Protein tyrosine phosphatase σ regulates the synapse number of zebrafish olfactory sensory neurons
J. Neurochem. (2011) 119, 532–543. The formation and refinement of synaptic connections are key steps of neural development to establish elaborate brain networks. To investigate the functional role of protein tyrosine phosphatase (PTP) σ, we employed an olfactory sensory neuron (OSN)‐specific gene m...
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description | J. Neurochem. (2011) 119, 532–543.
The formation and refinement of synaptic connections are key steps of neural development to establish elaborate brain networks. To investigate the functional role of protein tyrosine phosphatase (PTP) σ, we employed an olfactory sensory neuron (OSN)‐specific gene manipulation system in combination with in vivo imaging of transparent zebrafish embryos. Knockdown of PTPσ enhanced the accumulation of synaptic vesicles in the axon terminals of OSNs. The exaggerated accumulation of synaptic vesicles was restored to the normal level by the OSN‐specific expression of PTPσ, indicating that presynaptic PTPσ is responsible for the regulation of synaptic vesicle accumulation. Consistently, transient expression of a dominant‐negative form of PTPσ in OSNs enhanced the accumulation of synaptic vesicles. The exaggerated accumulation of synaptic vesicles was reproduced in transgenic zebrafish lines carrying an OSN‐specific expression vector of the dominant‐negative PTPσ. By electron microscopic analysis of the transgenic line, we found the significant increase of the number of OSN‐mitral cell synapses in the central zone of the olfactory bulb. The density of docked vesicles at the active zone was also increased significantly. Our results suggest that presynaptic PTPσ controls the number of OSN‐mitral cell synapses by suppressing their excessive increase. |
doi_str_mv | 10.1111/j.1471-4159.2011.07411.x |
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The formation and refinement of synaptic connections are key steps of neural development to establish elaborate brain networks. To investigate the functional role of protein tyrosine phosphatase (PTP) σ, we employed an olfactory sensory neuron (OSN)‐specific gene manipulation system in combination with in vivo imaging of transparent zebrafish embryos. Knockdown of PTPσ enhanced the accumulation of synaptic vesicles in the axon terminals of OSNs. The exaggerated accumulation of synaptic vesicles was restored to the normal level by the OSN‐specific expression of PTPσ, indicating that presynaptic PTPσ is responsible for the regulation of synaptic vesicle accumulation. Consistently, transient expression of a dominant‐negative form of PTPσ in OSNs enhanced the accumulation of synaptic vesicles. The exaggerated accumulation of synaptic vesicles was reproduced in transgenic zebrafish lines carrying an OSN‐specific expression vector of the dominant‐negative PTPσ. By electron microscopic analysis of the transgenic line, we found the significant increase of the number of OSN‐mitral cell synapses in the central zone of the olfactory bulb. The density of docked vesicles at the active zone was also increased significantly. Our results suggest that presynaptic PTPσ controls the number of OSN‐mitral cell synapses by suppressing their excessive increase.</description><identifier>ISSN: 0022-3042</identifier><identifier>EISSN: 1471-4159</identifier><identifier>DOI: 10.1111/j.1471-4159.2011.07411.x</identifier><identifier>PMID: 21812780</identifier><identifier>CODEN: JONRA9</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Animals ; Animals, Genetically Modified ; Biological and medical sciences ; Cell Count ; Cell physiology ; docked vesicle ; Embryo, Nonmammalian - cytology ; Embryo, Nonmammalian - enzymology ; Fundamental and applied biological sciences. Psychology ; Gene Knockdown Techniques ; Genetic Vectors - chemistry ; Molecular and cellular biology ; Olfactory Receptor Neurons - cytology ; Olfactory Receptor Neurons - embryology ; Olfactory Receptor Neurons - enzymology ; olfactory sensory neuron ; Olfactory system and olfaction. Gustatory system and gustation ; presynaptic differentiation ; Promoter Regions, Genetic ; protein tyrosine phosphatase σ ; Receptor-Like Protein Tyrosine Phosphatases, Class 2 - chemistry ; Receptor-Like Protein Tyrosine Phosphatases, Class 2 - genetics ; Receptor-Like Protein Tyrosine Phosphatases, Class 2 - physiology ; Sensory Receptor Cells - cytology ; Sensory Receptor Cells - enzymology ; Signal transduction ; synapse formation ; Synapses - enzymology ; Synapses - genetics ; synaptic vesicle ; Vertebrates: nervous system and sense organs ; Zebrafish ; Zebrafish Proteins - chemistry ; Zebrafish Proteins - deficiency ; Zebrafish Proteins - physiology</subject><ispartof>Journal of neurochemistry, 2011-11, Vol.119 (3), p.532-543</ispartof><rights>2011 The Authors. Journal of Neurochemistry © 2011 International Society for Neurochemistry</rights><rights>2015 INIST-CNRS</rights><rights>2011 The Authors. Journal of Neurochemistry © 2011 International Society for Neurochemistry.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4481-fcdfed5900cfbb2690173f3b4aaa3362430e1da04a38544e7e029ee50e4435253</citedby><cites>FETCH-LOGICAL-c4481-fcdfed5900cfbb2690173f3b4aaa3362430e1da04a38544e7e029ee50e4435253</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1471-4159.2011.07411.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1471-4159.2011.07411.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24740800$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21812780$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Xigui</creatorcontrib><creatorcontrib>Yoshida, Tomoyuki</creatorcontrib><creatorcontrib>Sagara, Hiroshi</creatorcontrib><creatorcontrib>Mikami, Yoshinori</creatorcontrib><creatorcontrib>Mishina, Masayoshi</creatorcontrib><title>Protein tyrosine phosphatase σ regulates the synapse number of zebrafish olfactory sensory neurons</title><title>Journal of neurochemistry</title><addtitle>J Neurochem</addtitle><description>J. Neurochem. (2011) 119, 532–543.
The formation and refinement of synaptic connections are key steps of neural development to establish elaborate brain networks. To investigate the functional role of protein tyrosine phosphatase (PTP) σ, we employed an olfactory sensory neuron (OSN)‐specific gene manipulation system in combination with in vivo imaging of transparent zebrafish embryos. Knockdown of PTPσ enhanced the accumulation of synaptic vesicles in the axon terminals of OSNs. The exaggerated accumulation of synaptic vesicles was restored to the normal level by the OSN‐specific expression of PTPσ, indicating that presynaptic PTPσ is responsible for the regulation of synaptic vesicle accumulation. Consistently, transient expression of a dominant‐negative form of PTPσ in OSNs enhanced the accumulation of synaptic vesicles. The exaggerated accumulation of synaptic vesicles was reproduced in transgenic zebrafish lines carrying an OSN‐specific expression vector of the dominant‐negative PTPσ. By electron microscopic analysis of the transgenic line, we found the significant increase of the number of OSN‐mitral cell synapses in the central zone of the olfactory bulb. The density of docked vesicles at the active zone was also increased significantly. Our results suggest that presynaptic PTPσ controls the number of OSN‐mitral cell synapses by suppressing their excessive increase.</description><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Biological and medical sciences</subject><subject>Cell Count</subject><subject>Cell physiology</subject><subject>docked vesicle</subject><subject>Embryo, Nonmammalian - cytology</subject><subject>Embryo, Nonmammalian - enzymology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Knockdown Techniques</subject><subject>Genetic Vectors - chemistry</subject><subject>Molecular and cellular biology</subject><subject>Olfactory Receptor Neurons - cytology</subject><subject>Olfactory Receptor Neurons - embryology</subject><subject>Olfactory Receptor Neurons - enzymology</subject><subject>olfactory sensory neuron</subject><subject>Olfactory system and olfaction. Gustatory system and gustation</subject><subject>presynaptic differentiation</subject><subject>Promoter Regions, Genetic</subject><subject>protein tyrosine phosphatase σ</subject><subject>Receptor-Like Protein Tyrosine Phosphatases, Class 2 - chemistry</subject><subject>Receptor-Like Protein Tyrosine Phosphatases, Class 2 - genetics</subject><subject>Receptor-Like Protein Tyrosine Phosphatases, Class 2 - physiology</subject><subject>Sensory Receptor Cells - cytology</subject><subject>Sensory Receptor Cells - enzymology</subject><subject>Signal transduction</subject><subject>synapse formation</subject><subject>Synapses - enzymology</subject><subject>Synapses - genetics</subject><subject>synaptic vesicle</subject><subject>Vertebrates: nervous system and sense organs</subject><subject>Zebrafish</subject><subject>Zebrafish Proteins - chemistry</subject><subject>Zebrafish Proteins - deficiency</subject><subject>Zebrafish Proteins - physiology</subject><issn>0022-3042</issn><issn>1471-4159</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkM1u1DAQgC1ERbeFV0C-IE5Zxj_5O3BAK6CgqnCAs-V4x2xWWTt4ErXhygP2lUjYpb0yhxlL883Y_hjjAtZijjf7tdClyLTI67UEIdZQ6jnfPWGrh8ZTtgKQMlOg5Tm7INoDiEIX4hk7l6ISsqxgxdzXFAdsAx-mFKkNyPtdpH5nB0vI73_zhD_Gzg5IfNghpynYfm6E8dBg4tHzX9gk61va8dh564aYJk4YaKkBxxQDPWdn3naEL071kn3_8P7b5iq7_vLx0-bddea0rkTm3dbjNq8BnG8aWdQgSuVVo621ShVSK0CxtaCtqnKtsUSQNWIOqLXKZa4u2evj3j7FnyPSYA4tOew6GzCOZKq6yqGQAmayOpJu_jQl9KZP7cGmyQgwi2GzN4tIs4g0i2Hz17C5m0dfni4ZmwNuHwb_KZ2BVyfAkrOdTza4lh45XWqoYOHeHrnbtsPpvx9gPt9slpP6A5l-mMo</recordid><startdate>201111</startdate><enddate>201111</enddate><creator>Chen, Xigui</creator><creator>Yoshida, Tomoyuki</creator><creator>Sagara, Hiroshi</creator><creator>Mikami, Yoshinori</creator><creator>Mishina, Masayoshi</creator><general>Blackwell Publishing Ltd</general><general>Wiley-Blackwell</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>201111</creationdate><title>Protein tyrosine phosphatase σ regulates the synapse number of zebrafish olfactory sensory neurons</title><author>Chen, Xigui ; Yoshida, Tomoyuki ; Sagara, Hiroshi ; Mikami, Yoshinori ; Mishina, Masayoshi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4481-fcdfed5900cfbb2690173f3b4aaa3362430e1da04a38544e7e029ee50e4435253</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Animals</topic><topic>Animals, Genetically Modified</topic><topic>Biological and medical sciences</topic><topic>Cell Count</topic><topic>Cell physiology</topic><topic>docked vesicle</topic><topic>Embryo, Nonmammalian - cytology</topic><topic>Embryo, Nonmammalian - enzymology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Knockdown Techniques</topic><topic>Genetic Vectors - chemistry</topic><topic>Molecular and cellular biology</topic><topic>Olfactory Receptor Neurons - cytology</topic><topic>Olfactory Receptor Neurons - embryology</topic><topic>Olfactory Receptor Neurons - enzymology</topic><topic>olfactory sensory neuron</topic><topic>Olfactory system and olfaction. Gustatory system and gustation</topic><topic>presynaptic differentiation</topic><topic>Promoter Regions, Genetic</topic><topic>protein tyrosine phosphatase σ</topic><topic>Receptor-Like Protein Tyrosine Phosphatases, Class 2 - chemistry</topic><topic>Receptor-Like Protein Tyrosine Phosphatases, Class 2 - genetics</topic><topic>Receptor-Like Protein Tyrosine Phosphatases, Class 2 - physiology</topic><topic>Sensory Receptor Cells - cytology</topic><topic>Sensory Receptor Cells - enzymology</topic><topic>Signal transduction</topic><topic>synapse formation</topic><topic>Synapses - enzymology</topic><topic>Synapses - genetics</topic><topic>synaptic vesicle</topic><topic>Vertebrates: nervous system and sense organs</topic><topic>Zebrafish</topic><topic>Zebrafish Proteins - chemistry</topic><topic>Zebrafish Proteins - deficiency</topic><topic>Zebrafish Proteins - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Xigui</creatorcontrib><creatorcontrib>Yoshida, Tomoyuki</creatorcontrib><creatorcontrib>Sagara, Hiroshi</creatorcontrib><creatorcontrib>Mikami, Yoshinori</creatorcontrib><creatorcontrib>Mishina, Masayoshi</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of neurochemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Xigui</au><au>Yoshida, Tomoyuki</au><au>Sagara, Hiroshi</au><au>Mikami, Yoshinori</au><au>Mishina, Masayoshi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Protein tyrosine phosphatase σ regulates the synapse number of zebrafish olfactory sensory neurons</atitle><jtitle>Journal of neurochemistry</jtitle><addtitle>J Neurochem</addtitle><date>2011-11</date><risdate>2011</risdate><volume>119</volume><issue>3</issue><spage>532</spage><epage>543</epage><pages>532-543</pages><issn>0022-3042</issn><eissn>1471-4159</eissn><coden>JONRA9</coden><abstract>J. Neurochem. (2011) 119, 532–543.
The formation and refinement of synaptic connections are key steps of neural development to establish elaborate brain networks. To investigate the functional role of protein tyrosine phosphatase (PTP) σ, we employed an olfactory sensory neuron (OSN)‐specific gene manipulation system in combination with in vivo imaging of transparent zebrafish embryos. Knockdown of PTPσ enhanced the accumulation of synaptic vesicles in the axon terminals of OSNs. The exaggerated accumulation of synaptic vesicles was restored to the normal level by the OSN‐specific expression of PTPσ, indicating that presynaptic PTPσ is responsible for the regulation of synaptic vesicle accumulation. Consistently, transient expression of a dominant‐negative form of PTPσ in OSNs enhanced the accumulation of synaptic vesicles. The exaggerated accumulation of synaptic vesicles was reproduced in transgenic zebrafish lines carrying an OSN‐specific expression vector of the dominant‐negative PTPσ. By electron microscopic analysis of the transgenic line, we found the significant increase of the number of OSN‐mitral cell synapses in the central zone of the olfactory bulb. The density of docked vesicles at the active zone was also increased significantly. Our results suggest that presynaptic PTPσ controls the number of OSN‐mitral cell synapses by suppressing their excessive increase.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>21812780</pmid><doi>10.1111/j.1471-4159.2011.07411.x</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Animals, Genetically Modified Biological and medical sciences Cell Count Cell physiology docked vesicle Embryo, Nonmammalian - cytology Embryo, Nonmammalian - enzymology Fundamental and applied biological sciences. Psychology Gene Knockdown Techniques Genetic Vectors - chemistry Molecular and cellular biology Olfactory Receptor Neurons - cytology Olfactory Receptor Neurons - embryology Olfactory Receptor Neurons - enzymology olfactory sensory neuron Olfactory system and olfaction. Gustatory system and gustation presynaptic differentiation Promoter Regions, Genetic protein tyrosine phosphatase σ Receptor-Like Protein Tyrosine Phosphatases, Class 2 - chemistry Receptor-Like Protein Tyrosine Phosphatases, Class 2 - genetics Receptor-Like Protein Tyrosine Phosphatases, Class 2 - physiology Sensory Receptor Cells - cytology Sensory Receptor Cells - enzymology Signal transduction synapse formation Synapses - enzymology Synapses - genetics synaptic vesicle Vertebrates: nervous system and sense organs Zebrafish Zebrafish Proteins - chemistry Zebrafish Proteins - deficiency Zebrafish Proteins - physiology |
title | Protein tyrosine phosphatase σ regulates the synapse number of zebrafish olfactory sensory neurons |
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