Issue

Vol. 10 No. 3 (2018)

Highly Sensitive MoS2–Indocyanine Green Hybrid for Photoacoustic Imaging of Orthotopic Brain Glioma at Deep Site

https://doi.org/10.1007/s40820-018-0202-8
Chengbo Liu
Research Laboratory for Biomedical Optics and Molecular Imaging, Shenzhen Key Laboratory for Molecular Imaging, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China
Jingqin Chen
Research Laboratory for Biomedical Optics and Molecular Imaging, Shenzhen Key Laboratory for Molecular Imaging, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China
Ying Zhu
Research Laboratory for Biomedical Optics and Molecular Imaging, Shenzhen Key Laboratory for Molecular Imaging, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China
Xiaojing Gong
Research Laboratory for Biomedical Optics and Molecular Imaging, Shenzhen Key Laboratory for Molecular Imaging, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China
Rongqin Zheng
Department of Medical Ultrasound, The Third Affiliated Hospital of Sun Yat-Sen University, Guangzhou 510630, People’s Republic of China
Ningbo Chen
Research Laboratory for Biomedical Optics and Molecular Imaging, Shenzhen Key Laboratory for Molecular Imaging, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China
Dong Chen
Research Laboratory for Biomedical Optics and Molecular Imaging, Shenzhen Key Laboratory for Molecular Imaging, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China
Huixiang Yan
Research Laboratory for Biomedical Optics and Molecular Imaging, Shenzhen Key Laboratory for Molecular Imaging, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China
Peng Zhang
Translational Medicine R&D Center, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China
Hairong Zheng
Paul C. Lauterbur Research Center for Biomedical Imaging, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China
Zonghai Sheng
Paul C. Lauterbur Research Center for Biomedical Imaging, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China
Liang Song
Research Laboratory for Biomedical Optics and Molecular Imaging, Shenzhen Key Laboratory for Molecular Imaging, Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, People’s Republic of China

Corresponding Author: Liang Song

liang.song@siat.ac.cn

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

MoS2–ICG hybrid Orthotopic brain glioma Photoacoustic imaging Molecular imaging
Liu, Chengbo, Jingqin Chen, Ying Zhu, Xiaojing Gong, Rongqin Zheng, Ningbo Chen, Dong Chen, Huixiang Yan, Peng Zhang, Hairong Zheng, Zonghai Sheng, and Liang Song. 2018. “Highly Sensitive MoS2–Indocyanine Green Hybrid for Photoacoustic Imaging of Orthotopic Brain Glioma at Deep Site”. Nano-Micro Letters 10 (3):48. https://doi.org/10.1007/s40820-018-0202-8.
Download Citation
Endnote/Zotero/Mendeley (RIS)
BibTeX
References
  1. 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
  2. X. Jiang, H. Xin, Q. Ren, J. Gu, L. Zhu et al., Nanoparticles of 2-deoxy-d-glucose functionalized poly (ethylene glycol)-co-poly (trimethylene carbonate) for dual-targeted drug delivery in glioma treatment. Biomaterials 35(1), 518–529 (2014). https://doi.org/10.1016/j.biomaterials.2013.09.094
  3. 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
  4. 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
  5. 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
  6. 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
  7. 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
  8. 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
  9. X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, L.V. Wang, Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain. Nat. Biotechnol. 21(7), 803–806 (2003). https://doi.org/10.1038/nbt839
  10. 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
  11. 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
  12. 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
  13. 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
  14. 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
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. 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
  32. 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
  33. 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
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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
  40. 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
  41. 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
  42. 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
  43. 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
  44. 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
  45. 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
Read More
Author biographies are not available.
Download this PDF file
PDF SUPPLEMENTARY MATERIAL
Statistic
Read Counter : 4353 Download : 3307

Most read articles by the same author(s)

1 2 > >>