Caspase 3–mediated stimulation of tumor cell repopulation during cancer radiotherapy

Cytotoxic cancer therapy can induce accelerated growth of surviving cancer cells, a phenomenon known as tumor repopulation. This report uncovers a mechanism by which caspase 3 activation in treated cells promotes growth of surviving cells, mediated by iPLA 2 and PGE 2 . The level of caspase 3 activa...

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Vydané v:	Nature medicine Ročník 17; číslo 7; s. 860 - 866
Hlavní autori:	Huang, Qian, Li, Fang, Liu, Xinjian, Li, Wenrong, Shi, Wei, Liu, Fei-Fei, O'Sullivan, Brian, He, Zhimin, Peng, Yuanlin, Tan, Aik-Choon, Zhou, Ling, Shen, Jingping, Han, Gangwen, Wang, Xiao-Jing, Thorburn, Jackie, Thorburn, Andrew, Jimeno, Antonio, Raben, David, Bedford, Joel S, Li, Chuan-Yuan
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	New York Nature Publishing Group US 01.07.2011 Nature Publishing Group
Predmet:	631/67/1059/485 631/80/82/23 631/80/86 692/699/67 Animals Apoptosis Apoptosis - radiation effects Biomedical and Life Sciences Biomedicine Cancer Research Cancer therapies Caspase 3 - metabolism Caspase 3 - physiology Cell Death - physiology Cell Death - radiation effects Cell Line, Tumor Cell Proliferation Cytotoxicity Dinoprostone - metabolism Dinoprostone - physiology Group VI Phospholipases A2 - metabolism Health aspects Humans Infectious Diseases Metabolic Diseases Mice Molecular Medicine Mortality Neoplasms, Experimental - radiotherapy Neurosciences Physiological aspects Prostaglandins E Radiation therapy Radiotherapy Repopulation Tumors United States
ISSN:	1078-8956, 1546-170X, 1546-170X
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Abstract	Cytotoxic cancer therapy can induce accelerated growth of surviving cancer cells, a phenomenon known as tumor repopulation. This report uncovers a mechanism by which caspase 3 activation in treated cells promotes growth of surviving cells, mediated by iPLA 2 and PGE 2 . The level of caspase 3 activation in human tumors also correlates with risk of relapse, suggesting that this pathway may be a determinant of therapeutic effects. In cancer treatment, apoptosis is a well-recognized cell death mechanism through which cytotoxic agents kill tumor cells. Here we report that dying tumor cells use the apoptotic process to generate potent growth-stimulating signals to stimulate the repopulation of tumors undergoing radiotherapy. Furthermore, activated caspase 3, a key executioner in apoptosis, is involved in the growth stimulation. One downstream effector that caspase 3 regulates is prostaglandin E 2 (PGE 2 ), which can potently stimulate growth of surviving tumor cells. Deficiency of caspase 3 either in tumor cells or in tumor stroma caused substantial tumor sensitivity to radiotherapy in xenograft or mouse tumors. In human subjects with cancer, higher amounts of activated caspase 3 in tumor tissues are correlated with markedly increased rate of recurrence and death. We propose the existence of a cell death–induced tumor repopulation pathway in which caspase 3 has a major role.
AbstractList	In cancer treatment, apoptosis is a well-recognized cell death mechanism through which cytotoxic agents kill tumor cells. Here we report that dying tumor cells use the apoptotic process to generate potent growth-stimulating signals to stimulate the repopulation of tumors undergoing radiotherapy. Surprisingly, activated caspase 3, a key executioner of apoptosis, plays key roles in the growth stimulation. One downstream effector that caspase 3 regulates is prostaglandin E2, which can potently stimulates growth of surviving tumor cells. Deficiency of caspase 3 either in tumor cells or in tumor stroma caused significant tumor sensitivity to radiotherapy in xenograft or mouse tumors. In human cancer patients, higher levels of activated caspase 3 in tumor tissues are correlated with significantly increased rate of recurrence and deaths. We propose the existence of a “Phoenix Rising” pathway of cell death-induced tumor repopulation in which caspase 3 plays key roles. In cancer treatment, apoptosis is a well-recognized cell death mechanism through which cytotoxic agents kill tumor cells. Here we report that dying tumor cells use the apoptotic process to generate potent growth-stimulating signals to stimulate the repopulation of tumors undergoing radiotherapy. Furthermore, activated caspase 3, a key executioner in apoptosis, is involved in the growth stimulation. One downstream effector that caspase 3 regulates is prostaglandin E2 (PGE2), which can potently stimulate growth of surviving tumor cells. Deficiency of caspase 3 either in tumor cells or in tumor stroma caused substantial tumor sensitivity to radiotherapy in xenograft or mouse tumors. In human subjects with cancer, higher amounts of activated caspase 3 in tumor tissues are correlated with markedly increased rate of recurrence and death. We propose the existence of a cell death-induced tumor repopulation pathway in which caspase 3 has a major role. [PUBLICATION ABSTRACT] In cancer treatment, apoptosis is a well-recognized cell death mechanism through which cytotoxic agents kill tumor cells. Here we report that dying tumor cells use the apoptotic process to generate potent growth-stimulating signals to stimulate the repopulation of tumors undergoing radiotherapy. Furthermore, activated caspase 3, a key executioner in apoptosis, is involved in the growth stimulation. One downstream effector that caspase 3 regulates is prostaglandin E(2) (PGE(2)), which can potently stimulate growth of surviving tumor cells. Deficiency of caspase 3 either in tumor cells or in tumor stroma caused substantial tumor sensitivity to radiotherapy in xenograft or mouse tumors. In human subjects with cancer, higher amounts of activated caspase 3 in tumor tissues are correlated with markedly increased rate of recurrence and death. We propose the existence of a cell death-induced tumor repopulation pathway in which caspase 3 has a major role. Cytotoxic cancer therapy can induce accelerated growth of surviving cancer cells, a phenomenon known as tumor repopulation. This report uncovers a mechanism by which caspase 3 activation in treated cells promotes growth of surviving cells, mediated by iPLA 2 and PGE 2 . The level of caspase 3 activation in human tumors also correlates with risk of relapse, suggesting that this pathway may be a determinant of therapeutic effects. In cancer treatment, apoptosis is a well-recognized cell death mechanism through which cytotoxic agents kill tumor cells. Here we report that dying tumor cells use the apoptotic process to generate potent growth-stimulating signals to stimulate the repopulation of tumors undergoing radiotherapy. Furthermore, activated caspase 3, a key executioner in apoptosis, is involved in the growth stimulation. One downstream effector that caspase 3 regulates is prostaglandin E 2 (PGE 2 ), which can potently stimulate growth of surviving tumor cells. Deficiency of caspase 3 either in tumor cells or in tumor stroma caused substantial tumor sensitivity to radiotherapy in xenograft or mouse tumors. In human subjects with cancer, higher amounts of activated caspase 3 in tumor tissues are correlated with markedly increased rate of recurrence and death. We propose the existence of a cell death–induced tumor repopulation pathway in which caspase 3 has a major role. In cancer treatment, apoptosis is a well-recognized cell death mechanism through which cytotoxic agents kill tumor cells. Here we report that dying tumor cells use the apoptotic process to generate potent growth-stimulating signals to stimulate the repopulation of tumors undergoing radiotherapy. Furthermore, activated caspase 3, a key executioner in apoptosis, is involved in the growth stimulation. One downstream effector that caspase 3 regulates is prostaglandin E(2) (PGE(2)), which can potently stimulate growth of surviving tumor cells. Deficiency of caspase 3 either in tumor cells or in tumor stroma caused substantial tumor sensitivity to radiotherapy in xenograft or mouse tumors. In human subjects with cancer, higher amounts of activated caspase 3 in tumor tissues are correlated with markedly increased rate of recurrence and death. We propose the existence of a cell death-induced tumor repopulation pathway in which caspase 3 has a major role.In cancer treatment, apoptosis is a well-recognized cell death mechanism through which cytotoxic agents kill tumor cells. Here we report that dying tumor cells use the apoptotic process to generate potent growth-stimulating signals to stimulate the repopulation of tumors undergoing radiotherapy. Furthermore, activated caspase 3, a key executioner in apoptosis, is involved in the growth stimulation. One downstream effector that caspase 3 regulates is prostaglandin E(2) (PGE(2)), which can potently stimulate growth of surviving tumor cells. Deficiency of caspase 3 either in tumor cells or in tumor stroma caused substantial tumor sensitivity to radiotherapy in xenograft or mouse tumors. In human subjects with cancer, higher amounts of activated caspase 3 in tumor tissues are correlated with markedly increased rate of recurrence and death. We propose the existence of a cell death-induced tumor repopulation pathway in which caspase 3 has a major role. In cancer treatment, apoptosis is a well-recognized cell death mechanism through which cytotoxic agents kill tumor cells. Here we report that dying tumor cells use the apoptotic process to generate potent growth-stimulating signals to stimulate the repopulation of tumors undergoing radiotherapy. Furthermore, activated caspase 3, a key executioner in apoptosis, is involved in the growth stimulation. One downstream effector that caspase 3 regulates is prostaglandin [E.sub.2] ([PGE.sub.2]), which can potently stimulate growth of surviving tumor cells. Deficiency of caspase 3 either in tumor cells or in tumor stroma caused substantial tumor sensitivity to radiotherapy in xenograft or mouse tumors. In human subjects with cancer, higher amounts of activated caspase 3 in tumor tissues are correlated with markedly increased rate of recurrence and death. We propose the existence of a cell death-induced tumor repopulation pathway in which caspase 3 has a major role.
Audience	Academic
Author	Bedford, Joel S Shi, Wei Raben, David Li, Fang O'Sullivan, Brian Zhou, Ling Liu, Xinjian He, Zhimin Jimeno, Antonio Wang, Xiao-Jing Li, Wenrong Thorburn, Andrew Han, Gangwen Li, Chuan-Yuan Huang, Qian Liu, Fei-Fei Tan, Aik-Choon Peng, Yuanlin Thorburn, Jackie Shen, Jingping
AuthorAffiliation	8 Department of Pathology, University of Colorado School of Medicine, Aurora, Colorado, USA 4 Department of Radiation Oncology and Ontario Cancer Institute, Princess Margaret Hospital, University of Toronto, Toronto, Ontario, Canada 11 Department of Pharmacology, University of Colorado School of Medicine, Aurora, Colorado, USA 9 Head and Neck Cancer Research Program, University of Colorado Cancer Center, Aurora, Colorado, USA 7 Department of Surgery, Shanghai First People’s Branch Hospital, Shanghai, China 5 Department of Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, CO, USA 10 Charles S. Gates Center for Stem Cell and Regenerative Medicine, University of Colorado School of Medicine, Aurora, Colorado, USA 1 Experimental Research Center, First People’s Hospital, Shanghai Jiaotong University, Shanghai, China 6 Department of Medicine, University of Colorado School of Medicine, Aurora, Colorado, USA 2 Department of Radiation Oncology, University of Colorad
AuthorAffiliation_xml	– name: 9 Head and Neck Cancer Research Program, University of Colorado Cancer Center, Aurora, Colorado, USA – name: 3 National Laboratory of Oncogenes and Related Genes Research, Cancer Institute, Shanghai Jiaotong University, Shanghai, China – name: 7 Department of Surgery, Shanghai First People’s Branch Hospital, Shanghai, China – name: 6 Department of Medicine, University of Colorado School of Medicine, Aurora, Colorado, USA – name: 10 Charles S. Gates Center for Stem Cell and Regenerative Medicine, University of Colorado School of Medicine, Aurora, Colorado, USA – name: 2 Department of Radiation Oncology, University of Colorado School of Medicine, Aurora, Colorado, USA – name: 11 Department of Pharmacology, University of Colorado School of Medicine, Aurora, Colorado, USA – name: 4 Department of Radiation Oncology and Ontario Cancer Institute, Princess Margaret Hospital, University of Toronto, Toronto, Ontario, Canada – name: 8 Department of Pathology, University of Colorado School of Medicine, Aurora, Colorado, USA – name: 1 Experimental Research Center, First People’s Hospital, Shanghai Jiaotong University, Shanghai, China – name: 5 Department of Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, CO, USA
Author_xml	– sequence: 1 givenname: Qian surname: Huang fullname: Huang, Qian organization: Experimental Research Center, First People's Hospital, Shanghai Jiao Tong University, Department of Radiation Oncology, University of Colorado School of Medicine, National Laboratory of Oncogenes and Related Genes Research, Cancer Institute, Shanghai Jiao Tong University – sequence: 2 givenname: Fang surname: Li fullname: Li, Fang organization: Department of Radiation Oncology, University of Colorado School of Medicine – sequence: 3 givenname: Xinjian surname: Liu fullname: Liu, Xinjian organization: Department of Radiation Oncology, University of Colorado School of Medicine – sequence: 4 givenname: Wenrong surname: Li fullname: Li, Wenrong organization: Department of Radiation Oncology, University of Colorado School of Medicine – sequence: 5 givenname: Wei surname: Shi fullname: Shi, Wei organization: Department of Radiation Oncology and Ontario Cancer Institute, Princess Margaret Hospital, University of Toronto – sequence: 6 givenname: Fei-Fei surname: Liu fullname: Liu, Fei-Fei organization: Department of Radiation Oncology and Ontario Cancer Institute, Princess Margaret Hospital, University of Toronto – sequence: 7 givenname: Brian surname: O'Sullivan fullname: O'Sullivan, Brian organization: Department of Radiation Oncology and Ontario Cancer Institute, Princess Margaret Hospital, University of Toronto – sequence: 8 givenname: Zhimin surname: He fullname: He, Zhimin organization: Department of Radiation Oncology, University of Colorado School of Medicine – sequence: 9 givenname: Yuanlin surname: Peng fullname: Peng, Yuanlin organization: Department of Environmental and Radiological Health Sciences, Colorado State University – sequence: 10 givenname: Aik-Choon surname: Tan fullname: Tan, Aik-Choon organization: Department of Medicine, University of Colorado School of Medicine – sequence: 11 givenname: Ling surname: Zhou fullname: Zhou, Ling organization: Department of Surgery, Shanghai First People's Branch Hospital – sequence: 12 givenname: Jingping surname: Shen fullname: Shen, Jingping organization: Department of Radiation Oncology, University of Colorado School of Medicine – sequence: 13 givenname: Gangwen surname: Han fullname: Han, Gangwen organization: Department of Pathology, University of Colorado School of Medicine – sequence: 14 givenname: Xiao-Jing surname: Wang fullname: Wang, Xiao-Jing organization: Department of Pathology, University of Colorado School of Medicine, Head and Neck Cancer Research Program, University of Colorado Cancer Center, Charles C. Gates Center for Regenerative Medicine and Stem Cell Biology, University of Colorado School of Medicine – sequence: 15 givenname: Jackie surname: Thorburn fullname: Thorburn, Jackie organization: Department of Pharmacology, University of Colorado School of Medicine – sequence: 16 givenname: Andrew surname: Thorburn fullname: Thorburn, Andrew organization: Department of Pharmacology, University of Colorado School of Medicine – sequence: 17 givenname: Antonio surname: Jimeno fullname: Jimeno, Antonio organization: Department of Medicine, University of Colorado School of Medicine, Head and Neck Cancer Research Program, University of Colorado Cancer Center, Charles C. Gates Center for Regenerative Medicine and Stem Cell Biology, University of Colorado School of Medicine – sequence: 18 givenname: David surname: Raben fullname: Raben, David organization: Department of Radiation Oncology, University of Colorado School of Medicine, Head and Neck Cancer Research Program, University of Colorado Cancer Center – sequence: 19 givenname: Joel S surname: Bedford fullname: Bedford, Joel S organization: Department of Environmental and Radiological Health Sciences, Colorado State University – sequence: 20 givenname: Chuan-Yuan surname: Li fullname: Li, Chuan-Yuan email: chuan.li@ucdenver.edu organization: Department of Radiation Oncology, University of Colorado School of Medicine, Charles C. Gates Center for Regenerative Medicine and Stem Cell Biology, University of Colorado School of Medicine, Department of Pharmacology, University of Colorado School of Medicine
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/21725296$$D View this record in MEDLINE/PubMed
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ContentType	Journal Article
Copyright	Springer Nature America, Inc. 2011 COPYRIGHT 2011 Nature Publishing Group Copyright Nature Publishing Group Jul 2011
Copyright_xml	– notice: Springer Nature America, Inc. 2011 – notice: COPYRIGHT 2011 Nature Publishing Group – notice: Copyright Nature Publishing Group Jul 2011
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Notes	ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 These authors contributed equally to this study. Author Contributions Q.H. and F.L. designed and conducted most of the experiments, analyzed data, and wrote the manuscript. X.L. and W.L. carried out analyses on modes of cell death in irradiated cells; W.S. carried out IHC analysis of human head and neck tumor samples; F.L. and B.O. provided human HNC samples and analyzed data from the samples; Z.H. conducted some of the caspase reporter experiments; Y.P. carried out arachidonic acid release experiments and J.S.B. analyzed relevant data of AA release; A-C.T. carried out data analyses of human clinical data; G.H. and X.W. helped with IHC analysis of murine tumor samples; J.S. constructed some of the plasmids used; A.J. and D.R. provided human head and neck tumor samples; L.Z. carried out IHC analysis of human breast cancer samples; J.T. and A.T. helped to conduct experiments on autophagy and necrosis; C.L. conceived the study, analyzed data, and wrote the manuscript. All authors read and agreed on the final manuscript.
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Snippet	Cytotoxic cancer therapy can induce accelerated growth of surviving cancer cells, a phenomenon known as tumor repopulation. This report uncovers a mechanism by... In cancer treatment, apoptosis is a well-recognized cell death mechanism through which cytotoxic agents kill tumor cells. Here we report that dying tumor cells...
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SubjectTerms	631/67/1059/485 631/80/82/23 631/80/86 692/699/67 Animals Apoptosis Apoptosis - radiation effects Biomedical and Life Sciences Biomedicine Cancer Research Cancer therapies Caspase 3 - metabolism Caspase 3 - physiology Cell Death - physiology Cell Death - radiation effects Cell Line, Tumor Cell Proliferation Cytotoxicity Dinoprostone - metabolism Dinoprostone - physiology Group VI Phospholipases A2 - metabolism Health aspects Humans Infectious Diseases Metabolic Diseases Mice Molecular Medicine Mortality Neoplasms, Experimental - radiotherapy Neurosciences Physiological aspects Prostaglandins E Radiation therapy Radiotherapy Repopulation Tumors
Title	Caspase 3–mediated stimulation of tumor cell repopulation during cancer radiotherapy
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