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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Veröffentlicht in:Journal of neurochemistry 2011-11, Vol.119 (3), p.532-543
Hauptverfasser: Chen, Xigui, Yoshida, Tomoyuki, Sagara, Hiroshi, Mikami, Yoshinori, Mishina, Masayoshi
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container_issue 3
container_start_page 532
container_title Journal of neurochemistry
container_volume 119
creator Chen, Xigui
Yoshida, Tomoyuki
Sagara, Hiroshi
Mikami, Yoshinori
Mishina, Masayoshi
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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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><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. 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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. 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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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