Tubulin Polymerization Promoting Protein, Ringmaker, and MAP1B Homolog Futsch Coordinate Microtubule Organization and Synaptic Growth

Ringmaker (Ringer) is homologous to the human Tubulin Polymerization Promoting Proteins (TPPPs) that are implicated in the stabilization and bundling of microtubules (MTs) that are particularly important for neurons and are also implicated in synaptic organization and plasticity. No functional data...

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Published inFrontiers in cellular neuroscience Vol. 13; p. 192
Main Authors Shi, Qian, Lin, Yong Qi, Saliba, Afaf, Xie, Jing, Neely, G Gregory, Banerjee, Swati
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Research Foundation 15.05.2019
Frontiers Media S.A
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Abstract Ringmaker (Ringer) is homologous to the human Tubulin Polymerization Promoting Proteins (TPPPs) that are implicated in the stabilization and bundling of microtubules (MTs) that are particularly important for neurons and are also implicated in synaptic organization and plasticity. No functional data exist that have addressed the role of TPPP in synapse organization in any system. Here, we present the phenotypic and functional characterization of mutants during larval neuromuscular junction (NMJ) synaptic development. mutants show reduced synaptic growth and transmission and display phenotypic similarities and genetic interactions with the homolog of vertebrate Microtubule Associated Protein (MAP)1B, Immunohistochemical and biochemical analyses show that individual and combined loss of Ringer and Futsch cause a significant reduction in MT loops at the NMJs and reduced acetylated-tubulin levels. Presynaptic over-expression of Ringer and Futsch causes elevated levels of acetylated-tubulin and significant increase in NMJ MT loops. These results indicate that Ringer and Futsch regulate synaptic MT organization in addition to synaptic growth. Together our findings may inform studies on the close mammalian homolog, TPPP, and provide insights into the role of MTs and associated proteins in synapse growth and organization.
AbstractList Drosophila Ringmaker (Ringer) is homologous to the human T ubulin P olymerization P romoting P roteins (TPPPs) that are implicated in the stabilization and bundling of microtubules (MTs) that are particularly important for neurons and are also implicated in synaptic organization and plasticity. No in vivo functional data exist that have addressed the role of TPPP in synapse organization in any system. Here, we present the phenotypic and functional characterization of ringer mutants during Drosophila larval neuromuscular junction (NMJ) synaptic development. ringer mutants show reduced synaptic growth and transmission and display phenotypic similarities and genetic interactions with the Drosophila homolog of vertebrate M icrotubule A ssociated P rotein (MAP)1B, futsch. Immunohistochemical and biochemical analyses show that individual and combined loss of Ringer and Futsch cause a significant reduction in MT loops at the NMJs and reduced acetylated-tubulin levels. Presynaptic over-expression of Ringer and Futsch causes elevated levels of acetylated-tubulin and significant increase in NMJ MT loops. These results indicate that Ringer and Futsch regulate synaptic MT organization in addition to synaptic growth. Together our findings may inform studies on the close mammalian homolog, TPPP, and provide insights into the role of MTs and associated proteins in synapse growth and organization.
Drosophila Ringmaker (Ringer) is homologous to the human Tubulin Polymerization Promoting Proteins (TPPPs) that are implicated in the stabilization and bundling of microtubules (MTs) that are particularly important for neurons and are also implicated in synaptic organization and plasticity. No in vivo functional data exist that have addressed the role of TPPP in synapse organization in any system. Here, we present the phenotypic and functional characterization of ringer mutants during Drosophila larval neuromuscular junction (NMJ) synaptic development. ringer mutants show reduced synaptic growth and transmission and display phenotypic similarities and genetic interactions with the Drosophila homolog of vertebrate Microtubule Associated Protein (MAP)1B, futsch. Immunohistochemical and biochemical analyses show that individual and combined loss of Ringer and Futsch cause a significant reduction in MT loops at the NMJs and reduced acetylated-tubulin levels. Presynaptic over-expression of Ringer and Futsch causes elevated levels of acetylated-tubulin and significant increase in NMJ MT loops. These results indicate that Ringer and Futsch regulate synaptic MT organization in addition to synaptic growth. Together our findings may inform studies on the close mammalian homolog, TPPP, and provide insights into the role of MTs and associated proteins in synapse growth and organization.
Ringmaker (Ringer) is homologous to the human Tubulin Polymerization Promoting Proteins (TPPPs) that are implicated in the stabilization and bundling of microtubules (MTs) that are particularly important for neurons and are also implicated in synaptic organization and plasticity. No functional data exist that have addressed the role of TPPP in synapse organization in any system. Here, we present the phenotypic and functional characterization of mutants during larval neuromuscular junction (NMJ) synaptic development. mutants show reduced synaptic growth and transmission and display phenotypic similarities and genetic interactions with the homolog of vertebrate Microtubule Associated Protein (MAP)1B, Immunohistochemical and biochemical analyses show that individual and combined loss of Ringer and Futsch cause a significant reduction in MT loops at the NMJs and reduced acetylated-tubulin levels. Presynaptic over-expression of Ringer and Futsch causes elevated levels of acetylated-tubulin and significant increase in NMJ MT loops. These results indicate that Ringer and Futsch regulate synaptic MT organization in addition to synaptic growth. Together our findings may inform studies on the close mammalian homolog, TPPP, and provide insights into the role of MTs and associated proteins in synapse growth and organization.
Author Neely, G Gregory
Xie, Jing
Shi, Qian
Banerjee, Swati
Saliba, Afaf
Lin, Yong Qi
AuthorAffiliation 2 The Dr. John and Anne Chong Lab for Functional Genomics, Charles Perkins Centre and School of Life and Environmental Sciences, The University of Sydney , Sydney, NSW , Australia
1 Department of Cellular and Integrative Physiology, Long School of Medicine, University of Texas Health , San Antonio, TX , United States
3 Xiangya School of Medicine, Central South University , Changsha , China
AuthorAffiliation_xml – name: 3 Xiangya School of Medicine, Central South University , Changsha , China
– name: 2 The Dr. John and Anne Chong Lab for Functional Genomics, Charles Perkins Centre and School of Life and Environmental Sciences, The University of Sydney , Sydney, NSW , Australia
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31156389$$D View this record in MEDLINE/PubMed
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Copyright © 2019 Shi, Lin, Saliba, Xie, Neely and Banerjee. 2019 Shi, Lin, Saliba, Xie, Neely and Banerjee
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Keywords acetylation
microtubule
Ringmaker
Futsch
TPPP
synapse
Language English
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Notes Edited by: Davide Cervia, Università degli Studi della Tuscia, Italy
This article was submitted to Cellular Neurophysiology, a section of the journal Frontiers in Cellular Neuroscience
Reviewed by: Timothy Mosca, Thomas Jefferson University, United States; Archan Ganguly, University of California, San Diego, United States; Judit Ovadi, Hungarian Academy of Sciences (MTA), Hungary
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SSID ssj0062648
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Snippet Ringmaker (Ringer) is homologous to the human Tubulin Polymerization Promoting Proteins (TPPPs) that are implicated in the stabilization and bundling of...
Drosophila Ringmaker (Ringer) is homologous to the human Tubulin Polymerization Promoting Proteins (TPPPs) that are implicated in the stabilization and...
Drosophila Ringmaker (Ringer) is homologous to the human T ubulin P olymerization P romoting P roteins (TPPPs) that are implicated in the stabilization and...
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StartPage 192
SubjectTerms acetylation
Cytoskeleton
Drosophila
Functional plasticity
Futsch
Insects
microtubule
Microtubule-associated protein 1
Microtubules
Nervous system
Neuromuscular junctions
Neuroscience
Overexpression
Polymerization
Proteins
Ringmaker
synapse
Synaptic plasticity
Synaptic transmission
Synaptogenesis
TPPP
Tubulin
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Title Tubulin Polymerization Promoting Protein, Ringmaker, and MAP1B Homolog Futsch Coordinate Microtubule Organization and Synaptic Growth
URI https://www.ncbi.nlm.nih.gov/pubmed/31156389
https://www.proquest.com/docview/2282550732
https://pubmed.ncbi.nlm.nih.gov/PMC6529516
https://doaj.org/article/0d6cdeb1913a40a2822e2930318297b3
Volume 13
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