Synergistically Enhancing the Therapeutic Effect of Radiation Therapy with Radiation Activatable and Reactive Oxygen Species-Releasing Nanostructures

Cheng, Kai; Sano, Michael; Jenkins, Cesare H.; Zhang, Guanglei; Vernekohl, Don; Zhao, Wei; Wei, Chenxi; Zhang, Yan; Zhang, Zhe; Liu, Yijin; Cheng, Zhen; Xing, Lei

doi:10.1021/acsnano.8b02038

Title: Synergistically Enhancing the Therapeutic Effect of Radiation Therapy with Radiation Activatable and Reactive Oxygen Species-Releasing Nanostructures

Journal Article · Tue Apr 24 00:00:00 EDT 2018 · ACS Nano

DOI:https://doi.org/10.1021/acsnano.8b02038· OSTI ID:1461481

Cheng, Kai ^[1]; Sano, Michael ^[1]; Jenkins, Cesare H. ^[1]; Zhang, Guanglei ^[1]; Vernekohl, Don ^[1]; Zhao, Wei ^[1]; Wei, Chenxi ^[2]; Zhang, Yan ^[2]; Zhang, Zhe ^[3];

^[2];

^[3];

^[1]

Stanford Univ., CA (United States). Dept. of Radiation Oncology, School of Medicine
SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Stanford Univ., CA (United States). Molecular Imaging Program at Stanford (MIPS) and Dept. of Radiology

Nanoparticle-based radio-sensitizers can amplify the effects of radiation therapy on tumor tissue even at relatively low concentrations while reducing the potential side effects to healthy surrounding tissues. In this study, we investigated a hybrid anisotropic nanostructure, composed of gold (Au) and titanium dioxide TiO₂, as a radio-sensitizer for radiation therapy of triple negative breast cancer (TNBC). In contrast to other gold-based radio sensitizers, dumbbell-like Au-TiO₂ nanoparticles (DATs) show a synergistic therapeutic effect on radiation therapy, mainly because of strong asymmetric electric coupling between the high atomic number metals and dielectric oxides at their interfaces. The generation of secondary electrons and reactive oxygen species (ROS) from DATs triggered by X-ray irradiation can significantly enhance the radiation effect. After endocytosed by cancer cells, DATs can generate a large amount of ROS under X-ray irradiation, eventually inducing cancer cell apoptosis. Significant tumor growth suppression and overall improvement in survival rate in a TNBC tumor model have been successfully demonstrated under DATs uptake for a radio-sensitized radiation therapy.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1461481

Journal Information:: ACS Nano, Vol. 12, Issue 5; ISSN 1936-0851

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 76 works

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References (40)

Strategies to improve radiotherapy with targeted drugs Begg, Adrian C.; Stewart, Fiona A.; Vens, Conchita Nature Reviews Cancer, Vol. 11, Issue 4 https://doi.org/10.1038/nrc3007	journal	March 2011
Ultrahigh dose-rate FLASH irradiation increases the differential response between normal and tumor tissue in mice Favaudon, V.; Caplier, L.; Monceau, V. Science Translational Medicine, Vol. 6, Issue 245 https://doi.org/10.1126/scitranslmed.3008973	journal	July 2014
Radiation therapy primes tumors for nanotherapeutic delivery via macrophage-mediated vascular bursts Miller, Miles A.; Chandra, Ravi; Cuccarese, Michael F. Science Translational Medicine, Vol. 9, Issue 392 https://doi.org/10.1126/scitranslmed.aal0225	journal	May 2017
Cancer Nanomedicine: From Drug Delivery to Imaging Chow, E. K. -H.; Ho, D. Science Translational Medicine, Vol. 5, Issue 216 https://doi.org/10.1126/scitranslmed.3005872	journal	December 2013
Nanoparticles for Radiation Therapy Enhancement: the Key Parameters Retif, Paul; Pinel, Sophie; Toussaint, Magali Theranostics, Vol. 5, Issue 9 https://doi.org/10.7150/thno.11642	journal	January 2015
Scintillating Nanoparticles as Energy Mediators for Enhanced Photodynamic Therapy Kamkaew, Anyanee; Chen, Feng; Zhan, Yonghua ACS Nano, Vol. 10, Issue 4 https://doi.org/10.1021/acsnano.6b01401	journal	April 2016
Nanoparticles in radiation oncology: From bench-side to bedside Rancoule, Chloé; Magné, Nicolas; Vallard, Alexis Cancer Letters, Vol. 375, Issue 2 https://doi.org/10.1016/j.canlet.2016.03.011	journal	June 2016
Key clinical beam parameters for nanoparticle-mediated radiation dose amplification Detappe, Alexandre; Kunjachan, Sijumon; Drané, Pascal Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34040	journal	September 2016
Roadmap to Clinical Use of Gold Nanoparticles for Radiation Sensitization Schuemann, Jan; Berbeco, Ross; Chithrani, Devika B. International Journal of Radiation OncologyBiologyPhysics, Vol. 94, Issue 1 https://doi.org/10.1016/j.ijrobp.2015.09.032	journal	January 2016
Harnessing the Power of Nanotechnology for Enhanced Radiation Therapy Goel, Shreya; Ni, Dalong; Cai, Weibo ACS Nano, Vol. 11, Issue 6 https://doi.org/10.1021/acsnano.7b03675	journal	May 2017
Nanoscale Energy Deposition by X-ray Absorbing Nanostructures Carter, Joshua D.; Cheng, Neal N.; Qu, Yongquan The Journal of Physical Chemistry B, Vol. 111, Issue 40 https://doi.org/10.1021/jp075253u	journal	October 2007
X-ray-Induced Energy Transfer between Nanomaterials under X-ray Irradiation Sharmah, Arjun; Yao, Zi; Lu, Lei The Journal of Physical Chemistry C, Vol. 120, Issue 5 https://doi.org/10.1021/acs.jpcc.5b11859	journal	February 2016
Multiplication Algorithm for Combined Physical and Chemical Enhancement of X-ray Effect by Nanomaterials Davidson, R. Andrew; Guo, Ting The Journal of Physical Chemistry C, Vol. 119, Issue 33 https://doi.org/10.1021/acs.jpcc.5b05309	journal	August 2015
Chemical Enhancement by Nanomaterials under X-ray Irradiation Cheng, Neal N.; Starkewolf, Zane; Davidson, R. Andrew Journal of the American Chemical Society, Vol. 134, Issue 4 https://doi.org/10.1021/ja210239k	journal	January 2012
Designing Core–Shell Gold and Selenium Nanocomposites for Cancer Radiochemotherapy Chang, Yanzhou; He, Lizhen; Li, Zhibin ACS Nano, Vol. 11, Issue 5 https://doi.org/10.1021/acsnano.7b01346	journal	April 2017
Construction and Validation of Nano Gold Tripods for Molecular Imaging of Living Subjects Cheng, Kai; Kothapalli, Sri-Rajasekhar; Liu, Hongguang Journal of the American Chemical Society, Vol. 136, Issue 9 https://doi.org/10.1021/ja412001e	journal	February 2014
Janus Au-TiO ₂ Photocatalysts with Strong Localization of Plasmonic Near-Fields for Efficient Visible-Light Hydrogen Generation Seh, Zhi Wei; Liu, Shuhua; Low, Michelle Advanced Materials, Vol. 24, Issue 17 https://doi.org/10.1002/adma.201104241	journal	March 2012
Anisotropic Growth of Titania onto Various Gold Nanostructures: Synthesis, Theoretical Understanding, and Optimization for Catalysis Seh, Zhi Wei; Liu, Shuhua; Zhang, Shuang-Yuan Angewandte Chemie International Edition, Vol. 50, Issue 43 https://doi.org/10.1002/anie.201104943	journal	September 2011
Titania-Coated Metal Nanostructures Seh, Zhi Wei; Liu, Shuhua; Han, Ming-Yong Chemistry - An Asian Journal, Vol. 7, Issue 10 https://doi.org/10.1002/asia.201200265	journal	June 2012
Titanium and Zinc Oxide Nanoparticles Are Proton-Coupled Electron Transfer Agents Schrauben, J. N.; Hayoun, R.; Valdez, C. N. Science, Vol. 336, Issue 6086 https://doi.org/10.1126/science.1220234	journal	June 2012
Titania supported gold nanoparticles as photocatalyst Primo, Ana; Corma, Avelino; García, Hermenegildo Phys. Chem. Chem. Phys., Vol. 13, Issue 3 https://doi.org/10.1039/C0CP00917B	journal	January 2011
Breaking the depth dependency of phototherapy with Cerenkov radiation and low-radiance-responsive nanophotosensitizers Kotagiri, Nalinikanth; Sudlow, Gail P.; Akers, Walter J. Nature Nanotechnology, Vol. 10, Issue 4 https://doi.org/10.1038/nnano.2015.17	journal	March 2015
Dual-Wavelength Irradiation and Dox Delivery for Cancer Cell Ablation with Photocatalytic Pr Doped TiO ₂ /NGO Hybrid Nanocomposite Jang, Hongje; Choi, Myung-Ho; Yim, Yeajee Advanced Healthcare Materials, Vol. 4, Issue 12 https://doi.org/10.1002/adhm.201500157	journal	June 2015
UV-Emitting Upconversion-Based TiO ₂ Photosensitizing Nanoplatform: Near-Infrared Light Mediated in Vivo Photodynamic Therapy via Mitochondria-Involved Apoptosis Pathway Hou, Zhiyao; Zhang, Yuanxin; Deng, Kerong ACS Nano, Vol. 9, Issue 3 https://doi.org/10.1021/nn506107c	journal	February 2015
Titania Coated Upconversion Nanoparticles for Near-Infrared Light Triggered Photodynamic Therapy Lucky, Sasidharan Swarnalatha; Muhammad Idris, Niagara; Li, Zhengquan ACS Nano, Vol. 9, Issue 1 https://doi.org/10.1021/nn503450t	journal	January 2015
Anisotropic Growth of TiO ₂ onto Gold Nanorods for Plasmon-Enhanced Hydrogen Production from Water Reduction Wu, Binghui; Liu, Deyu; Mubeen, Syed Journal of the American Chemical Society, Vol. 138, Issue 4 https://doi.org/10.1021/jacs.5b11341	journal	January 2016
Affibody modified and radiolabeled gold–Iron oxide hetero-nanostructures for tumor PET, optical and MR imaging Yang, Meng; Cheng, Kai; Qi, Shibo Biomaterials, Vol. 34, Issue 11 https://doi.org/10.1016/j.biomaterials.2013.01.014	journal	April 2013
Direct Evidence of Chelated Geometry of Catechol on TiO ₂ by a Combined Solid-State NMR and DFT Study Finkelstein-Shapiro, Daniel; Davidowski, Stephen K.; Lee, Paul B. The Journal of Physical Chemistry C, Vol. 120, Issue 41 https://doi.org/10.1021/acs.jpcc.6b08041	journal	October 2016
Porous Hollow Fe ₃ O ₄ Nanoparticles for Targeted Delivery and Controlled Release of Cisplatin Cheng, Kai; Peng, Sheng; Xu, Chenjie Journal of the American Chemical Society, Vol. 131, Issue 30 https://doi.org/10.1021/ja903300f	journal	August 2009
Effect of Ceria on Gold–Titania Catalysts for the Water–Gas Shift Reaction: Fundamental Studies for Au/CeO _x /TiO ₂ (110) and Au/CeO _x /TiO ₂ Powders Si, Rui; Tao, Jing; Evans, Jaime The Journal of Physical Chemistry C, Vol. 116, Issue 44 https://doi.org/10.1021/jp3089325	journal	October 2012
The effect of sedimentation and diffusion on cellular uptake of gold nanoparticles Cho, Eun Chul; Zhang, Qiang; Xia, Younan Nature Nanotechnology, Vol. 6, Issue 6 https://doi.org/10.1038/nnano.2011.58	journal	April 2011
Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations Kalyanaraman, Balaraman; Darley-Usmar, Victor; Davies, Kelvin J. A. Free Radical Biology and Medicine, Vol. 52, Issue 1 https://doi.org/10.1016/j.freeradbiomed.2011.09.030	journal	January 2012
The Fate and Toxicity of Raman-Active Silica-Gold Nanoparticles in Mice Thakor, A. S.; Luong, R.; Paulmurugan, R. Science Translational Medicine, Vol. 3, Issue 79 https://doi.org/10.1126/scitranslmed.3001963	journal	April 2011
Hybrid Nanotrimers for Dual T ₁ and T ₂ -Weighted Magnetic Resonance Imaging Cheng, Kai; Yang, Meng; Zhang, Ruiping ACS Nano, Vol. 8, Issue 10 https://doi.org/10.1021/nn500188y	journal	October 2014
The One Year Fate of Iron Oxide Coated Gold Nanoparticles in Mice Kolosnjaj-Tabi, Jelena; Javed, Yasir; Lartigue, Lénaic ACS Nano, Vol. 9, Issue 8 https://doi.org/10.1021/acsnano.5b00042	journal	July 2015
Advances in Image-Guided Radiation Therapy Dawson, Laura A.; Jaffray, David A. Journal of Clinical Oncology, Vol. 25, Issue 8 https://doi.org/10.1200/JCO.2006.09.9515	journal	March 2007
Strategies for optimizing the response of cancer and normal tissues to radiation Moding, Everett J.; Kastan, Michael B.; Kirsch, David G. Nature Reviews Drug Discovery, Vol. 12, Issue 7 https://doi.org/10.1038/nrd4003	journal	July 2013
Average Physical Enhancement by Nanomaterials under X-ray Irradiation Davidson, R. Andrew; Guo, Ting The Journal of Physical Chemistry C, Vol. 118, Issue 51 https://doi.org/10.1021/jp509471m	journal	December 2014
Metal/Semiconductor Hybrid Nanostructures for Plasmon-Enhanced Applications Jiang, Ruibin; Li, Benxia; Fang, Caihong Advanced Materials, Vol. 26, Issue 31 https://doi.org/10.1002/adma.201400203	journal	April 2014
Protein:Colloid Conjugates for Surface Enhanced Raman Scattering: Stability and Control of Protein Orientation Keating, Christine D.; Kovaleski, Kenneth M.; Natan, Michael J. The Journal of Physical Chemistry B, Vol. 102, Issue 47 https://doi.org/10.1021/jp982723z	journal	November 1998

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Anisotropic Gold Nanoparticles in Biomedical Applications Kohout, Claudia; Santi, Cristina; Polito, Laura International Journal of Molecular Sciences, Vol. 19, Issue 11 https://doi.org/10.3390/ijms19113385	journal	October 2018
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An Ultrasound Activated Vesicle of Janus Au‐MnO Nanoparticles for Promoted Tumor Penetration and Sono‐Chemodynamic Therapy of Orthotopic Liver Cancer Lin, Xiahui; Liu, Shuya; Zhang, Xuan Angewandte Chemie, Vol. 132, Issue 4 https://doi.org/10.1002/ange.201912768	journal	December 2019
Radionuclide ¹⁸⁸ Re‐Loaded Photothermal Hydrogel for Cancer Theranostics Wang, Yangyun; Li, Linlin; Shi, Xingpeng Particle & Particle Systems Characterization, Vol. 37, Issue 2 https://doi.org/10.1002/ppsc.201900421	journal	January 2020
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A gold nanoparticle system for the enhancement of radiotherapy and simultaneous monitoring of reactive-oxygen-species formation Choi, By Jihye; Jung, Kyung Oh; Graves, Edward E. Nanotechnology, Vol. 29, Issue 50 https://doi.org/10.1088/1361-6528/aae272	journal	October 2018
Breaking the Depth Dependence by Nanotechnology‐Enhanced X‐Ray‐Excited Deep Cancer Theranostics Fan, Wenpei; Tang, Wei; Lau, Joseph Advanced Materials, Vol. 31, Issue 12 https://doi.org/10.1002/adma.201806381	journal	January 2019
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62 RADIOLOGY AND NUCLEAR MEDICINE
59 BASIC BIOLOGICAL SCIENCES
Radiation/chemo therapy
radio sensitizer
reactive oxygen species
gold-titanium oxide nanoparticles
heterogeneous interface
triple negative breast cancers