The Caenorhabditis elegans Eph receptor activates NCK and N-WASP, and inhibits Ena/VASP to regulate growth cone dynamics during axon guidance

The Eph receptor tyrosine kinases (RTKs) are regulators of cell migration and axon guidance. However, our understanding of the molecular mechanisms by which Eph RTKs regulate these processes is still incomplete. To understand how Eph receptors regulate axon guidance in Caenorhabditis elegans, we scr...

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Published inPLoS genetics Vol. 8; no. 2; p. e1002513
Main Authors Mohamed, Ahmed M, Boudreau, Jeffrey R, Yu, Fabian P S, Liu, Jun, Chin-Sang, Ian D
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.02.2012
Public Library of Science (PLoS)
Subjects
Actins - physiology
Adaptor Proteins, Signal Transducing - genetics
Adaptor Proteins, Signal Transducing - metabolism
Animals
Animals, Genetically Modified
Biology
Caenorhabditis elegans - cytology
Caenorhabditis elegans - physiology
Caenorhabditis elegans Proteins - genetics
Caenorhabditis elegans Proteins - metabolism
Cell Adhesion Molecules - genetics
Cell Adhesion Molecules - metabolism
Cell Cycle Proteins - genetics
Cell Cycle Proteins - metabolism
Cells
Cytoskeleton - physiology
Genetics
Growth Cones - physiology
Growth Cones - ultrastructure
Medical research
Microfilament Proteins - genetics
Microfilament Proteins - metabolism
Nematodes
Neurons - physiology
Neurons - ultrastructure
Oncogene Proteins - genetics
Oncogene Proteins - metabolism
Phosphoproteins - genetics
Phosphoproteins - metabolism
Proteins
Receptor Protein-Tyrosine Kinases - genetics
Receptor Protein-Tyrosine Kinases - metabolism
Signal Transduction
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Abstract The Eph receptor tyrosine kinases (RTKs) are regulators of cell migration and axon guidance. However, our understanding of the molecular mechanisms by which Eph RTKs regulate these processes is still incomplete. To understand how Eph receptors regulate axon guidance in Caenorhabditis elegans, we screened for suppressors of axon guidance defects caused by a hyperactive VAB-1/Eph RTK. We identified NCK-1 and WSP-1/N-WASP as downstream effectors of VAB-1. Furthermore, VAB-1, NCK-1, and WSP-1 can form a complex in vitro. We also report that NCK-1 can physically bind UNC-34/Enabled (Ena), and suggest that VAB-1 inhibits the NCK-1/UNC-34 complex and negatively regulates UNC-34. Our results provide a model of the molecular events that allow the VAB-1 RTK to regulate actin dynamics for axon guidance. We suggest that VAB-1/Eph RTK can stop axonal outgrowth by inhibiting filopodia formation at the growth cone by activating Arp2/3 through a VAB-1/NCK-1/WSP-1 complex and by inhibiting UNC-34/Ena activity.
AbstractList The Eph receptor tyrosine kinases (RTKs) are regulators of cell migration and axon guidance. However, our understanding of the molecular mechanisms by which Eph RTKs regulate these processes is still incomplete. To understand how Eph receptors regulate axon guidance in Caenorhabditis elegans, we screened for suppressors of axon guidance defects caused by a hyperactive VAB-1/Eph RTK. We identified NCK-1 and WSP-1/N-WASP as downstream effectors of VAB-1. Furthermore, VAB-1, NCK-1, and WSP-1 can form a complex in vitro. We also report that NCK-1 can physically bind UNC-34/Enabled (Ena), and suggest that VAB-1 inhibits the NCK-1/UNC-34 complex and negatively regulates UNC-34. Our results provide a model of the molecular events that allow the VAB-1 RTK to regulate actin dynamics for axon guidance. We suggest that VAB-1/Eph RTK can stop axonal outgrowth by inhibiting filopodia formation at the growth cone by activating Arp2/3 through a VAB-1/NCK-1/WSP-1 complex and by inhibiting UNC-34/Ena activity.
The Eph receptor tyrosine kinases (RTKs) are regulators of cell migration and axon guidance. However, our understanding of the molecular mechanisms by which Eph RTKs regulate these processes is still incomplete. To understand how Eph receptors regulate axon guidance in Caenorhabditis elegans , we screened for suppressors of axon guidance defects caused by a hyperactive VAB-1/Eph RTK. We identified NCK-1 and WSP-1/N-WASP as downstream effectors of VAB-1. Furthermore, VAB-1, NCK-1, and WSP-1 can form a complex in vitro . We also report that NCK-1 can physically bind UNC-34/Enabled (Ena), and suggest that VAB-1 inhibits the NCK-1/UNC-34 complex and negatively regulates UNC-34. Our results provide a model of the molecular events that allow the VAB-1 RTK to regulate actin dynamics for axon guidance. We suggest that VAB-1/Eph RTK can stop axonal outgrowth by inhibiting filopodia formation at the growth cone by activating Arp2/3 through a VAB-1/NCK-1/WSP-1 complex and by inhibiting UNC-34/Ena activity. The correct wiring of the nervous system depends on the ability of axons to properly interpret extracellular cues that guide them to their targets. The Eph receptor tyrosine kinases (RTKs) have roles in guiding axons, but their signaling pathways are not completely understood. In this study, we used the nematode Caenorhabditis elegans to study how the VAB-1 Eph RTK regulates the growth cone structure for axon guidance. Genetic and molecular data show that VAB-1 regulates the conserved molecules NCK-1, WSP-1/N-WASP, and UNC-34/Ena. Our study provides a model of how the VAB-1 Eph RTK modulates the growth cone structure to inhibit axonal outgrowth. We show that activated VAB-1 can inhibit an NCK-1/UNC-34 interaction by binding to the NCK-1 SH2 domain. We also show that NCK-1 and WSP-1 can physically interact and that VAB-1/NCK-1 and WSP-1 form a complex in vitro . We suggest that the VAB-1 Eph RTK can contribute to the termination of axon outgrowth by two methods: 1) The VAB-1/NCK-1/WSP-1 complex activates ARP-2/3 to change the actin growth cone dynamics to that of a branched structure thus reducing the number of filopodia, and 2) VAB-1 inhibits axon extension by inhibiting UNC-34/Ena's function in actin polymerization.
  The Eph receptor tyrosine kinases (RTKs) are regulators of cell migration and axon guidance. However, our understanding of the molecular mechanisms by which Eph RTKs regulate these processes is still incomplete. To understand how Eph receptors regulate axon guidance in Caenorhabditis elegans, we screened for suppressors of axon guidance defects caused by a hyperactive VAB-1/Eph RTK. We identified NCK-1 and WSP-1/N-WASP as downstream effectors of VAB-1. Furthermore, VAB-1, NCK-1, and WSP-1 can form a complex in vitro. We also report that NCK-1 can physically bind UNC-34/Enabled (Ena), and suggest that VAB-1 inhibits the NCK-1/UNC-34 complex and negatively regulates UNC-34. Our results provide a model of the molecular events that allow the VAB-1 RTK to regulate actin dynamics for axon guidance. We suggest that VAB-1/Eph RTK can stop axonal outgrowth by inhibiting filopodia formation at the growth cone by activating Arp2/3 through a VAB-1/NCK-1/WSP-1 complex and by inhibiting UNC-34/Ena activity.
Author Mohamed, Ahmed M
Boudreau, Jeffrey R
Chin-Sang, Ian D
Liu, Jun
Yu, Fabian P S
AuthorAffiliation Harvard University, United States of America
Department of Biology, Queen's University, Kingston, Canada
AuthorAffiliation_xml – name: Department of Biology, Queen's University, Kingston, Canada
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/22383893$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2012 Mohamed et al. 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: Mohamed AM, Boudreau JR, Yu FPS, Liu J, Chin-Sang ID (2012) The Caenorhabditis elegans Eph Receptor Activates NCK and N-WASP, and Inhibits Ena/VASP to Regulate Growth Cone Dynamics during Axon Guidance. PLoS Genet 8(2): e1002513. doi:10.1371/journal.pgen.1002513
Mohamed et al. 2012
Copyright_xml – notice: 2012 Mohamed et al. 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: Mohamed AM, Boudreau JR, Yu FPS, Liu J, Chin-Sang ID (2012) The Caenorhabditis elegans Eph Receptor Activates NCK and N-WASP, and Inhibits Ena/VASP to Regulate Growth Cone Dynamics during Axon Guidance. PLoS Genet 8(2): e1002513. doi:10.1371/journal.pgen.1002513
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Conceived and designed the experiments: IDC-S AMM. Performed the experiments: IDC-S AMM JRB FPSY JL. Analyzed the data: IDC-S AMM JRB FPSY. Contributed reagents/materials/analysis tools: IDC-S AMM JRB FPSY JL. Wrote the paper: IDC-S AMM.
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  article-title: Genes required for axon pathfinding and extension in the C. elegans nerve ring.
  publication-title: Development
  doi: 10.1242/dev.126.16.3679
  contributor:
    fullname: JA Zallen
SSID ssj0035897
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Snippet The Eph receptor tyrosine kinases (RTKs) are regulators of cell migration and axon guidance. However, our understanding of the molecular mechanisms by which...
  The Eph receptor tyrosine kinases (RTKs) are regulators of cell migration and axon guidance. However, our understanding of the molecular mechanisms by which...
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SubjectTerms Actins - physiology
Adaptor Proteins, Signal Transducing - genetics
Adaptor Proteins, Signal Transducing - metabolism
Animals
Animals, Genetically Modified
Biology
Caenorhabditis elegans - cytology
Caenorhabditis elegans - physiology
Caenorhabditis elegans Proteins - genetics
Caenorhabditis elegans Proteins - metabolism
Cell Adhesion Molecules - genetics
Cell Adhesion Molecules - metabolism
Cell Cycle Proteins - genetics
Cell Cycle Proteins - metabolism
Cells
Cytoskeleton - physiology
Genetics
Growth Cones - physiology
Growth Cones - ultrastructure
Medical research
Microfilament Proteins - genetics
Microfilament Proteins - metabolism
Nematodes
Neurons - physiology
Neurons - ultrastructure
Oncogene Proteins - genetics
Oncogene Proteins - metabolism
Phosphoproteins - genetics
Phosphoproteins - metabolism
Proteins
Receptor Protein-Tyrosine Kinases - genetics
Receptor Protein-Tyrosine Kinases - metabolism
Signal Transduction
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Title The Caenorhabditis elegans Eph receptor activates NCK and N-WASP, and inhibits Ena/VASP to regulate growth cone dynamics during axon guidance
URI https://www.ncbi.nlm.nih.gov/pubmed/22383893
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http://dx.doi.org/10.1371/journal.pgen.1002513
Volume 8
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