journal article·2018-04Open access

Multimodal selenium nanoshell-capped Au@mSiO2 nanoplatform for NIR-responsive chemo-photothermal therapy against metastatic breast cancer

Thiruganesh Ramasamy, Hima Bindu Ruttala, Pasupathi Sundaramoorthy, Bijay Kumar Poudel, Yu Seok Youn, Sae Kwang Ku, Han-Gon Choi, Chul Soon Yong, Jong Oh Kim

NPG Asia Materials· Volume 10· Issue 4

Abstract

Multimodal therapeutic agents based on novel nanomaterials for multidrug resistance have attracted increasing attention in cancer therapy. In this study, we describe the construction of a programmed mesoporous silica-capped gold nanorod covered with nano-selenium overcoat (Se@Au@mSiO 2 ) nanoparticles as a multifunctional nanoplatform to incorporate materials with specific chemotherapeutic, chemoprevention, and photoablation/hyperthermia functions that collectively contribute to enhance anticancer efficacy in multidrug-resistant breast cancer. The triplecombination-based nanosized Se@Au@mSiO 2 /DOX effectively accumulates in the tumor and the release of the therapeutic cargo could be remotely manipulated by mild near-infrared (NIR) irradiation. Se@Au@mSiO 2 /DOX notably enhances the cell killing effect through induction of cell apoptosis. In addition, Se@Au@mSiO 2 /DOX inhibits tumor cell growth through cell cycle arrest and induction of apoptosis via suppression of the Src/FAK/AKT signaling pathways. Synergistic Se-photothermal-chemotherapy combination exhibits significant tumor growth suppression and delayed tumor progression in vivo. Immunohistochemistry analysis shows elevated numbers of caspase-3 and PARPimmunolabeled cells and decreased Ki-67 + and CD31 + cancer cells in the tumor mass. No noticeable signs of organ damage or toxicity are observed after treatment with Se@Au@mSiO 2 /DOX (NIR+), which is further supported by hematology and biochemical analyses. Thus, Se@Au@mSiO 2 /DOX has potential for the clinical treatment of metastatic breast cancers with little or no adverse effects.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: Nanoplatforms for cancer theranostics · Advanced Nanomaterials in Catalysis · Selenium in Biological Systems

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (46)

Show source-provided references
1. Ferlay, J. et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer 127, 2893–2917 (2010).10.1002/ijc.25516 ↗
2. Yager, P. et al. Microfluidic diagnostic technologies for global public health. Nature 442, 412–418 (2006).10.1038/nature05064 ↗
3. Peer, D. et al. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2, 751–760 (2007).10.1038/nnano.2007.387 ↗
4. Du, Q. et al. Synergistic anticancer effects of curcumin and resveratrol in Hepa1-6 hepatocellular carcinoma cells. Oncol. Rep. 29, 1851–1858 (2013).10.3892/or.2013.2310 ↗
5. Qiu, L. et al. A cell-targeted, size-photocontrollable, nuclear-uptake nanodrug delivery system for drug-resistant cancer therapy. Nano Lett. 15, 457–463 (2014).10.1021/nl503777s ↗
6. Rayman, M. P. The importance of selenium to human health. Lancet 356, 233–241 (2000).10.1016/S0140-6736(00)02490-9 ↗
7. Hu, H. et al. Methylseleninic acid enhances taxane drug efficacy against human prostate cancer and down-regulates antiapoptotic proteins Bcl-XL and surviving. Clin. Cancer Res. 14, 1150–1158 (2008).10.1158/1078-0432.CCR-07-4037 ↗
8. Sun, D. et al. The effects of luminescent ruthenium (II) polypyridyl functionalized selenium nanoparticles on bFGF-induced angiogenesis and AKT/ERK signaling. Biomaterials 34, 171–180 (2013).10.1016/j.biomaterials.2012.09.031 ↗
9. Liu, W. et al. Selenium nanoparticles as a carrier of 5-fluorouracil to achieve anticancer synergism. ACS Nano 6, 6578–6591 (2012).10.1021/nn202452c ↗
10. Fakih, M., Cao, S., Durrani, F. A. & Rustum, Y. M. Selenium protects against toxicity induced by anticancer drugs and augments antitumor activity: a highly selective, new, and novel approach for the treatment of solid tumors. Clin. Colorectal Cancer 5, 132–135 (2005).10.3816/CCC.2005.n.026 ↗
11. Zhang, J., Wang, X. & Xu, T. Elemental selenium at nano size (Nano-Se) as a potential chemopreventive agent with reduced risk of selenium toxicity: comparison with se-methylselenocysteine in mice. Toxicol. Sci. 101, 22–31 (2008).10.1093/toxsci/kfm221 ↗
12. Ramasamy, T. et al. Smart chemistry-based nanosized drug delivery systems for systemic applications: A comprehensive review. J Control. Release 258, 226–253 (2017).10.1016/j.jconrel.2017.04.043 ↗
13. You, J. et al. Effective photothermal chemotherapy using doxorubicin-loaded gold nanospheres that target EphB4 receptors in tumors. Cancer Res. 72, 4777–4786 (2012).10.1158/0008-5472.CAN-12-1003 ↗
14. Hyvärinen, M. Ultraviolet Light Protection and Weathering Properties of Wood-polypropylene Composites. Doctoral Dissertation, Acta Universitatis Lappeenrantaensis (2014).
15. Li, X., Takashima, M., Yuba, E., Harada, A. & Kono, K. PEGylated PAMAM dendrimer–doxorubicin conjugate-hybridized gold nanorod for combined photothermal-chemotherapy. Biomaterials 35, 6576–6584 (2014).10.1016/j.biomaterials.2014.04.043 ↗
16. Huang, X., Jain, P. K., El-Sayed, I. H. & El-Sayed, M. A. Plasmonic photothermal therapy (PPTT) using gold nanoparticles. Lasers Med. Sci. 23, 217–228 (2008).10.1007/s10103-007-0470-x ↗
17. Dykman, L. & Khlebtsov, N. Gold nanoparticles in biomedical applications: recent advances and perspectives. Chem. Soc. Rev. 41, 2256–2282 (2012).10.1039/C1CS15166E ↗
18. Hauck, T. S., Jennings, T. L., Yatsenko, T., Kumaradas, J. C. & Chan, W. C. Enhancing the toxicity of cancer chemotherapeutics with gold nanorod hyperthermia. Adv. Mater. 20, 3832–3838 (2008).10.1002/adma.200800921 ↗
19. You, J., Zhang, G. & Li, C. Exceptionally high payload of doxorubicin in hollow gold nanospheres for near-infrared light-triggered drug release. ACS Nano 4, 1033–1041 (2010).10.1021/nn901181c ↗
20. Shen, S. et al. Targeting mesoporous silica-encapsulated gold nanorods for chemo-photothermal therapy with near-infrared radiation. Biomaterials 34, 3150–3158 (2013).10.1016/j.biomaterials.2013.01.051 ↗
21. DeLisser, H. et al. Vascular endothelial platelet endothelial cell adhesion molecule 1 (PECAM-1) regulates advanced metastatic progression. Proc. Natl Acad. Sci. 107, 18616–18621 (2010).10.1073/pnas.1004654107 ↗
22. Awasthi, N., Zhang, C., Ruan, W., Schwarz, M. A. & Schwarz, R. E. BMS-754807, a small-molecule inhibitor of insulin-like growth factor-1 receptor/insulin receptor, enhances gemcitabine response in pancreatic cancer. Mol. Cancer Ther. 11, 2644–2653 (2012).10.1158/1535-7163.MCT-12-0447 ↗
23. Sau, T. K. & Murphy, C. J. Seeded high yield synthesis of short Au nanorods in aqueous solution. Langmuir 20, 6414–6420 (2004).10.1021/la049463z ↗
24. Ramasamy, T. et al. pH sensitive polyelectrolyte complex micelles for highly effective combination chemotherapy. J. Mater. Chem. B 2, 6324–6333 (2014).10.1039/C4TB00867G ↗
25. Ramasamy, T. et al. Layer-by-layer assembly of liposomal nanoparticles with PEGylated polyelectrolytes enhances systemic delivery of multiple anticancer drugs. Acta Biomater. 10, 5116–5127 (2014).10.1016/j.actbio.2014.08.021 ↗
26. Ramasamy, T. et al. Layer-by-layer coated lipid–polymer hybrid nanoparticles designed for use in anticancer drug delivery. Carbohydr. Polym. 102, 653–661 (2014).10.1016/j.carbpol.2013.11.009 ↗
27. Ramasamy, T. et al. Chitosan-based polyelectrolyte complexes as potential nanoparticulate carriers: physicochemical and biological characterization. Pharm. Res. 31, 1302–1314 (2014).10.1007/s11095-013-1251-9 ↗
28. Zhang, Z., Wang, J. & Chen, C. Near‐infrared light‐mediated nanoplatforms for cancer thermo‐chemotherapy and optical imaging. Adv. Mater. 25, 3869–3880 (2013).10.1002/adma.201301890 ↗
29. Ramasamy, T. et al. Engineering of a lipid-polymer nanoarchitectural platform for highly effective combination therapy of doxorubicin and irinotecan. Chem. Commun. 51, 5758–5761 (2015).10.1039/C5CC00482A ↗
30. Ramasamy, T., Kim, J., Choi, H. G., Yong, C. S. & Kim, J. O. Novel dual drug-loaded block ionomer complex micelles for enhancing the efficacy of chemotherapy treatments. J. Biomed. Nanotechnol. 10, 1304–1312 (2014).10.1166/jbn.2014.1821 ↗
31. Varkouhi, A. K., Scholte, M., Storm, G. & Haisma, H. J. Endosomal escape pathways for delivery of biologicals. J. Control. Release 151, 220–228 (2011).10.1016/j.jconrel.2010.11.004 ↗
32. Tran, T. H. et al. Tumor-targeting, pH-sensitive nanoparticles for docetaxel delivery to drug-resistant cancer cells. Int. J. Nanomed. 10, 5249 (2015).
33. Ramasamy, T. et al. Engineering of cell microenvironment-responsive polypeptide nanovehicle co-encapsulating a synergistic combination of small molecules for effective chemotherapy in solid tumors. Acta Biomater. 48, 131–143 (2017).10.1016/j.actbio.2016.10.034 ↗
34. Ramasamy, T. et al. Cationic drug-based self-assembled polyelectrolyte complex micelles: Physicochemical, pharmacokinetic, and anticancer activity analysis. Colloids Surf. B: Biointerfaces 146, 152–160 (2016).10.1016/j.colsurfb.2016.06.004 ↗
35. Shrestha, R., Elsabahy, M., Florez-Malaver, S., Samarajeewa, S. & Wooley, K. L. Endosomal escape and siRNA delivery with cationic shell crosslinked knedel-like nanoparticles with tunable buffering capacities. Biomaterials 33, 8557–8568 (2012).10.1016/j.biomaterials.2012.07.054 ↗
36. Meng, H. et al. Use of size and a copolymer design feature to improve the biodistribution and the enhanced permeability and retention effect of doxorubicin-loaded mesoporous silica nanoparticles in a murine xenograft tumor model. ACS Nano 5, 4131–4144 (2011).10.1021/nn200809t ↗
37. Suematsu, N., Hosoda, M. & Fujimori, K. Protective effects of quercetin against hydrogen peroxide-induced apoptosis in human neuronal SH-SY5Y cells. Neurosci. Lett. 504, 223–227 (2011).10.1016/j.neulet.2011.09.028 ↗
38. Gorrini, C., Harris, I. S. & Mak, T. W. Modulation of oxidative stress as an anticancer strategy. Nat. Rev. Drug Discov. 12, 931–947 (2013).10.1038/nrd4002 ↗
39. Broude, E. et al. p21Waf1/Cip1/Sdi1 mediates retinoblastoma protein degradation. Oncogene 26, 6954–6958 (2007).10.1038/sj.onc.1210516 ↗
40. Sundaramoorthy, P. et al. Engineering of caveolae-specific self-micellizing anticancer lipid nanoparticles to enhance the chemotherapeutic efficacy of oxaliplatin in colorectal cancer cells. Acta Biomater. 42, 220–231 (2016).10.1016/j.actbio.2016.07.006 ↗
41. Falck, J., Mailand, N., Syljuåsen, R. G., Bartek, J. & Lukas, J. The ATM–Chk2–Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 410, 842–847 (2001).10.1038/35071124 ↗
42. Ruttala, H. B. et al. Molecularly targeted co-delivery of a histone deacetylase inhibitor and paclitaxel by lipid-protein hybrid nanoparticles for synergistic combinational chemotherapy. Oncotarget 8, 14925 (2017).10.18632/oncotarget.14742 ↗
43. Ruttala, H. B. et al. Multiple polysaccharide-drug complex-loaded liposomes: A unique strategy in drug loading and cancer targeting. Carbohydr. Polym. 176, 57–66 (2017).10.1016/j.carbpol.2017.05.062 ↗
44. Fang, E. F. et al. Trichosanthin inhibits breast cancer cell proliferation in both cell lines and nude mice by promotion of apoptosis. PLoS ONE 7, e41592 (2012).10.1371/journal.pone.0041592 ↗
45. Qin, Y. et al. Cardamonin exerts potent activity against multiple myeloma through blockade of NF-κB pathway in vitro. Leuk. Res. 36, 514–520 (2012).10.1016/j.leukres.2011.11.014 ↗
46. Ramasamy, T. et al. Polypeptide-based micelles for delivery of irinotecan: physicochemical and in vivo characterization. Pharm. Res. 32, 1947–1956 (2015).10.1007/s11095-014-1588-8 ↗