Tumour irradiation combined with vascular-targeted photodynamic therapy enhances antitumour effects in pre-clinical prostate cancer

Background There is a need to improve the treatment of prostate cancer (PCa) and reduce treatment side effects. Vascular-targeted photodynamic therapy (VTP) is a focal therapy for low-risk low-volume localised PCa, which rapidly disrupts targeted tumour vessels. There is interest in expanding the us...

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Published in:	British journal of cancer Vol. 125; no. 4; pp. 534 - 546
Main Authors:	Sjoberg, Hanna T., Philippou, Yiannis, Magnussen, Anette L., Tullis, Iain D. C., Bridges, Esther, Chatrian, Andrea, Lefebvre, Joel, Tam, Ka Ho, Murphy, Emma A., Rittscher, Jens, Preise, Dina, Agemy, Lilach, Yechezkel, Tamar, Smart, Sean C., Kinchesh, Paul, Gilchrist, Stuart, Allen, Danny P., Scheiblin, David A., Lockett, Stephen J., Wink, David A., Lamb, Alastair D., Mills, Ian G., Harris, Adrian, Muschel, Ruth J., Vojnovic, Boris, Scherz, Avigdor, Hamdy, Freddie C., Bryant, Richard J.
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 17.08.2021 Nature Publishing Group
Subjects:	631/67/1059/485 692/4028/546 Allografts Animals Biomedical and Life Sciences Biomedicine Cancer Research Cell Line, Tumor Clinical trials Combined Modality Therapy Dose Fractionation, Radiation Drug Resistance Epidemiology Human Umbilical Vein Endothelial Cells Humans Magnetic resonance imaging Male Mice Microenvironments Molecular Medicine Neovascularization, Pathologic - therapy Oncology Permeability Photochemotherapy - methods Photodynamic therapy Prostate cancer Prostatic Neoplasms - blood supply Prostatic Neoplasms - therapy Radiation therapy Survival Analysis Tumor Microenvironment Tumors Xenograft Model Antitumor Assays
ISSN:	0007-0920, 1532-1827, 1532-1827
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Abstract	Background There is a need to improve the treatment of prostate cancer (PCa) and reduce treatment side effects. Vascular-targeted photodynamic therapy (VTP) is a focal therapy for low-risk low-volume localised PCa, which rapidly disrupts targeted tumour vessels. There is interest in expanding the use of VTP to higher-risk disease. Tumour vasculature is characterised by vessel immaturity, increased permeability, aberrant branching and inefficient flow. FRT alters the tumour microenvironment and promotes transient ‘vascular normalisation’. We hypothesised that multimodality therapy combining fractionated radiotherapy (FRT) and VTP could improve PCa tumour control compared against monotherapy with FRT or VTP. Methods We investigated whether sequential delivery of FRT followed by VTP 7 days later improves flank TRAMP-C1 PCa tumour allograft control compared to monotherapy with FRT or VTP. Results FRT induced ‘vascular normalisation’ changes in PCa flank tumour allografts, improving vascular function as demonstrated using dynamic contrast-enhanced magnetic resonance imaging. FRT followed by VTP significantly delayed tumour growth in flank PCa allograft pre-clinical models, compared with monotherapy with FRT or VTP, and improved overall survival. Conclusion Combining FRT and VTP may be a promising multimodal approach in PCa therapy. This provides proof-of-concept for this multimodality treatment to inform early phase clinical trials.
AbstractList	There is a need to improve the treatment of prostate cancer (PCa) and reduce treatment side effects. Vascular-targeted photodynamic therapy (VTP) is a focal therapy for low-risk low-volume localised PCa, which rapidly disrupts targeted tumour vessels. There is interest in expanding the use of VTP to higher-risk disease. Tumour vasculature is characterised by vessel immaturity, increased permeability, aberrant branching and inefficient flow. FRT alters the tumour microenvironment and promotes transient 'vascular normalisation'. We hypothesised that multimodality therapy combining fractionated radiotherapy (FRT) and VTP could improve PCa tumour control compared against monotherapy with FRT or VTP.BACKGROUNDThere is a need to improve the treatment of prostate cancer (PCa) and reduce treatment side effects. Vascular-targeted photodynamic therapy (VTP) is a focal therapy for low-risk low-volume localised PCa, which rapidly disrupts targeted tumour vessels. There is interest in expanding the use of VTP to higher-risk disease. Tumour vasculature is characterised by vessel immaturity, increased permeability, aberrant branching and inefficient flow. FRT alters the tumour microenvironment and promotes transient 'vascular normalisation'. We hypothesised that multimodality therapy combining fractionated radiotherapy (FRT) and VTP could improve PCa tumour control compared against monotherapy with FRT or VTP.We investigated whether sequential delivery of FRT followed by VTP 7 days later improves flank TRAMP-C1 PCa tumour allograft control compared to monotherapy with FRT or VTP.METHODSWe investigated whether sequential delivery of FRT followed by VTP 7 days later improves flank TRAMP-C1 PCa tumour allograft control compared to monotherapy with FRT or VTP.FRT induced 'vascular normalisation' changes in PCa flank tumour allografts, improving vascular function as demonstrated using dynamic contrast-enhanced magnetic resonance imaging. FRT followed by VTP significantly delayed tumour growth in flank PCa allograft pre-clinical models, compared with monotherapy with FRT or VTP, and improved overall survival.RESULTSFRT induced 'vascular normalisation' changes in PCa flank tumour allografts, improving vascular function as demonstrated using dynamic contrast-enhanced magnetic resonance imaging. FRT followed by VTP significantly delayed tumour growth in flank PCa allograft pre-clinical models, compared with monotherapy with FRT or VTP, and improved overall survival.Combining FRT and VTP may be a promising multimodal approach in PCa therapy. This provides proof-of-concept for this multimodality treatment to inform early phase clinical trials.CONCLUSIONCombining FRT and VTP may be a promising multimodal approach in PCa therapy. This provides proof-of-concept for this multimodality treatment to inform early phase clinical trials. There is a need to improve the treatment of prostate cancer (PCa) and reduce treatment side effects. Vascular-targeted photodynamic therapy (VTP) is a focal therapy for low-risk low-volume localised PCa, which rapidly disrupts targeted tumour vessels. There is interest in expanding the use of VTP to higher-risk disease. Tumour vasculature is characterised by vessel immaturity, increased permeability, aberrant branching and inefficient flow. FRT alters the tumour microenvironment and promotes transient 'vascular normalisation'. We hypothesised that multimodality therapy combining fractionated radiotherapy (FRT) and VTP could improve PCa tumour control compared against monotherapy with FRT or VTP. We investigated whether sequential delivery of FRT followed by VTP 7 days later improves flank TRAMP-C1 PCa tumour allograft control compared to monotherapy with FRT or VTP. FRT induced 'vascular normalisation' changes in PCa flank tumour allografts, improving vascular function as demonstrated using dynamic contrast-enhanced magnetic resonance imaging. FRT followed by VTP significantly delayed tumour growth in flank PCa allograft pre-clinical models, compared with monotherapy with FRT or VTP, and improved overall survival. Combining FRT and VTP may be a promising multimodal approach in PCa therapy. This provides proof-of-concept for this multimodality treatment to inform early phase clinical trials. Background There is a need to improve the treatment of prostate cancer (PCa) and reduce treatment side effects. Vascular-targeted photodynamic therapy (VTP) is a focal therapy for low-risk low-volume localised PCa, which rapidly disrupts targeted tumour vessels. There is interest in expanding the use of VTP to higher-risk disease. Tumour vasculature is characterised by vessel immaturity, increased permeability, aberrant branching and inefficient flow. FRT alters the tumour microenvironment and promotes transient ‘vascular normalisation’. We hypothesised that multimodality therapy combining fractionated radiotherapy (FRT) and VTP could improve PCa tumour control compared against monotherapy with FRT or VTP. Methods We investigated whether sequential delivery of FRT followed by VTP 7 days later improves flank TRAMP-C1 PCa tumour allograft control compared to monotherapy with FRT or VTP. Results FRT induced ‘vascular normalisation’ changes in PCa flank tumour allografts, improving vascular function as demonstrated using dynamic contrast-enhanced magnetic resonance imaging. FRT followed by VTP significantly delayed tumour growth in flank PCa allograft pre-clinical models, compared with monotherapy with FRT or VTP, and improved overall survival. Conclusion Combining FRT and VTP may be a promising multimodal approach in PCa therapy. This provides proof-of-concept for this multimodality treatment to inform early phase clinical trials. BackgroundThere is a need to improve the treatment of prostate cancer (PCa) and reduce treatment side effects. Vascular-targeted photodynamic therapy (VTP) is a focal therapy for low-risk low-volume localised PCa, which rapidly disrupts targeted tumour vessels. There is interest in expanding the use of VTP to higher-risk disease. Tumour vasculature is characterised by vessel immaturity, increased permeability, aberrant branching and inefficient flow. FRT alters the tumour microenvironment and promotes transient ‘vascular normalisation’. We hypothesised that multimodality therapy combining fractionated radiotherapy (FRT) and VTP could improve PCa tumour control compared against monotherapy with FRT or VTP.MethodsWe investigated whether sequential delivery of FRT followed by VTP 7 days later improves flank TRAMP-C1 PCa tumour allograft control compared to monotherapy with FRT or VTP.ResultsFRT induced ‘vascular normalisation’ changes in PCa flank tumour allografts, improving vascular function as demonstrated using dynamic contrast-enhanced magnetic resonance imaging. FRT followed by VTP significantly delayed tumour growth in flank PCa allograft pre-clinical models, compared with monotherapy with FRT or VTP, and improved overall survival.ConclusionCombining FRT and VTP may be a promising multimodal approach in PCa therapy. This provides proof-of-concept for this multimodality treatment to inform early phase clinical trials.
Author	Rittscher, Jens Lockett, Stephen J. Chatrian, Andrea Scheiblin, David A. Murphy, Emma A. Gilchrist, Stuart Agemy, Lilach Mills, Ian G. Lamb, Alastair D. Sjoberg, Hanna T. Lefebvre, Joel Philippou, Yiannis Magnussen, Anette L. Tullis, Iain D. C. Vojnovic, Boris Kinchesh, Paul Hamdy, Freddie C. Wink, David A. Scherz, Avigdor Harris, Adrian Bryant, Richard J. Yechezkel, Tamar Muschel, Ruth J. Bridges, Esther Allen, Danny P. Smart, Sean C. Tam, Ka Ho Preise, Dina
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Oncol.2013321110.3389/fonc.2013.00211 MurataRSiemannDWOvergaardJHorsmanMRImproved tumor response by combining radiation and the vascular-damaging drug 5,6-dimethylxanthenone-4-acetic acidRadiat. Res.20011565035091:CAS:528:DC%2BD3MXosV2lurs%3D10.1667/0033-7587(2001)156[0503:ITRBCR]2.0.CO;2 Trachtenberg, J., Bogaards, A., Weersink, R. A., Haider, M. A., Evans, A., McCluskey, S. A. et al. Vascular targeted photodynamic therapy with palladium-bacteriopheophorbide photosensitizer for recurrent prostate cancer following definitive radiation therapy: assessment of safety and treatment response. J. Urol.178, 1974–1979 (2007). Alexandrov, L. B., Nik-Zainal, S., Wedge, D. C., Aparicio, S. DW Siemann (1450_CR55) 2002; 53 S Loeb (1450_CR10) 2007; 69 MC Schabel (1450_CR32) 2008; 53 HU Ahmed (1450_CR38) 2009; 18 1450_CR43 1450_CR42 1450_CR41 1450_CR40 1450_CR46 1450_CR45 1450_CR44 1450_CR49 L Li (1450_CR54) 1998; 42 1450_CR50 1450_CR51 1450_CR14 CM Moore (1450_CR39) 2009; 6 MT Park (1450_CR47) 2012; 53 1450_CR13 T Yamazaki (1450_CR34) 2018; 5 1450_CR12 1450_CR11 1450_CR18 1450_CR17 Y Philippou (1450_CR35) 2020; 17 1450_CR15 1450_CR59 1450_CR19 D Preise (1450_CR16) 2011; 10 HJ Park (1450_CR48) 2012; 177 WR Wilson (1450_CR56) 1998; 42 1450_CR21 DW Siemann (1450_CR57) 2003; 13 1450_CR20 1450_CR25 1450_CR22 1450_CR29 1450_CR28 CY Hsu (1450_CR7) 2010; 105 1450_CR27 1450_CR26 JF Ward (1450_CR9) 2005; 95 BS Carver (1450_CR5) 2006; 176 S Goel (1450_CR24) 2012; 2 HE Barker (1450_CR23) 2015; 15 R Murata (1450_CR58) 2001; 156 1450_CR31 1450_CR30 1450_CR36 1450_CR33 S Azzi (1450_CR52) 2013; 3 D Hanahan (1450_CR53) 2011; 144 1450_CR8 1450_CR37 1450_CR6 GD Grossfeld (1450_CR2) 2002; 60 1450_CR4 1450_CR3 1450_CR1
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Snippet	Background There is a need to improve the treatment of prostate cancer (PCa) and reduce treatment side effects. Vascular-targeted photodynamic therapy (VTP) is... There is a need to improve the treatment of prostate cancer (PCa) and reduce treatment side effects. Vascular-targeted photodynamic therapy (VTP) is a focal... BackgroundThere is a need to improve the treatment of prostate cancer (PCa) and reduce treatment side effects. Vascular-targeted photodynamic therapy (VTP) is...
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SubjectTerms	631/67/1059/485 692/4028/546 Allografts Animals Biomedical and Life Sciences Biomedicine Cancer Research Cell Line, Tumor Clinical trials Combined Modality Therapy Dose Fractionation, Radiation Drug Resistance Epidemiology Human Umbilical Vein Endothelial Cells Humans Magnetic resonance imaging Male Mice Microenvironments Molecular Medicine Neovascularization, Pathologic - therapy Oncology Permeability Photochemotherapy - methods Photodynamic therapy Prostate cancer Prostatic Neoplasms - blood supply Prostatic Neoplasms - therapy Radiation therapy Survival Analysis Tumor Microenvironment Tumors Xenograft Model Antitumor Assays
Title	Tumour irradiation combined with vascular-targeted photodynamic therapy enhances antitumour effects in pre-clinical prostate cancer
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