Kinase/phosphatase overexpression reveals pathways regulating hippocampal neuron morphology

Abstract Development and regeneration of the nervous system requires the precise formation of axons and dendrites. Kinases and phosphatases are pervasive regulators of cellular function and have been implicated in controlling axodendritic development and regeneration. We undertook a gain‐of‐function...

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Main Authors: William J Buchser, Tatiana I Slepak, Omar Gutierrez‐Arenas, John L Bixby, Vance P Lemmon
Format: Article
Language:English
Published: Springer Nature 2010-07-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.1038/msb.2010.52
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author William J Buchser
Tatiana I Slepak
Omar Gutierrez‐Arenas
John L Bixby
Vance P Lemmon
author_facet William J Buchser
Tatiana I Slepak
Omar Gutierrez‐Arenas
John L Bixby
Vance P Lemmon
author_sort William J Buchser
collection DOAJ
description Abstract Development and regeneration of the nervous system requires the precise formation of axons and dendrites. Kinases and phosphatases are pervasive regulators of cellular function and have been implicated in controlling axodendritic development and regeneration. We undertook a gain‐of‐function analysis to determine the functions of kinases and phosphatases in the regulation of neuron morphology. Over 300 kinases and 124 esterases and phosphatases were studied by high‐content analysis of rat hippocampal neurons. Proteins previously implicated in neurite growth, such as ERK1, GSK3, EphA8, FGFR, PI3K, PKC, p38, and PP1a, were confirmed to have effects in our functional assays. We also identified novel positive and negative neurite growth regulators. These include neuronal‐developmentally regulated kinases such as the activin receptor, interferon regulatory factor 6 (IRF6) and neural leucine‐rich repeat 1 (LRRN1). The protein kinase N2 (PKN2) and choline kinase α (CHKA) kinases, and the phosphatases PPEF2 and SMPD1, have little or no established functions in neuronal function, but were sufficient to promote neurite growth. In addition, pathway analysis revealed that members of signaling pathways involved in cancer progression and axis formation enhanced neurite outgrowth, whereas cytokine‐related pathways significantly inhibited neurite formation.
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spelling doaj-art-e4fe5268fc9b4703a757be2f87c790cb2025-08-20T02:18:35ZengSpringer NatureMolecular Systems Biology1744-42922010-07-016111610.1038/msb.2010.52Kinase/phosphatase overexpression reveals pathways regulating hippocampal neuron morphologyWilliam J Buchser0Tatiana I Slepak1Omar Gutierrez‐Arenas2John L Bixby3Vance P Lemmon4The Miami Project to Cure Paralysis, Departments of Pharmacology and Neurological Surgery, and Neuroscience Program, University of Miami, Miller School of MedicineThe Miami Project to Cure Paralysis, Departments of Pharmacology and Neurological Surgery, and Neuroscience Program, University of Miami, Miller School of MedicineThe Miami Project to Cure Paralysis, Departments of Pharmacology and Neurological Surgery, and Neuroscience Program, University of Miami, Miller School of MedicineThe Miami Project to Cure Paralysis, Departments of Pharmacology and Neurological Surgery, and Neuroscience Program, University of Miami, Miller School of MedicineThe Miami Project to Cure Paralysis, Departments of Pharmacology and Neurological Surgery, and Neuroscience Program, University of Miami, Miller School of MedicineAbstract Development and regeneration of the nervous system requires the precise formation of axons and dendrites. Kinases and phosphatases are pervasive regulators of cellular function and have been implicated in controlling axodendritic development and regeneration. We undertook a gain‐of‐function analysis to determine the functions of kinases and phosphatases in the regulation of neuron morphology. Over 300 kinases and 124 esterases and phosphatases were studied by high‐content analysis of rat hippocampal neurons. Proteins previously implicated in neurite growth, such as ERK1, GSK3, EphA8, FGFR, PI3K, PKC, p38, and PP1a, were confirmed to have effects in our functional assays. We also identified novel positive and negative neurite growth regulators. These include neuronal‐developmentally regulated kinases such as the activin receptor, interferon regulatory factor 6 (IRF6) and neural leucine‐rich repeat 1 (LRRN1). The protein kinase N2 (PKN2) and choline kinase α (CHKA) kinases, and the phosphatases PPEF2 and SMPD1, have little or no established functions in neuronal function, but were sufficient to promote neurite growth. In addition, pathway analysis revealed that members of signaling pathways involved in cancer progression and axis formation enhanced neurite outgrowth, whereas cytokine‐related pathways significantly inhibited neurite formation.https://doi.org/10.1038/msb.2010.52bioinformaticsdevelopmentfunctional genomicsmetabolic and regulatory networksneuroscience
spellingShingle William J Buchser
Tatiana I Slepak
Omar Gutierrez‐Arenas
John L Bixby
Vance P Lemmon
Kinase/phosphatase overexpression reveals pathways regulating hippocampal neuron morphology
Molecular Systems Biology
bioinformatics
development
functional genomics
metabolic and regulatory networks
neuroscience
title Kinase/phosphatase overexpression reveals pathways regulating hippocampal neuron morphology
title_full Kinase/phosphatase overexpression reveals pathways regulating hippocampal neuron morphology
title_fullStr Kinase/phosphatase overexpression reveals pathways regulating hippocampal neuron morphology
title_full_unstemmed Kinase/phosphatase overexpression reveals pathways regulating hippocampal neuron morphology
title_short Kinase/phosphatase overexpression reveals pathways regulating hippocampal neuron morphology
title_sort kinase phosphatase overexpression reveals pathways regulating hippocampal neuron morphology
topic bioinformatics
development
functional genomics
metabolic and regulatory networks
neuroscience
url https://doi.org/10.1038/msb.2010.52
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AT omargutierrezarenas kinasephosphataseoverexpressionrevealspathwaysregulatinghippocampalneuronmorphology
AT johnlbixby kinasephosphataseoverexpressionrevealspathwaysregulatinghippocampalneuronmorphology
AT vanceplemmon kinasephosphataseoverexpressionrevealspathwaysregulatinghippocampalneuronmorphology