading process establishment. Local cGMP elevation or sGC expression rescues the effects of PlexinA3 knockdown or PlexinA3-Scribble complex disruption. During neuronal polarization, leading process and apical dendrite development are directed by a scaffold that links Semaphorin cue to cGMP increase. The development of the apical dendrite from the leading process of the bipolar pyramidal neuron might be directed by spatially organized extrinsic cues acting on localized intrinsic determinants. The extracellular cues regulating apical dendrite polarization remain elusive. We show that leading process and apical dendrite development are directed by class III Semaphorins and mediated by a localized cGMP-synthesizing complex. The scaffolding protein Scribble that associates with the cGMP-synthesizing enzyme soluble guanylate cyclase (sGC) also associates with the Semaphorin3A (Sema3A) co-receptor PlexinA3. Deletion or knockdown of PlexinA3 and Sema3A or disruption of PlexinA3-Scribble association prevents Sema3A-mediated cGMP increase and causes defects in apical dendrite development. These manipulations also impair bipolar polarity and leading process establishment. Local cGMP elevation or sGC expression rescues the effects of PlexinA3 knockdown or PlexinA3-Scribble complex disruption. During neuronal polarization, leading process and apical dendrite development are directed by a scaffold that links Semaphorin cue to cGMP increase.The development of the apical dendrite from the leading process of the bipolar pyramidal neuron might be directed by spatially organized extrinsic cues acting on localized intrinsic determinants. The extracellular cues regulating apical dendrite polarization remain elusive. We show that leading process and apical dendrite development are directed by class III Semaphorins and mediated by a localized cGMP-synthesizing complex. The scaffolding protein Scribble that associates with the cGMP-synthesizing enzyme soluble guanylate cyclase (sGC) also associates with the Semaphorin3A (Sema3A) co-receptor PlexinA3. Deletion or knockdown of PlexinA3 and Sema3A or disruption of PlexinA3-Scribble association prevents Sema3A-mediated cGMP increase and causes defects in apical dendrite development. These manipulations also impair bipolar polarity and leading process establishment. Local cGMP elevation or sGC expression rescues the effects of PlexinA3 knockdown or PlexinA3-Scribble complex disruption. During neuronal polarization, leading process and apical dendrite development are directed by a scaffold that links Semaphorin cue to cGMP increase. The development of the apical dendrite from the leading process of the bipolar pyramidal neuron might be directed by spatially organized extrinsic cues acting on localized intrinsic determinants. The extracellular cues regulating apical dendrite polarization remain elusive. We show that leading process and apical dendrite development are directed by class III Semaphorins and mediated by a localized cGMP-synthesizing complex. The scaffolding protein Scribble that associates with the cGMP-synthesizing enzyme soluble guanylate cyclase (sGC) also associates with the Semaphorin3A (Sema3A) co-receptor PlexinA3. Deletion or knockdown of PlexinA3 and Sema3A or disruption of PlexinA3-Scribble association prevents Sema3A-mediated cGMP increase and causes defects in apical dendrite development. These manipulations also impair bipolar polarity and leading process establishment. Local cGMP elevation or sGC expression rescues the effects of PlexinA3 knockdown or PlexinA3-Scribble complex disruption. During neuronal polarization, leading process and apical dendrite development are directed by a scaffold that links Semaphorin cue to cGMP increase. Szczurkowska et al. show that spatially directed Sema3A may promote development of the leading process and the apical dendrite via the co-receptor PlexinA3 by orchestrating localized cGMP increase on the scaffold protein, Scribble, at the leading edge of developing pyramidal neurons.
ArticleNumber	110483
Author	Martin, Jacqueline Chien, Chia Te Szczurkowska, Joanna Guo, Alan Singh, Ravnit Dadson, Doreen Pautot, Sophie Lee, Seong-Il Tran, Tracy S. Khan, Tamor A. Shelly, Maya Martinez, Edward
AuthorAffiliation	1 Department of Neurobiology and Behavior, Stony Brook University, Stony Brook, NY 11794, USA 5 Lead contact 3 ITAV – CNRS USR 3505, 31106 Toulouse, France 4 These authors contributed equally 2 Department of Biological Sciences, Rutgers University, Newark, NJ 07102, USA
AuthorAffiliation_xml	– name: 3 ITAV – CNRS USR 3505, 31106 Toulouse, France – name: 4 These authors contributed equally – name: 1 Department of Neurobiology and Behavior, Stony Brook University, Stony Brook, NY 11794, USA – name: 2 Department of Biological Sciences, Rutgers University, Newark, NJ 07102, USA – name: 5 Lead contact
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CitedBy_id	crossref_primary_10_1007_s00210_023_02484_8 crossref_primary_10_1016_j_ydbio_2022_07_002
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Keywords	apical dendrite development protein scaffold PlexinA3 Semaphorin3A Scribble hippocampal CA1 cGMP neuron polarization
Language	English
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 PMCID: PMC8994670 AUTHOR CONTRIBUTIONS J.S., A.G., J.M., S.-I.L., and M.S. designed and performed the experiments and analyzed and interpreted the data. S.P. assisted with the FRET experiments. E.M. and T.S.T. performed the Sema3A expression experiments, generated Sema3A, provided the PlexinA3−/− mice, and provided critical comments on the manuscript. C.T.C., T.A.K., R.S., and D.D. assisted with tissue culture and immunostaining experiments, and with data analyses. J.S., A.G., and M.S. wrote the manuscript with input from all other authors. M.S. conceived the idea for this project and supervised the study.
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Snippet	The development of the apical dendrite from the leading process of the bipolar pyramidal neuron might be directed by spatially organized extrinsic cues acting...
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SubjectTerms	apical dendrite development Cells, Cultured cGMP Cyclic GMP Cyclic GMP - metabolism Dendrites Dendrites - metabolism hippocampal CA1 Life Sciences Neurogenesis neuron polarization PlexinA3 protein scaffold Scribble Semaphorin-3A Semaphorin-3A - metabolism Semaphorin-3A - pharmacology Semaphorin3A Semaphorins Semaphorins - metabolism
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Title	Semaphorin3A/PlexinA3 association with the Scribble scaffold for cGMP increase is required for apical dendrite development
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