Image-guided synergistic photothermal therapy using photoresponsive imaging agent-loaded graphene-based nanosheets.

We report the image-guided synergistic photothermal antitumor effects of photoresponsive near-infrared (NIR) imaging agent, indocyanine green (ICG), by loading onto hyaluronic acid-anchored, reduced graphene oxide (HArGO) nanosheets. Loading of ICG onto either rGO (ICG/rGO) or HArGO (ICG/HArGO) substantially improved the photostability of photoresponsive ICG upon NIR irradiation. After 1min of irradiation, the NIR absorption peak of ICG almost disappeared whereas the peak of ICG on rGO or HArGO was retained even after 5min of irradiation. Compared with plain rGO, HArGO provided greater cellular delivery of ICG and photothermal tumor cell-killing effects upon laser irradiation in CD44-positive KB cells. The temperature of cell suspensions treated with ICG/HArGO was 2.4-fold higher than that of cells treated with free ICG. Molecular imaging revealed that intravenously administered ICG/HArGO accumulated in KB tumor tissues higher than ICG/rGO or free ICG. Local temperatures in tumor tissues of laser-irradiated KB cell-bearing nude mice were highest in those intravenously administered ICG/HArGO, and were sufficient to trigger thermal-induced complete tumor ablation. Immunohistologically stained tumors also showed the highest percentages of apoptotic cells in the group treated with ICG/HArGO. These results suggest that photoresponsive ICG-loaded HArGO nanosheets could serve as a potential theranostic nano-platform for image-guided and synergistic photothermal antitumor therapy.

[1]  Jianfang Wang,et al.  Mass-Based Photothermal Comparison Among Gold Nanocrystals, PbS Nanocrystals, Organic Dyes, and Carbon Black , 2013 .

[2]  G. Wallace,et al.  Processable aqueous dispersions of graphene nanosheets. , 2008, Nature nanotechnology.

[3]  Yu-Kyoung Oh,et al.  Reduced graphene oxide nanosheets coated with an anti-angiogenic anticancer low-molecular-weight heparin derivative for delivery of anticancer drugs. , 2014, Journal of controlled release : official journal of the Controlled Release Society.

[4]  H. Dai,et al.  Ultrasmall reduced graphene oxide with high near-infrared absorbance for photothermal therapy. , 2011, Journal of the American Chemical Society.

[5]  Chunying Chen,et al.  Near‐Infrared Light‐Mediated Nanoplatforms for Cancer Thermo‐Chemotherapy and Optical Imaging , 2013, Advanced materials.

[6]  James H. Adair,et al.  Targeted indocyanine-green-loaded calcium phosphosilicate nanoparticles for in vivo photodynamic therapy of leukemia. , 2011, ACS nano.

[7]  Sanyog Jain,et al.  Hyaluronate tethered, "smart" multiwalled carbon nanotubes for tumor-targeted delivery of doxorubicin. , 2012, Bioconjugate chemistry.

[8]  L. Prodi,et al.  Photothermal sensitisation and therapeutic properties of a novel far-red absorbing cyanine. , 2009, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[9]  Yu-Kyoung Oh,et al.  Safety and tumor tissue accumulation of pegylated graphene oxide nanosheets for co-delivery of anticancer drug and photosensitizer. , 2013, Biomaterials.

[10]  K. Choi,et al.  A facile, one-step nanocarbon functionalization for biomedical applications. , 2012, Nano letters.

[11]  M. Maia,et al.  Biochemical Analysis and Decomposition Products of Indocyanine Green in Relation to Solvents, Dye Concentrations and Laser Exposure , 2013, Ophthalmologica.

[12]  Chen-Sheng Yeh,et al.  Gold nanomaterials conjugated with indocyanine green for dual-modality photodynamic and photothermal therapy. , 2012, Biomaterials.

[13]  Vishal Saxena,et al.  Degradation kinetics of indocyanine green in aqueous solution. , 2003, Journal of pharmaceutical sciences.

[14]  T. Desmettre,et al.  Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography. , 2000, Survey of ophthalmology.

[15]  J. K. Chen,et al.  Theoretical analysis of thermal damage in biological tissues caused by laser irradiation. , 2007, Molecular & cellular biomechanics : MCB.

[16]  Hong Yang,et al.  Micelles assembled with carbocyanine dyes for theranostic near-infrared fluorescent cancer imaging and photothermal therapy. , 2013, Biomaterials.

[17]  Wolfgang Bäumler,et al.  Light-induced decomposition of indocyanine green. , 2008, Investigative ophthalmology & visual science.

[18]  Yuehe Lin,et al.  Graphene and graphene oxide: biofunctionalization and applications in biotechnology , 2011, Trends in Biotechnology.

[19]  Soondong Lee,et al.  Structure-dependent photothermal anticancer effects of carbon-based photoresponsive nanomaterials. , 2014, Biomaterials.

[20]  Clare C. Byeon,et al.  Tumor regression in vivo by photothermal therapy based on gold-nanorod-loaded, functional nanocarriers. , 2011, ACS nano.

[21]  Z. Dai,et al.  Indocyanine green loaded SPIO nanoparticles with phospholipid-PEG coating for dual-modal imaging and photothermal therapy. , 2013, Biomaterials.

[22]  Lucian Mocan,et al.  Advances in cancer therapy through the use of carbon nanotube-mediated targeted hyperthermia , 2011, International journal of nanomedicine.

[23]  Jun Wang,et al.  Combating the drug resistance of cisplatin using a platinum prodrug based delivery system. , 2012, Angewandte Chemie.

[24]  Jianjie Ma,et al.  Core–Shell Nanoparticle-Based Peptide Therapeutics and Combined Hyperthermia for Enhanced Cancer Cell Apoptosis , 2014, ACS nano.

[25]  N. Yamazaki,et al.  Sentinel lymph node biopsy guided by indocyanine green fluorescence for cutaneous melanoma. , 2011, European journal of dermatology : EJD.

[26]  Kai Yang,et al.  Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy. , 2010, Nano letters.

[27]  Gang Liu,et al.  Dye-enhanced graphene oxide for photothermal therapy and photoacoustic imaging. , 2013, Journal of materials chemistry. B.

[28]  Jinhui Wu,et al.  Application of near-infrared dyes for tumor imaging, photothermal, and photodynamic therapies. , 2013, Journal of pharmaceutical sciences.

[29]  G. Gazelle,et al.  Thermal ablation therapy for focal malignancy: a unified approach to underlying principles, techniques, and diagnostic imaging guidance. , 2000, AJR. American journal of roentgenology.

[30]  P. Kamat,et al.  Reduced graphene oxide and porphyrin. An interactive affair in 2-D. , 2010, ACS nano.

[31]  Jin-Sil Choi,et al.  Double-effector nanoparticles: a synergistic approach to apoptotic hyperthermia. , 2012, Angewandte Chemie.

[32]  Yu-Kyoung Oh,et al.  Cholesteryl hyaluronic acid-coated, reduced graphene oxide nanosheets for anti-cancer drug delivery. , 2013, Biomaterials.