Mild Endoplasmic Reticulum Stress Promotes Retinal Neovascularization via Induction of BiP/GRP78
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{"title"=>"Mild Endoplasmic Reticulum Stress Promotes Retinal Neovascularization via Induction of BiP/GRP78", "type"=>"journal", "authors"=>[{"first_name"=>"Shinsuke", "last_name"=>"Nakamura", "scopus_author_id"=>"35303495400"}, {"first_name"=>"Haruka", "last_name"=>"Takizawa", "scopus_author_id"=>"37018759700"}, {"first_name"=>"Masamitsu", "last_name"=>"Shimazawa", "scopus_author_id"=>"6602683783"}, {"first_name"=>"Yuhei", "last_name"=>"Hashimoto", "scopus_author_id"=>"55633145500"}, {"first_name"=>"Sou", "last_name"=>"Sugitani", "scopus_author_id"=>"55178594200"}, {"first_name"=>"Kazuhiro", "last_name"=>"Tsuruma", "scopus_author_id"=>"6505831524"}, {"first_name"=>"Hideaki", "last_name"=>"Hara", "scopus_author_id"=>"56799750000"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84875475183", "pui"=>"368602228", "doi"=>"10.1371/journal.pone.0060517", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"84875475183", "pmid"=>"23544152"}, "id"=>"82dda575-6387-3455-816e-ecb669ba775d", "abstract"=>"Endoplasmic reticulum (ER) stress occurs as a result of accumulation of unfolded or misfolded proteins in the ER and is involved in the mechanisms of various diseases, such as cancer and neurodegeneration. The goal of the present study was to clarify the relationship between ER stress and pathological neovascularization in the retina. Proliferation and migration of human retinal microvascular endothelial cells (HRMEC) were assessed in the presence of ER stress inducers, such as tunicamycin and thapsigargin. The expression of ER chaperone immunoglobulin heavy-chain binding protein (BiP), known as Grp78, was evaluated by real time RT-PCR, immunostaining, and Western blotting. Tunicamycin or thapsigargin was injected into the intravitreal body of oxygen-induced retinopathy (OIR) model mice at postnatal day 14 (P14) and retinal neovascularization was quantified at P17. The expression and localization of BiP in the retina was also evaluated in the OIR model. Exposure to tunicamycin and thapsigargin increased the proliferation and migration of HRMEC. Tunicamycin enhanced the expression of BiP in HRMEC at both the mRNA level and at the protein level on the cell surface, and increased the formation of a BiP/T-cadherin immunocomplex. In OIR model mice, retinal neovascularization was accelerated by treatments with ER stress inducers. BiP was particularly observed in the pathological vasculature and retinal microvascular endothelial cells, and the increase of BiP expression was correlated with retinal neovascularization. In conclusion, ER stress may contribute to the formation of abnormal vasculature in the retina via BiP complexation with T-cadherin, which then promotes endothelial cell proliferation and migration.", "link"=>"http://www.mendeley.com/research/mild-endoplasmic-reticulum-stress-promotes-retinal-neovascularization-via-induction-bipgrp78", "reader_count"=>26, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>3, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>5, "Student > Master"=>8, "Student > Bachelor"=>4, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>3, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>5, "Student > Master"=>8, "Student > Bachelor"=>4, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>4, "Mathematics"=>1, "Agricultural and Biological Sciences"=>12, "Medicine and Dentistry"=>6, "Neuroscience"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Neuroscience"=>{"Neuroscience"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Portugal"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/999076"], "description"=>"<p>HRMEC were cultured in a 96-well plate (at a density of 2×10<sup>3</sup> cells/well), and were then supplemented with the indicated concentrations of (A) tunicamycin or (B) thapsigargin for 2 h, and measurements were made by WST-8 assay. Data are shown as mean ± S.E.M. (n = 6 or 12). *, p<0.05; **, p<0.01 vs. Control (Dunnett's multiple-comparison test). ##, p<0.01 vs. Control (Student's <i>t</i>-test). Migration of HRMEC was assessed using a wound-healing assay. Briefly, 90% confluent monolayers of HRMEC were scratch-wounded, and then incubated for 24 h. Images of the wounded monolayer of HRMEC were taken at 24 h after treatment for 2 h with (C) tunicamycin or (D) thapsigargin. Migration was estimated by measurement of cell numbers within the wounded region. The indicated concentrations of (E) tunicamycin and (F) thapsigargin increased migration compared to the control. Scale bars indicate 500 µm. Data are shown as mean ± S.E.M. (n = 3 to 7). *, p<0.05; **, p<0.01 vs. Control (Dunnett's multiple-comparison test).</p>", "links"=>[], "tags"=>["stress-induced", "proliferation"], "article_id"=>661100, "categories"=>["Physiology", "Cell Biology", "Medicine"], "users"=>["Shinsuke Nakamura", "Haruka Takizawa", "Masamitsu Shimazawa", "Yuhei Hashimoto", "Sou Sugitani", "Kazuhiro Tsuruma", "Hideaki Hara"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060517.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ER_stress_induced_proliferation_and_migration_in_HRMEC_/661100", "title"=>"ER stress-induced proliferation and migration in HRMEC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-28 08:08:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/999079"], "description"=>"<p>(A) Representative images of migration test with tunicamycin at 10 µg/mL and thapsigargin at 10 µM are shown. (B) Both tunicamycin at 10 µg/mL and thapsigargin at 10 µM inhibited the cell migration in HRMEC. Fluorescence micrographs of Hoechst 33342 and PI staining are shown at 24 h after treatment for 2 h with (C) tunicamycin or (D) thapsigargin. Scale bar represents 100 µm. The dead cells were increased with (E) tunicamycin or (F) thapsigargin. Data are shown as mean ± S.E.M. (n = 6). *, p<0.05; **, p<0.01 vs. Control (Dunnett's multiple-comparison test). (G) Fluorescence photomicrographs of HRMEC triple-stained with propidium iodide (PI), annexin V-FITC, and Hoechst 33342, with tunicamycin. Red: Propidium Iodide, Green: Annexin V, blue: Hoechst33342. Scale bar represents 100 µm. (H) The apoptotic cells were significantly increased with tunicamycin at 3 and 10 µg/mL. Scale bar represents 100 µm. Data are shown as mean ± S.E.M. (n = 4). *, p<0.05; **, p<0.01 vs. Control (Dunnett's multiple-comparison test).</p>", "links"=>[], "tags"=>["er", "stress-induced", "hrmec"], "article_id"=>661103, "categories"=>["Physiology", "Cell Biology", "Medicine"], "users"=>["Shinsuke Nakamura", "Haruka Takizawa", "Masamitsu Shimazawa", "Yuhei Hashimoto", "Sou Sugitani", "Kazuhiro Tsuruma", "Hideaki Hara"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060517.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Severe_ER_stress_induced_cell_death_of_HRMEC_via_the_apoptotis_/661103", "title"=>"Severe ER stress-induced cell death of HRMEC <i>via</i> the apoptotis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-28 08:09:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/999082"], "description"=>"<p>(A) Electron microscopic images are shown for 2 h with tunicamycin at 0.1 µg/mL. Tunicamycin induced the mild dilation of endoplasmic reticulum (ER). Scale bar represents 500 nm. Arrows indicate the ER in HRMEC. The mRNA levels of (B) <i>BiP</i> and (C) <i>CHOP</i> in HRMEC were determined by real-time RT-PCR and normalized against <i>β-actin</i>. Data are shown as mean ± S.E.M. (n = 4 to 6). *, p<0.05 vs. Control (Student's <i>t</i>-test). (D) <i>XBP-1</i> mRNA was not spliced by treatment with tunicamycin. HRMEC were harvested at 10 min, 30 min, 1 h, and 2 h after addition of tunicamycin, or at 10 and 22 h after incubation. Typical gel images of spliced or unspliced <i>XBP-1</i> bands at each sampling point were generated by MCE-202 MultiNA, a microchip based capillary electrophoresis system for DNA analysis (n = 3 or 4). (E) The mRNA level of <i>VEGF</i>, as a common angiogenic factor, was determined by real-time RT-PCR before and after the induction of <i>BiP</i> mRNA and <i>CHOP</i> mRNA, but no differences were apparent between the control and tunicamycin treated groups. Data are shown as mean ± S.E.M. (n = 4 or 5). For 1 h, p = 0.80; for 2 h, p = 0.91; for 12 h, p = 0.99 vs. Control (Student's <i>t</i>-test).</p>", "links"=>[], "tags"=>["activated", "transcription", "mrna", "dilation", "er"], "article_id"=>661106, "categories"=>["Physiology", "Cell Biology", "Medicine"], "users"=>["Shinsuke Nakamura", "Haruka Takizawa", "Masamitsu Shimazawa", "Yuhei Hashimoto", "Sou Sugitani", "Kazuhiro Tsuruma", "Hideaki Hara"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060517.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tunicamycin_at_low_concentration_activated_the_transcription_of_BiP_and_CHOP_mRNA_with_the_mild_dilation_of_ER_in_HRMEC_/661106", "title"=>"Tunicamycin at low concentration activated the transcription of <i>BiP</i> and <i>CHOP</i> mRNA with the mild dilation of ER in HRMEC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-28 08:09:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/999085"], "description"=>"<p>HRMEC were treated with 10 ng/ml of tunicamycin for 2 h. (A) BiP on the cell surface was precipitated after biotinylation to detect cell surface protein in untreated (control) or tunicamycin treated cells. (B) BiP and T-cadherin were immunoprecipitated with the anti-KDEL antibody to confirm the association of BiP with T-cadherin. Whole lysate without immunoprecipitation with the anti-BiP antibody was similarly evaluated. (C) After the membrane extraction, BiP and T-cadherin were immunoprecipitated with the anti-T-cadherin antibody and detected by using Western blotting with the anti-BiP antibody. Whole lysate without immunoprecipitation with the anti-VEGF receptor-2 (VEGFR-2) antibody was similarly evaluated to confirm the success of the membrane extraction. (D) Immunostaining showed the presence of BiP and T-cadherin on the surface of HRMEC. Scale bar indicates 30 µm.</p>", "links"=>[], "tags"=>["stress-induced", "complexes"], "article_id"=>661109, "categories"=>["Physiology", "Cell Biology", "Medicine"], "users"=>["Shinsuke Nakamura", "Haruka Takizawa", "Masamitsu Shimazawa", "Yuhei Hashimoto", "Sou Sugitani", "Kazuhiro Tsuruma", "Hideaki Hara"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060517.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ER_stress_induced_formation_of_BiP_T_cadherin_complexes_on_the_surface_of_HRMEC_/661109", "title"=>"ER stress-induced formation of BiP/T-cadherin complexes on the surface of HRMEC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-28 08:09:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/999087"], "description"=>"<p>The original images (A, C and G, I), together with the analyzed images (B, D and H, J) obtained using the Angiogenesis Tube Formation module in Metamorph, are shown. Scale bars indicate 500 µm and 100 µm (in box). Green labels in the analyzed images show the node regions. Quantitative analysis was performed on the entire retinal microvasculature in flat-mounted retinas obtained at P17. Tunicamycin at 3 µg/ml and thapsigargin at 1 µM increased (vs. vehicle) both the number of nodes (E, K) and the node areas (F, L), which are indexes of pathological neovascularization as calculated using the Angiogenesis Tube Formation module. Data are shown as mean ± S.E.M. (n = 5 to 9). *, p<0.05; **, p<0.01 vs.Vehicle (Student's <i>t</i>-test).</p>", "links"=>[], "tags"=>["thapsigargin", "accelerated", "retinal", "neovascularization", "murine", "oxygen-induced", "retinopathy"], "article_id"=>661111, "categories"=>["Physiology", "Cell Biology", "Medicine"], "users"=>["Shinsuke Nakamura", "Haruka Takizawa", "Masamitsu Shimazawa", "Yuhei Hashimoto", "Sou Sugitani", "Kazuhiro Tsuruma", "Hideaki Hara"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060517.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tunicamycin_and_thapsigargin_accelerated_retinal_neovascularization_in_a_murine_oxygen_induced_retinopathy_OIR_model_/661111", "title"=>"Tunicamycin and thapsigargin accelerated retinal neovascularization in a murine oxygen-induced retinopathy (OIR) model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-28 08:10:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/999090"], "description"=>"<p>(A) OIR model mice at P17, treated with 3 µg/ml of tunicamycin at P14, were perfused with FITC-dextran and the retinas were stained with anti-BiP antibody. The original images (green channel) and BiP stained images (red channel) are shown, along with the analyzed images. (B) BiP (green channel) and CD31 (red channel) staining in flat-mounted retinas of P17 mice, under normoxia or subjected to the OIR protocol, following tunicamycin injection. Arrowheads and arrows indicate normal vessels and newly formed vessels anterior to internal limiting membrane, respectively. Scale bars indicate 50 µm. The complexes of BiP and T-cadherin in the retina were immunoprecipitated with the anti-T-cadherin antibody and detected by using Western blotting with the anti-BiP antibody (C), or by the Coomassie-staining (D).</p>", "links"=>[], "tags"=>["retinal", "vascular", "endothelial", "cells", "murine", "oxygen-induced", "retinopathy"], "article_id"=>661114, "categories"=>["Physiology", "Cell Biology", "Medicine"], "users"=>["Shinsuke Nakamura", "Haruka Takizawa", "Masamitsu Shimazawa", "Yuhei Hashimoto", "Sou Sugitani", "Kazuhiro Tsuruma", "Hideaki Hara"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060517.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BiP_was_expressed_in_the_retinal_vascular_endothelial_cells_of_a_murine_oxygen_induced_retinopathy_OIR_model_/661114", "title"=>"BiP was expressed in the retinal vascular endothelial cells of a murine oxygen-induced retinopathy (OIR) model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-28 08:11:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/999091"], "description"=>"<p>(A) The representative photographs are shown the retinal flat-mount (the upper images) and the higher magnification version of part of the corresponding upper images (the lower images). Arrows indicate newly formed vessels anterior to internal limiting membrane. Scale bars indicate 500 µm (Upper images) and 100 µm (Lower images). Quantitative analysis was performed on the entire retinal microvasculature time-dependently. In the OIR model, retinal neovascularization at P14 and P17 significantly increased both the number of nodes (B) and the nodes area (C), compared to that at P12. In the retina of the same individual, BiP induction was caused time-dependently (D). Relative intensity was described by the intensity of BiP divided by β-actin (E). Data are shown as mean ± S.E.M. (n = 6 to 9). *, p<0.05, **, p<0.01 vs. OIR mice at P12 (Dunnett's multiple-comparison test).</p>", "links"=>[], "tags"=>["bip", "retinal", "neovascularization", "murine", "oxygen-induced", "retinopathy"], "article_id"=>661115, "categories"=>["Physiology", "Cell Biology", "Medicine"], "users"=>["Shinsuke Nakamura", "Haruka Takizawa", "Masamitsu Shimazawa", "Yuhei Hashimoto", "Sou Sugitani", "Kazuhiro Tsuruma", "Hideaki Hara"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060517.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_expression_of_BiP_was_associated_with_retinal_neovascularization_of_a_murine_oxygen_induced_retinopathy_OIR_model_/661115", "title"=>"The expression of BiP was associated with retinal neovascularization of a murine oxygen-induced retinopathy (OIR) model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-28 08:12:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/999094"], "description"=>"<p>(A) HRMEC were cultured in a 96-well plate (at a density of 2×10<sup>3</sup> cells/well), and were then supplemented with the indicated concentrations of BiX for 1 h, and measurements were made by WST-8 assay. Data are shown as mean ± S.E.M. (n = 6). *, p<0.05 vs. Control (Dunnett's multiple-comparison test). Migration of HRMEC was assessed using a wound-healing assay. (B) Images of the wounded monolayer of HRMEC were taken at 24 h after treatment for 1 h with BiX. (C) The indicated concentrations of BiX increased migration compared to the control. Scale bars indicate 500 µm. Data are shown as mean ± S.E.M. (n = 4). **, p<0.01 vs. Control (Dunnett's multiple-comparison test). The original images (D, F and J, L), together with the analyzed images (E, G and K, M) obtained using the Angiogenesis Tube Formation module in Metamorph, are shown. Scale bars indicate 500 µm and 100 µm (in box). Quantitative analysis was performed on the entire retinal microvasculature in flat-mounted retinas obtained at P17. BiX at 1 µM and BiP small interfering (si) RNA at 1 µg/mL increased (vs. vehicle) both the number of nodes (E, K) and the node areas (F, L), which are indexes of pathological neovascularization as calculated using the Angiogenesis Tube Formation module. Data are shown as mean ± S.E.M. (n = 4 or 5). *, p<0.05 vs.Vehicle (Student's <i>t</i>-test).</p>", "links"=>[], "tags"=>["regulates", "retinal"], "article_id"=>661118, "categories"=>["Physiology", "Cell Biology", "Medicine"], "users"=>["Shinsuke Nakamura", "Haruka Takizawa", "Masamitsu Shimazawa", "Yuhei Hashimoto", "Sou Sugitani", "Kazuhiro Tsuruma", "Hideaki Hara"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0060517.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BiP_protein_levels_regulates_retinal_neovascularization_/661118", "title"=>"BiP protein levels regulates retinal neovascularization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-28 08:12:40"}

PMC Usage Stats | Further Information

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Relative Metric

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