Iron oxide nanoparticle-based theranostics for cancer imaging and therapy

Abstract

Theranostic platform, which is equipped with both diagnostic and therapeutic functions, is a promising approach in cancer treatment. From various nanotheranostics studied, iron oxide nanoparticles have advantages since IONPs have good biocompatibility and spatial imaging capability. This review is focused on the IONP-based nanotheranostics for cancer imaging and treatment. The most recent progress for applications of IONP nanotheranostics is summarized, which includes IONP-based diagnosis, magnetic resonance imaging (MRI), multimodal imaging, chemotherapy, hyperthermal therapy, photodynamic therapy, and gene delivery. Future perspectives and challenges are also outlined for the potential development of IONP based theranostics in clinical use.

Keywords

theranostics / iron oxide nanoparticles / MRI / drug delivery / photothermal therapy / photodynamic therapy

References

[1] Tietze R, Lyer S, Dürr S, Alexiou C. Nanoparticles for cancer therapy using magnetic forces. Nanomedicine-UK, 2012, 7(3): 447–457

[2] Zhang Z, Wang J, Chen C. Near-infrared light-mediated nanoplatforms for cancer thermo-chemotherapy and optical imaging. Advanced Materials, 2013, 25(28): 3869–3880

[3] Yuan A, Wu J, Tang X, Zhao L, Xu F, Hu Y. Application of near-infrared dyes for tumor imaging, photothermal, and photodynamic therapies. Journal of Pharmaceutical Sciences, 2013, 102(1): 6–28

[4] Menon J U, Jadeja P, Tambe P, Vu K, Yuan B, Nguyen K T. Nanomaterials for photo-based diagnostic and therapeutic applications. Theranostics, 2013, 3(3): 152–166

[5] Ryu J H, Koo H, Sun I C, Yuk S H, Choi K, Kim K, Kwon I C. Tumor-targeting multi-functional nanoparticles for theragnosis: new paradigm for cancer therapy. Advanced Drug Delivery Reviews, 2012, 64(13): 1447–1458

[6] Xie J, Lee S, Chen X. Nanoparticle-based theranostic agents. Advanced Drug Delivery Reviews, 2010, 62(11): 1064–1079

[7] Ho D, Sun X, Sun S. Monodisperse magnetic nanoparticles for theranostic applications. Accounts of Chemical Research, 2011, 44(10): 875–882

[8] Sun S, Zeng H, Robinson D B, Raoux S, Rice P M, Wang S X, Li G. Monodisperse MFe₂O₄ (M= Fe, Co, Mn) nanoparticles. Journal of the American Chemical Society, 2004, 126(1): 273–279

[9] Laurent S, Forge D, Port M, Roch A, Robic C, Vander Elst L, Muller R N. Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chemical Reviews, 2008, 108(6): 2064–2110

[10] Park J, Lee E, Hwang N M, Kang M, Kim S C, Hwang Y, Park J G, Noh H J, Kim J Y, Park J H, Hyeon T. One-nanometer-scale size-controlled synthesis of monodisperse magnetic iron oxide nanoparticles. Angewandte Chemie International Edition in English,, 2005, 44(19): 2873–2877

[11] Huang J, Zhong X, Wang L, Yang L, Mao H. Improving the magnetic resonance imaging contrast and detection methods with engineered magnetic nanoparticles. Theranostics, 2012, 2(1): 86–102

[12] Huang Y, He S, Cao W, Cai K, Liang X J. Biomedical nanomaterials for imaging-guided cancer therapy. Nanoscale, 2012, 4(20): 6135–6149

[13] Wang J, Huang Y, David A E, Chertok B, Zhang L, Yu F, Yang V C. Magnetic nanoparticles for MRI of brain tumors. Current Pharmaceutical Biotechnology, 2012, 13(12): 2403–2416

[14] Psimadas D, Baldi G, Ravagli C, Comes Franchini M, Locatelli E, Innocenti C, Sangregorio C, Loudos G. Comparison of the magnetic, radiolabeling, hyperthermic and biodistribution properties of hybrid nanoparticles bearing CoFe₂O₄ and Fe₃O₄ metal cores. Nanotechnology, 2014, 25(2): 025101

[15] Lee S H, Kim B H, Na H B, Hyeon T. Paramagnetic inorganic nanoparticles as T1 MRI contrast agents. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, 2014, 6(2): 196–209

[16] Xiao N, Gu W, Wang H, Deng Y, Shi X, Ye L. T1-T2 dual-modal MRI of brain gliomas using PEGylated Gd-doped iron oxide nanoparticles. Journal of Colloid and Interface Science, 2014, 417: 159–165

[17] Ragheb R R T, Kim D, Bandyopadhyay A, Chahboune H, Bulutoglu B, Ezaldein H, Criscione J M, Fahmy T M. Induced clustered nanoconfinement of superparamagnetic iron oxide in biodegradable nanoparticles enhances transverse relaxivity for targeted theranostics. Magnetic Resonance in Medicine, 2013, 70(6): 1748–1760

[18] Balasubramaniam S, Kayandan S, Lin Y N, Kelly D F, House M J, Woodward R C, St Pierre T G, Riffle J S, Davis R M. Toward design of magnetic nanoparticle clusters stabilized by biocompatible diblock copolymers for T₂-weighted MRI contrast. Langmuir, 2014, 30(6): 1580–1587

[19] Tähkä S, Laiho A, Kostiainen M A. Diblock-copolymer-mediated self-assembly of protein-stabilized iron oxide nanoparticle clusters for magnetic resonance imaging. Chemistry, 2014, 20(10): 2718–2722

[20] Lee G Y, Qian W P, Wang L, Wang Y A, Staley C A, Satpathy M, Nie S, Mao H, Yang L. Theranostic nanoparticles with controlled release of gemcitabine for targeted therapy and MRI of pancreatic cancer. ACS Nano, 2013, 7(3): 2078–2089

[21] Zhang L, Zhong X, Wang L, Chen H, Wang Y A, Yeh J, Yang L, Mao H. T₁-weighted ultrashort echo time method for positive contrast imaging of magnetic nanoparticles and cancer cells bound with the targeted nanoparticles. Journal of Magnetic Resonance Imaging, 2011, 33(1): 194–202

[22] Xie J, Liu G, Eden H S, Ai H, Chen X. Surface-engineered magnetic nanoparticle platforms for cancer imaging and therapy. Accounts of Chemical Research, 2011, 44(10): 883–892

[23] Lin X, Xie J, Niu G, Zhang F, Gao H, Yang M, Quan Q, Aronova M A, Zhang G, Lee S, Leapman R, Chen X. Chimeric ferritin nanocages for multiple function loading and multimodal imaging. Nano Letters, 2011, 11(2): 814–819

[24] Chen Y C, Wen S, Shang S A, Cui Y, Luo B, Teng G J. Magnetic resonance and near-infrared imaging using a novel dual-modality nano-probe for dendritic cell tracking in vivo. Cytotherapy, 2014, 16(5): 699–710

[25] Lee H Y, Li Z, Chen K, Hsu A R, Xu C, Xie J, Sun S, Chen X. PET/MRI dual-modality tumor imaging using arginine-glycine-aspartic (RGD)-conjugated radiolabeled iron oxide nanoparticles. Journal of Nuclear Medicine, 2008, 49(8): 1371–1379

[26] Xie J, Chen K, Huang J, Lee S, Wang J, Gao J, Li X, Chen X. PET/NIRF/MRI triple functional iron oxide nanoparticles. Biomaterials, 2010, 31(11): 3016–3022

[27] Key J, Cooper C, Kim A Y, Dhawan D, Knapp D W, Kim K, Park J H, Choi K, Kwon I C, Park K, Leary J F. In vivo NIRF and MR dual-modality imaging using glycol chitosan nanoparticles. Journal of Controlled Release, 2012, 163(2): 249–255

[28] Sun Z, Huang P, Tong G, Lin J, Jin A, Rong P, Zhu L, Nie L, Niu G, Cao F, Chen X. VEGF-loaded graphene oxide as theranostics for multi-modality imaging-monitored targeting therapeutic angiogenesis of ischemic muscle. Nanoscale, 2013, 5(15): 6857–6866

[29] Key J, Aryal S, Gentile F, Ananta J S, Zhong M, Landis M D, Decuzzi P. Engineering discoidal polymeric nanoconstructs with enhanced magneto-optical properties for tumor imaging. Biomaterials, 2013, 34(21): 5402–5410

[30] Cao C, Wang X, Cai Y, Sun L, Tian L, Wu H, He X, Lei H, Liu W, Chen G, Zhu R, Pan Y. Targeted in vivo imaging of microscopic tumors with ferritin-based nanoprobes across biological barriers. Advanced Materials, 2014, 26(16): 2566–2571

[31] Zhang Y, Zhang B, Liu F, Luo J, Bai J. In vivo tomographic imaging with fluorescence and MRI using tumor-targeted dual-labeled nanoparticles. International Journal of Nanomedicine, 2014, 9: 33–41

[32] Zou P, Chen H, Paholak H J, Sun D. Noninvasive fluorescence resonance energy transfer imaging of in vivo premature drug release from polymeric nanoparticles. Molecular Pharmaceutics, 2013, 10(11): 4185–4194

[33] Niu C, Wang Z, Lu G, Krupka T M, Sun Y, You Y, Song W, Ran H, Li P, Zheng Y. Doxorubicin loaded superparamagnetic PLGA-iron oxide multifunctional microbubbles for dual-mode US/MR imaging and therapy of metastasis in lymph nodes. Biomaterials, 2013, 34(9): 2307–2317

[34] Chertok B, David A E, Yang V C. Brain tumor targeting of magnetic nanoparticles for potential drug delivery: effect of administration route and magnetic field topography. Journal of Controlled Release, 2011, 155(3): 393–399

[35] Ye F, Barrefelt A, Asem H, Abedi-Valugerdi M, El-Serafi I, Saghafian M, Abu-Salah K, Alrokayan S, Muhammed M, Hassan M. Biodegradable polymeric vesicles containing magnetic nanoparticles, quantum dots and anticancer drugs for drug delivery and imaging. Biomaterials, 2014, 35(12): 3885–3894

[36] Javid A, Ahmadian S, Saboury A A, Kalantar S M, Rezaei-Zarchi S, Shahzad S. Biocompatible APTES-PEG modified magnetite nanoparticles: Effective carriers of antineoplastic agents to ovarian cancer. Applied Biochemistry and Biotechnology, 2014, 173(1): 36–54

[37] Zou P, Yu Y, Wang Y A, Zhong Y, Welton A, Galbán C, Wang S, Sun D. Superparamagnetic iron oxide nanotheranostics for targeted cancer cell imaging and pH-dependent intracellular drug release. Molecular Pharmaceutics, 2010, 7(6): 1974–1984

[38] El-Dakdouki M H, Zhu D C, El-Boubbou K, Kamat M, Chen J, Li W, Huang X. Development of multifunctional hyaluronan-coated nanoparticles for imaging and drug delivery to cancer cells. Biomacromolecules, 2012, 13(4): 1144–1151

[39] Zhang J, Shin M C, Yang V C. Magnetic targeting of novel heparinized iron oxide nanoparticles evaluated in a 9L-glioma mouse model. Pharmaceutical Research, 2014, 31(3): 579–592

[40] Zhang J, Shin M C, David A E, Zhou J, Lee K, He H, Yang V C. Long-circulating heparin-functionalized magnetic nanoparticles for potential application as a protein drug delivery platform. Molecular Pharmaceutics, 2013, 10(10): 3892–3902

[41] Chiang W H, Huang W C, Chang C W, Shen M Y, Shih Z F, Huang Y F, Lin S C, Chiu H C. Functionalized polymersomes with outlayered polyelectrolyte gels for potential tumor-targeted delivery of multimodal therapies and MR imaging. Journal of Controlled Release, 2013, 168(3): 280–288

[42] Gupta A K, Gupta M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials, 2005, 26(18): 3995–4021

[43] Ito A, Shinkai M, Honda H, Kobayashi T. Medical application of functionalized magnetic nanoparticles. Journal of Bioscience and Bioengineering, 2005, 100(1): 1–11

[44] Chen H W, Burnett J, Zhang F X, Zhang J M, Paholak H, Sun D X. Highly crystallized iron oxide nanoparticles as effective and biodegradable mediators for photothermal cancer therapy. Journal of Materials Chemistry B, 2014, 2(7): 757–765

[45] Maier-Hauff K, Rothe R, Scholz R, Gneveckow U, Wust P, Thiesen B, Feussner A, von Deimling A, Waldoefner N, Felix R, Jordan A. Intracranial thermotherapy using magnetic nanoparticles combined with external beam radiotherapy: results of a feasibility study on patients with glioblastoma multiforme. Journal of Neuro-Oncology, 2007, 81(1): 53–60

[46] Béalle G, Di Corato R, Kolosnjaj-Tabi J, Dupuis V, Clément O, Gazeau F, Wilhelm C, Ménager C. Ultra magnetic liposomes for MR imaging, targeting, and hyperthermia. Langmuir, 2012, 28(32): 11834–11842

[47] Johannsen M, Thiesen B, Wust P, Jordan A. Magnetic nanoparticle hyperthermia for prostate cancer. International Journal of Hyperthermia, 2010, 26(8): 790–795

[48] Silva A C, Oliveira T R, Mamani J B, Malheiros S M, Malavolta L, Pavon L F, Sibov T T, Amaro E Jr, Tannús A, Vidoto E L, Martins M J, Santos R S, Gamarra L F. Application of hyperthermia induced by superparamagnetic iron oxide nanoparticles in glioma treatment. International Journal of Nanomedicine, 2011, 6: 591–603

[49] Laurent S, Dutz S, Häfeli U O, Mahmoudi M. Magnetic fluid hyperthermia: focus on superparamagnetic iron oxide nanoparticles. Advances in Colloid and Interface Science, 2011, 166(1-2): 8–23

[50] Chiang W H, Ho V T, Chen H H, Huang W C, Huang Y F, Lin S C, Chern C S, Chiu H C. Superparamagnetic hollow hybrid nanogels as a potential guidable vehicle system of stimuli-mediated MR imaging and multiple cancer therapeutics. Langmuir, 2013, 29(21): 6434–6443

[51] Kievit F M, Zhang M. Surface engineering of iron oxide nanoparticles for targeted cancer therapy. Accounts of Chemical Research, 2011, 44(10): 853–862

[52] Nie X, Chen C. Au nanostructures: an emerging prospect in cancer theranostics. Science China Life Sciences, 2012, 55(10): 872–883

[53] Choi W I, Sahu A, Kim Y H, Tae G. Photothermal cancer therapy and imaging based on gold nanorods. Annals of Biomedical Engineering, 2012, 40(2): 534–546

[54] Thakare V S, Das M, Jain A K, Patil S, Jain S. Carbon nanotubes in cancer theragnosis. Nanomedicine, 2010, 5(8): 1277–1301

[55] Feng L, Wu L, Qu X. New horizons for diagnostics and therapeutic applications of graphene and graphene oxide. Advanced Materials, 2013, 25(2): 168–186

[56] Sahu A, Choi W I, Lee J H, Tae G. Graphene oxide mediated delivery of methylene blue for combined photodynamic and photothermal therapy. Biomaterials, 2013, 34(26): 6239–6248

[57] Ke H, Wang J, Tong S, Jin Y, Wang S, Qu E, Bao G, Dai Z. Gold nanoshelled liquid perfluorocarbon magnetic nanocapsules: a nanotheranostic platform for bimodal ultrasound/magnetic resonance imaging guided photothermal tumor ablation. Theranostics, 2014, 4(1): 12–23

[58] Chen W, Ayala-Orozco C, Biswal N C, Perez-Torres C, Bartels M, Bardhan R, Stinnet G, Liu X D, Ji B, Deorukhkar A, Brown L V, Guha S, Pautler R G, Krishnan S, Halas N J, Joshi A. Targeting pancreatic cancer with magneto-fluorescent theranostic gold nanoshells. Nanomedicine, Posted online on September 24, 2013, Pages:1–14

[59] Wang X, Liu H, Chen D, Meng X, Liu T, Fu C, Hao N, Zhang Y, Wu X, Ren J, Tang F. Multifunctional Fe₃O₄@P(St/MAA)@chitosan@Au core/shell nanoparticles for dual imaging and photothermal therapy. ACS Applied Materials & Interfaces, 2013, 5(11): 4966–4971

[60] Melancon M P, Lu W, Zhong M, Zhou M, Liang G, Elliott A M, Hazle J D, Myers J N, Li C, Stafford R J. Targeted multifunctional gold-based nanoshells for magnetic resonance-guided laser ablation of head and neck cancer. Biomaterials, 2011, 32(30): 7600–7608

[61] Fan Z, Shelton M, Singh A K, Senapati D, Khan S A, Ray P C. Multifunctional plasmonic shell-magnetic core nanoparticles for targeted diagnostics, isolation, and photothermal destruction of tumor cells. ACS Nano, 2012, 6(2): 1065–1073

[62] Cheng L, Yang K, Li Y, Chen J, Wang C, Shao M, Lee S T, Liu Z. Facile preparation of multifunctional upconversion nanoprobes for multimodal imaging and dual-targeted photothermal therapy. Angewandte Chemie International Edition in English, 2011, 50(32): 7385–7390

[63] Hu Y, Meng L, Niu L, Lu Q. Facile synthesis of superparamagnetic Fe₃O₄@polyphosphazene@Au shells for magnetic resonance imaging and photothermal therapy. ACS Applied Materials & Interfaces, 2013, 5(11): 4586–4591

[64] Ohulchanskyy T Y, Kopwitthaya A, Jeon M, Guo M, Law W C, Furlani E P, Kim C, Prasad P N. Phospholipid micelle-based magneto-plasmonic nanoformulation for magnetic field-directed, imaging-guided photo-induced cancer therapy. Nanomedicine-UK, 2013, 9(8): 1192–1202

[65] Wang C, Irudayaraj J. Multifunctional magnetic-optical nanoparticle probes for simultaneous detection, separation, and thermal ablation of multiple pathogens. Small, 2010, 6(2): 283–289

[66] Kirui D K, Khalidov I, Wang Y, Batt C A. Targeted near-IR hybrid magnetic nanoparticles for in vivo cancer therapy and imaging. Nanomedicine-UK, 2013, 9(5): 702–711

[67] Kirui D K, Rey D A, Batt C A. Gold hybrid nanoparticles for targeted phototherapy and cancer imaging. Nanotechnology, 2010, 21(10): 105105

[68] Shi X, Gong H, Li Y, Wang C, Cheng L, Liu Z. Graphene-based magnetic plasmonic nanocomposite for dual bioimaging and photothermal therapy. Biomaterials, 2013, 34(20): 4786–4793

[69] 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. Advanced Materials, 2012, 24(14): 1868–1872

[70] Ma Y, Tong S, Bao G, Gao C, Dai Z. Indocyanine green loaded SPIO nanoparticles with phospholipid-PEG coating for dual-modal imaging and photothermal therapy. Biomaterials, 2013, 34(31): 7706–7714

[71] Wang C, Xu H, Liang C, Liu Y, Li Z, Yang G, Cheng L, Li Y, Liu Z. Iron oxide @ polypyrrole nanoparticles as a multifunctional drug carrier for remotely controlled cancer therapy with synergistic antitumor effect. ACS Nano, 2013, 7(8): 6782–6795

[72] Shen S, Kong F, Guo X, Wu L, Shen H, Xie M, Wang X, Jin Y, Ge Y. CMCTS stabilized Fe₃O₄ particles with extremely low toxicity as highly efficient near-infrared photothermal agents for in vivo tumor ablation. Nanoscale, 2013, 5(17): 8056–8066

[73] Chu M, Shao Y, Peng J, Dai X, Li H, Wu Q, Shi D. Near-infrared laser light mediated cancer therapy by photothermal effect of Fe₃O₄ magnetic nanoparticles. Biomaterials, 2013, 34(16): 4078–4088

[74] Levy M, Luciani N, Alloyeau D, Elgrabli D, Deveaux V, Pechoux C, Chat S, Wang G, Vats N, Gendron F, Factor C, Lotersztajn S, Luciani A, Wilhelm C, Gazeau F. Long term in vivo biotransformation of iron oxide nanoparticles. Biomaterials, 2011, 32(16): 3988–3999

[75] 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

[76] Tassa C, Shaw S Y, Weissleder R. Dextran-coated iron oxide nanoparticles: a versatile platform for targeted molecular imaging, molecular diagnostics, and therapy. Accounts of Chemical Research, 2011, 44(10): 842–852

[77] Yoon H J, Lim T G, Kim J H, Cho Y M, Kim Y S, Chung U S, Kim J H, Choi B W, Koh W G, Jang W D. Fabrication of multifunctional layer-by-layer nanocapsules toward the design of theragnostic nano-platform. Biomacromolecules, 2014, 15(4): 1382–1389

[78] Shi J, Yu X, Wang L, Liu Y, Gao J, Zhang J, Ma R, Liu R, Zhang Z. PEGylated fullerene/iron oxide nanocomposites for photodynamic therapy, targeted drug delivery and MR imaging. Biomaterials, 2013, 34(37): 9666–9677

[79] Huang G, Chen H, Dong Y, Luo X, Yu H, Moore Z, Bey E A, Boothman D A, Gao J. Superparamagnetic iron oxide nanoparticles: amplifying ROS stress to improve anticancer drug efficacy. Theranostics, 2013, 3(2): 116–126

[80] Taratula O, Garbuzenko O, Savla R, Wang Y A, He H, Minko T. Multifunctional nanomedicine platform for cancer specific delivery of siRNA by superparamagnetic iron oxide nanoparticles-dendrimer complexes. Current Drug Delivery, 2011, 8(1): 59–69

[81] Tang C, Russell P J, Martiniello-Wilks R, Rasko J E, Khatri A. Concise review: Nanoparticles and cellular carriers-allies in cancer imaging and cellular gene therapy? Stem Cells (Dayton, Ohio), 2010, 28(9): 1686–1702

[82] Medarova Z, Pham W, Farrar C, Petkova V, Moore A. In vivo imaging of siRNA delivery and silencing in tumors. Nature Medicine, 2007, 13(3): 372–377

[83] Chen J, Zhu S, Tong L, Li J, Chen F, Han Y, Zhao M, Xiong W. Superparamagnetic iron oxide nanoparticles mediated (131)I-hVEGF siRNA inhibits hepatocellular carcinoma tumor growth in nude mice. BMC Cancer, 2014, 14(1): 114

[84] Turcheniuk K, Tarasevych A V, Kukhar V P, Boukherroub R, Szunerits S. Recent advances in surface chemistry strategies for the fabrication of functional iron oxide based magnetic nanoparticles. Nanoscale, 2013, 5(22): 10729–10752

[85] Hu S H, Hsieh T Y, Chiang C S, Chen P J, Chen Y Y, Chiu T L, Chen S Y. Surfactant-free, lipo-polymersomes stabilized by iron oxide nanoparticles/polymer interlayer for synergistically targeted and magnetically guided gene delivery. Advanced Healthcare Materials, 2014, 3(2): 273–282

[86] Jiang S, Eltoukhy A A, Love K T, Langer R, Anderson D G. Lipidoid-coated iron oxide nanoparticles for efficient DNA and siRNA delivery. Nano Letters, 2013, 13(3): 1059–1064

[87] Yathindranath V, Sun Z, Worden M, Donald L J, Thliveris J A, Miller D W, Hegmann T. One-pot synthesis of iron oxide nanoparticles with functional silane shells: a versatile general precursor for conjugations and biomedical applications. Langmuir, 2013, 29(34): 10850–10858

[88] Wang C, Ravi S, Martinez G V, Chinnasamy V, Raulji P, Howell M, Davis Y, Mallela J, Seehra M S, Mohapatra S. Dual-purpose magnetic micelles for MRI and gene delivery. Journal of Controlled Release, 2012, 163(1): 82–92

[89] He H, David A, Chertok B, Cole A, Lee K, Zhang J, Wang J, Huang Y, Yang V C. Magnetic nanoparticles for tumor imaging and therapy: a so-called theranostic system. Pharmaceutical Research, 2013, 30(10): 2445–2458

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