Sustained Induction of Collagen Synthesis by TGF-β Requires Regulated Intramembrane Proteolysis of CREB3L1
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{"title"=>"Sustained induction of collagen synthesis by TGF-β requires regulated intramembrane proteolysis of CREB3L1", "type"=>"journal", "authors"=>[{"first_name"=>"Qiuyue", "last_name"=>"Chen", "scopus_author_id"=>"46260925700"}, {"first_name"=>"Ching En", "last_name"=>"Lee", "scopus_author_id"=>"56381674700"}, {"first_name"=>"Bray", "last_name"=>"Denard", "scopus_author_id"=>"24490808900"}, {"first_name"=>"Jin", "last_name"=>"Ye", "scopus_author_id"=>"55547034400"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"25310401", "doi"=>"10.1371/journal.pone.0108528", "sgr"=>"84907907056", "scopus"=>"2-s2.0-84907907056", "issn"=>"19326203", "pui"=>"600148324"}, "id"=>"c97e55c7-b18c-3578-a65c-ed55d7138ce4", "abstract"=>"CREB3L1 (cAMP response element binding protein 3-like 1), a transcription factor synthesized as a membrane-bound precursor and activated through Regulated Intramembrane Proteolysis (RIP), is essential for collagen production by osteoblasts during bone development. Here, we show that TGF-β (transforming growth factor-β), a cytokine known to stimulate production of collagen during wound healing and fibrotic diseases, induces proteolytic activation of CREB3L1 in human A549 cells. This activation results from inhibition of expression of TM4SF20 (transmembrane 4 L6 family member 20), which normally inhibits RIP of CREB3L1. Cleavage of CREB3L1 releases its NH2-terminal domain from membranes, allowing it to enter the nucleus where it binds to Smad4 to activate transcription of genes encoding proteins required for assembly of collagen-containing extracellular matrix. Our findings raise the possibility that inhibition of RIP of CREB3L1 could prevent excess deposition of collagen in certain fibrotic diseases.", "link"=>"http://www.mendeley.com/research/sustained-induction-collagen-synthesis-tgf%CE%B2-requires-regulated-intramembrane-proteolysis-creb3l1", "reader_count"=>15, "reader_count_by_academic_status"=>{"Student > Doctoral Student"=>2, "Researcher"=>3, "Student > Ph. D. Student"=>4, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>3}, "reader_count_by_user_role"=>{"Student > Doctoral Student"=>2, "Researcher"=>3, "Student > Ph. D. Student"=>4, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>3}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>6, "Medicine and Dentistry"=>4, "Neuroscience"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>6}, "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"=>{"Japan"=>1, "Russia"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1715221"], "description"=>"<p>(<i>A</i>) On day 0, A549 cells were seeded at 1×10<sup>5</sup> cells per 60 mm dish. On day 1, the cells were transfected with indicted siRNAs. On day 3, cells were treated with or without 1 ng/ml TGF-β for 12 h. cells were then harvested for quantification of TM4SF20 mRNA by RT-QPCR. The amount of the mRNA in cells that were not treated with TGF-β and transfected with the control siRNA is set to 1. (<i>B</i>) On day 0, A549 cells were seeded at 4×10<sup>5</sup> cells per 60 mm dish. On day 1, the cells were treated with 1 ng/ml TGF-β for the indicated time. Cells were then harvested for quantification of TM4SF20 mRNA by RT-QPCR. The amount of the mRNA in cells immediately before the TGF-β treatment is set to 1. (<i>C and D</i>) On day 0, A549 cells were seeded at 1×10<sup>5</sup> cells per 60 mm dish. On day 1, the cells were transfected with indicted siRNAs. On day 3, cells were treated with or without 1 ng/ml TGF-β. On day 4, 24 h after the treatment, cells were harvested for quantification of TM4SF20 mRNA as described in <i>A</i> (<i>C</i>), and analysis of RIP of CREB3L1 as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108528#pone-0108528-g001\" target=\"_blank\">Fig. 1<i>A</i></a> (<i>D</i>). (<i>E and F</i>) On day 0, A549 and A549/pTM4SF20 cells were seeded at 4×10<sup>5</sup> cells per 60 mm dish. On day 1, cells were treated with or without 1 ng/ml TGF-β. On day 2, 24 h after the treatment, cells were harvested for quantification of TM4SF20 mRNA by RT-QPCR, with the amount of the mRNA in A549 cells that were not treated with TGF-β set to 1 (<i>E</i>), and analysis of RIP of CREB3L1 as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108528#pone-0108528-g001\" target=\"_blank\">Fig. 1<i>A</i></a> (<i>F</i>). (<i>A–G</i>) Bar graphs are reported as mean ± S.E.M. of three independent experiments.</p>", "links"=>[], "tags"=>["genes encoding proteins", "rip", "CREB 3L", "CREB 3L CREB 3L", "Regulated Intramembrane Proteolysis", "fibrotic diseases", "collagen", "nh", "4SF", "tm", "tgf", "CREB 3L releases", "CREB 3L Cleavage"], "article_id"=>1202560, "categories"=>["Biological Sciences"], "users"=>["Qiuyue Chen", "Ching-En Lee", "Bray Denard", "Jin Ye"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108528.g004", "stats"=>{"downloads"=>0, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TGF_946_induces_CREB3L1_cleavage_by_inhibiting_expression_of_TM4SF20_/1202560", "title"=>"TGF-β induces CREB3L1 cleavage by inhibiting expression of TM4SF20.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-13 03:02:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/1715222"], "description"=>"<p>(<i>A</i>) A549 cells were set up, treated, and analyzed with immunoblot with indicated antibodies as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108528#pone-0108528-g001\" target=\"_blank\">Fig. 1<i>C</i></a>. (<i>B–D</i>) On day 0, A549 cells were seeded at 4×10<sup>5</sup> cells per 60 mm dish. On day 1, cells were treated with 0.5 µM RDEA119 or PD0325901 for 3 h followed by treatment with 1 ng/ml TGF-β as indicated. On day 2, 24 h after the TGF-β treatment, cells were harvested for immunoblot analysis with indicated antibodies (<i>B and D</i>) and quantification of TM4SF20 mRNA with RT-QPCR, with the amount of the mRNA in untreated cells set to 1 (Results are reported as mean ± S.E.M. of three independent experiments) (<i>C</i>).</p>", "links"=>[], "tags"=>["genes encoding proteins", "rip", "CREB 3L", "CREB 3L CREB 3L", "Regulated Intramembrane Proteolysis", "fibrotic diseases", "collagen", "nh", "4SF", "tm", "tgf", "CREB 3L releases", "CREB 3L Cleavage"], "article_id"=>1202561, "categories"=>["Biological Sciences"], "users"=>["Qiuyue Chen", "Ching-En Lee", "Bray Denard", "Jin Ye"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108528.g005", "stats"=>{"downloads"=>0, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TGF_946_induces_cleavage_of_CREB3L1_through_activation_of_ERKs_/1202561", "title"=>"TGF-β induces cleavage of CREB3L1 through activation of ERKs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-13 03:02:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/1715223"], "description"=>"<p>In the absence of TGF-β, Smad2 and Smad3 (Smad2/3) are not phosphorylated. RIP of CREB3L1 is blocked by TM4SF20. In the absence of activation of these transcription factors, expression of collagen is not induced. Acute exposure of cells to TGF-β results in heterodimerization of two TGF-β receptors, namely TGFβRI and TGFβRII. Consequently, Smad2/3 are phosphorylated by the activated receptor, allowing them to form a complex with Smad4 to drive transcription of collagen. TGF-β treatment also leads to phosphorylation of ERKs, which in turn inhibit transcription of TM4SF20. In cells chronically exposed to TGF-β, the amount of phosphorylated Smad2/3 is drastically reduced. Owing to depletion of TM4SF20, CREB3L1 is cleaved by S1P and S2P. This cleavage releases the NH<sub>2</sub>-terminal domain of CREB3L1 from membranes, allowing it to form a complex with Smad4 to continue activating transcription of collagen.</p>", "links"=>[], "tags"=>["genes encoding proteins", "rip", "CREB 3L", "CREB 3L CREB 3L", "Regulated Intramembrane Proteolysis", "fibrotic diseases", "collagen", "nh", "4SF", "tm", "tgf", "CREB 3L releases", "CREB 3L Cleavage"], "article_id"=>1202562, "categories"=>["Biological Sciences"], "users"=>["Qiuyue Chen", "Ching-En Lee", "Bray Denard", "Jin Ye"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108528.g006", "stats"=>{"downloads"=>0, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_model_illustrating_the_role_of_CREB3L1_in_TGF_946_induced_collagen_synthesis_/1202562", "title"=>"A model illustrating the role of CREB3L1 in TGF-β-induced collagen synthesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-13 03:02:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/1715208"], "description"=>"<p>(<i>A–C</i>) On day 0, A549 cells were seeded at 4×10<sup>5</sup> cells per 60-mm dish. On day 1, cells were treated with 1 ng/ml TGF-β for the indicated time. For treatment longer than 24 h, cells were changed to fresh medium containing TGF-β once every 24 h. (<i>A</i> and <i>B</i>) Cells were harvested and separated into nuclear and membrane fractions, and analyzed by immunoblot analysis with indicated antibodies. Immunoblot analysis with antibodies against calnexin and lysine-specific demethylase 1 (LSD1) served as loading controls for membrane and nuclear fractions, respectively. (<i>C</i>) Cell lysate was subjected to immunoblot analysis with indicated antibodies.</p>", "links"=>[], "tags"=>["genes encoding proteins", "rip", "CREB 3L", "CREB 3L CREB 3L", "Regulated Intramembrane Proteolysis", "fibrotic diseases", "collagen", "nh", "4SF", "tm", "tgf", "CREB 3L releases", "CREB 3L Cleavage"], "article_id"=>1202548, "categories"=>["Biological Sciences"], "users"=>["Qiuyue Chen", "Ching-En Lee", "Bray Denard", "Jin Ye"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108528.g001", "stats"=>{"downloads"=>2, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TGF_946_induces_RIP_of_CREB3L1_/1202548", "title"=>"TGF-β induces RIP of CREB3L1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-13 03:02:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/1715228", "https://ndownloader.figshare.com/files/1715229"], "description"=>"<div><p>CREB3L1 (cAMP response element binding protein 3-like 1), a transcription factor synthesized as a membrane-bound precursor and activated through Regulated Intramembrane Proteolysis (RIP), is essential for collagen production by osteoblasts during bone development. Here, we show that TGF-β (transforming growth factor-β), a cytokine known to stimulate production of collagen during wound healing and fibrotic diseases, induces proteolytic activation of CREB3L1 in human A549 cells. This activation results from inhibition of expression of TM4SF20 (transmembrane 4 L6 family member 20), which normally inhibits RIP of CREB3L1. Cleavage of CREB3L1 releases its NH<sub>2</sub>-terminal domain from membranes, allowing it to enter the nucleus where it binds to Smad4 to activate transcription of genes encoding proteins required for assembly of collagen-containing extracellular matrix. Our findings raise the possibility that inhibition of RIP of CREB3L1 could prevent excess deposition of collagen in certain fibrotic diseases.</p></div>", "links"=>[], "tags"=>["genes encoding proteins", "rip", "CREB 3L", "CREB 3L CREB 3L", "Regulated Intramembrane Proteolysis", "fibrotic diseases", "collagen", "nh", "4SF", "tm", "tgf", "CREB 3L releases", "CREB 3L Cleavage"], "article_id"=>1202567, "categories"=>["Biological Sciences"], "users"=>["Qiuyue Chen", "Ching-En Lee", "Bray Denard", "Jin Ye"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0108528.s001", "https://dx.doi.org/10.1371/journal.pone.0108528.s002"], "stats"=>{"downloads"=>8, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sustained_Induction_of_Collagen_Synthesis_by_TGF_946_Requires_Regulated_Intramembrane_Proteolysis_of_CREB3L1_/1202567", "title"=>"Sustained Induction of Collagen Synthesis by TGF-β Requires Regulated Intramembrane Proteolysis of CREB3L1", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-10-13 03:02:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/1715213"], "description"=>"<p>(A–F) On day 0, A549 cells were seeded at 1×10<sup>5</sup> cells per 60 mm dish. On day 1, the cells were transfected with indicted siRNAs. (A) On day 3, cells were harvested for quantification of CREB3L1 mRNA by real time-quantitative PCR (RT-QPCR). The amount of the mRNA in cells transfected with the control siRNA is set to 1. (B–F) On day 3, cells were treated with 0.5 ng/ml TGF-β for the indicated time as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108528#pone-0108528-g001\" target=\"_blank\">Fig. 1</a>. Cells were then harvested for quantification of indicated mRNA through RT-QPCR. The amount of the indicated mRNA in cells transfected with the control siRNA immediately before the TGF-β treatment is set to 1. (A–F) Results are reported as mean ± S.E.M. of three independent experiments.</p>", "links"=>[], "tags"=>["genes encoding proteins", "rip", "CREB 3L", "CREB 3L CREB 3L", "Regulated Intramembrane Proteolysis", "fibrotic diseases", "collagen", "nh", "4SF", "tm", "tgf", "CREB 3L releases", "CREB 3L Cleavage"], "article_id"=>1202552, "categories"=>["Biological Sciences"], "users"=>["Qiuyue Chen", "Ching-En Lee", "Bray Denard", "Jin Ye"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108528.g002", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sustained_induction_of_collagen_synthesis_by_TGF_946_requires_CREB3L1_/1202552", "title"=>"Sustained induction of collagen synthesis by TGF-β requires CREB3L1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-13 03:02:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/1715215"], "description"=>"<p>(<i>A</i>) Quantification of Smad4 mRNA through RT-QPCR following transfection of indicated siRNA was performed as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108528#pone-0108528-g002\" target=\"_blank\">Fig. 2<i>A</i></a>. (<i>B</i>) On day 0, A549 cells were seeded at 1×10<sup>5</sup> cells per 60 mm dish. On day 1, the cells were transfected with indicted siRNAs. On day 3, cells were treated with or without 1 ng/ml TGF-β. On day 4, 24 h after the treatment, cells were harvested and analyzed as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108528#pone-0108528-g001\" target=\"_blank\">Fig. 1<i>A</i></a>. (<i>C–D</i>) Quantification of the indicated mRNA following transfection with the indicated siRNA and treatment with TGF-β for the indicated time was performed as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108528#pone-0108528-g002\" target=\"_blank\">Fig. 2<i>C</i></a>. (<i>E</i>) On day 0, A549 cells were seeded at 4×10<sup>5</sup> cells per 60 mm dish. On day 1, cells were treated with or without 1 ng/ml TGF-β. On day 2, 24 h after the treatment, cells were harvested. Cell lysates were subjected to immunoprecipitation with the indicated antibodies. The immunoprecipitates (pellet) from 2 dishes of the cells and supernatant (sup) from 0.7 dishes of the cells were analyzed by immunoblot analysis with the indicated antibodies. (<i>F–H</i>) On day 0, Huh7 cells were seeded at 5×10<sup>4</sup> cells per 60 mm dish. On day 1, cells were transfected with indicted siRNAs. On day 3, cells were treated with or without 500 nM doxorubicin. (<i>F and H</i>) On day 4, 24 h after the treatment, cells were harvested for quantification of indicated mRNA by RT-QPCR. The amount of the mRNA in cells that were not treated with doxorubicin and transfected with the control siRNA is set to 1. (<i>G</i>) On day 4, 24 h after the treatment, cells were harvested and RIP of CREB3L1 was analyzed as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0108528#pone-0108528-g001\" target=\"_blank\">Fig. 1<i>A</i></a>. (<i>A, C, D, F and H</i>) Results are reported as mean ± S.E.M. of three independent experiments.</p>", "links"=>[], "tags"=>["genes encoding proteins", "rip", "CREB 3L", "CREB 3L CREB 3L", "Regulated Intramembrane Proteolysis", "fibrotic diseases", "collagen", "nh", "4SF", "tm", "tgf", "CREB 3L releases", "CREB 3L Cleavage"], "article_id"=>1202554, "categories"=>["Biological Sciences"], "users"=>["Qiuyue Chen", "Ching-En Lee", "Bray Denard", "Jin Ye"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0108528.g003", "stats"=>{"downloads"=>1, "page_views"=>39, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Smad4_is_a_co_factor_for_CREB3L1_to_induce_transcription_of_COL1A1_and_SPARC_/1202554", "title"=>"Smad4 is a co-factor for CREB3L1 to induce transcription of <i>COL1A1</i> and <i>SPARC</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-13 03:02:06"}

PMC Usage Stats | Further Information

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Relative Metric

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2019-04-06 02:38:26 UTC
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http://counter-101.soma.plos.org/api/v1.0/stats/doi/10.1371%2Fjournal.pone.0108528
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