Mechanism of Neuronal versus Endothelial Cell Uptake of Alzheimer's Disease Amyloid β Protein
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{"title"=>"Mechanism of Neuronal versus endothelial cell uptake of Alzheimer's disease amyloid β protein", "type"=>"journal", "authors"=>[{"first_name"=>"Karunya K.", "last_name"=>"Kandimalla", "scopus_author_id"=>"6506468634"}, {"first_name"=>"Olenych G.", "last_name"=>"Scott", "scopus_author_id"=>"57196097178"}, {"first_name"=>"Smita", "last_name"=>"Fulzele", "scopus_author_id"=>"57196093938"}, {"first_name"=>"Michael W.", "last_name"=>"Davidson", "scopus_author_id"=>"7401858367"}, {"first_name"=>"Joseph F.", "last_name"=>"Poduslo", "scopus_author_id"=>"7006286404"}], "year"=>2009, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"19247480", "doi"=>"10.1371/journal.pone.0004627", "sgr"=>"84935851672", "scopus"=>"2-s2.0-84935851672", "issn"=>"19326203", "pui"=>"618784021"}, "id"=>"6be63759-bcf2-3c4e-aa9c-69cc54173e29", "abstract"=>"Alzheimer's disease (AD) is characterized by significant neurodegeneration in the cortex and hippocampus; intraneuronal tangles of hyperphosphorylated tau protein; and accumulation of β-amyloid (Aβ) proteins 40 and 42 in the brain parenchyma as well as in the cerebral vasculature. The current understanding that AD is initiated by the neuronal accumulation of Aβ proteins due to their inefficient clearance at the blood-brain-barrier (BBB), places the neurovascular unit at the epicenter of AD pathophysiology. The objective of this study is to investigate cellular mechanisms mediating the internalization of Aβ proteins in the principle constituents of the neurovascular unit, neurons and BBB endothelial cells. Laser confocal micrographs of wild type (WT) mouse brain slices treated with fluorescein labeled Aβ40 (F-Aβ40) demonstrated selective accumulation of the protein in a subpopulation of cortical and hippocampal neurons via nonsaturable, energy independent, and nonendocytotic pathways. This groundbreaking finding, which challenges the conventional belief that Aβ proteins are internalized by neurons via receptor mediated endocytosis, was verified in differentiated PC12 cells and rat primary hippocampal (RPH) neurons through laser confocal microscopy and flow cytometry studies. Microscopy studies have demonstrated that a significant proportion of F-Aβ40 or F-Aβ42 internalized by differentiated PC12 cells or RPH neurons is located outside of the endosomal or lysosomal compartments, which may accumulate without degradation. In contrast, BBME cells exhibit energy dependent uptake of F-Aβ40, and accumulate the protein in acidic cell organelle, indicative of endocytotic uptake. Such a phenomenal difference in the internalization of Aβ40 between neurons and BBB endothelial cells may provide essential clues to understanding how various cells can differentially regulate Aβ proteins and help explain the vulnerability of cortical and hippocampal neurons to Aβ toxicity.", "link"=>"http://www.mendeley.com/research/mechanism-neuronal-versus-endothelial-cell-uptake-alzheimers-disease-amyloid-%CE%B2-protein-1", "reader_count"=>8, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>4, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>4, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Unspecified"=>1, "Agricultural and Biological Sciences"=>2, "Neuroscience"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Neuroscience"=>{"Neuroscience"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>0}

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  • {"files"=>["https://ndownloader.figshare.com/files/908111"], "description"=>"<p>A–D: Uptake of fluorescein labeled Aβ40 (F-Aβ40) and Alexa Fluor® 633 labeled transferrin (AF633-Trf), clathrin-mediated endocytosis marker, in rat primary hippocampal (RPH) neurons following 30 min incubation at 37°C. (A) F-Aβ40 uptake; (B) Uptake of AF633-Trf; (C) Superimposition of images A and B; (D) Overlay of fluorescence images on the DIC image of RPH neurons. E–G: Uptake of F-Aβ40 and AF633-Trf in RPH neurons at 4°C. (E) Uptake of F-Aβ40; (F) No significant neuronal uptake of AF633-Trf at 4°C; (G) Superimposition of images D and E on the DIC image of RPH neurons; H–J: Uptake of F-Aβ40 and AF633-Trf in RPH neurons treated with 10 mM Sodium Azide and 50 mM 2-deoxy glucose, agents that are known to deplete cellular ATP. (H) Uptake of F-Aβ40; (I) No significant cellular uptake of AF633-Trf was observed; (J) Superimposition of images H and I on the DIC image of neurons.</p>", "links"=>[], "tags"=>["biochemistry/cell signaling and trafficking structures", "biophysics/cell signaling and trafficking structures", "cell biology/neuronal and glial cell biology", "neuroscience/cognitive neuroscience", "neuroscience/neurobiology of disease and regeneration", "mental health/alzheimer disease", "mental health/dementia", "neurological disorders/alzheimer disease"], "article_id"=>578562, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g010", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_10_/578562", "title"=>"Figure 10", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:51:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/906838"], "description"=>"<p>A–D: Uptake of fluorescein labeled Aβ40 (F-Aβ40) and Alexa Fluor® 633 labeled transferrin (AF633-Trf), clathrin-mediated endocytosis marker, by differentiated PC12 cells following 30 min incubation. (A) F-Aβ40 uptake; (B) Uptake of AF633-Trf; (C) Superimposition of images A and B; (D) Sparse co-localization of F-Aβ40 and AF633-Trf as indicated by the white masked areas. E–G: Uptake of F-Aβ40 and AF633-Trf in differentiated PC12 cells subjected conditions that inhibit clathrin mediated endocytosis (hypotonic shock for 5 min followed by incubation with potassium free salt solution for 30 min). (E) Uptake of F-Aβ40; (F) Substantial reduction in AF633-Trf; (G). Superimposition of images E and F on the differential interference contrast (DIC) image to show the condition of the cells.</p>", "links"=>[], "tags"=>["biochemistry/cell signaling and trafficking structures", "biophysics/cell signaling and trafficking structures", "cell biology/neuronal and glial cell biology", "neuroscience/cognitive neuroscience", "neuroscience/neurobiology of disease and regeneration", "mental health/alzheimer disease", "mental health/dementia", "neurological disorders/alzheimer disease"], "article_id"=>577283, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_4_/577283", "title"=>"Figure 4", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:43:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/908284"], "description"=>"<p>A–D: F-Aβ40 uptake into the acidic compartments of bovine brain microvascular endothelial (BBME) cells labeled by Lysotracker Red® (60×). (A) Uptake of F-Aβ40 (B) Uptake of Lysotracker Red®; (C) Superimposition of images A and B; (D) A magnified portion of image C (enclosed in the white rectangle) to show co-localization of both fluorophores. I–II: Histograms of fluorescence intensity in BBME cells treated with (I) F-Aβ40: (A) Untreated control, (B) at 4°C, (C) at 37°C; and (II) AF633-Trf: (A) Untreated control, (B) at 4°C, (C) at 37°C.</p>", "links"=>[], "tags"=>["biochemistry/cell signaling and trafficking structures", "biophysics/cell signaling and trafficking structures", "cell biology/neuronal and glial cell biology", "neuroscience/cognitive neuroscience", "neuroscience/neurobiology of disease and regeneration", "mental health/alzheimer disease", "mental health/dementia", "neurological disorders/alzheimer disease"], "article_id"=>578729, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g011", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_11_/578729", "title"=>"Figure 11", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:52:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/907327"], "description"=>"<p>A–C: Accumulation of fluorescein labeled Aβ40 (F-Aβ40) and Dil labeled low density lipoprotein (Dil-LDL) in the late endosomes of differentiated PC12 cells following a 15 min treatment. (A) F-Aβ40 uptake; (B) Uptake of Dil-LDL; (C) Superimposition of images A and B indicate only a partial co-localization, shown by the white masked areas. D: Co-localization of F-Aβ40 and Dil-LDL in differentiated PC12 cells following a 30 min treatment.</p>", "links"=>[], "tags"=>["biochemistry/cell signaling and trafficking structures", "biophysics/cell signaling and trafficking structures", "cell biology/neuronal and glial cell biology", "neuroscience/cognitive neuroscience", "neuroscience/neurobiology of disease and regeneration", "mental health/alzheimer disease", "mental health/dementia", "neurological disorders/alzheimer disease"], "article_id"=>577775, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g006", "stats"=>{"downloads"=>3, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_6_/577775", "title"=>"Figure 6", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:46:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/907783"], "description"=>"<p>I–IV: Uptake of fluorescein labeled Aβ40 (F-Aβ40) and Alexa Fluor® 633 labeled transferrin (AF633-Trf) in differentiated PC12 cells at 4°C. (I) Uptake of F-Aβ40 (20×); (II) Uptake of AF633-Trf (20×). III–IV: Histograms of fluorescence intensity in differentiated PC12 cells treated with: (III) F-Aβ40: (A) Untreated control, (B) At 4°C, (C) At 37°C; and (IV) AF633-Trf: (A) Untreated control, (B) At 4°C, (C) At 37°C. V–VIII: Uptake of F-Aβ40 and AF633-Trf in differentiated PC12 cells treated with 10 mM Sodium Azide and 50 mM 2-deoxy glucose, agents that are known to deplete cellular ATP. (V) Uptake of F-Aβ40 (40×); (VI) Uptake of AF633-Trf (40×). VII–VIII: Histograms of F-Aβ40 fluorescence intensity in differentiated PC12 cells (VII) F-Aβ40: (A) Untreated control, (B) ATP depleted cells, (C) Normal cells; and (VIII) AF633-Trf: (A) Untreated control; (B) ATP depleted cells; (C) Normal cells.</p>", "links"=>[], "tags"=>["biochemistry/cell signaling and trafficking structures", "biophysics/cell signaling and trafficking structures", "cell biology/neuronal and glial cell biology", "neuroscience/cognitive neuroscience", "neuroscience/neurobiology of disease and regeneration", "mental health/alzheimer disease", "mental health/dementia", "neurological disorders/alzheimer disease"], "article_id"=>578226, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g008", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_8_/578226", "title"=>"Figure 8", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:49:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/906597"], "description"=>"<p>A–D: Extent of fluorescein labeled Aβ40 (F-Aβ40) uptake in the acidic compartments of differentiated PC12 cells labeled by Lysotracker Red® (40×); (A) F-Aβ40 uptake (B) Uptake of Lysotracker Red®; (C) Superimposition of images A and B; (D) Partial co-localization of Lysotracker Red® and F-Aβ40 indicated by white masked areas. E–G: Extent of F-Aβ40 uptake in the acidic compartments of rat primary hippocampal (RPH) neurons labeled by Lysotracker Red® (40×); (E) F-Aβ40 uptake (F) Uptake of Lysotracker Red® Red; (G) Superimposition of images E and F.</p>", "links"=>[], "tags"=>["biochemistry/cell signaling and trafficking structures", "biophysics/cell signaling and trafficking structures", "cell biology/neuronal and glial cell biology", "neuroscience/cognitive neuroscience", "neuroscience/neurobiology of disease and regeneration", "mental health/alzheimer disease", "mental health/dementia", "neurological disorders/alzheimer disease"], "article_id"=>577045, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g003", "stats"=>{"downloads"=>1, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_3_/577045", "title"=>"Figure 3", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:42:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/907944"], "description"=>"<p>A–D: Uptake of fluorescein labeled Aβ42 (F-Aβ42) and Alexa Fluor® 633 labeled transferrin (AF633-Trf), clathrin-mediated endocytosis marker, by differentiated PC12 cells following 30 min incubation. (A) F-Aβ42 uptake; (B) Uptake of AF633-Trf; (C) Superimposition of images A and B show limited co-localization of F-Aβ42 and AF633-Trf. (D) A magnified portion of image C (enclosed in the white rectangle) to indicate the lack of co-localization of both fluorophores. I–II: Histograms of fluorescence intensity in differentiated PC12 cells treated with (I) F-Aβ42; and (II) AF633-Trf, at 37°C and 4°C.</p>", "links"=>[], "tags"=>["biochemistry/cell signaling and trafficking structures", "biophysics/cell signaling and trafficking structures", "cell biology/neuronal and glial cell biology", "neuroscience/cognitive neuroscience", "neuroscience/neurobiology of disease and regeneration", "mental health/alzheimer disease", "mental health/dementia", "neurological disorders/alzheimer disease"], "article_id"=>578391, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g009", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_9_/578391", "title"=>"Figure 9", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:50:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/906285"], "description"=>"<p>A–B: Uptake of F-Aβ40 by a subpopulation of (A) cortical neurons (20×) and; (B) hippocampal neurons (20×). C–I: Effect of temperature on the uptake of F-Aβ40 and AF633-Trf by the pyramidal neurons (63× and 3× optical zoom). C–F: Uptake of F-Aβ40 and AF633-Trf at 37°C (C) F-Aβ40 uptake; (D) AF633-Trf uptake; (E) Superimposition of images C and D; (F) Limited co-localization of F-Aβ40 and AF633-Trf, indicated by white masked areas, was found only around the edges of pyramidal neurons. G–I: Uptake of F-Aβ40 and AF633-Trf at 4°C (G) F-Aβ40 uptake; (H) Inhibition of AF633-Trf internalization; (I) Superimposition of images G and H.</p>", "links"=>[], "tags"=>["uptake", "fluorescein", "labeled", "alexa", "633", "transferrin", "slices", "30", "min"], "article_id"=>576719, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g001", "stats"=>{"downloads"=>2, "page_views"=>31, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cellular_uptake_of_a_fluorescein_labeled_A_946_40_F_A_946_40_and_Alexa_Fluor_174_633_labeled_transferrin_AF633_Trf_in_wild_type_mouse_brain_slices_after_30_min_incubation_/576719", "title"=>"Cellular uptake of a fluorescein labeled Aβ40 (F-Aβ40) and Alexa Fluor® 633 labeled transferrin (AF633-Trf) in wild type mouse brain slices after 30 min incubation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:40:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/906483"], "description"=>"<p>(I) Effect of donor concentration and temperature on the uptake of <sup>125</sup>I-Aβ40 in wild type (WT) mouse brain slices. (II) Effect of endocytotic inhibitor dansyl cadaverine on the uptake of <sup>125</sup>I-Aβ40 (450 ng/ml) in WT mouse brain slices. (III) Histograms of fluorescence intensity in differentiated PC12 cells exposed to various concentrations of F-Aβ40. (A) Untreated cells; (B) Cells incubated with 0.65 µM F-Aβ40; (C) Cells incubated with 1.3 µM F-Aβ40; (D) Cells incubated with 3.2 µM F-Aβ40; (E) Cells incubated with 3.2 µM F-Aβ40+32 µM unlabeled Aβ40.</p>", "links"=>[], "tags"=>["biochemistry/cell signaling and trafficking structures", "biophysics/cell signaling and trafficking structures", "cell biology/neuronal and glial cell biology", "neuroscience/cognitive neuroscience", "neuroscience/neurobiology of disease and regeneration", "mental health/alzheimer disease", "mental health/dementia", "neurological disorders/alzheimer disease"], "article_id"=>576924, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_2_/576924", "title"=>"Figure 2", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:41:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/907087"], "description"=>"<p>A–C: Co-localization of fluorescein labeled Aβ40 (F-Aβ40) and Alexa Fluor® 633 labeled transferrin (AF633-Trf) in PC12 cells following: (A) 15 min; (B) 45 min; and (C) 60 min incubation. White masked areas indicate the extent of co-localization of F-Aβ40 and AF633-Trf. D: Cellular internalization of F-Aβ40 and AF633-Trf established by the XY, XZ, and YZ projections of differentiated PC12 cells treated with the fluorophores for 60 min. Optical sections (planes 1–45) were obtained from the coverslip bottom to the cell surface with a 0.6 µm Z-step interval.</p>", "links"=>[], "tags"=>["biochemistry/cell signaling and trafficking structures", "biophysics/cell signaling and trafficking structures", "cell biology/neuronal and glial cell biology", "neuroscience/cognitive neuroscience", "neuroscience/neurobiology of disease and regeneration", "mental health/alzheimer disease", "mental health/dementia", "neurological disorders/alzheimer disease"], "article_id"=>577533, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_5_/577533", "title"=>"Figure 5", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:45:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/907600"], "description"=>"<p>A–D: Uptake of fluorescein labeled Aβ40 (F-Aβ40) and Alexa Fluor® 647 labeled cholera toxin (AF647-CT), caveolae-mediated endocytosis marker, by differentiated PC12 cells following 30 min incubation. (A) F-Aβ40 uptake; (B) Uptake of AF647-CT; (C) Sparse co-localization of F-Aβ40 and AF647-CT as indicated by the white masked areas; (D) Superimposition of images A and B on the differential interference contrast (DIC) image to show the location of the fluorophores in the cells. E–G: Uptake of F-Aβ40 and AF647-CT in differentiated PC12 cells treated with filipin, which is known to inhibit caveolae mediated endocytosis. (E) Uptake of F-Aβ40; (F) Substantial reduction in AF647-CT uptake in the cells treated with filipin; (G). Superimposition of images E and F on the differential interference contrast (DIC) image to show the health of filipin treated cells.</p>", "links"=>[], "tags"=>["biochemistry/cell signaling and trafficking structures", "biophysics/cell signaling and trafficking structures", "cell biology/neuronal and glial cell biology", "neuroscience/cognitive neuroscience", "neuroscience/neurobiology of disease and regeneration", "mental health/alzheimer disease", "mental health/dementia", "neurological disorders/alzheimer disease"], "article_id"=>578047, "categories"=>["Biophysics", "Cell Biology", "Biochemistry", "Neuroscience", "Mental Health"], "users"=>["Karunya K. Kandimalla", "Olenych G. Scott", "Smita Fulzele", "Michael W. Davidson", "Joseph F. Poduslo"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0004627.g007", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Figure_7_/578047", "title"=>"Figure 7", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 06:48:03"}

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Relative Metric

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