NMDA receptor-mediated PIP5K activation to produce PI(4,5)P₂ is essential for AMPA receptor endocytosis during LTD
NMDA receptor activation leads to clathrin-dependent endocytosis of postsynaptic AMPA receptors. Although this process controls long-term depression (LTD) induction in the hippocampus, how it is regulated by neuronal activities is not completely clear. Here, we show that Ca²⁺ influx through the NMDA...
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| Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2012-01, Vol.73 (1), p.135-148 |
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| creator | Unoki, Takamitsu Matsuda, Shinji Kakegawa, Wataru Van, Ngo Thai Bich Kohda, Kazuhisa Suzuki, Atsushi Funakoshi, Yuji Hasegawa, Hiroshi Yuzaki, Michisuke Kanaho, Yasunori |
| description | NMDA receptor activation leads to clathrin-dependent endocytosis of postsynaptic AMPA receptors. Although this process controls long-term depression (LTD) induction in the hippocampus, how it is regulated by neuronal activities is not completely clear. Here, we show that Ca²⁺ influx through the NMDA receptor activates calcineurin and protein phosphatase 1 to dephosphorylate phosphatidylinositol 4-phosphate 5-kinaseγ661 (PIP5Kγ661), the major phosphatidylinositol 4,5-bisphosphate (PI(4,5)P₂)-producing enzyme in the brain. Bimolecular fluorescence complementation analysis revealed that the dephosphorylated PIP5Kγ661 became associated with the clathrin adaptor protein complex AP-2 at postsynapses in situ. NMDA-induced AMPA receptor endocytosis and low-frequency stimulation-induced LTD were completely blocked by inhibiting the association between dephosphorylated PIP5Kγ661 and AP-2 and by overexpression of a kinase-dead PIP5Kγ661 mutant in hippocampal neurons. Furthermore, knockdown of PIP5Kγ661 inhibited the NMDA-induced AMPA receptor endocytosis. Therefore, NMDA receptor activation controls AMPA receptor endocytosis during hippocampal LTD by regulating PIP5Kγ661 activity at postsynapses. |
| doi_str_mv | 10.1016/j.neuron.2011.09.034 |
| format | Article |
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Although this process controls long-term depression (LTD) induction in the hippocampus, how it is regulated by neuronal activities is not completely clear. Here, we show that Ca²⁺ influx through the NMDA receptor activates calcineurin and protein phosphatase 1 to dephosphorylate phosphatidylinositol 4-phosphate 5-kinaseγ661 (PIP5Kγ661), the major phosphatidylinositol 4,5-bisphosphate (PI(4,5)P₂)-producing enzyme in the brain. Bimolecular fluorescence complementation analysis revealed that the dephosphorylated PIP5Kγ661 became associated with the clathrin adaptor protein complex AP-2 at postsynapses in situ. NMDA-induced AMPA receptor endocytosis and low-frequency stimulation-induced LTD were completely blocked by inhibiting the association between dephosphorylated PIP5Kγ661 and AP-2 and by overexpression of a kinase-dead PIP5Kγ661 mutant in hippocampal neurons. Furthermore, knockdown of PIP5Kγ661 inhibited the NMDA-induced AMPA receptor endocytosis. Therefore, NMDA receptor activation controls AMPA receptor endocytosis during hippocampal LTD by regulating PIP5Kγ661 activity at postsynapses.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2011.09.034</identifier><identifier>PMID: 22243752</identifier><language>eng</language><publisher>United States</publisher><subject>Actins - metabolism ; Adaptor Protein Complex 2 - metabolism ; Animals ; Animals, Newborn ; Biophysics ; Brain ; Cells, Cultured ; Disks Large Homolog 4 Protein ; Dose-Response Relationship, Drug ; Electric Stimulation ; Embryo, Mammalian ; Endocytosis - drug effects ; Endocytosis - genetics ; Endocytosis - physiology ; Enzyme Inhibitors - pharmacology ; Excitatory Amino Acid Agonists - pharmacology ; Gene Expression Regulation - drug effects ; Gene Expression Regulation - genetics ; Green Fluorescent Proteins - genetics ; Guanylate Kinases - metabolism ; Hippocampus - cytology ; Immunoprecipitation ; In Vitro Techniques ; Long-Term Synaptic Depression - drug effects ; Long-Term Synaptic Depression - genetics ; Long-Term Synaptic Depression - physiology ; Membrane Proteins - metabolism ; Mice ; Mice, Inbred ICR ; Mutation - genetics ; N-Methylaspartate - pharmacology ; Nerve Tissue Proteins - metabolism ; Neurons - drug effects ; Neurons - physiology ; Patch-Clamp Techniques ; Phosphotransferases (Alcohol Group Acceptor) - genetics ; Phosphotransferases (Alcohol Group Acceptor) - metabolism ; Protein Transport - drug effects ; Protein Transport - genetics ; Receptors, AMPA - genetics ; Receptors, AMPA - metabolism ; Receptors, N-Methyl-D-Aspartate - metabolism ; RNA, Small Interfering ; Time Factors ; Transfection</subject><ispartof>Neuron (Cambridge, Mass.), 2012-01, Vol.73 (1), p.135-148</ispartof><rights>Copyright © 2012 Elsevier Inc. 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Although this process controls long-term depression (LTD) induction in the hippocampus, how it is regulated by neuronal activities is not completely clear. Here, we show that Ca²⁺ influx through the NMDA receptor activates calcineurin and protein phosphatase 1 to dephosphorylate phosphatidylinositol 4-phosphate 5-kinaseγ661 (PIP5Kγ661), the major phosphatidylinositol 4,5-bisphosphate (PI(4,5)P₂)-producing enzyme in the brain. Bimolecular fluorescence complementation analysis revealed that the dephosphorylated PIP5Kγ661 became associated with the clathrin adaptor protein complex AP-2 at postsynapses in situ. NMDA-induced AMPA receptor endocytosis and low-frequency stimulation-induced LTD were completely blocked by inhibiting the association between dephosphorylated PIP5Kγ661 and AP-2 and by overexpression of a kinase-dead PIP5Kγ661 mutant in hippocampal neurons. Furthermore, knockdown of PIP5Kγ661 inhibited the NMDA-induced AMPA receptor endocytosis. Therefore, NMDA receptor activation controls AMPA receptor endocytosis during hippocampal LTD by regulating PIP5Kγ661 activity at postsynapses.</description><subject>Actins - metabolism</subject><subject>Adaptor Protein Complex 2 - metabolism</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Biophysics</subject><subject>Brain</subject><subject>Cells, Cultured</subject><subject>Disks Large Homolog 4 Protein</subject><subject>Dose-Response Relationship, Drug</subject><subject>Electric Stimulation</subject><subject>Embryo, Mammalian</subject><subject>Endocytosis - drug effects</subject><subject>Endocytosis - genetics</subject><subject>Endocytosis - physiology</subject><subject>Enzyme Inhibitors - pharmacology</subject><subject>Excitatory Amino Acid Agonists - pharmacology</subject><subject>Gene Expression Regulation - drug effects</subject><subject>Gene Expression Regulation - genetics</subject><subject>Green Fluorescent Proteins - genetics</subject><subject>Guanylate Kinases - metabolism</subject><subject>Hippocampus - cytology</subject><subject>Immunoprecipitation</subject><subject>In Vitro Techniques</subject><subject>Long-Term Synaptic Depression - drug effects</subject><subject>Long-Term Synaptic Depression - genetics</subject><subject>Long-Term Synaptic Depression - physiology</subject><subject>Membrane Proteins - metabolism</subject><subject>Mice</subject><subject>Mice, Inbred ICR</subject><subject>Mutation - genetics</subject><subject>N-Methylaspartate - pharmacology</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Neurons - drug effects</subject><subject>Neurons - physiology</subject><subject>Patch-Clamp Techniques</subject><subject>Phosphotransferases (Alcohol Group Acceptor) - genetics</subject><subject>Phosphotransferases (Alcohol Group Acceptor) - metabolism</subject><subject>Protein Transport - drug effects</subject><subject>Protein Transport - genetics</subject><subject>Receptors, AMPA - genetics</subject><subject>Receptors, AMPA - metabolism</subject><subject>Receptors, N-Methyl-D-Aspartate - metabolism</subject><subject>RNA, Small Interfering</subject><subject>Time Factors</subject><subject>Transfection</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkclOwzAQhi0EgrK8AUK-ARIJ3mLXx4pdFOgBzlZiT1CqNi62g9Qrj8qTkKosR05zmO-fGc2H0CElOSVUnk_zFrrg25wRSnOic8LFBhpQolUmqNabaECGWmaSKb6DdmOcEkJFoek22mGMCa4KNkDp8eFyhANYWCQfsjm4pkzg8ORuUtzj0qbmvUyNb3HyeBG86yz0vRNxVpxOPj8-cBMxxAhtasoZrn3Ao4fJ3zwMrfN2mXzsOdeFpn3F4-fLfbRVl7MIB991D71cXz1f3Gbjp5u7i9E4s5yLlClSO1EIqQmHitTcWSll5YQtqeJUuIqzoaVcck0LAFlXaqir2kkQ2kolHd9Dx-u5_eVvHcRk5k20MJuVLfguGs2I0lop_T9JZcGI1MOeFGvSBh9jgNosQjMvw9JQYlZizNSsxZiVGEO06cX0saPvBV3VP_k39GOCfwG7WotE</recordid><startdate>20120112</startdate><enddate>20120112</enddate><creator>Unoki, Takamitsu</creator><creator>Matsuda, Shinji</creator><creator>Kakegawa, Wataru</creator><creator>Van, Ngo Thai Bich</creator><creator>Kohda, Kazuhisa</creator><creator>Suzuki, Atsushi</creator><creator>Funakoshi, Yuji</creator><creator>Hasegawa, Hiroshi</creator><creator>Yuzaki, Michisuke</creator><creator>Kanaho, Yasunori</creator><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><scope>7TK</scope></search><sort><creationdate>20120112</creationdate><title>NMDA receptor-mediated PIP5K activation to produce PI(4,5)P₂ is essential for AMPA receptor endocytosis during LTD</title><author>Unoki, Takamitsu ; Matsuda, Shinji ; Kakegawa, Wataru ; Van, Ngo Thai Bich ; Kohda, Kazuhisa ; Suzuki, Atsushi ; Funakoshi, Yuji ; Hasegawa, Hiroshi ; Yuzaki, Michisuke ; Kanaho, Yasunori</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c334t-70fd4546903eb0f3dc666bd4ca17314db328c1363915ee6fb789bfd6e49c676d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Actins - metabolism</topic><topic>Adaptor Protein Complex 2 - metabolism</topic><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Biophysics</topic><topic>Brain</topic><topic>Cells, Cultured</topic><topic>Disks Large Homolog 4 Protein</topic><topic>Dose-Response Relationship, Drug</topic><topic>Electric Stimulation</topic><topic>Embryo, Mammalian</topic><topic>Endocytosis - drug effects</topic><topic>Endocytosis - genetics</topic><topic>Endocytosis - physiology</topic><topic>Enzyme Inhibitors - pharmacology</topic><topic>Excitatory Amino Acid Agonists - pharmacology</topic><topic>Gene Expression Regulation - drug effects</topic><topic>Gene Expression Regulation - genetics</topic><topic>Green Fluorescent Proteins - genetics</topic><topic>Guanylate Kinases - metabolism</topic><topic>Hippocampus - cytology</topic><topic>Immunoprecipitation</topic><topic>In Vitro Techniques</topic><topic>Long-Term Synaptic Depression - drug effects</topic><topic>Long-Term Synaptic Depression - genetics</topic><topic>Long-Term Synaptic Depression - physiology</topic><topic>Membrane Proteins - metabolism</topic><topic>Mice</topic><topic>Mice, Inbred ICR</topic><topic>Mutation - genetics</topic><topic>N-Methylaspartate - pharmacology</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>Neurons - drug effects</topic><topic>Neurons - physiology</topic><topic>Patch-Clamp Techniques</topic><topic>Phosphotransferases (Alcohol Group Acceptor) - genetics</topic><topic>Phosphotransferases (Alcohol Group Acceptor) - metabolism</topic><topic>Protein Transport - drug effects</topic><topic>Protein Transport - genetics</topic><topic>Receptors, AMPA - genetics</topic><topic>Receptors, AMPA - metabolism</topic><topic>Receptors, N-Methyl-D-Aspartate - metabolism</topic><topic>RNA, Small Interfering</topic><topic>Time Factors</topic><topic>Transfection</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Unoki, Takamitsu</creatorcontrib><creatorcontrib>Matsuda, Shinji</creatorcontrib><creatorcontrib>Kakegawa, Wataru</creatorcontrib><creatorcontrib>Van, Ngo Thai Bich</creatorcontrib><creatorcontrib>Kohda, Kazuhisa</creatorcontrib><creatorcontrib>Suzuki, Atsushi</creatorcontrib><creatorcontrib>Funakoshi, Yuji</creatorcontrib><creatorcontrib>Hasegawa, Hiroshi</creatorcontrib><creatorcontrib>Yuzaki, Michisuke</creatorcontrib><creatorcontrib>Kanaho, Yasunori</creatorcontrib><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><collection>Neurosciences Abstracts</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Unoki, Takamitsu</au><au>Matsuda, Shinji</au><au>Kakegawa, Wataru</au><au>Van, Ngo Thai Bich</au><au>Kohda, Kazuhisa</au><au>Suzuki, Atsushi</au><au>Funakoshi, Yuji</au><au>Hasegawa, Hiroshi</au><au>Yuzaki, Michisuke</au><au>Kanaho, Yasunori</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>NMDA receptor-mediated PIP5K activation to produce PI(4,5)P₂ is essential for AMPA receptor endocytosis during LTD</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2012-01-12</date><risdate>2012</risdate><volume>73</volume><issue>1</issue><spage>135</spage><epage>148</epage><pages>135-148</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>NMDA receptor activation leads to clathrin-dependent endocytosis of postsynaptic AMPA receptors. Although this process controls long-term depression (LTD) induction in the hippocampus, how it is regulated by neuronal activities is not completely clear. Here, we show that Ca²⁺ influx through the NMDA receptor activates calcineurin and protein phosphatase 1 to dephosphorylate phosphatidylinositol 4-phosphate 5-kinaseγ661 (PIP5Kγ661), the major phosphatidylinositol 4,5-bisphosphate (PI(4,5)P₂)-producing enzyme in the brain. Bimolecular fluorescence complementation analysis revealed that the dephosphorylated PIP5Kγ661 became associated with the clathrin adaptor protein complex AP-2 at postsynapses in situ. NMDA-induced AMPA receptor endocytosis and low-frequency stimulation-induced LTD were completely blocked by inhibiting the association between dephosphorylated PIP5Kγ661 and AP-2 and by overexpression of a kinase-dead PIP5Kγ661 mutant in hippocampal neurons. Furthermore, knockdown of PIP5Kγ661 inhibited the NMDA-induced AMPA receptor endocytosis. Therefore, NMDA receptor activation controls AMPA receptor endocytosis during hippocampal LTD by regulating PIP5Kγ661 activity at postsynapses.</abstract><cop>United States</cop><pmid>22243752</pmid><doi>10.1016/j.neuron.2011.09.034</doi><tpages>14</tpages></addata></record> |
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| subjects | Actins - metabolism Adaptor Protein Complex 2 - metabolism Animals Animals, Newborn Biophysics Brain Cells, Cultured Disks Large Homolog 4 Protein Dose-Response Relationship, Drug Electric Stimulation Embryo, Mammalian Endocytosis - drug effects Endocytosis - genetics Endocytosis - physiology Enzyme Inhibitors - pharmacology Excitatory Amino Acid Agonists - pharmacology Gene Expression Regulation - drug effects Gene Expression Regulation - genetics Green Fluorescent Proteins - genetics Guanylate Kinases - metabolism Hippocampus - cytology Immunoprecipitation In Vitro Techniques Long-Term Synaptic Depression - drug effects Long-Term Synaptic Depression - genetics Long-Term Synaptic Depression - physiology Membrane Proteins - metabolism Mice Mice, Inbred ICR Mutation - genetics N-Methylaspartate - pharmacology Nerve Tissue Proteins - metabolism Neurons - drug effects Neurons - physiology Patch-Clamp Techniques Phosphotransferases (Alcohol Group Acceptor) - genetics Phosphotransferases (Alcohol Group Acceptor) - metabolism Protein Transport - drug effects Protein Transport - genetics Receptors, AMPA - genetics Receptors, AMPA - metabolism Receptors, N-Methyl-D-Aspartate - metabolism RNA, Small Interfering Time Factors Transfection |
| title | NMDA receptor-mediated PIP5K activation to produce PI(4,5)P₂ is essential for AMPA receptor endocytosis during LTD |
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