Antiangiogenesis-Combined Photothermal Therapy in the Second Near-Infrared Window at Laser Powers Below the Skin Tolerance Threshold
Corresponding Author: Jianfang Wang
Nano-Micro Letters,
Vol. 11 (2019), Article Number: 93
Abstract
Photothermal agents with strong light absorption in the second near-infrared (NIR-II) region (1000–1350 nm) are strongly desired for successful photothermal therapy (PTT). In this work, titania-coated Au nanobipyramids (NBP@TiO2) with a strong plasmon resonance in the NIR-II window were synthesized. The NBP@TiO2 nanostructures have a high photothermal conversion efficiency of (93.3 ± 5.2)% under 1064-nm laser irradiation. They are also capable for loading an anticancer drug combretastatin A-4 phosphate (CA4P). In vitro PTT studies reveal that 1064-nm laser irradiation can efficiently ablate human lung cancer A549 cells and enhance the anticancer effect of CA4P. Moreover, the CA4P-loaded NBP@TiO2 nanostructures combined with PTT induce a synergistic antiangiogenesis effect. In vivo studies show that such CA4P-loaded NBP@TiO2 nanostructures under mild 1064-nm laser irradiation at an optical power density of 0.4 W cm−2, which is lower than the skin tolerance threshold value, exhibit a superior antitumor effect. This work presents not only the development of the NBP@TiO2 nanostructures as a novel photothermal agent responsive in the NIR-II window but also a unique combined chemo-photothermal therapy strategy for cancer therapy.
Highlights:
1 Titania-coated Au nanobipyramids (NBP@TiO2) with a high photothermal conversion efficiency in the NIR-II window are synthesized.
2 The TiO2 shell is capable for the loading of the anticancer drug combretastatin A-4 phosphate (CA4P).
3 The CA4P-loaded NBP@TiO2 nanostructures subjected with photothermal therapy induce synergistic anticancer and antiangiogenesis effects under 1064-nm laser irradiation at a power density lower than the skin tolerance threshold value.
Keywords
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- V. Shanmugam, S. Selvakumar, C.-S. Yeh, Near-infrared light-responsive nanomaterials in cancer therapeutics. Chem. Soc. Rev. 43, 6254–6587 (2014). https://doi.org/10.1039/c4cs00011k
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References
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A.M. Smith, M.C. Mancini, S.M. Nie, Bioimaging: second window for in vivo imaging. Nat. Nanotechnol. 4, 710–711 (2009). https://doi.org/10.1038/nnano.2009.326
A.N. Bashkatov, E.A. Genina, V.I. Kochubey, V.V. Tuchin, Optical properties of human skin, subcutaneous and mucous tissues in the wavelength range from 400 to 2000 nm. J. Phys D-Appl. Phys. 38, 2543–2555 (2005). https://doi.org/10.1088/0022-3727/38/15/004
X.G. Ding, C.H. Liow, M.X. Zhang, R.J. Huang, C.Y. Li et al., Surface plasmon resonance enhanced light absorption and photothermal therapy in the second near-infrared window. J. Am. Chem. Soc. 136, 15684–15693 (2014). https://doi.org/10.1021/ja508641z
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M.-F. Tsai, S.-H. Chang, F.-Y. Cheng, V. Shanmugam, Y.-S. Cheng et al., Au nanorod design as light-absorber in the first and second biological near-infrared windows for in vivo photothermal therapy. ACS Nano 7, 5330–5342 (2013). https://doi.org/10.1021/nn401187c
X.J. Yu, K. Yang, X.Y. Chen, W.W. Li, Black hollow silicon oxide nanoparticles as highly efficient photothermal agents in the second near-infrared window for in vivo cancer therapy. Biomaterials 143, 120–129 (2017). https://doi.org/10.1016/j.biomaterials.2017.07.037
C.S. Guo, H.J. Yu, B. Feng, W.D. Gao, M. Yan et al., Highly efficient ablation of metastatic breast cancer using ammonium–tungsten–bronze nanocube as a novel 1064 nm-laser-driven photothermal agent. Biomaterials 52, 407–416 (2015). https://doi.org/10.1016/j.biomaterials.2015.02.054
T.T. Sun, J.H. Dou, S. Liu, X. Wang, X.H. Zheng et al., Second near-infrared conjugated polymer nanoparticles for photoacoustic imaging and photothermal therapy. ACS Appl. Mater. Interfaces 10, 7919–7926 (2018). https://doi.org/10.1021/acsami.8b01458
B. Guo, Z.H. Sheng, D.H. Hu, C.B. Liu, H.R. Zheng et al., Through scalp and skull NIR-II photothermal therapy of deep orthotopic brain tumors with precise photoacoustic imaging guidance. Adv. Mater. 30, e1802591 (2018). https://doi.org/10.1002/adma.201802591
Z.Y. Cao, L.Z. Feng, G.B. Zhang, J.X. Wang, S. Shen et al., Semiconducting polymer-based nanoparticles with strong absorbance in NIR-II window for in vivo photothermal therapy and photoacoustic imaging. Biomaterials 155, 103–111 (2018). https://doi.org/10.1016/j.biomaterials.2017.11.016
T.T. Sun, J.F. Han, S. Liu, X. Wang, Z.Y. Wang et al., Tailor-made semiconducting polymers for second near-infrared photothermal therapy of orthotopic liver cancer. ACS Nano 13, 7345–7354 (2019). https://doi.org/10.1021/acsnano.9b03910
S.Q. He, J. Song, J.L. Qu, Z. Cheng, Crucial breakthrough of second near-infrared biological window fluorophores: design and synthesis toward multimodal imaging and theranostics. Chem. Soc. Rev. 47, 4258–4728 (2018). https://doi.org/10.1039/c8cs00234g
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R. Vankayala, K.C. Hwang, Near-infrared-light-activatable nanomaterial-mediated phototheranostic nanomedicines: an emerging paradigm for cancer treatment. Adv. Mater. 30, 1706320 (2018). https://doi.org/10.1002/adma.201706320
H.J. Chen, L. Shao, Q. Li, J.F. Wang, Gold nanorods and their plasmonic properties. Chem. Soc. Rev. 42, 2679–2724 (2013). https://doi.org/10.1039/c2cs35367a
Y.N. Xia, W.Y. Li, C.M. Cobley, J.Y. Chen, X.H. Xia et al., Gold nanocages: from synthesis to theranostic applications. Acc. Chem. Res. 44, 914–924 (2011). https://doi.org/10.1021/ar200061q
Y.D. Jin, Multifunctional compact hybrid Au nanoshells: a new generation of nanoplasmonic probes for biosensing, imaging, and controlled release. Acc. Chem. Res. 47, 138–148 (2014). https://doi.org/10.1021/ar400086e
C.M. Cobley, J.Y. Chen, E.C. Cho, L.V. Wang, Y.N. Xia, Gold nanostructures: a class of multifunctional materials for biomedical applications. Chem. Soc. Rev. 40, 44–56 (2011). https://doi.org/10.1039/b821763g
H.J. Chen, L. Shao, T. Ming, Z.H. Sun, C.M. Zhao et al., Understanding the photothermal conversion efficiency of gold nanocrystals. Small 6, 2272–2280 (2010). https://doi.org/10.1002/smll.201001109
Q. Li, X.L. Zhuo, S. Li, Q.F. Ruan, Q.-H. Xu et al., Production of monodisperse gold nanobipyramids with number percentages approaching 100% and evaluation of their plasmonic properties. Adv. Opt. Mater. 3, 801–812 (2015). https://doi.org/10.1002/adom.201400505
X.J. Zhu, W. Feng, J. Chang, Y.-W. Tan, J.C. Li et al., Temperature-feedback upconversion nanocomposite for accurate photothermal therapy at facile temperature. Nat. Commun. 7, 10437 (2016). https://doi.org/10.1038/ncomms10437
Q. Chen, C. Liang, C. Wang, Z. Liu, An imagable and photothermal “Abraxane-like” nanodrug for combination cancer therapy to treat subcutaneous and metastatic breast tumors. Adv. Mater. 27, 903–910 (2015). https://doi.org/10.1002/adma.201404308
Y. Yang, W.J. Zhu, Z.L. Dong, Y. Chao, L. Xu et al., 1D coordination polymer nanofibers for low-temperature photothermal therapy. Adv. Mater. 29, 1703588 (2017). https://doi.org/10.1002/adma.201703588
C. Viallard, B. Larrivée, Tumor angiogenesis and vascular normalization: alternative therapeutic targets. Angiogenesis 20, 409–426 (2017). https://doi.org/10.1007/s10456-017-9562-9
G.M. Tozer, C. Kanthou, B.C. Baguley, Disrupting tumour blood vessels. Nat. Rev. Cancer 5, 423–435 (2005). https://doi.org/10.1038/nrc1628
M.R. Horsman, Angiogenesis and vascular targeting: relevance for hyperthermia. Int. J. Hyperth. 24, 57–65 (2008). https://doi.org/10.1080/02656730701829710
X.-M. Zhu, C.H. Fang, H.L. Jia, Y. Huang, C.H. Cheng et al., Cellular uptake behaviour, photothermal therapy performance, and cytotoxicity of gold nanorods with various coatings. Nanoscale 6, 11462–11472 (2014). https://doi.org/10.1039/c4nr03865g
X.S. Kou, W.H. Ni, C.-K. Tsung, K. Chan, H.-Q. Lin et al., Growth of gold bipyramids with improved yield and their curvature-directed oxidation. Small 3, 2103–2113 (2007). https://doi.org/10.1002/smll.200700379
E.A. Jaffe, Cell biology of endothelial cells. Hum. Pathol. 18, 234–239 (1987). https://doi.org/10.1016/S0046-8177(87)80005-9
E. Porcù, R. Bortolozzi, G. Basso, G. Viola, Recent advances in vascular disrupting agents in cancer therapy. Future Med. Chem. 6, 1485–1498 (2014). https://doi.org/10.4155/fmc.14.104
S.J. Lunt, S. Akerman, S.A. Hill, M. Fisher, V.J. Wright et al., Vascular effects dominate solid tumor response to treatment with combretastatin A-4-phosphate. Int. J. Cancer 129, 1979–1989 (2011). https://doi.org/10.1002/ijc.25848
C. Kanthou, G.M. Tozer, The tumor vascular targeting agent combretastatin A-4-phosphate induces reorganization of the actin cytoskeleton and early membrane blebbing in human endothelial cells. Blood 99, 2060–2069 (2002). https://doi.org/10.1182/blood.v99.6.2060
G. Nagaiah, S.C. Remick, Combretastatin A4 phosphate: a novel vascular disrupting agent. Future Oncol. 6, 1219–1228 (2010). https://doi.org/10.2217/fon.10.90
P.A. Connor, A.J. McQuillan, Phosphate adsorption onto TiO2 from aqueous solutions: an in situ internal reflection infrared spectroscopic study. Langmuir 15, 2916–2921 (1999). https://doi.org/10.1021/la980894p
X.-M. Zhu, J. Yuan, K.C. Leung, S.-F. Lee, K.W. Sham et al., Hollow superparamagnetic iron oxide nanoshells as a hydrophobic anticancer drug carrier: intracelluar pH-dependent drug release and enhanced cytotoxicity. Nanoscale 4, 5744–5754 (2012). https://doi.org/10.1039/c2nr30960b
H.P. Eikesdal, S.T. Bjorkhaug, O. Dahl, Hyperthermia exhibits anti-vascular activity in the s.c. BT4An rat glioma: lack of interaction with the angiogenesis inhibitor batimastat. Int. J. Hyperth. 18, 141–152 (2002). https://doi.org/10.1080/02656730110090712
L.F. Fajardo, S.D. Prionas, J. Kowalski, H.H. Kwan, Hyperthermia inhibits angiogenesis. Radiat. Res. 114, 297–306 (1988). https://doi.org/10.2307/3577226
C. Dumontet, M.A. Jordan, Microtubule-binding agents: a dynamic field of cancer therapeutics. Nat. Rev. Drug Discov. 9, 790–803 (2010). https://doi.org/10.1038/nrd3253
J. Griggs, J.C. Metcalfe, R. Hesketh, Targeting tumour vasculature: the development of combretastatin A4. Lancet Oncol. 2, 82–87 (2001). https://doi.org/10.1016/S1470-2045(00)00224-2
N.M. Dimitrijevic, Z.V. Saponjic, B.M. Rabatic, T. Rajh, Assembly and charge transfer in hybrid TiO2 architectures using biotin–avidin as a connector. J. Am. Chem. Soc. 127, 13441345 (2005). https://doi.org/10.1021/ja0458118
K.T. Thurn, T. Paunesku, A.G. Wu, E.M. Brown, B. Lai et al., Labeling TiO2 nanoparticles with dyes for optical fluorescence microscopy and determination of TiO2–DNA nanoconjugate stability. Small 5, 1318–1325 (2009). https://doi.org/10.1002/smll.200801458
M.G. Li, K.T. Al-Jamal, K. Kostarelos, J. Reineke, Physiologically based pharmacokinetic modeling of nanoparticles. ACS Nano 4, 6303–6317 (2010). https://doi.org/10.1021/nn1018818
M.H. Li, X.T. Sun, N. Zhang, W. Wang, Y. Yang et al., NIR-activated polydopamine-coated carrier-free “nanobomb” for in situ on-demand drug release. Adv. Sci. 5, 1800155 (2018). https://doi.org/10.1002/advs.201800155
M.B. Zheng, C.X. Yue, Y.F. Ma, P. Gong, P.F. Zhao et al., Single-step assembly of DOX/ICG loaded lipid–polymer nanoparticles for highly effective chemo-photothermal combination therapy. ACS Nano 7, 2056–2067 (2013). https://doi.org/10.1021/nn400334y
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