Regulation of neuronal morphogenesis and positioning by ubiquitin-specific proteases in the cerebellum
Ubiquitin signaling mechanisms play fundamental roles in the cell-intrinsic control of neuronal morphogenesis and connectivity in the brain. However, whereas specific ubiquitin ligases have been implicated in key steps of neural circuit assembly, the roles of ubiquitin-specific proteases (USPs) in t...
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| description | Ubiquitin signaling mechanisms play fundamental roles in the cell-intrinsic control of neuronal morphogenesis and connectivity in the brain. However, whereas specific ubiquitin ligases have been implicated in key steps of neural circuit assembly, the roles of ubiquitin-specific proteases (USPs) in the establishment of neuronal connectivity have remained unexplored. Here, we report a comprehensive analysis of USP family members in granule neuron morphogenesis and positioning in the rodent cerebellum. We identify a set of 32 USPs that are expressed in granule neurons. We also characterize the subcellular localization of the 32 USPs in granule neurons using a library of expression plasmids encoding GFP-USPs. In RNAi screens of the 32 neuronally expressed USPs, we uncover novel functions for USP1, USP4, and USP20 in the morphogenesis of granule neuron dendrites and axons and we identify a requirement for USP30 and USP33 in granule neuron migration in the rodent cerebellar cortex in vivo. These studies reveal that specific USPs with distinct spatial localizations harbor key functions in the control of neuronal morphogenesis and positioning in the mammalian cerebellum, with important implications for our understanding of the cell-intrinsic mechanisms that govern neural circuit assembly in the brain. |
| doi_str_mv | 10.1371/journal.pone.0117076 |
| format | Article |
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However, whereas specific ubiquitin ligases have been implicated in key steps of neural circuit assembly, the roles of ubiquitin-specific proteases (USPs) in the establishment of neuronal connectivity have remained unexplored. Here, we report a comprehensive analysis of USP family members in granule neuron morphogenesis and positioning in the rodent cerebellum. We identify a set of 32 USPs that are expressed in granule neurons. We also characterize the subcellular localization of the 32 USPs in granule neurons using a library of expression plasmids encoding GFP-USPs. In RNAi screens of the 32 neuronally expressed USPs, we uncover novel functions for USP1, USP4, and USP20 in the morphogenesis of granule neuron dendrites and axons and we identify a requirement for USP30 and USP33 in granule neuron migration in the rodent cerebellar cortex in vivo. These studies reveal that specific USPs with distinct spatial localizations harbor key functions in the control of neuronal morphogenesis and positioning in the mammalian cerebellum, with important implications for our understanding of the cell-intrinsic mechanisms that govern neural circuit assembly in the brain.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0117076</identifier><identifier>PMID: 25607801</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Assembly ; Axons ; Axons - metabolism ; Brain ; Cell cycle ; Cell migration ; Cells, Cultured ; Cerebellum ; Cerebellum - cytology ; Cerebellum - enzymology ; Cerebellum - growth & development ; Connectivity ; Dendrites ; Dendrites - metabolism ; Enzymes ; Granular materials ; Granule cells ; In vivo methods and tests ; Kinases ; Ligases ; Localization ; Medical schools ; Morphogenesis ; Neural circuitry ; Neural networks ; Neurobiology ; Neurons ; Neurosciences ; Plasmids ; Positioning devices (machinery) ; Proteases ; Proteins ; Rats ; RNA-mediated interference ; Screens ; Signal Transduction ; Signaling ; Spatial discrimination ; Ubiquitin ; Ubiquitin - metabolism ; Ubiquitin-Specific Proteases - genetics ; Ubiquitin-Specific Proteases - metabolism</subject><ispartof>PloS one, 2015-01, Vol.10 (1), p.e0117076-e0117076</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Anckar, Bonni. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Anckar, Bonni 2015 Anckar, Bonni</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c622t-abf389a8a86fdaf428b18d162c4355c00287155c0115c40b3b5cfab481bd58633</citedby><cites>FETCH-LOGICAL-c622t-abf389a8a86fdaf428b18d162c4355c00287155c0115c40b3b5cfab481bd58633</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4301861/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4301861/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25607801$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Anckar, Julius</creatorcontrib><creatorcontrib>Bonni, Azad</creatorcontrib><title>Regulation of neuronal morphogenesis and positioning by ubiquitin-specific proteases in the cerebellum</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Ubiquitin signaling mechanisms play fundamental roles in the cell-intrinsic control of neuronal morphogenesis and connectivity in the brain. However, whereas specific ubiquitin ligases have been implicated in key steps of neural circuit assembly, the roles of ubiquitin-specific proteases (USPs) in the establishment of neuronal connectivity have remained unexplored. Here, we report a comprehensive analysis of USP family members in granule neuron morphogenesis and positioning in the rodent cerebellum. We identify a set of 32 USPs that are expressed in granule neurons. We also characterize the subcellular localization of the 32 USPs in granule neurons using a library of expression plasmids encoding GFP-USPs. In RNAi screens of the 32 neuronally expressed USPs, we uncover novel functions for USP1, USP4, and USP20 in the morphogenesis of granule neuron dendrites and axons and we identify a requirement for USP30 and USP33 in granule neuron migration in the rodent cerebellar cortex in vivo. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Anckar, Julius</au><au>Bonni, Azad</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Regulation of neuronal morphogenesis and positioning by ubiquitin-specific proteases in the cerebellum</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-01-21</date><risdate>2015</risdate><volume>10</volume><issue>1</issue><spage>e0117076</spage><epage>e0117076</epage><pages>e0117076-e0117076</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Ubiquitin signaling mechanisms play fundamental roles in the cell-intrinsic control of neuronal morphogenesis and connectivity in the brain. However, whereas specific ubiquitin ligases have been implicated in key steps of neural circuit assembly, the roles of ubiquitin-specific proteases (USPs) in the establishment of neuronal connectivity have remained unexplored. Here, we report a comprehensive analysis of USP family members in granule neuron morphogenesis and positioning in the rodent cerebellum. We identify a set of 32 USPs that are expressed in granule neurons. We also characterize the subcellular localization of the 32 USPs in granule neurons using a library of expression plasmids encoding GFP-USPs. In RNAi screens of the 32 neuronally expressed USPs, we uncover novel functions for USP1, USP4, and USP20 in the morphogenesis of granule neuron dendrites and axons and we identify a requirement for USP30 and USP33 in granule neuron migration in the rodent cerebellar cortex in vivo. These studies reveal that specific USPs with distinct spatial localizations harbor key functions in the control of neuronal morphogenesis and positioning in the mammalian cerebellum, with important implications for our understanding of the cell-intrinsic mechanisms that govern neural circuit assembly in the brain.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25607801</pmid><doi>10.1371/journal.pone.0117076</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Analysis Animals Assembly Axons Axons - metabolism Brain Cell cycle Cell migration Cells, Cultured Cerebellum Cerebellum - cytology Cerebellum - enzymology Cerebellum - growth & development Connectivity Dendrites Dendrites - metabolism Enzymes Granular materials Granule cells In vivo methods and tests Kinases Ligases Localization Medical schools Morphogenesis Neural circuitry Neural networks Neurobiology Neurons Neurosciences Plasmids Positioning devices (machinery) Proteases Proteins Rats RNA-mediated interference Screens Signal Transduction Signaling Spatial discrimination Ubiquitin Ubiquitin - metabolism Ubiquitin-Specific Proteases - genetics Ubiquitin-Specific Proteases - metabolism |
| title | Regulation of neuronal morphogenesis and positioning by ubiquitin-specific proteases in the cerebellum |
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