Cardiac Glycoside Glucoevatromonoside Induces Cancer Type-Specific Cell Death

Cardiac glycosides (CGs) are natural compounds used traditionally to treat congestive heart diseases. Recent investigations repositioned CGs as potential anticancer agents. To discover novel cytotoxic CG scaffolds, we selected the cardenolide glucoevatromonoside (GEV) out of 46 CGs for its low nanom...

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Published in:Frontiers in pharmacology Vol. 9; p. 70
Main Authors: Schneider, Naira F Z, Cerella, Claudia, Lee, Jin-Young, Mazumder, Aloran, Kim, Kyung Rok, de Carvalho, Annelise, Munkert, Jennifer, Pádua, Rodrigo M, Kreis, Wolfgang, Kim, Kyu-Won, Christov, Christo, Dicato, Mario, Kim, Hyun-Jung, Han, Byung Woo, Braga, Fernão C, Simões, Cláudia M O, Diederich, Marc
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Language:English
Published: Switzerland Frontiers Media S.A 01-03-2018
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Abstract Cardiac glycosides (CGs) are natural compounds used traditionally to treat congestive heart diseases. Recent investigations repositioned CGs as potential anticancer agents. To discover novel cytotoxic CG scaffolds, we selected the cardenolide glucoevatromonoside (GEV) out of 46 CGs for its low nanomolar anti-lung cancer activity. GEV presented reduced toxicity toward non-cancerous cell types (lung MRC-5 and PBMC) and high-affinity binding to the Na /K -ATPase α subunit, assessed by computational docking. GEV-induced cell death was caspase-independent, as investigated by a multiparametric approach, and culminates in severe morphological alterations in A549 cells, monitored by transmission electron microscopy, live cell imaging and flow cytometry. This non-canonical cell death was not preceded or accompanied by exacerbation of autophagy. In the presence of GEV, markers of autophagic flux (e.g. LC3I-II conversion) were impacted, even in presence of bafilomycin A1. Cell death induction remained unaffected by calpain, cathepsin, parthanatos, or necroptosis inhibitors. Interestingly, GEV triggered caspase-dependent apoptosis in U937 acute myeloid leukemia cells, witnessing cancer-type specific cell death induction. Differential cell cycle modulation by this CG led to a G2/M arrest, cyclin B1 and p53 downregulation in A549, but not in U937 cells. We further extended the anti-cancer potential of GEV to 3D cell culture using clonogenic and spheroid formation assays and validated our findings by zebrafish xenografts. Altogether, GEV shows an interesting anticancer profile with the ability to exert cytotoxic effects via induction of different cell death modalities.
AbstractList Cardiac glycosides (CGs) are natural compounds used traditionally to treat congestive heart diseases. Recent investigations repositioned CGs as potential anticancer agents. To discover novel cytotoxic CG scaffolds, we selected the cardenolide glucoevatromonoside (GEV) out of 46 CGs for its low nanomolar anti-lung cancer activity. GEV presented reduced toxicity toward non-cancerous cell types (lung MRC-5 and PBMC) and high-affinity binding to the Na+/K+-ATPase α subunit, assessed by computational docking. GEV-induced cell death was caspase-independent, as investigated by a multiparametric approach, and culminates in severe morphological alterations in A549 cells, monitored by transmission electron microscopy, live cell imaging and flow cytometry. This non-canonical cell death was not preceded or accompanied by exacerbation of autophagy. In the presence of GEV, markers of autophagic flux (e.g. LC3I-II conversion) were impacted, even in presence of bafilomycin A1. Cell death induction remained unaffected by calpain, cathepsin, parthanatos, or necroptosis inhibitors. Interestingly, GEV triggered caspase-dependent apoptosis in U937 acute myeloid leukemia cells, witnessing cancer-type specific cell death induction. Differential cell cycle modulation by this CG led to a G2/M arrest, cyclin B1 and p53 downregulation in A549, but not in U937 cells. We further extended the anti-cancer potential of GEV to 3D cell culture using clonogenic and spheroid formation assays and validated our findings in vivo by zebrafish xenografts. Altogether, GEV shows an interesting anticancer profile with the ability to exert cytotoxic effects via induction of different cell death modalities.
Cardiac glycosides (CGs) are natural compounds used traditionally to treat congestive heart diseases. Recent investigations repositioned CGs as potential anticancer agents. To discover novel cytotoxic CG scaffolds, we selected the cardenolide glucoevatromonoside (GEV) out of 46 CGs for its low nanomolar anti-lung cancer activity. GEV presented reduced toxicity toward non-cancerous cell types (lung MRC-5 and PBMC) and high-affinity binding to the Na + /K + -ATPase α subunit, assessed by computational docking. GEV-induced cell death was caspase-independent, as investigated by a multiparametric approach, and culminates in severe morphological alterations in A549 cells, monitored by transmission electron microscopy, live cell imaging and flow cytometry. This non-canonical cell death was not preceded or accompanied by exacerbation of autophagy. In the presence of GEV, markers of autophagic flux (e.g. LC3I-II conversion) were impacted, even in presence of bafilomycin A1. Cell death induction remained unaffected by calpain, cathepsin, parthanatos, or necroptosis inhibitors. Interestingly, GEV triggered caspase-dependent apoptosis in U937 acute myeloid leukemia cells, witnessing cancer-type specific cell death induction. Differential cell cycle modulation by this CG led to a G2/M arrest, cyclin B1 and p53 downregulation in A549, but not in U937 cells. We further extended the anti-cancer potential of GEV to 3D cell culture using clonogenic and spheroid formation assays and validated our findings in vivo by zebrafish xenografts. Altogether, GEV shows an interesting anticancer profile with the ability to exert cytotoxic effects via induction of different cell death modalities.
Cardiac glycosides (CGs) are natural compounds used traditionally to treat congestive heart diseases. Recent investigations repositioned CGs as potential anticancer agents. To discover novel cytotoxic CG scaffolds, we selected the cardenolide glucoevatromonoside (GEV) out of 46 CGs for its low nanomolar anti-lung cancer activity. GEV presented reduced toxicity toward non-cancerous cell types (lung MRC-5 and PBMC) and high-affinity binding to the Na /K -ATPase α subunit, assessed by computational docking. GEV-induced cell death was caspase-independent, as investigated by a multiparametric approach, and culminates in severe morphological alterations in A549 cells, monitored by transmission electron microscopy, live cell imaging and flow cytometry. This non-canonical cell death was not preceded or accompanied by exacerbation of autophagy. In the presence of GEV, markers of autophagic flux (e.g. LC3I-II conversion) were impacted, even in presence of bafilomycin A1. Cell death induction remained unaffected by calpain, cathepsin, parthanatos, or necroptosis inhibitors. Interestingly, GEV triggered caspase-dependent apoptosis in U937 acute myeloid leukemia cells, witnessing cancer-type specific cell death induction. Differential cell cycle modulation by this CG led to a G2/M arrest, cyclin B1 and p53 downregulation in A549, but not in U937 cells. We further extended the anti-cancer potential of GEV to 3D cell culture using clonogenic and spheroid formation assays and validated our findings by zebrafish xenografts. Altogether, GEV shows an interesting anticancer profile with the ability to exert cytotoxic effects via induction of different cell death modalities.
Author Munkert, Jennifer
Schneider, Naira F Z
Christov, Christo
Cerella, Claudia
Lee, Jin-Young
Mazumder, Aloran
Simões, Cláudia M O
de Carvalho, Annelise
Han, Byung Woo
Kim, Hyun-Jung
Kim, Kyung Rok
Kreis, Wolfgang
Kim, Kyu-Won
Braga, Fernão C
Diederich, Marc
Pádua, Rodrigo M
Dicato, Mario
AuthorAffiliation 6 SNU-Harvard Neurovascular Protection Center, College of Pharmacy and Research Institute of Pharmaceutical Sciences, Seoul National University , Seoul , South Korea
4 Department of Biology, Friedrich-Alexander Universität, Erlangen-Nürnberg , Erlangen , Germany
5 Departamento de Produtos Farmacêuticos, Faculdade de Farmácia, Universidade Federal de Minas Gerais , Belo Horizonte , Brazil
1 Laboratorio de Virologia Applicada, Departamento de Ciências Farmacêuticas, Centro de Ciências da Saúde, Universidade Federal de Santa Catarina , Florianópolis , Brazil
2 Laboratoire de Biologie Moléculaire et Cellulaire du Cancer, Hôpital Kirchberg , Luxembourg , Luxembourg
8 College of Pharmacy, Chung-Ang University , Seoul , South Korea
7 Faculté de Médecine, Université de Lorraine , Nancy , France
3 Department of Pharmacy, Research Institute of Pharmaceutical Sciences, College of Pharmacy, Seoul National University , Seoul , South Korea
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  surname: Diederich
  fullname: Diederich, Marc
  organization: Department of Pharmacy, Research Institute of Pharmaceutical Sciences, College of Pharmacy, Seoul National University, Seoul, South Korea
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ContentType Journal Article
Copyright Copyright © 2018 Schneider, Cerella, Lee, Mazumder, Kim, de Carvalho, Munkert, Pádua, Kreis, Kim, Christov, Dicato, Kim, Han, Braga, Simões and Diederich. 2018 Schneider, Cerella, Lee, Mazumder, Kim, de Carvalho, Munkert, Pádua, Kreis, Kim, Christov, Dicato, Kim, Han, Braga, Simões and Diederich
Copyright_xml – notice: Copyright © 2018 Schneider, Cerella, Lee, Mazumder, Kim, de Carvalho, Munkert, Pádua, Kreis, Kim, Christov, Dicato, Kim, Han, Braga, Simões and Diederich. 2018 Schneider, Cerella, Lee, Mazumder, Kim, de Carvalho, Munkert, Pádua, Kreis, Kim, Christov, Dicato, Kim, Han, Braga, Simões and Diederich
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Keywords lung cancer
non-canonical cell death
apoptosis
cardiac glycoside
glucoevatromonoside
Language English
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This article was submitted to Ethnopharmacology, a section of the journal Frontiers in Pharmacology
Edited by: Thomas Efferth, Johannes Gutenberg-Universität Mainz, Germany
Reviewed by: Linlin Lu, International Institute for Translational Chinese Medicine, China; Wentzel Christoffel Gelderblom, Cape Peninsula University of Technology, South Africa
These authors have contributed equally to this work.
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Snippet Cardiac glycosides (CGs) are natural compounds used traditionally to treat congestive heart diseases. Recent investigations repositioned CGs as potential...
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SubjectTerms apoptosis
cardiac glycoside
glucoevatromonoside
lung cancer
non-canonical cell death
Pharmacology
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Title Cardiac Glycoside Glucoevatromonoside Induces Cancer Type-Specific Cell Death
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