Role of Smad Proteins in Resistance to BMP-Induced Growth Inhibition in B-Cell Lymphoma
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{"title"=>"Role of Smad Proteins in Resistance to BMP-Induced Growth Inhibition in B-Cell Lymphoma", "type"=>"journal", "authors"=>[{"first_name"=>"Kanutte", "last_name"=>"Huse", "scopus_author_id"=>"35082130700"}, {"first_name"=>"Maren", "last_name"=>"Bakkebø", "scopus_author_id"=>"36717401900"}, {"first_name"=>"Sébastien", "last_name"=>"Wälchli", "scopus_author_id"=>"6602556159"}, {"first_name"=>"Morten P.", "last_name"=>"Oksvold", "scopus_author_id"=>"6603395931"}, {"first_name"=>"Vera I.", "last_name"=>"Hilden", "scopus_author_id"=>"36717714900"}, {"first_name"=>"Lise", "last_name"=>"Forfang", "scopus_author_id"=>"22953649100"}, {"first_name"=>"May L.", "last_name"=>"Bredahl", "scopus_author_id"=>"6508353833"}, {"first_name"=>"Knut", "last_name"=>"Liestøl", "scopus_author_id"=>"7004166270"}, {"first_name"=>"Ash A.", "last_name"=>"Alizadeh", "scopus_author_id"=>"7006542787"}, {"first_name"=>"Erlend B.", "last_name"=>"Smeland", "scopus_author_id"=>"35397579900"}, {"first_name"=>"June H.", "last_name"=>"Myklebust", "scopus_author_id"=>"7006500316"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84867003141", "pmid"=>"23049692", "sgr"=>"84867003141", "doi"=>"10.1371/journal.pone.0046117", "issn"=>"19326203", "pui"=>"365767540"}, "id"=>"fbb30f5b-af8a-3365-b0aa-d1855d8c3ea1", "abstract"=>"Bone morphogenetic protein (BMP) expression and signaling are altered in a variety of cancers, but the functional impact of these alterations is uncertain. In this study we investigated the impact of expression of multiple BMPs and their signaling pathway components in human B-cell lymphoma. BMP messages, in particular BMP7, were detected in normal and malignant B cells. Addition of exogenous BMPs inhibited DNA synthesis in most lymphoma cell lines examined, but some cell lines were resistant. Tumor specimens from three out of five lymphoma patients were also resistant to BMPs, as determined by no activation of the BMP effectors Smad1/5/8. We have previously shown that BMP-7 potently induced apoptosis in normal B cells, which was in contrast to no or little inhibitory effect of this BMP in the lymphoma cells tested. BMP-resistance mechanisms were investigated by comparing sensitive and resistant cell lines. While BMP receptors are downregulated in many cancers, we documented similar receptor levels in resistant and sensitive lymphoma cells. We found a positive correlation between activation of Smad1/5/8 and inhibition of DNA synthesis. Gene expression analysis of two independent data sets showed that the levels of inhibitory Smads varied across different B-cell lymphoma. Furthermore, stable overexpression of Smad7 in two different BMP-sensitive cell lines with low endogenous levels of SMAD7, rendered them completely resistant to BMPs. This work highlights the role of Smads in determining the sensitivity to BMPs and shows that upregulation of Smad7 in cancer cells is sufficient to escape the negative effects of BMPs.", "link"=>"http://www.mendeley.com/research/role-smad-proteins-resistance-bmpinduced-growth-inhibition-bcell-lymphoma", "reader_count"=>10, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>4, "Student > Master"=>4, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>4, "Student > Master"=>4, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>6, "Medicine and Dentistry"=>2, "Sports and Recreations"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>6}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/566389"], "description"=>"<p>(A) BMP receptor expression in OCI-Ly3. (B-C) Relative receptor expression in lymphoma cell lines (B; means ± SEM, <i>n</i> = 3) and CD20<sup>+</sup>CD3<sup>−</sup>Igκ/Igλ<sup>+</sup> malignant B cells from lymphoma patient samples (C). Values represent median fluorescent intensity (MFI) of each BMP receptor relative to the MFI of the isotype control.</p>", "links"=>[], "tags"=>["-resistant", "lymphoma", "cells", "bmp"], "article_id"=>236871, "categories"=>["Cancer", "Molecular Biology", "Cell Biology", "Hematology"], "users"=>["Kanutte Huse", "Maren Bakkebø", "Sébastien Wälchli", "Morten P. Oksvold", "Vera I. Hilden", "Lise Forfang", "May L. Bredahl", "Knut Liestøl", "Ash A. Alizadeh", "Erlend B. Smeland", "June H. Myklebust"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046117.g003", "stats"=>{"downloads"=>3, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BMP_sensitive_and_resistant_lymphoma_cells_express_BMP_receptors_/236871", "title"=>"BMP-sensitive and -resistant lymphoma cells express BMP receptors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-01 01:54:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/567133"], "description"=>"a<p>nd = not determined.</p>", "links"=>[], "tags"=>["receptor", "cells", "infiltrating", "fl", "lymph", "node"], "article_id"=>237607, "categories"=>["Cancer", "Molecular Biology", "Cell Biology", "Hematology"], "users"=>["Kanutte Huse", "Maren Bakkebø", "Sébastien Wälchli", "Morten P. Oksvold", "Vera I. Hilden", "Lise Forfang", "May L. Bredahl", "Knut Liestøl", "Ash A. Alizadeh", "Erlend B. Smeland", "June H. Myklebust"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046117.t001", "stats"=>{"downloads"=>6, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BMP_receptor_expression_in_tumor_B_cells_and_in_normal_infiltrating_B_cells_from_FL_patient_lymph_node_specimens_/237607", "title"=>"BMP receptor expression in tumor B cells and in normal infiltrating B cells from FL patient lymph node specimens.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-10-01 02:06:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/566605"], "description"=>"<p>(A) Lymphoma cell lines were stimulated with BMPs for one hour and analyzed for the expression of pSmad1/5/8 by Western blotting. (B) BMP-induced phosphorylation of Smad1/5 and non-Smad pathways were determined by phospho-flow cytometry in lymphoma cell lines treated with or without BMPs for one hour. Shown is one representative of three independent experiments. (C) BMP-induced phosphorylation of Smad1/5/8 was quantified by densitometric analysis and normalized to the positive control, and mean OD-values (<i>n</i> = 3) are plotted against mean values for relative DNA synthesis for the corresponding BMP (from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0046117#pone-0046117-g002\" target=\"_blank\">Figure 2A</a>) for each cell line. The parallel lines are based on analysis of covariance; <i>p</i> = 0.015. (D) Tumor samples from five different lymphoma patients were treated with BMPs for one hour and analyzed for the expression of pSmad1/5/8. Anti-PGK1 was used as loading control and vertical lines indicate cutting of gel.</p>", "links"=>[], "tags"=>["phosphorylation", "resistant", "lymphoma"], "article_id"=>237090, "categories"=>["Cancer", "Molecular Biology", "Cell Biology", "Hematology"], "users"=>["Kanutte Huse", "Maren Bakkebø", "Sébastien Wälchli", "Morten P. Oksvold", "Vera I. Hilden", "Lise Forfang", "May L. Bredahl", "Knut Liestøl", "Ash A. Alizadeh", "Erlend B. Smeland", "June H. Myklebust"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046117.g004", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reduced_phosphorylation_of_Smad1_5_8_in_resistant_lymphoma_cells_/237090", "title"=>"Reduced phosphorylation of Smad1/5/8 in resistant lymphoma cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-01 01:58:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/566072"], "description"=>"<p><i>BMP</i> mRNA expression was determined by real-time RT-PCR, and the results are relative to the expression in human fetal brain tissue. (A) Centrocytes (CD19<sup>+</sup>CD38<sup>+</sup>IgD<sup>−</sup>CD77<sup>-</sup>) or centroblasts (CD19<sup>+</sup>CD38<sup>+</sup>IgD<sup>−</sup>CD77<sup>+</sup>) from normal human tonsils (relative expression ± SD of duplicates). (B) Lymphoma cell lines (means ± SEM, <i>n</i> = 3 for <i>BMP6</i>; <i>n</i> = 5 for <i>BMP7</i>). (C) Purified malignant B cells (CD20<sup>+</sup>CD10<sup>+</sup>Igκ/Igλ<sup>+</sup>) or tumor-infiltrating T cells (CD20<sup>−</sup>CD3<sup>+</sup>) from lymphoma patient samples (relative expression ± SD of duplicates). (D) Relative expression of <i>BMP6</i> and <i>BMP7</i> across non-Hodgkin’s lymphoma (NHL; left of line) and in normal B-cell populations (right of line) obtained from gene expression data set <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0046117#pone.0046117-Basso1\" target=\"_blank\">[16]</a>. (E-F) Protein expression of BMP-7 was determined by Western blot analysis. Protein bands correspond to propeptide (lower band) and uncleaved full-length monomer (upper band). HeLa_BMP-7: Lysate from HeLa cells transfected with BMP-7. β-tubulin was used as loading control. One representative experiment (E) and mean values (F) of BMP-7 levels are shown (means ± SEM, <i>n</i> = 3).</p>", "links"=>[], "tags"=>["malignant", "cells"], "article_id"=>236559, "categories"=>["Cancer", "Molecular Biology", "Cell Biology", "Hematology"], "users"=>["Kanutte Huse", "Maren Bakkebø", "Sébastien Wälchli", "Morten P. Oksvold", "Vera I. Hilden", "Lise Forfang", "May L. Bredahl", "Knut Liestøl", "Ash A. Alizadeh", "Erlend B. Smeland", "June H. Myklebust"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046117.g001", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Normal_and_malignant_B_cells_express_BMP6_and_BMP7_/236559", "title"=>"Normal and malignant B cells express <i>BMP6</i> and <i>BMP7</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-01 01:49:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/566820"], "description"=>"<p>(A) Real-time RT-PCR analysis of <i>SMAD6</i> and <i>SMAD7</i> expression in lymphoma cell lines, relative to their expression in the osteogenic sarcoma cell line Saos-2 (<i>SMAD6</i>; means ± SD, <i>n</i> = 2) or human fetal brain tissue (<i>SMAD7</i>; means ± SD, <i>n</i> = 5). (B) Relative expression of inhibitory <i>SMAD</i>s across NHLs (left of line) and in normal B-cell populations (right of line) obtained from a gene expression data set from Basso et al. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0046117#pone.0046117-Basso1\" target=\"_blank\">[16]</a>.</p>", "links"=>[], "tags"=>["inhibitory", "lymphoma"], "article_id"=>237309, "categories"=>["Cancer", "Molecular Biology", "Cell Biology", "Hematology"], "users"=>["Kanutte Huse", "Maren Bakkebø", "Sébastien Wälchli", "Morten P. Oksvold", "Vera I. Hilden", "Lise Forfang", "May L. Bredahl", "Knut Liestøl", "Ash A. Alizadeh", "Erlend B. Smeland", "June H. Myklebust"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046117.g006", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_inhibitory_SMAD_s_in_lymphoma_cells_/237309", "title"=>"Expression of inhibitory <i>SMAD</i>s in lymphoma cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-01 02:01:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/566999"], "description"=>"<p>(A–B) Smad1 and Smad5 expression was measured by Western blotting in cell lines. Anti-PGK1 was used as loading control. One representative experiment (A) and mean values of optical density from densitometric measurements (B; ± SEM, <i>n</i> = 3) are shown. (C) Relative expression of <i>SMAD1</i> and <i>SMAD5</i> across NHLs in data set from Basso et al. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0046117#pone.0046117-Basso1\" target=\"_blank\">[16]</a>.</p>", "links"=>[], "tags"=>["r-smads", "lymphoma"], "article_id"=>237486, "categories"=>["Cancer", "Molecular Biology", "Cell Biology", "Hematology"], "users"=>["Kanutte Huse", "Maren Bakkebø", "Sébastien Wälchli", "Morten P. Oksvold", "Vera I. Hilden", "Lise Forfang", "May L. Bredahl", "Knut Liestøl", "Ash A. Alizadeh", "Erlend B. Smeland", "June H. Myklebust"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046117.g007", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_R_Smads_in_lymphoma_cells_/237486", "title"=>"Expression of R-Smads in lymphoma cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-01 02:04:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/300597", "https://ndownloader.figshare.com/files/300639", "https://ndownloader.figshare.com/files/300686", "https://ndownloader.figshare.com/files/300735", "https://ndownloader.figshare.com/files/300765", "https://ndownloader.figshare.com/files/300772", "https://ndownloader.figshare.com/files/300782", "https://ndownloader.figshare.com/files/300799", "https://ndownloader.figshare.com/files/300837", "https://ndownloader.figshare.com/files/300850", "https://ndownloader.figshare.com/files/300913", "https://ndownloader.figshare.com/files/300979", "https://ndownloader.figshare.com/files/301043", "https://ndownloader.figshare.com/files/301110"], "description"=>"<div><p>Bone morphogenetic protein (BMP) expression and signaling are altered in a variety of cancers, but the functional impact of these alterations is uncertain. In this study we investigated the impact of expression of multiple BMPs and their signaling pathway components in human B-cell lymphoma. <em>BMP</em> messages, in particular <em>BMP7</em>, were detected in normal and malignant B cells. Addition of exogenous BMPs inhibited DNA synthesis in most lymphoma cell lines examined, but some cell lines were resistant. Tumor specimens from three out of five lymphoma patients were also resistant to BMPs, as determined by no activation of the BMP effectors Smad1/5/8. We have previously shown that BMP-7 potently induced apoptosis in normal B cells, which was in contrast to no or little inhibitory effect of this BMP in the lymphoma cells tested. BMP-resistance mechanisms were investigated by comparing sensitive and resistant cell lines. While BMP receptors are downregulated in many cancers, we documented similar receptor levels in resistant and sensitive lymphoma cells. We found a positive correlation between activation of Smad1/5/8 and inhibition of DNA synthesis. Gene expression analysis of two independent data sets showed that the levels of inhibitory Smads varied across different B-cell lymphoma. Furthermore, stable overexpression of Smad7 in two different BMP-sensitive cell lines with low endogenous levels of <em>SMAD7</em>, rendered them completely resistant to BMPs. This work highlights the role of Smads in determining the sensitivity to BMPs and shows that upregulation of Smad7 in cancer cells is sufficient to escape the negative effects of BMPs.</p> </div>", "links"=>[], "tags"=>["smad", "proteins", "bmp-induced", "inhibition", "B-cell", "lymphoma"], "article_id"=>119275, "categories"=>["Cancer", "Molecular Biology", "Cell Biology", "Hematology"], "users"=>["Kanutte Huse", "Maren Bakkebø", "Sébastien Wälchli", "Morten P. Oksvold", "Vera I. Hilden", "Lise Forfang", "May L. Bredahl", "Knut Liestøl", "Ash A. Alizadeh", "Erlend B. Smeland", "June H. Myklebust"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0046117.s001", "https://dx.doi.org/10.1371/journal.pone.0046117.s002", "https://dx.doi.org/10.1371/journal.pone.0046117.s003", "https://dx.doi.org/10.1371/journal.pone.0046117.s004", "https://dx.doi.org/10.1371/journal.pone.0046117.s005", "https://dx.doi.org/10.1371/journal.pone.0046117.s006", "https://dx.doi.org/10.1371/journal.pone.0046117.s007", "https://dx.doi.org/10.1371/journal.pone.0046117.s008", "https://dx.doi.org/10.1371/journal.pone.0046117.s009", "https://dx.doi.org/10.1371/journal.pone.0046117.s010", "https://dx.doi.org/10.1371/journal.pone.0046117.s011", "https://dx.doi.org/10.1371/journal.pone.0046117.s012", "https://dx.doi.org/10.1371/journal.pone.0046117.s013", "https://dx.doi.org/10.1371/journal.pone.0046117.s014"], "stats"=>{"downloads"=>13, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Role_of_Smad_Proteins_in_Resistance_to_BMP_Induced_Growth_Inhibition_in_B_Cell_Lymphoma/119275", "title"=>"Role of Smad Proteins in Resistance to BMP-Induced Growth Inhibition in B-Cell Lymphoma", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-10-01 02:34:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/566247"], "description"=>"<p>(A and C) Lymphoma cell lines were stimulated with various BMPs alone (A; <i>n</i> = 6, *<i>p</i><0.05) or in the presence of interleukins and CD40L (C; Sudhl-6 cells, <i>n</i> ≥2) for three days before measuring <sup>3</sup>H-thymidine incorporation. Results are normalized to unstimulated control in each experiment. (B) Tracking of cell division by CFSE labeling of Sudhl-6 cells cultured with or without BMP-2 or BMP-6 for three days. One representative of four independent experiments is shown.</p>", "links"=>[], "tags"=>["bmps", "proliferation", "B-cell", "lymphoma"], "article_id"=>236732, "categories"=>["Cancer", "Molecular Biology", "Cell Biology", "Hematology"], "users"=>["Kanutte Huse", "Maren Bakkebø", "Sébastien Wälchli", "Morten P. Oksvold", "Vera I. Hilden", "Lise Forfang", "May L. Bredahl", "Knut Liestøl", "Ash A. Alizadeh", "Erlend B. Smeland", "June H. Myklebust"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046117.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_BMPs_on_proliferation_of_B_cell_lymphoma_cell_lines_/236732", "title"=>"Effects of BMPs on proliferation of B-cell lymphoma cell lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-01 01:52:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/566730"], "description"=>"<p>Sudhl-6 and Raji cells were retrovirally transduced with GFP control vector or SMAD7_2A_GFP vector, and FACS sorted into GFP<sup>−</sup> or GFP<sup>+</sup> cells. Smad1, Smad5 and 2A-tagged Smad7 expression was measured by Western blotting, and anti-actin was used as loading control. (B) SMAD7_2A_GFP-transduced cells were treated with or without BMP-2 or BMP-4 for three days before <sup>3</sup>H-thymidine incorporation was measured. Results are normalized to the unstimulated control (mean ± SD of triplicate wells). The experiments have been reproduced. (C) BMP-induced signaling was measured by treating retroviral transduced cells with or without BMP-2 or BMP-4 for one hour, followed by detection of GFP, pSmad1/5 and Smad2 by phospho-flow cytometry. The experiments have been reproduced.</p>", "links"=>[], "tags"=>["smad7", "lymphoma", "cells", "renders", "resistant", "bmp-induced"], "article_id"=>237207, "categories"=>["Cancer", "Molecular Biology", "Cell Biology", "Hematology"], "users"=>["Kanutte Huse", "Maren Bakkebø", "Sébastien Wälchli", "Morten P. Oksvold", "Vera I. Hilden", "Lise Forfang", "May L. Bredahl", "Knut Liestøl", "Ash A. Alizadeh", "Erlend B. Smeland", "June H. Myklebust"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046117.g005", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overexpression_of_Smad7_in_sensitive_lymphoma_cells_renders_them_resistant_to_BMP_induced_growth_inhibition_/237207", "title"=>"Overexpression of Smad7 in sensitive lymphoma cells renders them resistant to BMP-induced growth inhibition.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-01 02:00:07"}

PMC Usage Stats | Further Information

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Relative Metric

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