Extracellular vesicle-associated IGF2BP3 tunes Ewing sarcoma cell migration and affects PI3K/Akt pathway in neighboring cells
Ewing sarcoma (EWS) is a challenging pediatric cancer characterized by vast intra-tumor heterogeneity. We evaluated the RNA-binding protein IGF2BP3, whose high expression correlates with a poor prognosis and an elevated tendency of metastases, as a possible soluble mediator of inter-cellular communi...
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| Veröffentlicht in: | Cancer gene therapy 2023-09, Vol.30 (9), p.1285-1295 |
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| creator | Mancarella, Caterina Giusti, Veronica Caldoni, Giulia Laginestra, Maria Antonella Parra, Alessandro Toracchio, Lisa Giordano, Giorgia Roncuzzi, Laura Piazzi, Manuela Blalock, William Columbaro, Marta De Feo, Alessandra Scotlandi, Katia |
| description | Ewing sarcoma (EWS) is a challenging pediatric cancer characterized by vast intra-tumor heterogeneity. We evaluated the RNA-binding protein IGF2BP3, whose high expression correlates with a poor prognosis and an elevated tendency of metastases, as a possible soluble mediator of inter-cellular communication in EWS. Our data demonstrate that (i) IGF2BP3 is detected in cell supernatants, and it is released inside extracellular vesicles (EVs); (ii) EVs from IGF2BP3-positive or IGF2BP3-negative EWS cells reciprocally affect cell migration but not the proliferation of EWS recipient cells; (iii) EVs derived from IGF2BP3-silenced cells have a distinct miRNA cargo profile and inhibit the PI3K/Akt pathway in recipient cells; (iv) the 11 common differentially expressed miRNAs associated with IGF2BP3-positive and IGF2BP3-negative EVs correctly group IGF2BP3-positive and IGF2BP3-negative clinical tissue specimens. Overall, our data suggest that IGF2BP3 can participate in the modulation of phenotypic heterogeneity. |
| doi_str_mv | 10.1038/s41417-023-00637-8 |
| format | Article |
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We evaluated the RNA-binding protein IGF2BP3, whose high expression correlates with a poor prognosis and an elevated tendency of metastases, as a possible soluble mediator of inter-cellular communication in EWS. Our data demonstrate that (i) IGF2BP3 is detected in cell supernatants, and it is released inside extracellular vesicles (EVs); (ii) EVs from IGF2BP3-positive or IGF2BP3-negative EWS cells reciprocally affect cell migration but not the proliferation of EWS recipient cells; (iii) EVs derived from IGF2BP3-silenced cells have a distinct miRNA cargo profile and inhibit the PI3K/Akt pathway in recipient cells; (iv) the 11 common differentially expressed miRNAs associated with IGF2BP3-positive and IGF2BP3-negative EVs correctly group IGF2BP3-positive and IGF2BP3-negative clinical tissue specimens. Overall, our data suggest that IGF2BP3 can participate in the modulation of phenotypic heterogeneity.</description><identifier>ISSN: 0929-1903</identifier><identifier>ISSN: 1476-5500</identifier><identifier>EISSN: 1476-5500</identifier><identifier>DOI: 10.1038/s41417-023-00637-8</identifier><identifier>PMID: 37353558</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>1-Phosphatidylinositol 3-kinase ; 13 ; 13/44 ; 13/95 ; 14/28 ; 14/34 ; 14/63 ; 38/61 ; 38/91 ; 631/67/1798 ; 692/699/67 ; 82/1 ; 82/80 ; AKT protein ; Biomedical and Life Sciences ; Biomedicine ; Cancer ; Cell adhesion & migration ; Cell growth ; Cell interactions ; Cell migration ; Cell proliferation ; CRISPR ; DNA methylation ; Epigenetics ; Ewing's sarcoma ; Ewings sarcoma ; Extracellular vesicles ; Gene Expression ; Gene Therapy ; Metastases ; Metastasis ; MicroRNAs ; miRNA ; Nanoparticles ; Patients ; Pediatrics ; Proteins ; RNA-binding protein ; Tumors</subject><ispartof>Cancer gene therapy, 2023-09, Vol.30 (9), p.1285-1295</ispartof><rights>The Author(s) 2023</rights><rights>2023. The Author(s).</rights><rights>The Author(s) 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). 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We evaluated the RNA-binding protein IGF2BP3, whose high expression correlates with a poor prognosis and an elevated tendency of metastases, as a possible soluble mediator of inter-cellular communication in EWS. Our data demonstrate that (i) IGF2BP3 is detected in cell supernatants, and it is released inside extracellular vesicles (EVs); (ii) EVs from IGF2BP3-positive or IGF2BP3-negative EWS cells reciprocally affect cell migration but not the proliferation of EWS recipient cells; (iii) EVs derived from IGF2BP3-silenced cells have a distinct miRNA cargo profile and inhibit the PI3K/Akt pathway in recipient cells; (iv) the 11 common differentially expressed miRNAs associated with IGF2BP3-positive and IGF2BP3-negative EVs correctly group IGF2BP3-positive and IGF2BP3-negative clinical tissue specimens. Overall, our data suggest that IGF2BP3 can participate in the modulation of phenotypic heterogeneity.</description><subject>1-Phosphatidylinositol 3-kinase</subject><subject>13</subject><subject>13/44</subject><subject>13/95</subject><subject>14/28</subject><subject>14/34</subject><subject>14/63</subject><subject>38/61</subject><subject>38/91</subject><subject>631/67/1798</subject><subject>692/699/67</subject><subject>82/1</subject><subject>82/80</subject><subject>AKT protein</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Cancer</subject><subject>Cell adhesion & migration</subject><subject>Cell growth</subject><subject>Cell interactions</subject><subject>Cell migration</subject><subject>Cell proliferation</subject><subject>CRISPR</subject><subject>DNA methylation</subject><subject>Epigenetics</subject><subject>Ewing's sarcoma</subject><subject>Ewings sarcoma</subject><subject>Extracellular vesicles</subject><subject>Gene 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Ther</addtitle><date>2023-09-01</date><risdate>2023</risdate><volume>30</volume><issue>9</issue><spage>1285</spage><epage>1295</epage><pages>1285-1295</pages><issn>0929-1903</issn><issn>1476-5500</issn><eissn>1476-5500</eissn><abstract>Ewing sarcoma (EWS) is a challenging pediatric cancer characterized by vast intra-tumor heterogeneity. We evaluated the RNA-binding protein IGF2BP3, whose high expression correlates with a poor prognosis and an elevated tendency of metastases, as a possible soluble mediator of inter-cellular communication in EWS. Our data demonstrate that (i) IGF2BP3 is detected in cell supernatants, and it is released inside extracellular vesicles (EVs); (ii) EVs from IGF2BP3-positive or IGF2BP3-negative EWS cells reciprocally affect cell migration but not the proliferation of EWS recipient cells; (iii) EVs derived from IGF2BP3-silenced cells have a distinct miRNA cargo profile and inhibit the PI3K/Akt pathway in recipient cells; (iv) the 11 common differentially expressed miRNAs associated with IGF2BP3-positive and IGF2BP3-negative EVs correctly group IGF2BP3-positive and IGF2BP3-negative clinical tissue specimens. 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| ispartof | Cancer gene therapy, 2023-09, Vol.30 (9), p.1285-1295 |
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| subjects | 1-Phosphatidylinositol 3-kinase 13 13/44 13/95 14/28 14/34 14/63 38/61 38/91 631/67/1798 692/699/67 82/1 82/80 AKT protein Biomedical and Life Sciences Biomedicine Cancer Cell adhesion & migration Cell growth Cell interactions Cell migration Cell proliferation CRISPR DNA methylation Epigenetics Ewing's sarcoma Ewings sarcoma Extracellular vesicles Gene Expression Gene Therapy Metastases Metastasis MicroRNAs miRNA Nanoparticles Patients Pediatrics Proteins RNA-binding protein Tumors |
| title | Extracellular vesicle-associated IGF2BP3 tunes Ewing sarcoma cell migration and affects PI3K/Akt pathway in neighboring cells |
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