Evaluation of Antitumoral Activity in a 3D Cell Model of a Src Inhibitor Prodrug for Glioblastoma Treatment

<b>Background</b>: Three-dimensional (3D) cell models may bridge the gap between two-dimensional (2D) cell cultures and animal models. Technical advances have led to the development of 3D-bioprinted cell models, characterized by greater reproducibility and the ability to mimic in vivo co...

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Main Authors: Letizia Clementi, Federica Poggialini, Francesca Musumeci, Julia Taglienti, Emanuele Cornacchia, Chiara Vagaggini, Anna Carbone, Giancarlo Grossi, Elena Dreassi, Adriano Angelucci, Silvia Schenone
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Language:English
Published: MDPI AG 2025-05-01
Series:Pharmaceutics
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Online Access:https://www.mdpi.com/1999-4923/17/6/704
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author Letizia Clementi
Federica Poggialini
Francesca Musumeci
Julia Taglienti
Emanuele Cornacchia
Chiara Vagaggini
Anna Carbone
Giancarlo Grossi
Elena Dreassi
Adriano Angelucci
Silvia Schenone
author_facet Letizia Clementi
Federica Poggialini
Francesca Musumeci
Julia Taglienti
Emanuele Cornacchia
Chiara Vagaggini
Anna Carbone
Giancarlo Grossi
Elena Dreassi
Adriano Angelucci
Silvia Schenone
author_sort Letizia Clementi
collection DOAJ
description <b>Background</b>: Three-dimensional (3D) cell models may bridge the gap between two-dimensional (2D) cell cultures and animal models. Technical advances have led to the development of 3D-bioprinted cell models, characterized by greater reproducibility and the ability to mimic in vivo conditions. Glioblastoma multiforme (GBM) is a highly aggressive brain tumor with poor clinical outcomes due to its heterogeneity, angiogenic activity, and invasiveness. Src family kinases (SFKs) play a crucial role in GBM progression, making them attractive targets for drug development. Here, we show results about the pharmacological profile of a new prodrug synthesized from a Src inhibitor, <b>SI306</b>. <b>Methods</b>: Three-dimensional-bioprinted GBM cell models were used in predicting the antitumor activity of the prodrug <b>SI306-PD2</b> with respect to its precursor, <b>SI306</b>. <b>Results</b>: Since the prodrug releases the active inhibitor through the cleavage by specific enzymes, <b>SI306-PD2</b> was analyzed for stability and release kinetics in various media, including fetal bovine serum (FBS), which is normally used in cell culture. In comparison to <b>SI306</b>, <b>SI306-PD2</b> demonstrated higher solubility in water, higher permeability across gastrointestinal and blood–brain barrier membranes, and the ability to release the drug in the presence of FBS progressively. In the 2D GBM cell model, using U87 and U251 cell lines, both compounds similarly reduced tumor cell viability. In 3D-bioprinted cell models, in the presence of an FBS-free medium, <b>SI306-PD2</b> exhibited a more effective antitumor activity compared to <b>SI306</b>, reducing the proliferation and diameter of U251 spheroids grown within the bioprinted scaffold in a statistically significant manner. The analysis of proteins extracted from 3D scaffolds confirmed that <b>SI306-PD2</b> inhibited Src activation more efficiently than <b>SI306</b>. <b>Conclusions</b>: Our study suggests that, when tissue permeability represents a discriminating characteristic, bioprinted cell models can provide a valid alternative for studying the cytotoxicity of new antitumor compounds. This approach has permitted us to ascertain the potential of the prodrug <b>SI306-PD2</b> as a therapeutic agent for GBM, demonstrating better tissue penetration and antiproliferative efficacy compared to the precursor compound <b>SI306</b>.
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spelling doaj-art-4e5ad6b19e3947f89c2153b4d547ddfa2025-08-20T02:21:53ZengMDPI AGPharmaceutics1999-49232025-05-0117670410.3390/pharmaceutics17060704Evaluation of Antitumoral Activity in a 3D Cell Model of a Src Inhibitor Prodrug for Glioblastoma TreatmentLetizia Clementi0Federica Poggialini1Francesca Musumeci2Julia Taglienti3Emanuele Cornacchia4Chiara Vagaggini5Anna Carbone6Giancarlo Grossi7Elena Dreassi8Adriano Angelucci9Silvia Schenone10Department of Biotechnological and Applied Clinical Sciences, University of L’Aquila, Via Vetoio, 67100 L’Aquila, ItalyDepartment of Biotechnology, Chemistry and Pharmacy, University of Siena, Via Aldo Moro, 2, 53100 Siena, ItalyDepartment of Pharmacy, University of Genoa, Viale Benedetto XV, 3, 16132 Genoa, ItalyDepartment of Biotechnological and Applied Clinical Sciences, University of L’Aquila, Via Vetoio, 67100 L’Aquila, ItalyDepartment of Biotechnological and Applied Clinical Sciences, University of L’Aquila, Via Vetoio, 67100 L’Aquila, ItalyDepartment of Biotechnology, Chemistry and Pharmacy, University of Siena, Via Aldo Moro, 2, 53100 Siena, ItalyDepartment of Pharmacy, University of Genoa, Viale Benedetto XV, 3, 16132 Genoa, ItalyDepartment of Pharmacy, University of Genoa, Viale Benedetto XV, 3, 16132 Genoa, ItalyDepartment of Biotechnology, Chemistry and Pharmacy, University of Siena, Via Aldo Moro, 2, 53100 Siena, ItalyDepartment of Biotechnological and Applied Clinical Sciences, University of L’Aquila, Via Vetoio, 67100 L’Aquila, ItalyDepartment of Pharmacy, University of Genoa, Viale Benedetto XV, 3, 16132 Genoa, Italy<b>Background</b>: Three-dimensional (3D) cell models may bridge the gap between two-dimensional (2D) cell cultures and animal models. Technical advances have led to the development of 3D-bioprinted cell models, characterized by greater reproducibility and the ability to mimic in vivo conditions. Glioblastoma multiforme (GBM) is a highly aggressive brain tumor with poor clinical outcomes due to its heterogeneity, angiogenic activity, and invasiveness. Src family kinases (SFKs) play a crucial role in GBM progression, making them attractive targets for drug development. Here, we show results about the pharmacological profile of a new prodrug synthesized from a Src inhibitor, <b>SI306</b>. <b>Methods</b>: Three-dimensional-bioprinted GBM cell models were used in predicting the antitumor activity of the prodrug <b>SI306-PD2</b> with respect to its precursor, <b>SI306</b>. <b>Results</b>: Since the prodrug releases the active inhibitor through the cleavage by specific enzymes, <b>SI306-PD2</b> was analyzed for stability and release kinetics in various media, including fetal bovine serum (FBS), which is normally used in cell culture. In comparison to <b>SI306</b>, <b>SI306-PD2</b> demonstrated higher solubility in water, higher permeability across gastrointestinal and blood–brain barrier membranes, and the ability to release the drug in the presence of FBS progressively. In the 2D GBM cell model, using U87 and U251 cell lines, both compounds similarly reduced tumor cell viability. In 3D-bioprinted cell models, in the presence of an FBS-free medium, <b>SI306-PD2</b> exhibited a more effective antitumor activity compared to <b>SI306</b>, reducing the proliferation and diameter of U251 spheroids grown within the bioprinted scaffold in a statistically significant manner. The analysis of proteins extracted from 3D scaffolds confirmed that <b>SI306-PD2</b> inhibited Src activation more efficiently than <b>SI306</b>. <b>Conclusions</b>: Our study suggests that, when tissue permeability represents a discriminating characteristic, bioprinted cell models can provide a valid alternative for studying the cytotoxicity of new antitumor compounds. This approach has permitted us to ascertain the potential of the prodrug <b>SI306-PD2</b> as a therapeutic agent for GBM, demonstrating better tissue penetration and antiproliferative efficacy compared to the precursor compound <b>SI306</b>.https://www.mdpi.com/1999-4923/17/6/704bioprinttargeted therapytyrosine kinasepyrazolo[3,4-<i>d</i>]pyrimidinesanticancer therapy
spellingShingle Letizia Clementi
Federica Poggialini
Francesca Musumeci
Julia Taglienti
Emanuele Cornacchia
Chiara Vagaggini
Anna Carbone
Giancarlo Grossi
Elena Dreassi
Adriano Angelucci
Silvia Schenone
Evaluation of Antitumoral Activity in a 3D Cell Model of a Src Inhibitor Prodrug for Glioblastoma Treatment
Pharmaceutics
bioprint
targeted therapy
tyrosine kinase
pyrazolo[3,4-<i>d</i>]pyrimidines
anticancer therapy
title Evaluation of Antitumoral Activity in a 3D Cell Model of a Src Inhibitor Prodrug for Glioblastoma Treatment
title_full Evaluation of Antitumoral Activity in a 3D Cell Model of a Src Inhibitor Prodrug for Glioblastoma Treatment
title_fullStr Evaluation of Antitumoral Activity in a 3D Cell Model of a Src Inhibitor Prodrug for Glioblastoma Treatment
title_full_unstemmed Evaluation of Antitumoral Activity in a 3D Cell Model of a Src Inhibitor Prodrug for Glioblastoma Treatment
title_short Evaluation of Antitumoral Activity in a 3D Cell Model of a Src Inhibitor Prodrug for Glioblastoma Treatment
title_sort evaluation of antitumoral activity in a 3d cell model of a src inhibitor prodrug for glioblastoma treatment
topic bioprint
targeted therapy
tyrosine kinase
pyrazolo[3,4-<i>d</i>]pyrimidines
anticancer therapy
url https://www.mdpi.com/1999-4923/17/6/704
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