Exploring the potential of selective FKBP51 inhibitors on melanoma: an investigation of their in vitro and in vivo effects

Abstract FKBP51 is a marker of melanocyte malignancy, correlating with vertical growth phase and lesion thickness. It promotes the typical features of epithelial to mesenchymal transition and sustains apoptosis resistance. The present study aimed to assess in vitro and in vivo the efficacy against m...

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Main Authors: Laura Marrone, Valeria Di Giacomo, Chiara Malasomma, Marialuisa Alessandra Vecchione, Felix Hausch, Massimiliano Cacace, Lucia D’Esposito, Martina Tufano, Paolo D’Arrigo, Maria Fiammetta Romano, Simona Romano
Format: Article
Language:English
Published: Nature Publishing Group 2025-04-01
Series:Cell Death Discovery
Online Access:https://doi.org/10.1038/s41420-025-02430-y
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author Laura Marrone
Valeria Di Giacomo
Chiara Malasomma
Marialuisa Alessandra Vecchione
Felix Hausch
Massimiliano Cacace
Lucia D’Esposito
Martina Tufano
Paolo D’Arrigo
Maria Fiammetta Romano
Simona Romano
author_facet Laura Marrone
Valeria Di Giacomo
Chiara Malasomma
Marialuisa Alessandra Vecchione
Felix Hausch
Massimiliano Cacace
Lucia D’Esposito
Martina Tufano
Paolo D’Arrigo
Maria Fiammetta Romano
Simona Romano
author_sort Laura Marrone
collection DOAJ
description Abstract FKBP51 is a marker of melanocyte malignancy, correlating with vertical growth phase and lesion thickness. It promotes the typical features of epithelial to mesenchymal transition and sustains apoptosis resistance. The present study aimed to assess in vitro and in vivo the efficacy against melanoma of selective small molecules targeting FKBP51, called SAFits. Our findings reveal differing outcomes for SAFits in vitro compared to in vivo. SAFit increased the doxorubicin and dacarbazine cytotoxicity of cultured melanoma cells and was effective in impairing NF-κB activity and related pro-survival genes. Moreover, SAFit affected TGF-β-signaling and reduced the capability of melanoma cells to migrate through transwell filters and invade the matrigel. Unexpectedly, SAFit was ineffective in reducing tumor growth in a syngeneic melanoma mouse model. A study of the tumor microenvironment revealed an enrichment of M2 macrophages in SAFit-treated mice. Western blot assay showed reduced levels of perforin in protein extracted from SAFit-treated tumor samples. Ex-vivo experiments showed that M1 and M2 macrophages exerted an opposite effect on the cytotoxic capacity of CD8 T cells, supporting the hypothesis that enrichment in M2 macrophages induced by SAFit could accelerate the exhaustion of CD8 lymphocytes. In conclusion, our study shows that selective FKBP51 targeting agents hinder the intrinsic pro-survival pathways of melanoma cells but simultaneously exacerbate immune suppression within the tumor microenvironment, and, therefore, they have not proven to be effective in vivo to counteract melanoma growth.
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spelling doaj-art-e52e675e575047f5b8003f255a8dd9352025-08-20T03:08:02ZengNature Publishing GroupCell Death Discovery2058-77162025-04-0111111010.1038/s41420-025-02430-yExploring the potential of selective FKBP51 inhibitors on melanoma: an investigation of their in vitro and in vivo effectsLaura Marrone0Valeria Di Giacomo1Chiara Malasomma2Marialuisa Alessandra Vecchione3Felix Hausch4Massimiliano Cacace5Lucia D’Esposito6Martina Tufano7Paolo D’Arrigo8Maria Fiammetta Romano9Simona Romano10Department of Molecular Medicine and Medical Biotechnologies, Federico II UniversityDepartment of Molecular Medicine and Medical Biotechnologies, Federico II UniversityDepartment of Molecular Medicine and Medical Biotechnologies, Federico II UniversityDepartment of Molecular Medicine and Medical Biotechnologies, Federico II UniversityTechnical University Darmstadt Institute of Organic Chemistry and BiochemistryCentro Servizi Veterinari, Federico II UniversityCentro Servizi Veterinari, Federico II UniversitySamuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical CenterDepartment of Molecular Medicine and Medical Biotechnologies, Federico II UniversityDepartment of Molecular Medicine and Medical Biotechnologies, Federico II UniversityDepartment of Molecular Medicine and Medical Biotechnologies, Federico II UniversityAbstract FKBP51 is a marker of melanocyte malignancy, correlating with vertical growth phase and lesion thickness. It promotes the typical features of epithelial to mesenchymal transition and sustains apoptosis resistance. The present study aimed to assess in vitro and in vivo the efficacy against melanoma of selective small molecules targeting FKBP51, called SAFits. Our findings reveal differing outcomes for SAFits in vitro compared to in vivo. SAFit increased the doxorubicin and dacarbazine cytotoxicity of cultured melanoma cells and was effective in impairing NF-κB activity and related pro-survival genes. Moreover, SAFit affected TGF-β-signaling and reduced the capability of melanoma cells to migrate through transwell filters and invade the matrigel. Unexpectedly, SAFit was ineffective in reducing tumor growth in a syngeneic melanoma mouse model. A study of the tumor microenvironment revealed an enrichment of M2 macrophages in SAFit-treated mice. Western blot assay showed reduced levels of perforin in protein extracted from SAFit-treated tumor samples. Ex-vivo experiments showed that M1 and M2 macrophages exerted an opposite effect on the cytotoxic capacity of CD8 T cells, supporting the hypothesis that enrichment in M2 macrophages induced by SAFit could accelerate the exhaustion of CD8 lymphocytes. In conclusion, our study shows that selective FKBP51 targeting agents hinder the intrinsic pro-survival pathways of melanoma cells but simultaneously exacerbate immune suppression within the tumor microenvironment, and, therefore, they have not proven to be effective in vivo to counteract melanoma growth.https://doi.org/10.1038/s41420-025-02430-y
spellingShingle Laura Marrone
Valeria Di Giacomo
Chiara Malasomma
Marialuisa Alessandra Vecchione
Felix Hausch
Massimiliano Cacace
Lucia D’Esposito
Martina Tufano
Paolo D’Arrigo
Maria Fiammetta Romano
Simona Romano
Exploring the potential of selective FKBP51 inhibitors on melanoma: an investigation of their in vitro and in vivo effects
Cell Death Discovery
title Exploring the potential of selective FKBP51 inhibitors on melanoma: an investigation of their in vitro and in vivo effects
title_full Exploring the potential of selective FKBP51 inhibitors on melanoma: an investigation of their in vitro and in vivo effects
title_fullStr Exploring the potential of selective FKBP51 inhibitors on melanoma: an investigation of their in vitro and in vivo effects
title_full_unstemmed Exploring the potential of selective FKBP51 inhibitors on melanoma: an investigation of their in vitro and in vivo effects
title_short Exploring the potential of selective FKBP51 inhibitors on melanoma: an investigation of their in vitro and in vivo effects
title_sort exploring the potential of selective fkbp51 inhibitors on melanoma an investigation of their in vitro and in vivo effects
url https://doi.org/10.1038/s41420-025-02430-y
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