Deciphering the alteration of MAP2 interactome caused by a schizophrenia-associated phosphorylation

Microtubule-associated protein 2 (MAP2) is a crucial regulator of dendritic structure and neuronal function, orchestrating diverse protein interactions within the microtubule network. We have shown MAP2 is hyperphosphorylated at serine 1782 (S1782) in schizophrenia and phosphomimetic mutation of S17...

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Main Authors: Jiali Lyu, Matthew L MacDonald, Shelby Ruiz, Shinnyi Chou, Jordan Gilardi, Serena C Buchwald, Melanie J Grubisha, Robert A Sweet
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Neurobiology of Disease
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Online Access:http://www.sciencedirect.com/science/article/pii/S0969996124003334
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author Jiali Lyu
Matthew L MacDonald
Shelby Ruiz
Shinnyi Chou
Jordan Gilardi
Serena C Buchwald
Melanie J Grubisha
Robert A Sweet
author_facet Jiali Lyu
Matthew L MacDonald
Shelby Ruiz
Shinnyi Chou
Jordan Gilardi
Serena C Buchwald
Melanie J Grubisha
Robert A Sweet
author_sort Jiali Lyu
collection DOAJ
description Microtubule-associated protein 2 (MAP2) is a crucial regulator of dendritic structure and neuronal function, orchestrating diverse protein interactions within the microtubule network. We have shown MAP2 is hyperphosphorylated at serine 1782 (S1782) in schizophrenia and phosphomimetic mutation of S1782 in mice (MAP2S1782E) is sufficient to impair dendritic architecture. We sought to determine how this hyperphosphorylation affects the MAP2 interactome to provide insights into the disorder's mechanisms. We investigated the MAP2 interactome using co-immunoprecipitation and mass spectrometry in MAP2S1782E and MAP2WT mice. We found that S1782E MAP2 led to a substantial disruption of protein-protein interactions relative to WT MAP2. Reduced interactions with PDZ domain-containing proteins, calmodulin-binding proteins, ribosome proteins, and kinesin proteins may all contribute to dendritic impairments induced by S1782E, and may be linked to schizophrenia pathogenesis. Interestingly, novel gain-of-function interactions with PPM1L and KLHL8 nominated these as regulators of phosphoS1782 MAP2 abundance and potential therapeutic targets in schizophrenia.
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spelling doaj-art-73ea272b0e6a461d87af77dfd091cca02024-12-14T06:29:53ZengElsevierNeurobiology of Disease1095-953X2024-12-01203106731Deciphering the alteration of MAP2 interactome caused by a schizophrenia-associated phosphorylationJiali Lyu0Matthew L MacDonald1Shelby Ruiz2Shinnyi Chou3Jordan Gilardi4Serena C Buchwald5Melanie J Grubisha6Robert A Sweet7School of Medicine, Tsinghua University, China; Translational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, United States of AmericaTranslational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, United States of America; Health Sciences Mass Spectrometry Core, University of Pittsburgh, United States of AmericaDepartment of Neurobiology, University of Pittsburgh, United States of AmericaTranslational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, United States of AmericaTranslational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, United States of AmericaTranslational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, United States of AmericaTranslational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, United States of AmericaTranslational Neuroscience Program, Department of Psychiatry, University of Pittsburgh, United States of America; Department of Neurology, University of Pittsburgh, United States of America; Corresponding author at: Biomedical Science Tower, Rm W-1645, 3811 O'Hara Street, Pittsburgh, PA 15213-2593, United States of America.Microtubule-associated protein 2 (MAP2) is a crucial regulator of dendritic structure and neuronal function, orchestrating diverse protein interactions within the microtubule network. We have shown MAP2 is hyperphosphorylated at serine 1782 (S1782) in schizophrenia and phosphomimetic mutation of S1782 in mice (MAP2S1782E) is sufficient to impair dendritic architecture. We sought to determine how this hyperphosphorylation affects the MAP2 interactome to provide insights into the disorder's mechanisms. We investigated the MAP2 interactome using co-immunoprecipitation and mass spectrometry in MAP2S1782E and MAP2WT mice. We found that S1782E MAP2 led to a substantial disruption of protein-protein interactions relative to WT MAP2. Reduced interactions with PDZ domain-containing proteins, calmodulin-binding proteins, ribosome proteins, and kinesin proteins may all contribute to dendritic impairments induced by S1782E, and may be linked to schizophrenia pathogenesis. Interestingly, novel gain-of-function interactions with PPM1L and KLHL8 nominated these as regulators of phosphoS1782 MAP2 abundance and potential therapeutic targets in schizophrenia.http://www.sciencedirect.com/science/article/pii/S0969996124003334MAP2ProteomicsProtein-protein interactionPhosphorylation
spellingShingle Jiali Lyu
Matthew L MacDonald
Shelby Ruiz
Shinnyi Chou
Jordan Gilardi
Serena C Buchwald
Melanie J Grubisha
Robert A Sweet
Deciphering the alteration of MAP2 interactome caused by a schizophrenia-associated phosphorylation
Neurobiology of Disease
MAP2
Proteomics
Protein-protein interaction
Phosphorylation
title Deciphering the alteration of MAP2 interactome caused by a schizophrenia-associated phosphorylation
title_full Deciphering the alteration of MAP2 interactome caused by a schizophrenia-associated phosphorylation
title_fullStr Deciphering the alteration of MAP2 interactome caused by a schizophrenia-associated phosphorylation
title_full_unstemmed Deciphering the alteration of MAP2 interactome caused by a schizophrenia-associated phosphorylation
title_short Deciphering the alteration of MAP2 interactome caused by a schizophrenia-associated phosphorylation
title_sort deciphering the alteration of map2 interactome caused by a schizophrenia associated phosphorylation
topic MAP2
Proteomics
Protein-protein interaction
Phosphorylation
url http://www.sciencedirect.com/science/article/pii/S0969996124003334
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