Ionic Selectivity and Permeation Properties of Human PIEZO1 Channels
Publication Date
May 08, 2015
Journal
PLOS ONE
Authors
Radhakrishnan Gnanasambandam, Chilman Bae, Philip A. Gottlieb & Frederick Sachs
Volume
10
Issue
5
Pages
e0125503
DOI
https://dx.plos.org/10.1371/journal.pone.0125503
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0125503
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/25955826
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4425559
Europe PMC
http://europepmc.org/abstract/MED/25955826
Web of Science
000356768100056
Scopus
84948821212
Mendeley
http://www.mendeley.com/research/ionic-selectivity-permeation-properties-human-piezo1-channels
Events
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Mendeley | Further Information

{"title"=>"Ionic selectivity and permeation properties of human PIEZO1 channels", "type"=>"journal", "authors"=>[{"first_name"=>"Radhakrishnan", "last_name"=>"Gnanasambandam", "scopus_author_id"=>"16642904400"}, {"first_name"=>"Chilman", "last_name"=>"Bae", "scopus_author_id"=>"23495016500"}, {"first_name"=>"Philip A.", "last_name"=>"Gottlieb", "scopus_author_id"=>"7102391234"}, {"first_name"=>"Frederick", "last_name"=>"Sachs", "scopus_author_id"=>"35586122700"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84948821212", "sgr"=>"84948821212", "pui"=>"608068399", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"25955826", "doi"=>"10.1371/journal.pone.0125503"}, "id"=>"d73524a9-83a8-30b6-8c9b-eee6d3a04692", "abstract"=>"Members of the eukaryotic PIEZO family (the human orthologs are noted hPIEZO1 and hPIEZO2) form cation-selective mechanically-gated channels. We characterized the selectivity of human PIEZO1 (hPIEZO1) for alkali ions: K+, Na+, Cs+ and Li+; organic cations: TMA and TEA, and divalents: Ba2+, Ca2+, Mg2+ and Mn2+. All monovalent ions permeated the channel. At a membrane potential of -100 mV, Cs+, Na+ and K+ had chord conductances in the range of 35-55 pS with the exception of Li+, which had a significantly lower conductance of ~ 23 pS. The divalents decreased the single-channel permeability of K+, presumably because the divalents permeated slowly and occupied the open channel for a significant fraction of the time. In cell-attached mode, 90 mM extracellular divalents had a conductance for inward currents carried by the divalents of: 25 pS for Ba2+ and 15 pS for Ca2+ at -80 mV and 10 pS for Mg2+ at -50 mV. The organic cations, TMA and TEA, permeated slowly and attenuated K+ currents much like the divalents. As expected, the channel K+ conductance increased with K+ concentration saturating at ~ 45 pS and the KD of K+ for the channel was 32 mM. Pure divalent ion currents were of lower amplitude than those with alkali ions and the channel opening rate was lower in the presence of divalents than in the presence of monovalents. Exposing cells to the actin disrupting reagent cytochalasin D increased the frequency of openings in cell-attached patches probably by reducing mechanoprotection.", "link"=>"http://www.mendeley.com/research/ionic-selectivity-permeation-properties-human-piezo1-channels", "reader_count"=>30, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>5, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>1, "Student > Master"=>2, "Student > Bachelor"=>1, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>5, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>1, "Student > Master"=>2, "Student > Bachelor"=>1, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Materials Science"=>1, "Agricultural and Biological Sciences"=>11, "Medicine and Dentistry"=>4, "Neuroscience"=>5, "Physics and Astronomy"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Neuroscience"=>{"Neuroscience"=>5}, "Chemistry"=>{"Chemistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>11}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>2}}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/4332043"], "description"=>"<p>(A) Permeability ratios were determined by using the Goldman-Hodgkin-Katz (GHK) equation for monovalent cations. I/V relationships were obtained from outside-out patches with Cs<sup><b>+</b></sup>, Na<sup><b>+</b></sup> or Li<sup><b>+</b></sup> on the cytoplasmic side and K<sup><b>+</b></sup> on the extracellular side. The reversal potentials were compensated <i>a posteriori</i> for the liquid junction potentials resulting from assymetric ion composition across the outside-out patch. The monovalent pipette solutions did not contain Ca<sup><b>2+</b></sup> or Mg<sup><b>2+</b></sup> ions. (B) Conductance as a function of K<sup><b>+</b></sup> ion concentration ([K<sup><b>+</b></sup>]) in cell-attached patches (n = 3 patches for each concentration). The pipette solutions did not contain Ca<sup><b>2+</b></sup> or Mg<sup><b>2+</b></sup>. The comparison across concentrations was performed for a fixed driving force of 40 mV. The conductance versus [K<sup><b>+</b></sup>] data were curve-fitted using the Michealis-Menten equation: . The junction potentials were ignored because they were within 0–2 mV. Single channel traces corresponding to 10 mM, 30 mM, 100 mM and 300 mM are shown in the inset.</p>", "links"=>[], "tags"=>["90 mM extracellular divalents", "hPIEZO", "reagent cytochalasin D", "conductance", "Human PIEZO 1 Channels Members", "pS", "TMA", "Pure divalent ion currents", "mV", "alkali ions", "KD", "eukaryotic PIEZO family", "channel opening rate"], "article_id"=>2669281, "categories"=>["Biophysics", "Biochemistry", "Microbiology", "Cell Biology", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Chemical Sciences not elsewhere classified", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Infectious Diseases"], "users"=>["Radhakrishnan Gnanasambandam", "Chilman Bae", "Philip A. Gottlieb", "Frederick Sachs"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0125503.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Permeability_ratio_of_monovalent_ions_and_the_relationship_between_K_sup_sup_and_conductance_/2669281", "title"=>"Permeability ratio of monovalent ions and the relationship between [K<sup>+</sup>] and conductance.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-08 13:55:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/4332049"], "description"=>"<p>(A) Currents from channels activated in response to suction in a cell-attached patch with 90 mM extracellular Ba<sup><b>2+</b></sup> held at -80 mV (n = 10). (B) Current from a cell (pre-exposed to cytochalasin D) showing multiple channels activated by suction with 90 mM extracellular (in the pipette) Ca<sup><b>2+</b></sup> (n = 10). The inset shows a single opening from which the calculated conductance was ~15 pS at -80 mV. (B) The conductance of the channel using 90 mM extracellular Mg<sup><b>2+</b></sup> was ~10 pS at -50 mV (n = 4). Correcting for the junction potentials (-7.8 mV, -8.3 mV and -9.1 mV for 90 mM Ba<sup><b>2+</b></sup>, Ca<sup><b>2+</b></sup> and Mg<sup><b>2+</b></sup>, respectively) would cause a minor increase in the chord conductance.</p>", "links"=>[], "tags"=>["90 mM extracellular divalents", "hPIEZO", "reagent cytochalasin D", "conductance", "Human PIEZO 1 Channels Members", "pS", "TMA", "Pure divalent ion currents", "mV", "alkali ions", "KD", "eukaryotic PIEZO family", "channel opening rate"], "article_id"=>2669287, "categories"=>["Biophysics", "Biochemistry", "Microbiology", "Cell Biology", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Chemical Sciences not elsewhere classified", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Infectious Diseases"], "users"=>["Radhakrishnan Gnanasambandam", "Chilman Bae", "Philip A. Gottlieb", "Frederick Sachs"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0125503.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Divalent_ions_traverse_hPIEZO1_channels_/2669287", "title"=>"Divalent ions traverse hPIEZO1 channels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-08 13:55:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/4332055"], "description"=>"<p>(A) Unitary currents in the presence of 1 mM Ba<sup><b>2+</b></sup> in the pipette with K<sup><b>+</b></sup> saline (right). There is a leftward shift in the mean current amplitude when the concentration of Ba<sup><b>2+</b></sup> is increased from 100 μM to 1 mM as shown by the amplitude histogram (at -80 mV). A similar shift in unitary current is observed with an increase in Ca<sup><b>2+</b></sup> (B) and with an increase in Mg<sup><b>2+</b></sup> (C). Three patches with multiple openings were analyzed for each concentration.</p>", "links"=>[], "tags"=>["90 mM extracellular divalents", "hPIEZO", "reagent cytochalasin D", "conductance", "Human PIEZO 1 Channels Members", "pS", "TMA", "Pure divalent ion currents", "mV", "alkali ions", "KD", "eukaryotic PIEZO family", "channel opening rate"], "article_id"=>2669293, "categories"=>["Biophysics", "Biochemistry", "Microbiology", "Cell Biology", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Chemical Sciences not elsewhere classified", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Infectious Diseases"], "users"=>["Radhakrishnan Gnanasambandam", "Chilman Bae", "Philip A. Gottlieb", "Frederick Sachs"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0125503.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/K_sup_sup_unitary_current_amplitude_is_reduced_by_1_mM_divalent_ions_/2669293", "title"=>"K<sup>+</sup> unitary current amplitude is reduced by 1 mM divalent ions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-08 13:55:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/4332061"], "description"=>"<p>I/V plots for mixtures of K<sup>+</sup> with Ba<sup>2+</sup> (A), Ca<sup>2+</sup> (B) or Mg<sup>2+</sup> (C) in the pipette saline of cell-attached patches. Three concentrations (squares: 10 μM, circles: 100 μM and triangles: 1 mM) were used for each divalent ion used in the mixture (D) Unitary amplitude in the presence of each divalent (i<sub>dival</sub>) has been normalized to that of pure K<sup><b>+</b></sup> current in divalent-free pipette solution (i<sub>dival-free</sub>) at -80 mV. Student’s t-tests were performed to examine if reductions in current amplitudes were statistically significant (*: P < 0.01; n.s.: not significant). The reduction of unitary K<sup><b>+</b></sup> current is greatest with Ca<sup><b>2+</b></sup>. The junction potentials were in the range of 0.3–0.5 mV for 1 mM Ba<sup><b>2+</b></sup>, Ca<sup><b>2+</b></sup> or Mg<sup><b>2+</b></sup> (highest concentration) included in the pipette solution.</p>", "links"=>[], "tags"=>["90 mM extracellular divalents", "hPIEZO", "reagent cytochalasin D", "conductance", "Human PIEZO 1 Channels Members", "pS", "TMA", "Pure divalent ion currents", "mV", "alkali ions", "KD", "eukaryotic PIEZO family", "channel opening rate"], "article_id"=>2669299, "categories"=>["Biophysics", "Biochemistry", "Microbiology", "Cell Biology", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Chemical Sciences not elsewhere classified", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Infectious Diseases"], "users"=>["Radhakrishnan Gnanasambandam", "Chilman Bae", "Philip A. Gottlieb", "Frederick Sachs"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0125503.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Current_Voltage_I_V_relationships_with_a_mix_of_divalents_and_K_sup_sup_ions_/2669299", "title"=>"Current-Voltage (I/V) relationships with a mix of divalents and K<sup>+</sup> ions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-08 13:55:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/4332031"], "description"=>"<div><p>Members of the eukaryotic <i>PIEZO</i> family (the human orthologs are noted <i>hPIEZO1</i> and <i>hPIEZO2</i>) form cation-selective mechanically-gated channels. We characterized the selectivity of human PIEZO1 (hPIEZO1) for alkali ions: K<sup>+</sup>, Na<sup>+</sup>, Cs<sup>+</sup> and Li<sup>+</sup>; organic cations: TMA and TEA, and divalents: Ba<sup>2+</sup>, Ca<sup>2+</sup>, Mg<sup>2+</sup> and Mn<sup>2+</sup>. All monovalent ions permeated the channel. At a membrane potential of -100 mV, Cs<sup>+</sup>, Na<sup>+</sup> and K<sup>+</sup> had chord conductances in the range of 35–55 pS with the exception of Li<sup>+</sup>, which had a significantly lower conductance of ~ 23 pS. The divalents decreased the single-channel permeability of K<sup>+</sup>, presumably because the divalents permeated slowly and occupied the open channel for a significant fraction of the time. In cell-attached mode, 90 mM extracellular divalents had a conductance for inward currents carried by the divalents of: 25 pS for Ba<sup>2+</sup> and 15 pS for Ca<sup>2+</sup> at -80 mV and 10 pS for Mg<sup>2+</sup> at -50 mV. The organic cations, TMA and TEA, permeated slowly and attenuated K<sup>+</sup> currents much like the divalents. As expected, the channel K<sup>+</sup> conductance increased with K<sup>+</sup> concentration saturating at ~ 45 pS and the K<sub>D</sub> of K<sup>+</sup> for the channel was 32 mM. Pure divalent ion currents were of lower amplitude than those with alkali ions and the channel opening rate was lower in the presence of divalents than in the presence of monovalents. Exposing cells to the actin disrupting reagent cytochalasin D increased the frequency of openings in cell-attached patches probably by reducing mechanoprotection.</p></div>", "links"=>[], "tags"=>["90 mM extracellular divalents", "hPIEZO", "reagent cytochalasin D", "conductance", "Human PIEZO 1 Channels Members", "pS", "TMA", "Pure divalent ion currents", "mV", "alkali ions", "KD", "eukaryotic PIEZO family", "channel opening rate"], "article_id"=>2669269, "categories"=>["Biophysics", "Biochemistry", "Microbiology", "Cell Biology", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Chemical Sciences not elsewhere classified", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Infectious Diseases"], "users"=>["Radhakrishnan Gnanasambandam", "Chilman Bae", "Philip A. Gottlieb", "Frederick Sachs"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0125503", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Ionic_Selectivity_and_Permeation_Properties_of_Human_PIEZO1_Channels/2669269", "title"=>"Ionic Selectivity and Permeation Properties of Human PIEZO1 Channels", "pos_in_sequence"=>0, "defined_type"=>6, "published_date"=>"2015-05-08 13:55:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/4332064"], "description"=>"<p>Current elicited from outside-out patches in response to 500 ms <i>positive</i> pressure pulses. Pipette solutions contained either 150 mM TMA or 150 mM TEA, 10 HEPES at pH 7.4. Divalent ions were not included in the pipette solution. For 150 mM TMA, the current would reverse near +45 mV, whereas with 150 mM TEA, the reversal potential would be near +8 mV (n = 3 patches) after compensating for the junction potential. The calculated junction potential was -5.0 mV for the 150 mM TMA containing pipette solution and -7.7 mV for the 150 mM TEA containing pipette solution.</p>", "links"=>[], "tags"=>["90 mM extracellular divalents", "hPIEZO", "reagent cytochalasin D", "conductance", "Human PIEZO 1 Channels Members", "pS", "TMA", "Pure divalent ion currents", "mV", "alkali ions", "KD", "eukaryotic PIEZO family", "channel opening rate"], "article_id"=>2669302, "categories"=>["Biophysics", "Biochemistry", "Microbiology", "Cell Biology", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Chemical Sciences not elsewhere classified", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Infectious Diseases"], "users"=>["Radhakrishnan Gnanasambandam", "Chilman Bae", "Philip A. Gottlieb", "Frederick Sachs"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0125503.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Permeation_of_TMA_and_TEA_in_outside_out_patches_/2669302", "title"=>"Permeation of TMA and TEA in outside-out patches.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-08 13:55:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/4332037"], "description"=>"<p>(A) Unitary currents from <i>hPIEZO1</i> cDNA transfected cells in response to pressure steps (pipette suction) applied via a cell-attached pipette containing K<sup><b>+</b></sup>. A linear fit of the I/V relationship yielded a slope conductance of 47 pS (n = 6). (B) Amplitude histograms of the unitary open channel current for the indicated voltages (n = 6). The calculated chord conductance was 47 pS at -80 mV and 53 pS at -100 mV. (C) I/V relationships for monovalent ions Cs<sup><b>+</b></sup> (n = 3), Na<sup><b>+</b></sup> (n = 6) and Li<sup><b>+</b></sup> (n = 5); the linear fits were extrapolated to intersect the abscissa. K<sup><b>+</b></sup> is our standard for comparison. The unitary current with Cs<sup><b>+</b></sup> and Na<sup><b>+</b></sup> were lower than that with K<sup><b>+</b></sup>. With Li<sup><b>+</b></sup> as the current carrying ion the unitary current was approximately halved.</p>", "links"=>[], "tags"=>["90 mM extracellular divalents", "hPIEZO", "reagent cytochalasin D", "conductance", "Human PIEZO 1 Channels Members", "pS", "TMA", "Pure divalent ion currents", "mV", "alkali ions", "KD", "eukaryotic PIEZO family", "channel opening rate"], "article_id"=>2669275, "categories"=>["Biophysics", "Biochemistry", "Microbiology", "Cell Biology", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Chemical Sciences not elsewhere classified", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Infectious Diseases"], "users"=>["Radhakrishnan Gnanasambandam", "Chilman Bae", "Philip A. Gottlieb", "Frederick Sachs"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0125503.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Extracellular_K_sup_sup_currents_through_hPIEZO1_channels_/2669275", "title"=>"Extracellular K<sup>+</sup> currents through hPIEZO1 channels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-08 13:55:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/4332070"], "description"=>"<p>(A) Bar graph summarizing the effect of increasing concentrations of TMA or TEA (20 mM to 150 mM) on the unitary conductance when the main permeant ion was K<sup><b>+</b></sup> in cell-attached patches. Student’s t-tests were performed to examine if reductions in current amplitudes (mean ± s.e.m) were statistically significant (*: P < 0.01; n.s.: not significant). As <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0125503#pone.0125503.g005\" target=\"_blank\">Fig 5</a> shows, both TMA and TEA can traverse the channel. The current traces shown below the bar graph (left: TMA, right: TEA) highlight the decrease in unitary current with TEA compared to TMA, suggesting TEA is the better blocker (n = 3 patches for each organic ion concentration). The junction potentials were ignored (for mixed solutions of TMA and TEA) because they were between -0.5mV and -3.7 mV for 20–150 mM TMA; for 20–150 mM TEA they were between -0.7 mV and -5.3 mV. (B) Current from outside-out patches with mixed solutions of K<sup><b>+</b></sup> with either TMA or TEA (n = 3). The current is due to the permeation of both organic cations and K<sup><b>+</b></sup>. As expected, the amplitude of current produced with mixed solutions is lower compared to that with pure K<sup><b>+</b></sup>.</p>", "links"=>[], "tags"=>["90 mM extracellular divalents", "hPIEZO", "reagent cytochalasin D", "conductance", "Human PIEZO 1 Channels Members", "pS", "TMA", "Pure divalent ion currents", "mV", "alkali ions", "KD", "eukaryotic PIEZO family", "channel opening rate"], "article_id"=>2669308, "categories"=>["Biophysics", "Biochemistry", "Microbiology", "Cell Biology", "Molecular Biology", "Environmental Sciences not elsewhere classified", "Chemical Sciences not elsewhere classified", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Infectious Diseases"], "users"=>["Radhakrishnan Gnanasambandam", "Chilman Bae", "Philip A. Gottlieb", "Frederick Sachs"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0125503.g007", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Titration_of_K_sup_sup_currents_by_TMA_and_TEA_/2669308", "title"=>"Titration of K<sup>+</sup> currents by TMA and TEA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-08 13:55:59"}

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  • {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"9", "full-text"=>"8", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"17", "full-text"=>"22", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"5", "full-text"=>"3", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"18", "full-text"=>"18", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"14", "full-text"=>"15", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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