AMTAC-19, a Spiro-Acridine Compound, Induces In Vitro Antitumor Effect via the ROS-ERK/JNK Signaling Pathway

Colorectal cancer remains a significant cause of mortality worldwide. A spiro-acridine derivative, (<i>E</i>)-1′-((4-bromobenzylidene)amino)-5′-oxo-1′,5′-dihydro-10<i>H</i>-spiro[acridine-9,2′-pyrrole]-4′-carbonitrile (AMTAC-19), showed significant cytotoxicity in HCT-116 col...

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Main Authors: Valgrícia Matias de Sousa, Sâmia Sousa Duarte, Rafael Carlos Ferreira, Natália Ferreira de Sousa, Marcus Tullius Scotti, Luciana Scotti, Marcelo Sobral da Silva, Josean Fechine Tavares, Ricardo Olímpio de Moura, Juan Carlos Ramos Gonçalves, Marianna Vieira Sobral
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Language:English
Published: MDPI AG 2024-11-01
Series:Molecules
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Online Access:https://www.mdpi.com/1420-3049/29/22/5344
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author Valgrícia Matias de Sousa
Sâmia Sousa Duarte
Rafael Carlos Ferreira
Natália Ferreira de Sousa
Marcus Tullius Scotti
Luciana Scotti
Marcelo Sobral da Silva
Josean Fechine Tavares
Ricardo Olímpio de Moura
Juan Carlos Ramos Gonçalves
Marianna Vieira Sobral
author_facet Valgrícia Matias de Sousa
Sâmia Sousa Duarte
Rafael Carlos Ferreira
Natália Ferreira de Sousa
Marcus Tullius Scotti
Luciana Scotti
Marcelo Sobral da Silva
Josean Fechine Tavares
Ricardo Olímpio de Moura
Juan Carlos Ramos Gonçalves
Marianna Vieira Sobral
author_sort Valgrícia Matias de Sousa
collection DOAJ
description Colorectal cancer remains a significant cause of mortality worldwide. A spiro-acridine derivative, (<i>E</i>)-1′-((4-bromobenzylidene)amino)-5′-oxo-1′,5′-dihydro-10<i>H</i>-spiro[acridine-9,2′-pyrrole]-4′-carbonitrile (AMTAC-19), showed significant cytotoxicity in HCT-116 colorectal carcinoma cells (half maximal inhibitory concentration, IC50 = 10.35 ± 1.66 µM) and antioxidant effects after 48 h of treatment. In this study, Molegro Virtual Docker v.6.0.1 software was used to investigate the interactions between AMTAC-19 and the Extracellular Signal-Regulated Kinase 1 (ERK1), c-Jun N-terminal Kinase 1 (JNK1), and p38 Mitogen-Activated Protein Kinase α (p38α MAPK). In vitro assays were conducted in HCT-116 cells to evaluate the effect of AMTAC-19 on the modulation of these proteins’ activities using flow cytometry. Furthermore, the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay in the presence or absence of ERK1/2, JNK, and p38 MAPK inhibitors was used to evaluate the involvement of these enzymes in AMTAC-19 cytotoxicity. ROS production was assessed using the 2,7-dichlorodihydrofluorescein diacetate (DCFH-DA) assay at various incubation times (30 min, 1 h, 6 h, 12 h, and 24 h), and the MTT assay using N-acetyl-L-cysteine (NAC) was performed. In silico results indicated that AMTAC-19 interacts with ERK1, JNK1, and p38α MAPK. Additionally, AMTAC-19 activated ERK1/2 and JNK1 in HCT-116 cells, and its cytotoxicity was significantly reduced in the presence of ERK1/2 and JNK inhibitors. AMTAC-19 also induced a significant increase in ROS production (30 min and 1 h), while NAC pretreatment reduced its cytotoxicity. These findings support AMTAC-19′s in vitro antitumor effect through ROS-dependent activation of ERK and JNK pathways.
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spelling doaj-art-139f568071074f7ebd084358d9fc985d2025-08-20T01:53:57ZengMDPI AGMolecules1420-30492024-11-012922534410.3390/molecules29225344AMTAC-19, a Spiro-Acridine Compound, Induces In Vitro Antitumor Effect via the ROS-ERK/JNK Signaling PathwayValgrícia Matias de Sousa0Sâmia Sousa Duarte1Rafael Carlos Ferreira2Natália Ferreira de Sousa3Marcus Tullius Scotti4Luciana Scotti5Marcelo Sobral da Silva6Josean Fechine Tavares7Ricardo Olímpio de Moura8Juan Carlos Ramos Gonçalves9Marianna Vieira Sobral10Postgraduate Program in Natural Products and Bioactive Synthetics, Federal University of Paraíba, João Pessoa 58051-970, PB, BrazilPostgraduate Program in Natural Products and Bioactive Synthetics, Federal University of Paraíba, João Pessoa 58051-970, PB, BrazilPostgraduate Program in Natural Products and Bioactive Synthetics, Federal University of Paraíba, João Pessoa 58051-970, PB, BrazilPostgraduate Program in Natural Products and Bioactive Synthetics, Federal University of Paraíba, João Pessoa 58051-970, PB, BrazilPostgraduate Program in Natural Products and Bioactive Synthetics, Federal University of Paraíba, João Pessoa 58051-970, PB, BrazilPostgraduate Program in Natural Products and Bioactive Synthetics, Federal University of Paraíba, João Pessoa 58051-970, PB, BrazilPostgraduate Program in Natural Products and Bioactive Synthetics, Federal University of Paraíba, João Pessoa 58051-970, PB, BrazilPostgraduate Program in Natural Products and Bioactive Synthetics, Federal University of Paraíba, João Pessoa 58051-970, PB, BrazilDrug Development and Synthesis Laboratory, Department of Pharmacy, State University of Paraíba, João Pessoa 58070-450, PB, BrazilPostgraduate Program in Natural Products and Bioactive Synthetics, Federal University of Paraíba, João Pessoa 58051-970, PB, BrazilPostgraduate Program in Natural Products and Bioactive Synthetics, Federal University of Paraíba, João Pessoa 58051-970, PB, BrazilColorectal cancer remains a significant cause of mortality worldwide. A spiro-acridine derivative, (<i>E</i>)-1′-((4-bromobenzylidene)amino)-5′-oxo-1′,5′-dihydro-10<i>H</i>-spiro[acridine-9,2′-pyrrole]-4′-carbonitrile (AMTAC-19), showed significant cytotoxicity in HCT-116 colorectal carcinoma cells (half maximal inhibitory concentration, IC50 = 10.35 ± 1.66 µM) and antioxidant effects after 48 h of treatment. In this study, Molegro Virtual Docker v.6.0.1 software was used to investigate the interactions between AMTAC-19 and the Extracellular Signal-Regulated Kinase 1 (ERK1), c-Jun N-terminal Kinase 1 (JNK1), and p38 Mitogen-Activated Protein Kinase α (p38α MAPK). In vitro assays were conducted in HCT-116 cells to evaluate the effect of AMTAC-19 on the modulation of these proteins’ activities using flow cytometry. Furthermore, the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay in the presence or absence of ERK1/2, JNK, and p38 MAPK inhibitors was used to evaluate the involvement of these enzymes in AMTAC-19 cytotoxicity. ROS production was assessed using the 2,7-dichlorodihydrofluorescein diacetate (DCFH-DA) assay at various incubation times (30 min, 1 h, 6 h, 12 h, and 24 h), and the MTT assay using N-acetyl-L-cysteine (NAC) was performed. In silico results indicated that AMTAC-19 interacts with ERK1, JNK1, and p38α MAPK. Additionally, AMTAC-19 activated ERK1/2 and JNK1 in HCT-116 cells, and its cytotoxicity was significantly reduced in the presence of ERK1/2 and JNK inhibitors. AMTAC-19 also induced a significant increase in ROS production (30 min and 1 h), while NAC pretreatment reduced its cytotoxicity. These findings support AMTAC-19′s in vitro antitumor effect through ROS-dependent activation of ERK and JNK pathways.https://www.mdpi.com/1420-3049/29/22/5344colorectal carcinomaoxidative stressMAPKs
spellingShingle Valgrícia Matias de Sousa
Sâmia Sousa Duarte
Rafael Carlos Ferreira
Natália Ferreira de Sousa
Marcus Tullius Scotti
Luciana Scotti
Marcelo Sobral da Silva
Josean Fechine Tavares
Ricardo Olímpio de Moura
Juan Carlos Ramos Gonçalves
Marianna Vieira Sobral
AMTAC-19, a Spiro-Acridine Compound, Induces In Vitro Antitumor Effect via the ROS-ERK/JNK Signaling Pathway
Molecules
colorectal carcinoma
oxidative stress
MAPKs
title AMTAC-19, a Spiro-Acridine Compound, Induces In Vitro Antitumor Effect via the ROS-ERK/JNK Signaling Pathway
title_full AMTAC-19, a Spiro-Acridine Compound, Induces In Vitro Antitumor Effect via the ROS-ERK/JNK Signaling Pathway
title_fullStr AMTAC-19, a Spiro-Acridine Compound, Induces In Vitro Antitumor Effect via the ROS-ERK/JNK Signaling Pathway
title_full_unstemmed AMTAC-19, a Spiro-Acridine Compound, Induces In Vitro Antitumor Effect via the ROS-ERK/JNK Signaling Pathway
title_short AMTAC-19, a Spiro-Acridine Compound, Induces In Vitro Antitumor Effect via the ROS-ERK/JNK Signaling Pathway
title_sort amtac 19 a spiro acridine compound induces in vitro antitumor effect via the ros erk jnk signaling pathway
topic colorectal carcinoma
oxidative stress
MAPKs
url https://www.mdpi.com/1420-3049/29/22/5344
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