Characterization of a Prawn OA/TA Receptor in Xenopus Oocytes Suggests Functional Selectivity between Octopamine and Tyramine
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{"title"=>"Characterization of a prawn OA/TA receptor in xenopus oocytes suggests functional selectivity between octopamine and tyramine", "type"=>"journal", "authors"=>[{"first_name"=>"Sami H.", "last_name"=>"Jezzini", "scopus_author_id"=>"6507531036"}, {"first_name"=>"Dalynés S.", "last_name"=>"Reyes-Colón", "scopus_author_id"=>"26421747200"}, {"first_name"=>"María A.", "last_name"=>"Sosa", "scopus_author_id"=>"7005907750"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84908565783", "issn"=>"19326203", "pmid"=>"25350749", "doi"=>"10.1371/journal.pone.0111314", "pui"=>"600310444", "scopus"=>"2-s2.0-84908565783"}, "id"=>"5dad258d-5c8a-3a82-a772-0f7c71e6c1e9", "abstract"=>"Here we report the characterization of an octopamine/tyramine (OA/TA or TyrR1) receptor (OA/TAMac) cloned from the freshwater prawn, Macrobrachium rosenbergii, an animal used in the study of agonistic social behavior. The invertebrate OA/TA receptors are seven trans-membrane domain G-protein coupled receptors that are related to vertebrate adrenergic receptors. Behavioral studies in arthropods indicate that octopaminergic signaling systems modulate fight or flight behaviors with octopamine and/or tyramine functioning in a similar way to the adrenalins in vertebrate systems. Despite the importance of octopamine signaling in behavioral studies of decapod crustaceans there are no functional data available for any of their octopamine or tyramine receptors. We expressed OA/TAMac in Xenopus oocytes where agonist-evoked trans-membrane currents were used as readouts of receptor activity. The currents were most effectively evoked by tyramine but were also evoked by octopamine and dopamine. They were effectively blocked by yohimbine. The electrophysiological approach we used enabled the continuous observation of complex dynamics over time. Using voltage steps, we were able to simultaneously resolve two types of endogenous currents that are affected over different time scales. At higher concentrations we observe that octopamine and tyramine can produce different and opposing effects on both of these currents, presumably through the activity of the single expressed receptor type. The pharmacological profile and apparent functional-selectivity are consistent with properties first observed in the OA/TA receptor from the insect Drosophila melanogaster. As the first functional data reported for any crustacean OA/TA receptor, these results suggest that functional-selectivity between tyramine and octopamine is a feature of this receptor type that may be conserved among arthropods.", "link"=>"http://www.mendeley.com/research/characterization-prawn-oata-receptor-xenopus-oocytes-suggests-functional-selectivity-between-octopam", "reader_count"=>6, "reader_count_by_academic_status"=>{"Researcher"=>2, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>2, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Agricultural and Biological Sciences"=>4, "Neuroscience"=>1}, "reader_count_by_subdiscipline"=>{"Neuroscience"=>{"Neuroscience"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>4}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1768302"], "description"=>"<p>The biogenic amines are structurally similar small molecules. Tyramine, octopamine, dopamine, and histamine are naturally occurring <i>bona fide</i> neurotransmitters in invertebrates. In vertebrates β-phenylethylamine is a trace amine and synephrine is a synthetic adrenergic receptor agonist.</p>", "links"=>[], "tags"=>["tyramine", "Xenopus Oocytes Suggests Functional Selectivity", "octopamine", "insect Drosophila melanogaster", "oa", "receptor type"], "article_id"=>1220981, "categories"=>["Biological Sciences"], "users"=>["Sami H. Jezzini", "Dalynés Reyes-Colón", "María A. Sosa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111314.g001", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Aminergic_agonists_tested_on_OA_TA_Mac_/1220981", "title"=>"Aminergic agonists tested on OA/TA<sub>Mac</sub>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-28 19:05:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1768334"], "description"=>"<p>(<b>A</b>) A concentration series applied to a single oocyte. Color-coding corresponds to the same responses examined in more detail in B and C. (<b>B</b>) The low amplitude of the TA response was not due to cumulative buildup of desensitization because it could be observed upon the first high-concentration application. An initial 100 µM TA response (black) is aligned by the stimulus application (black bar) with a second 100 µM response (grey). The plateau amplitude changes very little between the first and second response indicating that the small size is not a function of repetitive application. Desensitization of the second response is apparent in the tail as a reduction in amplitude, and as a loss of minor oscillation. (<b>C</b>) The plateau limits he amplitude of the TA response. Responses from A (color coded from 0.1 µM to 1000 µM) are aligned by the response onset and overlaid. The rank-order of rise rate at the initial rise (asterisk) and amplitudes at points indicated are listed from lowest to highest. The rise rate appears to be a direct function of concentration. The tail amplitude after the second rise is also a direct function of concentration, whereas the plateau amplitude becomes an inverse function at higher concentrations. This indicates that rise rate and plateau amplitude are distinct functions of concentration. (<b>D</b>) A quantitative analysis of the observations in C shows that the process underlying the plateau is specific to TA. The scatter-plot shows the amplitude of each individual response plotted against its maximum rise-rate. Data include all responses from experiments plotted in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0111314#pone-0111314-g003\" target=\"_blank\">Figure 3C</a>. The Spearman rank-order correlation (r<sub>S</sub>) between rise rate and peak amplitude for TA evoked responses is relatively weak (r<sub>S</sub> = 0.52, p = 0.046), whereas for octopamine (OA) (r<sub>S</sub> = 0.93, p = 2e–7) and dopamine (DA) (r<sub>S</sub> = 0.97, p = 2e–7) it is strong. These correlations differ significantly between TA and the other two amines (TA vs OA, p = 0.002; TA vs DA, p = 0.0006) but not between OA and DA (OA vs DA, p = 0.382) (Fisher's z transformation for correlation coefficients, two-tailed Student's t-test). Each measurable response to an application of TA (4 oocytes, n = 15 responses), OA (6 oocytes, n = 24 responses), or DA (5 oocytes, n = 14 responses) was treated as an independent sample.</p>", "links"=>[], "tags"=>["tyramine", "Xenopus Oocytes Suggests Functional Selectivity", "octopamine", "insect Drosophila melanogaster", "oa", "receptor type"], "article_id"=>1220994, "categories"=>["Biological Sciences"], "users"=>["Sami H. Jezzini", "Dalynés Reyes-Colón", "María A. Sosa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111314.g004", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tyramine_TA_selectively_evokes_an_intracellular_process_that_limits_the_response_amplitude_/1220994", "title"=>"Tyramine (TA) selectively evokes an intracellular process that limits the response amplitude.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-28 19:05:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1768354"], "description"=>"<p>I<sub>Cl-T</sub> is an endogenous calcium-dependent transient chloride current coupled to extra-celluar calcium influx. It is thought to arise from a single type of channel <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0111314#pone.0111314-Kuruma1\" target=\"_blank\">[53]</a>. At a high concentration tyramine (TA) reversibly increases I<sub>Cl-T</sub> and octopamine (OA) reversibly decreases it. (<b>A</b>) The voltage command protocol used to measure I<sub>Cl-T</sub> is shown with an example current. The first step to +40 mV from the holding potential of −20 mV evokes no I<sub>Cl-T</sub> and provides the baseline. The hyperpolarizing step to −140 mV induces calcium influx that causes I<sub>Cl-T</sub> to appear during the second step to +40 mV <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0111314#pone.0111314-Kuruma1\" target=\"_blank\">[53]</a>. The amplitude of I<sub>Cl-T</sub> was measured as the difference between the first step and the peak of the transient current evoked by the second. (<b>B</b>) Measurements of I<sub>Cl-T</sub> were taken every minute during the I<sub>D</sub> evoked by long applications of 1 mM TA and 1 mM OA. The vertical lines are the currents evoked by the voltage command pulse used to measure I<sub>Cl-T</sub> (as shown in A). Their true amplitude was clipped from the image during figure preparation. Below the trace individual I<sub>Cl-T</sub> transients are shown. Δ I<sub>Cl-T</sub> is the difference in amplitude of these transients measured at different time points. The amplitude of I<sub>Cl-T</sub> increases during continuous TA application and decreases during continuous OA application. There was a 38 minute washout period between the TA and OA applications. (<b>C</b>) All measurements of I<sub>Cl-T</sub> taken over the entire duration of the experiment shown in B. (<b>D</b>) Data from 4 different oocytes showing Δ I<sub>Cl-T</sub> at the 3 and 8 minute post-transmitter application time points. Data from oocyte #1 are shown in B and C. The 8 minute time point was not taken for the OA response of oocytes #3 (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0111314#pone.0111314.s002\" target=\"_blank\">Fig. S2</a>) and #4.</p>", "links"=>[], "tags"=>["tyramine", "Xenopus Oocytes Suggests Functional Selectivity", "octopamine", "insect Drosophila melanogaster", "oa", "receptor type"], "article_id"=>1221007, "categories"=>["Biological Sciences"], "users"=>["Sami H. Jezzini", "Dalynés Reyes-Colón", "María A. Sosa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111314.g006", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differential_modulation_of_a_transient_chloride_current_by_tyramine_TA_and_octopamine_OA_/1221007", "title"=>"Differential modulation of a transient chloride current by tyramine (TA) and octopamine (OA).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-28 19:05:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1768320"], "description"=>"<p>(<b>A</b>) Representative responses to concentration series in three different oocytes injected with OA/TA<sub>Mac</sub> using a 30 second perfusion-switch. Oocytes were voltage clamped at −60 mV. Octopamine (OA) and dopamine (DA) consistently evoked currents that increased in amplitude up to the maximum concentration. In contrast, currents evoked by tyramine (TA) increased in amplitude up to around 10 µM. TA-evoked responses also exhibited a more complex waveform at high-concentration. In some oocytes TA evoked oscillations that became more pronounced with increasing concentration. (<b>B</b>) The salient features of the high-concentration TA-evoked response are labeled. These include the abrupt appearance of a plateau during agonist application (black bar) followed by a second rise occurring during washout. In some oocytes oscillations appeared during recovery that were never seen with octopamine or dopamine. (<b>C</b>) The mean amplitudes of normalized currents (I/I<sub>max</sub>) recorded as in A are plotted against the concentration of agonist in µM. For TA, values measured and normalized at both the peak (black) and plateau (grey) are shown. Approximate EC<sub>50</sub> values estimated from the plot are TA (EC<sub>50</sub>≈0.2 µM), OA (EC<sub>50</sub>≈21 µM), and DA (EC<sub>50</sub>≈63 µM). Error bars represent standard deviation of the normalized values and are shown in one direction for TA for clarity. Oocytes were injected with OA/TA<sub>Mac</sub> receptor cRNA only (TA n = 4 oocytes; OA n = 6 oocytes; DA n = 5 oocytes).</p>", "links"=>[], "tags"=>["tyramine", "Xenopus Oocytes Suggests Functional Selectivity", "octopamine", "insect Drosophila melanogaster", "oa", "receptor type"], "article_id"=>1220985, "categories"=>["Biological Sciences"], "users"=>["Sami H. Jezzini", "Dalynés Reyes-Colón", "María A. Sosa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111314.g003", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_dose_dependence_of_transmitter_evoked_direct_current_I_D_in_oocytes_expressing_the_OA_TA_Mac_GPCR_/1220985", "title"=>"The dose dependence of transmitter evoked direct-current (I<sub>D</sub>) in oocytes expressing the OA/TA<sub>Mac</sub> GPCR.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-28 19:05:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1768380", "https://ndownloader.figshare.com/files/1768381", "https://ndownloader.figshare.com/files/1768382", "https://ndownloader.figshare.com/files/1768383", "https://ndownloader.figshare.com/files/1768384", "https://ndownloader.figshare.com/files/1768385", "https://ndownloader.figshare.com/files/1768387", "https://ndownloader.figshare.com/files/1768388", "https://ndownloader.figshare.com/files/1768389"], "description"=>"<div><p>Here we report the characterization of an octopamine/tyramine (OA/TA or TyrR1) receptor (OA/TA<sub>Mac</sub>) cloned from the freshwater prawn, <i>Macrobrachium rosenbergii</i>, an animal used in the study of agonistic social behavior. The invertebrate OA/TA receptors are seven trans-membrane domain G-protein coupled receptors that are related to vertebrate adrenergic receptors. Behavioral studies in arthropods indicate that octopaminergic signaling systems modulate fight or flight behaviors with octopamine and/or tyramine functioning in a similar way to the adrenalins in vertebrate systems. Despite the importance of octopamine signaling in behavioral studies of decapod crustaceans there are no functional data available for any of their octopamine or tyramine receptors. We expressed OA/TA<sub>Mac</sub> in <i>Xenopus</i> oocytes where agonist-evoked trans-membrane currents were used as readouts of receptor activity. The currents were most effectively evoked by tyramine but were also evoked by octopamine and dopamine. They were effectively blocked by yohimbine. The electrophysiological approach we used enabled the continuous observation of complex dynamics over time. Using voltage steps, we were able to simultaneously resolve two types of endogenous currents that are affected over different time scales. At higher concentrations we observe that octopamine and tyramine can produce different and opposing effects on both of these currents, presumably through the activity of the single expressed receptor type. The pharmacological profile and apparent functional-selectivity are consistent with properties first observed in the OA/TA receptor from the insect <i>Drosophila melanogaster</i>. As the first functional data reported for any crustacean OA/TA receptor, these results suggest that functional-selectivity between tyramine and octopamine is a feature of this receptor type that may be conserved among arthropods.</p></div>", "links"=>[], "tags"=>["tyramine", "Xenopus Oocytes Suggests Functional Selectivity", "octopamine", "insect Drosophila melanogaster", "oa", "receptor type"], "article_id"=>1221015, "categories"=>["Biological Sciences"], "users"=>["Sami H. Jezzini", "Dalynés Reyes-Colón", "María A. Sosa"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0111314.s001", "https://dx.doi.org/10.1371/journal.pone.0111314.s002", "https://dx.doi.org/10.1371/journal.pone.0111314.s003", "https://dx.doi.org/10.1371/journal.pone.0111314.s004", "https://dx.doi.org/10.1371/journal.pone.0111314.s005", "https://dx.doi.org/10.1371/journal.pone.0111314.s006", "https://dx.doi.org/10.1371/journal.pone.0111314.s007", "https://dx.doi.org/10.1371/journal.pone.0111314.s008", "https://dx.doi.org/10.1371/journal.pone.0111314.s009"], "stats"=>{"downloads"=>6, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Characterization_of_a_Prawn_OA_TA_Receptor_in_Xenopus_Oocytes_Suggests_Functional_Selectivity_between_Octopamine_and_Tyramine/1221015", "title"=>"Characterization of a Prawn OA/TA Receptor in <i>Xenopus</i> Oocytes Suggests Functional Selectivity between Octopamine and Tyramine", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-10-28 19:05:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1768310"], "description"=>"<p>The response is complex because the relative amplitudes change with concentration and apparent equilibrium is not reached for all concentrations. (<b>A and B</b>) Representative responses to prolonged applications at lower (10 µM) and higher (100 µM) concentrations. (<b>A</b>) TA evokes the greatest amplitude response at 10 µM. The responses never reach equilibrium. Instead, they begin to decline prior to the removal of agonist (end of black bar). (<b>B</b>) At 100 µM the currents appear to approach a plateau. The TA response plateaus more quickly causing its amplitude to be small relative to OA or DA. Oocytes were voltage clamped at −60 mV. Each of the three transmitters were applied to the same single oocytes using focal application via a triple-barrel pipette. Oocytes were co-injected with OA/TA<sub>Mac</sub> receptor and CFTR cRNA. (Also see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0111314#pone-0111314-g006\" target=\"_blank\">Fig. 6B</a> for another example of long octopamine application).</p>", "links"=>[], "tags"=>["tyramine", "Xenopus Oocytes Suggests Functional Selectivity", "octopamine", "insect Drosophila melanogaster", "oa", "receptor type"], "article_id"=>1220984, "categories"=>["Biological Sciences"], "users"=>["Sami H. Jezzini", "Dalynés Reyes-Colón", "María A. Sosa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111314.g002", "stats"=>{"downloads"=>1, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Octopamine_OA_dopamine_DA_and_tyramine_TA_evoke_complex_currents_in_oocytes_injected_with_OA_TA_Mac_cRNA_/1220984", "title"=>"Octopamine (OA), dopamine (DA), and tyramine (TA) evoke complex currents in oocytes injected with OA/TA<sub>Mac</sub> cRNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-28 19:05:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1768338"], "description"=>"<p>(<b>A</b>) The relative amplitude of agonist evoked direct-currents (I<sub>D</sub>) within single oocytes. (+/−)-octopamine (OA), β-phenylethylamine (β-PEA), (+/−)-synephrine (SA), (−)-quinpirole (QP), and histamine (HA) were all applied at 50 µM and normalized to the amplitude of the OA-evoked current. In this experimental set the response to OA ranged from 64 nA to 150 nA with a mean of 119 nA and a standard deviation of 32 nA (n = 6). (<b>B</b>) Relative efficacy of antagonists. Antagonists were applied as a mixture with 50 µM OA. The concentration series for each antagonist was tested on a different oocyte injected with OA/TA<sub>Mac</sub> only and voltage clamped at −60 mV. Current amplitudes were normalized to the response at lowest antagonist concentration which was zero in most experiments. All antagonists were tested on 3 to 5 oocytes. Error bars in A and B represent the standard deviation of the normalized values.</p>", "links"=>[], "tags"=>["tyramine", "Xenopus Oocytes Suggests Functional Selectivity", "octopamine", "insect Drosophila melanogaster", "oa", "receptor type"], "article_id"=>1220997, "categories"=>["Biological Sciences"], "users"=>["Sami H. Jezzini", "Dalynés Reyes-Colón", "María A. Sosa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111314.g005", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_pharmacological_profile_of_OA_TA_Mac_/1220997", "title"=>"The pharmacological profile of OA/TA<sub>Mac</sub>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-28 19:05:20"}

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Relative Metric

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