Abstract
Cancer has been a significant threat to human health with more than eight million deaths each year in the world. Therefore, there is a significant need for novel technologies to effectively treat cancer and ultimately reduce cancer recurrences, treatment costs, number of radical cystectomies and mortality. A promising therapeutic platform for cancer is offered by nanoparticle-mediated therapy. This review highlights the development and applications of various nanoparticle platforms for photo-induced hyperthermia and immunotherapy. Taking advantage of gold's high biocompatibility, gold nanoparticles (GNPs) can be injected intravenously and accumulate preferentially in cancer cells due to the enhanced permeability and retention effect. Various gold nanoplatforms including nanospheres, nanoshells, nanorods, nanocages and nanostars have been used for effective photothermal treatment of various cancers. GNPs have also been used in immunotherapies, involving cancer antigen and immune adjuvant delivery as well as combination therapies with photothermal therapy. Among GNPs platforms, gold nanostars (GNS) have great therapeutic potential due to their unique star-shaped geometry that dramatically enhances light absorption and provides high photon-to-heat conversion efficiency due to the plasmonic effect. This photothermal process can be exploited to specifically ablate tumors and, more importantly, to amplify the antitumor immune response following the highly immunogenic thermal death of cancer cells. GNS-mediated photothermal therapy combined with checkpoint immunotherapy has been found to reverse tumor-mediated immunosuppression, thereby leading to the treatment of not only primary tumors but also cancer metastasis, as well as to induce effective long-lasting immunity, in other words, an anticancer ‘vaccine’ effect.
References
- 1 . Hyperthermia in oncology. Int. J. Hyperthermia 17(1), 1–18 (2001).
- 2 . Hyperthermia as adjunct to intravesical chemotherapy for bladder cancer. Biomed. Res. Int. 2013, 262313 (2013).
- 3 The cellular and molecular basis of hyperthermia. Crit. Rev. Oncol./Hematol. 43(1), 33–56 (2002).
- 4 Old and new facts about hyperthermia-induced modulations of the immune system. Int. J. Hyperthermia 28(6), 528–542 (2012).
- 5 Biological rationales and clinical applications of temperature controlled hyperthermia – implications for multimodal cancer treatments. Curr. Med. Chem. 17(27), 3045–3057 (2010).
- 6 Hyperthermia in combined treatment of cancer. Lancet Oncol. 3(8), 487–497 (2002).
- 7 Nanoshell-enabled photonics-based imaging and therapy of cancer. Technol. Cancer Res. Treat. 3(1), 33–40 (2004).
- 8 . Macrophage cell membrane camouflaged Au nanoshells for in vivo prolonged circulation life and enhanced cancer photothermal therapy. ACS Appl. Mater. Interfaces 8, 9610–9618 (2016).
- 9 . Near-infrared-activated nanocalorifiers in microcapsules: vapor bubble generation for in vivo enhanced cancer therapy. Angew. Chem. Int. Ed. 54, 12782–12787 (2015).
- 10 . Molecular parameters of hyperthermia for radiosensitization. Crit. Rev. Eukaryot. Gene Expr. 19(3), 235–251 (2009).
- 11 Growth inhibition of re-challenge B16 melanoma transplant by conjugates of melanogenesis substrate and magnetite nanoparticles as the basis for developing melanoma-targeted chemo-thermo-immunotherapy. J. Biomed. Biotechnol. 2009, 457936 (2009).
- 12 . Biointerfacing polymeric microcapsules for in vivo near-infrared light-triggered drug release. Nanoscale 7, 19092–19098 (2015).
- 13 . Hyperthermia and thermosensitive liposomes for improved delivery of chemotherapeutic drugs to solid tumors. Pharm. Res. 27(8), 1750–1754 (2010).
- 14 . Immunological responses triggered by photothermal therapy with carbon nanotubes in combination with anti-CTLA-4 therapy to inhibit cancer metastasis. Adv. Mater. 26(48), 8154–8162 (2014).
- 15 . A study of the nucleation and growth processes in the synthesis of colloidal gold. Disc. Faraday Soc. 11, 55–75 (1951).
- 16 . The color of colloidal gold. J. Colloid Sci. 9, 26–35 (1954).
- 17 . Controlled nucleation for the regulation of the particle size in monodisperse gold suspensions. Nature Phys. Sci. 241(105), 20 (1973).
- 18 A feasible strategy for self-assembly of gold nanoparticles via dithiol-PEG for photothermal therapy of cancers. RSC Adv. 8, 6120–6124 (2018).
- 19 . Cantharidin-encapsulated thermal-sensitive liposomes coated with gold nanoparticles for enhanced photothermal therapy on A431 cells. Int. J. Nanomedicine 13, 2143–2160 (2018).
- 20 . IR780-dye loaded gold nanoparticles as new near infrared activatable nanotheranostics agents for simultaneous photodynamic and photothermal therapy and intracellular tracking by surface enhanced resonant Raman scattering imaging. J. Colloid Interface Sci. 517, 239–250 (2018).
- 21 . Porphyrin derivative conjugated with gold nanoparticles for dual-modality photodynamic and photothermal therapies in vitro. ACS Biomater. Sci. Eng 4, 963–972 (2018).
- 22 . Synthesis and characterization of small-sized gold nanoparticles coated by bovine serum albumin (BSA) for cancer photothermal therapy. Photodiagnosis Photodyn. Ther. 21, 201–210 (2018).
- 23 . Gold nanostars for surface-enhanced Raman scattering: synthesis, characterization and optimization. J. Phys. Chem. C 112(48), 18849–18859 (2008).
- 24 . Gold nanostars: surfactant-free synthesis, 3D modelling, and two-photon photoluminescence imaging. Nanotechnology 23(7), 075102 (2012).
- 25 . TAT peptide-functionalized gold nanostars: enhanced intracellular delivery and efficient NIR photothermal therapy using ultralow irradiance. J. Am. Soc. Chem. 134(28), 11358–11361 (2012).
- 26 A plasmonic gold nanostar theranostic probe for in vivo tumor imaging and photothermal therapy. Theranostics 5(9), 946–960 (2015).
- 27 . In vivo particle tracking and photothermal ablation using plasmon-resonant gold nanostars. Nanomedicine: NBM 8(8), 1355–1363 (2012).
- 28 . Recent progress in cancer thermal therapy using gold nanoparticles. J. Phys. Chem. C 120(9), 4691–4716 (2016).
- 29 . Nanoengineering of optical resonances. Chem. Phys. Lett. 288(2–4), 243–247 (1998).
- 30 . A hybridization model for the plasmon response of complex nanostructures. Science 302(5644), 419–422 (2003).
- 31 Metal nanoshells. Ann. Biomed. Eng. 34(1), 15–22 (2006).
- 32 . Universal scaling of plasmon coupling in metal nanostructures: extension from particle pairs to nanoshells. Nano Lett. 7(9), 2854–2858 (2007).
- 33 A new era for cancer treatment: gold-nanoparticle-mediated thermal therapies. Small 7(2), 169–183 (2011).
- 34 Nanoshell-mediated near-infrared thermal therapy of tumors under magnetic resonance guidance. Proc. Natl Acad. Sci. USA 100(23), 13549–13554 (2003).
- 35 . Photo-thermal tumor ablation in mice using near infrared-absorbing nanoparticles. Cancer Lett. 209(2), 171–176 (2004).
- 36 Gold nanoshell bioconjugates for molecular imaging in living cells. Opt. Lett. 30(9), 1012–1014 (2005).
- 37 . Efficacy of laser-activated gold nanoshells in ablating prostate cancer cells in vitro. J. Endourol. 21(8), 939–943 (2007).
- 38 . Immunonanoshells for targeted photothermal ablation in medulloblastoma and glioma: an in vitro evaluation using human cell lines. J. Neurooncol. 86(2), 165–172 (2008).
- 39 . EphrinAl-targeted nanoshells for photothermal ablation of prostate cancer cells. Int. J. Nanomed. 3(3), 351 (2008).
- 40 . In vitro photothermal study of gold nanoshells functionalized with small targeting peptides to liver cancer cells. J. Mater. Sc. Mater. Med. 21(2), 665–674 (2010).
- 41 Feasibility study of particle-assisted laser ablation of brain tumors in orthotopic canine model. Cancer Res. 69(4), 1659–1667 (2009).
- 42 . Selective cell targeting with light-absorbing microparticles and nanoparticles. Biophys. J. 84(6), 4023–4032 (2003).
- 43 . Photothermal detection of local thermal effects during selective nanophotothermolysis. Appl. Phys. Lett. 83(24), 4897–4899 (2003).
- 44 . Photothermal guidance for selective photothermolysis with nanoparticles. Presented at: Laser Interaction with Tissue and Cells Xv (2004).
- 45 . Synergistic enhancement of selective nanophotothermolysis with gold nanoclusters: potential for cancer therapy. Lasers Surg. Med. 37(3), 219–226 (2005).
- 46 . Self-assembling nanoclusters in living systems: application for integrated photothermal nanodiagnostics and nanotherapy. Nanomedicine: NBM 1(4), 326–345 (2005).
- 47 LANTCET: elimination of solid tumor cells with photothermal bubbles generated around clusters of gold nanoparticles. Nanomedicine 3(5), 647–667 (2008).
- 48 . The potential use of the enhanced nonlinear properties of gold nanospheres in photothermal cancer therapy. Lasers Sur. Med. 39(9), 747–753 (2007).
- 49 . Method of laser activated nano-thermolysis for elimination of tumor cells. Cancer Lett. 239(1), 36–45 (2006).
- 50 Comparative study of photothermolysis of cancer cells with nuclear-targeted or cytoplasm-targeted gold nanospheres: continuous wave or pulsed lasers. J. Biomed. Opt. 15(5), 058002 (2010).
- 51 . Form of ultramicroscopic particles of silver. Ann. Phys. 47(10), 270–284 (1915).
- 52 . Mechanism of silver (I)-assisted growth of gold nanorods and bipyramids. J. Phys. Chem. B 109(47), 22192–22200 (2005).
- 53 . Preparation and growth mechanism of gold nanorods (NRs) using seed-mediated growth method. Chem. Mater. 15(10), 1957–1962 (2003).
- 54 Anisotropic metal nanoparticles: synthesis, assembly, and optical applications. J. Phys. Chem. B 109(29), 13857–13870 (2005).
- 55 . Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods. J. Am. Soc. Chem. 128(6), 2115–2120 (2006).
- 56 . Calculated absorption and scattering properties of gold nanoparticles of different size, shape and composition: applications in biological imaging and biomedicine. J. Phys. Chem. B 110(14), 7238–7248 (2006).
- 57 . Gold nanorod-sensitized cell death: microscopic observation of single living cells irradiated by pulsed near-infrared laser light in the presence of gold nanorods. Chem. Lett. 35(5), 500–501 (2006).
- 58 . Photothermal reshaping of gold nanorods prevents further cell death. Nanotechnology 17(17), 4431 (2006).
- 59 Gold nanorod assisted near-infrared plasmonic photothermal therapy (PPTT) of squamous cell carcinoma in mice. Cancer Lett. 269(1), 57–66 (2008).
- 60 . Photothermal therapy in a murine colon cancer model using near-infrared absorbing gold nanorods. J. Biomed. Opt. 15(1), 018001 (2010).
- 61 Computationally guided photothermal tumor therapy using long-circulating gold nanorod antennas. Cancer Res. 69(9), 3892–3900 (2009).
- 62 Magnetic iron oxide nanoworms for tumor targeting and imaging. Adv. Mater. 20(9), 1630–1635 (2008).
- 63 . Synthesis, characterization, and tunable optical properties of hollow gold nanospheres. J. Phys. Chem. B 110(40), 19935–19944 (2006).
- 64 In vitro and in vivo targeting of hollow gold nanoshells directed at epidermal growth factor receptor for photothermal ablation therapy. Mol. Cancer. Ther. 7(6), 1730–1739 (2008).
- 65 Targeted photothermal ablation of murine melanomas with melanocyte-stimulating hormone analog-conjugated hollow gold nanospheres. Clin. Cancer Res. 15(3), 876–886 (2009).
- 66 . Hollow gold nanoparticles encapsulating horseradish peroxidase. Biomaterials 26(33), 6743–6753 (2005).
- 67 Gold nanoshelled liquid perfluorocarbon nanocapsules for combined dual modal ultrasound/CT imaging and photothermal therapy of cancer. Small 10(6), 1220–1227 (2014).
- 68 . Template-engaged replacement reaction: a one-step approach to the large-scale synthesis of metal nanostructures with hollow interiors. Nano Lett. 2(5), 481–485 (2002).
- 69 Immuno gold nanocages with tailored optical properties for targeted photothermal destruction of cancer cells. Nano Lett. 7(5), 1318–1322 (2007).
- 70 . A quantitative study on the photothermal effect of immuno gold nanocages targeted to breast cancer cells. ACS Nano 2(8), 1645–1652 (2008).
- 71 Gold nanocages as photothermal transducers for cancer treatment. Small 6(7), 811–817 (2010).
- 72 Plasmonics-enhanced and optically modulated delivery of gold nanostars into brain tumor. Nanoscale 6(8), 4078–4082 (2014).
- 73 Shape-dependent two-photon photoluminescence of single gold nanoparticles. J. Phys. Chem. C 118(25), 13904–13911 (2014).
- 74 . Plasmonic gold nanostars for multi-modality sensing and diagnostics. Sensors 15(2), 3706–3720 (2015).
- 75 . Quintuple-modality (SERS-MRI-CT-TPL-PTT) plasmonic nanoprobe for theranostics. Nanoscale 5(24), 12126–12131 (2013).
- 76 . Theranostics for cancer therapy. Curr. Drug Deliv. 10(3), 357–362 (2013).
- 77 . Analysis of the toxicity of gold nano particles on the immune system: effect on dendritic cell functions. J. Nanopart. Res. 12(1), 55–60 (2010).
- 78 . Cytotoxicity and immunological response of gold and silver nanoparticles of different sizes. Small 5(13), 1553–1561 (2009).
- 79 . Size-dependent attenuation of TLR9 signaling by gold nanoparticles in macrophages. J. Immunol. 188(1), 68–76 (2012).
- 80 Gold nanoparticles downregulate interleukin-1S-induced pro-inflammatory responses. Small 9(3), 472–477 (2013).
- 81 . Activation of inflammasomes by tumor cell death mediated by gold nanoshells. Biomaterials 33(7), 2197–2205 (2012).
- 82 Enhancement of tumor thermal therapy using gold nanoparticle–assisted tumor necrosis factor-α delivery. Mol. Cancer Ther. 5(4), 1014–1020 (2006).
- 83 Elimination of metastatic melanoma using gold nanoshell-enabled photothermal therapy and adoptive T cell transfer. PLoS One 8(7), e69073 (2013).
- 84 Gold nanocages covered by smart polymers for controlled release with near-infrared light. Nature Mater. 8(12), 935 (2009).
- 85 Photothermal-chemotherapy with doxorubicin-loaded hollow gold nanospheres: a platform for near-infrared light-trigged drug release. J. Control. Release 158(2), 319–328 (2012).
- 86 Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J. Exp. Med. 202(12), 1691–1701 (2005).
- 87 . The future of CpG immunotherapy in cancer. Immunotherapy 5(1), 1–3 (2013).
- 88 Gold nanoparticle delivery of modified CpG stimulates macrophages and inhibits tumor growth for enhanced immunotherapy. PloS One 8(5), e63550 (2013).
- 88 . Antitumor immunologically modified carbon nanotubes for photothermal therapy. Biomaterials 33(11), 3235–3242 (2012).
- 90 High-density sub-100-nm peptide–gold nanoparticle complexes improve vaccine presentation by dendritic cells in vitro. Nanoscale Res. Lett. 8(1), 72 (2013).
- 91 Imageable antigen-presenting gold nanoparticle vaccines for effective cancer immunotherapy in vivo. Angew. Chem. Int. Ed. 51(35), 8800–8805 (2012).
- 92 . Cellular uptake of gold nanoparticles bearing HIV gp120 oligomannosides. Bioconjug. Chem. 23(4), 814–825 (2012).
- 93 A cellular Trojan Horse for delivery of therapeutic nanoparticles into tumors. Nano Lett. 7(12), 3759–3765 (2007).
- 94 T cells enhance gold nanoparticle delivery to tumors in vivo. Nanoscale Res. Lett. 6(1), 283 (2011).
- 95 Synergistic Immuno Photothermal Nanotherapy (SYMPHONY) for the treatment of unresectable and metastatic cancers. Sci. Rep. 7(1), 8606 (2017).
- 96 . What potential does plasmonics-amplified synergistic immuno photothermal nanotherapy have for treatment of cancer? Nanomedicine 13(2), 139–144 (2018).
- 97 Shining gold nanostars: from cancer diagnostics to photothermal treatment and immunotherapy. J. Immunol. Sci. 2(1), 1–8 (2018).
- 98 . Photothermal therapy with immune-adjuvant nanoparticles together with checkpoint blockade for effective cancer immunotherapy. Nat. Commun. 7, 13 (2016).