Tachpyridine, a metal chelator, induces G2 cell-cycle arrest, activates checkpoint kinases, and sensitizes cells to ionizing radiation
Iron is critical for cell growth and proliferation. Iron chelators are being explored for a number of clinical applications, including the treatment of neurodegenerative disorders, heart disease, and cancer. To uncover mechanisms of action of tachpyridine, a chelator currently undergoing preclinical...
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Published in | Blood Vol. 106; no. 9; pp. 3191 - 3199 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Washington, DC
Elsevier Inc
01.11.2005
The Americain Society of Hematology 2005 by The American Society of Hematology |
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Abstract | Iron is critical for cell growth and proliferation. Iron chelators are being explored for a number of clinical applications, including the treatment of neurodegenerative disorders, heart disease, and cancer. To uncover mechanisms of action of tachpyridine, a chelator currently undergoing preclinical evaluation as an anticancer agent, cell-cycle analysis was performed. Tachpyridine arrested cells at G2, a radiosensitive phase of the cell cycle, and enhanced the sensitivity of cancer cells but not nontransformed cells to ionizing radiation. G2 arrest was p53 independent and was accompanied by activation of the checkpoint kinases CHK1 and CHK2. G2 arrest was blocked by UCN-01, a CHK1 inhibitor, but proceeded in CHK2 knock-out cells, indicating a critical role for CHK1 in G2 arrest. Tachpyridine-induced cell-cycle arrest was abrogated in cells treated with caffeine, an inhibitor of the ataxia-telangiectasia mutated/ataxia-telangiectasia-mutated and Rad3-related (ATM/ATR) kinases. Further, G2 arrest proceeded in ATM-deficient cells but was blocked in ATR-deficient cells, implicating ATR as the proximal kinase in tachpyridine-mediated G2 arrest. Collectively, our results suggest that iron chelators may function as antitumor and radioenhancing agents and uncover a previously unexplored activity of iron chelators in activation of ATR and checkpoint kinases. |
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AbstractList | Iron is critical for cell growth and proliferation. Iron chelators are being explored for a number of clinical applications, including the treatment of neurodegenerative disorders, heart disease, and cancer. To uncover mechanisms of action of tachpyridine, a chelator currently undergoing preclinical evaluation as an anticancer agent, cell-cycle analysis was performed. Tachpyridine arrested cells at G2, a radiosensitive phase of the cell cycle, and enhanced the sensitivity of cancer cells but not nontransformed cells to ionizing radiation. G2 arrest was p53 independent and was accompanied by activation of the checkpoint kinases CHK1 and CHK2. G2 arrest was blocked by UCN-01, a CHK1 inhibitor, but proceeded in CHK2 knock-out cells, indicating a critical role for CHK1 in G2 arrest. Tachpyridine-induced cell-cycle arrest was abrogated in cells treated with caffeine, an inhibitor of the ataxia-telangiectasia mutated/ataxia-telangiectasia-mutated and Rad3-related (ATM/ATR) kinases. Further, G2 arrest proceeded in ATM-deficient cells but was blocked in ATR-deficient cells, implicating ATR as the proximal kinase in tachpyridine-mediated G2 arrest. Collectively, our results suggest that iron chelators may function as antitumor and radioenhancing agents and uncover a previously unexplored activity of iron chelators in activation of ATR and checkpoint kinases. Iron is critical for cell growth and proliferation. Iron chelators are being explored for a number of clinical applications, including the treatment of neurodegenerative disorders, heart disease, and cancer. To uncover mechanisms of action of tachpyridine, a chelator currently undergoing preclinical evaluation as an anticancer agent, cell-cycle analysis was performed. Tachpyridine arrested cells at G 2 , a radiosensitive phase of the cell cycle, and enhanced the sensitivity of cancer cells but not nontransformed cells to ionizing radiation. G 2 arrest was p53 independent and was accompanied by activation of the checkpoint kinases CHK1 and CHK2. G 2 arrest was blocked by UCN-01, a CHK1 inhibitor, but proceeded in CHK2 knock-out cells, indicating a critical role for CHK1 in G 2 arrest. Tachpyridine-induced cell-cycle arrest was abrogated in cells treated with caffeine, an inhibitor of the ataxia-telangiectasia mutated/ataxia-telangiectasia-mutated and Rad3 -related (ATM/ATR) kinases. Further, G 2 arrest proceeded in ATM-deficient cells but was blocked in ATR-deficient cells, implicating ATR as the proximal kinase in tachpyridine-mediated G 2 arrest. Collectively, our results suggest that iron chelators may function as antitumor and radioenhancing agents and uncover a previously unexplored activity of iron chelators in activation of ATR and checkpoint kinases. |
Author | Turner, JoLyn Beardsley, Dillon Torti, Suzy V. Koumenis, Constantinos Torti, Frank M. Cody, Brooke Brechbiel, Martin W. Brown, Kevin D. Kute, Timothy E. Planalp, Roy P. |
AuthorAffiliation | From the Department of Biochemistry, Wake Forest University Health Sciences; the Department of Radiation Biology, Wake Forest University Health Sciences; the Department of Pathology, Wake Forest University Health Sciences; the Department of Chemistry, University of New Hampshire, Durham, NH; the National Cancer Institute, Bethesda, MD; the Department of Biochemistry and Molecular Biology, University of Florida College of Medicine, Gainesville, FL; the Department of Cancer Biology, Wake Forest University Health Sciences; and the Comprehensive Cancer Center, Wake Forest University Health Sciences, Winston-Salem, NC |
AuthorAffiliation_xml | – name: From the Department of Biochemistry, Wake Forest University Health Sciences; the Department of Radiation Biology, Wake Forest University Health Sciences; the Department of Pathology, Wake Forest University Health Sciences; the Department of Chemistry, University of New Hampshire, Durham, NH; the National Cancer Institute, Bethesda, MD; the Department of Biochemistry and Molecular Biology, University of Florida College of Medicine, Gainesville, FL; the Department of Cancer Biology, Wake Forest University Health Sciences; and the Comprehensive Cancer Center, Wake Forest University Health Sciences, Winston-Salem, NC |
Author_xml | – sequence: 1 givenname: JoLyn surname: Turner fullname: Turner, JoLyn – sequence: 2 givenname: Constantinos surname: Koumenis fullname: Koumenis, Constantinos – sequence: 3 givenname: Timothy E. surname: Kute fullname: Kute, Timothy E. – sequence: 4 givenname: Roy P. surname: Planalp fullname: Planalp, Roy P. – sequence: 5 givenname: Martin W. surname: Brechbiel fullname: Brechbiel, Martin W. – sequence: 6 givenname: Dillon surname: Beardsley fullname: Beardsley, Dillon – sequence: 7 givenname: Brooke surname: Cody fullname: Cody, Brooke – sequence: 8 givenname: Kevin D. surname: Brown fullname: Brown, Kevin D. – sequence: 9 givenname: Frank M. surname: Torti fullname: Torti, Frank M. email: storti@wfubmc.edu – sequence: 10 givenname: Suzy V. surname: Torti fullname: Torti, Suzy V. |
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Copyright | 2005 American Society of Hematology 2006 INIST-CNRS 2005 by The American Society of Hematology 2005 |
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Keywords | Antineoplastic agent Human Checkpoint kinase Enzyme Transferases Iron Metal Biological activity Ionizing radiation Radiosensitizing agent Tachpyridine Kinase Cell cycle Chelating agent Mechanism of action |
Language | English |
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Notes | Reprints: Suzy V. Torti, Department of Biochemistry, Medical Center Blvd, Winston Salem, NC 27157; e-mail: storti@wfubmc.edu. The publication costs of this article were defrayed in part by page charge payment. Therefore, and solely to indicate this fact, this article is hereby marked “advertisement” in accordance with 18 U.S.C. section 1734. Prepublished online as Blood First Edition Paper, July 12, 2005; DOI 10.1182/blood-2005-03-1263. Supported by the National Institutes of Health (grant no. DK 57781) (S.V.T.); preclinical development of tachpyridine was supported by a grant from the National Cancer Institute (NCI) Rapid Access to Intervention Development (RAID) and the NCI Rapid Access to NCI Discovery Resources (RAND) programs of the National Institutes of Health (S.V.T.); and grant CA102289 (K.B.). |
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SubjectTerms | Antineoplastic agents Ataxia Telangiectasia Mutated Proteins Biological and medical sciences Cell Cycle Proteins - metabolism Cell Division - drug effects Cell Division - radiation effects Cell Line, Tumor Checkpoint Kinase 1 Checkpoint Kinase 2 Chelating Agents - pharmacology Chemotherapy Cyclohexylamines - pharmacology DNA-Binding Proteins - metabolism Enzyme Activation - drug effects Enzyme Activation - radiation effects G2 Phase - drug effects G2 Phase - radiation effects Humans Medical sciences Metals - antagonists & inhibitors Metals - metabolism Neoplasia Neoplasms - metabolism Neoplasms - pathology Pharmacology. Drug treatments Phosphorylation - drug effects Protein Kinases - metabolism Protein-Serine-Threonine Kinases - metabolism Pyridines - pharmacology Radiation, Ionizing Tumor Suppressor Protein p53 - deficiency Tumor Suppressor Protein p53 - genetics Tumor Suppressor Protein p53 - metabolism Tumor Suppressor Proteins - metabolism |
Title | Tachpyridine, a metal chelator, induces G2 cell-cycle arrest, activates checkpoint kinases, and sensitizes cells to ionizing radiation |
URI | https://dx.doi.org/10.1182/blood-2005-03-1263 https://www.ncbi.nlm.nih.gov/pubmed/16014567 https://pubmed.ncbi.nlm.nih.gov/PMC1895322 |
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