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ErbB2 Targeted Epigenetic Modulation: Anti-tumor Efficacy of the ADC Trastuzumab-HDACi ST8176AA1

Targeted therapy using monoclonal antibodies conjugated to toxins is gaining space in the treatment of cancer. Here, we report the anti-tumor effect of a new antibody drug conjugate (ADC) delivering a HDAC inhibitor to ErbB2+ solid tumors. Trastuzumab was partially reduced with tris [2-carboxyethyl]...

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Autores principales: Milazzo, Ferdinando Maria, Vesci, Loredana, Anastasi, Anna Maria, Chiapparino, Caterina, Rosi, Antonio, Giannini, Giuseppe, Taddei, Maurizio, Cini, Elena, Faltoni, Valentina, Petricci, Elena, Battistuzzi, Gianfranco, Salvini, Laura, Carollo, Valeria, De Santis, Rita
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6989603/
https://www.ncbi.nlm.nih.gov/pubmed/32039017
http://dx.doi.org/10.3389/fonc.2019.01534
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author Milazzo, Ferdinando Maria
Vesci, Loredana
Anastasi, Anna Maria
Chiapparino, Caterina
Rosi, Antonio
Giannini, Giuseppe
Taddei, Maurizio
Cini, Elena
Faltoni, Valentina
Petricci, Elena
Battistuzzi, Gianfranco
Salvini, Laura
Carollo, Valeria
De Santis, Rita
author_facet Milazzo, Ferdinando Maria
Vesci, Loredana
Anastasi, Anna Maria
Chiapparino, Caterina
Rosi, Antonio
Giannini, Giuseppe
Taddei, Maurizio
Cini, Elena
Faltoni, Valentina
Petricci, Elena
Battistuzzi, Gianfranco
Salvini, Laura
Carollo, Valeria
De Santis, Rita
author_sort Milazzo, Ferdinando Maria
collection PubMed
description Targeted therapy using monoclonal antibodies conjugated to toxins is gaining space in the treatment of cancer. Here, we report the anti-tumor effect of a new antibody drug conjugate (ADC) delivering a HDAC inhibitor to ErbB2+ solid tumors. Trastuzumab was partially reduced with tris [2-carboxyethyl] phosphine (TCEP) and conjugated to ST7464AA1, the active form of the prodrug HDAC inhibitor ST7612AA1, through a maleimide-thiol linker to obtain the Antibody Drug Conjugate (ADC) ST8176AA1. The average drug/antibody ratio (DAR) was 4.5 as measured by hydrophobic interaction chromatography (HIC). Binding of ST8176AA1 to ErbB2 receptor and internalization in tumor cells were investigated by enzyme-linked immunosorbent assay (ELISA), surface plasmon resonance (SPR), cytofluorimetry, and High Content Screening (HCS) Imaging. The biological activity of the ADC was evaluated in vitro and in vivo by measuring cell proliferation/cell cycle, apoptosis/DNA damage, tubulin, and histone acetylation and modulation of Epithelial/Mesenchymal Transition (EMT) markers. Receptor binding and internalization of ST8176AA1 were confirmed to be similar to trastuzumab. Higher anti-tumor activity of ST8176AA1 compared to trastuzumab was observed in vitro in tumor cell lines. Such higher activity correlated with increased acetylation of histones and alfa-tubulin as a consequence of HDAC inhibitor-mediated epigenetic modulation that also induced increased expression of ErbB2 and estrogen receptor in triple negative breast cancer cells. Consistently with in vitro data, ST8176AA1 exhibited higher tumor growth inhibition than trastuzumab in xenograft models of ovary and colon carcinoma and in two patient-derived xenograft (PDX) models of pancreatic carcinoma. Immunohistochemistry analysis of tumor masses showed lower expression of the proliferation marker Ki67 and higher expression of cleaved caspase-3 in mice treated with the ADC compared to those treated with trastuzumab and results correlated with increased acetylation of both histones and tubulin. Collectively, present data indicate that ADC ST8176AA1 can target epigenetic modulation to ErbB2+ tumors. Interestingly, the amount of HDACi estimated to be delivered at the ST8176AA1 effective dose would correspond to ~1/1,000 of ST7612AA1 effective dose. Therefore, ST8176AA1 is an attractive new therapeutic candidate because it exhibits increased anti-tumor potency compared to trastuzumab by exerting epigenetic modulation at a much safer dose compared to standard HDACi-based therapeutic protocols.
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spelling pubmed-69896032020-02-07 ErbB2 Targeted Epigenetic Modulation: Anti-tumor Efficacy of the ADC Trastuzumab-HDACi ST8176AA1 Milazzo, Ferdinando Maria Vesci, Loredana Anastasi, Anna Maria Chiapparino, Caterina Rosi, Antonio Giannini, Giuseppe Taddei, Maurizio Cini, Elena Faltoni, Valentina Petricci, Elena Battistuzzi, Gianfranco Salvini, Laura Carollo, Valeria De Santis, Rita Front Oncol Oncology Targeted therapy using monoclonal antibodies conjugated to toxins is gaining space in the treatment of cancer. Here, we report the anti-tumor effect of a new antibody drug conjugate (ADC) delivering a HDAC inhibitor to ErbB2+ solid tumors. Trastuzumab was partially reduced with tris [2-carboxyethyl] phosphine (TCEP) and conjugated to ST7464AA1, the active form of the prodrug HDAC inhibitor ST7612AA1, through a maleimide-thiol linker to obtain the Antibody Drug Conjugate (ADC) ST8176AA1. The average drug/antibody ratio (DAR) was 4.5 as measured by hydrophobic interaction chromatography (HIC). Binding of ST8176AA1 to ErbB2 receptor and internalization in tumor cells were investigated by enzyme-linked immunosorbent assay (ELISA), surface plasmon resonance (SPR), cytofluorimetry, and High Content Screening (HCS) Imaging. The biological activity of the ADC was evaluated in vitro and in vivo by measuring cell proliferation/cell cycle, apoptosis/DNA damage, tubulin, and histone acetylation and modulation of Epithelial/Mesenchymal Transition (EMT) markers. Receptor binding and internalization of ST8176AA1 were confirmed to be similar to trastuzumab. Higher anti-tumor activity of ST8176AA1 compared to trastuzumab was observed in vitro in tumor cell lines. Such higher activity correlated with increased acetylation of histones and alfa-tubulin as a consequence of HDAC inhibitor-mediated epigenetic modulation that also induced increased expression of ErbB2 and estrogen receptor in triple negative breast cancer cells. Consistently with in vitro data, ST8176AA1 exhibited higher tumor growth inhibition than trastuzumab in xenograft models of ovary and colon carcinoma and in two patient-derived xenograft (PDX) models of pancreatic carcinoma. Immunohistochemistry analysis of tumor masses showed lower expression of the proliferation marker Ki67 and higher expression of cleaved caspase-3 in mice treated with the ADC compared to those treated with trastuzumab and results correlated with increased acetylation of both histones and tubulin. Collectively, present data indicate that ADC ST8176AA1 can target epigenetic modulation to ErbB2+ tumors. Interestingly, the amount of HDACi estimated to be delivered at the ST8176AA1 effective dose would correspond to ~1/1,000 of ST7612AA1 effective dose. Therefore, ST8176AA1 is an attractive new therapeutic candidate because it exhibits increased anti-tumor potency compared to trastuzumab by exerting epigenetic modulation at a much safer dose compared to standard HDACi-based therapeutic protocols. Frontiers Media S.A. 2020-01-23 /pmc/articles/PMC6989603/ /pubmed/32039017 http://dx.doi.org/10.3389/fonc.2019.01534 Text en Copyright © 2020 Milazzo, Vesci, Anastasi, Chiapparino, Rosi, Giannini, Taddei, Cini, Faltoni, Petricci, Battistuzzi, Salvini, Carollo and De Santis. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Oncology
Milazzo, Ferdinando Maria
Vesci, Loredana
Anastasi, Anna Maria
Chiapparino, Caterina
Rosi, Antonio
Giannini, Giuseppe
Taddei, Maurizio
Cini, Elena
Faltoni, Valentina
Petricci, Elena
Battistuzzi, Gianfranco
Salvini, Laura
Carollo, Valeria
De Santis, Rita
ErbB2 Targeted Epigenetic Modulation: Anti-tumor Efficacy of the ADC Trastuzumab-HDACi ST8176AA1
title ErbB2 Targeted Epigenetic Modulation: Anti-tumor Efficacy of the ADC Trastuzumab-HDACi ST8176AA1
title_full ErbB2 Targeted Epigenetic Modulation: Anti-tumor Efficacy of the ADC Trastuzumab-HDACi ST8176AA1
title_fullStr ErbB2 Targeted Epigenetic Modulation: Anti-tumor Efficacy of the ADC Trastuzumab-HDACi ST8176AA1
title_full_unstemmed ErbB2 Targeted Epigenetic Modulation: Anti-tumor Efficacy of the ADC Trastuzumab-HDACi ST8176AA1
title_short ErbB2 Targeted Epigenetic Modulation: Anti-tumor Efficacy of the ADC Trastuzumab-HDACi ST8176AA1
title_sort erbb2 targeted epigenetic modulation: anti-tumor efficacy of the adc trastuzumab-hdaci st8176aa1
topic Oncology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6989603/
https://www.ncbi.nlm.nih.gov/pubmed/32039017
http://dx.doi.org/10.3389/fonc.2019.01534
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