Imaging ERK and PKA Activation in Single Dendritic Spines during Structural Plasticity
Extracellular signal-regulated kinase (ERK) and protein kinase A (PKA) play important roles in LTP and spine structural plasticity. While fluorescence resonance energy transfer (FRET)-based sensors for these kinases had previously been developed, they did not provide sufficient sensitivity for imagi...
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| Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2017-03, Vol.93 (6), p.1315-1324.e3 |
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| creator | Tang, Shen Yasuda, Ryohei |
| description | Extracellular signal-regulated kinase (ERK) and protein kinase A (PKA) play important roles in LTP and spine structural plasticity. While fluorescence resonance energy transfer (FRET)-based sensors for these kinases had previously been developed, they did not provide sufficient sensitivity for imaging small neuronal compartments, such as single dendritic spines in brain slices. Here we improved the sensitivity of FRET-based kinase sensors for monitoring kinase activity under two-photon fluorescence lifetime imaging microscopy (2pFLIM). Using these improved sensors, we succeeded in imaging ERK and PKA activation in single dendritic spines during structural long-term potentiation (sLTP) in hippocampal CA1 pyramidal neurons, revealing that the activation of these kinases spreads widely with length constants of more than 10 μm. The strategy for improvement of sensors used here should be applicable for developing highly sensitive biosensors for various protein kinases.
[Display omitted]
•Highly sensitive ERK and PKA FLIM sensors with novel fluorophore pair•Image ERK and PKA activation in single dendritic spines during structural plasticity•Mobile and immobilized sensors resolve spatiotemporal pattern of kinase activity
Tang and Yasuda designed highly sensitive sensors for ERK and PKA and measured the spatiotemporal dynamics of the activation of these kinases in dendrites during spine structural plasticity of single dendritic spines. |
| doi_str_mv | 10.1016/j.neuron.2017.02.032 |
| format | Article |
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[Display omitted]
•Highly sensitive ERK and PKA FLIM sensors with novel fluorophore pair•Image ERK and PKA activation in single dendritic spines during structural plasticity•Mobile and immobilized sensors resolve spatiotemporal pattern of kinase activity
Tang and Yasuda designed highly sensitive sensors for ERK and PKA and measured the spatiotemporal dynamics of the activation of these kinases in dendrites during spine structural plasticity of single dendritic spines.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2017.02.032</identifier><identifier>PMID: 28285819</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>A kinase-anchoring protein ; Actin ; Adenosine kinase ; Amino acid sequence ; Animals ; Biosensors ; Brain slice preparation ; CA1 Region, Hippocampal - metabolism ; Calcium influx ; Calcium signalling ; Cell activation ; Cells, Cultured ; Cerebellum ; Circular dichroism ; Cyclic AMP ; Cyclic AMP-Dependent Protein Kinases - metabolism ; Dendrites ; Dendritic Spines - enzymology ; Dendritic Spines - physiology ; Electrical stimuli ; Epidermal growth factor ; Extracellular Signal-Regulated MAP Kinases - metabolism ; Female ; FLIM ; Fluorescence Resonance Energy Transfer - methods ; FRET ; Hippocampus ; Humans ; kinase ; Kinases ; Long-term depression ; Long-term potentiation ; Long-Term Potentiation - physiology ; LTP ; Male ; Mice ; Microscopy, Fluorescence, Multiphoton ; Mutation ; Neuronal Plasticity - physiology ; Neurons ; Phosphorylation ; Protein kinase ; Proteins ; Pyramidal Cells - metabolism ; Rodents ; Sensors ; Signal transduction ; signaling ; synaptic plasticity ; Transcription factors ; α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</subject><ispartof>Neuron (Cambridge, Mass.), 2017-03, Vol.93 (6), p.1315-1324.e3</ispartof><rights>2017 Elsevier Inc.</rights><rights>Copyright © 2017 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Mar 22, 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c557t-aff00c59407fb0ac94a5ead767c499d1c77842543d4876253ecfee4766e1dbd3</citedby><cites>FETCH-LOGICAL-c557t-aff00c59407fb0ac94a5ead767c499d1c77842543d4876253ecfee4766e1dbd3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuron.2017.02.032$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3536,27903,27904,45974</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28285819$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tang, Shen</creatorcontrib><creatorcontrib>Yasuda, Ryohei</creatorcontrib><title>Imaging ERK and PKA Activation in Single Dendritic Spines during Structural Plasticity</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>Extracellular signal-regulated kinase (ERK) and protein kinase A (PKA) play important roles in LTP and spine structural plasticity. While fluorescence resonance energy transfer (FRET)-based sensors for these kinases had previously been developed, they did not provide sufficient sensitivity for imaging small neuronal compartments, such as single dendritic spines in brain slices. Here we improved the sensitivity of FRET-based kinase sensors for monitoring kinase activity under two-photon fluorescence lifetime imaging microscopy (2pFLIM). Using these improved sensors, we succeeded in imaging ERK and PKA activation in single dendritic spines during structural long-term potentiation (sLTP) in hippocampal CA1 pyramidal neurons, revealing that the activation of these kinases spreads widely with length constants of more than 10 μm. The strategy for improvement of sensors used here should be applicable for developing highly sensitive biosensors for various protein kinases.
[Display omitted]
•Highly sensitive ERK and PKA FLIM sensors with novel fluorophore pair•Image ERK and PKA activation in single dendritic spines during structural plasticity•Mobile and immobilized sensors resolve spatiotemporal pattern of kinase activity
Tang and Yasuda designed highly sensitive sensors for ERK and PKA and measured the spatiotemporal dynamics of the activation of these kinases in dendrites during spine structural plasticity of single dendritic spines.</description><subject>A kinase-anchoring protein</subject><subject>Actin</subject><subject>Adenosine kinase</subject><subject>Amino acid sequence</subject><subject>Animals</subject><subject>Biosensors</subject><subject>Brain slice preparation</subject><subject>CA1 Region, Hippocampal - metabolism</subject><subject>Calcium influx</subject><subject>Calcium signalling</subject><subject>Cell activation</subject><subject>Cells, Cultured</subject><subject>Cerebellum</subject><subject>Circular dichroism</subject><subject>Cyclic AMP</subject><subject>Cyclic AMP-Dependent Protein Kinases - metabolism</subject><subject>Dendrites</subject><subject>Dendritic Spines - enzymology</subject><subject>Dendritic Spines - physiology</subject><subject>Electrical stimuli</subject><subject>Epidermal growth factor</subject><subject>Extracellular Signal-Regulated MAP Kinases - metabolism</subject><subject>Female</subject><subject>FLIM</subject><subject>Fluorescence Resonance Energy Transfer - methods</subject><subject>FRET</subject><subject>Hippocampus</subject><subject>Humans</subject><subject>kinase</subject><subject>Kinases</subject><subject>Long-term depression</subject><subject>Long-term potentiation</subject><subject>Long-Term Potentiation - physiology</subject><subject>LTP</subject><subject>Male</subject><subject>Mice</subject><subject>Microscopy, Fluorescence, Multiphoton</subject><subject>Mutation</subject><subject>Neuronal Plasticity - physiology</subject><subject>Neurons</subject><subject>Phosphorylation</subject><subject>Protein kinase</subject><subject>Proteins</subject><subject>Pyramidal Cells - metabolism</subject><subject>Rodents</subject><subject>Sensors</subject><subject>Signal transduction</subject><subject>signaling</subject><subject>synaptic plasticity</subject><subject>Transcription factors</subject><subject>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UcFuEzEUtBAVDYU_QMgSFy67tb1ee31BitpSqlaiIhVXy7HfBkcbb7C9kfr3OEpbWg6c3uHNzJt5g9AHSmpKqDhd1wGmOIaaESprwmrSsFdoRomSFadKvUYz0ilRCSabY_Q2pTUhlLeKvkHHrGNd21E1Qz-vNmblwwpf_LjGJjh8ez3Hc5v9zmQ_BuwDXpT1APgcgos-e4sXWx8gYTfFPXGR42TzFM2AbweTCsDn-3foqDdDgvcP8wTdfb24O_tW3Xy_vDqb31S2bWWuTN8TYlvFieyXxFjFTQvGSSEtV8pRK2XHWcsbxzspWNuA7QG4FAKoW7rmBH05yG6n5QachZCLD72NfmPivR6N1y83wf_Sq3GnBeHlA7wIfH4QiOPvCVLWG58sDIMJME5J03K2oy1t9tBP_0DX4xRDSVdQxaVQomMFxQ8oG8eUIvRPZijR-970Wh960_veNGG69FZoH58HeSI9FvU3KZRv7jxEnayHYMH5CDZrN_r_X_gDEWqsDQ</recordid><startdate>20170322</startdate><enddate>20170322</enddate><creator>Tang, Shen</creator><creator>Yasuda, Ryohei</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</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>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20170322</creationdate><title>Imaging ERK and PKA Activation in Single Dendritic Spines during Structural Plasticity</title><author>Tang, Shen ; Yasuda, Ryohei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c557t-aff00c59407fb0ac94a5ead767c499d1c77842543d4876253ecfee4766e1dbd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>A kinase-anchoring protein</topic><topic>Actin</topic><topic>Adenosine kinase</topic><topic>Amino acid sequence</topic><topic>Animals</topic><topic>Biosensors</topic><topic>Brain slice preparation</topic><topic>CA1 Region, Hippocampal - metabolism</topic><topic>Calcium influx</topic><topic>Calcium signalling</topic><topic>Cell activation</topic><topic>Cells, Cultured</topic><topic>Cerebellum</topic><topic>Circular dichroism</topic><topic>Cyclic AMP</topic><topic>Cyclic AMP-Dependent Protein Kinases - metabolism</topic><topic>Dendrites</topic><topic>Dendritic Spines - enzymology</topic><topic>Dendritic Spines - physiology</topic><topic>Electrical stimuli</topic><topic>Epidermal growth factor</topic><topic>Extracellular Signal-Regulated MAP Kinases - metabolism</topic><topic>Female</topic><topic>FLIM</topic><topic>Fluorescence Resonance Energy Transfer - methods</topic><topic>FRET</topic><topic>Hippocampus</topic><topic>Humans</topic><topic>kinase</topic><topic>Kinases</topic><topic>Long-term depression</topic><topic>Long-term potentiation</topic><topic>Long-Term Potentiation - physiology</topic><topic>LTP</topic><topic>Male</topic><topic>Mice</topic><topic>Microscopy, Fluorescence, Multiphoton</topic><topic>Mutation</topic><topic>Neuronal Plasticity - physiology</topic><topic>Neurons</topic><topic>Phosphorylation</topic><topic>Protein kinase</topic><topic>Proteins</topic><topic>Pyramidal Cells - metabolism</topic><topic>Rodents</topic><topic>Sensors</topic><topic>Signal transduction</topic><topic>signaling</topic><topic>synaptic plasticity</topic><topic>Transcription factors</topic><topic>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tang, Shen</creatorcontrib><creatorcontrib>Yasuda, Ryohei</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tang, Shen</au><au>Yasuda, Ryohei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Imaging ERK and PKA Activation in Single Dendritic Spines during Structural Plasticity</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2017-03-22</date><risdate>2017</risdate><volume>93</volume><issue>6</issue><spage>1315</spage><epage>1324.e3</epage><pages>1315-1324.e3</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>Extracellular signal-regulated kinase (ERK) and protein kinase A (PKA) play important roles in LTP and spine structural plasticity. While fluorescence resonance energy transfer (FRET)-based sensors for these kinases had previously been developed, they did not provide sufficient sensitivity for imaging small neuronal compartments, such as single dendritic spines in brain slices. Here we improved the sensitivity of FRET-based kinase sensors for monitoring kinase activity under two-photon fluorescence lifetime imaging microscopy (2pFLIM). Using these improved sensors, we succeeded in imaging ERK and PKA activation in single dendritic spines during structural long-term potentiation (sLTP) in hippocampal CA1 pyramidal neurons, revealing that the activation of these kinases spreads widely with length constants of more than 10 μm. The strategy for improvement of sensors used here should be applicable for developing highly sensitive biosensors for various protein kinases.
[Display omitted]
•Highly sensitive ERK and PKA FLIM sensors with novel fluorophore pair•Image ERK and PKA activation in single dendritic spines during structural plasticity•Mobile and immobilized sensors resolve spatiotemporal pattern of kinase activity
Tang and Yasuda designed highly sensitive sensors for ERK and PKA and measured the spatiotemporal dynamics of the activation of these kinases in dendrites during spine structural plasticity of single dendritic spines.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>28285819</pmid><doi>10.1016/j.neuron.2017.02.032</doi><oa>free_for_read</oa></addata></record> |
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| ispartof | Neuron (Cambridge, Mass.), 2017-03, Vol.93 (6), p.1315-1324.e3 |
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| source | MEDLINE; Cell Press Free Archives; Elsevier ScienceDirect Journals; EZB-FREE-00999 freely available EZB journals |
| subjects | A kinase-anchoring protein Actin Adenosine kinase Amino acid sequence Animals Biosensors Brain slice preparation CA1 Region, Hippocampal - metabolism Calcium influx Calcium signalling Cell activation Cells, Cultured Cerebellum Circular dichroism Cyclic AMP Cyclic AMP-Dependent Protein Kinases - metabolism Dendrites Dendritic Spines - enzymology Dendritic Spines - physiology Electrical stimuli Epidermal growth factor Extracellular Signal-Regulated MAP Kinases - metabolism Female FLIM Fluorescence Resonance Energy Transfer - methods FRET Hippocampus Humans kinase Kinases Long-term depression Long-term potentiation Long-Term Potentiation - physiology LTP Male Mice Microscopy, Fluorescence, Multiphoton Mutation Neuronal Plasticity - physiology Neurons Phosphorylation Protein kinase Proteins Pyramidal Cells - metabolism Rodents Sensors Signal transduction signaling synaptic plasticity Transcription factors α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors |
| title | Imaging ERK and PKA Activation in Single Dendritic Spines during Structural Plasticity |
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