Tumor Angiogenesis Targeted Radiosensitization Therapy Using Gold Nanoprobes Guided by MRI/SPECT Imaging

ACS Applied Materials and Interfaces

Volumn 8, Issue 3, 2016, Pages 1718-1732

  Yang, Yi ^a   Zhang, Lu ^a   Cai, Jiali ^b   Li, Xiao ^c   Cheng, Dengfeng ^c   Su, Huilan ^a   Zhang, Jianping ^d   Liu, Shiyuan ^b   Shi, Hongcheng ^c   Zhang, Yingjian ^d   Zhang, Chunfu ^a,e  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

^d FUDAN UNIVERSITY SHANGHAI CANCER CENTER   (China)

^e SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

gold nanoparticles; MRI SPECT; radiotherapy; theranostics; v 3 integrin

Indexed keywords

FIBER OPTIC SENSORS; GOLD; MAGNETIC RESONANCE IMAGING; METAL NANOPARTICLES; NANOPARTICLES; PARTICLE SIZE; RADIOTHERAPY; TUMORS;

ENHANCED PERMEABILITY; GOLD NANOPARTICLES; INTEGRINS; OPTIMAL PARTICLE SIZES; RADIO-SENSITIZATION; THERANOSTICS; TUMOR ACCUMULATION; TUMOR ANGIOGENESIS;

PROBES;

ARGINYL-GLYCYL-ASPARTIC ACID; GADOLINIUM; GOLD; METAL NANOPARTICLE; OLIGOPEPTIDE; TECHNETIUM; VITRONECTIN RECEPTOR;

ANIMAL; BAGG ALBINO MOUSE; CELL DEATH; CELL FRACTIONATION; CHEMISTRY; DRUG EFFECTS; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NUCLEAR MAGNETIC RESONANCE IMAGING; NUDE MOUSE; PATHOLOGY; RADIATION TOLERANCE; SINGLE PHOTON EMISSION COMPUTED TOMOGRAPHY; TISSUE DISTRIBUTION; TUMOR CELL LINE; VASCULARIZATION;

ANIMALS; CELL DEATH; CELL LINE, TUMOR; GADOLINIUM; GOLD; HUMANS; IMMUNOHISTOCHEMISTRY; INTEGRIN ALPHAVBETA3; MAGNETIC RESONANCE IMAGING; METAL NANOPARTICLES; MICE, INBRED BALB C; MICE, NUDE; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; OLIGOPEPTIDES; RADIATION TOLERANCE; SUBCELLULAR FRACTIONS; TECHNETIUM; TISSUE DISTRIBUTION; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON;

EID: 84955481635     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b09274     Document Type: Article

References (75)

1. Dreaden, E. C.; Alkilany, A. M.; Huang, X.; Murphy, C. J.; El-Sayed, M. A. The golden age: gold nanoparticles for biomedicine Chem. Soc. Rev. 2012, 41, 2740-2779 10.1039/C1CS15237H
2. Biju, V. Chemical modifications and bioconjugate reactions of nanomaterials for sensing, imaging, drug delivery and therapy Chem. Soc. Rev. 2014, 43, 744-764 10.1039/C3CS60273G
3. Kircher, M. F.; de la Zerda, A.; Jokerst, J. V.; Zavaleta, C. L.; Kempen, P. J.; Mittra, E.; Pitter, K.; Huang, R.; Campos, C.; Habte, F.; Sinclair, R.; Brennan, C. W.; Mellinghoff, I. K.; Holland, E. C.; Gambhir, S. S. A Brain Tumor Molecular Imaging Strategy Using a New Triple-Modality MRI-Photoacoustic-Raman Nanoparticle Nat. Med. 2012, 18 (5) 829-834 10.1038/nm.2721
4. Hainfeld, J. F.; Dilmanian, F. A.; Slatkin, D. N.; Smilowitz, H. M. Radiotherapy enhancement with gold nanoparticles J. Pharm. Pharmacol. 2008, 60, 977-985 10.1211/jpp.60.8.0005
5. Li, Y. J.; Perkins, A. L.; Su, Y.; Ma, Y.; Colson, L.; Horne, D. A.; Chen, Y. Gold nanoparticles as a platform for creating a multivalent poly-SUMO chain inhibitor that also augments ionizing radiation Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 4092-4097 10.1073/pnas.1109131109
6. Ngwa, W.; Kumar, R.; Sridhar, S.; Korideck, H.; Zygmanski, P.; Cormack, R. A.; Berbeco, R.; Makrigiorgos, G. M. Targeted radiotherapy with gold nanoparticles: current status and future perspectives Nanomedicine 2014, 9 (7) 1063-1082 10.2217/nnm.14.55
7. Setua, S.; OuberaI, M.; Piccirillo, S. G.; Watts, C.; Welland, M. Cisplatin-tethered gold nanospheres for multimodal chemo-radiotherapy of glioblastoma Nanoscale 2014, 6, 10865-10873 10.1039/C4NR03693J
8. Yang, Y.-S.; Carney, R. P.; Stellacci, F.; Irvine, D. J. Enhancing Radiotherapy by Lipid Nanocapsule-Mediated Delivery of Amphiphilic Gold Nanoparticles to Intracellular Membranes ACS Nano 2014, 8 (9) 8992-9002 10.1021/nn502146r
9. Veigele, W. J. Photon cross sections from 0.1 keV to 1 MeV for elements Z = 1 to Z= 94∗ At. Data Nucl. Data Tables 1973, 5, 51-111 10.1016/S0092-640X(73)80015-4
10. Mullenger, L.; Singh, B.; Ormerod, M.; Dean, C. Chemical Study of the Radiosensitization of Micrococcus sodonensis by Iodine Compounds Nature 1967, 216, 372-374 10.1038/216372a0
11. Bernhard, E. J.; Mitchell, J. B.; Deen, D.; Cardell, M.; Rosenthal, D. I.; Brown, J. M. Reevaluating gadolinium(III) texaphyrin as a radiosensitizing agent Can. Res. 2000, 60, 86-91
12. Chou, L. Y. T.; Chan, W. C. W. Fluorescence-Tagged Gold Nanoparticles for Rapidly Characterizing the Size-Dependent Biodistribution in Tumor Models Adv. Healthcare Mater. 2012, 1, 714-721 10.1002/adhm.201200084
13. Perrault, S. D.; Walkey, C.; Jennings, T.; Fischer, H. C.; Chan, W. C. W. Mediating Tumor Targeting Efficiency of Nanoparticles Through Design Nano Lett. 2009, 9, 1909-1915 10.1021/nl900031y
14. Zhang, G.; Yang, Z.; Lu, W.; Zhang, R.; Huang, Q.; Tian, M.; Li, L.; Liang, D.; Li, C. Influence of anchoring ligands and particle size on the colloidal stability and in vivo biodistribution of polyethylene glycol-coated gold nanoparticles in tumor-xenografted mice Biomaterials 2009, 30, 1928-1936 10.1016/j.biomaterials.2008.12.038
15. Zhang, X. D.; Wu, D.; Shen, X.; Chen, J.; Sun, Y. M.; Liu, P. X.; Liang, X. J. Size-dependent radiosensitization of PEG-coated gold nanoparticles for cancer radiation therapy Biomaterials 2012, 33, 6408-6419 10.1016/j.biomaterials.2012.05.047
16. Wang, Y.; Liu, Y.; Luehmann, H.; Xia, X.; Brown, P.; Jarreau, C.; Welch, M.; Xia, Y. Evaluating the Pharmacokinetics and In Vivo Cancer Targeting Capability of Au Nanocages by Positron Emission Tomography Imaging ACS Nano 2012, 6 (7) 5880-5888 10.1021/nn300464r
17. Alric, C.; Taleb, J.; Duc, G. L.; Mandon, C.; Billotey, C.; Meur-Herland, A. L.; Brochard, T.; Vocanson, F.; Janier, M.; Perriat, P.; Roux, S.; Tillement, O. Gadolinium Chelate Coated Gold Nanoparticles As Contrast Agents for Both X-ray Computed Tomography and Magnetic Resonance Imaging J. Am. Chem. Soc. 2008, 130, 5908-5915 10.1021/ja078176p
18. Dufort, S.; Bianchi, A.; Henry, M.; Lux, F.; Le Duc, G.; Josserand, V.; Louis, C.; Perriat, P.; Crémillieux, Y.; Tillement, O.; Coll, J.-L. Nebulized Gadolinium-Based Nanoparticles: A Theranostic Approach for Lung Tumor Imaging and Radiosensitization Small 2015, 11 (2) 215-221 10.1002/smll.201401284
19. Melemenidis, S.; Jefferson, A.; Ruparelia, N.; Akhtar, A. M.; Xie, J.; Allen, D.; Hamilton, A.; Larkin, J. R.; Perez-Balderas, F.; Smart, S. C.; Muschel, R. J.; Chen, X.; Sibson, N. R.; Choudhury, R. P. Molecular Magnetic Resonance Imaging of Angiogenesis In Vivo using Polyvalent Cyclic RGD-Iron Oxide Microparticle Conjugates Theranostics 2015, 5 (5) 515-529 10.7150/thno.10319
20. Kim, Y.-H.; Jeon, J.; Hong, S. H.; Rhim, W.-K.; Lee, Y.-S.; Youn, H.; Chung, J.-K.; Lee, M. C.; Lee, D. S.; Kang, K. W.; Nam, J.-M. Tumor Targeting and Imaging Using Cyclic RGDPEGylated Gold Nanoparticle Probes with Directly Conjugated Iodine-125 Small 2011, 7 (14) 2052-2060 10.1002/smll.201100927
21. Bogdanov, A. A.; Gupta, S.; Koshkina, N.; Corr, S. J.; Zhang, S.; Curley, S. A.; Han, G. Gold Nanoparticles Stabilized with MPEG-Grafted Poly(L-lysine): in Vitro and in Vivo Evaluation of a Potential Theranostic Agent Bioconjugate Chem. 2015, 26, 39-50 10.1021/bc5005087
22. Zhou, M.; Chen, Y.; Adachi, M.; Wen, X.; Erwin, B.; Mawlawi, O.; Lai, S. Y.; Li, C. Single agent nanoparticle for radiotherapy and radio-photothermal therapy in anaplastic thyroid cancer Biomaterials 2015, 57, 41-49 10.1016/j.biomaterials.2015.04.013
23. Hill, T. K.; Abdulahad, A.; Kelkar, S. S.; Marini, F. C.; Long, T. E.; Provenzale, J. M.; Mohs, A. M. Indocyanine Green-Loaded Nanoparticles for Image-Guided Tumor Surgery Bioconjugate Chem. 2015, 26, 294-303 10.1021/bc5005679
24. Xiong, L. Q.; Shuhendler, A. J.; Rao, J. H. Selfluminescing BRET-FRET near-infrared dots for in vivo lymph-node mapping and tumour imaging Nat. Commun. 2012, 3, 1193 10.1038/ncomms2197
25. Freund, B.; Tromsdorf, U. I.; Bruns, O. T.; Heine, M.; Giemsa, A.; Bartelt, A.; Salmen, S. C.; Raabe, N.; Heeren, J.; Ittrich, H.; Reimer, R.; Hohenberg, H.; Schumacher, U.; Weller, H.; Nielsen, P. A Simple and Widely Applicable Method to 59Fe-Radiolabel Monodisperse Superparamagnetic Iron Oxide Nanoparticles for In Vivo Quantification Studies ACS Nano 2012, 6 (8) 7318-7325 10.1021/nn3024267
26. Fan, Q.; Cheng, K.; Hu, X.; Ma, X.; Zhang, R.; Yang, M.; Lu, X.; Xing, L.; Huang, W.; Gambhir, S. S.; Cheng, Z. Transferring Biomarker into Molecular Probe: Melanin Nanoparticle as a Naturally Active Platform for Multimodality Imaging J. Am. Chem. Soc. 2014, 136, 15185-15194 10.1021/ja505412p
27. Tang, Y.; Zhang, C.; Wang, J.; Lin, X.; Zhang, L.; Yang, Y.; Wang, Y.; Zhang, Z.; Bulte, J. W. M.; Yang, G.-Y. MRI/SPECT/Fluorescent Tri-Modal Probe for Evaluating the Homing and Therapeutic Effi cacy of Transplanted Mesenchymal Stem Cells in a Rat Ischemic Stroke Model Adv. Funct. Mater. 2015, 25, 1024-1034 10.1002/adfm.201402930
28. Chithrani, D. B.; Jelveh, S.; Jalali, F.; Van Prooijen, M.; Allen, C.; Bristow, R. G.; Hill, R. P.; Jaffray, D. A. Gold nanoparticles as radiation sensitizers in cancer therapy Radiat. Res. 2010, 173 (6) 719-728 10.1667/RR1984.1
29. Jeremic, B.; Aguerri, A. R.; Filipovic, N. Radiosensitization by gold nanoparticles Clin. Transl. Oncol. 2013, 15, 593-601 10.1007/s12094-013-1003-7
30. Choi, C. H.; Alabi, C. A.; Webster, P.; Davis, M. E. Mechanism of active targeting in solid tumors with transferrin-containing gold nanoparticles Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (3) 1235-1240 10.1073/pnas.0914140107
31. Hainfeld, J. F.; Lin, L.; Slatkin, D. N.; Dilmanian, F. A.; Vadas, T. M.; Smilowitz, H. M. Gold nanoparticle hyperthermia reduces radiotherapy dose Nanomedicine (N. Y., NY, U. S.) 2014, 10, 1609-1617 10.1016/j.nano.2014.05.006
32. Khoshgard, K.; Hashemi, B.; Arbabi, A.; Rasaee, M. J.; Soleimani, M. Radiosensitization effect of folate-conjugated gold nanoparticles on HeLa cancer cells under orthovoltage superficial radiotherapy techniques Phys. Med. Biol. 2014, 59, 2249-2263 10.1088/0031-9155/59/9/2249
33. Gao, C.; Vuong, J.; Zhang, Q.; Liu, Y.; Yin, Y. One-step seeded growth of Au nanoparticles with widely tunable sizes Nanoscale 2012, 4, 2875-2878 10.1039/c2nr30300k
34. Wang, Y.; Liu, X.; Hnatowich, D. J. An improved synthesis of NHS-MAG3 for conjugation and radiolabeling of biomolecules with 99mTc at room temperature Nat. Protoc. 2007, 2 (4) 972-978 10.1038/nprot.2007.144
35. Cheng, D.; Li, X.; Zhang, C.; Tan, H.; Wang, C.; Pang, L.; Shi, H. Detection of Vulnerable Atherosclerosis Plaques with a Dual-Modal Single-Photon-Emission Computed Tomography/Magnetic Resonance Imaging Probe Targeting Apoptotic Macrophages ACS Appl. Mater. Interfaces 2015, 7, 2847-2855 10.1021/am508118x
36. Ellman, G. L.; Courtney, K. D.; Andres, V., jr.; Featherstone, R. M. A new and rapid colorimetric determination of acetylcholinesterase activity Biochem. Pharmacol. 1961, 7 (2) 88-90 10.1016/0006-2952(61)90145-9
37. Hu, M.-L. Measurement of Protein Thiol Groups and Glutathione in Plasma Methods Enzymol. 1994, 233, 380-385 10.1016/S0076-6879(94)33044-1
38. Xue, S.; Zhang, C.; Yang, Y.; Zhang, L.; Cheng, D.; Zhang, J.; Shi, H.; Zhang, Y. 99mTc-Labeled Iron Oxide Nanoparticles for Dual-Contrast (T1/T2) Magnetic Resonance and Dual-Modality Imaging of Tumor Angiogenesis J. Biomed. Nanotechnol. 2015, 11, 1027-1037 10.1166/jbn.2015.2023
39. Zhang, C.; Xie, X.; Liang, S.; Li, M.; Liu, Y.; Gu, H. Mono-dispersed high magnetic resonance sensitive magnetite nanocluster probe for detection of nascent tumors by magnetic resonance molecular imaging Nanomedicine: NBM 2012, 8, 996-1006 10.1016/j.nano.2011.11.013
40. Fan, W.; Shen, B.; Bu, W.; Chen, F.; Zhao, K.; Zhang, S.; Zhou, L.; Peng, W.; Xiao, Q.; Xing, H.; Liu, J.; Ni, D.; He, Q.; Shi, J. Rattle-Structured Multifunctional Nanotheranostics for Synergetic Chemo-/Radiotherapy and Simultaneous Magnetic/Luminescent Dual-Mode Imaging J. Am. Chem. Soc. 2013, 135, 6494-6503 10.1021/ja312225b
41. Hacker, M.; Bachmann, K.; Messer, W. Pharmacology: Principles and Practice; Elsevier, Oxford, U.K., 2009; pp 240-245.
42. McQuade, C.; Al Zaki, A.; Desai, Y.; Vido, M.; Sakhuja, T.; Cheng, Z.; Hickey, R. J.; Joh, D.; Park, S.-J.; Kao, G.; Dorsey, J. F.; Tsourkas, A. A Multifunctional Nanoplatform for Imaging, Radiotherapy, and the Prediction of Therapeutic Response Small 2015, 11 (7) 834-843 10.1002/smll.201401927
43. Zhou, C.; Hao, G.; Thomas, P.; Liu, J.; Yu, M.; Sun, S.; Öz, O. K.; Sun, X.; Zheng, J. Near-Infrared Emitting Radioactive Gold Nanoparticles with Molecular Pharmacokinetics Angew. Chem., Int. Ed. 2012, 51, 10118-10122 10.1002/anie.201203031
44. Liang, X.; Li, Y.; Li, X.; Jing, L.; Deng, Z.; Yue, X.; Li, C.; Dai, Z. PEGylated Polypyrrole Nanoparticles Conjugating Gadolinium Chelates for Dual-Modal MRI/Photoacoustic Imaging Guided Photothermal Therapy of Cancer Adv. Funct. Mater. 2015, 25, 1451-1462 10.1002/adfm.201402338
45. Yu, S.-B.; Watson, A. D. Metal-based x-ray contrast media Chem. Rev. 1999, 99, 2353 10.1021/cr980441p
46. Coughlin, A. J.; Ananta, J. S.; Deng, N.; Larina, I. V.; Decuzzi, P.; West, J. L. Gadolinium-Conjugated Gold Nanoshells for Multimodal Diagnostic Imaging and Photothermal Cancer Therapy Small 2014, 10 (3) 556-565 10.1002/smll.201302217
47. Song, Y.; Xu, X.; MacRenaris, K. W.; Zhang, X.-Q.; Mirkin, C. A.; Meade, T. J. Multimodal Gadolinium-Enriched DNA-Gold Nanoparticle Conjugates for Cellular Imaging Angew. Chem., Int. Ed. 2009, 48, 9143-9147 10.1002/anie.200904666
48. 3+ chelates: Linker effects on the relaxivity Dalton Trans. 2015, 44 (9) 4016-4031 10.1039/C4DT03210A
49. Patra, H. K.; Banerjee, S.; Chaudhuri, U.; Lahiri, P.; Dasgupta, A. K. Cell selective response to gold nanoparticles Nanomedicine 2007, 3, 111-119 10.1016/j.nano.2007.03.005
50. Pan, Y.; Neuss, S.; Leifert, A.; Fischler, M.; Wen, F.; Simon, U. et al. Size-dependent cytotoxicity of gold nanoparticles Small 2007, 3, 1941-1949 10.1002/smll.200700378
51. Irigoyen, M.; Pajares, M. J.; Agorreta, J.; Ponz-Sarvisé, M. P.; Salvo, E.; Lozano, M. D. et al. TGFBI expression is associated with a better response to chemotherapy in NSCLC Mol. Cancer 2010, 9, 130-142 10.1186/1476-4598-9-130
52. Douglass, M.; Bezak, E.; Penfold, S. Monte Carlo investigation of the increased radiation deposition due to gold nanoparticles using kilovoltage and megavoltage photons in a 3D randomized cell model Med. Phys. 2013, 40, 071710 10.1118/1.4808150
53. Cai, Z.; Pignol, J.-P.; Chattopadhyay, N.; Kwon, Y. L.; Lechtman, E.; Reilly, R. M. Investigation of the effects of cell model and subcellular location of gold nanoparticles on nuclear dose enhancement factors using Monte Carlo simulation Med. Phys. 2013, 40, 114101 10.1118/1.4823787
54. Khemtong, C.; Kessinger, C. W.; Ren, J.; Bey, E. A.; Yang, S. G.; Guthi, J. S.; Boothman, D. A.; Sherry, A. D.; Gao, J. In vivo Off-Resonance Saturation Magnetic Resonance Imaging of AvB3-Targeted Superparamagnetic Nanoparticles Cancer Res. 2009, 69 (4) 1651-1658 10.1158/0008-5472.CAN-08-3231
55. 99mTc-Labeled Gold Nanoparticles Conjugated to c[RGDfK(C)] for Molecular Imaging of Tumor α(v)β(3) Expression Bioconjugate Chem. 2011, 22, 913-922 10.1021/bc100551s
56. Yu, M.; Zheng, J. Clearance Pathways and Tumor Targeting of Imaging Nanoparticles ACS Nano 2015, 9 (7) 6655-6674 10.1021/acsnano.5b01320
57. Alric, C.; Miladi, I.; Kryza, D.; Taleb, J.; Lux, F.; Bazzi, R.; Billotey, C.; Janier, M.; Perriat, P.; Roux, S.; Tillement, O. The biodistribution of gold nanoparticles designed for renal clearance Nanoscale 2013, 5, 5930-5939 10.1039/c3nr00012e
58. Oliver, P. L. Detection of DNA damage in individual cells by analysis of histone H2AX phosphorylation Methods Cell Biol. 2004, 75, 355-373 10.1016/S0091-679X(04)75014-1
59. Frens, G. Controlled Nucleation for the Regulation of the Particle Size in Monodisperse Gold Suspensions Nature, Phys. Sci. 1973, 241, 20 10.1038/physci241020a0
60. Bastús, N. G.; Comenge, J.; Puntes, V. Kinetically Controlled Seeded Growth Synthesis of Citrate-Stabilized Gold Nanoparticles of up to 200 nm: Size Focusing versus Ostwald Ripening Langmuir 2011, 27, 11098-11105 10.1021/la201938u
61. Folkman, J. Angiogenesis in cancer, vascular, rheumatoid and other disease Nat. Med. 1995, 1, 27-31 10.1038/nm0195-27
62. Carmeliet, P.; Jain, R. K. Angiogenesis in cancer and other diseases Nature 2000, 407, 249-257 10.1038/35025220
63. Hagedorn, M.; Bikfalvi, A. Target molecules for antiangiogenic therapy: From basic research to clinical trials Crit Rev. Oncol/Hematol. 2000, 34, 89-110 10.1016/S1040-8428(00)00056-1
64. Folkman, J.; Klagsbrun, M. Angiogenic Factors Science 1987, 235, 442-447 10.1126/science.2432664
65. Garcia-Barros, M.; Paris, F.; Cordon-Cardo, C.; Lyden, D.; Rafii, S.; Haimovitz-Friedman, A.; Fuks, Z.; Kolesnick, R. Tumor response to radiotherapy regulated by endothelial cell apoptosis Science 2003, 300 (5622) 1155-1159
66. Joh, D. Y.; Sun, L.; Stangl, M.; Al Zaki, A.; Murty, S.; Santoiemma, P. P.; Davis, J. J.; Baumann, B. C.; Alonso-Basanta, M.; Bhang, D.; Kao, G. D.; Tsourkas, A.; Dorsey, J. F. Selective Targeting of Brain Tumors with Gold Nanoparticle-Induced Radiosensitization PLoS One 2013, 8 (4) e62425 10.1371/journal.pone.0062425
67. Berbeco, R. I.; Ngwa, W.; Makrigiorgos, G. M. Localized dose enhancement to tumor blood vessel endothelial cells via megavoltage x-rays and targeted gold nanoparticles: new potential for external beam radiotherapy Int. J. Radiat. Oncol., Biol., Phys. 2011, 81, 270-276 10.1016/j.ijrobp.2010.10.022
68. Ngwa, W.; Makrigiorgos, G. M.; Berbeco, R. I. Applying gold nanoparticles as tumor-vascular disrupting agents during brachytherapy: estimation of endothelial dose enhancement Phys. Med. Biol. 2010, 55, 6533-6548 10.1088/0031-9155/55/21/013
69. Zhang, P.; Qiao, Y.; Wang, C.; Ma, L.; Su, M. Enhanced radiation therapy with internalized polyelectrolyte modified nanoparticles Nanoscale 2014, 6, 10095-10099 10.1039/C4NR01564A
70. Miladi, I.; Alric, C.; Dufort, S.; Mowat, P.; Dutour, A.; Mandon, C.; Laurent, G.; Bräuer-Krisch, E.; Herath, N.; Coll, J.-L.; Dutreix, M.; Lux, F.; Bazzi, R.; Billotey, C.; Janier, M.; Perriat, P.; Le Duc, G.; Roux, S.; Tillement, O. T. The In Vivo Radiosensitizing Effect of Gold Nanoparticles Based MRI Contrast Agents Small 2014, 10 (6) 1116-1124 10.1002/smll.201302303
71. Zhang, X.-D.; Luo, Z.; Chen, J.; Shen, X.; Song, S.; Sun, Y.; Fan, S.; Fan, F.; Leong, D. T.; Xie, J. Ultrasmall Au 10-12 (SG) 10-12 Nanomolecules for High Tumor Specifi city and Cancer Radiotherapy Adv. Mater. 2014, 26, 4565-4568 10.1002/adma.201400866
72. Zhang, X.-D.; Chen, J.; Luo, Z.; Wu, D.; Shen, X.; Song, S.-S.; Sun, Y.-M.; Liu, P.-X.; Zhao, J.; Huo, S.; Fan, S.; Fan, F.; Liang, X.-J.; Xie, J. Enhanced Tumor Accumulation of Sub-2 nm Gold Nanoclusters for Cancer Radiation Therapy Adv. Healthcare Mater. 2014, 3, 133-141 10.1002/adhm.201300189
73. Butterworth, K. T.; McMahon, S. J.; Currell, F. J.; Prise, K. M. Physical basis and biological mechanisms of gold nanoparticle radiosensitization Nanoscale 2012, 4, 4830-4838 10.1039/c2nr31227a
74. McMahon, S. J.; Hyland, W. B.; Muir, M. F.; Coulter, J. A.; Jain, S.; Butterworth, K. T.; Schettino, G.; Dickson, G. R.; Hounsell, A. R.; O'Sullivan, J. M.; Prise, K. M.; Hirst, D. G.; Currell, F. J. Biological consequences of nanoscale energy deposition near irradiated heavy atom nanoparticles Sci. Rep. 2011, 1, 18 10.1038/srep00018
75. Cai, Q. Y.; Kim, S. H.; Choi, K. S.; Kim, S. Y.; Byun, S. J.; Kim, K. W.; Park, S. H.; Juhng, S. K.; Yoon, K.-H. Colloidal gold nanoparticles as a blood-pool contrast agent for X-ray computed tomography in mice Invest. Radiol. 2007, 42, 797-806 10.1097/RLI.0b013e31811ecdcd