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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Vydáno v:	The Journal of clinical investigation Ročník 123; číslo 10; s. 4344 - 4358
Hlavní autoři:	Cheng, Joseph C., Bai, Aiping, Beckham, Thomas H., Marrison, S. Tucker, Yount, Caroline L., Young, Katherine, Lu, Ping, Bartlett, Anne M., Wu, Bill X., Keane, Barry J., Armeson, Kent E., Marshall, David T., Keane, Thomas E., Smith, Michael T., Jones, E. Ellen, Drake, Richard R., Bielawska, Alicja, Norris, James S., Liu, Xiang
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States American Society for Clinical Investigation 01.10.2013
Témata:	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 United States
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.
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
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24091326$$D View this record in MEDLINE/PubMed
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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 Authorship note: James S. Norris and Xiang Liu are co–senior authors.
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PublicationCentury	2000
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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StartPage	4344
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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