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Nano Research 2018, 11(3): 1456-1469 https://doi.org/10.1007/s12274-017-1762-5
Research Article | Issue | Published: 02 February 2018

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

Show Author's Information Hui Zhang1,2,  Haiyun Li1,2,  Huizhen Fan1,2,  Jiao Yan1,2,  Dejing Meng1,2,  Shuai Hou1,  Yinglu Ji1,  Xiaochun Wu1( )
CAS Key Laboratory of Standardization and Measurement for NanotechnologyCAS Center for Excellence in NanoscienceNational Center for Nanoscience and TechnologyBeijing100190China
University of the Chinese Academy of SciencesBeijing100190China
Keywords:
plasmon resonance energy transfer, gold nanorods, chlorine 6, singlet oxygen, photodynamic therapy
Cite this article:
Zhang H, Li H, Fan H, et al. Formation of plasmon quenching dips greatly enhances 1O2 generation in a chlorin e6–gold nanorod coupled system. Nano Research, 2018, 11(3): 1456-1469. https://doi.org/10.1007/s12274-017-1762-5
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Abstract Full text Electronic supplementary material About this article

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.


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Electronic supplementary material
About this article

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

Show Author's information Hui Zhang1,2, Haiyun Li1,2, Huizhen Fan1,2, Jiao Yan1,2, Dejing Meng1,2, Shuai Hou1, Yinglu Ji1, Xiaochun Wu1( )
CAS Key Laboratory of Standardization and Measurement for NanotechnologyCAS Center for Excellence in NanoscienceNational Center for Nanoscience and TechnologyBeijing100190China
University of the Chinese Academy of SciencesBeijing100190China

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

References(49)

1

DeRosa, M. C.; Crutchley, R. J. Photosensitized singlet oxygen and its applications. Chem. Rev. 2002, 233–234, 351–371.
DOI Google Scholar
2

Dolmans, D. E. J. G. J.; Fukumura, D.; Jain, R. K. Photodynamic therapy for cancer. Nat. Rev. Cancer 2003, 3, 380–387.
DOI Google Scholar
3

Alberti, M. N.; Orfanopoulos, M. Stereoelectronic and solvent effects on the allylic oxyfunctionalization of alkenes with singlet oxygen. Tetrahedron 2006, 62, 10660–10675.
DOI Google Scholar
4

Ogilby, P. R. Singlet oxygen: There is indeed something new under the sun. Chem. Soc. Rev. 2010, 39, 3181–3209.
DOI Google Scholar
5

Schweitzer, C.; Schmidt, R. Physical mechanisms of generation and deactivation of singlet oxygen. Chem. Rev. 2003, 103, 1685–1758.
DOI Google Scholar
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.
DOI Google Scholar
7

Castano, A. P.; Mroz, P.; Hamblin, M. R. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer 2006, 6, 535–545.
DOI Google Scholar
8

Allison, R. R.; Sibata, C. H. Oncologic photodynamic therapy photosensitizers: A clinical review. Photodiagn. Photodyn. Ther. 2010, 7, 61–75.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
12

Lucky, S. S.; Soo, K. C.; Zhang, Y. Nanoparticles in photodynamic therapy. Chem. Rev. 2015, 115, 1990–2042.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
31

Ni, W. H.; Ambj?rnsson, 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.
DOI Google Scholar
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.
DOI Google Scholar
33

DeLacy, B. G.; Miller, O. D.; Hsu, C. W.; Zander, Z.; Lacey, S.; Yagloski, R.; Fountain, A, W.; Valdes, E.; Anquillare, E.; Solja?i?, M. et al. Coherent plasmon–exciton coupling in silver platelet-J-aggregate nanocomposites. Nano Lett. 2015, 15, 2588–2593.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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.
DOI Google Scholar
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Publication history
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Acknowledgements

Publication history

Received: 18 April 2017
Revised: 06 July 2017
Accepted: 11 July 2017
Published: 02 February 2018
Issue date: March 2018

Copyright

© Tsinghua University Press and Springer-Verlag GmbH Germany 2017

Acknowledgements

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).

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