Potential antitumor activity of digitoxin and user-designed analog administered to human lung cancer cells
Cardiac glycosides (CGs), such as digitoxin, are traditionally used for treatment of congestive heart failure; recently they also gained attention for their anticancer properties. Previous studies showed that digitoxin and a synthetic L-sugar monosaccharide analog treatment decreases cancer cell pro...
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| Published in | Biochimica et biophysica acta. General subjects Vol. 1864; no. 11; p. 129683 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
Elsevier B.V
01.11.2020
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| Online Access | Get full text |
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| Abstract | Cardiac glycosides (CGs), such as digitoxin, are traditionally used for treatment of congestive heart failure; recently they also gained attention for their anticancer properties. Previous studies showed that digitoxin and a synthetic L-sugar monosaccharide analog treatment decreases cancer cell proliferation, increases apoptosis, and pro-adhesion abilities; however, no reports are available on their potential to alter lung cancer cell cytoskeleton structure and reduce migratory ability. Herein, we investigated the anticancer effects of digitoxin and its analog, digitoxigenin-α-L-rhamnoside (D6MA), to establish whether cytoskeleton reorganization and reduced motility are drug-induced cellular outcomes.
We treated non-small cell lung carcinoma cells (NSCLCs) with sub-therapeutic, therapeutic, and toxic concentrations of digitoxin and D6MA respectively, followed by both single point and real-time assays to evaluate changes in cellular gene and protein expression, adhesion, elasticity, and migration.
Digitoxin and D6MA induced a decrease in matrix metalloproteinases expression via altered focal adhesion signaling and a suppression of the phosphoinositide 3-kinases / protein kinase B pathway which lead to enhanced adhesion, altered elasticity, and reduced motility of NSCLCs. Global gene expression analysis identified dose-dependent changes to nuclear factor kappa-light-chain-enhancer, epithelial tumor, and microtubule dynamics signaling.
Our study demonstrates that digitoxin and D6MA can target antitumor signaling pathways to alter NSCLC cytoskeleton and migratory ability to thus potentially reduce their tumorigenicity.
Discovering signaling pathways that control cancer's cell phenotype and how such pathways are affected by CG treatment will potentially allow for active usage of synthetic CG analogs as therapeutic agents in advanced lung conditions.
[Display omitted]
•Synthetic cardiac glycoside analogs hold promise as potent anti-neoplastic agents.•Digitoxigenin-α-L-rhamnoside (D6MA) was more potent than digitoxin.•D6MA decreased lung cancer cell migration, volume, and elasticity.•D6MA suppressed PI3K/AKT and MMP expression via altered focal adhesion signaling.•D6MA potentially shifts lung cancer cell phenotype toward an epithelial-like state. |
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| AbstractList | Cardiac glycosides (CGs), such as digitoxin, are traditionally used for treatment of congestive heart failure; recently they also gained attention for their anticancer properties. Previous studies showed that digitoxin and a synthetic L-sugar monosaccharide analog treatment decreases cancer cell proliferation, increases apoptosis, and pro-adhesion abilities; however, no reports are available on their potential to alter lung cancer cell cytoskeleton structure and reduce migratory ability. Herein, we investigated the anticancer effects of digitoxin and its analog, digitoxigenin-α-L-rhamnoside (D6MA), to establish whether cytoskeleton reorganization and reduced motility are drug-induced cellular outcomes.BACKGROUNDCardiac glycosides (CGs), such as digitoxin, are traditionally used for treatment of congestive heart failure; recently they also gained attention for their anticancer properties. Previous studies showed that digitoxin and a synthetic L-sugar monosaccharide analog treatment decreases cancer cell proliferation, increases apoptosis, and pro-adhesion abilities; however, no reports are available on their potential to alter lung cancer cell cytoskeleton structure and reduce migratory ability. Herein, we investigated the anticancer effects of digitoxin and its analog, digitoxigenin-α-L-rhamnoside (D6MA), to establish whether cytoskeleton reorganization and reduced motility are drug-induced cellular outcomes.We treated non-small cell lung carcinoma cells (NSCLCs) with sub-therapeutic, therapeutic, and toxic concentrations of digitoxin and D6MA respectively, followed by both single point and real-time assays to evaluate changes in cellular gene and protein expression, adhesion, elasticity, and migration.METHODSWe treated non-small cell lung carcinoma cells (NSCLCs) with sub-therapeutic, therapeutic, and toxic concentrations of digitoxin and D6MA respectively, followed by both single point and real-time assays to evaluate changes in cellular gene and protein expression, adhesion, elasticity, and migration.Digitoxin and D6MA induced a decrease in matrix metalloproteinases expression via altered focal adhesion signaling and a suppression of the phosphoinositide 3-kinases / protein kinase B pathway which lead to enhanced adhesion, altered elasticity, and reduced motility of NSCLCs. Global gene expression analysis identified dose-dependent changes to nuclear factor kappa-light-chain-enhancer, epithelial tumor, and microtubule dynamics signaling.RESULTSDigitoxin and D6MA induced a decrease in matrix metalloproteinases expression via altered focal adhesion signaling and a suppression of the phosphoinositide 3-kinases / protein kinase B pathway which lead to enhanced adhesion, altered elasticity, and reduced motility of NSCLCs. Global gene expression analysis identified dose-dependent changes to nuclear factor kappa-light-chain-enhancer, epithelial tumor, and microtubule dynamics signaling.Our study demonstrates that digitoxin and D6MA can target antitumor signaling pathways to alter NSCLC cytoskeleton and migratory ability to thus potentially reduce their tumorigenicity.CONCLUSIONSOur study demonstrates that digitoxin and D6MA can target antitumor signaling pathways to alter NSCLC cytoskeleton and migratory ability to thus potentially reduce their tumorigenicity.Discovering signaling pathways that control cancer's cell phenotype and how such pathways are affected by CG treatment will potentially allow for active usage of synthetic CG analogs as therapeutic agents in advanced lung conditions.SIGNIFICANCEDiscovering signaling pathways that control cancer's cell phenotype and how such pathways are affected by CG treatment will potentially allow for active usage of synthetic CG analogs as therapeutic agents in advanced lung conditions. Cardiac glycosides (CGs), such as digitoxin, are traditionally used for treatment of congestive heart failure; recently they also gained attention for their anticancer properties. Previous studies showed that digitoxin and a synthetic L-sugar monosaccharide analog treatment decreases cancer cell proliferation, increases apoptosis, and pro-adhesion abilities; however, no reports are available on their potential to alter lung cancer cell cytoskeleton structure and reduce migratory ability. Herein, we investigated the anticancer effects of digitoxin and its analog, digitoxigenin-α-L-rhamnoside (D6MA), to establish whether cytoskeleton reorganization and reduced motility are drug-induced cellular outcomes.We treated non-small cell lung carcinoma cells (NSCLCs) with sub-therapeutic, therapeutic, and toxic concentrations of digitoxin and D6MA respectively, followed by both single point and real-time assays to evaluate changes in cellular gene and protein expression, adhesion, elasticity, and migration.Digitoxin and D6MA induced a decrease in matrix metalloproteinases expression via altered focal adhesion signaling and a suppression of the phosphoinositide 3-kinases / protein kinase B pathway which lead to enhanced adhesion, altered elasticity, and reduced motility of NSCLCs. Global gene expression analysis identified dose-dependent changes to nuclear factor kappa-light-chain-enhancer, epithelial tumor, and microtubule dynamics signaling.Our study demonstrates that digitoxin and D6MA can target antitumor signaling pathways to alter NSCLC cytoskeleton and migratory ability to thus potentially reduce their tumorigenicity.Discovering signaling pathways that control cancer's cell phenotype and how such pathways are affected by CG treatment will potentially allow for active usage of synthetic CG analogs as therapeutic agents in advanced lung conditions. Cardiac glycosides (CGs), such as digitoxin, are traditionally used for treatment of congestive heart failure; recently they also gained attention for their anticancer properties. Previous studies showed that digitoxin and a synthetic L-sugar monosaccharide analog treatment decreases cancer cell proliferation, increases apoptosis, and pro-adhesion abilities; however, no reports are available on their potential to alter lung cancer cell cytoskeleton structure and reduce migratory ability. Herein, we investigated the anticancer effects of digitoxin and its analog, digitoxigenin-α-L-rhamnoside (D6MA), to establish whether cytoskeleton reorganization and reduced motility are drug-induced cellular outcomes. We treated non-small cell lung carcinoma cells (NSCLCs) with sub-therapeutic, therapeutic, and toxic concentrations of digitoxin and D6MA respectively, followed by both single point and real-time assays to evaluate changes in cellular gene and protein expression, adhesion, elasticity, and migration. Digitoxin and D6MA induced a decrease in matrix metalloproteinases expression via altered focal adhesion signaling and a suppression of the phosphoinositide 3-kinases / protein kinase B pathway which lead to enhanced adhesion, altered elasticity, and reduced motility of NSCLCs. Global gene expression analysis identified dose-dependent changes to nuclear factor kappa-light-chain-enhancer, epithelial tumor, and microtubule dynamics signaling. Our study demonstrates that digitoxin and D6MA can target antitumor signaling pathways to alter NSCLC cytoskeleton and migratory ability to thus potentially reduce their tumorigenicity. Discovering signaling pathways that control cancer's cell phenotype and how such pathways are affected by CG treatment will potentially allow for active usage of synthetic CG analogs as therapeutic agents in advanced lung conditions. Cardiac glycosides (CGs), such as digitoxin, are traditionally used for treatment of congestive heart failure; recently they also gained attention for their anticancer properties. Previous studies showed that digitoxin and a synthetic L-sugar monosaccharide analog treatment decreases cancer cell proliferation, increases apoptosis, and pro-adhesion abilities; however, no reports are available on their potential to alter lung cancer cell cytoskeleton structure and reduce migratory ability. Herein, we investigated the anticancer effects of digitoxin and its analog, digitoxigenin-α-L-rhamnoside (D6MA), to establish whether cytoskeleton reorganization and reduced motility are drug-induced cellular outcomes. We treated non-small cell lung carcinoma cells (NSCLCs) with sub-therapeutic, therapeutic, and toxic concentrations of digitoxin and D6MA respectively, followed by both single point and real-time assays to evaluate changes in cellular gene and protein expression, adhesion, elasticity, and migration. Digitoxin and D6MA induced a decrease in matrix metalloproteinases expression via altered focal adhesion signaling and a suppression of the phosphoinositide 3-kinases / protein kinase B pathway which lead to enhanced adhesion, altered elasticity, and reduced motility of NSCLCs. Global gene expression analysis identified dose-dependent changes to nuclear factor kappa-light-chain-enhancer, epithelial tumor, and microtubule dynamics signaling. Our study demonstrates that digitoxin and D6MA can target antitumor signaling pathways to alter NSCLC cytoskeleton and migratory ability to thus potentially reduce their tumorigenicity. Discovering signaling pathways that control cancer's cell phenotype and how such pathways are affected by CG treatment will potentially allow for active usage of synthetic CG analogs as therapeutic agents in advanced lung conditions. [Display omitted] •Synthetic cardiac glycoside analogs hold promise as potent anti-neoplastic agents.•Digitoxigenin-α-L-rhamnoside (D6MA) was more potent than digitoxin.•D6MA decreased lung cancer cell migration, volume, and elasticity.•D6MA suppressed PI3K/AKT and MMP expression via altered focal adhesion signaling.•D6MA potentially shifts lung cancer cell phenotype toward an epithelial-like state. |
| ArticleNumber | 129683 |
| Author | Wagner, Alixandra Eldawud, Reem Gupta, Neha Dinu, Cerasela Zoica Dong, Chenbo Rojanasakul, Yon Stueckle, Todd A. O'Doherty, George |
| AuthorAffiliation | a Department of Chemical and Biomedical Engineering, West Virginia University, Morgantown, WV, 26506, USA c Department of Chemistry and Chemical Biology, Northeastern University, Boston, MA, 02115, USA b Department of Basic Pharmaceutical Sciences, West Virginia University, Morgantown, WV, 26506, USA d Health Effects Laboratory Division, National Institute for Occupational Safety and Health, Morgantown, WV, 26505, USA |
| AuthorAffiliation_xml | – name: c Department of Chemistry and Chemical Biology, Northeastern University, Boston, MA, 02115, USA – name: a Department of Chemical and Biomedical Engineering, West Virginia University, Morgantown, WV, 26506, USA – name: d Health Effects Laboratory Division, National Institute for Occupational Safety and Health, Morgantown, WV, 26505, USA – name: b Department of Basic Pharmaceutical Sciences, West Virginia University, Morgantown, WV, 26506, USA |
| Author_xml | – sequence: 1 givenname: Reem surname: Eldawud fullname: Eldawud, Reem organization: Department of Chemical and Biomedical Engineering, West Virginia University, Morgantown, WV 26506, USA – sequence: 2 givenname: Alixandra surname: Wagner fullname: Wagner, Alixandra organization: Department of Chemical and Biomedical Engineering, West Virginia University, Morgantown, WV 26506, USA – sequence: 3 givenname: Chenbo surname: Dong fullname: Dong, Chenbo organization: Department of Chemical and Biomedical Engineering, West Virginia University, Morgantown, WV 26506, USA – sequence: 4 givenname: Neha surname: Gupta fullname: Gupta, Neha organization: Department of Chemical and Biomedical Engineering, West Virginia University, Morgantown, WV 26506, USA – sequence: 5 givenname: Yon surname: Rojanasakul fullname: Rojanasakul, Yon organization: Department of Basic Pharmaceutical Sciences, West Virginia University, Morgantown, WV 26506, USA – sequence: 6 givenname: George surname: O'Doherty fullname: O'Doherty, George organization: Department of Chemistry and Chemical Biology, Northeastern University, Boston, MA 02115, USA – sequence: 7 givenname: Todd A. surname: Stueckle fullname: Stueckle, Todd A. organization: Health Effects Laboratory Division, National Institute for Occupational Safety and Health, Morgantown, WV 26505, USA – sequence: 8 givenname: Cerasela Zoica surname: Dinu fullname: Dinu, Cerasela Zoica organization: Department of Chemical and Biomedical Engineering, West Virginia University, Morgantown, WV 26506, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32679249$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1039_D2CC05280F crossref_primary_10_3892_or_2024_8762 crossref_primary_10_1016_j_biochi_2023_04_010 crossref_primary_10_1186_s12964_023_01317_8 crossref_primary_10_3389_fmolb_2023_1327740 crossref_primary_10_1007_s00216_025_05836_w crossref_primary_10_1016_j_cjac_2022_100220 |
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| Keywords | BCA CG E Lung cancer Anti-tumor activity DEG AFM ECIS DTX Therapeutic alternatives Synthetic analog Cardiac glycosides MFI Chemotherapy Digitoxin D6MA |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 R.E.D., A.W., C.D., and N.G. performed research and analyzed data; Y.R. and G.OD.-contributed with D6MA product and technical expertise, T.A.S. and C.Z.D. designed research; R.E.D., A.W., T.A.S. and C.Z.D. wrote the paper; all authors approved the paper. Authors have contributed equally to this work. Author contributions |
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| SubjectTerms | adhesion Anti-tumor activity antineoplastic activity Antineoplastic Agents - chemistry Antineoplastic Agents - pharmacology apoptosis Carcinoma, Non-Small-Cell Lung - drug therapy Carcinoma, Non-Small-Cell Lung - pathology Cardiac glycosides Cell Line, Tumor Cell Movement - drug effects cell proliferation Chemotherapy Cytoskeleton - drug effects Cytoskeleton - pathology Digitoxin Digitoxin - analogs & derivatives Digitoxin - pharmacology dose response epithelium focal adhesions gene expression genes heart failure human diseases Humans Lung cancer lung neoplasms Lung Neoplasms - drug therapy Lung Neoplasms - pathology lungs metalloproteinases microtubules neoplasm cells non-specific serine/threonine protein kinase protein synthesis signal transduction Synthetic analog Therapeutic alternatives therapeutics toxicity |
| Title | Potential antitumor activity of digitoxin and user-designed analog administered to human lung cancer cells |
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