ELMO1 Is Upregulated in AML CD34+ Stem/Progenitor Cells, Mediates Chemotaxis and Predicts Poor Prognosis in Normal Karyotype AML
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{"title"=>"ELMO1 is upregulated in AML CD34+ stem/progenitor cells, mediates chemotaxis and predicts poor prognosis in normal karyotype AML", "type"=>"journal", "authors"=>[{"first_name"=>"Marta E.", "last_name"=>"Capala", "scopus_author_id"=>"56367858000"}, {"first_name"=>"Edo", "last_name"=>"Vellenga", "scopus_author_id"=>"7102102458"}, {"first_name"=>"Jan Jacob", "last_name"=>"Schuringa", "scopus_author_id"=>"6603540082"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"600407299", "pmid"=>"25360637", "doi"=>"10.1371/journal.pone.0111568", "scopus"=>"2-s2.0-84910002320", "sgr"=>"84910002320", "issn"=>"19326203"}, "id"=>"3fc7aa40-7010-3149-8102-ecd5c2fc1849", "abstract"=>"Both normal as well leukemic hematopoietic stem cells critically depend on their microenvironment in the bone marrow for processes such as self-renewal, survival and differentiation, although the exact pathways that are involved remain poorly understood. We performed transcriptome analysis on primitive CD34+ acute myeloid leukemia (AML) cells (n = 46), their more differentiated CD34- leukemic progeny, and normal CD34+ bone marrow cells (n = 31) and focused on differentially expressed genes involved in adhesion and migration. Thus, Engulfment and Motility protein 1 (ELMO1) was identified amongst the top 50 most differentially expressed genes. ELMO1 is a crucial link in the signaling cascade that leads to activation of RAC GTPases and cytoskeleton rearrangements. We confirmed increased ELMO1 expression at the mRNA and protein level in a panel of AML samples and showed that high ELMO1 expression is an independent negative prognostic factor in normal karyotype (NK) AML in three large independent patient cohorts. Downmodulation of ELMO1 in human CB CD34+ cells did not significantly alter expansion, progenitor frequency or differentiation in stromal co-cultures, but did result in a decreased frequency of stem cells in LTC-IC assays. In BCR-ABL-transduced human CB CD34+ cells depletion of ELMO1 resulted in a mild decrease in proliferation, but replating capacity of progenitors was severely impaired. Downregulation of ELMO1 in a panel of primary CD34+ AML cells also resulted in reduced long-term growth in stromal co-cultures in two out of three cases. Pharmacological inhibition of the ELMO1 downstream target RAC resulted in a severely impaired proliferation and survival of leukemic cells. Finally, ELMO1 depletion caused a marked decrease in SDF1-induced chemotaxis of leukemic cells. Taken together, these data show that inhibiting the ELMO1-RAC axis might be an alternative way to target leukemic cells.", "link"=>"http://www.mendeley.com/research/elmo1-upregulated-aml-cd34-stemprogenitor-cells-mediates-chemotaxis-predicts-poor-prognosis-normal-k", "reader_count"=>4, "reader_count_by_academic_status"=>{"Researcher"=>3, "Student > Postgraduate"=>1}, "reader_count_by_user_role"=>{"Researcher"=>3, "Student > Postgraduate"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>3}, "reader_count_by_subdiscipline"=>{"Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1774851", "https://ndownloader.figshare.com/files/1774852", "https://ndownloader.figshare.com/files/1774853", "https://ndownloader.figshare.com/files/1774854"], "description"=>"<div><p>Both normal as well leukemic hematopoietic stem cells critically depend on their microenvironment in the bone marrow for processes such as self-renewal, survival and differentiation, although the exact pathways that are involved remain poorly understood. We performed transcriptome analysis on primitive CD34<sup>+</sup> acute myeloid leukemia (AML) cells (n = 46), their more differentiated CD34<sup>−</sup> leukemic progeny, and normal CD34<sup>+</sup> bone marrow cells (n = 31) and focused on differentially expressed genes involved in adhesion and migration. Thus, Engulfment and Motility protein 1 (ELMO1) was identified amongst the top 50 most differentially expressed genes. ELMO1 is a crucial link in the signaling cascade that leads to activation of RAC GTPases and cytoskeleton rearrangements. We confirmed increased ELMO1 expression at the mRNA and protein level in a panel of AML samples and showed that high ELMO1 expression is an independent negative prognostic factor in normal karyotype (NK) AML in three large independent patient cohorts. Downmodulation of ELMO1 in human CB CD34<sup>+</sup> cells did not significantly alter expansion, progenitor frequency or differentiation in stromal co-cultures, but did result in a decreased frequency of stem cells in LTC-IC assays. In BCR-ABL-transduced human CB CD34<sup>+</sup> cells depletion of ELMO1 resulted in a mild decrease in proliferation, but replating capacity of progenitors was severely impaired. Downregulation of ELMO1 in a panel of primary CD34<sup>+</sup> AML cells also resulted in reduced long-term growth in stromal co-cultures in two out of three cases. Pharmacological inhibition of the ELMO1 downstream target RAC resulted in a severely impaired proliferation and survival of leukemic cells. Finally, ELMO1 depletion caused a marked decrease in SDF1-induced chemotaxis of leukemic cells. Taken together, these data show that inhibiting the ELMO1-RAC axis might be an alternative way to target leukemic cells.</p></div>", "links"=>[], "tags"=>["rac", "leukemic cells", "ELMO 1 depletion", "ELMO 1 expression", "Motility protein 1", "Normal Karyotype AML", "nk", "cb", "ELMO 1", "Predicts Poor Prognosis", "target leukemic cells", "sdf"], "article_id"=>1225293, "categories"=>["Biological Sciences"], "users"=>["Marta E. Capala", "Edo Vellenga", "Jan Jacob Schuringa"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0111568.s001", "https://dx.doi.org/10.1371/journal.pone.0111568.s002", "https://dx.doi.org/10.1371/journal.pone.0111568.s003", "https://dx.doi.org/10.1371/journal.pone.0111568.s004"], "stats"=>{"downloads"=>4, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ELMO1_Is_Upregulated_in_AML_CD34_Stem_Progenitor_Cells_Mediates_Chemotaxis_and_Predicts_Poor_Prognosis_in_Normal_Karyotype_AML_/1225293", "title"=>"ELMO1 Is Upregulated in AML CD34+ Stem/Progenitor Cells, Mediates Chemotaxis and Predicts Poor Prognosis in Normal Karyotype AML", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-10-31 03:45:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1774845"], "description"=>"<p>(A) CB CD34<sup>+</sup> cells were transduced with BCR-ABL-expressing vector, sorted and plated on MS5 stroma. Cells were allowed to proliferate for 5 days after which RAC inhibitor was added to the following concentrations: 20 µM, 40 µM or 100 µM. Co-cultures were demi-depopulated on indicated days for analysis. Cumulative cell count is shown representative of 3 independent experiments. (B) CD34<sup>+</sup> cells were sorted from BC CML patient sample and plated on MS5 stroma. Cells were allowed to proliferate for 5 days after which RAC inhibitor was added to the following concentrations: 20 µM, 40 µM or 100 µM. Co-cultures were demi-depopulated on indicated days for analysis. Cumulative cell count is shown representative of 3 independent experiments. (C) BCR-ABL transduced cells as described in (A) were treated with 50 µM NSC for 3 days after which suspension cells were harvested and stained with Annexin V to assess apoptosis. (D) TF-1 and THP-1 cells were transduced with control scrambled shRNA vector (shSCR) or with ELMO1-targeting shRNA vector (shELMO1) and migration was evaluated in a transwell assay. The percentage of migrating cells relative to control is shown as an average of 3 independent experiments.</p>", "links"=>[], "tags"=>["rac", "leukemic cells", "ELMO 1 depletion", "ELMO 1 expression", "Motility protein 1", "Normal Karyotype AML", "nk", "cb", "ELMO 1", "Predicts Poor Prognosis", "target leukemic cells", "sdf"], "article_id"=>1225287, "categories"=>["Biological Sciences"], "users"=>["Marta E. Capala", "Edo Vellenga", "Jan Jacob Schuringa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111568.g005", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Global_inhibition_of_RAC_activity_severely_impairs_proliferation_and_survival_of_leukemic_cells_while_ELMO1_depletion_strongly_affects_migration_/1225287", "title"=>"Global inhibition of RAC activity severely impairs proliferation and survival of leukemic cells while ELMO1 depletion strongly affects migration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-31 03:45:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1774846"], "description"=>"<p>Abbreviations: <i>FLT3</i>, fms-related tyrosine kinase 3; ITD, internal tandem duplication; NK, normal karyotype; <i>NPM1</i>, nucleophosmin 1; NPMc<sup>+</sup>, cytoplasmic dislocalization of NPM1; wt, wild type.</p><p>Summary of clinical parameters of AML patients used in this study.</p>", "links"=>[], "tags"=>["rac", "leukemic cells", "ELMO 1 depletion", "ELMO 1 expression", "Motility protein 1", "Normal Karyotype AML", "nk", "cb", "ELMO 1", "Predicts Poor Prognosis", "target leukemic cells", "sdf"], "article_id"=>1225288, "categories"=>["Biological Sciences"], "users"=>["Marta E. Capala", "Edo Vellenga", "Jan Jacob Schuringa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111568.t001", "stats"=>{"downloads"=>2, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_clinical_parameters_of_AML_patients_used_in_this_study_/1225288", "title"=>"Summary of clinical parameters of AML patients used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-10-31 03:45:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1774841"], "description"=>"<p>(A) CB CD34<sup>+</sup> stem/progenitor cells were double-transduced with BCR-ABL and either control scrambled shRNA vector (shSCR) or with ELMO1-targeting shRNA vector (shELMO1). FACS plots of transduction efficiency are shown. (B) 3×10<sup>5</sup> double-transduced cells per group were plated in liquid culture and followed for 35 day. Cumulative cell count is shown representative of 3 independent experiments. (C) 5×10<sup>3</sup> double-transduced cells were sorted per group and plated on MS5 stromal cells; cultures were demi-depopulated on indicated days for analysis and replated when stroma showed signs of detaching. Cumulative cell growth is shown for a representative experiment of 3 independent experiments and the average of those 3 experiments is shown in (D). (E) Suspension cells from MS5 co-cultures as described in panel B were analyzed for progenitor frequency by CFC assay. 10<sup>3</sup> freshly transduced cells or 10<sup>4</sup> cells from each co-culture were plated in a CFC assay in methylcellulose in duplicate, and colonies were evaluated 2 weeks after plating. CFC cells were harvested and 10<sup>5</sup> cells were replated to assess secondary CFC formation. Total CFC numbers are shown from a representative of 3 independent experiments; error bars indicate standard deviation. * <i>P</i><0.05, ** <i>P</i><0.01, *** <i>P</i><0.001.</p>", "links"=>[], "tags"=>["rac", "leukemic cells", "ELMO 1 depletion", "ELMO 1 expression", "Motility protein 1", "Normal Karyotype AML", "nk", "cb", "ELMO 1", "Predicts Poor Prognosis", "target leukemic cells", "sdf"], "article_id"=>1225283, "categories"=>["Biological Sciences"], "users"=>["Marta E. Capala", "Edo Vellenga", "Jan Jacob Schuringa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111568.g003", "stats"=>{"downloads"=>3, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BCR_ABL_transformed_human_CB_CD34_show_proliferative_disadvantage_and_markedly_reduced_replating_capacity_upon_ELMO1_depletion_/1225283", "title"=>"BCR-ABL-transformed human CB CD34<sup>+</sup> show proliferative disadvantage and markedly reduced replating capacity upon ELMO1 depletion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-31 03:45:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1774840"], "description"=>"<p>(A) K562 cells were transduced with control scrambled shRNA vector (shSCR) or with ELMO1-targeting shRNA vectors (shELMO1), sorted and used for RNA extraction. Quantitative PCR was performed to measure ELMO1 expression in transduced cells. ELMO1 mRNA levels were normalized against RPL27 mRNA expression. Alternatively, cells were used for Western blot analysis to determine ELMO1 protein levels. (B) FACS plots showing transduction efficiencies of cord blood (CB) CD34<sup>+</sup> stem/progenitor cells transduced with shSCR or shELMO1. (C) 3×10<sup>5</sup> transduced and sorted cells per group were plated in liquid culture and followed for thirty days. Cumulative cell count is showed representative of 3 independent experiments. (D) 10<sup>5</sup> transduced and sorted cells per group were plated on MS5 stromal cells and kept in the co-culture for 5 weeks; cultures were demi-depopulated weekly for analysis. Weekly cumulative cell growth is shown for a representative experiment of 3 independent experiments and the average of those 3 experiments is shown in (E). (F) Suspension cells from MS5 co-cultures as described in panel D were analyzed for progenitor frequency by CFC assay. 10<sup>4</sup> cells from each co-culture were plated in a CFC assay in methylcellulose in duplicate, and colonies were evaluated 2 weeks after plating. CFC cells were then harvested and 10<sup>5</sup> cells were re-plated to form secondary CFCs. CFU-GM and BFU-E numbers are shown from a representative of 3 independent experiments; error bars indicate standard deviation. (G) LTC-IC frequencies were determined in bulk on MS5 stromal cells. After 5 weeks of co-culture methylcellulose was added to and colonies were scored two weeks later. CFU -GM, colony-forming unit-granulocyte-macrophage; BFU-E, burst forming unit-erythroid. * <i>P</i><0.05, ** <i>P</i><0.01, *** <i>P</i><0.001.</p>", "links"=>[], "tags"=>["rac", "leukemic cells", "ELMO 1 depletion", "ELMO 1 expression", "Motility protein 1", "Normal Karyotype AML", "nk", "cb", "ELMO 1", "Predicts Poor Prognosis", "target leukemic cells", "sdf"], "article_id"=>1225282, "categories"=>["Biological Sciences"], "users"=>["Marta E. Capala", "Edo Vellenga", "Jan Jacob Schuringa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111568.g002", "stats"=>{"downloads"=>2, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ELMO1_downmodulation_in_human_CB_CD34_cells_does_not_alter_growth_colony_formation_or_differentiation_but_significantly_decreases_stem_cell_frequency_/1225282", "title"=>"ELMO1 downmodulation in human CB CD34+ cells does not alter growth, colony formation or differentiation, but significantly decreases stem cell frequency.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-31 03:45:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1774843"], "description"=>"<p>AML CD34<sup>+</sup> cells were transduced with control scrambled shRNA vector (shSCR) or with ELMO1-targeting shRNA vector (shELMO1). After washing away the virus all the cells were plated on MS5 stroma; cultures were demi-depopulated on indicated days for analysis. Cumulative cell growth is shown for each AML sample studied.</p>", "links"=>[], "tags"=>["rac", "leukemic cells", "ELMO 1 depletion", "ELMO 1 expression", "Motility protein 1", "Normal Karyotype AML", "nk", "cb", "ELMO 1", "Predicts Poor Prognosis", "target leukemic cells", "sdf"], "article_id"=>1225285, "categories"=>["Biological Sciences"], "users"=>["Marta E. Capala", "Edo Vellenga", "Jan Jacob Schuringa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111568.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ELMO1_depletion_in_primary_AML_CD34_cells_impairs_long_term_expansion_on_stroma_/1225285", "title"=>"ELMO1 depletion in primary AML CD34<sup>+</sup> cells impairs long-term expansion on stroma.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-31 03:45:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/1774837"], "description"=>"<p>(A) VENN diagram displaying the overlap in AML CD34<sup>+</sup> specific and AML CD34− specific transcriptomes compared to NBM CD34<sup>+</sup> cells <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0111568#pone.0111568-Bonardi1\" target=\"_blank\">[17]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0111568#pone.0111568-deJonge1\" target=\"_blank\">[18]</a>. (B) 1677 AML CD34<sup>+</sup>-specific genes were subjected to Gene Ontology (GO) analysis for Cellular Component (CC) of which several CCs are shown. (C) 1677 AML CD34<sup>+</sup>-specific genes were subjected to GO analysis for terms associated with adhesion and migration. (D) ELMO1 mRNA was significantly higher expressed in AML CD34<sup>+</sup> (n = 46) as compared to AML CD34<sup>−</sup> cells (<i>p</i><0.0001), as well as to NBM CD34<sup>+</sup> cells (n = 31) (<i>p</i><0.0001). (E) Increased expression of ELMO1 was further confirmed by independent Q-PCRs in a panel of 11 AML and 6 NBM samples. (F, G) The increase in ELMO1 mRNA was paralleled by increased protein levels in two representative cases. (H) High expression of ELMO1 predicts poor survival in a cohort of NK AML patients (based on <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0111568#pone.0111568-Valk1\" target=\"_blank\">[6]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0111568#pone.0111568-deJonge2\" target=\"_blank\">[29]</a>) (p = 0.0034).</p>", "links"=>[], "tags"=>["rac", "leukemic cells", "ELMO 1 depletion", "ELMO 1 expression", "Motility protein 1", "Normal Karyotype AML", "nk", "cb", "ELMO 1", "Predicts Poor Prognosis", "target leukemic cells", "sdf"], "article_id"=>1225279, "categories"=>["Biological Sciences"], "users"=>["Marta E. Capala", "Edo Vellenga", "Jan Jacob Schuringa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0111568.g001", "stats"=>{"downloads"=>3, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ELMO1_expression_is_increased_in_AML_CD34_cells_and_predicts_poor_prognosis_in_normal_karyotype_AML_patients_/1225279", "title"=>"ELMO1 expression is increased in AML CD34<sup>+</sup> cells and predicts poor prognosis in normal karyotype AML patients.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-10-31 03:45:25"}

PMC Usage Stats | Further Information

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Relative Metric

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