Advertisement

Nano Research

, Volume 11, Issue 3, pp 1456–1469 | Cite as

Formation of plasmon quenching dips greatly enhances 1O2 generation in a chlorin e6–gold nanorod coupled system

  • Hui Zhang
  • Haiyun Li
  • Huizhen Fan
  • Jiao Yan
  • Dejing Meng
  • Shuai Hou
  • Yinglu Ji
  • Xiaochun WuEmail author
Research Article

Abstract

Photodynamic therapy (PDT), as a noninvasive therapeutic method, has been actively explored recently for cancer treatment. However, owing to the weak absorption in the optically transparent windows of biological tissues, most commercial photosensitizers (PSs) exhibit low singlet oxygen (1O2) quantum yields when excited by light within this window. Finding the best way to boost 1O2 production for clinical applications using light sources within this window is, thus, a great challenge. Herein, we tackle this problem using plasmon resonance energy transfer (PRET) from plasmonic nanoparticles (NPs) to PSs and demonstrate that the formation of plasmon quenching dips is an effective way to enhance 1O2 generation. The combination of the photosensitizer chlorin e6 (Ce6) and gold nanorods (AuNR) was employed as a model system. We observed a clear quenching dip in the longitudinal surface plasmon resonance (LSPR) band of the AuNRs when the LSPR band overlaps with the Q band of Ce6 and the spacing between Ce6 and the rods is within the acting distance of PRET. Upon irradiation with 660 nm continuous-wave laser light, we obtained a seven-fold enhancement in the 1O2 signal intensity compared with that of a non-PRET sample, as determined using the 1O2 electron spin resonance probe 2,2,6,6-tetramethyl-4-piperidine (TEMP). Furthermore, we demonstrated that the PRET effect is more efficient in enhancing 1O2 yield than the often-employed local field enhancement effect. The effectiveness of PRET is further extended to the in vitro level. Considering the flexibility in manipulating the localized SPR properties of plasmonic nanoparticles/nanostructures, our findings suggest that PRET-based strategies may be a general way to overcome the deficiency of most commercial organic PSs in biological optically transparent windows and promote their applications in clinical tumor treatments.

Keywords

plasmon resonance energy transfer gold nanorods chlorine 6 singlet oxygen photodynamic therapy 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was supported by the Ministry of Science and Technology of China (Nos. 2016YFA0200903 and 2011CB932802), and the National Natural Science Foundation of China (Nos. 91127013 and 21173056).

Supplementary material

12274_2017_1762_MOESM1_ESM.pdf (3 mb)
Formation of plasmon quenching dips greatly enhances 1O2 generation in a chlorin e6–gold nanorod coupled system

References

  1. [1]
    DeRosa, M. C.; Crutchley, R. J. Photosensitized singlet oxygen and its applications. Chem. Rev. 2002, 233–234, 351–371.Google Scholar
  2. [2]
    Dolmans, D. E. J. G. J.; Fukumura, D.; Jain, R. K. Photodynamic therapy for cancer. Nat. Rev. Cancer 2003, 3, 380–387.CrossRefGoogle Scholar
  3. [3]
    Alberti, M. N.; Orfanopoulos, M. Stereoelectronic and solvent effects on the allylic oxyfunctionalization of alkenes with singlet oxygen. Tetrahedron 2006, 62, 10660–10675.CrossRefGoogle Scholar
  4. [4]
    Ogilby, P. R. Singlet oxygen: There is indeed something new under the sun. Chem. Soc. Rev. 2010, 39, 3181–3209.CrossRefGoogle Scholar
  5. [5]
    Schweitzer, C.; Schmidt, R. Physical mechanisms of generation and deactivation of singlet oxygen. Chem. Rev. 2003, 103, 1685–1758.CrossRefGoogle Scholar
  6. [6]
    Kuimova, M. K.; Botchway, S. W.; Parker, A. W.; Balaz, M.; Collins, H. A.; Anderson, H. L.; Suhling, K.; Ogilby, P. R. Imaging intracellular viscosity of a single cell during photoinduced cell death. Nat. Chem. 2009, 1, 69–73.CrossRefGoogle Scholar
  7. [7]
    Castano, A. P.; Mroz, P.; Hamblin, M. R. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer 2006, 6, 535–545.CrossRefGoogle Scholar
  8. [8]
    Allison, R. R.; Sibata, C. H. Oncologic photodynamic therapy photosensitizers: A clinical review. Photodiagn. Photodyn. Ther. 2010, 7, 61–75.CrossRefGoogle Scholar
  9. [9]
    Celli, J. P.; Spring, B. Q.; Rizvi, I.; Evans, C. L.; Samkoe, K. S.; Verma, S.; Pogue, B. W.; Hasan, T. Imaging and photodynamic therapy: Mechanisms, monitoring, and optimization. Chem. Rev. 2010, 110, 2795–2838.CrossRefGoogle Scholar
  10. [10]
    Agostinis, P.; Berg, K.; Cengel, K. A.; Foster, T. H.; Girotti, A. W.; Gollnick, S. O.; Hahn, S. M.; Hamblin, M. R.; Juzeniene, A.; Kessel, D. et al. Photodynamic therapy of cancer: An update. CA-Cancer J. Clin. 2011, 61, 250–281.CrossRefGoogle Scholar
  11. [11]
    Allison, R. R.; Downie, G. H.; Cuenca, R.; Hu, X. H.; Childs, C. J.; Sibata, C. H. Photosensitizers in clinical PDT. Photodiagn. Photodyn. Ther. 2004, 1, 27–42.CrossRefGoogle Scholar
  12. [12]
    Lucky, S. S.; Soo, K. C.; Zhang, Y. Nanoparticles in photodynamic therapy. Chem. Rev. 2015, 115, 1990–2042.CrossRefGoogle Scholar
  13. [13]
    Paszko, E.; Ehrhardt, C.; Senge, M.O.; Kelleher, D. P.; Reynolds, J. V. Nanodrug applications in photodynamic therapy. Photodiagn. Photodyn. Ther. 2011, 8, 14–29.CrossRefGoogle Scholar
  14. [14]
    Bechet, D.; Couleaud, P.; Frochot, C.; Viriot, M. L.; Guillemin, F.; Barberi-Heyob, M. Nanoparticles as vehicles for delivery of photodynamic therapy agents. Trends Biotechnol. 2008, 26, 612–621.CrossRefGoogle Scholar
  15. [15]
    Rana, S.; Bajaj, A.; Mout, R.; Rotello, V. M. Monolayer coated gold nanoparticles for delivery applications. Adv. Drug Delivery Rev. 2012, 64, 200–216.CrossRefGoogle Scholar
  16. [16]
    Gao, L.; Fei, J. B.; Zhao, J.; Li, H.; Cui, Y.; Li, J. B. Hypocrellin-loaded gold nanocages with high two-photon efficiency for photothermal/photodynamic cancer therapy in vitro. ACS Nano. 2012, 6, 8030–8040.CrossRefGoogle Scholar
  17. [17]
    Wang, S. J.; Huang, P.; Nie, L. M.; Xing, R. J.; Liu, D. B.; Wang, Z.; Lin, J.; Chen, S. H.; Niu, G.; Lu, G. M. et al. Single continuous wave laser induced photodynamic/plasmonic photothermal therapy using photosensitizer-functionalized gold nanostars. Adv. Mater. 2013, 25, 3055–3061.CrossRefGoogle Scholar
  18. [18]
    Lin, J.; Wang, S. J.; Huang, P.; Wang, Z.; Chen, S. H.; Niu, G.; Li, W. W.; He, J.; Cui, D. X.; Lu, G. M. et al. Photosensitizer-loaded gold vesicles with strong plasmonic coupling effect for imaging-guided photothermal/photodynamic therapy. ACS Nano 2013, 7, 5320–5329.CrossRefGoogle Scholar
  19. [19]
    Kreyling, W. G.; Abdelmonem, A. M.; Ali, Z.; Alves, F.; Geiser, M.; Haberl, N.; Hartmann, R.; Hirn, S.; de Aberasturi, D. J.; Kantner, K. et al. In vivo integrity of polymer-coated gold nanoparticles. Nat. Nanotechnol. 2015, 10, 619–623.CrossRefGoogle Scholar
  20. [20]
    Kuo, W. S.; Chang, C. N.; Chang, Y. T.; Yang, M. H.; Chien, Y. H.; Chen, S. J.; Yeh, C. S. Gold Nanorods in photodynamic therapy, as hyperthermia agents, and in near-infrared optical imaging. Angew. Chem., Int. Ed. 2010, 49, 2711–2715.CrossRefGoogle Scholar
  21. [21]
    Jang, B.; Park, J. Y.; Tung, C. H.; Kim, I. H.; Choi, Y. Gold nanorod-photosensitizer complex for near-infrared fluorescence imaging and photodynamic/photothermal therapy in vivo. ACS Nano 2011, 5, 1086–1094.CrossRefGoogle Scholar
  22. [22]
    Zhang, Z. J.; Wang, J.; Nie, X.; Wen, T.; Ji, Y. L.; Wu, X. C.; Zhao, Y. L.; Chen, C. Y. Near infrared laser-induced targeted cancer therapy using thermoresponsive polymer encapsulated gold nanorods. J. Am. Chem. Soc. 2014, 136, 7317–7326.CrossRefGoogle Scholar
  23. [23]
    Wang, J.; You, M. X.; Zhu, G. Z.; Shukoor, M. I.; Chen, Z.; Zhao, Z. L.; Altman, M. B.; Yuan, Q.; Zhu, Z.; Chen, Y. et al. Photosensitizer–gold nanorod composite for targeted multimodal therapy. Small 2013, 9, 3678–3684.CrossRefGoogle Scholar
  24. [24]
    Wang, N. N.; Zhao, Z. L.; Lv, Y. F.; Fan, H. H.; Bai, H. R.; Meng, H. M.; Long, Y. Q.; Fu, T.; Zhang, X. B.; Tan, W. H. Gold nanorod–photosensitizer conjugate with extracellular ph-driven tumor targeting ability for photothermal/ photodynamic therapy. Nano Res. 2014, 7, 1291–1301.CrossRefGoogle Scholar
  25. [25]
    Xu, Y. K.; He, R. Y.; Lin, D. D.; Ji, M. B.; Chen, J. Y. Laser beam controlled drug release from Ce6–gold nanorod composites in living cells: A FLIM study. Nanoscale 2015, 7, 2433–2441.CrossRefGoogle Scholar
  26. [26]
    Li, Y. Y.; Wen, T.; Zhao, R. F.; Liu, X. X.; Ji, T. J.; Wang, H.; Shi, X. W.; Shi, J.; Wei, J. Y.; Zhao, Y. L. et al. Localized electric field of plasmonic nanoplatform enhanced photodynamic tumor therapy. ACS Nano 2014, 8, 11529–11542.CrossRefGoogle Scholar
  27. [27]
    Lu, K. D.; He, C. B.; Lin, W. B. Nanoscale metal−organic framework for highly effective photodynamic therapy of resistant head and neck cancer. J. Am. Chem. Soc. 2014, 136, 16712–16715.CrossRefGoogle Scholar
  28. [28]
    Ding, X. S.; Han, B. H. Metallophthalocyanine-Based conjugated microporous polymers as highly efficient photosensitizers for singlet oxygen generation. Angew. Chem., Int. Ed. 2015, 54, 6536–6539.CrossRefGoogle Scholar
  29. [29]
    Lu, K. D.; He, C. B.; Lin, W. B. A chlorin-based nanoscale metal−organic framework for photodynamic therapy of colon cancers. J. Am. Chem. Soc. 2015, 137, 7600–7603.CrossRefGoogle Scholar
  30. [30]
    Park, J.; Jiang, Q.; Feng, D. W.; Mao, L. Q.; Zhou, H. C. Size-controlled synthesis of porphyrinic metal−organic framework and functionalization for targeted photodynamic therapy. J. Am. Chem. Soc. 2016, 138, 3518–3525.CrossRefGoogle Scholar
  31. [31]
    Ni, W. H.; Ambjörnsson, T.; Apell, S. P.; Chen, H. J.; Wang, J. F. Observing plasmonic–molecular resonance coupling on single gold nanorods. Nano Lett. 2010, 10, 77–84.CrossRefGoogle Scholar
  32. [32]
    Chen, H. J.; Ming, T.; Zhao, L.; Wang, F.; Sun, L. D.; Wang, J. F.; Yan, C. H. Plasmon–molecule interactions. Nanotoday 2010, 5, 494–505.CrossRefGoogle Scholar
  33. [33]
    DeLacy, B. G.; Miller, O. D.; Hsu, C. W.; Zander, Z.; Lacey, S.; Yagloski, R.; Fountain, A, W.; Valdes, E.; Anquillare, E.; Soljačić, M. et al. Coherent plasmon–exciton coupling in silver platelet-J-aggregate nanocomposites. Nano Lett. 2015, 15, 2588–2593.CrossRefGoogle Scholar
  34. [34]
    Chen, H. J.; Shao, L.; Woo, K. C.; Wang, J. F.; Lin, H. Q. Plasmonic−molecular resonance coupling: Plasmonic splitting versus energy transfer. J. Phys. Chem. C 2012, 116, 14088–14095.CrossRefGoogle Scholar
  35. [35]
    Choi, Y.; Kang, T.; Lee, L. P. Plasmon resonance energy transfer (PRET)-based molecular imaging of cytochrome c in living cells. Nano Lett. 2009, 9, 85–90.CrossRefGoogle Scholar
  36. [36]
    Qu, W. G.; Deng, B.; Zhong, S. L.; Shi, H. Y.; Wang, S. S.; Xu, A. W. Plasmonic resonance energy transfer-based nanospectroscopy for sensitive and selective detection of 2,4,6-trinitrotoluene (TNT). Chem. Commun. 2011, 47, 1237–1239.CrossRefGoogle Scholar
  37. [37]
    Li, J. T.; Cushing, S. K.; Meng, F. K.; Senty, T. R.; Bristow, A. D.; Wu, N. Q. Plasmon-induced resonance energy transfer for solar energy conversion. Nat. Photonics 2015, 9, 601–607.CrossRefGoogle Scholar
  38. [38]
    Nan, F.; Ding, S. J.; Ma, L.; Cheng, Z. Q.; Zhong, Y. T.; Zhang, Y. F.; Qiu, Y. H.; Li, X. G.; Zhou, L.; Wang, Q. Q. Plasmon resonance energy transfer and plexcitonic solar cell. Nanoscale 2016, 8, 15071–15078.CrossRefGoogle Scholar
  39. [39]
    Cao, Y.; Xie, T.; Qian, R. C.; Long, Y. T. Plasmon resonance energy transfer: Coupling between chromophore molecules and metallic nanoparticles. Small 2016, 13, 1601955.CrossRefGoogle Scholar
  40. [40]
    Hu, Z. J.; Hou, S.; Ji, Y. L.; Wen, T.; Liu, W. Q.; Zhang, H.; Shi, X. W.; Yan, J.; Wu, X. C. Fast characterization of gold nanorods ensemble by correlating its structure with optical extinction spectral features. AIP Adv. 2014, 4, 117137.CrossRefGoogle Scholar
  41. [41]
    Park, K.; Drummy, L. F.; Vaia, R. A. Ag Shell morphology on Au nanorod core: role of Ag precursor complex. J. Mater. Chem. 2011, 21, 15608–15618.CrossRefGoogle Scholar
  42. [42]
    Jadhao, M.; Ahirkar, P.; Kumar, H.; Joshi, R.; Meitei, O. R.; Ghosh, S. K. Surfactant induced aggregation-disaggregation of photodynamic active chlorin e6 and its relevant interaction with DNA alkylating Quinone in a biomimic micellar microenvironment. RSC Adv. 2015, 5, 81449–81460.CrossRefGoogle Scholar
  43. [43]
    Sen, T.; Patra, A. Resonance energy transfer from Rhodamine 6G to gold nanoparticles by steady-state and time-resolved spectroscopy. J. Phys. Chem. C 2008, 112, 3216–3222.CrossRefGoogle Scholar
  44. [44]
    Singh, M. P.; Strouse, G. F. Involvement of the LSPR spectral overlap for energy transfer between a dye and Au nanoparticle. J. Am. Chem. Soc. 2010, 132, 9383–9391.CrossRefGoogle Scholar
  45. [45]
    Pacioni, N. L.; González-Béjar, M; Alarcón, E.; McGilvray, K. L.; Scaiano, J. C. Surface Plasmons control the dynamics of excited triplet states in the presence of gold nanoparticles. J. Am. Chem. Soc. 2010, 132, 6298–6299.CrossRefGoogle Scholar
  46. [46]
    Gao, M. X.; Zou, H. Y.; Gao, P. F.; Liu, Y.; Li, N.; Li, Y. F.; Huang, C. Z. Insight into a reversible energy transfer system. Nanoscale 2016, 8, 16236–16242.CrossRefGoogle Scholar
  47. [47]
    Planas, O.; Macia, N.; Agut, M.; Nonell, S.; Heyne, B. Distance-dependent plasmon-enhanced singlet oxygen production and emission for bacterial inactivation. J. Am. Chem. Soc. 2016, 138, 2762–2768.CrossRefGoogle Scholar
  48. [48]
    Liu, G. L.; Long, Y. T.; Choi, Y.; Kang, T.; Lee, L. P. Quantized Plasmon quenching dips nanospectroscopy via Plasmon resonance energy transfer. Nat. Methods 2007, 4, 1015–1017.CrossRefGoogle Scholar
  49. [49]
    Wen, T.; Zhang, H.; Chong, Y.; Wamer, W. G.; Yin, J. J.; Wu, X. C. Probing hydroxyl radical generation from H2O2 upon Plasmon excitation of gold nanorods using electron spin resonance: Molecular oxygen-mediated activation. Nano Res. 2016, 9, 1663–1673.CrossRefGoogle Scholar

Copyright information

© Tsinghua University Press and Springer-Verlag GmbH Germany 2018

Authors and Affiliations

  • Hui Zhang
    • 1
    • 2
  • Haiyun Li
    • 1
    • 2
  • Huizhen Fan
    • 1
    • 2
  • Jiao Yan
    • 1
    • 2
  • Dejing Meng
    • 1
    • 2
  • Shuai Hou
    • 1
  • Yinglu Ji
    • 1
  • Xiaochun Wu
    • 1
    Email author
  1. 1.CAS Key Laboratory of Standardization and Measurement for Nanotechnology, CAS Center for Excellence in NanoscienceNational Center for Nanoscience and TechnologyBeijingChina
  2. 2.University of the Chinese Academy of SciencesBeijingChina

Personalised recommendations