Curcumin Induces EGFR Degradation in Lung Adenocarcinoma and Modulates p38 Activation in Intestine: The Versatile Adjuvant for Gefitinib Therapy
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{"title"=>"Curcumin induces EGFR degradation in lung adenocarcinoma and modulates p38 activation in intestine: The versatile adjuvant for gefitinib therapy", "type"=>"journal", "authors"=>[{"first_name"=>"Jen Yi", "last_name"=>"Lee", "scopus_author_id"=>"13905988700"}, {"first_name"=>"Yee Ming", "last_name"=>"Lee", "scopus_author_id"=>"23485998100"}, {"first_name"=>"Gee Chen", "last_name"=>"Chang", "scopus_author_id"=>"7402308947"}, {"first_name"=>"Sung Liang", "last_name"=>"Yu", "scopus_author_id"=>"7405731475"}, {"first_name"=>"Wan Yu", "last_name"=>"Hsieh", "scopus_author_id"=>"36101321000"}, {"first_name"=>"Jeremy J.W.", "last_name"=>"Chen", "scopus_author_id"=>"7501892959"}, {"first_name"=>"Huei Wen", "last_name"=>"Chen", "scopus_author_id"=>"57192539512"}, {"first_name"=>"Pan Chyr", "last_name"=>"Yang", "scopus_author_id"=>"7403932080"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-80051746642", "sgr"=>"80051746642", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0023756", "pmid"=>"21858220", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "pui"=>"362361280"}, "id"=>"dae3404e-4117-3e39-a779-eccf9819a39f", "abstract"=>"BACKGROUND: Non-small cell lung cancer (NSCLC) patients with L858R or exon 19 deletion mutations in epidermal growth factor receptor (EGFR) have good responses to the tyrosine kinase inhibitor (TKI), gefitinib. However, patients with wild-type EGFR and acquired mutation in EGFR T790M are resistant to gefitinib treatment. Here, we showed that curcumin can improve the efficiency of gefitinib in the resistant NSCLC cells both in vitro and in vivo models.\\n\\nMETHODS/PRINCIPAL FINDINGS: After screening 598 herbal and natural compounds, we found curcumin could inhibit cell proliferation in different gefitinib-resistant NSCLC cell lines; concentration-dependently down-regulate EGFR phosphorylation through promoting EGFR degradation in NSCLC cell lines with wild-type EGFR or T790M EGFR. In addition, the anti-tumor activity of gefitinib was potentiated via curcumin through blocking EGFR activation and inducing apoptosis in gefitinib-resistant NSCLC cell lines; also the combined treatment with curcumin and gefitinib exhibited significant inhibition in the CL1-5, A549 and H1975 xenografts tumor growth in SCID mice through reducing EGFR, c-MET, cyclin D1 expression, and inducing apoptosis activation through caspases-8, 9 and PARP. Interestingly, we observed that the combined treatment group represented better survival rate and less intestinal mucosal damage compare to gefitinib-alone therapy. We showed that curcumin attenuated the gefitinib-induced cell proliferation inhibition and apoptosis through altering p38 mitogen-activated protein kinase (MAPK) activation in intestinal epithelia cell.\\n\\nCONCLUSIONS/SIGNIFICANCE: Curcumin potentiates antitumor activity of gefitinib in cell lines and xenograft mice model of NSCLC through inhibition of proliferation, EGFR phosphorylation, and induction EGFR ubiquitination and apoptosis. In addition, curcumin attenuates gefitinib-induced gastrointestinal adverse effects via altering p38 activation. These findings provide a novel treatment strategy that curcumin as an adjuvant to increase the spectrum of the usage of gefitinib and overcome the gefitinib inefficiency in NSCLC patients.", "link"=>"http://www.mendeley.com/research/curcumin-induces-egfr-degradation-lung-adenocarcinoma-modulates-p38-activation-intestine-versatile-a", "reader_count"=>48, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>7, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>3, "Student > Master"=>5, "Other"=>6, "Student > Bachelor"=>7, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>7, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>3, "Student > Master"=>5, "Other"=>6, "Student > Bachelor"=>7, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>4, "Medicine and Dentistry"=>13, "Agricultural and Biological Sciences"=>20, "Pharmacology, Toxicology and Pharmaceutical Science"=>4, "Sports and Recreations"=>1, "Chemistry"=>3, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>13}, "Chemistry"=>{"Chemistry"=>3}, "Social Sciences"=>{"Social Sciences"=>1}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>4}}, "reader_count_by_country"=>{"Japan"=>1, "Brazil"=>1, "United Kingdom"=>1, "Portugal"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/745339"], "description"=>"<p>(A) Analysis the half-life of EGFR protein level in 100 µg/ml cycloheximide treated CL1-5 cells with or without 10 µM curcumin by Western blotting. (B) Western blotting analysis revealed that MG132 recover the EGFR level of the curcumin-affected EGFR protein depletion. β-actin used as the internal control and the numbers below the row of the EGFR indicate the densitometric values normalized with the relative β-actin value. (C) Detection of ubiquitin (Ub) levels by immunoprecipitation of EGFR in CL1-5, A549 and H1975 cells showed the elevation of poly-Ub expressions in the presence of curcumin (10–15 µM). Ub and EGFR levels were measured by Western blotting.</p>", "links"=>[], "tags"=>["modulates", "egfr", "accelerating", "degradation", "gefitinib-resistant", "nsclc"], "article_id"=>415693, "categories"=>["Cancer", "Biological Sciences", "Cell Biology", "Genetics", "Evolutionary Biology"], "users"=>["Jen-Yi Lee", "Yee-Ming Lee", "Gee-Chen Chang", "Sung-Liang Yu", "Wan-Yu Hsieh", "Jeremy J. W. Chen", "Huei-Wen Chen", "Pan-Chyr Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023756.g002", "stats"=>{"downloads"=>3, "page_views"=>259, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Curcumin_potentially_modulates_EGFR_expression_by_accelerating_protein_degradation_in_gefitinib_resistant_NSCLC_cell_lines_/415693", "title"=>"Curcumin potentially modulates EGFR expression by accelerating protein degradation in gefitinib-resistant NSCLC cell lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:40:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/745755"], "description"=>"<p>(A) Western blotting analysis the gefitinib-resistant relative proteins EGFR, AKT, c-MET, cyclin D1, and PCNA showed the expression inhibition in curcumin alone or in combination group of xenograft tumor tissues. Western blotting results are represented with β-actin used as the internal control. Samples were pooled together from three animals in each group were analyzed and representative data are shown. (B) Western blotting analysis showing that combination of curcumin and gefitinib inhibits the expression of pro-caspase-8, pro-caspase-9 and pro-PARP and enhances the level of the cleavage (c)-PARP in xenograft tumor tissues. Western blotting results are represented with β-actin used as the internal control. Samples were pooled together from three animals in each group were analyzed and representative data are shown. (C) H&E staining, immunohistochemical staining of proliferation marker PCNA and apoptosis detection of TUNEL analysis in xenograft tumor sections from each group indicating that curcumin inhibited the tumor cell proliferation and enhanced the apoptotic cell death of gefitinib under a light microscope (×400 magnification).</p>", "links"=>[], "tags"=>["enhances", "gefitinib", "gefitinib-resistant", "proteins", "inducing", "apoptosis", "cl1-5", "xenograft"], "article_id"=>416105, "categories"=>["Cancer", "Biological Sciences", "Cell Biology", "Genetics", "Evolutionary Biology"], "users"=>["Jen-Yi Lee", "Yee-Ming Lee", "Gee-Chen Chang", "Sung-Liang Yu", "Wan-Yu Hsieh", "Jeremy J. W. Chen", "Huei-Wen Chen", "Pan-Chyr Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023756.g005", "stats"=>{"downloads"=>2, "page_views"=>29, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Curcumin_enhances_the_effect_of_gefitinib_against_gefitinib_resistant_relative_proteins_and_by_inducing_apoptosis_activity_CL1_5_xenograft_tumors_/416105", "title"=>"Curcumin enhances the effect of gefitinib against gefitinib-resistant relative proteins and by inducing apoptosis activity CL1-5 xenograft tumors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:42:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/745969"], "description"=>"<p>(A) Caspase-Glo 3/7 assay analysis showing gefitinib induced caspase 3/7 activity in the dose-dependent manner in IEC-18 cell, but curcumin reversed this gefitinib-induced caspase activity. <i>Columns</i>, mean (n = 3); <i>bars</i>, SD. **, <i>P</i><0.01. Data are representative of two independent experiments. (B) Western blotting analysis showed that gefitinib increased active-p38 expression in a dose-dependent manner (0–20 µM). β-actin used as the internal control and the numbers below the row of the active-p38 indicate the densitometric values normalized with the relative β-actin value. (C) Western blotting analysis showed that curcumin and BIRB 796 decreased the gefitinib-induced p38 activation protein level in IEC-18 cell. β-actin used as the internal control and the numbers below the row of the active-p38 indicate the densitometric values normalized with the relative β-actin value. (D) MTT assay results showed curcumin and BIRB 796 prevent the IEC-18 cell viability from the gefitinib-induced toxic damage. <i>Columns</i>, mean (n = 6); <i>bars</i>, SEM. **, <i>P</i><0.01. Data are representative of two independent experiments.</p>", "links"=>[], "tags"=>["gefitinib-induced", "gastrointestinal", "modulating", "p38", "activation"], "article_id"=>416333, "categories"=>["Cancer", "Biological Sciences", "Cell Biology", "Genetics", "Evolutionary Biology"], "users"=>["Jen-Yi Lee", "Yee-Ming Lee", "Gee-Chen Chang", "Sung-Liang Yu", "Wan-Yu Hsieh", "Jeremy J. W. Chen", "Huei-Wen Chen", "Pan-Chyr Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023756.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Curcumin_reduces_gefitinib_induced_gastrointestinal_damage_through_modulating_p38_activation_in_vitro_/416333", "title"=>"Curcumin reduces gefitinib-induced gastrointestinal damage through modulating p38 activation <i>in vitro</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:43:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/746176"], "description"=>"<p>The EGFR status and ethnicities of the NSCLC cell lines used for herb compounds screening.</p>", "links"=>[], "tags"=>["egfr", "ethnicities", "nsclc", "lines", "compounds"], "article_id"=>416541, "categories"=>["Cancer", "Biological Sciences", "Cell Biology", "Genetics", "Evolutionary Biology"], "users"=>["Jen-Yi Lee", "Yee-Ming Lee", "Gee-Chen Chang", "Sung-Liang Yu", "Wan-Yu Hsieh", "Jeremy J. W. Chen", "Huei-Wen Chen", "Pan-Chyr Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023756.t001", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_EGFR_status_and_ethnicities_of_the_NSCLC_cell_lines_used_for_herb_compounds_screening_/416541", "title"=>"The EGFR status and ethnicities of the NSCLC cell lines used for herb compounds screening.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 15:44:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/745237"], "description"=>"<p>(A) MTT assay results showed susceptibility of gefitinib in all six lung adenocarcinoma cell lines. <i>Columns</i>, mean (n = 6); <i>bars</i>, SEM. Data are representative of two independent experiments. (B) MTT assay analysis showed curcumin harbored dose-dependent suppression of cell proliferation in five gefitinib-resistant NSCLC cell lines. <i>Columns</i>, mean (n = 6); <i>bars</i>, SEM. Data are representative of two independent experiments. (C) Western blotting analysis showed curcumin decrease the EGF (20 ng/ml)-induced EGFR and pEGFR, expression in CL1-5, A549 and H1975 cells in a dose-dependent manner (1–20 µM). β-actin used as the internal control and the numbers below the row of the EGFR and pEGFR indicate the densitometric values normalized with the relative β-actin value.</p>", "links"=>[], "tags"=>["inhibits", "proliferation", "down-regulates", "egfr", "activation", "gefitinib-resistant", "nsclc"], "article_id"=>415595, "categories"=>["Cancer", "Biological Sciences", "Cell Biology", "Genetics", "Evolutionary Biology"], "users"=>["Jen-Yi Lee", "Yee-Ming Lee", "Gee-Chen Chang", "Sung-Liang Yu", "Wan-Yu Hsieh", "Jeremy J. W. Chen", "Huei-Wen Chen", "Pan-Chyr Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023756.g001", "stats"=>{"downloads"=>4, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Curcumin_inhibits_cell_proliferation_and_down_regulates_EGFR_activation_in_gefitinib_resistant_NSCLC_cell_lines_/415595", "title"=>"Curcumin inhibits cell proliferation and down-regulates EGFR activation in gefitinib-resistant NSCLC cell lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:39:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/745853"], "description"=>"<p>(A) The animal survival rates for each group indicate that curcumin decreased mouse death caused by the adverse effects of gefitinib. (B) H&E staining analysis of intestine sections from each group showing that curcumin prevents villi damage; villi lengths were quantified (bar = 200 µm). <i>Columns</i>, mean (n = 3); <i>bars</i>, SEM. <i>P</i> = 0.0001 (gefitinib versus combination). (C) Apoptosis detection by TUNEL assay using intestine sections from each group. The results indicated that curcumin reduced the TUNEL-positive cells in the villi in the presence of gefitinib. (D) Quantification of TUNEL-positive cells as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0023756#s4\" target=\"_blank\">Materials and Methods</a>. <i>Columns</i>, mean (n = 10); <i>bars</i>, SEM. <i>P</i> = 0.0015 (gefitinib versus combination).</p>", "links"=>[], "tags"=>["attenuates", "gastrointestinal", "adverse", "gefitinib"], "article_id"=>416217, "categories"=>["Cancer", "Biological Sciences", "Cell Biology", "Genetics", "Evolutionary Biology"], "users"=>["Jen-Yi Lee", "Yee-Ming Lee", "Gee-Chen Chang", "Sung-Liang Yu", "Wan-Yu Hsieh", "Jeremy J. W. Chen", "Huei-Wen Chen", "Pan-Chyr Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023756.g006", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Curcumin_attenuates_the_gastrointestinal_adverse_effects_of_gefitinib_in_vivo_/416217", "title"=>"Curcumin attenuates the gastrointestinal adverse effects of gefitinib <i>in vivo</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:43:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/746105"], "description"=>"<p>Curcumin enhances the antitumor effects of gefitinib on lung adenocarcinoma are hypothesized to occur through the induction of EGFR degradation, the blockage of EGFR activation, promoting apoptosis, inhibiting the expression of c-MET, cyclin D1 and PCNA. On the other hand, curcumin attenuates the gefitinib-induced damage on intestinal epithelial cells through modulating p38 kinase activation and cell apoptosis.</p>", "links"=>[], "tags"=>["curcumin", "adenocarcinoma", "cells", "intestine", "epithelial"], "article_id"=>416472, "categories"=>["Cancer", "Biological Sciences", "Cell Biology", "Genetics", "Evolutionary Biology"], "users"=>["Jen-Yi Lee", "Yee-Ming Lee", "Gee-Chen Chang", "Sung-Liang Yu", "Wan-Yu Hsieh", "Jeremy J. W. Chen", "Huei-Wen Chen", "Pan-Chyr Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023756.g008", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Scheme_of_the_curcumin_regulatory_effects_on_lung_adenocarcinoma_cells_and_intestine_epithelial_cells_/416472", "title"=>"Scheme of the curcumin regulatory effects on lung adenocarcinoma cells and intestine epithelial cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:44:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/745613"], "description"=>"<p>(A) <i>left</i>, 10<sup>6</sup> CL1-5 cells were implanted s.c. in SCID mice and tumor volumes were monitored over time. <i>Points,</i> mean (n = 6); <i>bars</i>, SD; <i>right</i>, tumor volume in CL1-5 xenograft were measured on the last day of the experiment using vernier calipers. <i>Columns</i>, mean (n = 6); <i>bars</i>, SD. <i>P</i> = 0.0003 (control versus gefitinib), 0.0006 (control versus 1 g/kg and 60 mg/kg gefitinib) and 0.484 (1 g/kg and 60 mg/kg gefitinib versus gefitinib). (B) <i>left</i>, 10<sup>6</sup> A549 xenograft study processed as well as the methods in CL1-5 xenograft. <i>Points</i>, mean (n = 6); <i>bars</i>, SD; <i>right</i>, tumor volume in A549 xenograft were measured on the last day of the experiment using vernier calipers. <i>Columns</i>, mean (n = 6); <i>bars</i>, SD. <i>P</i> = 0.0028 (control versus combination), 0.02 (control versus gefitinib). (C) <i>left</i>, bioluminescence IVIS images of A549 xenograft mice were visualized in anesthetized animals after i.p. inoculation of D-luciferin. The photon flux were measured per second and depicted as the tumor volume at the indicated time using IVIS imaging. <i>Points</i>, mean (n = 6); <i>bars</i>, SD. <i>P</i> = 0.019 (control versus combination), 0.146 (control versus gefitinib). <i>right</i>, tumor volume in H1975 xenograft were measured on the last day of the experiment using vernier calipers. <i>Columns</i>, mean (n = 6); <i>bars</i>, SD. <i>P</i> = 0.0013 (control versus combination), 0.016 (control versus gefitinib) and 0.025 (gefitinib versus combination). The xenograft protocols were detail described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0023756#s4\" target=\"_blank\">Materials and Methods</a>.</p>", "links"=>[], "tags"=>["sensitizes", "gefitinib", "inhibiting", "gefitinib-resistant", "nsclc", "scid"], "article_id"=>415973, "categories"=>["Cancer", "Biological Sciences", "Cell Biology", "Genetics", "Evolutionary Biology"], "users"=>["Jen-Yi Lee", "Yee-Ming Lee", "Gee-Chen Chang", "Sung-Liang Yu", "Wan-Yu Hsieh", "Jeremy J. W. Chen", "Huei-Wen Chen", "Pan-Chyr Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023756.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Curcumin_sensitizes_the_effect_of_gefitinib_in_inhibiting_the_growth_of_gefitinib_resistant_NSCLC_in_SCID_mice_/415973", "title"=>"Curcumin sensitizes the effect of gefitinib in inhibiting the growth of gefitinib-resistant NSCLC in SCID mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:41:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/745461"], "description"=>"<p>(A) MTT assay results showed curcumin enhanced the anti-proliferative effect of gefitinib in CL1-5, A549 and H1975 gefitinib-resistant lung adenocarcinoma cell lines. <i>Columns</i>, mean (n = 6); <i>bars</i>, SEM. **, <i>P</i><0.01. Data are representative of two independent experiments. (B) Western blotting analysis showed curcumin improve the blockage of EGF (20 ng/ml)-induced EGFR and pEGFR expression of gefitinib in CL1-5, A549 and H1975 cell lines. β-actin used as the internal control and the numbers below the row of the pEGFR indicate the densitometric values normalized with the relative β-actin value. (C) Annexin V-FITC apoptosis assay results showed curcumin enhance the apoptotic effect of gefitinib, CL1-5 cell was treated agents as indicating. The <i>x</i> axis is Annexin-V-FITC, and the <i>y</i> axis is PI (propidium iodide) for all graphs represented; CL1-5, A549 and H1975 cells undergoing apoptosis were statistically counted the Annexin-V<sup>+</sup> and PI<sup>-</sup> levels of total cells in the lower right quadrant. <i>Columns</i>, mean (n = 3); <i>bars</i>, SD. *, <i>P</i><0.05, **, <i>P</i><0.01 and <i>P</i> = 0.331 (15 µM curcumin versus 1 µM gefitinib plus 15 µM curcumin). Data are representative of triplicate independent experiments. (D) Colony formation assay analysis represented curcumin enhance the colony inhibitory ability of gefitinib in CL1-5, A549 and H1975 cells. Cells cell was treated agents as indicating; V: vehicle control, G1, G5, G10, G15, C1, C5, C10, C15, G1+C1, G1+C5, G1+C10 and G1+C15: G and C indicated gefitinib and curcumin, and number showed the concentrations (µM) of the agents, respectively; Colony formation index (%) was expressed as the percent of cells number in the each groups compared to the vehicle control. Colonies were counted after 2 weeks of the experiment using crystal violet staining. <i>Columns</i>, mean (n = 3); <i>bars</i>, SD. Data are representative of two independent experiments.</p>", "links"=>[], "tags"=>["potentiates", "antitumor", "abilities", "gefitinib", "egfr", "apoptotic", "gefitinib-resistant", "nsclc"], "article_id"=>415819, "categories"=>["Cancer", "Biological Sciences", "Cell Biology", "Genetics", "Evolutionary Biology"], "users"=>["Jen-Yi Lee", "Yee-Ming Lee", "Gee-Chen Chang", "Sung-Liang Yu", "Wan-Yu Hsieh", "Jeremy J. W. Chen", "Huei-Wen Chen", "Pan-Chyr Yang"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0023756.g003", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Curcumin_potentiates_antitumor_abilities_of_gefitinib_in_cell_proliferation_EGFR_activation_apoptotic_ability_and_colony_formation_of_gefitinib_in_gefitinib_resistant_in_NSCLC_in_vitro_/415819", "title"=>"Curcumin potentiates antitumor abilities of gefitinib in cell proliferation, EGFR activation, apoptotic ability, and colony formation of gefitinib in gefitinib-resistant in NSCLC <i>in vitro</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:40:53"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"27", "full-text"=>"23", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"18", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"16", "full-text"=>"16", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
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  • {"unique-ip"=>"29", "full-text"=>"25", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"25", "full-text"=>"26", "pdf"=>"6", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"23", "full-text"=>"27", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
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  • {"unique-ip"=>"25", "full-text"=>"25", "pdf"=>"10", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"11", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"5"}
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  • {"unique-ip"=>"18", "full-text"=>"19", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
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  • {"unique-ip"=>"19", "full-text"=>"20", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"27", "full-text"=>"27", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"37", "full-text"=>"27", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"22", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"15", "full-text"=>"8", "pdf"=>"13", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"15", "full-text"=>"19", "pdf"=>"7", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"3"}
  • {"unique-ip"=>"24", "full-text"=>"28", "pdf"=>"4", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"4"}
  • {"unique-ip"=>"18", "full-text"=>"18", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"5"}
  • {"unique-ip"=>"21", "full-text"=>"23", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"6"}
  • {"unique-ip"=>"25", "full-text"=>"31", "pdf"=>"11", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"7"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"8"}

Relative Metric

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