Luteolin Inhibits Human Prostate Tumor Growth by Suppressing Vascular Endothelial Growth Factor Receptor 2-Mediated Angiogenesis
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{"title"=>"Luteolin Inhibits Human Prostate Tumor Growth by Suppressing Vascular Endothelial Growth Factor Receptor 2-Mediated Angiogenesis", "type"=>"journal", "authors"=>[{"first_name"=>"Poyil", "last_name"=>"Pratheeshkumar"}, {"first_name"=>"Young-Ok", "last_name"=>"Son"}, {"first_name"=>"Amit", "last_name"=>"Budhraja"}, {"first_name"=>"Xin", "last_name"=>"Wang"}, {"first_name"=>"Songze", "last_name"=>"Ding"}, {"first_name"=>"Lei", "last_name"=>"Wang"}, {"first_name"=>"Andrew", "last_name"=>"Hitron"}, {"first_name"=>"Jeong-Chae", "last_name"=>"Lee"}, {"first_name"=>"Donghern", "last_name"=>"Kim"}, {"first_name"=>"Sasidharan Padmaja", "last_name"=>"Divya"}, {"first_name"=>"Gang", "last_name"=>"Chen"}, {"first_name"=>"Zhuo", "last_name"=>"Zhang"}, {"first_name"=>"Jia", "last_name"=>"Luo"}, {"first_name"=>"Xianglin", "last_name"=>"Shi"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"23300633", "doi"=>"10.1371/journal.pone.0052279", "isbn"=>"1932-6203", "issn"=>"1932-6203"}, "id"=>"66067928-67b4-33d5-a4f2-e7ea488dfe01", "abstract"=>"Angiogenesis, the formation of new blood vessels from pre-existing vascular beds, is essential for tumor growth, invasion, and metastasis. Luteolin is a common dietary flavonoid found in fruits and vegetables. We studied the antiangiogenic activity of luteolin using in vitro, ex vivo, and in vivo models. In vitro studies using rat aortic ring assay showed that luteolin at non-toxic concentrations significantly inhibited microvessel sprouting and proliferation, migration, invasion and tube formation of endothelial cells, which are key events in the process of angiogenesis. Luteolin also inhibited ex vivo angiogenesis as revealed by chicken egg chorioallantoic membrane assay (CAM) and matrigel plug assay. Gelatin zymographic analysis demonstrated the inhibitory effect of luteolin on the activation of matrix metalloproteinases MMP-2 and MMP-9. Western blot analysis showed that luteolin suppressed VEGF induced phosphorylation of VEGF receptor 2 and their downstream protein kinases AKT, ERK, mTOR, P70S6K, MMP-2, and MMP-9 in HUVECs. Proinflammatory cytokines such as IL-1$β$, IL-6, IL-8, and TNF-$α$ level were significantly reduced by the treatment of luteolin in PC-3 cells. Luteolin (10 mg/kg/d) significantly reduced the volume and the weight of solid tumors in prostate xenograft mouse model, indicating that luteolin inhibited tumorigenesis by targeting angiogenesis. CD31 and CD34 immunohistochemical staining further revealed that the microvessel density could be remarkably suppressed by luteolin. Moreover, luteolin reduced cell viability and induced apoptosis in prostate cancer cells, which were correlated with the downregulation of AKT, ERK, mTOR, P70S6K, MMP-2, and MMP-9 expressions. Taken together, our findings demonstrate that luteolin inhibits human prostate tumor growth by suppressing vascular endothelial growth factor receptor 2-mediated angiogenesis.", "link"=>"http://www.mendeley.com/research/luteolin-inhibits-human-prostate-tumor-growth-suppressing-vascular-endothelial-growth-factor-recepto", "reader_count"=>22, "reader_count_by_academic_status"=>{"Researcher"=>6, "Student > Ph. D. Student"=>6, "Student > Master"=>2, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>6, "Student > Ph. D. Student"=>6, "Student > Master"=>2, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>2, "Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>11, "Medicine and Dentistry"=>4, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>11}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"India"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/514774"], "description"=>"<p>(a) Chemical structure of luteolin. (b) Effect of luteolin on HUVECs viability in culture. Cell viability was quantified by MTT assay. Values are means ± SD (mean of triplicate). *p<0.05 denotes a statistically significant difference from untreated controls. (c) Luteolin inhibits the VEGF induced proliferation of endothelial cells. HUVECs were treated with different concentrations of luteolin and VEGF for 48 h. Relative cell proliferation was determined by MTT assay. Values are means ± SD (mean of triplicate). *p<0.05 denotes a statistically significant difference from untreated controls; #p<0.05 denotes a statistically significant difference from VEGF control.</p>", "links"=>[], "tags"=>["inhibited", "vegf", "induced", "proliferation"], "article_id"=>185244, "categories"=>["Cancer", "Biotechnology", "Biochemistry", "Chemistry"], "users"=>["Poyil Pratheeshkumar", "Young-Ok Son", "Amit Budhraja", "Xin Wang", "Songze Ding", "Lei Wang", "Andrew Hitron", "Jeong-Chae Lee", "Donghern Kim", "Sasidharan Padmaja Divya", "Gang Chen", "Zhuo Zhang", "Jia Luo", "Xianglin Shi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0052279.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luteolin_inhibited_the_VEGF_induced_cell_proliferation_in_HUVECs_/185244", "title"=>"Luteolin inhibited the VEGF induced cell proliferation in HUVECs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 17:43:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/514925"], "description"=>"<p>(a) Luteolin inhibited HUVECs migration. Cells were starved to inactivate cell proliferation and then wounded by pipette tips. EGM-2 with or without 10 ng/mL VEGF and different dilutions of luteolin were added. Migrated cells were quantified by manual counting. (b) Luteolin inhibited HUVECs invasion. HUVECs with the indicated concentrations of luteolin were seeded into the upper compartment of invasion chambers. The bottom chambers were filled with EGM-2 supplemented with VEGF. After 24 h incubation, migrated cells were fixed, stained and quantified. (c) Luteolin inhibited the tube formation of HUVECs. HUVECs were treated with various dilutions of luteolin with VEGF for 24 h, cells were fixed, and tubular structures were photographed. Values are means ± SD (mean of triplicate). *p<0.05 denotes a statistically significant difference from untreated controls; #p<0.05 denotes a statistically significant difference from VEGF control.</p>", "links"=>[], "tags"=>["inhibited", "vegf-induced", "endothelial"], "article_id"=>185403, "categories"=>["Cancer", "Biotechnology", "Biochemistry", "Chemistry"], "users"=>["Poyil Pratheeshkumar", "Young-Ok Son", "Amit Budhraja", "Xin Wang", "Songze Ding", "Lei Wang", "Andrew Hitron", "Jeong-Chae Lee", "Donghern Kim", "Sasidharan Padmaja Divya", "Gang Chen", "Zhuo Zhang", "Jia Luo", "Xianglin Shi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0052279.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luteolin_inhibited_VEGF_induced_migration_invasion_and_tube_formation_of_endothelial_cells_/185403", "title"=>"Luteolin inhibited VEGF-induced migration, invasion, and tube formation of endothelial cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 17:44:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/515080"], "description"=>"<p>(a) Luteolin inhibits <i>ex vivo</i> angiogenesis in CAM assay. Fertile leghorn chicken eggs were candled on embryonic day 8; a small opening was made at the top of the live eggs. Luteolin for treatment was mixed with 0.5% methyl cellulose in water and gently placed on the CAM. The eggs were incubated for 48 h and photographed. Blood vessels density was quantified by Image J software and represented as a bar diagram. Values are means ± SD (mean of triplicate). *p<0.05 denotes a statistically significant difference from untreated controls; #p<0.05 denotes a statistically significant difference from 20 and 40 µmole/L luteolin. (b) Luteolin inhibits <i>ex vivo</i> angiogenesis in matrigel plug assay. Matrigel plug containg VEGF and luteolin were implanted into the CAM at day 9 of fertilized chicken eggs. After 96 h of incubation, the matrigel plugs were taken out and dispersed in PBS and incubated at 4°C overnight. Hemoglobin levels were determined using Drabkin’s reagent according to manufacturer instructions. Values are means ± SD (mean of triplicate). *p<0.05 denotes a statistically significant difference from untreated controls; #p<0.05 denotes a statistically significant difference from VEGF control. (c) Luteolin inhibits microvessel outgrowth from the rat aortic ring. Dorsal aorta from a freshly sacrificed Sprague–Dawley rat was cut into ∼1 mm long pieces using surgical blade. Each ring was placed in a collagen pre-coated 96-well plate. VEGF, with or without different dilutions of luteolin, was added to the wells. On day 6, the rings were analyzed by phase-contrast microscopy and microvessel outgrowths were quantified and photographed. Values are means ± SD (mean of triplicate). *p<0.05 denotes a statistically significant difference from untreated controls.</p>", "links"=>[], "tags"=>["inhibited", "angiogenesis", "cam", "matrigel", "plug", "assay", "aortic"], "article_id"=>185552, "categories"=>["Cancer", "Biotechnology", "Biochemistry", "Chemistry"], "users"=>["Poyil Pratheeshkumar", "Young-Ok Son", "Amit Budhraja", "Xin Wang", "Songze Ding", "Lei Wang", "Andrew Hitron", "Jeong-Chae Lee", "Donghern Kim", "Sasidharan Padmaja Divya", "Gang Chen", "Zhuo Zhang", "Jia Luo", "Xianglin Shi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0052279.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luteolin_inhibited_ex_vivo_angiogenesis_by_CAM_and_matrigel_plug_assay_and_in_vitro_angiogenesis_by_rat_aortic_ring_assay_/185552", "title"=>"Luteolin inhibited <i>ex vivo</i> angiogenesis by CAM and matrigel plug assay and <i>in vitro</i> angiogenesis by rat aortic ring assay.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 17:45:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/515203"], "description"=>"<p>(a) Luteolin suppressed the activation of VEGFR2 and their downstream signaling pathway triggered by VEGF in HUVECs. Proteins from different treatments was tested by Western blotting and probed with specific antibodies. Experiments were repeated for three times. (b) Luteolin inhibits the MMP-2 and MMP-9 production by HUVECs. 1) Condition medium from untreated HUVECs without trypsin activation. 2) Condition medium from untreated HUVECs after trypsin activation. 3) Condition medium from untreated HUVECs after trypsin activation+EDTA. 4) Condition medium from pretreated HUVECs (40 µmol/L luteolin) after trypsin activation. 5) Condition medium from pretreated HUVECs (20 µmol/L luteolin) after trypsin activation.</p>", "links"=>[], "tags"=>["inhibited", "activation", "vegfr2-mediated", "signaling"], "article_id"=>185682, "categories"=>["Cancer", "Biotechnology", "Biochemistry", "Chemistry"], "users"=>["Poyil Pratheeshkumar", "Young-Ok Son", "Amit Budhraja", "Xin Wang", "Songze Ding", "Lei Wang", "Andrew Hitron", "Jeong-Chae Lee", "Donghern Kim", "Sasidharan Padmaja Divya", "Gang Chen", "Zhuo Zhang", "Jia Luo", "Xianglin Shi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0052279.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luteolin_inhibited_the_activation_of_VEGFR2_mediated_signaling_pathways_/185682", "title"=>"Luteolin inhibited the activation of VEGFR2-mediated signaling pathways.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 17:45:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/515328"], "description"=>"<p>(a) Luteolin inhibited cell viability of PC-3 cells. Cell viability was quantified by MTT assay. Values are means ± SD (mean of triplicate). *p<0.05 denotes a statistically significant difference from untreated controls. (b) Luteolin inhibited VEGF secretion in PC-3 cells. VEGF level was estimated by ELISA method. Values are means ± SD (mean of triplicate). *p<0.05 denotes a statistically significant difference from untreated controls. (c) Luteolin inhibited PC-3 cells migration. Cells were starved to inactivate cell proliferation and then wounded by pipette tips. Various dilutions of luteolin were added into the wells and incubated for 24 h; migrated cells were quantified by manual counting. (d) Luteolin inhibited HUVECs invasion. HUVECs with the indicated concentrations of luteolin were seeded into the upper compartment of invasion chambers. The bottom chambers were filled with serum-free RPMI. After 24 h incubation, migrated cells were fixed, stained and quantified.</p>", "links"=>[], "tags"=>["inhibited", "prostate", "cancer"], "article_id"=>185811, "categories"=>["Cancer", "Biotechnology", "Biochemistry", "Chemistry"], "users"=>["Poyil Pratheeshkumar", "Young-Ok Son", "Amit Budhraja", "Xin Wang", "Songze Ding", "Lei Wang", "Andrew Hitron", "Jeong-Chae Lee", "Donghern Kim", "Sasidharan Padmaja Divya", "Gang Chen", "Zhuo Zhang", "Jia Luo", "Xianglin Shi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0052279.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luteolin_inhibited_cell_viability_migration_and_invasion_of_prostate_cancer_cells_/185811", "title"=>"Luteolin inhibited cell viability, migration, and invasion of prostate cancer cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 17:46:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/515451"], "description"=>"<p>Pro-inflammatory cytokines such as IL-1β, IL-6, IL-8, and TNF-α level were estimated by ELISA method according to the manufacturers’ recommendations. (a) IL-1β, (b) IL-6, (c) IL-8, and (c) TNF-α. Values are means ± SD (mean of triplicate). *p<0.05 denotes a statistically significant difference from untreated controls.</p>", "links"=>[], "tags"=>["inhibited", "pro-inflammatory", "cytokine", "pc-3"], "article_id"=>185936, "categories"=>["Cancer", "Biotechnology", "Biochemistry", "Chemistry"], "users"=>["Poyil Pratheeshkumar", "Young-Ok Son", "Amit Budhraja", "Xin Wang", "Songze Ding", "Lei Wang", "Andrew Hitron", "Jeong-Chae Lee", "Donghern Kim", "Sasidharan Padmaja Divya", "Gang Chen", "Zhuo Zhang", "Jia Luo", "Xianglin Shi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0052279.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luteolin_inhibited_pro_inflammatory_cytokine_production_in_PC_3_cells_/185936", "title"=>"Luteolin inhibited pro-inflammatory cytokine production in PC-3 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 17:47:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/515586"], "description"=>"<p>(a) Cells were stained with Annexin V/PI, and apoptosis was determined using flow cytometry. PC-3 cells were treated with various concentrations of luteolin for 48 h, after which apoptosis was determined by annexin V/PI staining with flow cytometry. (b) Luteolin induced PC-3 cancer cell apoptosis by the cleaved-PARP and Caspase-3 analysis. PC-3 cells were treated with luteolin for 48 h, and whole cell proteins were analysed by Western blotting with antipoly (ADP-ribose) polymerase (PARP) and anti-cleaved caspase-3.</p>", "links"=>[], "tags"=>["induced", "apoptosis", "prostate", "cancer"], "article_id"=>186065, "categories"=>["Cancer", "Biotechnology", "Biochemistry", "Chemistry"], "users"=>["Poyil Pratheeshkumar", "Young-Ok Son", "Amit Budhraja", "Xin Wang", "Songze Ding", "Lei Wang", "Andrew Hitron", "Jeong-Chae Lee", "Donghern Kim", "Sasidharan Padmaja Divya", "Gang Chen", "Zhuo Zhang", "Jia Luo", "Xianglin Shi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0052279.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luteolin_induced_apoptosis_in_prostate_cancer_cells_/186065", "title"=>"Luteolin induced apoptosis in prostate cancer cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 17:48:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/515734"], "description"=>"<p>Luteolin inhibited the activation of AKT/ERK/mTOR/p70S6K/MMP-2/MMP-9 pathway in PC-3 cells. Proteins from different treatments was tested by Western blotting and probed with specific antibodies. Experiments were repeated for three times.</p>", "links"=>[], "tags"=>["inhibited", "activation", "pathway", "prostate", "cancer"], "article_id"=>186212, "categories"=>["Cancer", "Biotechnology", "Biochemistry", "Chemistry"], "users"=>["Poyil Pratheeshkumar", "Young-Ok Son", "Amit Budhraja", "Xin Wang", "Songze Ding", "Lei Wang", "Andrew Hitron", "Jeong-Chae Lee", "Donghern Kim", "Sasidharan Padmaja Divya", "Gang Chen", "Zhuo Zhang", "Jia Luo", "Xianglin Shi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0052279.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luteolin_inhibited_the_activation_of_AKT_ERK_mTOR_p70S6K_MMP_2_MMP_9_pathway_in_prostate_cancer_cells_/186212", "title"=>"Luteolin inhibited the activation of AKT/ERK/mTOR/p70S6K/MMP-2/MMP-9 pathway in prostate cancer cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 17:48:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/515842"], "description"=>"<p>PC-3 cells were injected into 6-week old BALB/cA nude mice (5×10<sup>6</sup> cells per mouse). After tumors grew to about 100 mm<sup>3</sup>, mice were treated intraperitoneally with or without luteolin (10 mg/kg/d). (a) Solid tumors in the luteolin treated mice were significantly smaller than those in the control mice. Luteolin significantly reduced (b) tumor volume, and (c) tumor weight, (d) but had no effect on the body weight of mice. Values are means ± SD (mean of triplicate). *p<0.05 denotes a statistically significant difference from untreated controls.</p>", "links"=>[], "tags"=>["inhibited", "xenograft"], "article_id"=>186322, "categories"=>["Cancer", "Biotechnology", "Biochemistry", "Chemistry"], "users"=>["Poyil Pratheeshkumar", "Young-Ok Son", "Amit Budhraja", "Xin Wang", "Songze Ding", "Lei Wang", "Andrew Hitron", "Jeong-Chae Lee", "Donghern Kim", "Sasidharan Padmaja Divya", "Gang Chen", "Zhuo Zhang", "Jia Luo", "Xianglin Shi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0052279.g009"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luteolin_inhibited_tumor_growth_in_a_xenograft_mouse_model_/186322", "title"=>"Luteolin inhibited tumor growth in a xenograft mouse model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 17:49:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/515968"], "description"=>"<p>(a) Luteolin inhibited the activation of AKT/ERK/mTOR/p70S6K/MMP-2/MMP-9 pathway <i>in vivo</i>. Proteins from tumor tissue was tested by Western blotting and probed with specific antibodies. Experiments were repeated for three times. Luteolin inhibited tumor angiogenesis as evident from (b) CD31 and (c) CD34 immunohistochemistry. Tumor sections (5 µm) were incubated with a rabbit anti-CD31 and mouse anti-CD34 antibodies and were subsequently incubated with biotinylated anti-rabbit/anti-mouse secondary antibody, followed by staining with Vectastain ABC Kit.</p>", "links"=>[], "tags"=>["inhibited", "angiogenesis", "suppressing"], "article_id"=>186449, "categories"=>["Cancer", "Biotechnology", "Biochemistry", "Chemistry"], "users"=>["Poyil Pratheeshkumar", "Young-Ok Son", "Amit Budhraja", "Xin Wang", "Songze Ding", "Lei Wang", "Andrew Hitron", "Jeong-Chae Lee", "Donghern Kim", "Sasidharan Padmaja Divya", "Gang Chen", "Zhuo Zhang", "Jia Luo", "Xianglin Shi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0052279.g010"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Luteolin_inhibited_tumor_growth_and_tumor_angiogenesis_in_vivo_by_suppressing_AKT_ERK_mTOR_p70S6K_MMP_2_MMP_9_pathway_/186449", "title"=>"Luteolin inhibited tumor growth and tumor angiogenesis <i>in vivo</i> by suppressing AKT/ERK/mTOR/p70S6K/MMP-2/MMP-9 pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 17:50:13"}

PMC Usage Stats | Further Information

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Relative Metric

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