Multifunctional nanoparticle systems for combined chemo- and photothermal cancer therapy

Abstract

Hyperthermia has long been considered as an adjuvant therapy for treating various diseases. Cancer treatment exploiting hyperthermia shows great clinical potential for a wide range of tumors. Importantly, the efficacy of hyperthermal therapy has recently been enhanced by the development of functional nanomaterials. The unique physicochemical properties of nanomaterials afford the specific localization of hyperthermia to primary tumors and early-stage cancers. In particular, due to their high rate of light-to-heat conversion and their capacity to be activated by tissue-penetrating electromagnetic radiation, near-infrared (NIR) light-absorbing plasmonic nanomaterials have attracted considerable attention as candidates for noninvasive photothermal therapy. The purpose of this article is to provide a overview on the current development in multifunctional nanomaterials capable of combined hyperthermia-chemotherapy delivery.

Keywords

combination therapy / multifunctional nanoparticle / drug delivery / hyperthermia / photothermal therapy

References

[1] Ferlay J, Shin H-R, Bray F, . Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. International Journal of Cancer , 2010, 127(12): 2893–2917
[2] Glimelius B, Hoffman K, Sj?dén P O, . Chemotherapy improves survival and quality of life in advanced pancreatic and biliary cancer. Annals of Oncology , 1996, 7(6): 593–600
[3] Ferlay J, Autier P, Boniol M, . Estimates of the cancer incidence and mortality in Europe in 2006. Annals of Oncology , 2007, 18(3): 581–592
[4] McConnell J D, Roehrborn C G, Bautista O M, . The long-term effect of doxazosin, finasteride, and combination therapy on the clinical progression of benign prostatic hyperplasia. The New England Journal of Medicine , 2003, 349(25): 2387–2398
[5] O’Shaughnessy J, Miles D, Vukelja S, . Superior survival with capecitabine plus docetaxel combination therapy in anthracycline-pretreated patients with advanced breast cancer: phase III trial results. Journal of Clinical Oncology , 2002, 20(12): 2812–2823
[6] Bendas G, Rothe U, Scherphof G L, . The influence of repeated injections on pharmacokinetics and biodistribution of different types of sterically stabilized immunoliposomes. Biochimica et Biophysica Acta , 2003, 1609(1): 63–70
[7] Wilson K D, Raney S G, Sekirov L, . Effects of intravenous and subcutaneous administration on the pharmacokinetics, biodistribution, cellular uptake and immunostimulatory activity of CpG ODN encapsulated in liposomal nanoparticles. International Immunopharmacology , 2007, 7(8): 1064–1075
[8] Glazer E S, Curley S A. The ongoing history of thermal therapy for cancer. Surgical Oncology Clinics of North America , 2011, 20(2): 229–235
[9] Hildebrandt B, Wust P, Ahlers O, . The cellular and molecular basis of hyperthermia. Critical Reviews in Oncology/Hematology , 2002, 43(1): 33–56
[10] Wust P, Hildebrandt B, Sreenivasa G, . Hyperthermia in combined treatment of cancer. The Lancet Oncology , 2002, 3(8): 487–497
[11] Issels R D. Hyperthermia adds to chemotherapy. European Journal of Cancer , 2008, 44(17): 2546–2554
[12] Issels R, Hyperthermia combined with chemotherapy — biological rationale, clinical application, and treatment results. Onkologie , 1999, 22(5): 374–381
[13] Falk M H, Issels R D. Hyperthermia in oncology. International Journal of Hyperthermia , 2001, 17(1): 1–18
[14] Takahashi I, Emi Y, Hasuda S, . Clinical application of hyperthermia combined with anticancer drugs for the treatment of solid tumors. Surgery , 2002, 131(1 Supplement 1): S78–S84
[15] Cella D F, Tulsky D S, Gray G, . The Functional Assessment of Cancer Therapy scale: development and validation of the general measure. Journal of Clinical Oncology , 1993, 11(3): 570–579
[16] Peer D, Karp J M, Hong S, . Nanocarriers as an emerging platform for cancer therapy. Nature Nanotechnology , 2007, 2(12): 751–760
[17] Ferrari M. Cancer nanotechnology: opportunities and challenges. Nature Reviews. Cancer , 2005, 5(3): 161–171
[18] Melancon M P, Zhou M, Li C. Cancer theranostics with near-infrared light-activatable multimodal nanoparticles. Accounts of Chemical Research , 2011, 44(10): 947–956
[19] Sanvicens N, Marco M P. Multifunctional nanoparticles — properties and prospects for their use in human medicine. Trends in Biotechnology , 2008, 26(8): 425–433
[20] Wainwright M. Therapeutic applications of near-infrared dyes. Coloration Technology , 2010, 126(3): 115–126
[21] Mohamed F, Marchettini P, Stuart O A, . Thermal enhancement of new chemotherapeutic agents at moderate hyperthermia. Annals of Surgical Oncology , 2003, 10(4): 463–468
[22] Yuan A, Wu J, Tang X, . Application of near-infrared dyes for tumor imaging, photothermal, and photodynamic therapies. Journal of Pharmaceutical Sciences , 2013, 102(1): 6–28
[23] Lindner L H, Eichhorn M E, Eibl H, . Novel temperature-sensitive liposomes with prolonged circulation time. Clinical Cancer Research , 2004, 10(6): 2168–2178
[24] Lovell J F, Jin C S, Huynh E, . Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents. Nature Materials , 2011, 10(4): 324–332
[25] Manchanda R, Fernandez-Fernandez A, Nagesetti A, . Preparation and characterization of a polymeric (PLGA) nanoparticulate drug delivery system with simultaneous incorporation of chemotherapeutic and thermo-optical agents. Colloids and Surfaces B: Biointerfaces , 2010, 75(1): 260–267
[26] Zheng X, Xing D, Zhou F, . Indocyanine green-containing nanostructure as near infrared dual-functional targeting probes for optical imaging and photothermal therapy. Molecular Pharmaceutics , 2011, 8(2): 447–456
[27] Zheng X, Zhou F, Wu B, . Enhanced tumor treatment using biofunctional indocyanine green-containing nanostructure by intratumoral or intravenous injection. Molecular Pharmaceutics , 2012, 9(3): 514–522
[28] von Maltzahn G, Park J H, Agrawal A, . Computationally guided photothermal tumor therapy using long-circulating gold nanorod antennas. Cancer Research , 2009, 69(9): 3892–3900
[29] Hu M, Chen J, Li Z Y, . Gold nanostructures: engineering their plasmonic properties for biomedical applications. Chemical Society Reviews , 2006, 35(11): 1084–1094
[30] Hirsch L R, Jackson J B, Lee A, . A whole blood immunoassay using gold nanoshells. Analytical Chemistry , 2003, 75(10): 2377–2381
[31] Averitt R D, Westcott S L, Halas N J. Linear optical properties of gold nanoshells. Journal of the Optical Society of America B , 1999, 16(10): 1824–1832
[32] Shi W, Sahoo Y, Swihart M T, . Gold nanoshells on polystyrene cores for control of surface plasmon resonance. Langmuir , 2005, 21(4): 1610–1617
[33] Wu G, Mikhailovsky A, Khant H A, . Remotely triggered liposome release by near-infrared light absorption via hollow gold nanoshells. Journal of the American Chemical Society , 2008, 130(26): 8175–8177
[34] Melancon M P, Lu W, Yang Z, . In vitro and in vivo targeting of hollow gold nanoshells directed at epidermal growth factor receptor for photothermal ablation therapy. Molecular Cancer Therapeutics , 2008, 7(6): 1730–1739
[35] Liu H, Liu T, Wu X, . Targeting gold nanoshells on silica nanorattles: a drug cocktail to fight breast tumors via a single irradiation with near-infrared laser light. Advanced Materials , 2012, 24(6): 755–761
[36] Lee S-M, Park H, Choi J-W, . Multifunctional nanoparticles for targeted chemophotothermal treatment of cancer cells. Angewandte Chemie International Edition , 2011, 50(33): 7581–7586
[37] Park H, Yang J, Lee J, . Multifunctional nanoparticles for combined doxorubicin and photothermal treatments. ACS Nano , 2009, 3(10): 2919–2926
[38] Lee S-M, Park H, Yoo K-H. Synergistic cancer therapeutic effects of locally delivered drug and heat using multifunctional nanoparticles. Advanced Materials , 2010, 22(36): 4049–4053
[39] Kennedy L C, Bickford L R, Lewinski N A, . A new era for cancer treatment: gold-nanoparticle-mediated thermal therapies. Small , 2011, 7(2): 169–183
[40] Gao J, Bender C M, Murphy C J. Dependence of the gold nanorod aspect ratio on the nature of the directing surfactant in aqueous solution. Langmuir , 2003, 19(21): 9065–9070
[41] Jain P K, Lee K S, El-Sayed I H, . Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine. The Journal of Physical Chemistry B , 2006, 110(14): 7238–7248
[42] Zhang Z, Wang L, Wang J, . Mesoporous silica-coated gold nanorods as a light-mediated multifunctional theranostic platform for cancer treatment. Advanced Materials , 2012, 24(11): 1418–1423
[43] Hauck T S, Jennings T L, Yatsenko T, . Enhancing the toxicity of cancer chemotherapeutics with gold nanorod hyperthermia. Advanced Materials , 2008, 20(20): 3832–3838
[44] Dickerson E B, Dreaden E C, Huang X, . Gold nanorod assisted near-infrared plasmonic photothermal therapy (PPTT) of squamous cell carcinoma in mice. Cancer Letters , 2008, 269(1): 57–66
[45] Tang H, Shen S, Guo J, . Gold nanorods@mSiO₂ with a smart polymer shell responsive to thermo/near-infrared light for chemo-photothermal therapy. Journal of Materials Chemistry , 2012, 22(31): 16095–16103
[46] Xiao Y, Hong H, Matson V Z, . Gold nanorods conjugated with doxorubicin and cRGD for combined anticancer drug delivery and PET imaging. Theranostics , 2012, 2(8): 757–768
[47] Chen R, Zheng X, Qian H, . Combined near-IR photothermal therapy and chemotherapy using gold-nanorod/chitosan hybrid nanospheres to enhance the antitumor effect. Biomaterials Science , 2013, 1(3): 285–293
[48] Ren F, Bhana S, Norman D D, . Gold nanorods carrying paclitaxel for photothermal-chemotherapy of cancer. Bioconjugate Chemistry , 2013, 24(3): 376–386
[49] Wei Q, Ji J, Shen J. Synthesis of near-infrared responsive gold nanorod/PNIPAAm core/shell nanohybrids via surface initiated ATRP for smart drug delivery. Macromolecular Rapid Communications , 2008, 29(8): 645–650
[50] Book Newell B, Wang Y, Irudayaraj J. Multifunctional gold nanorod theragnostics probed by multi-photon imaging. European Journal of Medicinal Chemistry , 2012, 48: 330–337
[51] Chen J, Glaus C, Laforest R, . Gold nanocages as photothermal transducers for cancer treatment. Small , 2010, 6(7): 811–817
[52] Skrabalak S E, Chen J, Sun Y, . Gold nanocages: synthesis, properties, and applications. Accounts of Chemical Research , 2008, 41(12): 1587–1595
[53] Sun Y, Xia Y. Shape-controlled synthesis of gold and silver nanoparticles. Science , 2002, 298(5601): 2176–2179
[54] Chen J, Saeki F, Wiley B J, . Gold nanocages: bioconjugation and their potential use as optical imaging contrast agents. Nano Letters , 2005, 5(3): 473–477
[55] Moon G D, Choi S W, Cai X, . A new theranostic system based on gold nanocages and phase-change materials with unique features for photoacoustic imaging and controlled release. Journal of the American Chemical Society , 2011, 133(13): 4762–4765
[56] Bianco A, Kostarelos K, Prato M. Applications of carbon nanotubes in drug delivery. Current Opinion in Chemical Biology , 2005, 9(6): 674–679
[57] Shi Kam N W, O’Connell M, Wisdom J A, . Carbon nanotubes as multifunctional biological transporters and near-infrared agents for selective cancer cell destruction. Proceedings of the National Academy of Sciences of the United States of America , 2005, 102(33): 11600–11605
[58] Zhou F, Xing D, Ou Z, . Cancer photothermal therapy in the near-infrared region by using single-walled carbon nanotubes. Journal of Biomedical Optics , 2009, 14(2): 021009 (7 pages)
[59] Moon H K, Lee S H, Choi H C. In vivo near-infrared mediated tumor destruction by photothermal effect of carbon nanotubes. ACS Nano , 2009, 3(11): 3707–3713
[60] Chakravarty P, Marches R, Zimmerman N S, . Thermal ablation of tumor cells with antibody-functionalized single-walled carbon nanotubes. Proceedings of the National Academy of Sciences of the United States of America , 2008, 105(25): 8697–8702
[61] Fisher J W, Sarkar S, Buchanan C F, . Photothermal response of human and murine cancer cells to multiwalled carbon nanotubes after laser irradiation. Cancer Research , 2010, 70(23): 9855–9864
[62] Ghosh S, Dutta S, Gomes E, . Increased heating efficiency and selective thermal ablation of malignant tissue with DNA-encased multiwalled carbon nanotubes. ACS Nano , 2009, 3(9): 2667–2673
[63] Liu Z, Chen K, Davis C, . Drug delivery with carbon nanotubes for in vivo cancer treatment. Cancer Research , 2008, 68(16): 6652–6660
[64] Liu Z, Tabakman S, Welsher K, . Carbon nanotubes in biology and medicine: in vitro and in vivo detection, imaging and drug delivery. Nano Research , 2009, 2(2): 85–120
[65] Zhang W, Wang C, Li Z, . Unraveling stress-induced toxicity properties of graphene oxide and the underlying mechanism. Advanced Materials , 2012, 24(39): 5391–5397
[66] Chen H, Müller M B, Gilmore K J, . Mechanically strong, electrically conductive, and biocompatible graphene paper. Advanced Materials , 2008, 20(18): 3557–3561
[67] Liu Z, Robinson J T, Sun X, . PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. Journal of the American Chemical Society , 2008, 130(33): 10876–10877
[68] Yang K, Zhang S, Zhang G, . Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Letters , 2010, 10(9): 3318–3323
[69] Robinson J T, Tabakman S M, Liang Y, . Ultrasmall reduced graphene oxide with high near-infrared absorbance for photothermal therapy. Journal of the American Chemical Society , 2011, 133(17): 6825–6831
[70] Sherlock S P, Tabakman S M, Xie L, . Photothermally enhanced drug delivery by ultrasmall multifunctional FeCo/graphitic shell nanocrystals. ACS Nano , 2011, 5(2): 1505–1512
[71] Sherlock S P, Dai H. Multifunctional FeCo-graphitic carbon nanocrystals for combined imaging, drug delivery and tumor-specific photothermal therapy in mice. Nano Research , 2011, 4(12): 1248–1260
[72] Zhang W, Guo Z, Huang D, . Synergistic effect of chemo-photothermal therapy using PEGylated graphene oxide. Biomaterials , 2011, 32(33): 8555–8561
[73] Reddy L H, Arias J L, Nicolas J, . Magnetic nanoparticles: design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chemical Reviews , 2012, 112(11): 5818–5878
[74] Kumar C S S R, Mohammad F. Magnetic nanomaterials for hyperthermia-based therapy and controlled drug delivery. Advanced Drug Delivery Reviews , 2011, 63(9): 789–808
[75] Laurent S, Dutz S, H?feli U O, . Magnetic fluid hyperthermia: focus on superparamagnetic iron oxide nanoparticles. Advances in Colloid and Interface Science , 2011, 166(1–2): 8–23
[76] Ito A, Shinkai M, Honda H, . Medical application of functionalized magnetic nanoparticles. Journal of Bioscience and Bioengineering , 2005, 100(1): 1–11
[77] Hu S H, Liao B J, Chiang C S, . Core-shell nanocapsules stabilized by single-component polymer and nanoparticles for magneto-chemotherapy/hyperthermia with multiple drugs. Advanced Materials , 2012, 24(27): 3627–3632
[78] Al-Jamal W T, Kostarelos K. Liposome–nanoparticle hybrids for multimodal diagnostic and therapeutic applications. Nanomedicine , 2007, 2(1): 85–98
[79] Kim J, Park S, Lee J E, . Designed fabrication of multifunctional magnetic gold nanoshells and their application to magnetic resonance imaging and photothermal therapy. Angewandte Chemie International Edition , 2006, 45(46): 7754–7758
[80] Ma M, Chen H, Chen Y, . Au capped magnetic core/mesoporous silica shell nanoparticles for combined photothermo-/chemo-therapy and multimodal imaging. Biomaterials , 2012, 33(3): 989–998
[81] Sugarbaker P H, Mora J T, Carmignani P, . Update on chemotherapeutic agents utilized for perioperative intraperitoneal chemotherapy. Oncologist , 2005, 10(2): 112–122
[82] Levi-Polyachenko N H, Carroll D L, Stewart IV J H. Applications of carbon-based nanomaterials for drug delivery in oncology. In: Cataldo F, Da Ros T, eds. Carbon Materials: Chemistry and Physics (Volume 1). Medicinal Chemistry and Pharmacological Potential of Fullerenes and Carbon Nanotubes . Springer, 2008, 223 –266
[83] Calderwood S K, Khaleque M A, Sawyer D B, . Heat shock proteins in cancer: chaperones of tumorigenesis. Trends in Biochemical Sciences , 2006, 31(3): 164–172
[84] Zhu M, Nie G, Meng H, . Physicochemical properties determine nanomaterial cellular uptake, transport, and fate. Accounts of Chemical Research , 2013, 46(3): 622–631
[85] Wang B, He X, Zhang Z, . Metabolism of nanomaterials in vivo: blood circulation and organ clearance. Accounts of Chemical Research , 2013, 46(3): 761–769