Prd1 associates with the clathrin adaptor α-Adaptin and the kinesin-3 Imac/Unc-104 to govern dendrite pruning in Drosophila
Refinement of the nervous system depends on selective removal of excessive axons/dendrites, a process known as pruning. Drosophila ddaC sensory neurons prune their larval dendrites via endo-lysosomal degradation of the L1-type cell adhesion molecule (L1-CAM), Neuroglian (Nrg). Here, we have identifi...
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Published in | PLoS biology Vol. 16; no. 8; p. e2004506 |
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Abstract | Refinement of the nervous system depends on selective removal of excessive axons/dendrites, a process known as pruning. Drosophila ddaC sensory neurons prune their larval dendrites via endo-lysosomal degradation of the L1-type cell adhesion molecule (L1-CAM), Neuroglian (Nrg). Here, we have identified a novel gene, pruning defect 1 (prd1), which governs dendrite pruning of ddaC neurons. We show that Prd1 colocalizes with the clathrin adaptor protein α-Adaptin (α-Ada) and the kinesin-3 immaculate connections (Imac)/Uncoordinated-104 (Unc-104) in dendrites. Moreover, Prd1 physically associates with α-Ada and Imac, which are both critical for dendrite pruning. Prd1, α-Ada, and Imac promote dendrite pruning via the regulation of endo-lysosomal degradation of Nrg. Importantly, genetic interactions among prd1, α-adaptin, and imac indicate that they act in the same pathway to promote dendrite pruning. Our findings indicate that Prd1, α-Ada, and Imac act together to regulate discrete distribution of α-Ada/clathrin puncta, facilitate endo-lysosomal degradation, and thereby promote dendrite pruning in sensory neurons. |
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AbstractList | Refinement of the nervous system depends on selective removal of excessive axons/dendrites, a process known as pruning.
Drosophila
ddaC sensory neurons prune their larval dendrites via endo-lysosomal degradation of the L1-type cell adhesion molecule (L1-CAM), Neuroglian (Nrg). Here, we have identified a novel gene,
pruning defect 1
(
prd1
), which governs dendrite pruning of ddaC neurons. We show that Prd1 colocalizes with the clathrin adaptor protein α-Adaptin (α-Ada) and the kinesin-3 immaculate connections (Imac)/Uncoordinated-104 (Unc-104) in dendrites. Moreover, Prd1 physically associates with α-Ada and Imac, which are both critical for dendrite pruning. Prd1, α-Ada, and Imac promote dendrite pruning via the regulation of endo-lysosomal degradation of Nrg. Importantly, genetic interactions among
prd1
,
α-adaptin
, and
imac
indicate that they act in the same pathway to promote dendrite pruning. Our findings indicate that Prd1, α-Ada, and Imac act together to regulate discrete distribution of α-Ada/clathrin puncta, facilitate endo-lysosomal degradation, and thereby promote dendrite pruning in sensory neurons.
During the maturation of the nervous system, some neurons can selectively eliminate their unnecessary connections, including dendrites and axons, to retain specific connections. In
Drosophila
, a class of sensory neurons lose all their larval dendrites during metamorphosis, when they transition from larvae to adults. We previously showed that these neurons prune their dendrites via lysosome-mediated degradation of a cell-adhesion protein, Neuroglian. In this paper, we identified a previously uncharacterized gene,
pruning defect 1
(
prd1
), which plays an important role in dendrite pruning. We show that Prd1 is localized and complexed with α-Adaptin and Imac, two other proteins that are also essential for dendrite pruning. Moreover, Prd1, α-Adaptin, and Imac act in a common pathway to promote dendrite pruning by down-regulating Neuroglian protein. Thus, our study highlights a mechanism whereby Prd1, α-Adaptin, and Imac act together to regulate distribution of α-Adaptin/clathrin puncta, facilitate lysosome-dependent protein degradation, and thereby promote dendrite pruning in
Drosophila
sensory neurons. Refinement of the nervous system depends on selective removal of excessive axons/dendrites, a process known as pruning. Drosophila ddaC sensory neurons prune their larval dendrites via endo-lysosomal degradation of the L1-type cell adhesion molecule (L1-CAM), Neuroglian (Nrg). Here, we have identified a novel gene, pruning defect 1 (prd1), which governs dendrite pruning of ddaC neurons. We show that Prd1 colocalizes with the clathrin adaptor protein α-Adaptin (α-Ada) and the kinesin-3 immaculate connections (Imac)/Uncoordinated-104 (Unc-104) in dendrites. Moreover, Prd1 physically associates with α-Ada and Imac, which are both critical for dendrite pruning. Prd1, α-Ada, and Imac promote dendrite pruning via the regulation of endo-lysosomal degradation of Nrg. Importantly, genetic interactions among prd1, α-adaptin, and imac indicate that they act in the same pathway to promote dendrite pruning. Our findings indicate that Prd1, α-Ada, and Imac act together to regulate discrete distribution of α-Ada/clathrin puncta, facilitate endo-lysosomal degradation, and thereby promote dendrite pruning in sensory neurons. |
Author | Tang, Quan Yu, Fengwei Zong, Wenhui Zhang, Heng Wang, Yan |
AuthorAffiliation | 2 NUS Graduate School for Integrative Sciences and Engineering, Centre for Life Sciences, Singapore 3 Neuroscience and Behavioral Disorder Program, Duke-NUS Graduate Medical School Singapore, Singapore Oregon Health and Science University, United States of America 1 Temasek Life Sciences Laboratory and Department of Biological Sciences, 1 Research Link, National University of Singapore, Singapore |
AuthorAffiliation_xml | – name: Oregon Health and Science University, United States of America – name: 3 Neuroscience and Behavioral Disorder Program, Duke-NUS Graduate Medical School Singapore, Singapore – name: 1 Temasek Life Sciences Laboratory and Department of Biological Sciences, 1 Research Link, National University of Singapore, Singapore – name: 2 NUS Graduate School for Integrative Sciences and Engineering, Centre for Life Sciences, Singapore |
Author_xml | – sequence: 1 givenname: Wenhui surname: Zong fullname: Zong, Wenhui organization: Temasek Life Sciences Laboratory and Department of Biological Sciences, 1 Research Link, National University of Singapore, Singapore – sequence: 2 givenname: Yan surname: Wang fullname: Wang, Yan organization: Temasek Life Sciences Laboratory and Department of Biological Sciences, 1 Research Link, National University of Singapore, Singapore – sequence: 3 givenname: Quan surname: Tang fullname: Tang, Quan organization: Temasek Life Sciences Laboratory and Department of Biological Sciences, 1 Research Link, National University of Singapore, Singapore – sequence: 4 givenname: Heng surname: Zhang fullname: Zhang, Heng organization: Temasek Life Sciences Laboratory and Department of Biological Sciences, 1 Research Link, National University of Singapore, Singapore – sequence: 5 givenname: Fengwei orcidid: 0000-0003-0268-199X surname: Yu fullname: Yu, Fengwei organization: Neuroscience and Behavioral Disorder Program, Duke-NUS Graduate Medical School Singapore, Singapore |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30142146$$D View this record in MEDLINE/PubMed |
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Snippet | Refinement of the nervous system depends on selective removal of excessive axons/dendrites, a process known as pruning. Drosophila ddaC sensory neurons prune... Refinement of the nervous system depends on selective removal of excessive axons/dendrites, a process known as pruning. Drosophila ddaC sensory neurons prune... |
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SubjectTerms | Adaptin Autophagy Axons Biology and Life Sciences Cell adhesion Cell adhesion molecules Clathrin Defects Degradation Dendrites Drosophila Insects Kinases Kinesin Laboratories Life sciences Lysosomes Nervous system Neurodegeneration Neurons Proteins Pruning Research and Analysis Methods Sensory neurons Software |
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Title | Prd1 associates with the clathrin adaptor α-Adaptin and the kinesin-3 Imac/Unc-104 to govern dendrite pruning in Drosophila |
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