Skip to main content
SpringerLink
Log in

Core-satellite metal-organic framework@upconversion nanoparticle superstructures via electrostatic self-assembly for efficient photodynamic theranostics

  • Research Article
  • Published:
Nano Research Aims and scope Submit manuscript

Abstract

The nanoplatforms based on upconversion nanoparticles (UCNPs) have shown great promise in amplified photodynamic therapy (PDT) triggered by near-infrared (NIR) light. However, their practical in vivo applications are hindered by the overheating effect of 980 nm excitation and low utilization of upconversion luminescence (UCL) by photosensitizers. To solve these defects, core-satellite metal-organic framework@UCNP superstructures, composed of a single metal-organic framework (MOF) NP as the core and Nd3+-sensitized UCNPs as the satellites, are designed and synthesized via a facile electrostatic self-assembly strategy. The superstructures realize a high co-loading capacity of chlorin e6 (Ce6) and rose bengal (RB) benefitted from the highly porous nature of MOF NPs, showing a strong spectral overlap between maximum absorption of photosensitizers and emission of UCNPs. The in vitro and in vivo experiments demonstrate that the dual-photosensitizer superstructures have trimodal (magnetic resonance (MR)/UCL/fluorescence (FL)) imaging functions and excellent antitumor effectiveness of PDT at 808 nm NIR light excitation, avoiding the laser irradiation-induced overheating issue. This study provides new insights for the development of highly efficient PDT nanodrugs toward precision theranostics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Lovell, J. F.; Liu, T. W. B.; Chen, J.; Zheng, G. Activatable photosensitizers for imaging and therapy. Chem. Rev. 2010, 110, 2839–2857.

    CAS  Google Scholar 

  2. Ye, S. Y.; Rao, J. M.; Qiu, S. H.; Zhao, J. L.; He, H.; Yan, Z. L.; Yang, T.; Deng, Y. B.; Ke, H. T.; Yang, H. et al. Rational design of conjugated photosensitizers with controllable photoconversion for dually cooperative phototherapy. Adv. Mater. 2018, 30, 1801216.

    Google Scholar 

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

    CAS  Google Scholar 

  4. Chen, W. S.; Ouyang, J.; Liu, H.; Chen, M.; Zeng, K.; Sheng, J. P.; Liu, Z. J.; Han, Y. J.; Wang, L. Q.; Li, J. et al. Black phosphorus nanosheet-based drug delivery system for synergistic photodynamic/photothermal/chemotherapy of cancer. Adv. Mater. 2017, 29, 1603864.

    Google Scholar 

  5. Fan, W. P.; Huang, P.; Chen, X. Y. Overcoming the Achilles’ heel of photodynamic therapy. Chem. Soc. Rev. 2016, 45, 6488–6519.

    CAS  Google Scholar 

  6. Deng, K. R.; Li, C. X.; Huang, S. S.; Xing, B. G.; Jin, D. Y.; Zeng, Q. G.; Hou, Z. Y.; Lin, J. Recent progress in near infrared light triggered photodynamic therapy. Small 2017, 13, 1702299.

    Google Scholar 

  7. Wang, C.; Cheng, L.; Liu, Z. Upconversion nanoparticles for photodynamic therapy and other cancer therapeutics. Theranostics 2013, 3, 317–330.

    Google Scholar 

  8. Li, F. Y.; Du, Y.; Liu, J. N.; Sun, H.; Wang, J.; Li, R. Q.; Kim, D.; Hyeon, T.; Ling, D. S. Responsive assembly of upconversion nanoparticles for pH-activated and near-infrared-triggered photodynamic therapy of deep tumors. Adv. Mater. 2018, 30, 1802808.

    Google Scholar 

  9. Liu, Y. Y.; Zhang, J. W.; Zuo, C. J.; Zhang, Z.; Ni, D. L.; Zhang, C.; Wang, J.; Zhang, H.; Yao, Z. W.; Bu, W. B. Upconversion nanophotosensitizer targeting into mitochondria for cancer apoptosis induction and cyt c fluorescence monitoring. Nano Res. 2016, 9, 3257–3266.

    CAS  Google Scholar 

  10. Fan, W. P.; Bu, W. B.; Shi, J. L. On the latest three-stage development of nanomedicines based on upconversion nanoparticles. Adv. Mater. 2016, 28, 3987–4011.

    CAS  Google Scholar 

  11. Yan, S. Q.; Zeng, X. M.; Tang, Y. A.; Liu, B. F.; Wang, Y.; Liu, X. G. Activating antitumor immunity and antimetastatic effect through polydopamine-encapsulated core-shell upconversion nanoparticles. Adv. Mater. 2019, 31, 1905825.

    CAS  Google Scholar 

  12. Zhou, B.; Shi, B. Y.; Jin, D. Y.; Liu, X. G. Controlling upconversion nanocrystals for emerging applications. Nat. Nanotechnol. 2015, 70, 924–936.

    Google Scholar 

  13. Bai, G. X.; Tsang, M. K.; Hao, J. H. Luminescent ions in advanced composite materials for multifunctional applications. Adv. Funct. Mater. 2016, 26, 6330–6350.

    CAS  Google Scholar 

  14. Zhang, D. D.; Wen, L. W.; Huang, R.; Wang, H. H.; Hu, X. L.; Xing, D. Mitochondrial specific photodynamic therapy by rare-earth nanoparticles mediated near-infrared graphene quantum dots. Biomaterials 2018, 153, 14–26.

    CAS  Google Scholar 

  15. He, S.; Johnson, N. J. J.; Huu, V. A. N.; Huang, Y. R.; Almutairi, A. Leveraging spectral matching between photosensitizers and upconversion nanoparticles for 808 nm-activated photodynamic therapy. Chem. Mater. 2018, 30, 3991–4000.

    CAS  Google Scholar 

  16. Chen, Y.; Ren, J. L.; Tian, D.; Li, Y. C.; Jiang, H.; Zhu, J. T. Polymer-upconverting nanoparticle hybrid micelles for enhanced synergistic chemo-photodynamic therapy: Effects of emission-absorption spectral match. Biomacromolecules 2019, 20, 4044–4052.

    CAS  Google Scholar 

  17. Wang, Y. F.; Liu, G. Y.; Sun, L. D.; Xiao, J. W.; Zhou, J. C.; Yan, C. H. Nd3+-sensitized upconversion nanophosphors: Efficient in vivo bioimaging probes with minimized heating effect. ACS Nano 2013, 7, 7200–7206.

    CAS  Google Scholar 

  18. Liu, B.; Chen, Y. Y.; Li, C. X.; He, F.; Hou, Z. Y.; Huang, S. S.; Zhu, H. M.; Chen, X. Y.; Lin, J. Poly(acrylic acid) modification of Nd3+-sensitized upconversion nanophosphors for highly efficient UCL imaging and pH-responsive drug delivery. Adv. Funct. Mater. 2015, 25, 4717–4729.

    CAS  Google Scholar 

  19. Hou, Z. Y.; Deng, K. R.; Wang, M. F.; Liu, Y. H.; Chang, M. Y.; Huang, S. S.; Li, C. X.; Wei, Y.; Cheng, Z. Y.; Han, G. et al. Hydrogenated titanium oxide decorated upconversion nanoparticles: Facile laser modified synthesis and 808 nm near-infrared light triggered phototherapy. Chem. Mater. 2019, 31, 774–784.

    CAS  Google Scholar 

  20. Ai, X. Z.; Ho, C. J. H.; Aw, J.; Attia, A. B. E.; Mu, J.; Wang, Y.; Wang, X. Y.; Wang, Y.; Liu, X. G.; Chen, H. B. et al. In vivo covalent cross-linking of photon-converted rare-earth nanostructures for tumour localization and theranostics. Nat. Commun. 2016, 7, 10432.

    CAS  Google Scholar 

  21. Li, Y.; Tang, J. L.; Pan, D. X.; Sun, L. D.; Chen, C. Y.; Liu, Y.; Wang, Y. F.; Shi, S.; Yan, C. H. A versatile imaging and therapeutic platform based on dual-band luminescent lanthanide nanoparticles toward tumor metastasis inhibition. ACS Nano 2016, 70, 2766–2773.

    Google Scholar 

  22. Liu, B.; Li, C. X.; Yang, P. P.; Hou, Z. Y.; Lin, J. 808-nm-light-excited lanthanide-doped nanoparticles: Rational design, luminescence control and theranostic applications. Adv. Mater. 2017, 29, 1605434.

    Google Scholar 

  23. Lu, S.; Tu, D. T.; Hu, P.; Xu, J.; Li, R. F.; Wang, M.; Chen, Z.; Huang, M. D.; Chen, X. Y. Multifunctional nano-bioprobes based on rattle-structured upconverting luminescent nanoparticles. Angew. Chem., Int. Ed. 2015, 54, 7915–7919.

    CAS  Google Scholar 

  24. Idris, N. M.; Gnanasammandhan, M. K.; Zhang, J.; Ho, P. C.; Mahendran, R.; Zhang, Y. In vivo photodynamic therapy using upconversion nanoparticles as remote-controlled nanotransducers. Nat. Med. 2012, 78, 1580–1585.

    Google Scholar 

  25. Liang, L. E.; Care, A.; Zhang, R.; Lu, Y. Q.; Packer, N. H.; Sunna, A.; Qian, Y.; Zvyagin, A. V. Facile assembly of functional upconversion nanoparticles for targeted cancer imaging and photodynamic therapy. ACS Appl. Mater. Interfaces 2016, 8, 11945–11953.

    CAS  Google Scholar 

  26. Xu, J. T.; Yang, P. P.; Sun, M. D.; Bi, H. T.; Liu, B.; Yang, D.; Gai, S. L.; He, F.; Lin, J. Highly emissive dye-sensitized upconversion nanostructure for dual-photosensitizer photodynamic therapy and bioimaging. ACS Nano 2017, 77, 4133–4144.

    Google Scholar 

  27. Wang, S. Z.; McGuirk, C. M.; d’Aquino, A.; Mason, J. A.; Mirkin, C. A. Metal-organic framework nanoparticles. Adv. Mater. 2018, 30, 1800202.

    Google Scholar 

  28. Horcajada, P.; Chalati, T.; Serre, C.; Gillet, B.; Sebrie, C.; Baati, T.; Eubank, J. F.; Heurtaux, D.; Clayette, P.; Kreuz, C. et al. Porous metal-organic-framework nanoscale carriers as a potential platform for drug delivery and imaging. Nat. Mater. 2010, 9, 172–178.

    CAS  Google Scholar 

  29. Zhang, L. Y.; Liu, C.; Gao, Y.; Li, Z. H.; Xing, J.; Ren, W. Z.; Zhang, L. L.; Li, A. G.; Lu, G. M.; Wu, A. G. et al. ZD2-engineered gold nanostar@metal-organic framework nanoprobes for T1-weighted magnetic resonance imaging and photothermal therapy specifically toward triple-negative breast cancer. Adv. Healthcare Mater. 2018, 7, 1801144.

    Google Scholar 

  30. He, Z. M.; Huang, X. L.; Wang, C.; Li, X. L.; Liu, Y. J.; Zhou, Z. J.; Wang, S.; Zhang, F. W.; Wang, Z. T.; Jacobson, O. et al. A catalase-like metal-organic framework nanohybrid for O2-evolving synergistic chemoradiotherapy. Angew. Chem., Int. Ed. 2019, 58, 8752–8756.

    CAS  Google Scholar 

  31. Neufeld, M. J.; DuRoss, A. N.; Landry, M. R.; Winter, H.; Goforth, A. M.; Sun, C. Co-delivery of PARP and PI3K inhibitors by nanoscale metal-organic frameworks for enhanced tumor chemoradiation. Nano Res. 2019, 12, 3003–3017.

    CAS  Google Scholar 

  32. Lu, K. D.; Aung, T.; Guo, N. N.; Weichselbaum, R.; Lin, W. B. Nanoscale metal-organic frameworks for therapeutic, imaging, and sensing applications. Adv. Mater. 2018, 30, 1707634.

    Google Scholar 

  33. Zhang, Z.; Sang, W.; Xie, L. S.; Dai, Y. L. Metal-organic frameworks for multimodal bioimaging and synergistic cancer chemotherapy. Coordin. Chem. Rev. 2019, 399, 213022.

    CAS  Google Scholar 

  34. Sun, C. Y.; Qin, C.; Wang, C. G.; Su, Z. M.; Wang, S.; Wang, X. L.; Yang, G. S.; Shao, K. Z.; Lan, Y. Q.; Wang, E. B. Chiral nanoporous metal-organic frameworks with high porosity as materials for drug delivery. Adv. Mater. 2011, 23, 5629–5632.

    CAS  Google Scholar 

  35. Cheng, H.; Zhu, J. Y.; Li, S. Y.; Zeng, J. Y.; Lei, Q.; Chen, K. W.; Zhang, C.; Zhang, X. Z. An O2 Self-sufficient biomimetic nanoplatform for highly specific and efficient photodynamic therapy. Adv. Funct. Mater. 2016, 26, 7847–7860.

    CAS  Google Scholar 

  36. 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.

    CAS  Google Scholar 

  37. 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.

    CAS  Google Scholar 

  38. Min, H.; Wang, J.; Qi, Y. Q.; Zhang, Y. L.; Han, X. X.; Xu, Y.; Xu, J. C.; Li, Y.; Chen, L.; Cheng, K. M. et al. Biomimetic metal-organic framework nanoparticles for cooperative combination of antiangiogenesis and photodynamic therapy for enhanced efficacy. Adv. Mater. 2019, 31, 1808200.

    Google Scholar 

  39. Ni, K. Y.; Luo, T. K.; Lan, G. X.; Culbert, A.; Song, Y.; Wu, T.; Jiang, X. M.; Lin, W. B. A nanoscale metal-organic framework to mediate photodynamic therapy and deliver CpG oligodeoxynucleotides to enhance antigen presentation and cancer immunotherapy. Angew. Chem. 2020, 132, 1124–1128.

    Google Scholar 

  40. Zhu, W. J.; Yang, Y.; Jin, Q. T.; Chao, Y.; Tian, L. L.; Liu, J. J.; Dong, Z. L.; Liu, Z. Two-dimensional metal-organic-framework as a unique theranostic nano-platform for nuclear imaging and chemophotodynamic cancer therapy. Nano Res. 2019, 12, 1307–1312.

    CAS  Google Scholar 

  41. He, L. C.; Brasino, M.; Mao, C. C.; Cho, S.; Park, W.; Goodwin, A. P.; Cha, J. N. DNA-assembled core-satellite upconverting-metal-organic framework nanoparticle superstructures for efficient photodynamic therapy. Small 2017, 13, 1700504.

    Google Scholar 

  42. Li, Y. F.; Di, Z. H.; Gao, J. H.; Cheng, P.; Di, C. Z.; Zhang, G.; Liu, B.; Shi, X. H.; Sun, L. D.; Li, L. et al. Heterodimers made of upconversion nanoparticles and metal-organic frameworks. J. Am. Chem. Soc. 2017, 139, 13804–13810.

    CAS  Google Scholar 

  43. Shao, Y. L.; Liu, B.; Di, Z. H.; Zhang, G.; Sun, L. D.; Li, L. L.; Yan, C. H. Engineering of upconverted metal-organic frameworks for near-infrared light-triggered combinational photodynamic/chemo-/immunotherapy against hypoxic tumors. J. Am. Chem. Soc. 2020, 142, 3939–3946.

    CAS  Google Scholar 

  44. Liu, C.; Liu, B.; Zhao, J.; Di, Z. H.; Chen, D. Q.; Gu, Z. J.; Li, L. L.; Zhao, Y. L. Nd3+-sensitized upconversion metal-organic frameworks for mitochondria-targeted amplified photodynamic therapy. Angew. Chem., Int. Ed. 2020, 59, 2634–2638.

    CAS  Google Scholar 

  45. Lv, R. C.; Yang, D.; Yang, P. P.; Xu, J. T.; He, F.; Gai, S. L.; Li, C. X.; Dai, Y. L.; Yang, G. X.; Lin, J. Integration of upconversion nanoparticles and ultrathin black phosphorus for efficient photodynamic theranostics under 808 nm near-infrared light irradiation. Chem. Mater. 2016, 28, 4724–4734.

    CAS  Google Scholar 

  46. Yuan, Z.; Zhang, L.; Li, S. Z.; Zhang, W. N.; Lu, M.; Pan, Y.; Xie, X. J.; Huang, L.; Huang, W. Paving metal-organic frameworks with upconversion nanoparticles via self-assembly. J. Am. Chem. Soc. 2018, 140, 15507–15515.

    CAS  Google Scholar 

  47. Liu, J. N.; Bu, W. B.; Pan, L. M.; Zhang, S. J.; Chen, F.; Zhou, L. P.; Zhao, K. L.; Peng, W. J.; Shi, J. L. Simultaneous nuclear imaging and intranuclear drug delivery by nuclear-targeted multifunctional upconversion nanoprobes. Biomaterials 2012, 33, 7282–7290.

    CAS  Google Scholar 

  48. He, C. B.; Lu, K. D.; Lin, W. B. Nanoscale metal-organic frameworks for real-time intracellular pH sensing in live cells. J. Am. Chem. Soc. 2014, 136, 12253–12256.

    CAS  Google Scholar 

  49. Zeng, L. Y.; Pan, Y. W.; Zou, R. F.; Zhang, J. C.; Tian, Y.; Teng, Z. G.; Wang, S. J.; Ren, W. Z.; Xiao, X. S.; Zhang, J. C. et al. 808 nm-excited upconversion nanoprobes with low heating effect for targeted magnetic resonance imaging and high-efficacy photodynamic therapy in HER2-overexpressed breast cancer. Biomaterials 2016, 103, 116–127.

    CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by National Natural Science Foundation of China (NSFC, Nos. 21601140 and 21871214), the Fundamental Research Funds for the Central Universities, and Open Research Fund of State Key Laboratory of Bioelectronics.

Author information

Authors and Affiliations

  1. Key Laboratory of Combinatorial Biosynthesis and Drug Discovery, Hubei Province Engineering and Technology Research Center for Fluorinated Pharmaceuticals, School of Pharmaceutical Sciences, Wuhan University, Wuhan, 430071, China

    Zhike Li, Xi Qiao, Guihua He, Xin Sun, Danhua Feng, Liefeng Hu & Jian Tian

  2. State Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering, Southeast University, Nanjing, 210096, China

    Hua Xu

  3. Ministry-of-Education Key Laboratory for the Synthesis and Application of Organic Functional Molecules, Hubei Collaborative Innovation Center for Advanced Organic Chemical Materials, College of Chemistry and Chemical Engineering, Hubei University, Wuhan, 430062, China

    Hai-Bing Xu

  4. Department of Chemistry, University of North Texas, Denton, TX, 76201, USA

    Shengqian Ma

Authors
  1. Zhike Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xi Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guihua He
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Danhua Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Liefeng Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hua Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hai-Bing Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shengqian Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jian Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shengqian Ma or Jian Tian.

Electronic Supplementary Material

12274_2020_3025_MOESM1_ESM.pdf

Core-satellite metal-organic framework@upconversion nanoparticle superstructures via electrostatic self-assembly for efficient photodynamic theranostics

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Z., Qiao, X., He, G. et al. Core-satellite metal-organic framework@upconversion nanoparticle superstructures via electrostatic self-assembly for efficient photodynamic theranostics. Nano Res. 13, 3377–3386 (2020). https://doi.org/10.1007/s12274-020-3025-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12274-020-3025-0

Keywords

Search

Navigation