WIP is a negative regulator of neuronal maturation and synaptic activity

A. Franco; S. Knafo; I. Banon-Rodriguez; P. Merino-Serrais; I. Fernaud-Espinosa; M. Nieto; J. J. Garrido; J. A. Esteban; F. Wandosell; I. M. Anton

doi:10.1093/cercor/bhr199

WIP is a negative regulator of neuronal maturation and synaptic activity

A. Franco, S. Knafo, I. Banon-Rodriguez, P. Merino-Serrais, I. Fernaud-Espinosa, M. Nieto, J. J. Garrido, J. A. Esteban, F. Wandosell, I. M. Anton

Research output: Contribution to journal › Article › peer-review

Abstract

Wiskott-Aldrich syndrome protein (WASP)-interacting protein (WIP) is an actin-binding protein involved in the regulation of actin polymerization in cells, such as fibroblasts and lymphocytes. Despite its recognized function in non-neuronal cells, the role of WIP in the central nervous system has not been examined previously. We used WIP-deficient mice to examine WIP function both in vivo and in vitro. We report here that WIP ^-/- hippocampal neurons exhibit enlargement of somas as well as overgrowth of neuritic and dendritic branches that are more evident in early developmental stages. Dendritic arborization and synaptogenesis, which includes generation of postsynaptic dendritic spines, are actin-dependent processes that occur in parallel at later stages. WIP deficiency also increases the amplitude and frequency of miniature excitatory postsynaptic currents, suggesting that WIP ^-/- neurons have more mature synapses than wild-type neurons. These findings reveal WIP as a previously unreported regulator of neuronal maturation and synaptic activity.

Original language	English
Pages (from-to)	1191-1202
Number of pages	12
Journal	Cerebral Cortex
Volume	22
Issue number	5
DOIs	https://doi.org/10.1093/cercor/bhr199
State	Published - May 2012
Externally published	Yes

Bibliographical note

Funding Information:
Grants from Consejo Superior de Investigaciones Científicas-Comunidad de Madrid (CCG08-CSIC/SAL-3471), CSIC (PIE2-00720I002), and the Spanish Ministry of Education and Science (BFU2007-64144 and BFU2010-21374) to I.M.A., from Centro de Investigación Biomédica en Red Enfermedades Neurodegener-ativas (Instituto de Salud Carlos III), the Plan Nacional DGCYT (SAF2009-12249-C02-01) to F.W. and SAF2010-15676 to S.K., and by an institutional grant from the Fundación Ramón Areces. A.F. was a recipient of an FPU MEC fellowship (AP2005-3405), I.B. held a contract from the Comunidad Autónoma de Madrid and S.K., a Ramón y Cajal contract.

Keywords

N-WASP
dendritic spine
electrophysiology
neuritogenesis
synapse

ASJC Scopus subject areas

Cognitive Neuroscience
Cellular and Molecular Neuroscience

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10.1093/cercor/bhr199

Cite this

@article{7a79228d11994f7e82f5c90e686887ed,

title = "WIP is a negative regulator of neuronal maturation and synaptic activity",

abstract = "Wiskott-Aldrich syndrome protein (WASP)-interacting protein (WIP) is an actin-binding protein involved in the regulation of actin polymerization in cells, such as fibroblasts and lymphocytes. Despite its recognized function in non-neuronal cells, the role of WIP in the central nervous system has not been examined previously. We used WIP-deficient mice to examine WIP function both in vivo and in vitro. We report here that WIP -/- hippocampal neurons exhibit enlargement of somas as well as overgrowth of neuritic and dendritic branches that are more evident in early developmental stages. Dendritic arborization and synaptogenesis, which includes generation of postsynaptic dendritic spines, are actin-dependent processes that occur in parallel at later stages. WIP deficiency also increases the amplitude and frequency of miniature excitatory postsynaptic currents, suggesting that WIP -/- neurons have more mature synapses than wild-type neurons. These findings reveal WIP as a previously unreported regulator of neuronal maturation and synaptic activity.",

keywords = "N-WASP, dendritic spine, electrophysiology, neuritogenesis, synapse",

author = "A. Franco and S. Knafo and I. Banon-Rodriguez and P. Merino-Serrais and I. Fernaud-Espinosa and M. Nieto and Garrido, {J. J.} and Esteban, {J. A.} and F. Wandosell and Anton, {I. M.}",

note = "Funding Information: Grants from Consejo Superior de Investigaciones Cient{\'i}ficas-Comunidad de Madrid (CCG08-CSIC/SAL-3471), CSIC (PIE2-00720I002), and the Spanish Ministry of Education and Science (BFU2007-64144 and BFU2010-21374) to I.M.A., from Centro de Investigaci{\'o}n Biom{\'e}dica en Red Enfermedades Neurodegener-ativas (Instituto de Salud Carlos III), the Plan Nacional DGCYT (SAF2009-12249-C02-01) to F.W. and SAF2010-15676 to S.K., and by an institutional grant from the Fundaci{\'o}n Ram{\'o}n Areces. A.F. was a recipient of an FPU MEC fellowship (AP2005-3405), I.B. held a contract from the Comunidad Aut{\'o}noma de Madrid and S.K., a Ram{\'o}n y Cajal contract.",

year = "2012",

month = may,

doi = "10.1093/cercor/bhr199",

language = "English",

volume = "22",

pages = "1191--1202",

journal = "Cerebral Cortex",

issn = "1047-3211",

publisher = "Oxford University Press",

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T1 - WIP is a negative regulator of neuronal maturation and synaptic activity

AU - Franco, A.

AU - Knafo, S.

AU - Banon-Rodriguez, I.

AU - Merino-Serrais, P.

AU - Fernaud-Espinosa, I.

AU - Nieto, M.

AU - Garrido, J. J.

AU - Esteban, J. A.

AU - Wandosell, F.

AU - Anton, I. M.

N1 - Funding Information: Grants from Consejo Superior de Investigaciones Científicas-Comunidad de Madrid (CCG08-CSIC/SAL-3471), CSIC (PIE2-00720I002), and the Spanish Ministry of Education and Science (BFU2007-64144 and BFU2010-21374) to I.M.A., from Centro de Investigación Biomédica en Red Enfermedades Neurodegener-ativas (Instituto de Salud Carlos III), the Plan Nacional DGCYT (SAF2009-12249-C02-01) to F.W. and SAF2010-15676 to S.K., and by an institutional grant from the Fundación Ramón Areces. A.F. was a recipient of an FPU MEC fellowship (AP2005-3405), I.B. held a contract from the Comunidad Autónoma de Madrid and S.K., a Ramón y Cajal contract.

PY - 2012/5

Y1 - 2012/5

N2 - Wiskott-Aldrich syndrome protein (WASP)-interacting protein (WIP) is an actin-binding protein involved in the regulation of actin polymerization in cells, such as fibroblasts and lymphocytes. Despite its recognized function in non-neuronal cells, the role of WIP in the central nervous system has not been examined previously. We used WIP-deficient mice to examine WIP function both in vivo and in vitro. We report here that WIP -/- hippocampal neurons exhibit enlargement of somas as well as overgrowth of neuritic and dendritic branches that are more evident in early developmental stages. Dendritic arborization and synaptogenesis, which includes generation of postsynaptic dendritic spines, are actin-dependent processes that occur in parallel at later stages. WIP deficiency also increases the amplitude and frequency of miniature excitatory postsynaptic currents, suggesting that WIP -/- neurons have more mature synapses than wild-type neurons. These findings reveal WIP as a previously unreported regulator of neuronal maturation and synaptic activity.

AB - Wiskott-Aldrich syndrome protein (WASP)-interacting protein (WIP) is an actin-binding protein involved in the regulation of actin polymerization in cells, such as fibroblasts and lymphocytes. Despite its recognized function in non-neuronal cells, the role of WIP in the central nervous system has not been examined previously. We used WIP-deficient mice to examine WIP function both in vivo and in vitro. We report here that WIP -/- hippocampal neurons exhibit enlargement of somas as well as overgrowth of neuritic and dendritic branches that are more evident in early developmental stages. Dendritic arborization and synaptogenesis, which includes generation of postsynaptic dendritic spines, are actin-dependent processes that occur in parallel at later stages. WIP deficiency also increases the amplitude and frequency of miniature excitatory postsynaptic currents, suggesting that WIP -/- neurons have more mature synapses than wild-type neurons. These findings reveal WIP as a previously unreported regulator of neuronal maturation and synaptic activity.

KW - N-WASP

KW - dendritic spine

KW - electrophysiology

KW - neuritogenesis

KW - synapse

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DO - 10.1093/cercor/bhr199

M3 - Article

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AN - SCOPUS:84860176645

SN - 1047-3211

VL - 22

SP - 1191

EP - 1202

JO - Cerebral Cortex

JF - Cerebral Cortex

IS - 5

ER -

WIP is a negative regulator of neuronal maturation and synaptic activity

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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