Mechanisms of nanoparticle radiosensitization

Advanced Review

Ivan Kempson

Published Online: Jul 19 2020

DOI: 10.1002/wnan.1656

Full article on Wiley Online Library: HTML PDF

Can't access this content? Tell your librarian.

Abstract Metal‐based nanoparticles applied to potentiating the effects of radiotherapy have drawn significant attention from the research community and are now available clinically. By improving our mechanistic understanding, nanoparticles are likely to evolve to provide very significant improvements in radiotherapy outcomes with only incremental increase in cost. This review critically assesses the inconsistent observations surrounding physical, physicochemical, chemical and biological mechanisms of radiosensitization. In doing so, a number of needs are identified for continuing research and are highlighted. The large degree of variability from one nanoparticle to another emphasizes that it is a mistake to generalize nanoparticle radiosensitizer mechanisms. Nanoparticle formulations should be considered in an analogous way as pharmacological agents and as a broad class of therapeutic agents, needing to be considered with a high degree of individuality with respect to their interactions and ultimate impact on radiobiological response. In the same way that no universal anti‐cancer drug exists, it is unlikely that a single nanoparticle formulation will lead to the best therapeutic outcomes for all cancers. The high degree of complexity and variability in mechanistic action provides notable opportunities for nanoparticle formulations to be optimized for specific indications. This article is categorized under: Therapeutic Approaches and Drug Discovery > Emerging Technologies Nanotechnology Approaches to Biology > Nanoscale Systems in Biology

Average tumor volume after: (a) no treatment (triangles, n = 12); (b) gold only (diamonds, n = 4); (c) irradiation only (30 Gy, 250 kVp, circles, n = 11); (d) intravenous gold injection (1.35 g Au/kg) followed by irradiation (squares, n = 10). (Reprinted with permission from Hainfeld et al. (2004). Copyright 2004 IPEM. IOP Publishing

[ Normal View | Magnified View ]

A model of the surface of a cell nucleus with an intensity map of reactive oxygen species, enhanced by the presence of gold nanoparticles, interacting with the membrane transposed. The lighter spots indicate highly localized and heterogeneous damage can result. Courtesy of Dylan Peukert

[ Normal View | Magnified View ]

An incident X‐ray (green) is incident on a 20 nm diameter nanoparticle (yellow) which results in the ejection and multiple ionizing interactions of electrons (red tracks). (Reprinted with permission from Butterworth et al. (2012). Copyright 2012 The Royal Society of Chemistry

[ Normal View | Magnified View ]

Three‐dimensional magnetic resonance imaging reconstructions of brain metastases from various primary sites after intravenous injection of AGuIX nanoparticles. (Reprinted with permission from Lux et al. (2019). Copyright 2019

[ Normal View | Magnified View ]

References

Aghighi,, M., Pisani,, L., Theruvath,, A. J., Muehe,, A. M., Donig,, J., Khan,, R., … Daldrup‐Link,, H. E. (2018). Ferumoxytol is not retained in kidney allografts in patients undergoing acute rejection. Molecular Imaging and Biology, 20(1), 139–149. https://doi.org/10.1007/s11307-017-1084-8
Ahmad,, R., Schettino,, G., Royle,, G., Barry,, M., Pankhurst,, Q. A., Tillement,, O., … Ricketts,, K. (2020). Radiobiological implications of nanoparticles following radiation treatment. Particle and Particle Systems Characterization, 1900411, 1–10.
Akhuemonkhan,, E., Parian,, A., Carson,, K. A., & Hutfless,, S. (2018). Adverse reactions after intravenous iron infusion among inflammatory bowel disease patients in the United States, 2010–2014. Inflammatory Bowel Diseases, 24(9), 1801–1807. https://doi.org/10.1093/ibd/izy063
Alvarado,, M. D., Mittendorf,, E. A., Teshome,, M., Thompson,, A. M., Bold,, R. J., Gittleman,, M. A., … Hunt,, K. K. (2019). SentimagIC: A non‐inferiority trial comparing superparamagnetic iron oxide versus technetium‐99m and blue dye in the detection of axillary sentinel nodes in patients with early‐stage breast cancer. Annals of Surgical Oncology, 26(11), 3510–3516. https://doi.org/10.1245/s10434-019-07577-4
Amirrashedi,, M., Riyahialam,, N., Mostaar,, A., Haghgoo,, S., Gorji,, E., & Jaberi,, R. (2015). Dose enhancement in radiotherapy by novel application of gadolinium based MRI contrast agent nanomagnetic particles in gel dosimetry. Paper presented at the IFMBE Proceedings,
Arakha,, M., Roy,, J., Nayak,, P. S., Mallick,, B., & Jha,, S. (2017). Zinc oxide nanoparticle energy band gap reduction triggers the oxidative stress resulting into autophagy‐mediated apoptotic cell death. Free Radical Biology and Medicine, 110, 42–53. https://doi.org/10.1016/j.freeradbiomed.2017.05.015
AshaRani,, P. V., Mun,, G. L. K., Hande,, M. P., & Valiyaveettil,, S. (2009). Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano, 3(2), 279–290. https://doi.org/10.1021/nn800596w
Balasubramanian,, S. K., Jittiwat,, J., Manikandan,, J., Ong,, C. N., Yu,, L. E., & Ong,, W. Y. (2010). Biodistribution of gold nanoparticles and gene expression changes in the liver and spleen after intravenous administration in rats. Biomaterials, 31(8), 2034–2042. https://doi.org/10.1016/j.biomaterials.2009.11.079
Berdys,, J., Anusiewicz,, I., Skurski,, P., & Simons,, J. (2004). Damage to model DNA fragments from very low‐energy (%3C1 eV) electrons. Journal of the American Chemical Society, 126(20), 6441–6447. https://doi.org/10.1021/ja049876m
Bonvalot,, S., Le Pechoux,, C., De Baere,, T., Kantor,, G., Buy,, X., Stoeckle,, E., … Soria,, J. C. (2017). First‐in‐human study testing a new radioenhancer using nanoparticles (NBTXR3) activated by radiation therapy in patients with locally advanced soft tissue sarcomas. Clinical Cancer Research, 23(4), 908–917. https://doi.org/10.1158/1078-0432.CCR-16-1297
Bonvalot,, S., Rutkowski,, P. L., Thariat,, J., Carrère,, S., Ducassou,, A., Sunyach,, M. P., … Papai,, Z. (2019). NBTXR3, a first‐in‐class radioenhancer hafnium oxide nanoparticle, plus radiotherapy versus radiotherapy alone in patients with locally advanced soft‐tissue sarcoma (Act.In.Sarc): A multicentre, phase 2–3, randomised, controlled trial. The Lancet Oncology, 20(8), 1148–1159. https://doi.org/10.1016/S1470-2045(19)30326-2
Bort,, G., Lux,, F., Dufort,, S., Crémillieux,, Y., Verry,, C., & Tillement,, O. (2020). EPR‐mediated tumor targeting using ultrasmall‐hybrid nanoparticles: From animal to human with theranostic AGuIX nanoparticles. Theranostics, 10(3), 1319–1331. https://doi.org/10.7150/thno.37543
Brun,, E., & Sicard‐Roselli,, C. (2016). Actual questions raised by nanoparticle radiosensitization. Radiation Physics and Chemistry, 128, 134–142. https://doi.org/10.1016/j.radphyschem.2016.05.024
Butterworth,, K. T., McMahon,, S. J., Currell,, F. J., & Prise,, K. M. (2012). Physical basis and biological mechanisms of gold nanoparticle radiosensitization. Nanoscale, 4(16), 4830–4838. Retrieved from http://www.scopus.com/inward/record.url?eid=2-s2.0-84864493211%26partnerID=40%26md5=dc6d8d62ad45aa56ee0706a57ac21da8
Butterworth,, K. T., McMahon,, S. J., Taggart,, L. E., & Prise,, K. M. (2013). Radiosensitization by gold nanoparticles: Effective at megavoltage energies and potential role of oxidative stress. Translational Cancer Research, 2(4), 269–279. https://doi.org/10.3978/j.issn.2218-676X.2013.08.03
Byrne,, H. L., Gholami,, Y., & Kuncic,, Z. (2017). Impact of fluorescence emission from gold atoms on surrounding biological tissue—Implications for nanoparticle radio‐enhancement. Physics in Medicine and Biology, 62(8), 3097–3110. https://doi.org/10.1088/1361-6560/aa6233
Cai,, R., & Chen,, C. (2019). The crown and the scepter: Roles of the protein corona in nanomedicine. Advanced Materials, 31(45), 1805740. https://doi.org/10.1002/adma.201805740
Cai,, X., Chen,, H. H., Wang,, C. L., Chen,, S. T., Lai,, S. F., Chien,, C. C., … Margaritondo,, G. (2011). Imaging the cellular uptake of tiopronin‐modified gold nanoparticles. Analytical and Bioanalytical Chemistry, 401, 809–816. https://doi.org/10.1007/s00216-011-4986-3
Carmona,, A., Roudeau,, S., L`Homel,, B., Pouzoulet,, F., Bonnet‐Boissinot,, S., Prezado,, Y., & Ortega,, R. (2017). Heterogeneous intratumoral distribution of gadolinium nanoparticles within U87 human glioblastoma xenografts unveiled by micro‐PIXE imaging. Analytical Biochemistry, 523, 50–57. https://doi.org/10.1016/j.ab.2017.02.010
Chandran,, P., Riviere,, J. E., & Monteiro‐Riviere,, N. A. (2017). Surface chemistry of gold nanoparticles determines the biocorona composition impacting cellular uptake, toxicity and gene expression profiles in human endothelial cells. Nanotoxicology, 11(4), 507–519. https://doi.org/10.1080/17435390.2017.1314036
Chen,, H. H., Chien,, C. C., Petibois,, C., Wang,, C. L., Chu,, Y. S., Lai,, S. F., … Margaritondo,, G. (2011). Quantitative analysis of nanoparticle internalization in mammalian cells by high resolution X‐ray microscopy. Journal of Nanobiotechnology, 9. Retrieved from http://www.scopus.com/inward/record.url?eid=2-s2.0-79953761257%26partnerID=40%26md5=c981c193d6a4a79811a28c492eae9eac, 14.
Cheng,, N. N., Starkewolf,, Z., Davidson,, R. A., Sharmah,, A., Lee,, C., Lien,, J., & Guo,, T. (2012). Chemical enhancement by nanomaterials under X‐ray irradiation. Journal of the American Chemical Society, 134(4), 1950–1953 Retrieved from http://www.scopus.com/inward/record.url?eid=2-s2.0-84856430020%26partnerID=40%26md5=334ef3a254a442470986fdaf543526f4
Chithrani,, D. B., Jelveh,, S., Jalali,, F., Van Prooijen,, M., Allen,, C., Bristow,, R. G., … Jaffray,, D. A. (2010). Gold nanoparticles as radiation sensitizers in cancer therapy. Radiation Research, 173(6), 719–728. https://doi.org/10.1667/RR1984.1
Chiu,, S. J., Lee,, M. Y., Chou,, W. G., & Lin,, L. Y. (2003). Germanium oxide enhances the radiosensitivity of cells. Radiation Research, 159(3), 391–400. https://doi.org/10.1667/0033-7587(2003)159[0391:GOETRO]2.0.CO;2
Cho,, J., Gonzalez‐Lepera,, C., Manohar,, N., Kerr,, M., Krishnan,, S., & Cho,, S. H. (2016). Quantitative investigation of physical factors contributing to gold nanoparticle‐mediated proton dose enhancement. Physics in Medicine and Biology, 61(6), 2562–2581. https://doi.org/10.1088/0031-9155/61/6/2562
Cho,, S. H. (2005). Estimation of tumour dose enhancement due to gold nanoparticles during typical radiation treatments: A preliminary Monte Carlo study. Physics in Medicine and Biology, 50(15), N163–N173. https://doi.org/10.1088/0031-9155/50/15/N01
Chompoosor,, A., Saha,, K., Ghosh,, P. S., MacArthy,, D. J., Miranda,, O. R., Zhu,, Z. J., … Rotello,, V. M. (2010). The role of surface functionality on acute cytotoxicity, ROS generation and DNA damage by cationic gold nanoparticles. Small, 6(20), 2246–2249. https://doi.org/10.1002/smll.201000463
Coulter,, J. A., Hyland,, W. B., Nicol,, J., & Currell,, F. J. (2013). Radiosensitising nanoparticles as novel cancer therapeutics—Pipe dream or realistic prospect? Clinical Oncology, 25(10), 593–603. https://doi.org/10.1016/j.clon.2013.06.011
Coulter,, J. A., Jain,, S., Butterworth,, K. T., Taggart,, L. E., Dickson,, G. R., McMahon,, S. J., … Prise,, K. M. (2012). Cell type‐dependent uptake, localization, and cytotoxicity of 1.9 nm gold nanoparticles. International Journal of Nanomedicine, 7, 2673–2685. https://doi.org/10.2147/IJN.S31751
Cui,, L., Her,, S., Dunne,, M., Borst,, G. R., De Souza,, R., Bristow,, R. G., … Allen,, C. (2017). Significant radiation enhancement effects by gold nanoparticles in combination with cisplatin in triple negative breast cancer cells and tumor xenografts. Radiation Research, 187(2), 147–160. https://doi.org/10.1667/RR14578.1
Detappe,, A., Kunjachan,, S., Rottmann,, J., Robar,, J., Tsiamas,, P., Korideck,, H., … Berbeco,, R. (2015). AGuIX nanoparticles as a promising platform for image‐guided radiation therapy. Cancer Nanotechnology, 6(1), 4. https://doi.org/10.1186/s12645-015-0012-3
Dimitriou,, N. M., Tsekenis,, G., Balanikas,, E. C., Pavlopoulou,, A., Mitsiogianni,, M., Mantso,, T., … Georgakilas,, A. G. (2017). Gold nanoparticles, radiations and the immune system: Current insights into the physical mechanisms and the biological interactions of this new alliance towards cancer therapy. Pharmacology and Therapeutics, 178, 1–17. https://doi.org/10.1016/j.pharmthera.2017.03.006
Din,, F. U., Aman,, W., Ullah,, I., Qureshi,, O. S., Mustapha,, O., Shafique,, S., & Zeb,, A. (2017). Effective use of nanocarriers as drug delivery systems for the treatment of selected tumors. International Journal of Nanomedicine, 12, 7291–7309. https://doi.org/10.2147/IJN.S146315
Ding,, L., Yao,, C., Yin,, X., Li,, C., Huang,, Y., Wu,, M., … Wu,, M. (2018). Size, shape, and protein corona determine cellular uptake and removal mechanisms of gold nanoparticles. Small, 14(42), 1–13. https://doi.org/10.1002/smll.201801451
Dufort,, S., Appelboom,, G., Verry,, C., Barbier,, E. L., Lux,, F., Bräuer‐Krisch,, E., … Le Duc,, G. (2019). Ultrasmall theranostic gadolinium‐based nanoparticles improve high‐grade rat glioma survival. Journal of Clinical Neuroscience, 67, 215–219. https://doi.org/10.1016/j.jocn.2019.05.065
Falk,, M. (2017). Nanodiamonds and nanoparticles as tumor cell radiosensitizers‐promising results but an obscure mechanism of action. Annals of Translational Medicine, 5(1), 1–4. https://doi.org/10.21037/atm.2016.12.62
Ferrero,, V., Visonà,, G., Dalmasso,, F., Gobbato,, A., Cerello,, P., Strigari,, L., … Attili,, A. (2017). Targeted dose enhancement in radiotherapy for breast cancer using gold nanoparticles, part 1: A radiobiological model study. Medical Physics, 44(5), 1983–1992. https://doi.org/10.1002/mp.12180
Foldbjerg,, R., Dang,, D. A., & Autrup,, H. (2011). Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Archives of Toxicology, 85(7), 743–750. https://doi.org/10.1007/s00204-010-0545-5
Fortuin,, A. S., Brüggemann,, R., van der Linden,, J., Panfilov,, I., Israël,, B., Scheenen,, T. W. J., & Barentsz,, J. O. (2018). Ultra‐small superparamagnetic iron oxides for metastatic lymph node detection: Back on the block. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, 10(1), e1471. https://doi.org/10.1002/wnan.1471
Ghita,, M., McMahon,, S. J., Taggart,, L. E., Butterworth,, K. T., Schettino,, G., & Prise,, K. M. (2017). A mechanistic study of gold nanoparticle radiosensitisation using targeted microbeam irradiation. Scientific Reports, 7, 1–12. https://doi.org/10.1038/srep44752
Gilles,, M., Brun,, E., & Sicard‐Roselli,, C. (2014). Gold nanoparticles functionalization notably decreases radiosensitization through hydroxyl radical production under ionizing radiation. Colloids and Surfaces B: Biointerfaces, 123, 770–777. https://doi.org/10.1016/j.colsurfb.2014.10.028
Grall,, R., Girard,, H., Saad,, L., Petit,, T., Gesset,, C., Combis‐Schlumberger,, M., … Chevillard,, S. (2015). Impairing the radioresistance of cancer cells by hydrogenated nanodiamonds. Biomaterials, 61, 290–298. https://doi.org/10.1016/j.biomaterials.2015.05.034
Grodzik,, M., Sawosz,, E., Wierzbicki,, M., Orlowski,, P., Hotowy,, A., Niemiec,, T., … Chwalibog,, A. (2011). Nanoparticles of carbon allotropes inhibit glioblastoma multiforme angiogenesis in vivo. International Journal of Nanomedicine, 6, 3041–3048 Retrieved from https://www.scopus.com/inward/record.uri?eid=2-s2.0-84862593862%26partnerID=40%26md5=ab2d321f8b5f00709baf1699ec5b662e
Grodzik,, M., Szczepaniak,, J., Strojny‐Cieslak,, B., Hotowy,, A., Wierzbicki,, M., Jaworski,, S., … Chwalibog,, A. (2019). Diamond nanoparticles downregulate expression of CycD and Cyce in glioma cells. Molecules, 24(8), 1–16. https://doi.org/10.3390/molecules24081549
Hainfeld,, J. F., Slatkin,, D. N., & Smilowitz,, H. M. (2004). The use of gold nanoparticles to enhance radiotherapy in mice. Physics in Medicine and Biology, 49, N309–N315.
Hatoyama,, K., Kitamura,, N., Takano‐Kasuya,, M., Tokunaga,, M., Oikawa,, T., Ohta,, M., … Gonda,, K. (2019). Quantitative analyses of amount and localization of radiosensitizer gold nanoparticles interacting with cancer cells to optimize radiation therapy. Biochemical and Biophysical Research Communications, 508(4), 1093–1100. https://doi.org/10.1016/j.bbrc.2018.12.016
Heckert,, E. G., Karakoti,, A. S., Seal,, S., & Self,, W. T. (2008). The role of cerium redox state in the SOD mimetic activity of nanoceria. Biomaterials, 29(18), 2705–2709. https://doi.org/10.1016/j.biomaterials.2008.03.014
Her,, S., Jaffray,, D. A., & Allen,, C. (2017). Gold nanoparticles for applications in cancer radiotherapy: Mechanisms and recent advancements. Advanced Drug Delivery Reviews, 109, 84–101. https://doi.org/10.1016/j.addr.2015.12.012
Herold,, D. M., Das,, I. J., Stobbe,, C. C., Iyer,, R. V., & Chapman,, J. D. (2000). Gold microspheres: A selective technique for producing biologically effective dose enhancement. International Journal of Radiation Biology, 76(10), 1357–1364 Retrieved from https://www.scopus.com/inward/record.uri?eid=2-s2.0-0033808270%26partnerID=40%26md5=ed386651ed0a2da7b83f5bfea9091301
Howard,, D., Sebastian,, S., Le,, Q. V.‐C., Thierry,, B., & Kempson,, I. (2020). Chemical mechanisms of nanoparticle Radiosensitization and radioprotection: A review of structure‐function relationships influencing reactive oxygen species. International Journal of Molecular Sciences, 21(2), 579.
Huang,, C. L., Hsiao,, I. L., Lin,, H. C., Wang,, C. F., Huang,, Y. J., & Chuang,, C. Y. (2015). Silver nanoparticles affect on gene expression of inflammatory and neurodegenerative responses in mouse brain neural cells. Environmental Research, 136, 253–263. https://doi.org/10.1016/j.envres.2014.11.006
Ito,, S., Miyoshi,, N., Degraff,, W. G., Nagashima,, K., Kirschenbaum,, L. J., & Riesz,, P. (2009). Enhancement of 5‐Aminolevulinic acid‐induced oxidative stress on two cancer cell lines by gold nanoparticles. Free Radical Research, 43(12), 1214–1224. https://doi.org/10.3109/10715760903271249
Ivošev,, V., Sánchez,, G. J., Stefancikova,, L., Haidar,, D. A., González Vargas,, C. R., Yang,, X., … Lacombe,, S. (2020). Uptake and excretion dynamics of gold nanoparticles in cancer cells and fibroblasts. Nanotechnology, 31(13), 135102. https://doi.org/10.1088/1361-6528/ab5d82
Jain,, S., Coulter,, J. A., Hounsell,, A. R., Butterworth,, K. T., McMahon,, S. J., Hyland,, W. B., … Hirst,, D. G. (2011). Cell‐specific radiosensitization by gold nanoparticles at megavoltage radiation energies. International Journal of Radiation Oncology Biology Physics, 79(2), 531–539. https://doi.org/10.1016/j.ijrobp.2010.08.044
Jayaram,, D. T., Runa,, S., Kemp,, M. L., & Payne,, C. K. (2017). Nanoparticle‐induced oxidation of corona proteins initiates an oxidative stress response in cells. Nanoscale, 9(22), 7595–7601. https://doi.org/10.1039/c6nr09500c
Jeynes,, J. C. G., Merchant,, M. J., Spindler,, A., Wera,, A. C., & Kirkby,, K. J. (2014). Investigation of gold nanoparticle radiosensitization mechanisms using a free radical scavenger and protons of different energies. Physics in Medicine and Biology, 59(21), 6431–6443. https://doi.org/10.1088/0031-9155/59/21/6431
Jia,, H. Y., Liu,, Y., Zhang,, X. J., Han,, L., Du,, L. B., Tian,, Q., & Xu,, Y. C. (2009). Potential oxidative stress of gold nanoparticles by induced‐NO releasing in serum. Journal of the American Chemical Society, 131(1), 40–41. https://doi.org/10.1021/ja808033w
Khan,, M. M., Ansari,, S. A., Pradhan,, D., Ansari,, M. O., Han,, D. H., Lee,, J., & Cho,, M. H. (2014). Band gap engineered TiO₂ nanoparticles for visible light induced photoelectrochemical and photocatalytic studies. Journal of Materials Chemistry A, 2(3), 637–644. https://doi.org/10.1039/c3ta14052k
Kiessling,, F., Mertens,, M. E., Grimm,, J., & Lammers,, T. (2014). Nanoparticles for imaging: Top or flop? Radiology, 273(1), 10–28. https://doi.org/10.1148/radiol.14131520
Kim,, J. A., Aberg,, C., Salvati,, A., & Dawson,, K. A. (2012). Role of cell cycle on the cellular uptake and dilution of nanoparticles in a cell population. Nature Nanotechnology, 7(1), 62–68. https://doi.org/10.1038/nnano.2011.191
Kim,, J. K., Seo,, S. J., Kim,, K. H., Kim,, T. J., Chung,, M. H., Kim,, K. R., & Yang,, T. K. (2010). Therapeutic application of metallic nanoparticles combined with particle‐induced X‐ray emission effect. Nanotechnology, 21(42), 425102. https://doi.org/10.1088/0957-4484/21/42/425102
Klein,, S., Dell`Arciprete,, M. L., Wegmann,, M., Distel,, L. V. R., Neuhuber,, W., Gonzalez,, M. C., & Kryschi,, C. (2013). Oxidized silicon nanoparticles for radiosensitization of cancer and tissue cells. Biochemical and Biophysical Research Communications, 434(2), 217–222. https://doi.org/10.1016/j.bbrc.2013.03.042
Köhler,, C., Foiato,, T., Marnitz,, S., Schneider,, A., Le,, X., Dogan,, N. U., … Favero,, G. (2016). Potential surgical and oncologic consequences related to skin tattoos in the treatment of cervical cancer. Journal of Minimally Invasive Gynecology, 23(7), 1083–1087. https://doi.org/10.1016/j.jmig.2016.07.016
Kotb,, S., Detappe,, A., Lux,, F., Appaix,, F., Barbier,, E. L., Tran,, V. L., … Sancey,, L. (2016). Gadolinium‐based nanoparticles and radiation therapy for multiple brain melanoma metastases: Proof of concept before phase I trial. Theranostics, 6(3), 418–427. https://doi.org/10.7150/thno.14018
Krischer,, B., Forte,, S., Niemann,, T., Kubik‐Huch,, R. A., & Leo,, C. (2018). Feasibility of breast MRI after sentinel procedure for breast cancer with superparamagnetic tracers. European Journal of Surgical Oncology, 44(1), 74–79. https://doi.org/10.1016/j.ejso.2017.11.016
Le Duc,, G., Roux,, S., Paruta‐Tuarez,, A., Dufort,, S., Brauer,, E., Marais,, A., … Tillement,, O. (2014). Advantages of gadolinium based ultrasmall nanoparticles vs molecular gadolinium chelates for radiotherapy guided by MRI for glioma treatment. Cancer Nanotechnology, 5(1), 1–14. https://doi.org/10.1186/s12645-014-0004-8
Le Goas,, M., Paquirissamy,, A., Gargouri,, D., Fadda,, G., Testard,, F., Aymes‐Chodur,, C., … Carrot,, G. (2019). Irradiation effects on polymer‐grafted gold nanoparticles for cancer therapy. ACS Applied Bio Materials, 2(1), 144–154. https://doi.org/10.1021/acsabm.8b00484
Leung,, M. K. K., Chow,, J. C. L., Chithrani,, B. D., Lee,, M. J. G., Oms,, B., & Jaffray,, D. A. (2011). Irradiation of gold nanoparticles by x‐rays: Monte Carlo simulation of dose enhancements and the spatial properties of the secondary electrons production. Medical Physics, 38(2), 624–631. https://doi.org/10.1118/1.3539623
Lin,, Y., McMahon,, S. J., Scarpelli,, M., Paganetti,, H., & Schuemann,, J. (2014). Comparing gold nano‐particle enhanced radiotherapy with protons, megavoltage photons and kilovoltage photons: A Monte Carlo simulation. Physics in Medicine and Biology, 59(24), 7675–7689. https://doi.org/10.1088/0031-9155/59/24/7675
Liu,, C. J., Wang,, C. H., Chen,, S. T., Chen,, H. H., Leng,, W. H., Chien,, C. C., … Margaritondo,, G. (2010). Enhancement of cell radiation sensitivity by pegylated gold nanoparticles. Physics in Medicine and Biology, 55(4), 931–945 Retrieved from http://www.scopus.com/inward/record.url?eid=2-s2.0-76149129758%26partnerID=40%26md5=37564ce820a5414f5585dafc4c8aff79
Liu,, T., Kempson,, I., De Jonge,, M., Howard,, D. L., & Thierry,, B. (2014). Quantitative synchrotron X‐ray fluorescence study of the penetration of transferrin‐conjugated gold nanoparticles inside model tumour tissues. Nanoscale, 6(16), 9774–9782. Retrieved from http://www.scopus.com/inward/record.url?eid=2-s2.0-84905166057%26partnerID=40%26md5=00c716580ce500ef3a5b2565fcda0b18
Liu,, Y., Liu,, X., Jin,, X., He,, P., Zheng,, X., Dai,, Z., … Li,, Q. (2015). The dependence of radiation enhancement effect on the concentration of gold nanoparticles exposed to low‐ and high‐LET radiations. Physica Medica, 31(3), 210–218. https://doi.org/10.1016/j.ejmp.2015.01.006
Lorek,, A., Stojčev,, Z., Zarębski,, W., Kowalczyk,, M., & Szyluk,, K. (2019). Analysis of postoperative complications after 303 sentinel lymph node identification procedures using the sentimag® method in breast cancer patients. Medical Science Monitor, 25, 3154–3160. https://doi.org/10.12659/MSM.912758
Luchette,, M., Korideck,, H., Makrigiorgos,, M., Tillement,, O., & Berbeco,, R. (2014). Radiation dose enhancement of gadolinium‐based AGuIX nanoparticles on HeLa cells. Nanomedicine: Nanotechnology, Biology, and Medicine, 10(8), 1751–1755. https://doi.org/10.1016/j.nano.2014.06.004
Lux,, F., Tran,, V. L., Thomas,, E., Dufort,, S., Rossetti,, F., Martini,, M., … Tillement,, O. (2019). AGuiX® from bench to bedside‐transfer of an ultrasmall theranostic gadolinium‐based nanoparticle to clinical medicine. British Journal of Radiology, 92(1093), 20180365. https://doi.org/10.1259/bjr.20180365
Ma,, N., Liu,, P., He,, N., Gu,, N., Wu,, F. G., & Chen,, Z. (2017). Action of gold Nanospikes‐based Nanoradiosensitizers: Cellular internalization, radiotherapy, and autophagy. ACS Applied Materials and Interfaces, 9(37), 31526–31542. https://doi.org/10.1021/acsami.7b09599
Ma,, N., Wu,, F. G., Zhang,, X., Jiang,, Y. W., Jia,, H. R., Wang,, H. Y., … Chen,, Z. (2017). Shape‐dependent radiosensitization effect of gold nanostructures in cancer radiotherapy: Comparison of gold nanoparticles, nanospikes, and nanorods. ACS Applied Materials and Interfaces, 9(15), 13037–13048. https://doi.org/10.1021/acsami.7b01112
Maeda,, H., Tsukigawa,, K., & Fang,, J. (2016). A retrospective 30 years after discovery of the enhanced permeability and retention effect of solid tumors: Next‐generation chemotherapeutics and photodynamic therapy—Problems, solutions, and prospects. Microcirculation, 23(3), 173–182. https://doi.org/10.1111/micc.12228
Maggiorella,, L., Barouch,, G., Devaux,, C., Pottier,, A., Deutsch,, E., Bourhis,, J., … Levy,, L. (2012). Nanoscale radiotherapy with hafnium oxide nanoparticles. Future Oncology, 8(9), 1167–1181. https://doi.org/10.2217/fon.12.96
Marill,, J., Anesary,, N. M., Zhang,, P., Vivet,, S., Borghi,, E., Levy,, L., & Pottier,, A. (2014). Hafnium oxide nanoparticles: Toward an in vitro predictive biological effect? Radiation Oncology, 9(1), 1–11. https://doi.org/10.1186/1748-717X-9-150
Martin,, F., Burrow,, P. D., Cai,, Z., Cloutier,, P., Hunting,, D., & Sanche,, L. (2004). DNA strand breaks induced by 0‐4 eV electrons: The role of shape resonances. Physical Review Letters, 93(6), 68101–68104. https://doi.org/10.1103/PhysRevLett.93.068101
McMahon,, S. J., Hyland,, W. B., Muir,, M. F., Coulter,, J. A., Jain,, S., Butterworth,, K. T., … Currell,, F. J. (2011). Biological consequences of nanoscale deposition near irradiated heavy atom nanoparticles. Scientific Reports, 1(18), 1–8.
McQuaid,, H. N., Muir,, M. F., Taggart,, L. E., McMahon,, S. J., Coulter,, J. A., Hyland,, W. B., … Currell,, F. J. (2016). Imaging and radiation effects of gold nanoparticles in tumour cells. Scientific Reports, 6, 1–10. https://doi.org/10.1038/srep19442
Mishra,, P., Nayak,, B., & Dey,, R. K. (2016). PEGylation in anti‐cancer therapy: An overview. Asian Journal of Pharmaceutical Sciences, 11(3), 337–348. https://doi.org/10.1016/j.ajps.2015.08.011
Mousavi,, M., Nedaei,, H. A., Khoei,, S., Eynali,, S., Khoshgard,, K., Robatjazi,, M., & Iraji Rad,, R. (2017). Enhancement of radiosensitivity of melanoma cells by pegylated gold nanoparticles under irradiation of megavoltage electrons. International Journal of Radiation Biology, 93(2), 214–221. https://doi.org/10.1080/09553002.2017.1231944
Nel,, A., Xia,, T., Mädler,, L., & Li,, N. (2006). Toxic potential of materials at the nanolevel. Science, 311(5761), 622–627. https://doi.org/10.1126/science.1114397
Nicol,, J. R., Harrison,, E., O`Neill,, S. M., Dixon,, D., McCarthy,, H. O., & Coulter,, J. A. (2018). Unraveling the cell‐type dependent radiosensitizing effects of gold through the development of a multifunctional gold nanoparticle. Nanomedicine: Nanotechnology, Biology, and Medicine, 14(2), 439–449. https://doi.org/10.1016/j.nano.2017.11.019
Pagáčová,, E., Štefančíková,, L., Schmidt‐Kaler,, F., Hildenbrand,, G., Vičar,, T., Depeš,, D., … Falk,, M. (2019). Challenges and contradictions of metal nano‐particle applications for radio‐sensitivity enhancement in cancer therapy. International Journal of Molecular Sciences, 20(3), 1–25. https://doi.org/10.3390/ijms20030588
Pan,, Y., Leifert,, A., Ruau,, D., Neuss,, S., Bornemann,, J., Schmid,, G., … Jahnen‐Dechent,, W. (2009). Gold nanoparticles of diameter 1.4 nm trigger necrosis by oxidative stress and mitochondrial damage. Small, 5(18), 2067–2076. https://doi.org/10.1002/smll.200900466
Patra,, H. K., Banerjee,, S., Chaudhuri,, U., Lahiri,, P., & Dasgupta,, A. K. (2007). Cell selective response to gold nanoparticles. Nanomedicine: Nanotechnology, Biology, and Medicine, 3(2), 111–119. https://doi.org/10.1016/j.nano.2007.03.005
Penninckx,, S., Heuskin,, A. C., Michiels,, C., & Lucas,, S. (2018). The role of thioredoxin reductase in gold nanoparticle radiosensitization effects. Nanomedicine, 13(22), 2917–2937. https://doi.org/10.2217/nnm-2018-0171
Penninckx,, S., Heuskin,, A. C., Michiels,, C., & Lucas,, S. (2019). Thioredoxin reductase activity predicts gold nanoparticle radiosensitization effect. Nanomaterials, 9(2), 1–13. https://doi.org/10.3390/nano9020295
Peukert,, D., Incerti,, S., Kempson,, I., Douglass,, M., Karamitros,, M., Baldacchino,, G., & Bezak,, E. (2019). Validation and investigation of reactive species yields of Geant4‐DNA chemistry models. Medical Physics, 46(2), 983–998. https://doi.org/10.1002/mp.13332
Peukert,, D., Kempson,, I., Douglass,, M., & Bezak,, E. (2018). Metallic nanoparticle radiosensitisation of ion radiotherapy: A review. Physica Medica, 47, 121–128. https://doi.org/10.1016/j.ejmp.2018.03.004
Peukert,, D., Kempson,, I., Douglass,, M., & Bezak,, E. (2019). Gold nanoparticle enhanced proton therapy: Monte Carlo modeling of reactive species` distributions around a gold nanoparticle and the effects of nanoparticle proximity and clustering. International Journal of Molecular Sciences, 20(17), 1–22. https://doi.org/10.3390/ijms20174280
Peukert,, D., Kempson,, I., Douglass,, M., & Bezak,, E. (2020). Gold nanoparticle enhanced proton therapy: A Monte Carlo simulation of the effects of proton energy, nanoparticle size, coating material and coating thickness on dose and radiolysis yield. Medical Physics, 47(2), 651–661. https://doi.org/10.1002/mp.13923
Pirmohamed,, T., Dowding,, J. M., Singh,, S., Wasserman,, B., Heckert,, E., Karakoti,, A. S., … Self,, W. T. (2010). Nanoceria exhibit redox state‐dependent catalase mimetic activity. Chemical Communications, 46(16), 2736–2738. https://doi.org/10.1039/b922024k
Popov,, A. L., Zaichkina,, S. I., Popova,, N. R., Rozanova,, O. M., Romanchenko,, S. P., Ivanova,, O. S., … Ivanov,, V. K. (2016). Radioprotective effects of ultra‐small citrate‐stabilized cerium oxide nanoparticles in vitro and in vivo. RSC Advances, 6(108), 106141–106149. https://doi.org/10.1039/c6ra18566e
Porcel,, E., Kobayashi,, K., Usami,, N., Remita,, H., Le Sech,, C., & Lacombe,, S. (2011). Photosensitization of plasmid‐DNA loaded with platinum nano‐particles and irradiated by low energy X‐rays. Paper presented at the Journal of Physics: Conference Series.
Rieck,, K., Bromma,, K., Sung,, W., Bannister,, A., Schuemann,, J., & Chithrani,, D. B. (2019). Modulation of gold nanoparticle mediated radiation dose enhancement through synchronization of breast tumor cell population. British Journal of Radiology, 92(1100), 20190283. https://doi.org/10.1259/bjr.20190283
Rima,, W., Sancey,, L., Aloy,, M. T., Armandy,, E., Alcantara,, G. B., Epicier,, T., … Perriat,, P. (2013). Internalization pathways into cancer cells of gadolinium‐based radiosensitizing nanoparticles. Biomaterials, 34(1), 181–195. https://doi.org/10.1016/j.biomaterials.2012.09.029
Roa,, W., Zhang,, X., Guo,, L., Shaw,, A., Hu,, X., Xiong,, Y., … Xing,, J. Z. (2009). Gold nanoparticle sensitize radiotherapy of prostate cancer cells by regulation of the cell cycle. Nanotechnology, 20(37), 1–9. https://doi.org/10.1088/0957-4484/20/37/375101
Rosa,, S., Connolly,, C., Schettino,, G., Butterworth,, K. T., & Prise,, K. M. (2017). Biological mechanisms of gold nanoparticle radiosensitization. Cancer Nanotechnology, 8(1), 2. https://doi.org/10.1186/s12645-017-0026-0
Runa,, S., Lakadamyali,, M., Kemp,, M. L., & Payne,, C. K. (2017). TiO₂ nanoparticle‐induced oxidation of the plasma membrane: Importance of the protein corona. Journal of Physical Chemistry B, 121(37), 8619–8625. https://doi.org/10.1021/acs.jpcb.7b04208
Ruoslahti,, E. (2017). Tumor penetrating peptides for improved drug delivery. Advanced Drug Delivery Reviews, 110–111, 3–12. https://doi.org/10.1016/j.addr.2016.03.008
Sancey,, L., Kotb,, S., Truillet,, C., Appaix,, F., Marais,, A., Thomas,, E., … Tillement,, O. (2015). Long‐term in vivo clearance of gadolinium‐based AGuIX nanoparticles and their biocompatibility after systemic injection. ACS Nano, 9(3), 2477–2488. https://doi.org/10.1021/acsnano.5b00552
Sancey,, L., Lux,, F., Kotb,, S., Roux,, S., Dufort,, S., Bianchi,, A., … Tillement,, O. (2014). The use of theranostic gadolinium‐based nanoprobes to improve radiotherapy efficacy. British Journal of Radiology, 87(1041), 20140134. https://doi.org/10.1259/bjr.20140134
Sanche,, L. (2016). Interaction of low energy electrons with DNA: Applications to cancer radiation therapy. Radiation Physics and Chemistry, 128, 36–43. https://doi.org/10.1016/j.radphyschem.2016.05.008
Schuemann,, J., Berbeco,, R., Chithrani,, D. B., Cho,, S. H., Kumar,, R., McMahon,, S. J., … Krishnan,, S. (2016). Roadmap to clinical use of gold nanoparticles for radiation sensitization. International Journal of Radiation Oncology Biology Physics, 94(1), 189–205. https://doi.org/10.1016/j.ijrobp.2015.09.032
Shah,, N. B., Dong,, J., & Bischof,, J. C. (2011). Cellular uptake and nanoscale localization of gold nanoparticles in cancer using label‐free confocal Raman microscopy. Molecular Pharmaceutics, 8(1), 176–184. https://doi.org/10.1021/mp1002587
Sicard‐Roselli,, C., Brun,, E., Gilles,, M., Baldacchino,, G., Kelsey,, C., McQuaid,, H., … Currell,, F. (2014). A new mechanism for hydroxyl radical production in irradiated nanoparticle solutions. Small, 10(16), 3338–3346. https://doi.org/10.1002/smll.201400110
Simon,, V., Ceccaldi,, A., & Lévy,, L. (2010). Activatable nanoparticles for cancer treatment. Nanobiotix. Nanoscience: Nanobiotechnology and Nanobiology, 1121–1141. https://doi.org/10.1007/978-3-540-88633-4_25
Smith,, C. L., Ackerly,, T., Best,, S. P., Gagliardi,, F., Kie,, K., Little,, P. J., … Geso,, M. (2015). Determination of dose enhancement caused by gold‐nanoparticles irradiated with proton, X‐rays (kV and MV) and electron beams, using alanine/EPR dosimeters. Radiation Measurements, 82, 122–128. https://doi.org/10.1016/j.radmeas.2015.09.008
Sotiropoulos,, M., Henthorn,, N. T., Warmenhoven,, J. W., Mackay,, R. I., Kirkby,, K. J., & Merchant,, M. J. (2017). Modelling direct DNA damage for gold nanoparticle enhanced proton therapy. Nanoscale, 9(46), 18413–18422. https://doi.org/10.1039/c7nr07310k
Štefanciková,, L., Lacombe,, S., Salado,, D., Porcel,, E., Pagáčová,, E., Tillement,, O., … Falk,, M. (2016). Effect of gadolinium‐based nanoparticles on nuclear DNA damage and repair in glioblastoma tumor cells. Journal of Nanobiotechnology, 14(1), 1–15. https://doi.org/10.1186/s12951-016-0215-8
Taggart,, L. E., McMahon,, S. J., Currell,, F. J., Prise,, K. M., & Butterworth,, K. T. (2014). The role of mitochondrial function in gold nanoparticle mediated radiosensitisation. Cancer Nanotechnology, 5(1), 1–12. https://doi.org/10.1186/s12645-014-0005-7
Tamura,, D., Maeda,, D., Terada,, Y., & Goto,, A. (2019). Distribution of tattoo pigment in lymph nodes dissected for gynecological malignancy. International Journal of Surgical Pathology, 27(7), 773–777. https://doi.org/10.1177/1066896919846395
Taupin,, F., Flaender,, M., Delorme,, R., Brochard,, T., Mayol,, J. F., Arnaud,, J., … Elleaume,, H. (2015). Gadolinium nanoparticles and contrast agent as radiation sensitizers. Physics in Medicine and Biology, 60(11), 4449–4464. https://doi.org/10.1088/0031-9155/60/11/4449
Turnbull,, T., Douglass,, M., Williamson,, N. H., Howard,, D., Bhardwaj,, R., Lawrence,, M., … Kempson,, I. M. (2019). Cross‐correlative single‐cell analysis reveals biological mechanisms of nanoparticle radiosensitization. ACS Nano, 13(5), 5077–5090. https://doi.org/10.1021/acsnano.8b07982
Turnbull,, T., Thierry,, B., & Kempson,, I. (2019). A quantitative study of intercellular heterogeneity in gold nanoparticle uptake across multiple cell lines. Analytical and Bioanalytical Chemistry, 411(28), 7529–7538. https://doi.org/10.1007/s00216-019-02154-w
Verry,, C., Dufort,, S., Barbier,, E. L., Montigon,, O., Peoc`H,, M., Chartier,, P., … Le Duc,, G. (2016). MRI‐guided clinical 6‐MV radiosensitization of glioma using a unique gadolinium‐based nanoparticles injection. Nanomedicine, 11(18), 2405–2417. https://doi.org/10.2217/nnm-2016-0203
Verry,, C., Sancey,, L., Dufort,, S., Le Duc,, G., Mendoza,, C., Lux,, F., … Balosso,, J. (2019). Treatment of multiple brain metastases using gadolinium nanoparticles and radiotherapy: NANO‐RAD, a phase I study protocol. BMJ Open, 9(2), e023591. https://doi.org/10.1136/bmjopen-2018-023591
Vilotte,, F., Jumeau,, R., & Bourhis,, J. (2019). High Z nanoparticles and radiotherapy: A critical view. The Lancet Oncology, 20(10), e557. https://doi.org/10.1016/S1470-2045(19)30579-0
Vu,, V. P., Gifford,, G. B., Chen,, F., Benasutti,, H., Wang,, G., Groman,, E. V., … Simberg,, D. (2019). Immunoglobulin deposition on biomolecule corona determines complement opsonization efficiency of preclinical and clinical nanoparticles. Nature Nanotechnology, 14(3), 260–268. https://doi.org/10.1038/s41565-018-0344-3
Wang,, C., Jiang,, Y., Li,, X., & Hu,, L. (2015). Thioglucose‐bound gold nanoparticles increase the radiosensitivity of a triple‐negative breast cancer cell line (MDA‐MB‐231). Breast Cancer, 22(4), 413–420. https://doi.org/10.1007/s12282-013-0496-9
Wang,, C. H., Liu,, C. J., Chien,, C. C., Chen,, H. T., Hua,, T. E., Leng,, W. H., … Margaritondo,, G. (2011). X‐ray synthesized PEGylated (polyethylene glycol coated) gold nanoparticles in mice strongly accumulate in tumors. Materials Chemistry and Physics, 126(1–2), 352–356 Retrieved from http://www.scopus.com/inward/record.url?eid=2-s2.0-78751630389%26partnerID=40%26md5=703a8bf02961fb27f202406de12c3d35
Wang,, J., Deng,, X., Zhang,, F., Chen,, D., & Ding,, W. (2014). ZnO nanoparticle‐induced oxidative stress triggers apoptosis by activating JNK signaling pathway in cultured primary astrocytes. Nanoscale Research Letters, 9(1), 117. https://doi.org/10.1186/1556-276X-9-117
Wason,, M. S., Colon,, J., Das,, S., Seal,, S., Turkson,, J., Zhao,, J., & Baker,, C. H. (2013). Sensitization of pancreatic cancer cells to radiation by cerium oxide nanoparticle‐induced ROS production. Nanomedicine: Nanotechnology, Biology, and Medicine, 9(4), 558–569. https://doi.org/10.1016/j.nano.2012.10.010
Wu,, H., Lin,, J., Liu,, P., Huang,, Z., Zhao,, P., Jin,, H., … Gu,, N. (2015). Is the autophagy a friend or foe in the silver nanoparticles associated radiotherapy for glioma? Biomaterials, 62, 47–57. https://doi.org/10.1016/j.biomaterials.2015.05.033
Xie,, W. Z., Friedland,, W., Li,, W. B., Li,, C. Y., Oeh,, U., Qiu,, R., … Hoeschen,, C. (2015). Simulation on the molecular radiosensitization effect of gold nanoparticles in cells irradiated by x‐rays. Physics in Medicine and Biology, 60(16), 6195–6212. https://doi.org/10.1088/0031-9155/60/16/6195
Xu,, W., Luo,, T., Pang,, B., Li,, P., Zhou,, C., Huang,, P., … Fu,, S. (2012). The radiosensitization of melanoma cells by gold nanorods irradiated with MV X‐ray. Nano Biomedicine and Engineering, 4(1), 6–11. https://doi.org/10.5101/nbe.v4i1.p6-11
Yao,, X., Huang,, C., Chen,, X., Zheng,, Y., & Sanche,, L. (2015). Chemical radiosensitivity of DNA induced by gold nanoparticles. Journal of Biomedical Nanotechnology, 11(3), 478–485. https://doi.org/10.1166/jbn.2015.1922
Yasui,, H., Takeuchi,, R., Nagane,, M., Meike,, S., Nakamura,, Y., Yamamori,, T., … Inanami,, O. (2014). Radiosensitization of tumor cells through endoplasmic reticulum stress induced by PEGylated nanogel containing gold nanoparticles. Cancer Letters, 347(1), 151–158. https://doi.org/10.1016/j.canlet.2014.02.005
Zhang,, X., Liu,, Z., Lou,, Z., Chen,, F., Chang,, S., Miao,, Y., … Zhang,, H. (2018). Radiosensitivity enhancement of Fe₃O₄@Ag nanoparticles on human glioblastoma cells. Artificial Cells, Nanomedicine and Biotechnology, 46(sup1), 975–984. https://doi.org/10.1080/21691401.2018.1439843
Zhang,, X., Wang,, H., Coulter,, J. A., & Yang,, R. (2018). Octaarginine‐modified gold nanoparticles enhance the radiosensitivity of human colorectal cancer cell line LS180 to megavoltage radiation. International Journal of Nanomedicine, 13, 3541–3552. https://doi.org/10.2147/IJN.S161157
Zheng,, Y., Cloutier,, P., Hunting,, D. J., & Sanche,, L. (2008). Radiosensitization by gold nanoparticles: Comparison of DNA damage induced by low and high‐energy electrons. Journal of Biomedical Nanotechnology, 4(4), 469–473. https://doi.org/10.1166/jbn.2008.012
Zheng,, Y., Cloutier,, P., Hunting,, D. J., Sanche,, L., & Wagner,, J. R. (2005). Chemical basis of DNA sugar‐phosphate cleavage by low‐energy electrons. Journal of the American Chemical Society, 127(47), 16592–16598. https://doi.org/10.1021/ja054129q
Zhu,, C. D., Zheng,, Q., Wang,, L. X., Xu,, H. F., Tong,, J. L., Zhang,, Q. A., … Wu,, J. Q. (2015). Synthesis of novel galactose functionalized gold nanoparticles and its radiosensitizing mechanism. Journal of Nanobiotechnology, 13(1), 67. https://doi.org/10.1186/s12951-015-0129-x

Access to this WIREs title is by subscription only.

Recommend to Your
Librarian Now!

Mechanisms of nanoparticle radiosensitization

Browse by Topic

Access to this WIREs title is by subscription only.

The latest WIREs articles in your inbox