Novel tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid moiety induce cell cycle arrest and apoptosis in lung cancer cells by activation of DNA damage signaling

Lung cancer is still the leading cause of cancer-related death worldwide, indicating a necessity to develop more effective therapy. Acridine derivatives are potential anticancer agents due to their ability to intercalate DNA as well as inhibit enzymes involved in replication and transcription. Recen...

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Main Authors: Paweł Szymański, Paulina Olszewska, Elżbieta Mikiciuk-Olasik, Antoni Różalski, Agnieszka Maszewska, Łukasz Markiewicz, Magda Cuchra, Ireneusz Majsterek
Format: Article
Language:English
Published: SAGE Publishing 2017-03-01
Series:Tumor Biology
Online Access:https://doi.org/10.1177/1010428317695011
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author Paweł Szymański
Paulina Olszewska
Elżbieta Mikiciuk-Olasik
Antoni Różalski
Agnieszka Maszewska
Łukasz Markiewicz
Magda Cuchra
Ireneusz Majsterek
author_facet Paweł Szymański
Paulina Olszewska
Elżbieta Mikiciuk-Olasik
Antoni Różalski
Agnieszka Maszewska
Łukasz Markiewicz
Magda Cuchra
Ireneusz Majsterek
author_sort Paweł Szymański
collection DOAJ
description Lung cancer is still the leading cause of cancer-related death worldwide, indicating a necessity to develop more effective therapy. Acridine derivatives are potential anticancer agents due to their ability to intercalate DNA as well as inhibit enzymes involved in replication and transcription. Recently, we have evaluated anticancer activity of 32 novel acridine-based compounds. We found that the most effective were tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid containing eight and nine carbon atoms in the aliphatic chain. The aim of this study was to determine the molecular mechanisms of compounds-induced cell cycle arrest and apoptosis in human lung adenocarcinoma cells. All compounds activated Ataxia telangiectasia mutated kinase and phosphorylated histone H2A.X at Ser139 indicating DNA damage. Treatment of cells with the compounds increased phosphorylation and accumulation of p53 that regulate cell cycle as well as apoptosis. All compounds induced G0/1 cell cycle arrest by phosphorylation of cyclin-dependent kinase 2 at Tyr15 resulting in attenuation of the kinase activity. In addition, cyclopentaquinoline derivatives induced expression of cyclin-dependent kinase 2 inhibitor, p21; however, tetrahydroacridine derivatives had no significant effect on p21. Moreover, all compounds decreased the mitochondrial membrane potential accompanied by increased expression of Bax and down-regulation of Bcl-2, suggesting activation of the mitochondrial pathway. All compounds also significantly attenuated the migration rates of lung cancer cells. Collectively, our findings suggest a central role of activation of DNA damage signaling in response to new acridine derivatives treatment to induce cell cycle arrest and apoptosis in cancer cells and provide support for their further development as potential drug candidates.
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spelling doaj-art-3edb2775dc6b46dd9d337a46a7d4dc312025-08-20T03:33:31ZengSAGE PublishingTumor Biology1423-03802017-03-013910.1177/1010428317695011Novel tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid moiety induce cell cycle arrest and apoptosis in lung cancer cells by activation of DNA damage signalingPaweł Szymański0Paulina Olszewska1Elżbieta Mikiciuk-Olasik2Antoni Różalski3Agnieszka Maszewska4Łukasz Markiewicz5Magda Cuchra6Ireneusz Majsterek7Department of Pharmaceutical Chemistry, Drug Analyses and Radiopharmacy, Medical University, Łódź, PolandDepartment of Pharmaceutical Chemistry, Drug Analyses and Radiopharmacy, Medical University, Łódź, PolandDepartment of Pharmaceutical Chemistry, Drug Analyses and Radiopharmacy, Medical University, Łódź, PolandDepartment of Immunobiology of Bacteria, Institute of Microbiology, Biotechnology and Immunology, Faculty of Biology and Environmental Protection, University of Lodz, Łódź, PolandDepartment of Immunobiology of Bacteria, Institute of Microbiology, Biotechnology and Immunology, Faculty of Biology and Environmental Protection, University of Lodz, Łódź, PolandDepartment of Clinical Chemistry and Biochemistry, Medical University of Lodz, Łódź, PolandDepartment of Clinical Chemistry and Biochemistry, Medical University of Lodz, Łódź, PolandDepartment of Clinical Chemistry and Biochemistry, Medical University of Lodz, Łódź, PolandLung cancer is still the leading cause of cancer-related death worldwide, indicating a necessity to develop more effective therapy. Acridine derivatives are potential anticancer agents due to their ability to intercalate DNA as well as inhibit enzymes involved in replication and transcription. Recently, we have evaluated anticancer activity of 32 novel acridine-based compounds. We found that the most effective were tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid containing eight and nine carbon atoms in the aliphatic chain. The aim of this study was to determine the molecular mechanisms of compounds-induced cell cycle arrest and apoptosis in human lung adenocarcinoma cells. All compounds activated Ataxia telangiectasia mutated kinase and phosphorylated histone H2A.X at Ser139 indicating DNA damage. Treatment of cells with the compounds increased phosphorylation and accumulation of p53 that regulate cell cycle as well as apoptosis. All compounds induced G0/1 cell cycle arrest by phosphorylation of cyclin-dependent kinase 2 at Tyr15 resulting in attenuation of the kinase activity. In addition, cyclopentaquinoline derivatives induced expression of cyclin-dependent kinase 2 inhibitor, p21; however, tetrahydroacridine derivatives had no significant effect on p21. Moreover, all compounds decreased the mitochondrial membrane potential accompanied by increased expression of Bax and down-regulation of Bcl-2, suggesting activation of the mitochondrial pathway. All compounds also significantly attenuated the migration rates of lung cancer cells. Collectively, our findings suggest a central role of activation of DNA damage signaling in response to new acridine derivatives treatment to induce cell cycle arrest and apoptosis in cancer cells and provide support for their further development as potential drug candidates.https://doi.org/10.1177/1010428317695011
spellingShingle Paweł Szymański
Paulina Olszewska
Elżbieta Mikiciuk-Olasik
Antoni Różalski
Agnieszka Maszewska
Łukasz Markiewicz
Magda Cuchra
Ireneusz Majsterek
Novel tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid moiety induce cell cycle arrest and apoptosis in lung cancer cells by activation of DNA damage signaling
Tumor Biology
title Novel tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid moiety induce cell cycle arrest and apoptosis in lung cancer cells by activation of DNA damage signaling
title_full Novel tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid moiety induce cell cycle arrest and apoptosis in lung cancer cells by activation of DNA damage signaling
title_fullStr Novel tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid moiety induce cell cycle arrest and apoptosis in lung cancer cells by activation of DNA damage signaling
title_full_unstemmed Novel tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid moiety induce cell cycle arrest and apoptosis in lung cancer cells by activation of DNA damage signaling
title_short Novel tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid moiety induce cell cycle arrest and apoptosis in lung cancer cells by activation of DNA damage signaling
title_sort novel tetrahydroacridine and cyclopentaquinoline derivatives with fluorobenzoic acid moiety induce cell cycle arrest and apoptosis in lung cancer cells by activation of dna damage signaling
url https://doi.org/10.1177/1010428317695011
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