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Basal cell adhesion molecule (BCAM) promotes mesothelial-to-mesenchymal transition and tumor angiogenesis through paracrine signaling.

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Title: Basal cell adhesion molecule (BCAM) promotes mesothelial-to-mesenchymal transition and tumor angiogenesis through paracrine signaling.
Authors: Sivakumar, Suresh, Lieber, Sonja, Dietze, Raimund, Beutgen, Vanessa M., Sutor, Eileen C., Heidemann, Sophie, Finkernagel, Florian, Teply-Szymanski, Julia, Nist, Andrea, Stiewe, Thorsten, Roth, Katrin, Reinartz, Silke, Graumann, Johannes, Müller-Brüsselbach, Sabine, Müller, Rolf
Source: Cell Communication & Signaling; 3/13/2025, Vol. 23 Issue 1, p1-21, 21p
Subject Terms: CELL adhesion molecules, MEDICAL sciences, CYTOLOGY, LIFE sciences, CANCER cell migration
Abstract: Background: High expression of basal cell adhesion molecule (BCAM) is a hallmark of ovarian cancer (OC) progression. BCAM facilitates transcoelomic dissemination by promoting mesothelial cell clearance at peritoneal attachment sites of tumor cell spheroids. We investigated how BCAM mediates this effect and potentially drives other pro-metastatic functions. Methods: The impact of BCAM on the tumor cell secretome and the mesothelial cell phenotype was analyzed by affinity proteomics, bulk and single-cell RNA sequencing, life-cell and multiphoton microscopy, biochemical and functional in vitro assays as well as a murine tumor model. BCAM manipulation involved ectopic overexpression, inducible expression and treatment with soluble BCAM. Results: All forms of BCAM enhanced the secretion of cytokines that impact cell motility, mesenchymal differentiation and angiogenesis, including AREG, CXCL family members, FGF2, TGFB2, and VEGF. Notably, their levels in OC ascites were correlated with BCAM expression, and recombinant BCAM-induced cytokines triggered mesothelial-mesenchymal transition (MMT). Mesothelial cells undergoing MMT exhibited enhanced motility away from attaching tumor spheroids, leading to mesothelial clearance at spheroid attachment sites. BCAM-mediated MMT-associated transcriptional changes were also observed in subpopulations of omental mesothelial cells from OC patients, and were associated with poor survival. Consistent with the secretome data, BCAM induced endothelial tube formation in vitro and markedly promoted tumor angiogenesis in a mouse model. Conclusion: We have identified previously unknown functions of the BCAM-induced secretome potentially impacting distinct stages of OC metastasis. While BCAM's impact on MMT may facilitate initiation of micrometastases, neo-angiogenesis is essential for tumor growth. Taken together with the observed clinical adverse association, our findings underscore the potential of BCAM as a therapeutic target. [ABSTRACT FROM AUTHOR]
Copyright of Cell Communication & Signaling is the property of BioMed Central and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.)
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  Data: Basal cell adhesion molecule (BCAM) promotes mesothelial-to-mesenchymal transition and tumor angiogenesis through paracrine signaling.
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  Data: <searchLink fieldCode="AR" term="%22Sivakumar%2C+Suresh%22">Sivakumar, Suresh</searchLink><br /><searchLink fieldCode="AR" term="%22Lieber%2C+Sonja%22">Lieber, Sonja</searchLink><br /><searchLink fieldCode="AR" term="%22Dietze%2C+Raimund%22">Dietze, Raimund</searchLink><br /><searchLink fieldCode="AR" term="%22Beutgen%2C+Vanessa+M%2E%22">Beutgen, Vanessa M.</searchLink><br /><searchLink fieldCode="AR" term="%22Sutor%2C+Eileen+C%2E%22">Sutor, Eileen C.</searchLink><br /><searchLink fieldCode="AR" term="%22Heidemann%2C+Sophie%22">Heidemann, Sophie</searchLink><br /><searchLink fieldCode="AR" term="%22Finkernagel%2C+Florian%22">Finkernagel, Florian</searchLink><br /><searchLink fieldCode="AR" term="%22Teply-Szymanski%2C+Julia%22">Teply-Szymanski, Julia</searchLink><br /><searchLink fieldCode="AR" term="%22Nist%2C+Andrea%22">Nist, Andrea</searchLink><br /><searchLink fieldCode="AR" term="%22Stiewe%2C+Thorsten%22">Stiewe, Thorsten</searchLink><br /><searchLink fieldCode="AR" term="%22Roth%2C+Katrin%22">Roth, Katrin</searchLink><br /><searchLink fieldCode="AR" term="%22Reinartz%2C+Silke%22">Reinartz, Silke</searchLink><br /><searchLink fieldCode="AR" term="%22Graumann%2C+Johannes%22">Graumann, Johannes</searchLink><br /><searchLink fieldCode="AR" term="%22Müller-Brüsselbach%2C+Sabine%22">Müller-Brüsselbach, Sabine</searchLink><br /><searchLink fieldCode="AR" term="%22Müller%2C+Rolf%22">Müller, Rolf</searchLink>
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  Data: Cell Communication & Signaling; 3/13/2025, Vol. 23 Issue 1, p1-21, 21p
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  Data: <searchLink fieldCode="DE" term="%22CELL+adhesion+molecules%22">CELL adhesion molecules</searchLink><br /><searchLink fieldCode="DE" term="%22MEDICAL+sciences%22">MEDICAL sciences</searchLink><br /><searchLink fieldCode="DE" term="%22CYTOLOGY%22">CYTOLOGY</searchLink><br /><searchLink fieldCode="DE" term="%22LIFE+sciences%22">LIFE sciences</searchLink><br /><searchLink fieldCode="DE" term="%22CANCER+cell+migration%22">CANCER cell migration</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Background: High expression of basal cell adhesion molecule (BCAM) is a hallmark of ovarian cancer (OC) progression. BCAM facilitates transcoelomic dissemination by promoting mesothelial cell clearance at peritoneal attachment sites of tumor cell spheroids. We investigated how BCAM mediates this effect and potentially drives other pro-metastatic functions. Methods: The impact of BCAM on the tumor cell secretome and the mesothelial cell phenotype was analyzed by affinity proteomics, bulk and single-cell RNA sequencing, life-cell and multiphoton microscopy, biochemical and functional in vitro assays as well as a murine tumor model. BCAM manipulation involved ectopic overexpression, inducible expression and treatment with soluble BCAM. Results: All forms of BCAM enhanced the secretion of cytokines that impact cell motility, mesenchymal differentiation and angiogenesis, including AREG, CXCL family members, FGF2, TGFB2, and VEGF. Notably, their levels in OC ascites were correlated with BCAM expression, and recombinant BCAM-induced cytokines triggered mesothelial-mesenchymal transition (MMT). Mesothelial cells undergoing MMT exhibited enhanced motility away from attaching tumor spheroids, leading to mesothelial clearance at spheroid attachment sites. BCAM-mediated MMT-associated transcriptional changes were also observed in subpopulations of omental mesothelial cells from OC patients, and were associated with poor survival. Consistent with the secretome data, BCAM induced endothelial tube formation in vitro and markedly promoted tumor angiogenesis in a mouse model. Conclusion: We have identified previously unknown functions of the BCAM-induced secretome potentially impacting distinct stages of OC metastasis. While BCAM's impact on MMT may facilitate initiation of micrometastases, neo-angiogenesis is essential for tumor growth. Taken together with the observed clinical adverse association, our findings underscore the potential of BCAM as a therapeutic target. [ABSTRACT FROM AUTHOR]
– Name: Abstract
  Label:
  Group: Ab
  Data: <i>Copyright of Cell Communication & Signaling is the property of BioMed Central and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract.</i> (Copyright applies to all Abstracts.)
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