Interleukin-1β mediates a tumor-supporting environment prompted by IGF1 in triple-negative breast cancer (TNBC)

Abstract Background The intricate mechanisms that associate obesity with triple-negative breast cancer (TNBC) remain to be disclosed. Considering that obesity is linked with an increased bioavailability of the insulin-like growth factor 1 (IGF1), we evaluated whether IGF1 triggers aggressive feature...

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Main Authors: Domenica Scordamaglia, Marianna Talia, Francesca Cirillo, Azzurra Zicarelli, Adelina Assunta Mondino, Salvatore De Rosis, Marika Di Dio, Francesca Silvestri, Chiara Meliti, Anna Maria Miglietta, Carlo Capalbo, Ernestina Marianna De Francesco, Antonino Belfiore, Marcello Maggiolini, Rosamaria Lappano
Format: Article
Language:English
Published: BMC 2025-06-01
Series:Journal of Translational Medicine
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Online Access:https://doi.org/10.1186/s12967-025-06730-w
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Summary:Abstract Background The intricate mechanisms that associate obesity with triple-negative breast cancer (TNBC) remain to be disclosed. Considering that obesity is linked with an increased bioavailability of the insulin-like growth factor 1 (IGF1), we evaluated whether IGF1 triggers aggressive features in TNBC cells and the molecular paths involved. Methods Gene expression and Chromatin Immunoprecipitation experiments, ELISA, immunoblotting, immunoprecipitation and immunofluorescence assays, combined with two-dimensional and three-dimensional in vitro model-based studies, were used to investigate the molecular mechanisms through which IGF1 may promote proliferative and motile responses in TNBC cells and reprogram normal fibroblasts into cancer-associated fibroblasts (CAFs)-like cells. The translational relevance of the results obtained was supported by bioinformatics analyses leveraging data from extensive TNBC patient databases. Results We found that the cytokine interleukin-1β (IL-1β) mediates certain IGF1 actions within the tumor microenvironment, hence facilitating the TNBC landscape. Mechanistically, we assessed that the IGF1/IGF1 receptor (IGFIR) axis induces the collagen VI-dependent activation of discoidin domain receptor 1 (DDR1) and the subsequent increase of the G protein estrogen receptor (GPER), toward IL-1β regulation and secretion. Consequently, IL-1β promoted both the autocrine stimulation of TNBC cells and the differentiation of normal fibroblasts into cancer-associated fibroblasts (CAFs)-like cells, which in turn achieved a proliferative profile and enhanced the motility of TNBC cells. Conclusions IL-1β may be considered as a therapeutic target in more comprehensive approaches in obese TNBC patients exhibiting high IGF-1 bioavailability.
ISSN:1479-5876