Mismatched Appositions of Presynaptic and Postsynaptic Components in Isolated Hippocampal Neurons
To determine whether presynaptic input is necessary for postsynaptic differentiation, we isolated hippocampal neurons in microisland culture and thus deprived pyramidal cells of GABA input and GABAergic neurons of glutamate input. We find that glutamate input is necessary for clustering the AMPA-typ...
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| Veröffentlicht in: | The Journal of neuroscience 2000-11, Vol.20 (22), p.8344-8353 |
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| creator | Rao, Anuradha Cha, Eric M Craig, Ann Marie |
| description | To determine whether presynaptic input is necessary for postsynaptic differentiation, we isolated hippocampal neurons in microisland culture and thus deprived pyramidal cells of GABA input and GABAergic neurons of glutamate input. We find that glutamate input is necessary for clustering the AMPA-type glutamate receptor but not for clustering the NMDA receptor or the associated PSD-95 family scaffold in GABAergic cells; GABA input is not necessary for clustering the GABA(A) receptor or gephyrin in pyramidal cells. Isolated neurons showed a surprising mismatch of presynaptic and postsynaptic components. For example, in isolated pyramidal neurons, although GABA(A) receptor clusters covered |
| doi_str_mv | 10.1523/JNEUROSCI.20-22-08344.2000 |
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We find that glutamate input is necessary for clustering the AMPA-type glutamate receptor but not for clustering the NMDA receptor or the associated PSD-95 family scaffold in GABAergic cells; GABA input is not necessary for clustering the GABA(A) receptor or gephyrin in pyramidal cells. Isolated neurons showed a surprising mismatch of presynaptic and postsynaptic components. For example, in isolated pyramidal neurons, although GABA(A) receptor clusters covered <4% of the dendritic surface and presynaptic boutons covered <12%, a full two-thirds of the GABA(A) receptor clusters were localized inappropriately opposite the non-GABAergic, presumed glutamatergic, terminals. Furthermore, inhibitory and excitatory postsynaptic components were segregated into separate clusters in isolated cells and apposed to separate boutons of a single axon. Thus, GABA(A) receptors were clustered opposite some terminals, whereas NMDA receptors were clustered opposite other terminals of a single axon. These results suggest the involvement of a synaptogenic signal common to glutamate and GABA synapses that permits experimentally induced mismatching of presynaptic and postsynaptic components in isolated neurons, as well as a second specificity-conferring signal that mediates appropriate matching in mixed cultures.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.20-22-08344.2000</identifier><identifier>PMID: 11069941</identifier><language>eng</language><publisher>United States: Soc Neuroscience</publisher><subject>Animals ; Carrier Proteins - metabolism ; Cell Differentiation - physiology ; Cells, Cultured ; Disks Large Homolog 4 Protein ; Excitatory Postsynaptic Potentials - drug effects ; Excitatory Postsynaptic Potentials - physiology ; GABA-A Receptor Antagonists ; gamma-Aminobutyric Acid - metabolism ; gamma-Aminobutyric Acid - pharmacology ; Glutamate Decarboxylase - metabolism ; Glutamic Acid - metabolism ; Glutamic Acid - pharmacology ; Hippocampus - cytology ; Hippocampus - diagnostic imaging ; Hippocampus - drug effects ; Hippocampus - metabolism ; Intracellular Signaling Peptides and Proteins ; Membrane Proteins - metabolism ; Nerve Tissue Proteins - metabolism ; Neural Inhibition - physiology ; Neurons - cytology ; Neurons - drug effects ; Neurons - metabolism ; Pyramidal Cells - cytology ; Pyramidal Cells - drug effects ; Pyramidal Cells - metabolism ; Radionuclide Imaging ; Rats ; Receptor Aggregation - drug effects ; Receptor Aggregation - physiology ; Receptors, AMPA - antagonists & inhibitors ; Receptors, AMPA - metabolism ; Receptors, GABA-A - metabolism ; Receptors, Glutamate - metabolism ; Receptors, N-Methyl-D-Aspartate - antagonists & inhibitors ; Receptors, N-Methyl-D-Aspartate - metabolism ; Synapses - metabolism ; Synaptophysin - metabolism</subject><ispartof>The Journal of neuroscience, 2000-11, Vol.20 (22), p.8344-8353</ispartof><rights>Copyright © 2000 Society for Neuroscience 2000</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c485t-b69272f8cf106d81fe5e9f4143b0ce3aba6a39d3371dceab3d1d1e0b33e693</citedby><cites>FETCH-LOGICAL-c485t-b69272f8cf106d81fe5e9f4143b0ce3aba6a39d3371dceab3d1d1e0b33e693</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/PMC6773189/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6773189/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27923,27924,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/11069941$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rao, Anuradha</creatorcontrib><creatorcontrib>Cha, Eric M</creatorcontrib><creatorcontrib>Craig, Ann Marie</creatorcontrib><title>Mismatched Appositions of Presynaptic and Postsynaptic Components in Isolated Hippocampal Neurons</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>To determine whether presynaptic input is necessary for postsynaptic differentiation, we isolated hippocampal neurons in microisland culture and thus deprived pyramidal cells of GABA input and GABAergic neurons of glutamate input. We find that glutamate input is necessary for clustering the AMPA-type glutamate receptor but not for clustering the NMDA receptor or the associated PSD-95 family scaffold in GABAergic cells; GABA input is not necessary for clustering the GABA(A) receptor or gephyrin in pyramidal cells. Isolated neurons showed a surprising mismatch of presynaptic and postsynaptic components. For example, in isolated pyramidal neurons, although GABA(A) receptor clusters covered <4% of the dendritic surface and presynaptic boutons covered <12%, a full two-thirds of the GABA(A) receptor clusters were localized inappropriately opposite the non-GABAergic, presumed glutamatergic, terminals. Furthermore, inhibitory and excitatory postsynaptic components were segregated into separate clusters in isolated cells and apposed to separate boutons of a single axon. Thus, GABA(A) receptors were clustered opposite some terminals, whereas NMDA receptors were clustered opposite other terminals of a single axon. These results suggest the involvement of a synaptogenic signal common to glutamate and GABA synapses that permits experimentally induced mismatching of presynaptic and postsynaptic components in isolated neurons, as well as a second specificity-conferring signal that mediates appropriate matching in mixed cultures.</description><subject>Animals</subject><subject>Carrier Proteins - metabolism</subject><subject>Cell Differentiation - physiology</subject><subject>Cells, Cultured</subject><subject>Disks Large Homolog 4 Protein</subject><subject>Excitatory Postsynaptic Potentials - drug effects</subject><subject>Excitatory Postsynaptic Potentials - physiology</subject><subject>GABA-A Receptor Antagonists</subject><subject>gamma-Aminobutyric Acid - metabolism</subject><subject>gamma-Aminobutyric Acid - pharmacology</subject><subject>Glutamate Decarboxylase - metabolism</subject><subject>Glutamic Acid - metabolism</subject><subject>Glutamic Acid - pharmacology</subject><subject>Hippocampus - cytology</subject><subject>Hippocampus - diagnostic imaging</subject><subject>Hippocampus - drug effects</subject><subject>Hippocampus - metabolism</subject><subject>Intracellular Signaling Peptides and Proteins</subject><subject>Membrane Proteins - metabolism</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Neural Inhibition - physiology</subject><subject>Neurons - cytology</subject><subject>Neurons - drug effects</subject><subject>Neurons - metabolism</subject><subject>Pyramidal Cells - cytology</subject><subject>Pyramidal Cells - drug effects</subject><subject>Pyramidal Cells - metabolism</subject><subject>Radionuclide Imaging</subject><subject>Rats</subject><subject>Receptor Aggregation - drug effects</subject><subject>Receptor Aggregation - physiology</subject><subject>Receptors, AMPA - antagonists & inhibitors</subject><subject>Receptors, AMPA - metabolism</subject><subject>Receptors, GABA-A - metabolism</subject><subject>Receptors, Glutamate - metabolism</subject><subject>Receptors, N-Methyl-D-Aspartate - antagonists & inhibitors</subject><subject>Receptors, N-Methyl-D-Aspartate - metabolism</subject><subject>Synapses - metabolism</subject><subject>Synaptophysin - metabolism</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2000</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkctu2zAQRYmiReM8fqEQumhWSviSKHVRwDDSxEFeSNI1QVGjmIVEKiRdI38fOjbcdpUVB-SZg-FchL4SfEIKyk4vb85-3d8-zOYnFOeU5rhinKca4w9okog6pxyTj2iCqcB5yQXfQ_sh_E6AwER8RnuE4LKuOZkgdW3CoKJeQJtNx9EFE42zIXNdduchvFg1RqMzZdvszoW4u5i5YXQWbAyZsdk8uF7FpLgwyaHVMKo-u4GlT6pD9KlTfYCj7XmA7n-ePc4u8qvb8_lsepVrXhUxb8qaCtpVukuztRXpoIC644SzBmtgqlGlYnXLmCCtBtWwlrQEcMMYlDU7QD820nHZDJAAG73q5ejNoPyLdMrI_1-sWcgn90eWQjBSrQXftgLvnpcQohxM0ND3yoJbBinSSjnn4l2QiEoUvC4S-H0Dau9C8NDtpiFYrnOUuxwlxZJS-ZajXOeYmr_8-5-_rdvgEnC8ARbmabEyHmSKse8TTuRqtdoI1z72CvKbq9Y</recordid><startdate>20001115</startdate><enddate>20001115</enddate><creator>Rao, Anuradha</creator><creator>Cha, Eric M</creator><creator>Craig, Ann Marie</creator><general>Soc Neuroscience</general><general>Society for Neuroscience</general><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>7TK</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20001115</creationdate><title>Mismatched Appositions of Presynaptic and Postsynaptic Components in Isolated Hippocampal Neurons</title><author>Rao, Anuradha ; Cha, Eric M ; Craig, Ann Marie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c485t-b69272f8cf106d81fe5e9f4143b0ce3aba6a39d3371dceab3d1d1e0b33e693</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2000</creationdate><topic>Animals</topic><topic>Carrier Proteins - metabolism</topic><topic>Cell Differentiation - physiology</topic><topic>Cells, Cultured</topic><topic>Disks Large Homolog 4 Protein</topic><topic>Excitatory Postsynaptic Potentials - drug effects</topic><topic>Excitatory Postsynaptic Potentials - physiology</topic><topic>GABA-A Receptor Antagonists</topic><topic>gamma-Aminobutyric Acid - metabolism</topic><topic>gamma-Aminobutyric Acid - pharmacology</topic><topic>Glutamate Decarboxylase - metabolism</topic><topic>Glutamic Acid - metabolism</topic><topic>Glutamic Acid - pharmacology</topic><topic>Hippocampus - cytology</topic><topic>Hippocampus - diagnostic imaging</topic><topic>Hippocampus - drug effects</topic><topic>Hippocampus - metabolism</topic><topic>Intracellular Signaling Peptides and Proteins</topic><topic>Membrane Proteins - metabolism</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>Neural Inhibition - physiology</topic><topic>Neurons - cytology</topic><topic>Neurons - drug effects</topic><topic>Neurons - metabolism</topic><topic>Pyramidal Cells - cytology</topic><topic>Pyramidal Cells - drug effects</topic><topic>Pyramidal Cells - metabolism</topic><topic>Radionuclide Imaging</topic><topic>Rats</topic><topic>Receptor Aggregation - drug effects</topic><topic>Receptor Aggregation - physiology</topic><topic>Receptors, AMPA - antagonists & inhibitors</topic><topic>Receptors, AMPA - metabolism</topic><topic>Receptors, GABA-A - metabolism</topic><topic>Receptors, Glutamate - metabolism</topic><topic>Receptors, N-Methyl-D-Aspartate - antagonists & inhibitors</topic><topic>Receptors, N-Methyl-D-Aspartate - metabolism</topic><topic>Synapses - metabolism</topic><topic>Synaptophysin - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rao, Anuradha</creatorcontrib><creatorcontrib>Cha, Eric M</creatorcontrib><creatorcontrib>Craig, Ann Marie</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rao, Anuradha</au><au>Cha, Eric M</au><au>Craig, Ann Marie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mismatched Appositions of Presynaptic and Postsynaptic Components in Isolated Hippocampal Neurons</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2000-11-15</date><risdate>2000</risdate><volume>20</volume><issue>22</issue><spage>8344</spage><epage>8353</epage><pages>8344-8353</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>To determine whether presynaptic input is necessary for postsynaptic differentiation, we isolated hippocampal neurons in microisland culture and thus deprived pyramidal cells of GABA input and GABAergic neurons of glutamate input. We find that glutamate input is necessary for clustering the AMPA-type glutamate receptor but not for clustering the NMDA receptor or the associated PSD-95 family scaffold in GABAergic cells; GABA input is not necessary for clustering the GABA(A) receptor or gephyrin in pyramidal cells. Isolated neurons showed a surprising mismatch of presynaptic and postsynaptic components. For example, in isolated pyramidal neurons, although GABA(A) receptor clusters covered <4% of the dendritic surface and presynaptic boutons covered <12%, a full two-thirds of the GABA(A) receptor clusters were localized inappropriately opposite the non-GABAergic, presumed glutamatergic, terminals. Furthermore, inhibitory and excitatory postsynaptic components were segregated into separate clusters in isolated cells and apposed to separate boutons of a single axon. Thus, GABA(A) receptors were clustered opposite some terminals, whereas NMDA receptors were clustered opposite other terminals of a single axon. 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| subjects | Animals Carrier Proteins - metabolism Cell Differentiation - physiology Cells, Cultured Disks Large Homolog 4 Protein Excitatory Postsynaptic Potentials - drug effects Excitatory Postsynaptic Potentials - physiology GABA-A Receptor Antagonists gamma-Aminobutyric Acid - metabolism gamma-Aminobutyric Acid - pharmacology Glutamate Decarboxylase - metabolism Glutamic Acid - metabolism Glutamic Acid - pharmacology Hippocampus - cytology Hippocampus - diagnostic imaging Hippocampus - drug effects Hippocampus - metabolism Intracellular Signaling Peptides and Proteins Membrane Proteins - metabolism Nerve Tissue Proteins - metabolism Neural Inhibition - physiology Neurons - cytology Neurons - drug effects Neurons - metabolism Pyramidal Cells - cytology Pyramidal Cells - drug effects Pyramidal Cells - metabolism Radionuclide Imaging Rats Receptor Aggregation - drug effects Receptor Aggregation - physiology Receptors, AMPA - antagonists & inhibitors Receptors, AMPA - metabolism Receptors, GABA-A - metabolism Receptors, Glutamate - metabolism Receptors, N-Methyl-D-Aspartate - antagonists & inhibitors Receptors, N-Methyl-D-Aspartate - metabolism Synapses - metabolism Synaptophysin - metabolism |
| title | Mismatched Appositions of Presynaptic and Postsynaptic Components in Isolated Hippocampal Neurons |
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