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Erschienen in: Clinical and Translational Oncology 4/2019

08.10.2018 | Research Article

Modulation of cancer cells’ radiation response in the presence of folate conjugated Au@Fe2O3 nanocomplex as a targeted radiosensitizer

verfasst von: M. Mirrahimi, V. Hosseini, A. Shakeri-Zadeh, Z. Alamzadeh, S. K. Kamrava, N. Attaran, Z. Abed, H. Ghaznavi, S. M. A. Hosseini Nami

Erschienen in: Clinical and Translational Oncology | Ausgabe 4/2019

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Abstract

Objectives

To investigate the effects of Au@Fe2O3 core–shell nanoparticle (NP), with and without conjugation to folic acid (FA) as a targeting ligand, on radiosensitization of both cancer and healthy cells.

Methods

Au@Fe2O3 NPs were first synthesized, then modified with FA, and finally characterized. Radiation dose enhancement studies were performed on KB cancer cells and L929 healthy cells. NPs at the concentration of 20 µg/ml were first incubated with both cell lines and then different doses of 6 MV X-ray radiation were examined. The end effects were evaluated via MTT assay and flow cytometry using AnnexinV/PI kit.

Results

It was indicated that viability of KB cells has a much lower rate than L929 cells when the cells were treated by {(FA-Au@Fe2O3) + (X-ray)} regimen. Cell viability was even decreased significantly when X-ray dose increased. Moreover, flow cytometry studies revealed that FA-targeted NPs induced higher level of apoptosis for KB cancer cells than L929 healthy cells.

Conclusion

Our findings provide a new perspective on high ability of the synthesized FA-targeted Au@Fe2O3 NPs which may be considered as an efficient radiosensitizer in the process of targeted radiation therapy of cancer.
Literatur
2.
Zurück zum Zitat Ryu JH, Lee S, Son S, Kim SH, Leary JF, Choi K, et al. Theranostic nanoparticles for future personalized medicine. J Control Release. 2014;190:477–84.CrossRefPubMed Ryu JH, Lee S, Son S, Kim SH, Leary JF, Choi K, et al. Theranostic nanoparticles for future personalized medicine. J Control Release. 2014;190:477–84.CrossRefPubMed
3.
Zurück zum Zitat Wang C, Jiang Y, Li X, Hu L. Thioglucose-bound gold nanoparticles increase the radiosensitivity of a triple-negative breast cancer cell line (MDA-MB-231). Breast Cancer. 2015;22(4):413–20.CrossRefPubMed Wang C, Jiang Y, Li X, Hu L. Thioglucose-bound gold nanoparticles increase the radiosensitivity of a triple-negative breast cancer cell line (MDA-MB-231). Breast Cancer. 2015;22(4):413–20.CrossRefPubMed
4.
Zurück zum Zitat Liu J, Yang Y, Zhu W, Yi X, Dong Z, Xu X, et al. Nanoscale metal − organic frameworks for combined photodynamic & radiation therapy in cancer treatment. Biomaterials. 2016;97:1–9.CrossRefPubMed Liu J, Yang Y, Zhu W, Yi X, Dong Z, Xu X, et al. Nanoscale metal − organic frameworks for combined photodynamic & radiation therapy in cancer treatment. Biomaterials. 2016;97:1–9.CrossRefPubMed
5.
Zurück zum Zitat Deng Y, Li E, Cheng X, Zhu J, Lu S, Ge C, et al. Facile preparation of hybrid core–shell nanorods for photothermal and radiation combined therapy. Nanoscale. 2016;8(7):3895–9.CrossRefPubMed Deng Y, Li E, Cheng X, Zhu J, Lu S, Ge C, et al. Facile preparation of hybrid core–shell nanorods for photothermal and radiation combined therapy. Nanoscale. 2016;8(7):3895–9.CrossRefPubMed
6.
Zurück zum Zitat Kumar A, Zhang X, Liang X-J. Gold nanoparticles: emerging paradigm for targeted drug delivery system. Biotechnol Adv. 2013;31(5):593–606.CrossRefPubMed Kumar A, Zhang X, Liang X-J. Gold nanoparticles: emerging paradigm for targeted drug delivery system. Biotechnol Adv. 2013;31(5):593–606.CrossRefPubMed
7.
Zurück zum Zitat Rana S, Bajaj A, Mout R, Rotello VM. Monolayer coated gold nanoparticles for delivery applications. Adv Drug Deliv Rev. 2012;64(2):200–16.CrossRefPubMed Rana S, Bajaj A, Mout R, Rotello VM. Monolayer coated gold nanoparticles for delivery applications. Adv Drug Deliv Rev. 2012;64(2):200–16.CrossRefPubMed
8.
Zurück zum Zitat Al Zaki A, Cormode D, Tsourkas A, Dorsey JF. Increasing the therapeutic efficacy of radiotherapy using nanoparticles. Increasing the therapeutic ratio of radiotherapy. Berlin: Springer; 2017. p. 241–65.CrossRef Al Zaki A, Cormode D, Tsourkas A, Dorsey JF. Increasing the therapeutic efficacy of radiotherapy using nanoparticles. Increasing the therapeutic ratio of radiotherapy. Berlin: Springer; 2017. p. 241–65.CrossRef
9.
Zurück zum Zitat Her S, Jaffray DA, Allen C. Gold nanoparticles for applications in cancer radiotherapy: mechanisms and recent advancements. Advanced drug delivery reviews. 2017;109:84–101.CrossRefPubMed Her S, Jaffray DA, Allen C. Gold nanoparticles for applications in cancer radiotherapy: mechanisms and recent advancements. Advanced drug delivery reviews. 2017;109:84–101.CrossRefPubMed
10.
Zurück zum Zitat Shakeri-Zadeh A, Shiran M-B, Khoee S, Sharifi AM, Ghaznavi H, Khoei S. A new magnetic nanocapsule containing 5-fluorouracil: in vivo drug release, anti-tumor, and pro-apoptotic effects on CT26 cells allograft model. J Biomater Appl. 2014;29(4):548–56.CrossRefPubMed Shakeri-Zadeh A, Shiran M-B, Khoee S, Sharifi AM, Ghaznavi H, Khoei S. A new magnetic nanocapsule containing 5-fluorouracil: in vivo drug release, anti-tumor, and pro-apoptotic effects on CT26 cells allograft model. J Biomater Appl. 2014;29(4):548–56.CrossRefPubMed
11.
Zurück zum Zitat Lucarini M, Franchi P, Pedulli GF, Pengo P, Scrimin P, Pasquato L. EPR study of dialkyl nitroxides as probes to investigate the exchange of solutes between the ligand shell of monolayers of protected gold nanoparticles and aqueous solutions. J Am Chem Soc. 2004;126(30):9326–9.CrossRefPubMed Lucarini M, Franchi P, Pedulli GF, Pengo P, Scrimin P, Pasquato L. EPR study of dialkyl nitroxides as probes to investigate the exchange of solutes between the ligand shell of monolayers of protected gold nanoparticles and aqueous solutions. J Am Chem Soc. 2004;126(30):9326–9.CrossRefPubMed
12.
Zurück zum Zitat Boisselier E, Astruc D. Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity. Chem Soc Rev. 2009;38(6):1759–82.CrossRefPubMed Boisselier E, Astruc D. Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity. Chem Soc Rev. 2009;38(6):1759–82.CrossRefPubMed
16.
Zurück zum Zitat Zhang X, Xing JZ, Chen J, Ko L, Amanie J, Gulavita S, et al. Enhanced radiation sensitivity in prostate cancer by gold-nanoparticles. Clin Invest Med. 2008;31(3):160–7.CrossRef Zhang X, Xing JZ, Chen J, Ko L, Amanie J, Gulavita S, et al. Enhanced radiation sensitivity in prostate cancer by gold-nanoparticles. Clin Invest Med. 2008;31(3):160–7.CrossRef
17.
Zurück zum Zitat Kong T, Zeng J, Wang X, Yang X, Yang J, McQuarrie S, et al. Enhancement of radiation cytotoxicity in Breast-cancer cells by localized attachment of gold nanoparticles. Small. 2008;4(9):1537–43.CrossRefPubMed Kong T, Zeng J, Wang X, Yang X, Yang J, McQuarrie S, et al. Enhancement of radiation cytotoxicity in Breast-cancer cells by localized attachment of gold nanoparticles. Small. 2008;4(9):1537–43.CrossRefPubMed
18.
Zurück zum Zitat Zhang X-D, Wu D, Shen X, Chen J, Sun Y-M, Liu P-X, et al. Size-dependent radiosensitization of PEG-coated gold nanoparticles for cancer radiation therapy. Biomaterials. 2012;33(27):6408–19.CrossRefPubMed Zhang X-D, Wu D, Shen X, Chen J, Sun Y-M, Liu P-X, et al. Size-dependent radiosensitization of PEG-coated gold nanoparticles for cancer radiation therapy. Biomaterials. 2012;33(27):6408–19.CrossRefPubMed
19.
Zurück zum Zitat Hainfeld JF, Smilowitz HM, O’Connor MJ, Dilmanian FA, Slatkin DN. Gold nanoparticle imaging and radiotherapy of brain tumors in mice. Nanomedicine. 2013;8(10):1601–9.CrossRefPubMed Hainfeld JF, Smilowitz HM, O’Connor MJ, Dilmanian FA, Slatkin DN. Gold nanoparticle imaging and radiotherapy of brain tumors in mice. Nanomedicine. 2013;8(10):1601–9.CrossRefPubMed
20.
Zurück zum Zitat Tsiamas P, Liu B, Cifter F, Ngwa WF, Berbeco RI, Kappas C, et al. Impact of beam quality on megavoltage radiotherapy treatment techniques utilizing gold nanoparticles for dose enhancement. Phys Med Biol. 2013;58(3):451.CrossRefPubMed Tsiamas P, Liu B, Cifter F, Ngwa WF, Berbeco RI, Kappas C, et al. Impact of beam quality on megavoltage radiotherapy treatment techniques utilizing gold nanoparticles for dose enhancement. Phys Med Biol. 2013;58(3):451.CrossRefPubMed
21.
Zurück zum Zitat Eyvazzadeh N, Shakeri-Zadeh A, Fekrazad R, Amini E, Ghaznavi H, Kamrava SK. Gold-coated magnetic nanoparticle as a nanotheranostic agent for magnetic resonance imaging and photothermal therapy of cancer. Lasers Med Sci. 2017;32(7):1469–77.CrossRefPubMed Eyvazzadeh N, Shakeri-Zadeh A, Fekrazad R, Amini E, Ghaznavi H, Kamrava SK. Gold-coated magnetic nanoparticle as a nanotheranostic agent for magnetic resonance imaging and photothermal therapy of cancer. Lasers Med Sci. 2017;32(7):1469–77.CrossRefPubMed
22.
Zurück zum Zitat Wang L, Park H-Y, Stephanie I, Lim I, Schadt MJ, Mott D, et al. Core@ shell nanomaterials: gold-coated magnetic oxide nanoparticles. J Mater Chem. 2008;18(23):2629–35.CrossRef Wang L, Park H-Y, Stephanie I, Lim I, Schadt MJ, Mott D, et al. Core@ shell nanomaterials: gold-coated magnetic oxide nanoparticles. J Mater Chem. 2008;18(23):2629–35.CrossRef
23.
Zurück zum Zitat Beik J, Khademi S, Attaran N, Sarkar S, Shakeri-Zadeh A, Ghaznavi H, et al. A nanotechnology-based strategy to increase the efficiency of cancer diagnosis and therapy: folate-conjugated gold nanoparticles. Curr Med Chem. 2017;24(39):4399–416.CrossRefPubMed Beik J, Khademi S, Attaran N, Sarkar S, Shakeri-Zadeh A, Ghaznavi H, et al. A nanotechnology-based strategy to increase the efficiency of cancer diagnosis and therapy: folate-conjugated gold nanoparticles. Curr Med Chem. 2017;24(39):4399–416.CrossRefPubMed
24.
Zurück zum Zitat Samadian H, Hosseini-Nami S, Kamrava SK, Ghaznavi H, Shakeri-Zadeh A. Folate-conjugated gold nanoparticle as a new nanoplatform for targeted cancer therapy. J Cancer Res Clin Oncol. 2016;142(11):2217–29.CrossRefPubMed Samadian H, Hosseini-Nami S, Kamrava SK, Ghaznavi H, Shakeri-Zadeh A. Folate-conjugated gold nanoparticle as a new nanoplatform for targeted cancer therapy. J Cancer Res Clin Oncol. 2016;142(11):2217–29.CrossRefPubMed
25.
Zurück zum Zitat Mirrahimi M, Hosseini V, Kamrava SK, Attaran N, Beik J, Kooranifar S, et al. Selective heat generation in cancer cells using a combination of 808 nm laser irradiation and the folate-conjugated Fe2O3@ Au nanocomplex. Artificial cells, nanomedicine, and biotechnology. 2017:1–13. Mirrahimi M, Hosseini V, Kamrava SK, Attaran N, Beik J, Kooranifar S, et al. Selective heat generation in cancer cells using a combination of 808 nm laser irradiation and the folate-conjugated Fe2O3@ Au nanocomplex. Artificial cells, nanomedicine, and biotechnology. 2017:1–13.
26.
Zurück zum Zitat Shakeri-Zadeh A, Khoee S, Shiran M-B, Sharifi AM, Khoei S. Synergistic effects of magnetic drug targeting using a newly developed nanocapsule and tumor irradiation by ultrasound on CT26 tumors in BALB/c mice. J Mater Chem B. 2015;3(9):1879–87.CrossRef Shakeri-Zadeh A, Khoee S, Shiran M-B, Sharifi AM, Khoei S. Synergistic effects of magnetic drug targeting using a newly developed nanocapsule and tumor irradiation by ultrasound on CT26 tumors in BALB/c mice. J Mater Chem B. 2015;3(9):1879–87.CrossRef
27.
Zurück zum Zitat Sivakumar B, Aswathy RG, Sreejith R, Nagaoka Y, Iwai S, Suzuki M, et al. Bacterial exopolysaccharide based magnetic nanoparticles: a versatile nanotool for cancer cell imaging, targeted drug delivery and synergistic effect of drug and hyperthermia mediated cancer therapy. J Biomed Nanotechnol. 2014;10(6):885–99.CrossRefPubMed Sivakumar B, Aswathy RG, Sreejith R, Nagaoka Y, Iwai S, Suzuki M, et al. Bacterial exopolysaccharide based magnetic nanoparticles: a versatile nanotool for cancer cell imaging, targeted drug delivery and synergistic effect of drug and hyperthermia mediated cancer therapy. J Biomed Nanotechnol. 2014;10(6):885–99.CrossRefPubMed
28.
Zurück zum Zitat Banu H, Stanley B, Faheem S, Seenivasan R, Premkumar K, Vasanthakumar G. Thermal chemosensitization of breast cancer cells to cyclophosphamide treatment using folate receptor targeted gold nanoparticles. Plasmonics. 2014;9(6):1341–9.CrossRef Banu H, Stanley B, Faheem S, Seenivasan R, Premkumar K, Vasanthakumar G. Thermal chemosensitization of breast cancer cells to cyclophosphamide treatment using folate receptor targeted gold nanoparticles. Plasmonics. 2014;9(6):1341–9.CrossRef
29.
Zurück zum Zitat Beik J, Abed Z, Ghoreishi FS, Hosseini-Nami S, Mehrzadi S, Shakeri-Zadeh A, et al. Nanotechnology in hyperthermia cancer therapy: from fundamental principles to advanced applications. J Control Release. 2016;235:205–21.CrossRefPubMed Beik J, Abed Z, Ghoreishi FS, Hosseini-Nami S, Mehrzadi S, Shakeri-Zadeh A, et al. Nanotechnology in hyperthermia cancer therapy: from fundamental principles to advanced applications. J Control Release. 2016;235:205–21.CrossRefPubMed
30.
Zurück zum Zitat Chithrani BD, Ghazani AA, Chan WC. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 2006;6(4):662–8.CrossRef Chithrani BD, Ghazani AA, Chan WC. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 2006;6(4):662–8.CrossRef
31.
Zurück zum Zitat Hu R, Zheng M, Wu J, Li C, Shen D, Yang D, et al. Core-Shell magnetic gold nanoparticles for magnetic field-enhanced radio-photothermal therapy in cervical cancer. Nanomaterials. 2017;7(5):111.CrossRefPubMedCentral Hu R, Zheng M, Wu J, Li C, Shen D, Yang D, et al. Core-Shell magnetic gold nanoparticles for magnetic field-enhanced radio-photothermal therapy in cervical cancer. Nanomaterials. 2017;7(5):111.CrossRefPubMedCentral
32.
Zurück zum Zitat Peng X-H, Qian X, Mao H, Wang AY. Targeted magnetic iron oxide nanoparticles for tumor imaging and therapy. Int J Nanomed. 2008;3(3):311. Peng X-H, Qian X, Mao H, Wang AY. Targeted magnetic iron oxide nanoparticles for tumor imaging and therapy. Int J Nanomed. 2008;3(3):311.
33.
Zurück zum Zitat Chomoucka J, Drbohlavova J, Huska D, Adam V, Kizek R, Hubalek J. Magnetic nanoparticles and targeted drug delivering. Pharmacol Res. 2010;62(2):144–9.CrossRefPubMed Chomoucka J, Drbohlavova J, Huska D, Adam V, Kizek R, Hubalek J. Magnetic nanoparticles and targeted drug delivering. Pharmacol Res. 2010;62(2):144–9.CrossRefPubMed
34.
Zurück zum Zitat Wolfe T, Chatterjee D, Lee J, Grant JD, Bhattarai S, Tailor R, et al. Targeted gold nanoparticles enhance sensitization of prostate tumors to megavoltage radiation therapy in vivo. Nanomed Nanotechnol Biol Med. 2015;11(5):1277–83.CrossRef Wolfe T, Chatterjee D, Lee J, Grant JD, Bhattarai S, Tailor R, et al. Targeted gold nanoparticles enhance sensitization of prostate tumors to megavoltage radiation therapy in vivo. Nanomed Nanotechnol Biol Med. 2015;11(5):1277–83.CrossRef
35.
Zurück zum Zitat Khoei S, Mahdavi SR, Fakhimikabir H, Shakeri-Zadeh A, Hashemian A. The role of iron oxide nanoparticles in the radiosensitization of human prostate carcinoma cell line DU145 at megavoltage radiation energies. Int J Radiat Biol. 2014;90(5):351–6.CrossRefPubMed Khoei S, Mahdavi SR, Fakhimikabir H, Shakeri-Zadeh A, Hashemian A. The role of iron oxide nanoparticles in the radiosensitization of human prostate carcinoma cell line DU145 at megavoltage radiation energies. Int J Radiat Biol. 2014;90(5):351–6.CrossRefPubMed
36.
Zurück zum Zitat Khoshgard K, Hashemi B, Arbabi A, Rasaee MJ, Soleimani M. Radiosensitization effect of folate-conjugated gold nanoparticles on HeLa cancer cells under orthovoltage superficial radiotherapy techniques. Phys Med Biol. 2014;59(9):2249.CrossRefPubMed Khoshgard K, Hashemi B, Arbabi A, Rasaee MJ, Soleimani M. Radiosensitization effect of folate-conjugated gold nanoparticles on HeLa cancer cells under orthovoltage superficial radiotherapy techniques. Phys Med Biol. 2014;59(9):2249.CrossRefPubMed
37.
Zurück zum Zitat Gao B, Shen L, He K-W, Xiao W-H. GNRs@ SiO2-FA in combination with radiotherapy induces the apoptosis of HepG2 cells by modulating the expression of apoptosis-related proteins. Int J Mol Med. 2015;36(5):1282–90.CrossRefPubMedPubMedCentral Gao B, Shen L, He K-W, Xiao W-H. GNRs@ SiO2-FA in combination with radiotherapy induces the apoptosis of HepG2 cells by modulating the expression of apoptosis-related proteins. Int J Mol Med. 2015;36(5):1282–90.CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat Neshastehriz A, Tabei M, Maleki S, Eynali S, Shakeri-Zadeh A. Photothermal therapy using folate conjugated gold nanoparticles enhances the effects of 6MV X-ray on mouth epidermal carcinoma cells. J Photochem Photobiol, B. 2017;172:52–60.CrossRef Neshastehriz A, Tabei M, Maleki S, Eynali S, Shakeri-Zadeh A. Photothermal therapy using folate conjugated gold nanoparticles enhances the effects of 6MV X-ray on mouth epidermal carcinoma cells. J Photochem Photobiol, B. 2017;172:52–60.CrossRef
39.
Zurück zum Zitat Wyllie AH, Kerr JR, Currie A. Cell death: the significance of apoptosis. Int Rev Cytol. 1980;68:251–306.CrossRefPubMed Wyllie AH, Kerr JR, Currie A. Cell death: the significance of apoptosis. Int Rev Cytol. 1980;68:251–306.CrossRefPubMed
40.
Zurück zum Zitat Dewey WC, Ling CC, Meyn RE. Radiation-induced apoptosis: relevance to radiotherapy. Int J Radiat Oncol Biol Phys. 1995;33(4):781–96.CrossRefPubMed Dewey WC, Ling CC, Meyn RE. Radiation-induced apoptosis: relevance to radiotherapy. Int J Radiat Oncol Biol Phys. 1995;33(4):781–96.CrossRefPubMed
41.
Zurück zum Zitat Cohen-Jonathan E, Bernhard EJ, McKenna WG. How does radiation kill cells? Curr Opin Chem Biol. 1999;3(1):77–83.CrossRef Cohen-Jonathan E, Bernhard EJ, McKenna WG. How does radiation kill cells? Curr Opin Chem Biol. 1999;3(1):77–83.CrossRef
43.
Zurück zum Zitat Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer. 2002;2(4):277–88.CrossRef Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer. 2002;2(4):277–88.CrossRef
44.
Zurück zum Zitat Li P, Y-w S, Li B-x X, W-c SZ-l, Zhou C, et al. Photo-thermal effect enhances the efficiency of radiotherapy using Arg-Gly-Asp peptides-conjugated gold nanorods that target αvβ3 in melanoma cancer cells. J Nanobiotechnol. 2015;13(1):52.CrossRef Li P, Y-w S, Li B-x X, W-c SZ-l, Zhou C, et al. Photo-thermal effect enhances the efficiency of radiotherapy using Arg-Gly-Asp peptides-conjugated gold nanorods that target αvβ3 in melanoma cancer cells. J Nanobiotechnol. 2015;13(1):52.CrossRef
Metadaten
Titel
Modulation of cancer cells’ radiation response in the presence of folate conjugated Au@Fe2O3 nanocomplex as a targeted radiosensitizer
verfasst von
M. Mirrahimi
V. Hosseini
A. Shakeri-Zadeh
Z. Alamzadeh
S. K. Kamrava
N. Attaran
Z. Abed
H. Ghaznavi
S. M. A. Hosseini Nami
Publikationsdatum
08.10.2018
Verlag
Springer International Publishing
Erschienen in
Clinical and Translational Oncology / Ausgabe 4/2019
Print ISSN: 1699-048X
Elektronische ISSN: 1699-3055
DOI
https://doi.org/10.1007/s12094-018-1947-8

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