Dexamethasone Rapidly Increases GABA Release in the Dorsal Motor Nucleus of the Vagus via Retrograde Messenger-Mediated Enhancement of TRPV1 Activity
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{"title"=>"Dexamethasone Rapidly Increases GABA Release in the Dorsal Motor Nucleus of the Vagus via Retrograde Messenger-Mediated Enhancement of TRPV1 Activity", "type"=>"journal", "authors"=>[{"first_name"=>"Andrei V.", "last_name"=>"Derbenev", "scopus_author_id"=>"6506738218"}, {"first_name"=>"Bret N.", "last_name"=>"Smith", "scopus_author_id"=>"35485984100"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84880790040", "pmid"=>"23936221", "scopus"=>"2-s2.0-84880790040", "issn"=>"19326203", "pui"=>"369443181", "doi"=>"10.1371/journal.pone.0070505"}, "id"=>"ef74b7dd-7c44-32d8-9d3f-7c1f8512689e", "abstract"=>"Glucocorticoids influence vagal parasympathetic output to the viscera via mechanisms that include modulation of neural circuitry in the dorsal vagal complex, a principal autonomic regulatory center. Glucocorticoids can modulate synaptic neurotransmitter release elsewhere in the brain by inducing release of retrograde signalling molecules. We tested the hypothesis that the glucocorticoid agonist dexamethasone (DEX) modulates GABA release in the rat dorsal motor nucleus of the vagus (DMV). Whole-cell patch-clamp recordings revealed that DEX (1-10 µM) rapidly (i.e. within three minutes) increased the frequency of tetrodotoxin-resistant, miniature IPSCs (mIPSCs) in 67% of DMV neurons recorded in acutely prepared slices. Glutamate-mediated mEPSCs were also enhanced by DEX (10 µM), and blockade of ionotropic glutamate receptors reduced the DEX effect on mIPSC frequency. Antagonists of type I or II corticosteroid receptors blocked the effect of DEX on mIPSCs. The effect was mimicked by application of the membrane-impermeant BSA-conjugated DEX, and intracellular blockade of G protein function with GDP βS in the recorded cell prevented the effect of DEX. The enhancement of GABA release was blocked by the TRPV1 antagonists, 5'-iodoresiniferatoxin or capsazepine, but was not altered by the cannabinoid type 1 receptor antagonist AM251. The DEX effect was prevented by blocking fatty acid amide hydrolysis or by inhibiting anandamide transport, implicating involvement of the endocannabinoid system in the response. These findings indicate that DEX induces an enhancement of GABA release in the DMV, which is mediated by activation of TRPV1 receptors on afferent terminals. The effect is likely induced by anandamide or other 'endovanilloid', suggesting activation of a local retrograde signal originating from DMV neurons to enhance synaptic inhibition locally in response to glucocorticoids.", "link"=>"http://www.mendeley.com/research/dexamethasone-rapidly-increases-gaba-release-dorsal-motor-nucleus-vagus-via-retrograde-messengermedi", "reader_count"=>26, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Student > Doctoral Student"=>2, "Researcher"=>8, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>2, "Other"=>2, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Student > Doctoral Student"=>2, "Researcher"=>8, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>2, "Other"=>2, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>7, "Medicine and Dentistry"=>7, "Neuroscience"=>7}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Neuroscience"=>{"Neuroscience"=>7}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>7}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>4}}, "reader_count_by_country"=>{"United States"=>2, "Japan"=>1, "Chile"=>1, "Portugal"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1137437"], "description"=>"<p><b>A</b>. Continuous recording of mIPSCs observed at holding potential of -10 mV. <b>B</b>. mIPSCs recorded after application of a membrane-impermeable, BSA-conjugated DEX (10 µM). <b>A<sub>1</sub></b> and <b>B<sub>1</sub></b> are temporally-expanded, 2 s sections from boxed areas of traces A and B above (arrows). <b>C</b>. Cumulative plots of the inter-event interval distribution for mIPSCs before and after application of BSA-conjugated DEX from the recording in A and B (<i>P</i><0.05; K–S test). <b>D</b>. Changes in mIPSC frequency in responsive DMV neurons after 3 min application of BSA-conjugated DEX (10 µM; n=7; p<0.05).</p>", "links"=>[], "tags"=>["membrane", "impermeant", "bsa-conjugated", "dex", "enhanced", "mipsc", "suggesting", "activation", "nonclassical", "membrane-associated", "glucocorticoid"], "article_id"=>760094, "categories"=>["Biological Sciences"], "users"=>["Andrei V. Derbenev", "Bret N. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0070505.g003", "stats"=>{"downloads"=>0, "page_views"=>31, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_membrane_impermeant_BSA_conjugated_DEX_enhanced_mIPSC_frequency_suggesting_activation_of_a_nonclassical_membrane_associated_glucocorticoid_receptor_/760094", "title"=>"The membrane impermeant BSA-conjugated DEX enhanced mIPSC frequency, suggesting activation of a nonclassical membrane-associated glucocorticoid receptor.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-30 11:03:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1137434"], "description"=>"<p><b>A</b>. Continuous recording of mIPSCs observed at holding potential of -10 mV in the presence of tetrodotoxin (TTX; 1 µM). <b>B</b>. Recording of mIPSCs in the same cell after application of DEX (10 µM). <b>A<sub>1</sub></b> and <b>B<sub>1</sub></b> are temporally-expanded, 2 s sections from boxed areas of traces A and B, respectively. Recording pipette contained 140 mM Cs<sup>+</sup>. <b>C</b>. Cumulative frequency plots of the inter-event interval distribution for mIPSCs before and after application of DEX for the recording in A and B. A significant effect of DEX was detected in this cell using the Kolmogorov-Smirnov (K–S) test (<i>P</i><0.05). <b>D</b>. Change in mIPSC frequency observed 3 min after DEX application in DMV neurons that were determined to have responded to DEX by K–S test (n=8; p<0.05). <b>E</b>. The effect of DEX in responding cells as a function of concentration. The effect of the highest DEX concentration (10 µM) in the presence of kynurenic acid (KYN; 1 mM) is also shown. Numbers in parentheses above the bars indicate number of replicates; error bars indicate SE.</p>", "links"=>[], "tags"=>["mipsc", "dmv"], "article_id"=>760091, "categories"=>["Biological Sciences"], "users"=>["Andrei V. Derbenev", "Bret N. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0070505.g001", "stats"=>{"downloads"=>0, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dexamethasone_increases_mIPSC_frequency_in_DMV_neurons_/760091", "title"=>"Dexamethasone increases mIPSC frequency in DMV neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-30 11:03:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1137441"], "description"=>"<p>The effect of DEX on mIPSC frequency was prevented in the presence of the fatty acid amide hydrolyse (FAAH) inhibitor, URB597 (10 µM; n=11; P>0.05). Blocking anandamide transport with OMDM-2 (10 µM; n=6; P>0.05) or O-2093 (10 µM; n=6; P>0.05) also prevented the effect of DEX on mIPSC frequency.</p>", "links"=>[], "tags"=>["anandamide", "metabolism", "prevented"], "article_id"=>760098, "categories"=>["Biological Sciences"], "users"=>["Andrei V. Derbenev", "Bret N. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0070505.g006", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Blockade_of_anandamide_metabolism_or_transport_prevented_the_effect_of_DEX_/760098", "title"=>"Blockade of anandamide metabolism or transport prevented the effect of DEX.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-30 11:03:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1137436"], "description"=>"<p><b>A</b>. Continuous recordings of mIPSCs at a holding potential of -10 mV in the presence of the type I corticosteroid receptor antagonist, spironolactone (1 µM). <b>B</b>. The same cell after co-application of DEX (10 µM). <b>A<sub>1</sub></b> and <b>B<sub>1</sub></b> are temporally-expanded, 2 s sections from boxed areas of traces A and B (arrows). <b>C</b>. The DEX-induced increase in mIPSC frequency was never observed in the presence of type I and II corticosteroid receptors antagonists spironolactone (1 µM; n=9; p>0.05) or mifepristone (1 µM; n=9; p>0.05). Error bars indicate SE.</p>", "links"=>[], "tags"=>["glucocorticoid", "prevented", "receptor"], "article_id"=>760093, "categories"=>["Biological Sciences"], "users"=>["Andrei V. Derbenev", "Bret N. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0070505.g002", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rapid_glucocorticoid_effects_are_prevented_by_glucocorticoid_receptor_blockade_/760093", "title"=>"Rapid glucocorticoid effects are prevented by glucocorticoid receptor blockade.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-30 11:03:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1137440"], "description"=>"<p><b>A</b>. Continuous recordings of mIPSCs at a holding potential of -10 mV in the presence of the TRPV1 antagonist, 5’-iodoresiniferatoxin (5’-iRFT; 1 µM). <b>B</b>. The same cell after application of DEX (10 µM). <b>A<sub>1</sub></b> and <b>B<sub>1</sub></b> are temporally-expanded, 2 s sections from boxed areas of traces A and B (arrows). <b>C</b>. Cumulative frequency plots of data from the recording shown in A and B indicate no DEX-induced change in mIPSC inter-event interval (P>0.05; K–S test). <b>D</b>. The DEX-induced increase in mIPSC frequency was blocked with bath pre-application of 5’-iRFT (n=12; p>0.05) or capsazepine (CPZ; 10 µM; n=6; P>0.05). <b>E</b>. Application of DEX increased mIPSC frequency in the presence of the cannabinoid type 1 receptor antagonist, AM251 (20 µM; n=8; p<0.05).</p>", "links"=>[], "tags"=>["glucocorticoid-induced", "mipsc", "blocked", "trpv1"], "article_id"=>760097, "categories"=>["Biological Sciences"], "users"=>["Andrei V. Derbenev", "Bret N. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0070505.g005", "stats"=>{"downloads"=>3, "page_views"=>102, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_glucocorticoid_induced_increase_in_mIPSC_frequency_is_blocked_by_TRPV1_antagonists_/760097", "title"=>"The glucocorticoid-induced increase in mIPSC frequency is blocked by TRPV1 antagonists.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-30 11:03:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1137438"], "description"=>"<p><b>A</b>. Continuous recordings recording of mIPSCs after loading of the recorded cell with the G protein inhibitor, GDP <sub>β</sub>S (500 µM in the recording pipette). <b>B</b>. mIPSCs recorded in the same neuron after application of DEX (10 µM). <b>A<sub>1</sub></b> and <b>B<sub>1</sub></b> are temporally-expanded, 2 s sections from boxed areas of traces A and B (arrows). <b>C</b>. Cumulative plots of the inter-event interval distribution for mIPSCs in the GDP <sub>β</sub>S-loaded cell shown in A and B indicates no effect of DEX (<i>P</i>>0.05; K–S test). <b>D</b>. Graph of mean mIPSC frequency before and after DEX application in GDP <sub>β</sub>S-loaded neurons. No effect of DEX was observed in any neuron (n=13; P>0.05).</p>", "links"=>[], "tags"=>["protein-mediated", "responses", "recorded", "neuron", "prevents", "dex-induced", "mipsc"], "article_id"=>760095, "categories"=>["Biological Sciences"], "users"=>["Andrei V. Derbenev", "Bret N. Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0070505.g004", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Blockade_of_G_protein_mediated_responses_in_the_recorded_neuron_prevents_the_DEX_induced_change_in_mIPSC_frequency_/760095", "title"=>"Blockade of G protein-mediated responses in the recorded neuron prevents the DEX-induced change in mIPSC frequency.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-30 11:03:50"}

PMC Usage Stats | Further Information

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Relative Metric

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