The vesicle protein SAM-4 regulates the processivity of synaptic vesicle transport

Axonal transport of synaptic vesicles (SVs) is a KIF1A/UNC-104 mediated process critical for synapse development and maintenance yet little is known of how SV transport is regulated. Using C. elegans as an in vivo model, we identified SAM-4 as a novel conserved vesicular component regulating SV tran...

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Published inPLoS genetics Vol. 10; no. 10; p. e1004644
Main Authors Zheng, Qun, Ahlawat, Shikha, Schaefer, Anneliese, Mahoney, Tim, Koushika, Sandhya P, Nonet, Michael L
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.10.2014
Public Library of Science (PLoS)
Subjects
Animals
Animals, Genetically Modified
Axonal transport
Axonal Transport - genetics
Binding Sites
Biology and Life Sciences
Caenorhabditis elegans - genetics
Caenorhabditis elegans - metabolism
Caenorhabditis elegans Proteins - genetics
Caenorhabditis elegans Proteins - metabolism
Genetic aspects
Genetic regulation
Genetic research
Intercellular Signaling Peptides and Proteins
Medicine and Health Sciences
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mutation
Nematodes
Nerve Tissue Proteins - genetics
Nerve Tissue Proteins - metabolism
Neurites - metabolism
Neurons
Neurons - metabolism
Paralysis
Phosphoproteins - genetics
Phosphoproteins - metabolism
Phosphorylation
Proteins
Research and Analysis Methods
Synapses
Synaptic Vesicles - metabolism
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Abstract Axonal transport of synaptic vesicles (SVs) is a KIF1A/UNC-104 mediated process critical for synapse development and maintenance yet little is known of how SV transport is regulated. Using C. elegans as an in vivo model, we identified SAM-4 as a novel conserved vesicular component regulating SV transport. Processivity, but not velocity, of SV transport was reduced in sam-4 mutants. sam-4 displayed strong genetic interactions with mutations in the cargo binding but not the motor domain of unc-104. Gain-of-function mutations in the unc-104 motor domain, identified in this study, suppress the sam-4 defects by increasing processivity of the SV transport. Genetic analyses suggest that SAM-4, SYD-2/liprin-α and the KIF1A/UNC-104 motor function in the same pathway to regulate SV transport. Our data support a model in which the SV protein SAM-4 regulates the processivity of SV transport.
AbstractList Axonal transport of synaptic vesicles (SVs) is a KIF1A/UNC-104 mediated process critical for synapse development and maintenance yet little is known of how SV transport is regulated. Using C. elegans as an in vivo model, we identified SAM-4 as a novel conserved vesicular component regulating SV transport. Processivity, but not velocity, of SV transport was reduced in sam-4 mutants. sam-4 displayed strong genetic interactions with mutations in the cargo binding but not the motor domain of unc-104. Gain-of-function mutations in the unc-104 motor domain, identified in this study, suppress the sam-4 defects by increasing processivity of the SV transport. Genetic analyses suggest that SAM-4, SYD-2/liprin- α and the KIF1A/UNC-104 motor function in the same pathway to regulate SV transport. Our data support a model in which the SV protein SAM-4 regulates the processivity of SV transport.
  Axonal transport of synaptic vesicles (SVs) is a KIF1A/UNC-104 mediated process critical for synapse development and maintenance yet little is known of how SV transport is regulated. Using C. elegans as an in vivo model, we identified SAM-4 as a novel conserved vesicular component regulating SV transport. Processivity, but not velocity, of SV transport was reduced in sam-4 mutants. sam-4 displayed strong genetic interactions with mutations in the cargo binding but not the motor domain of unc-104. Gain-of-function mutations in the unc-104 motor domain, identified in this study, suppress the sam-4 defects by increasing processivity of the SV transport. Genetic analyses suggest that SAM-4, SYD-2/liprin-α and the KIF1A/UNC-104 motor function in the same pathway to regulate SV transport. Our data support a model in which the SV protein SAM-4 regulates the processivity of SV transport.
Axonal transport of synaptic vesicles (SVs) is a KIF1A/UNC-104 mediated process critical for synapse development and maintenance yet little is known of how SV transport is regulated. Using C. elegans as an in vivo model, we identified SAM-4 as a novel conserved vesicular component regulating SV transport. Processivity, but not velocity, of SV transport was reduced in sam-4 mutants. s am-4 displayed strong genetic interactions with mutations in the cargo binding but not the motor domain of unc-104 . Gain-of-function mutations in the unc-104 motor domain, identified in this study, suppress the sam-4 defects by increasing processivity of the SV transport. Genetic analyses suggest that SAM-4, SYD-2/liprin-α and the KIF1A/UNC-104 motor function in the same pathway to regulate SV transport. Our data support a model in which the SV protein SAM-4 regulates the processivity of SV transport. Most cellular components of neurons are synthesized in the cell body and must be transported great distances to form synapses at the ends of axons and dendrites. Neurons use a specialized axonal transport system consisting of microtubule cytoskeletal tracks and numerous molecular motors to shuttle specific cargo to specific destinations in the cell. Disruption of this transport system has severe consequences to human health. Disruption of specific neuronal motors are linked to hereditary neurodegenerative conditions including forms of Charcot Marie Tooth disease, several types of hereditary spastic paraplegia, and certain forms of amyotrophic lateral sclerosis motor neuron disease. Despite recent progress in defining the cargo of many of kinesin family motors in neurons, little is known about how the activity of these transport systems is regulated. Here, using a simple invertebrate model we identify and characterize a novel protein that regulates the efficacy of the KIF1A motor that mediates transport of synaptic vesicles. These studies define a new pathway regulating SV transport with potential links to human neurological disease.
Audience Academic
Author Mahoney, Tim
Ahlawat, Shikha
Koushika, Sandhya P
Zheng, Qun
Nonet, Michael L
Schaefer, Anneliese
AuthorAffiliation 2 National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India
3 Department of Neurology, Washington University Medical School, St. Louis, Missouri, United States of America
4 Huffington Center On Aging, Baylor College of Medicine, Houston, Texas, United States of America
University of California San Diego, United States of America
5 Department of Biological Sciences, Tata Institute of Fundamental Research, Colaba, Mumbai, India
1 Department of Anatomy and Neurobiology, Washington University Medical School, St. Louis, Missouri, United States of America
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ContentType Journal Article
Copyright COPYRIGHT 2014 Public Library of Science
2014 Zheng et al 2014 Zheng et al
2014 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Zheng Q, Ahlawat S, Schaefer A, Mahoney T, Koushika SP, Nonet ML (2014) The Vesicle Protein SAM-4 Regulates the Processivity of Synaptic Vesicle Transport. PLoS Genet 10(10): e1004644. doi:10.1371/journal.pgen.1004644
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– notice: 2014 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Zheng Q, Ahlawat S, Schaefer A, Mahoney T, Koushika SP, Nonet ML (2014) The Vesicle Protein SAM-4 Regulates the Processivity of Synaptic Vesicle Transport. PLoS Genet 10(10): e1004644. doi:10.1371/journal.pgen.1004644
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Conceived and designed the experiments: QZ MLN AS SPK. Performed the experiments: QZ SA AS TM SPK MLN. Analyzed the data: QZ SPK MLN. Wrote the paper: QZ MLN.
The authors have declared that no competing interests exist.
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SSID ssj0035897
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Snippet Axonal transport of synaptic vesicles (SVs) is a KIF1A/UNC-104 mediated process critical for synapse development and maintenance yet little is known of how SV...
  Axonal transport of synaptic vesicles (SVs) is a KIF1A/UNC-104 mediated process critical for synapse development and maintenance yet little is known of how...
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Open Access Repository
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StartPage e1004644
SubjectTerms Animals
Animals, Genetically Modified
Axonal transport
Axonal Transport - genetics
Binding Sites
Biology and Life Sciences
Caenorhabditis elegans - genetics
Caenorhabditis elegans - metabolism
Caenorhabditis elegans Proteins - genetics
Caenorhabditis elegans Proteins - metabolism
Genetic aspects
Genetic regulation
Genetic research
Intercellular Signaling Peptides and Proteins
Medicine and Health Sciences
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mutation
Nematodes
Nerve Tissue Proteins - genetics
Nerve Tissue Proteins - metabolism
Neurites - metabolism
Neurons
Neurons - metabolism
Paralysis
Phosphoproteins - genetics
Phosphoproteins - metabolism
Phosphorylation
Proteins
Research and Analysis Methods
Synapses
Synaptic Vesicles - metabolism
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Title The vesicle protein SAM-4 regulates the processivity of synaptic vesicle transport
URI https://www.ncbi.nlm.nih.gov/pubmed/25329901
https://search.proquest.com/docview/1615258523
https://pubmed.ncbi.nlm.nih.gov/PMC4199485
https://doaj.org/article/a6c1e199ecf04b3fab9351a3c2a888f2
http://dx.doi.org/10.1371/journal.pgen.1004644
Volume 10
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