Radiation-induced acid ceramidase confers prostate cancer resistance and tumor relapse
Escape of prostate cancer (PCa) cells from ionizing radiation-induced (IR-induced) killing leads to disease progression and cancer relapse. The influence of sphingolipids, such as ceramide and its metabolite sphingosine 1-phosphate, on signal transduction pathways under cell stress is important to s...
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| Published in: | The Journal of clinical investigation Vol. 123; no. 10; pp. 4344 - 4358 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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United States
American Society for Clinical Investigation
01.10.2013
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| ISSN: | 0021-9738, 1558-8238, 1558-8238 |
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| Abstract | Escape of prostate cancer (PCa) cells from ionizing radiation-induced (IR-induced) killing leads to disease progression and cancer relapse. The influence of sphingolipids, such as ceramide and its metabolite sphingosine 1-phosphate, on signal transduction pathways under cell stress is important to survival adaptation responses. In this study, we demonstrate that ceramide-deacylating enzyme acid ceramidase (AC) was preferentially upregulated in irradiated PCa cells. Radiation-induced AC gene transactivation by activator protein 1 (AP-1) binding on the proximal promoter was sensitive to inhibition of de novo ceramide biosynthesis, as demonstrated by promoter reporter and ChIP-qPCR analyses. Our data indicate that a protective feedback mechanism mitigates the apoptotic effect of IR-induced ceramide generation. We found that deregulation of c-Jun induced marked radiosensitization in vivo and in vitro, which was rescued by ectopic AC overexpression. AC overexpression in PCa clonogens that survived a fractionated 80-Gy IR course was associated with increased radioresistance and proliferation, suggesting a role for AC in radiotherapy failure and relapse. Immunohistochemical analysis of human PCa tissues revealed higher levels of AC after radiotherapy failure than those in therapy-naive PCa, prostatic intraepithelial neoplasia, or benign tissues. Addition of an AC inhibitor to an animal model of xenograft irradiation produced radiosensitization and prevention of relapse. These data indicate that AC is a potentially tractable target for adjuvant radiotherapy. |
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| AbstractList | Escape of prostate cancer (PCa) cells from ionizing radiation-induced (IR-induced) killing leads to disease progression and cancer relapse. The influence of sphingolipids, such as ceramide and its metabolite sphingosine 1-phosphate, on signal transduction pathways under cell stress is important to survival adaptation responses. In this study, we demonstrate that ceramide-deacylating enzyme acid ceramidase (AC) was preferentially upregulated in irradiated PCa cells. Radiation-induced AC gene transactivation by activator protein 1 (AP-1) binding on the proximal promoter was sensitive to inhibition of de novo ceramide biosynthesis, as demonstrated by promoter reporter and ChIP-qPCR analyses. Our data indicate that a protective feedback mechanism mitigates the apoptotic effect of IR-induced ceramide generation. We found that deregulation of c-Jun induced marked radiosensitization in vivo and in vitro, which was rescued by ectopic AC overexpression. AC overexpression in PCa clonogens that survived a fractionated 80-Gy IR course was associated with increased radioresistance and proliferation, suggesting a role for AC in radiotherapy failure and relapse. Immunohistochemical analysis of human PCa tissues revealed higher levels of AC after radiotherapy failure than those in therapy-naive PCa, prostatic intraepithelial neoplasia, or benign tissues. Addition of an AC inhibitor to an animal model of xenograft irradiation produced radiosensitization and prevention of relapse. These data indicate that AC is a potentially tractable target for adjuvant radiotherapy.Escape of prostate cancer (PCa) cells from ionizing radiation-induced (IR-induced) killing leads to disease progression and cancer relapse. The influence of sphingolipids, such as ceramide and its metabolite sphingosine 1-phosphate, on signal transduction pathways under cell stress is important to survival adaptation responses. In this study, we demonstrate that ceramide-deacylating enzyme acid ceramidase (AC) was preferentially upregulated in irradiated PCa cells. Radiation-induced AC gene transactivation by activator protein 1 (AP-1) binding on the proximal promoter was sensitive to inhibition of de novo ceramide biosynthesis, as demonstrated by promoter reporter and ChIP-qPCR analyses. Our data indicate that a protective feedback mechanism mitigates the apoptotic effect of IR-induced ceramide generation. We found that deregulation of c-Jun induced marked radiosensitization in vivo and in vitro, which was rescued by ectopic AC overexpression. AC overexpression in PCa clonogens that survived a fractionated 80-Gy IR course was associated with increased radioresistance and proliferation, suggesting a role for AC in radiotherapy failure and relapse. Immunohistochemical analysis of human PCa tissues revealed higher levels of AC after radiotherapy failure than those in therapy-naive PCa, prostatic intraepithelial neoplasia, or benign tissues. Addition of an AC inhibitor to an animal model of xenograft irradiation produced radiosensitization and prevention of relapse. These data indicate that AC is a potentially tractable target for adjuvant radiotherapy. Escape of prostate cancer (PCa) cells from ionizing radiation–induced (IR-induced) killing leads to disease progression and cancer relapse. The influence of sphingolipids, such as ceramide and its metabolite sphingosine 1-phosphate, on signal transduction pathways under cell stress is important to survival adaptation responses. In this study, we demonstrate that ceramide-deacylating enzyme acid ceramidase (AC) was preferentially upregulated in irradiated PCa cells. Radiation-induced AC gene transactivation by activator protein 1 (AP-1) binding on the proximal promoter was sensitive to inhibition of de novo ceramide biosynthesis, as demonstrated by promoter reporter and ChIP-qPCR analyses. Our data indicate that a protective feedback mechanism mitigates the apoptotic effect of IR-induced ceramide generation. We found that deregulation of c-Jun induced marked radiosensitization in vivo and in vitro, which was rescued by ectopic AC overexpression. AC overexpression in PCa clonogens that survived a fractionated 80-Gy IR course was associated with increased radioresistance and proliferation, suggesting a role for AC in radiotherapy failure and relapse. Immunohistochemical analysis of human PCa tissues revealed higher levels of AC after radiotherapy failure than those in therapy-naive PCa, prostatic intraepithelial neoplasia, or benign tissues. Addition of an AC inhibitor to an animal model of xenograft irradiation produced radiosensitization and prevention of relapse. These data indicate that AC is a potentially tractable target for adjuvant radiotherapy. Escape of prostate cancer (PCa) cells from ionizing radiation-induced (IR-induced) killing leads to disease progression and cancer relapse. The influence of sphingolipids, such as ceramide and its metabolite sphingosine 1-phosphate, on signal transduction pathways under cell stress is important to survival adaptation responses. In this study, the authors have demonstrated that, ceramide-deacylating enzyme acid ceramidase (AC) was preferentially upregulated in irradiated PCa cells. Radiation-induced AC gene transactivation by activator protein 1 binding on the proximal promoter was sensitive to inhibition of de novo ceramide biosynthesis, as demonstrated by promoter reporter and ChIP-qPCR analyses. They found that deregulation of c-Jun induced marked radiosensitization in vivo and in vitro, which was rescued by ectopic AC overexpression. AC overexpression in PCa clonogens that survived a fractionated 80-Gy IR course was associated with increased radioresistance and proliferation, suggesting a role for AC in radiotherapy failure and relapse. Immunohistochemical analysis of human PCa tissues revealed higher levels of AC after radiotherapy failure than those in therapy-naive PCa, prostatic intraepithelial neoplasia, or benign tissues. |
| Audience | Academic |
| Author | Wu, Bill X. Liu, Xiang Yount, Caroline L. Bai, Aiping Keane, Barry J. Beckham, Thomas H. Marrison, S. Tucker Jones, E. Ellen Drake, Richard R. Cheng, Joseph C. Armeson, Kent E. Marshall, David T. Bielawska, Alicja Bartlett, Anne M. Keane, Thomas E. Norris, James S. Young, Katherine Smith, Michael T. Lu, Ping |
| AuthorAffiliation | 1 Department of Microbiology and Immunology, 2 Department of Biochemistry, 3 Department of Radiation Oncology, 4 Department of Pathology and Laboratory Medicine, 5 Department of Biostatistics and Epidemiology, 6 Department of Urology, and 7 Department of Pharmacology, Medical University of South Carolina, Charleston, South Carolina, USA |
| AuthorAffiliation_xml | – name: 1 Department of Microbiology and Immunology, 2 Department of Biochemistry, 3 Department of Radiation Oncology, 4 Department of Pathology and Laboratory Medicine, 5 Department of Biostatistics and Epidemiology, 6 Department of Urology, and 7 Department of Pharmacology, Medical University of South Carolina, Charleston, South Carolina, USA |
| Author_xml | – sequence: 1 givenname: Joseph C. surname: Cheng fullname: Cheng, Joseph C. – sequence: 2 givenname: Aiping surname: Bai fullname: Bai, Aiping – sequence: 3 givenname: Thomas H. surname: Beckham fullname: Beckham, Thomas H. – sequence: 4 givenname: S. Tucker surname: Marrison fullname: Marrison, S. Tucker – sequence: 5 givenname: Caroline L. surname: Yount fullname: Yount, Caroline L. – sequence: 6 givenname: Katherine surname: Young fullname: Young, Katherine – sequence: 7 givenname: Ping surname: Lu fullname: Lu, Ping – sequence: 8 givenname: Anne M. surname: Bartlett fullname: Bartlett, Anne M. – sequence: 9 givenname: Bill X. surname: Wu fullname: Wu, Bill X. – sequence: 10 givenname: Barry J. surname: Keane fullname: Keane, Barry J. – sequence: 11 givenname: Kent E. surname: Armeson fullname: Armeson, Kent E. – sequence: 12 givenname: David T. surname: Marshall fullname: Marshall, David T. – sequence: 13 givenname: Thomas E. surname: Keane fullname: Keane, Thomas E. – sequence: 14 givenname: Michael T. surname: Smith fullname: Smith, Michael T. – sequence: 15 givenname: E. Ellen surname: Jones fullname: Jones, E. Ellen – sequence: 16 givenname: Richard R. surname: Drake fullname: Drake, Richard R. – sequence: 17 givenname: Alicja surname: Bielawska fullname: Bielawska, Alicja – sequence: 18 givenname: James S. surname: Norris fullname: Norris, James S. – sequence: 19 givenname: Xiang surname: Liu fullname: Liu, Xiang |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24091326$$D View this record in MEDLINE/PubMed |
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| PublicationDate | 2013-10-01 |
| PublicationDateYYYYMMDD | 2013-10-01 |
| PublicationDate_xml | – month: 10 year: 2013 text: 2013-10-01 day: 01 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States – name: Ann Arbor |
| PublicationTitle | The Journal of clinical investigation |
| PublicationTitleAlternate | J Clin Invest |
| PublicationYear | 2013 |
| Publisher | American Society for Clinical Investigation |
| Publisher_xml | – name: American Society for Clinical Investigation |
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| Snippet | Escape of prostate cancer (PCa) cells from ionizing radiation-induced (IR-induced) killing leads to disease progression and cancer relapse. The influence of... Escape of prostate cancer (PCa) cells from ionizing radiation–induced (IR-induced) killing leads to disease progression and cancer relapse. The influence of... |
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| SubjectTerms | Acid Ceramidase - antagonists & inhibitors Acid Ceramidase - genetics Acid Ceramidase - metabolism Amides - administration & dosage Amides - pharmacology Animals Biomedical research Cancer therapies Care and treatment Cell culture Cell Line, Tumor Enzyme Induction - radiation effects Enzymes Gene Expression Gene Expression Regulation, Neoplastic - radiation effects Genetic aspects Humans Hydrolases Injections, Intraperitoneal Ionizing radiation Kinases Male Mice Mice, Nude Neoplasm Recurrence, Local - enzymology Neoplasm Recurrence, Local - prevention & control Promoter Regions, Genetic Propanolamines - administration & dosage Propanolamines - pharmacology Properties Prostate cancer Prostatic Neoplasms - enzymology Prostatic Neoplasms - pathology Prostatic Neoplasms - radiotherapy Protein Binding Proteins Proto-Oncogene Proteins c-jun - metabolism Radiation therapy Radiation Tolerance Radiation-Sensitizing Agents - administration & dosage Radiation-Sensitizing Agents - pharmacology Radiotherapy Sphingolipids - metabolism Studies Transcription Factor AP-1 - metabolism Transcriptional Activation - radiation effects Tumors Xenograft Model Antitumor Assays |
| Title | Radiation-induced acid ceramidase confers prostate cancer resistance and tumor relapse |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/24091326 https://www.proquest.com/docview/1448810072 https://www.proquest.com/docview/1443404882 https://www.proquest.com/docview/1500779937 https://pubmed.ncbi.nlm.nih.gov/PMC3784522 |
| Volume | 123 |
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