Iron Oxide Nanoparticles for Breast Cancer Theranostics

Author(s): Md. Salman Shakil, Md. Ashraful Hasan*, Satya Ranjan Sarker*.

Journal Name: Current Drug Metabolism

Volume 20 , Issue 6 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: Breast cancer is the second leading cause of death in women worldwide. The extremely fast rate of metastasis and ability to develop resistance mechanism to all the conventional drugs make them very difficult to treat which are the causes of high morbidity and mortality of breast cancer patients. Scientists throughout the world have been focusing on the early detection of breast tumor so that treatment can be started at the very early stage. Moreover, conventional treatment processes such as chemotherapy, radiotherapy, and local surgery suffer from various limitations including toxicity, genetic mutation of normal cells, and spreading of cancer cells to healthy tissues. Therefore, new treatment regimens with minimum toxicity to normal cells need to be urgently developed.

Methods: Iron oxide nanoparticles have been widely used for targeting hyperthermia and imaging of breast cancer cells. They can be conjugated with drugs, proteins, enzymes, antibodies or nucleotides to deliver them to target organs, tissues or tumors using external magnetic field.

Results: Iron oxide nanoparticles have been successfully used as theranostic agents for breast cancer both in vitro and in vivo. Furthermore, their functionalization with drugs or functional biomolecules enhance their drug delivery efficiency and reduces the systemic toxicity of drugs.

Conclusion: This review mainly focuses on the versatile applications of superparamagnetic iron oxide nanoparticles on the diagnosis, treatment, and detecting progress of breast cancer treatment. Their wide application is because of their excellent superparamagnetic, biocompatible and biodegradable properties.

Keywords: Iron oxide nanoparticles, breast cancer, hyperthermia, photothermal therapy, MRI contrast agent, theranostics.

[1]
Qian, X.; Peng, X-H.; Ansari, D.O.; Yin-Goen, Q.; Chen, G.Z.; Shin, D.M.; Yang, L.; Young, A.N.; Wang, M.D.; Nie, S. In vivo tumor targeting and spectroscopic detection with surface-enhanced Raman nanoparticle tags. Nat. Biotechnol., 2008, 26(1), 83.
[2]
Yigit, M.V.; Moore, A.; Medarova, Z. Magnetic nanoparticles for cancer diagnosis and therapy. Pharm. Res., 2012, 29(5), 1180-1188.
[3]
Gao, L.; Liu, Y.; Kim, D.; Li, Y.; Hwang, G.; Naha, P.C.; Cormode, D.P.; Koo, H. Nanocatalysts promote Streptococcus mutans biofilm matrix degradation and enhance bacterial killing to suppress dental caries in vivo. Biomaterials, 2016, 101, 272-284.
[4]
Gu, L.; Fang, R.H.; Sailor, M.J.; Park, J-H. In vivo clearance and toxicity of monodisperse iron oxide nanocrystals. ACS Nano, 2012, 6(6), 4947-4954.
[5]
Liu, Y.; Naha, P.C.; Hwang, G.; Kim, D.; Huang, Y.; Simon-Soro, A.; Jung, H-I.; Ren, Z.; Li, Y.; Gubara, S. Topical ferumoxytol nanoparticles disrupt biofilms and prevent tooth decay in vivo via intrinsic catalytic activity. Nat. Commun., 2018, 9(1), 2920.
[6]
Gunduz, U.; Keskin, T.; Tansık, G.; Mutlu, P.; Yalcın, S.; Unsoy, G.; Yakar, A.; Khodadust, R.; Gunduz, G. Idarubicin-loaded folic acid conjugated magnetic nanoparticles as a targetable drug delivery system for breast cancer. Biomed. Pharmacother., 2014, 68(6), 729-736.
[7]
Kikumori, T.; Kobayashi, T.; Sawaki, M.; Imai, T. Anti-cancer effect of hyperthermia on breast cancer by magnetite nanoparticle-loaded anti-HER2 immunoliposomes. Breast Cancer Res. Treat., 2009, 113(3), 435.
[8]
Kumar, C.S.; Leuschner, C.; Doomes, E.; Henry, L.; Juban, M.; Hormes, J. Efficacy of lytic peptide-bound magnetite nanoparticles in destroying breast cancer cells. J. Nanosci. Nanotechnol., 2004, 4(3), 245-249.
[9]
Teraphongphom, N.; Chhour, P.; Eisenbrey, J.R.; Naha, P.C.; Witschey, W.R.; Opasanont, B.; Jablonowski, L.; Cormode, D.P.; Wheatley, M.A. Nanoparticle loaded polymeric microbubbles as contrast agents for multimodal imaging. Langmuir, 2015, 31(43), 11858-11867.
[10]
Chhour, P.; Gallo, N.; Cheheltani, R.; Williams, D.; Al-Zaki, A.; Paik, T.; Nichol, J.L.; Tian, Z.; Naha, P.C.; Witschey, W.R. Nanodisco balls: Control over surface versus core loading of diagnostically active nanocrystals into polymer nanoparticles. ACS Nano, 2014, 8(9), 9143-9153.
[11]
Naha, P.C.; Al Zaki, A.; Hecht, E.; Chorny, M.; Chhour, P.; Blankemeyer, E.; Yates, D.M.; Witschey, W.R.; Litt, H.I.; Tsourkas, A. Dextran coated bismuth-iron oxide nanohybrid contrast agents for computed tomography and magnetic resonance imaging. J. Mater. Chem. B, 2014, 2(46), 8239-8248.
[12]
Zhang, J.; Dewilde, A.H.; Chinn, P.; Foreman, A.; Barry, S.; Kanne, D.; Braunhut, S.J. Herceptin-directed nanoparticles activated by an alternating magnetic field selectively kill HER-2 positive human breast cells in vitro via hyperthermia. Int. J. Hyperthermia, 2011, 27(7), 682-697.
[13]
Sun, Y.; Zheng, Y.; Ran, H.; Zhou, Y.; Shen, H.; Chen, Y.; Chen, H.; Krupka, T.M.; Li, A.; Li, P. Superparamagnetic PLGA-iron oxide microcapsules for dual-modality US/MR imaging and high intensity focused US breast cancer ablation. Biomaterials, 2012, 33(24), 5854-5864.
[14]
Weigelt, B.; Peterse, J.L.; Van’t Veer, L.J. Breast cancer metastasis: Markers and models. Nat. Rev. Cancer, 2005, 5(8), 591.
[15]
Zou, Y.; Liu, P.; Liu, C-H.; Zhi, X-T. Doxorubicin-loaded mesoporous magnetic nanoparticles to induce apoptosis in breast cancer cells. Biomed. Pharmacother., 2015, 69, 355-360.
[16]
Ito, A.; Shinkai, M.; Honda, H.; Kobayashi, T. Medical application of functionalized magnetic nanoparticles. J. Biosci. Bioeng., 2005, 100(1), 1-11.
[17]
Ihemelandu, C.U.; Leffall Jr, L.D.; Dewitty, R.L.; Naab, T.J.; Mezghebe, H.M.; Makambi, K.H.; Adams-Campbell, L.; Frederick, W.A. Molecular breast cancer subtypes in premenopausal and postmenopausal African-American women: Age-specific prevalence and survival. J. Surg. Res., 2007, 143(1), 109-118.
[18]
Artemov, D.; Mori, N.; Okollie, B.; Bhujwalla, Z.M. MR molecular imaging of the Her‐2/neu receptor in breast cancer cells using targeted iron oxide nanoparticles. Magn. Reson. Med., 2003, 49(3), 403-408.
[19]
Högemann-Savellano, D.; Bos, E.; Blondet, C.; Sato, F.; Abe, T.; Josephson, L.; Weissleder, R.; Gaudet, J.; Sgroi, D.; Peters, P.J. The transferrin receptor: A potential molecular imaging marker for human cancer. Neoplasia, 2003, 5(6), 495-506.
[20]
Montet, X.; Montet-Abou, K.; Reynolds, F.; Weissleder, R.; Josephson, L. Nanoparticle imaging of integrins on tumor cells. Neoplasia, 2006, 8(3), 214-222.
[21]
Rosen, J.E.; Chan, L.; Shieh, D-B.; Gu, F.X. Iron oxide nanoparticles for targeted cancer imaging and diagnostics. Nanomedicine, 2012, 8(3), 275-290.
[22]
Yezhelyev, M.V.; Gao, X.; Xing, Y.; Al-Hajj, A.; Nie, S.; O’Regan, R.M. Emerging use of nanoparticles in diagnosis and treatment of breast cancer. Lancet Oncol., 2006, 7(8), 657-667.
[23]
Adolphi, N.L.; Butler, K.S.; Lovato, D.M.; Tessier, T.; Trujillo, J.E.; Hathaway, H.J.; Fegan, D.L.; Monson, T.C.; Stevens, T.E.; Huber, D.L. Imaging of Her2‐targeted magnetic nanoparticles for breast cancer detection: comparison of SQUID‐detected magnetic relaxometry and MRI. Contrast Media Mol. Imaging, 2012, 7(3), 308-319.
[24]
Kievit, F.M.; Stephen, Z.R.; Veiseh, O.; Arami, H.; Wang, T.; Lai, V.P.; Park, J.O.; Ellenbogen, R.G.; Disis, M.L.; Zhang, M. Targeting of primary breast cancers and metastases in a transgenic mouse model using rationally designed multifunctional SPIONs. ACS Nano, 2012, 6(3), 2591-2601.
[25]
Ma, Q.; Nakane, Y.; Mori, Y.; Hasegawa, M.; Yoshioka, Y.; Watanabe, T.M.; Gonda, K.; Ohuchi, N.; Jin, T. Multilayered, core/shell nanoprobes based on magnetic ferric oxide particles and quantum dots for multimodality imaging of breast cancer tumors. Biomaterials, 2012, 33(33), 8486-8494.
[26]
Alarifi, S.; Ali, D.; Alkahtani, S.; Alhader, M. Iron oxide nanoparticles induce oxidative stress, DNA damage, and caspase activation in the human breast cancer cell line. Biol. Trace Elem. Res., 2014, 159(1-3), 416-424.
[27]
Varshosaz, J.; Sadeghi-Aliabadi, H.; Ghasemi, S.; Behdadfar, B. Use of magnetic folate-dextran-retinoic acid micelles for dual targeting of doxorubicin in breast cancer. BioMed Res. Int., 2013, 2013680712
[28]
McBain, S.C.; Yiu, H.H.; Dobson, J. Magnetic nanoparticles for gene and drug delivery. Int. J. Nanomedicine, 2008, 3(2), 169.
[29]
Kossatz, S.; Grandke, J.; Couleaud, P.; Latorre, A.; Aires, A.; Crosbie-Staunton, K.; Ludwig, R.; Dähring, H.; Ettelt, V.; Lazaro-Carrillo, A. Efficient treatment of breast cancer xenografts with multifunctionalized iron oxide nanoparticles combining magnetic hyperthermia and anti-cancer drug delivery. Breast Cancer Res., 2015, 17(1), 66.
[30]
Holliday, D.L.; Speirs, V. Choosing the right cell line for breast cancer research. Breast Cancer Res., 2011, 13(4), 215.
[31]
Sørlie, T.; Perou, C.M.; Tibshirani, R.; Aas, T.; Geisler, S.; Johnsen, H.; Hastie, T.; Eisen, M.B.; Van De Rijn, M.; Jeffrey, S.S. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. USA, 2001, 98(19), 10869-10874.
[32]
Badve, S.; Dabbs, D.J.; Schnitt, S.J.; Baehner, F.L.; Decker, T.; Eusebi, V.; Fox, S.B.; Ichihara, S.; Jacquemier, J.; Lakhani, S.R. Basal-like and triple-negative breast cancers: A critical review with an emphasis on the implications for pathologists and oncologists. Mod. Pathol., 2011, 24(2), 157.
[33]
Prat, A.; Parker, J.S.; Karginova, O.; Fan, C.; Livasy, C.; Herschkowitz, J.I.; He, X.; Perou, C.M. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res., 2010, 12(5), R68.
[34]
Naha, P.C.; Lau, K.C.; Hsu, J.C.; Hajfathalian, M.; Mian, S.; Chhour, P.; Uppuluri, L.; McDonald, E.S.; Maidment, A.D.; Cormode, D.P. Gold silver alloy nanoparticles (GSAN): An imaging probe for breast cancer screening with dual-energy mammography or computed tomography. Nanoscale, 2016, 8(28), 13740-13754.
[35]
Hsu, J.C.; Naha, P.C.; Lau, K.C.; Chhour, P.; Hastings, R.; Moon, B.F.; Stein, J.M.; Witschey, W.; Mcdonald, E.S.; Maidment, A. An all-in-one nanoparticle (AION) contrast agent for breast cancer screening with DEM-CT-MRI-NIRF imaging. Nanoscale, 2018, 10(36), 17236-17248.
[36]
Karunamuni, R.; Naha, P.C.; Lau, K.C.; Al-Zaki, A.; Popov, A.V.; Delikatny, E.J.; Tsourkas, A.; Cormode, D.P.; Maidment, A.D. Development of silica-encapsulated silver nanoparticles as contrast agents intended for dual-energy mammography. Eur. Radiol., 2016, 26(9), 3301-3309.
[37]
Lim, E-K.; Kim, H-O.; Jang, E.; Park, J.; Lee, K.; Suh, J-S.; Huh, Y-M.; Haam, S. Hyaluronan-modified magnetic nanoclusters for detection of CD44-overexpressing breast cancer by MR imaging. Biomaterials, 2011, 32(31), 7941-7950.
[38]
Pályi-Krekk, Z.; Barok, M.; Isola, J.; Tammi, M.; Szöllo, J.; Nagy, P. Hyaluronan-induced masking of ErbB2 and CD44-enhanced trastuzumab internalisation in trastuzumab resistant breast cancer. Eur. J. Cancer, 2007, 43(16), 2423-2433.
[39]
Draffin, J.E.; McFarlane, S.; Hill, A.; Johnston, P.G.; Waugh, D.J. CD44 potentiates the adherence of metastatic prostate and breast cancer cells to bone marrow endothelial cells. Cancer Res., 2004, 64(16), 5702-5711.
[40]
Yang, H-M.; Park, C.W.; Woo, M-A.; Kim, M.I.; Jo, Y.M.; Park, H.G.; Kim, J-D. HER2/neu antibody conjugated poly (amino acid)-coated iron oxide nanoparticles for breast cancer MR imaging. Biomacromolecules, 2010, 11(11), 2866-2872.
[41]
Corsi, F.; Fiandra, L.; De Palma, C.; Colombo, M.; Mazzucchelli, S.; Verderio, P.; Allevi, R.; Tosoni, A.; Nebuloni, M.; Clementi, E. HER2 expression in breast cancer cells is downregulated upon active targeting by antibody-engineered multifunctional nanoparticles in mice. ACS Nano, 2011, 5(8), 6383-6393.
[42]
Larson, T.A.; Bankson, J.; Aaron, J.; Sokolov, K. Hybrid plasmonic magnetic nanoparticles as molecular specific agents for MRI/optical imaging and photothermal therapy of cancer cells. Nanotechnology, 2007, 18(32)325101
[43]
Meng, J.; Fan, J.; Galiana, G.; Branca, R.; Clasen, P.; Ma, S.; Zhou, J.; Leuschner, C.; Kumar, C.; Hormes, J. LHRH-functionalized superparamagnetic iron oxide nanoparticles for breast cancer targeting and contrast enhancement in MRI. Mater. Sci. Eng. C, 2009, 29(4), 1467-1479.
[44]
Meier, R.; Henning, T.D.; Boddington, S.; Tavri, S.; Arora, S.; Piontek, G.; Rudelius, M.; Corot, C.; Daldrup-Link, H.E. Breast cancers: MR imaging of folate-receptor expression with the folate-specific nanoparticle P1133. Radiology, 2010, 255(2), 527-535.
[45]
Li, T.; Shen, X.; Chen, Y.; Zhang, C.; Yan, J.; Yang, H.; Wu, C.; Zeng, H.; Liu, Y. Polyetherimide-grafted Fe3O4@ SiO2 nanoparticles as theranostic agents for simultaneous VEGF siRNA delivery and magnetic resonance cell imaging. Int. J. Nanomedicine, 2015, 10, 4279.
[46]
Turetschek, K.; Roberts, T.P.; Floyd, E.; Preda, A.; Novikov, V.; Shames, D.M.; Carter, W.O.; Brasch, R.C. Tumor microvascular characterization using ultrasmall superparamagnetic iron oxide particles (USPIO) in an experimental breast cancer model. J. Magn. Reson. Imaging, 2001, 13(6), 882-888.
[47]
Xu, H.; Cheng, L.; Wang, C.; Ma, X.; Li, Y.; Liu, Z. Polymer encapsulated upconversion nanoparticle/iron oxide nanocomposites for multimodal imaging and magnetic targeted drug delivery. Biomaterials, 2011, 32(35), 9364-9373.
[48]
Wate, P.S.; Banerjee, S.S.; Jalota-Badhwar, A.; Mascarenhas, R.R.; Zope, K.R.; Khandare, J.; Misra, R.D.K. Cellular imaging using biocompatible dendrimer-functionalized graphene oxide-based fluorescent probe anchored with magnetic nanoparticles. Nanotechnology, 2012, 23(41)415101
[49]
Yallapu, M.M.; Othman, S.F.; Curtis, E.T.; Bauer, N.A.; Chauhan, N.; Kumar, D.; Jaggi, M.; Chauhan, S.C. Curcumin-loaded magnetic nanoparticles for breast cancer therapeutics and imaging applications. Int. J. Nanomedicine, 2012, 7, 1761.
[50]
Zhong, Y.; Goltsche, K.; Cheng, L.; Xie, F.; Meng, F.; Deng, C.; Zhong, Z.; Haag, R. Hyaluronic acid-shelled acid-activatable paclitaxel prodrug micelles effectively target and treat CD44-overexpressing human breast tumor xenografts in vivo. Biomaterials, 2016, 84, 250-261.
[51]
Abdel-Ghany, M.; Cheng, H-C.; Elble, R.C.; Pauli, B.U. The breast cancer beta4 integrin and endothelial hCLCA2 mediate lung metastasis. J. Biol. Chem., 2001, 276(27), 25438-25446.
[52]
Zhao, Y.; Bachelier, R.; Treilleux, I.; Pujuguet, P.; Peyruchaud, O.; Baron, R.; Clément-Lacroix, P.; Clézardin, P. Tumor αvβ3 integrin is a therapeutic target for breast cancer bone metastases. Cancer Res., 2007, 67(12), 5821-5830.
[53]
Cariati, M.; Naderi, A.; Brown, J.P.; Smalley, M.J.; Pinder, S.E.; Caldas, C.; Purushotham, A.D. Alpha‐6 integrin is necessary for the tumourigenicity of a stem cell‐like subpopulation within the MCF7 breast cancer cell line. Int. J. Cancer, 2008, 122(2), 298-304.
[54]
White, D.E.; Kurpios, N.A.; Zuo, D.; Hassell, J.A.; Blaess, S.; Mueller, U.; Muller, W.J. Targeted disruption of β1-integrin in a transgenic mouse model of human breast cancer reveals an essential role in mammary tumor induction. Cancer Cell, 2004, 6(2), 159-170.
[55]
Daniels, T.R.; Delgado, T.; Helguera, G.; Penichet, M.L. The transferrin receptor part II: Targeted delivery of therapeutic agents into cancer cells. Clin. Immunol., 2006, 121(2), 159-176.
[56]
Peer, D.; Karp, J.M.; Hong, S.; Farokhzad, O.C.; Margalit, R.; Langer, R. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol., 2007, 2(12), 751.
[57]
Rimawi, M.F.; Mayer, I.A.; Forero, A.; Nanda, R.; Goetz, M.P.; Rodriguez, A.A.; Pavlick, A.C.; Wang, T.; Hilsenbeck, S.G.; Gutierrez, C. Multicenter phase II study of neoadjuvant lapatinib and trastuzumab with hormonal therapy and without chemotherapy in patients with human epidermal growth factor receptor 2-overexpressing breast cancer: TBCRC 006. J. Clin. Oncol., 2013, 31(14), 1726.
[58]
Goswami, S.; Sahai, E.; Wyckoff, J.B.; Cammer, M.; Cox, D.; Pixley, F.J.; Stanley, E.R.; Segall, J.E.; Condeelis, J.S. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res., 2005, 65(12), 5278-5283.
[59]
Nagy, A.; Schally, A.V. Targeting of cytotoxic luteinizing hormone-releasing hormone analogs to breast, ovarian, endometrial, and prostate cancers. Biol. Reprod., 2005, 73(5), 851-859.
[60]
Huang, S.; Shao, K.; Liu, Y.; Kuang, Y.; Li, J.; An, S.; Guo, Y.; Ma, H.; Jiang, C. Tumor-targeting and microenvironment-responsive smart nanoparticles for combination therapy of antiangiogenesis and apoptosis. ACS Nano, 2013, 7(3), 2860-2871.
[61]
Wang, L.; Zhang, W-J.; Xiu, B.; Ding, Y.; Li, P.; Zhu, Q.; Liang, A-B. Nanocomposite-siRNA approach for down-regulation of VEGF and its receptor in myeloid leukemia cells. Int. J. Biol. Macromol., 2014, 63, 49-55.
[62]
Laurent, S.; Dutz, S.; Häfeli, U.O.; Mahmoudi, M. Magnetic fluid hyperthermia: Focus on superparamagnetic iron oxide nanoparticles. Adv. Colloid Interface Sci., 2011, 166(1-2), 8-23.
[63]
Pankhurst, Q.A.; Connolly, J.; Jones, S.; Dobson, J. Applications of magnetic nanoparticles in biomedicine. J. Phys. D, 2003, 36(13), R167.
[64]
Sonvico, F.; Mornet, S.; Vasseur, S.; Dubernet, C.; Jaillard, D.; Degrouard, J.; Hoebeke, J.; Duguet, E.; Colombo, P.; Couvreur, P. Folate-conjugated iron oxide nanoparticles for solid tumor targeting as potential specific magnetic hyperthermia mediators: Synthesis, physicochemical characterization, and in vitro experiments. Bioconjug. Chem., 2005, 16(5), 1181-1188.
[65]
Overgaard, J. Effect of hyperthermia on malignant cells in vivo: A review and a hypothesis. Cancer, 1977, 39(6), 2637-2646.
[66]
Petryk, A.A.; Giustini, A.J.; Gottesman, R.E.; Trembly, B.S.; Hoopes, P.J. Comparison of magnetic nanoparticle and microwave hyperthermia cancer treatment methodology and treatment effect in a rodent breast cancer model. Int. J. Hyperthermia, 2013, 29(8), 819-827.
[67]
Marcu, A.; Pop, S.; Dumitrache, F.; Mocanu, M.; Niculite, C.; Gherghiceanu, M.; Lungu, C.; Fleaca, C.; Ianchis, R.; Barbut, A. Magnetic iron oxide nanoparticles as drug delivery system in breast cancer. Appl. Surf. Sci., 2013, 281, 60-65.
[68]
Baba, D.; Seiko, Y.; Nakanishi, T.; Zhang, H.; Arakaki, A.; Matsunaga, T.; Osaka, T. Effect of magnetite nanoparticles on living rate of MCF-7 human breast cancer cells. Colloids Surf. B, 2012, 95, 254-257.
[69]
Dilnawaz, F.; Singh, A.; Mohanty, C.; Sahoo, S.K. Dual drug loaded superparamagnetic iron oxide nanoparticles for targeted cancer therapy. Biomaterials, 2010, 31(13), 3694-3706.
[70]
Kumar, M.; Yigit, M.; Dai, G.; Moore, A.; Medarova, Z. Image-guided breast tumor therapy using a small interfering RNA nanodrug. Cancer Res., 2010, 70(19), 7553-7561.
[71]
Mikhaylova, M.; Stasinopoulos, I.; Kato, Y.; Artemov, D.; Bhujwalla, Z. Imaging of cationic multifunctional liposome-mediated delivery of COX-2 siRNA. Cancer Gene Ther., 2009, 16(3), 217.
[72]
Kong, G.; Dewhirst, M. Review hyperthermia and liposomes. Int. J. Hyperthermia, 1999, 15(5), 345-370.
[73]
Chari, R.V. Targeted cancer therapy: conferring specificity to cytotoxic drugs. Acc. Chem. Res., 2007, 41(1), 98-107.
[74]
Micheau, O.; Solary, E.; Hammann, A.; Martin, F.; Dimanche-Boitrel, M-T. Sensitization of cancer cells treated with cytotoxic drugs to fas-mediated cytotoxicity. J. Natl. Cancer Inst., 1997, 89(11), 783-789.
[75]
Lin, G.; Zhu, W.; Yang, L.; Wu, J.; Lin, B.; Xu, Y.; Cheng, Z.; Xia, C.; Gong, Q.; Song, B. Delivery of siRNA by MRI-visible nanovehicles to overcome drug resistance in MCF-7/ADR human breast cancer cells. Biomaterials, 2014, 35(35), 9495-9507.
[76]
Thoidingjam, S.; Tiku, A.B. New developments in breast cancer therapy: Role of iron oxide nanoparticles. Adv. Nat. Sci.: Nanosci. Nanotech., 2017, 8(2)023002
[77]
Yang, K.; Hu, L.; Ma, X.; Ye, S.; Cheng, L.; Shi, X.; Li, C.; Li, Y.; Liu, Z. Multimodal imaging guided photothermal therapy using functionalized graphene nanosheets anchored with magnetic nanoparticles. Adv. Mater., 2012, 24(14), 1868-1872.
[78]
Huang, X.; El-Sayed, I.H.; Qian, W.; El-Sayed, M.A. Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods. J. Am. Chem. Soc., 2006, 128(6), 2115-2120.
[79]
Huang, X.; El-Sayed, M.A. Gold nanoparticles: optical properties and implementations in cancer diagnosis and photothermal therapy. J. Adv. Res., 2010, 1(1), 13-28.
[80]
Macdonald, I.J.; Dougherty, T.J. Basic principles of photodynamic therapy. J. Porphyr. Phthalocyanines, 2001, 5(02), 105-129.
[81]
Hasan, T.; Ortel, B.; Solban, N.; Pogue, B. Photodynamic therapy of cancer. Cancer Med., 2003, 7, 537-548.
[82]
Choi, Y.; Weissleder, R.; Tung, C-H. Selective antitumor effect of novel protease-mediated photodynamic agent. Cancer Res., 2006, 66(14), 7225-7229.
[83]
Wang, C.; Sun, X.; Cheng, L.; Yin, S.; Yang, G.; Li, Y.; Liu, Z. Multifunctional theranostic red blood cells for magnetic‐field‐enhanced in vivo combination therapy of cancer. Adv. Mater., 2014, 26(28), 4794-4802.
[84]
Vallabani, N.S.; Karakoti, A.S.; Singh, S. ATP-mediated intrinsic peroxidase-like activity of Fe3O4-based nanozyme: One step detection of blood glucose at physiological pH. Colloids Surf. B, 2017, 153, 52-60.
[85]
Wu, Y.; Song, M.; Xin, Z.; Zhang, X.; Zhang, Y.; Wang, C.; Li, S.; Gu, N. Ultra-small particles of iron oxide as peroxidase for immunohistochemical detection. Nanotechnology, 2011, 22(22)225703
[86]
Fu, S.; Wang, S.; Zhang, X.; Qi, A.; Liu, Z.; Yu, X.; Chen, C.; Li, L. Structural effect of Fe3O4 nanoparticles on peroxidase-like activity for cancer therapy. Colloids Surf. B, 2017, 154, 239-245.
[87]
Vallabani, N. S.; Singh, S. Recent advances and future prospects of iron oxide nanoparticles in biomedicine and diagnostics. 3 Biotech., 2018, 8(6), 279.
[88]
Schrand, A.M.; Dai, L.; Schlager, J.J.; Hussain, S.M. Toxicity Testing of Nanomaterials.In: New Technologies for Toxicity Testing; Springer: New York City, 2012, pp. Chap.5,. 58-75.
[89]
Kedziorek, D.A.; Muja, N.; Walczak, P.; Ruiz‐Cabello, J.; Gilad, A.A.; Jie, C.C.; Bulte, J.W. Gene expression profiling reveals early cellular responses to intracellular magnetic labeling with superparamagnetic iron oxide nanoparticles. Magn. Reson. Med., 2010, 63(4), 1031-1043.
[90]
Shen, M.; Cai, H.; Wang, X.; Cao, X.; Li, K.; Wang, S.H.; Guo, R.; Zheng, L.; Zhang, G.; Shi, X. Facile one-pot preparation, surface functionalization, and toxicity assay of APTS-coated iron oxide nanoparticles. Nanotechnology, 2012, 23(10)105601
[91]
Singh, N.; Jenkins, G.J.; Asadi, R.; Doak, S.H. Potential toxicity of superparamagnetic iron oxide nanoparticles (SPION). Nano Rev., 2010, 1(1), 5358.
[92]
Naqvi, S.; Samim, M.; Abdin, M.; Ahmed, F.J.; Maitra, A.; Prashant, C.; Dinda, A.K. Concentration-dependent toxicity of iron oxide nanoparticles mediated by increased oxidative stress. Int. J. Nanomedicine, 2010, 5, 983.
[93]
Mahmoudi, M.; Serpooshan, V.; Laurent, S. Engineered nanoparticles for biomolecular imaging. Nanoscale, 2011, 3(8), 3007-3026.
[94]
Pawelczyk, E.; Arbab, A.S.; Chaudhry, A.; Balakumaran, A.; Robey, P.G.; Frank, J.A. In vitro model of bromodeoxyuridine or iron oxide nanoparticle uptake by activated macrophages from labeled stem cells: Implications for cellular therapy. Stem Cells, 2008, 26(5), 1366-1375.
[95]
Liu, G.; Gao, J.; Ai, H.; Chen, X. Applications and potential toxicity of magnetic iron oxide nanoparticles. Small, 2013, 9(9‐10), 1533-1545.
[96]
Wang, J.; Chen, Y.; Chen, B.; Ding, J.; Xia, G.; Gao, C.; Cheng, J.; Jin, N.; Zhou, Y.; Li, X. Pharmacokinetic parameters and tissue distribution of magnetic Fe3O4 nanoparticles in mice. Int. J. Nanomedicine, 2010, 5, 861.
[97]
Hoffmann, H.; Härtl, A.; Lisalo, E.; Pekkarinen, A. Failing effect of digoxin on myocardial uptake of violamycin B1. Acta Pharmacol. Toxicol., 1981, 49(2), 98-101.
[98]
Chen, Y.; Wan, Y.; Wang, Y.; Zhang, H.; Jiao, Z. Anticancer efficacy enhancement and attenuation of side effects of doxorubicin with titanium dioxide nanoparticles. Int. J. Nanomedicine, 2011, 6, 2321.
[99]
Brazel, C.; Huang, X. The Cost of optimal drug delivery: Reducing and preventing the burst effect in matrix systems. In: , Abstracts of Papers of the American Chemical Society; 1155 16th St, NW, Washington, DC 20036 USA,. , 2002, pp. U392-U392.


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Article Details

VOLUME: 20
ISSUE: 6
Year: 2019
Page: [446 - 456]
Pages: 11
DOI: 10.2174/1389200220666181122105043
Price: $58

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