Highly Sensitive MoS2–Indocyanine Green Hybrid for Photoacoustic Imaging of Orthotopic Brain Glioma at Deep Site
Corresponding Author: Liang Song
Nano-Micro Letters,
Vol. 10 No. 3 (2018), Article Number: 48
Abstract
Photoacoustic technology in combination with molecular imaging is a highly effective method for accurately diagnosing brain glioma. For glioma detection at a deeper site, contrast agents with higher photoacoustic imaging sensitivity are needed. Herein, we report a MoS2–ICG hybrid with indocyanine green (ICG) conjugated to the surface of MoS2 nanosheets. The hybrid significantly enhanced photoacoustic imaging sensitivity compared to MoS2 nanosheets. This conjugation results in remarkably high optical absorbance across a broad near-infrared spectrum, redshifting of the ICG absorption peak and photothermal/photoacoustic conversion efficiency enhancement of ICG. A tumor mass of 3.5 mm beneath the mouse scalp was clearly visualized by using MoS2–ICG as a contrast agent for the in vivo photoacoustic imaging of orthotopic glioma, which is nearly twofold deeper than the tumors imaged in our previous report using MoS2 nanosheet. Thus, combined with its good stability and high biocompatibility, the MoS2–ICG hybrid developed in this study has a great potential for high-efficiency tumor molecular imaging in translational medicine.
Highlights:
1 MoS2 nanosheets was covalently conjugated with indocyanine green (ICG) by facile mixing ICG-Sulfo-NHS and MoS2 nanosheets.
2 The 3.5 mm imaging depth demonstrated in this study is one of the deepest among all the glioma photoacoustic imaging research reported so far by using the nanoprobe in the NIR I spectral region.
3 The design and validation of the MoS2–ICG hybrid bring up an effective strategy for synthesizing highly sensitive photoacoustic nanoprobes, i.e., by covalently conjugating optical dyes with transition metal dichalcogenides.
Keywords
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- P. de Robles, K.M. Fiest, A.D. Frolkis, T. Pringsheim, C. Atta, C. St Germaine-Smith, L. Day, D. Lam, N. Jette, The worldwide incidence and prevalence of primary brain tumors: a systematic review and meta-analysis. Neuro-Oncology 17(6), 776–783 (2014). https://doi.org/10.1093/neuonc/nou283
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- X. Ma, M. Shi, Thermal evaporation deposition of few-layer MoS2 films. Nano-Micro Lett. 5(2), 135–139 (2013). https://doi.org/10.1007/BF03353741
- A.H. Loo, A. Bonanni, A. Ambrosi, M. Pumera, Molybdenum disulfide (MoS2) nanoflakes as inherently electroactive labels for DNA hybridization detection. Nanoscale 6, 11971–11975 (2014). https://doi.org/10.1039/c4nr03795b
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- Y. Liu, N. Kang, J. Lv, Z. Zhou, Q. Zhao, L. Ma, Z. Chen, L. Ren, L. Nie, Deep photoacoustic/luminescence/magnetic resonance multimodal imaging in living subjects using high-efficiency upconversion nanocomposites. Adv. Mater. 28(30), 6411–6419 (2016). https://doi.org/10.1002/adma.201506460
- Z. Sheng, D. Hu, M. Zheng, P. Zhao, H. Liu et al., Smart human serum albumin-indocyanine green nanoparticles generated by programmed assembly for dual-modal imaging-guided cancer synergistic phototherapy. ACS Nano 8(12), 12310–12322 (2014). https://doi.org/10.1021/nn5062386
- J. Chen, C. Liu, G. Zeng, Y. You, H. Wang et al., Indocyanine green loaded reduced graphene oxide for in vivo photoacoustic/fluorescence dual-modality tumor imaging. Nanoscale Res. Lett. 11(1), 85 (2016). https://doi.org/10.1186/s11671-016-1288-x
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References
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M. Shabihkhani, D. Telesca, M. Movassaghi, Y.B. Naeini, K.M. Naeini et al., Incidence, survival, pathology, and genetics of adult Latino Americans with glioblastoma. J. Neuro-Oncol. 132(2), 351–358 (2017). https://doi.org/10.1007/s11060-017-2377-0
P.Y. Wen, D.A. Reardon, Neuro-oncology in 2015: progress in glioma diagnosis, classification and treatment. Nat. Rev. Neurol. 12(2), 69–70 (2016). https://doi.org/10.1038/nrneurol.2015.242
R. Ahmed, M.J. Oborski, M. Hwang, F.S. Lieberman, J.M. Mountz, Malignant gliomas: current perspectives in diagnosis, treatment, and early response assessment using advanced quantitative imaging methods. Cancer Manag. Res. 24(6), 149–170 (2014). https://doi.org/10.2147/CMAR.S54726
K. Sagiyama, T. Mashimo, O. Togao, V. Vemireddy, K.J. Hatanpaa et al., In vivo chemical exchange saturation transfer imaging allows early detection of a therapeutic response in glioblastoma. Proc. Natl. Acad. Sci. U.S.A. 111(12), 4542–4547 (2014). https://doi.org/10.1073/pnas.1323855111
L.V. Wang, S. Hu, Photoacoustic tomography: in vivo imaging from organelles to organs. Science 335(6075), 1458–1462 (2012). https://doi.org/10.1126/science.1216210
C. Kim, C. Favazza, L.V. Wang, In vivo photoacoustic tomography of chemicals: high-resolution functional and molecular optical imaging at new depths. Chem. Rev. 110(5), 2756–2782 (2010). https://doi.org/10.1021/cr900266s
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J. Li, J. Rao, K. Pu, Recent progress on semiconducting polymer nanoparticles for molecular imaging and cancer phototherapy. Biomaterials 155, 217–235 (2018). https://doi.org/10.1016/j.biomaterials.2017.11.025
Y. Jiang, P.K. Upputuri, C. Xie, Y. Lyu, L. Zhang, Q. Xiong, M. Pramanik, K. Pu, Broadband absorbing semiconducting polymer nanoparticles for photoacoustic imaging in second near-infrared window. Nano Lett. 17(8), 4964–4969 (2017). https://doi.org/10.1021/acs.nanolett.7b02106
Y. Jiang, K. Pu, Advanced photoacoustic imaging applications of near-infrared absorbing organic nanoparticles. Small 13(30), 1700710 (2017). https://doi.org/10.1002/smll.201700710
Y. Lyu, X. Zhen, Y. Miao, K. Pu, Reaction-based semiconducting polymer nanoprobes for photoacoustic imaging of protein sulfenic acids. ACS Nano 11(1), 358–367 (2016). https://doi.org/10.1021/acsnano.6b05949
K. Pu, A.J. Shuhendler, J.V. Jokerst, J. Mei, S.S. Gambhir, Z. Bao, J. Rao, Semiconducting polymer nanoparticles as photoacoustic molecular imaging probes in living mice. Nat. Nanotechnol. 9(3), 233–239 (2014). https://doi.org/10.1038/nnano.2013.302
G. Li, Y. Chen, L. Zhang, M. Zhang, S. Li, L. Li, T. Wang, C. Wang, Facile approach to synthesize gold nanorod@polyacrylic acid/calcium phosphate yolk–shell nanoparticles for dual-mode imaging and pH/NIR-responsive drug delivery. Nano-Micro Lett. 10(1), 7 (2018). https://doi.org/10.1007/s40820-017-0155-3
G.P. Luke, D. Yeager, S.Y. Emelianov, Biomedical applications of photoacoustic imaging with exogenous contrast agents. Ann. Biomed. Eng. 40(2), 422–437 (2012). https://doi.org/10.1007/s10439-011-0449-4
D. Gao, Z. Sheng, Y. Liu, D. Hu, J. Zhang, X. Zhang, H. Zheng, Z. Yuan, Protein-modified CuS nanotriangles: a potential multimodal nanoplatform for in vivo tumor photoacoustic/magnetic resonance dual-modal imaging. Adv. Healthc. Mater. 6(1), 1601094 (2017). https://doi.org/10.1002/adhm.201601094
J.A. Copland, M. Eghtedari, V.L. Popov, N. Kotov, N. Mamedova, M. Motamedi, A.A. Oraevsky, Bioconjugated gold nanoparticles as a molecular based contrast agent: implications for imaging of deep tumors using optoacoustic tomography. Mol. Imaging Biol. 6(5), 341–349 (2004). https://doi.org/10.1016/j.mibio.2004.06.002
S. Mallidi, G.P. Luke, S. Emelianov, Photoacoustic imaging in cancer detection, diagnosis, and treatment guidance. Trends Biotechnol. 29(5), 213–221 (2011). https://doi.org/10.1016/j.tibtech.2011.01.006
M.F. Kircher, A. De La Zerda, J.V. Jokerst, C.L. Zavaleta, P.J. Kempen et al., A brain tumor molecular imaging strategy using a new triple-modality MRI-photoacoustic-Raman nanoparticle. Nat. Med. 18(5), 829–834 (2012). https://doi.org/10.1038/nm.2721
Q. Fan, K. Cheng, Z. Yang, R. Zhang, M. Yang et al., Perylene-diimide-based nanoparticles as highly efficient photoacoustic agents for deep brain tumor imaging in living mice. Adv. Mater. 27(5), 843–847 (2015). https://doi.org/10.1002/adma.201402972
J. Chen, C. Liu, D. Hu, F. Wang, H. Wu et al., Single-layer MoS2 nanosheets with amplified photoacoustic effect for highly sensitive photoacoustic imaging of orthotopic brain tumors. Adv. Funct. Mater. 26(47), 8715–8725 (2016). https://doi.org/10.1002/adfm.201603758
Y. Luo, Y. Zhang, Y. Zhao, X. Fang, J. Ren et al., Aligned carbon nanotube/molybdenum disulfide hybrids for effective fibrous supercapacitors and lithium ion batteries. J. Mater. Chem. A 3, 17553–17557 (2015). https://doi.org/10.1039/c5ta04703j
X. Ma, M. Shi, Thermal evaporation deposition of few-layer MoS2 films. Nano-Micro Lett. 5(2), 135–139 (2013). https://doi.org/10.1007/BF03353741
A.H. Loo, A. Bonanni, A. Ambrosi, M. Pumera, Molybdenum disulfide (MoS2) nanoflakes as inherently electroactive labels for DNA hybridization detection. Nanoscale 6, 11971–11975 (2014). https://doi.org/10.1039/c4nr03795b
Y.W. Wang, Y.Y. Fu, Q.L. Peng, S.S. Guo, G. Liu, J. Li, H.H. Yang, G.N. Chen, Dye-enhanced graphene oxide for photothermal therapy and photoacoustic imaging. J. Mater. Chem. B 1, 5762–5767 (2013). https://doi.org/10.1039/c3tb20986e
Y. Liu, N. Kang, J. Lv, Z. Zhou, Q. Zhao, L. Ma, Z. Chen, L. Ren, L. Nie, Deep photoacoustic/luminescence/magnetic resonance multimodal imaging in living subjects using high-efficiency upconversion nanocomposites. Adv. Mater. 28(30), 6411–6419 (2016). https://doi.org/10.1002/adma.201506460
Z. Sheng, D. Hu, M. Zheng, P. Zhao, H. Liu et al., Smart human serum albumin-indocyanine green nanoparticles generated by programmed assembly for dual-modal imaging-guided cancer synergistic phototherapy. ACS Nano 8(12), 12310–12322 (2014). https://doi.org/10.1021/nn5062386
J. Chen, C. Liu, G. Zeng, Y. You, H. Wang et al., Indocyanine green loaded reduced graphene oxide for in vivo photoacoustic/fluorescence dual-modality tumor imaging. Nanoscale Res. Lett. 11(1), 85 (2016). https://doi.org/10.1186/s11671-016-1288-x
Z. Sheng, D. Hu, M. Xue, M. He, P. Gong, L. Cai, Indocyanine green nanoparticles for theranostic applications. Nano-Micro Lett. 5(3), 145–150 (2013). https://doi.org/10.1007/BF03353743
X.H. Wang, H.S. Peng, W. Yang, Z.D. Ren, X.M. Liu, Y.A. Liu, Indocyanine green-platinum porphyrins integrated conjugated polymer hybrid nanoparticles for near-infrared-triggered photothermal and two-photon photodynamic therapy. J. Mater. Chem. B 5(9), 1856–1862 (2017). https://doi.org/10.1039/c6tb03215j
G. Guan, S. Zhang, S. Liu, Y. Cai, M. Low et al., Protein induces layer-by-layer exfoliation of transition metal dichalcogenides. J. Am. Chem. Soc. 137(19), 6152–6155 (2015). https://doi.org/10.1021/jacs.5b02780
J.M. Devoisselle, S. Soulie-Begu, H. Maillols, T. Desmettre, S.R. Mordon, Wavelength-resolved measurements of fluorescence lifetime of indocyanine green. J. Biomed. Opt. 16(6), 067010 (2011). https://doi.org/10.1117/1.3593386
J. Kneipp, H. Kneipp, W.L. Rice, K. Kneipp, Optical probes for biological applications based on surface-enhanced Raman scattering from indocyanine green on gold nanoparticles. Anal. Chem. 77(8), 2381–2385 (2005). https://doi.org/10.1021/ac050109v
Y. Li, T. Wen, R. Zhao, X. Liu, T. Ji et al., Localized electric field of plasmonic nanoplatform enhanced photodynamic tumor therapy. ACS Nano 8(11), 11529–11542 (2014). https://doi.org/10.1021/nn5047647
D. Hu, J. Zhang, G. Gao, Z. Sheng, H. Cui, L. Cai, Indocyanine green-loaded polydopamine-reduced graphene oxide nanocomposites with amplifying photoacoustic and photothermal effects for cancer theranostics. Theranostics 6(7), 1043–1052 (2016). https://doi.org/10.7150/thno.14566
Y. Wang, L.V. Wang, Förster resonance energy transfer photoacoustic microscopy. J. Biomed. Opt. 17(8), 0860071 (2012). https://doi.org/10.1117/1.JBO.17.8.086007
Y. Wang, J. Xia, L.V. Wang, Deep-tissue photoacoustic tomography of Förster resonance energy transfer. J. Biomed. Opt. 18(10), 101316 (2013). https://doi.org/10.1117/1.JBO.18.10.101316
F. Cayre, S. Mura, B. Andreiuk, D. Sobot, S. Gouazou, D. Desmaële, A.S. Klymchenko, P. Couvreur, In vivo FRET imaging to predict the risk associated with hepatic accumulation of squalene-based prodrug nanoparticles. Adv. Healthc. Mater. 7(3), 1700830 (2018). https://doi.org/10.1002/adhm.201700830
G. Ku, M. Zhou, S. Song, Q. Huang, J. Hazle, C. Li, Copper sulfide nanoparticles as a new class of photoacoustic contrast agent for deep tissue imaging at 1064 nm. ACS Nano 6(8), 7489–7496 (2012). https://doi.org/10.1021/nn302782y
J.H. Lee, G. Park, G.H. Hong, J. Choi, H.S. Choi, Design considerations for targeted optical contrast agents. Quant. Imaging Med. Surg. 2(4), 266–273 (2012). https://doi.org/10.3978/j.issn.2223-4292.2012.12.04
A. Ray, X. Wang, Y.E.K. Lee, H.J. Hah, G. Kim et al., Targeted blue nanoparticles as photoacoustic contrast agent for brain tumor delineation. Nano Res. 4(11), 1163–1173 (2011). https://doi.org/10.1007/s12274-011-0166-1
W. Lu, M.P. Melancon, C. Xiong, Q. Huang, A. Elliott et al., Effects of photoacoustic imaging and photothermal ablation therapy mediated by targeted hollow gold nanospheres in an orthotopic mouse xenograft model of glioma. Cancer Res. 71(19), 6116–6121 (2011). https://doi.org/10.1158/0008-5472
M.L. Li, J.T. Oh, X. Xie, G. Ku, W. Wang, C. Li, G. Lungu, G. Stoica, L.V. Wang, Simultaneous molecular and hypoxia imaging of brain tumors in vivo using spectroscopic photoacoustic tomography. Proc. IEEE Inst. Electr. Electron. Eng. 96(3), 481–489 (2008). https://doi.org/10.1109/JPROC.2007.913515
W. Li, R. Chen, J. Lv, H. Wang, Y. Liu, Y. Peng, Z. Qian, G. Fu, L. Nie, In vivo photoacoustic imaging of brain injury and rehabilitation by high-efficient near-infrared dye labeled mesenchymal stem cells with enhanced brain barrier permeability. Adv. Sci. 5(2), 1700277 (2018). https://doi.org/10.1002/advs.201700277