Preclinical anti-cancer activity and multiple mechanisms of action of a cationic silver complex bearing N-heterocyclic carbene ligands
Organometallic complexes offer the prospect of targeting multiple pathways that are important in cancer biology. Here, the preclinical activity and mechanism(s) of action of a silver-bis(N-heterocyclic carbine) complex (Ag8) were evaluated. Ag8 induced DNA damage via several mechanisms including top...
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| Published in | Cancer letters Vol. 403; pp. 98 - 107 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Ireland
Elsevier B.V
10.09.2017
Elsevier Limited |
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| Abstract | Organometallic complexes offer the prospect of targeting multiple pathways that are important in cancer biology. Here, the preclinical activity and mechanism(s) of action of a silver-bis(N-heterocyclic carbine) complex (Ag8) were evaluated. Ag8 induced DNA damage via several mechanisms including topoisomerase I/II and thioredoxin reductase inhibition and induction of reactive oxygen species. DNA damage induction was consistent with cytotoxicity observed against proliferating cells and Ag8 induced cell death by apoptosis. Ag8 also inhibited DNA repair enzyme PARP1, showed preferential activity against cisplatin resistant A2780 cells and potentiated the activity of temozolomide. Ag8 was substantially less active against non-proliferating non-cancer cells and selectively inhibited glycolysis in cancer cells. Ag8 also induced significant anti-tumour effects against cells implanted intraperitoneally in hollow fibres but lacked activity against hollow fibres implanted subcutaneously. Thus, Ag8 targets multiple pathways of importance in cancer biology, is less active against non-cancer cells and shows activity in vivo in a loco-regional setting.
•Selective cytotoxic effects against cancer cells as opposed to non-cancer cells in vitro.•Lack of cross-resistance to cisplatin in vitro and pharmacological properties that are distinct from cisplatin.•Inhibition of multiple targets including (i) Thioredoxin reductase (Trx-R); (ii) PARP-1; (iii) topoisomerases I and II (with preferential inhibition of topoisomerase I); (iv) glycolysis.•In vivo activity against hollow fibres implanted intraperitoneally. |
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| AbstractList | Organometallic complexes offer the prospect of targeting multiple pathways that are important in cancer biology. Here, the preclinical activity and mechanism(s) of action of a silver-bis(N-heterocyclic carbine) complex (Ag8) were evaluated. Ag8 induced DNA damage via several mechanisms including topoisomerase I/II and thioredoxin reductase inhibition and induction of reactive oxygen species. DNA damage induction was consistent with cytotoxicity observed against proliferating cells and Ag8 induced cell death by apoptosis. Ag8 also inhibited DNA repair enzyme PARP1, showed preferential activity against cisplatin resistant A2780 cells and potentiated the activity of temozolomide. Ag8 was substantially less active against non-proliferating non-cancer cells and selectively inhibited glycolysis in cancer cells. Ag8 also induced significant anti-tumour effects against cells implanted intraperitoneally in hollow fibres but lacked activity against hollow fibres implanted subcutaneously. Thus, Ag8 targets multiple pathways of importance in cancer biology, is less active against non-cancer cells and shows activity in vivo in a loco-regional setting.Organometallic complexes offer the prospect of targeting multiple pathways that are important in cancer biology. Here, the preclinical activity and mechanism(s) of action of a silver-bis(N-heterocyclic carbine) complex (Ag8) were evaluated. Ag8 induced DNA damage via several mechanisms including topoisomerase I/II and thioredoxin reductase inhibition and induction of reactive oxygen species. DNA damage induction was consistent with cytotoxicity observed against proliferating cells and Ag8 induced cell death by apoptosis. Ag8 also inhibited DNA repair enzyme PARP1, showed preferential activity against cisplatin resistant A2780 cells and potentiated the activity of temozolomide. Ag8 was substantially less active against non-proliferating non-cancer cells and selectively inhibited glycolysis in cancer cells. Ag8 also induced significant anti-tumour effects against cells implanted intraperitoneally in hollow fibres but lacked activity against hollow fibres implanted subcutaneously. Thus, Ag8 targets multiple pathways of importance in cancer biology, is less active against non-cancer cells and shows activity in vivo in a loco-regional setting. Abstract Organometallic complexes offer the prospect of targeting multiple pathways that are important in cancer biology. Here, the preclinical activity and mechanism(s) of action of a silver-bis( N -heterocyclic carbine) complex (Ag8) were evaluated. Ag8 induced DNA damage via several mechanisms including topoisomerase I/II and thioredoxin reductase inhibition and induction of reactive oxygen species. DNA damage induction was consistent with cytotoxicity observed against proliferating cells and Ag8 induced cell death by apoptosis. Ag8 also inhibited DNA repair enzyme PARP1, showed preferential activity against cisplatin resistant A2780 cells and potentiated the activity of temozolomide. Ag8 was substantially less active against non-proliferating non-cancer cells and selectively inhibited glycolysis in cancer cells. Ag8 also induced significant anti-tumour effects against cells implanted intraperitoneally in hollow fibres but lacked activity against hollow fibres implanted subcutaneously. Thus, Ag8 targets multiple pathways of importance in cancer biology, is less active against non-cancer cells and shows activity in vivo in a loco-regional setting. Organometallic complexes offer the prospect of targeting multiple pathways that are important in cancer biology. Here, the preclinical activity and mechanism(s) of action of a silver-bis(N-heterocyclic carbine) complex (Ag8) were evaluated. Ag8 induced DNA damage via several mechanisms including topoisomerase I/II and thioredoxin reductase inhibition and induction of reactive oxygen species. DNA damage induction was consistent with cytotoxicity observed against proliferating cells and Ag8 induced cell death by apoptosis. Ag8 also inhibited DNA repair enzyme PARP1, showed preferential activity against cisplatin resistant A2780 cells and potentiated the activity of temozolomide. Ag8 was substantially less active against non-proliferating non-cancer cells and selectively inhibited glycolysis in cancer cells. Ag8 also induced significant anti-tumour effects against cells implanted intraperitoneally in hollow fibres but lacked activity against hollow fibres implanted subcutaneously. Thus, Ag8 targets multiple pathways of importance in cancer biology, is less active against non-cancer cells and shows activity in vivo in a loco-regional setting. •Selective cytotoxic effects against cancer cells as opposed to non-cancer cells in vitro.•Lack of cross-resistance to cisplatin in vitro and pharmacological properties that are distinct from cisplatin.•Inhibition of multiple targets including (i) Thioredoxin reductase (Trx-R); (ii) PARP-1; (iii) topoisomerases I and II (with preferential inhibition of topoisomerase I); (iv) glycolysis.•In vivo activity against hollow fibres implanted intraperitoneally. Organometallic complexes offer the prospect of targeting multiple pathways that are important in cancer biology. Here, the preclinical activity and mechanism(s) of action of a silver-bis(N-heterocyclic carbine) complex (Ag8) were evaluated. Ag8 induced DNA damage via several mechanisms including topoisomerase I/II and thioredoxin reductase inhibition and induction of reactive oxygen species. DNA damage induction was consistent with cytotoxicity observed against proliferating cells and Ag8 induced cell death by apoptosis. Ag8 also inhibited DNA repair enzyme PARP1, showed preferential activity against cisplatin resistant A2780 cells and potentiated the activity of temozolomide. Ag8 was substantially less active against non-proliferating non-cancer cells and selectively inhibited glycolysis in cancer cells. Ag8 also induced significant anti-tumour effects against cells implanted intraperitoneally in hollow fibres but lacked activity against hollow fibres implanted subcutaneously. Thus, Ag8 targets multiple pathways of importance in cancer biology, is less active against non-cancer cells and shows activityin vivoin a loco-regional setting. Organometallic complexes offer the prospect of targeting multiple pathways that are important in cancer biology. Here, the preclinical activity and mechanism(s) of action of a silver-bis(N-heterocyclic carbine) complex (Ag8) were evaluated. Ag8 induced DNA damage via several mechanisms including topoisomerase I/II and thioredoxin reductase inhibition and induction of reactive oxygen species. DNA damage induction was consistent with cytotoxicity observed against proliferating cells and Ag8 induced cell death by apoptosis. Ag8 also inhibited DNA repair enzyme PARP1, showed preferential activity against cisplatin resistant A2780 cells and potentiated the activity of temozolomide. Ag8 was substantially less active against non-proliferating non-cancer cells and selectively inhibited glycolysis in cancer cells. Ag8 also induced significant anti-tumour effects against cells implanted intraperitoneally in hollow fibres but lacked activity against hollow fibres implanted subcutaneously. Thus, Ag8 targets multiple pathways of importance in cancer biology, is less active against non-cancer cells and shows activity in vivo in a loco-regional setting. |
| Author | Stratford, Ian J. Wheelhouse, Richard T. Latif, Ayşe Shepherd, Samantha Willans, Charlotte E. Shnyder, Steve D. Georgopoulos, Nikolaos T. Allison, Simon J. Baronou, Efstathia Phillips, Roger M. Sadiq, Maria Cooper, Patricia A. Dunnill, Chris |
| Author_xml | – sequence: 1 givenname: Simon J. surname: Allison fullname: Allison, Simon J. organization: School of Applied Sciences, University of Huddersfield, Queensgate, Huddersfield HD1 3DH, UK – sequence: 2 givenname: Maria surname: Sadiq fullname: Sadiq, Maria organization: Institute of Cancer Therapeutics, University of Bradford, Bradford BD7 1DP, UK – sequence: 3 givenname: Efstathia surname: Baronou fullname: Baronou, Efstathia organization: School of Pharmacy, University of Bradford, Bradford BD7 1DP, UK – sequence: 4 givenname: Patricia A. surname: Cooper fullname: Cooper, Patricia A. organization: Institute of Cancer Therapeutics, University of Bradford, Bradford BD7 1DP, UK – sequence: 5 givenname: Chris surname: Dunnill fullname: Dunnill, Chris organization: School of Applied Sciences, University of Huddersfield, Queensgate, Huddersfield HD1 3DH, UK – sequence: 6 givenname: Nikolaos T. surname: Georgopoulos fullname: Georgopoulos, Nikolaos T. organization: School of Applied Sciences, University of Huddersfield, Queensgate, Huddersfield HD1 3DH, UK – sequence: 7 givenname: Ayşe surname: Latif fullname: Latif, Ayşe organization: Division of Pharmacy and Optometry, Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, UK – sequence: 8 givenname: Samantha surname: Shepherd fullname: Shepherd, Samantha organization: School of Applied Sciences, University of Huddersfield, Queensgate, Huddersfield HD1 3DH, UK – sequence: 9 givenname: Steve D. surname: Shnyder fullname: Shnyder, Steve D. organization: Institute of Cancer Therapeutics, University of Bradford, Bradford BD7 1DP, UK – sequence: 10 givenname: Ian J. surname: Stratford fullname: Stratford, Ian J. organization: Division of Pharmacy and Optometry, Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, UK – sequence: 11 givenname: Richard T. surname: Wheelhouse fullname: Wheelhouse, Richard T. organization: School of Pharmacy, University of Bradford, Bradford BD7 1DP, UK – sequence: 12 givenname: Charlotte E. surname: Willans fullname: Willans, Charlotte E. organization: School of Chemistry, University of Leeds, Woodhouse Lane, Leeds LS2 9JT, UK – sequence: 13 givenname: Roger M. surname: Phillips fullname: Phillips, Roger M. email: r.m.phillips@hud.ac.uk organization: School of Applied Sciences, University of Huddersfield, Queensgate, Huddersfield HD1 3DH, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28624622$$D View this record in MEDLINE/PubMed |
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| Copyright | 2017 Crown Copyright © 2017. Published by Elsevier B.V. All rights reserved. Copyright Elsevier Limited Sep 10, 2017 |
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| Keywords | Thioredoxin reductase inhibitor Silver-N-heterocyclic carbene PARP1 inhibitor Topoisomerase inhibitor Glycolytic inhibitor Silver- N-heterocyclic carbene |
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| Snippet | Organometallic complexes offer the prospect of targeting multiple pathways that are important in cancer biology. Here, the preclinical activity and... Abstract Organometallic complexes offer the prospect of targeting multiple pathways that are important in cancer biology. Here, the preclinical activity and... |
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| SubjectTerms | Antigens, Neoplasm - metabolism Antineoplastic Agents - chemistry Antineoplastic Agents - pharmacology Antineoplastic Agents - toxicity Antineoplastic Combined Chemotherapy Protocols - pharmacology Apoptosis Apoptosis - drug effects Cancer Cancer therapies Cell death Cell Line, Tumor Cell Survival - drug effects Cisplatin Cisplatin - pharmacology Cytotoxicity Dacarbazine - analogs & derivatives Dacarbazine - pharmacology Deoxyribonucleic acid DNA DNA Damage DNA repair DNA topoisomerase DNA Topoisomerases, Type I - metabolism DNA Topoisomerases, Type II - metabolism DNA-Binding Proteins - metabolism Dose-Response Relationship, Drug Drug Resistance, Neoplasm Drug Synergism Flow cytometry Glycolysis Glycolysis - drug effects Glycolytic inhibitor Gold Hematology, Oncology and Palliative Medicine Humans Imidazoles - chemistry Imidazoles - pharmacology Imidazoles - toxicity Inhibitory Concentration 50 Kinases Ligands Neoplasms - drug therapy Neoplasms - metabolism Neoplasms - pathology Organometallic complexes Organometallic Compounds - chemistry Organometallic Compounds - pharmacology Organometallic Compounds - toxicity Oxidative Stress - drug effects PARP1 inhibitor Poly (ADP-Ribose) Polymerase-1 - antagonists & inhibitors Poly (ADP-Ribose) Polymerase-1 - metabolism Poly(ADP-ribose) polymerase Poly(ADP-ribose) Polymerase Inhibitors - pharmacology Reactive oxygen species Reactive Oxygen Species - metabolism Reductase Signal Transduction - drug effects Silver Silver-N-heterocyclic carbene Temozolomide Thioredoxin Thioredoxin Reductase 1 - antagonists & inhibitors Thioredoxin Reductase 1 - metabolism Thioredoxin reductase inhibitor Topoisomerase I Inhibitors - pharmacology Topoisomerase II Inhibitors - pharmacology Topoisomerase inhibitor Tumors |
| Title | Preclinical anti-cancer activity and multiple mechanisms of action of a cationic silver complex bearing N-heterocyclic carbene ligands |
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