Crushed Gold Shell Nanoparticles Labeled with Radioactive Iodine as a Theranostic Nanoplatform for Macrophage-Mediated Photothermal Therapy
Corresponding Author: Yong Hyun Jeon
Nano-Micro Letters,
Vol. 11 (2019), Article Number: 36
Abstract
Plasmonic nanostructure-mediated photothermal therapy (PTT) has proven to be a promising approach for cancer treatment, and new approaches for its effective delivery to tumor lesions are currently being developed. This study aimed to assess macrophage-mediated delivery of PTT using radioiodine-124-labeled gold nanoparticles with crushed gold shells (124I-Au@AuCBs) as a theranostic nanoplatform. 124I-Au@AuCBs exhibited effective photothermal conversion effects both in vitro and in vivo and were efficiently taken up by macrophages without cytotoxicity. After the administration of 124I-Au@AuCB-labeled macrophages to colon tumors, intensive signals were observed at tumor lesions, and subsequent in vivo PTT with laser irradiation yielded potent antitumor effects. The results indicate the considerable potential of 124I-Au@AuCBs as novel theranostic nanomaterials and the prominent advantages of macrophage-mediated cellular therapies in treating cancer and other diseases.
Highlights:
1 Crushed gold shell radionuclide nanoballs (124I-Au@AuCBs) were fabricated as unique photothermal therapeutics and nuclear medicine imaging nanoplatforms.
2 Macrophage-mediated delivery of 124I-Au@AuCBs and their potential photothermal therapy applications were demonstrated in mice with colon cancer.
Keywords
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X. Ji, R. Shao, A.M. Elliott, R.J. Stafford, E. Esparza-Coss et al., Bifunctional gold nanoshells with a superparamagnetic iron oxide–silica core suitable for both MR imaging and photothermal therapy. J. Phys. Chem. C 111(17), 6245–6251 (2007). https://doi.org/10.1021/jp0702245
H. Liu, D. Chen, L. Li, T. Liu, L. Tan, X. Wu, F. Tang, Multifunctional gold nanoshells on silica nanorattles: a platform for the combination of photothermal therapy and chemotherapy with low systemic toxicity. Angew. Chem. Int. Ed. 50(4), 891–895 (2011). https://doi.org/10.1002/anie.201002820
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Y. Wang, K.C. Black, H. Luehmann, W. Li, Y. Zhang et al., Comparison study of gold nanohexapods, nanorods, and nanocages for photothermal cancer treatment. ACS Nano 7(3), 2068–2077 (2013). https://doi.org/10.1021/nn304332s
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A.Z. Wang, R. Langer, O.C. Farokhzad, Nanoparticle delivery of cancer drugs. Annu. Rev. Med. 63, 185–198 (2012). https://doi.org/10.1146/annurev-med-040210-162544
X. Yi, K. Yang, C. Liang, X. Zhong, P. Ning et al., Imaging-guided combined photothermal and radiotherapy to treat subcutaneous and metastatic tumors using iodine-131-doped copper sulfide nanoparticles. Adv. Funct. Mater. 25(29), 4689–4699 (2015). https://doi.org/10.1002/adfm.201502003
T.D. Yang, W. Choi, T.H. Yoon, K.J. Lee, J.-S. Lee et al., In vivo photothermal treatment by the peritumoral injection of macrophages loaded with gold nanoshells. Biomed. Opt. Express 7(1), 185–193 (2016). https://doi.org/10.1364/BOE.7.000185
B.-K. Wang, X.-F. Yu, J.-H. Wang, Z.-B. Li, P.-H. Li, H. Wang, L. Song, P.K. Chu, C. Li, Gold-nanorods-siRNA nanoplex for improved photothermal therapy by gene silencing. Biomaterials 78, 27–39 (2016). https://doi.org/10.1016/j.biomaterials.2015.11.025
Y. Liu, M. Yang, J. Zhang, X. Zhi, C. Li, C. Zhang, F. Pan, K. Wang, Y. Yang, J. Martinez de la Fuentea, Human induced pluripotent stem cells for tumor targeted delivery of gold nanorods and enhanced photothermal therapy. ACS Nano 10(2), 2375–2385 (2016). https://doi.org/10.1021/acsnano.5b07172
S. Tang, M. Chen, N. Zheng, Sub-10-nm Pd nanosheets with renal clearance for efficient near-infrared photothermal cancer therapy. Small 10(15), 3139–3144 (2014). https://doi.org/10.1002/smll.201303631
S. Kang, S.H. Bhang, S. Hwang, J.K. Yoon, J. Song, H.K. Jang, S. Kim, B.S. Kim, Mesenchymal stem cells aggregate and deliver gold nanoparticles to tumors for photothermal therapy. ACS Nano 9(10), 9678–9690 (2015). https://doi.org/10.1021/acsnano.5b02207
M.-R. Choi, K.J. Stanton-Maxey, J.K. Stanley, C.S. Levin et al., A cellular trojan horse for delivery of therapeutic nanoparticles into tumors. Nano Lett. 7(12), 3759–3765 (2007). https://doi.org/10.1021/nl072209h
S.J. Madsen, S.-K. Baek, A.R. Makkouk, T. Krasieva, H. Hirschberg, Macrophages as cell-based delivery systems for nanoshells in photothermal therapy. Annu. Biomed. Eng. 40(2), 507–515 (2012). https://doi.org/10.1007/s10439-011-0415-1
J. Choi, H.-Y. Kim, E.J. Ju, J. Jung, J. Park et al., Use of macrophages to deliver therapeutic and imaging contrast agents to tumors. Biomaterials 33(16), 4195–4203 (2012). https://doi.org/10.1016/j.biomaterials.2012.02.022
M.T. Stephan, S.B. Stephan, P. Bak, J. Chen, D.J. Irvine, Synapse-directed delivery of immunomodulators using t-cell-conjugated nanoparticles. Biomaterials 33(23), 5776–5787 (2012). https://doi.org/10.1016/j.biomaterials.2012.04.029
Z. Li, H. Huang, S. Tang, Y. Li, X.-F. Yu et al., Small gold nanorods laden macrophages for enhanced tumor coverage in photothermal therapy. Biomaterials 74, 144–154 (2016). https://doi.org/10.1016/j.biomaterials.2015.09.038
S.B. Lee, D. Kumar, Y. Li, I.-K. Lee, S.J. Cho et al., Pegylated crushed gold shell-radiolabeled core nanoballs for in vivo tumor imaging with dual positron emission tomography and cerenkov luminescent imaging. J. Nanobiotechnol. 16(1), 41 (2018). https://doi.org/10.1186/s12951-018-0366-x
S.B. Lee, S.-W. Lee, S.Y. Jeong, G. Yoon, S.J. Cho et al., Engineering of radioiodine-labeled gold core–shell nanoparticles as efficient nuclear medicine imaging agents for trafficking of dendritic cells. ACS Appl. Mater. Interfaces 9(10), 8480–8489 (2017). https://doi.org/10.1021/acsami.6b14800
X. Cheng, X. Tian, A. Wu, J. Li, J. Tian et al., Protein corona influences cellular uptake of gold nanoparticles by phagocytic and nonphagocytic cells in a size-dependent manner. ACS Appl. Mater. Interfaces 7(37), 20568–20575 (2015). https://doi.org/10.1021/acsami.5b04290
A. Aderem, D.M. Underhill, Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17(1), 593–623 (1999). https://doi.org/10.1146/annurev.immunol.17.1.593
D.J. Irvine, M.C. Hanson, K. Rakhra, T. Tokatlian, Synthetic nanoparticles for vaccines and immunotherapy. Chem. Rev. 115(19), 11109–11146 (2015). https://doi.org/10.1021/acs.chemrev.5b00109
A.C. Anselmo, S. Mitragotri, Cell-mediated delivery of nanoparticles: taking advantage of circulatory cells to target nanoparticles. J. Control Release 190, 531–541 (2014). https://doi.org/10.1016/j.jconrel.2014.03.050