Skip to main content

Advertisement

Log in

Near-Infrared Light-Sensitive Liposomes for the Enhanced Photothermal Tumor Treatment by the Combination with Chemotherapy

  • Research Paper
  • Published:
Pharmaceutical Research Aims and scope Submit manuscript

Abstract

Purpose

To develop a near-infrared (NIR) light-sensitive liposome, which contains hollow gold nanospheres (HAuNS) and doxorubicin (DOX), and evaluate their potential utility for enhancing antitumor activity and controlling drug release.

Methods

The liposomes (DOX&HAuNS-TSL) were designed based on a thermal sensitive liposome (TSL) formulation, and hydrophobically modified HAuNS were attached onto the membrane of the liposomes. The behavior of DOX release from the liposomes was investigated by the dialysis, diffusion in agarose gel and cellular uptake of the drug. The biodistribution of DOX&HAuNS-TSL was assessed by i.v. injection in tumor-bearing nude mice. Antitumor efficacy was evaluated both histologically using excised tissue and intuitively by measuring the tumor size and weight.

Results

Rapid and repetitive DOX release from the liposomes (DOX&HAuNS-TSL), could be readily achieved upon NIR laser irradiation. The treatment of tumor cells with DOX&HAuNS-TSL followed by NIR laser irradiation showed significantly greater cytotoxicity than the treatment with DOX&HAuNS-TSL alone, DOX-TSL alone (chemotherapy alone) and HAuNS-TSL plus NIR laser irradiation (Photothermal ablation, PTA, alone). In vivo antitumor study indicated that the combination of simultaneous photothermal and chemotherapeutic effect mediated by DOX&HAuNS-TSL plus NIR laser presented a significantly higher antitumor efficacy than the PTA alone mediated by HAuNS-TSL plus NIR laser irradiation.

Conclusions

Our study could be as the valuable reference and direction for the clinical application of PTA in tumor therapy.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Loo C, Lowery A, Halas N, West J, Drezek R. Immunotargeted nanoshells for integrated cancer imaging and therapy. Nano Lett. 2005;5:709–11.

    Article  CAS  PubMed  Google Scholar 

  2. Schwartz JA, Shetty AM, Price RE, Stafford RJ, Wang JC, Uthamanthil RK, et al. Feasibility study of particle-assisted laser ablation of brain tumors in orthotopic canine model. Cancer Res. 2009;69:1659–67.

    Article  CAS  PubMed  Google Scholar 

  3. von Maltzahn G, Park J-H, Agrawal A, Bandaru NK, Das SK, Sailor MJ, et al. Computationally guided photothermal tumor therapy using long-circulating gold nanorod antennas. Cancer Res. 2009;69:3892–900.

    Article  PubMed Central  Google Scholar 

  4. Chen J, Glaus C, Laforest R, Zhang Q, Yang M, Gidding M, et al. Gold nanocages as photothermal transducers for cancer treatment. Small. 2010;6:811–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Abdulla-Al-Mamun M, Kusumoto Y, Mihata A, Islam MS, Ahmmad B. Plasmon-induced photothermal cell-killing effect of gold colloidal nanoparticles on epithelial carcinoma cells. Photochem Photobiol Sci. 2009;8:1125–9.

    Article  CAS  PubMed  Google Scholar 

  6. Wong SL, Mangu PB, Choti MA, Crocenzi TS, Dodd 3rd GD, Dorfman GS, et al. American Society of Clinical Oncology 2009 clinical evidence review on radiofrequency ablation of hepatic metastases from colorectal cancer. J Clin Oncol. 2010;28:493–508.

    Article  PubMed  Google Scholar 

  7. Dooley WC, Vargas HI, Fenn AJ, Tomaselli MB, Harness JK. Focused microwave thermotherapy for preoperative treatment of invasive breast cancer: a review of clinical studies. Ann Surg Oncol. 2010;17:1076–93.

    Article  PubMed  Google Scholar 

  8. Orsi F, Zhang L, Arnone P, Orgera G, Bonomo G, Vigna PD, et al. High-intensity focused ultrasound ablation: effective and safe therapy for solid tumors in difficult locations. AJR Am J Roentgenol. 2010;195:W245–52.

    Article  PubMed  Google Scholar 

  9. Kennedy LC, Bickford LR, Lewinski NA, Coughlin AJ, Hu Y, Day ES, et al. A new era for cancer treatment: gold–nanoparticle–mediated thermal therapies. Small. 2011;7:169–83.

    Article  CAS  PubMed  Google Scholar 

  10. Pilot Study of AuroLase Therapy in Refractory and/or Recurrent Tumors of the Head and Neck, http://clinicaltrials.gov/ct2/ show/NCT00848042 2010; (accessed September 2010).

  11. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol. 2007;2:751–60.

    Article  CAS  PubMed  Google Scholar 

  12. Sengupta S, Eavarone D, Capila I, Zhao G, Watson N, Kiziltepe T, et al. Temporal targeting of tumour cells and neovasculature with a nanoscale delivery system. Nature. 2005;436:568–72.

    Article  CAS  PubMed  Google Scholar 

  13. Abraham SA, Waterhouse DN, Mayer LD, Cullis PR, Madden TD, Bally MB. The liposomal formulation of doxorubicin. Methods Enzymol. 2005;391:71–9.

    Article  CAS  PubMed  Google Scholar 

  14. Obata Y, Tajima S, Takeoka S. Evaluation of pH-responsive liposomes containing amino acid-based zwitterionic lipids for improving intracellular drug delivery in vitro and in vivo. J Control Release. 2010;142:267–76.

    Article  CAS  PubMed  Google Scholar 

  15. Ducat E, Deprez J, Gillet A, Noel A, Evrard B, Peulen O, et al. Nuclear delivery of a therapeutic peptide by long circulating pH-sensitive liposomes: benefits over classical vesicles. Int J Pharm. 2011;420:319–32.

    Article  CAS  PubMed  Google Scholar 

  16. Paasonen L, Laaksonen T, Johans C, Yliperttula M, Kontturi K, Urtti A. Gold nanoparticles enable selective light-induced contents release from liposomes. J Control Release. 2007;122:86–93.

    Article  CAS  PubMed  Google Scholar 

  17. Paasonen L, Sipila T, Subrizi A, Laurinmaki P, Butcher SJ, Rappolt M, et al. Gold-embedded photosensitive liposomes for drug delivery: triggering mechanism and intracellular release. J Control Release. 2010;147:136–43.

    Article  CAS  PubMed  Google Scholar 

  18. Stadler B, Chandrawati R, Price AD, Chong SF, Breheney K, Postma A, et al. A microreactor with thousands of subcompartments: enzyme-loaded liposomes within polymer capsules. Angew Chem Int Ed Engl. 2009;48:4359–62.

    Article  CAS  PubMed  Google Scholar 

  19. Vamvakaki V, Fournier D, Chaniotakis NA. Fluorescence detection of enzymatic activity within a liposome based nano-biosensor. Biosens Bioelectron. 2005;21:384–8.

    Article  CAS  PubMed  Google Scholar 

  20. Dromi S, Frenkel V, Luk A, Traughber B, Angstadt M, Bur M, et al. Pulsed-high intensity focused ultrasound and low temperature-sensitive liposomes for enhanced targeted drug delivery and antitumor effect. Clin Cancer Res. 2007;13:2722–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Li L, ten Hagen TL, Schipper D, Wijnberg TM, van Rhoon GC, Eggermont AM, et al. Triggered content release from optimized stealth thermosensitive liposomes using mild hyperthermia. J Control Release. 2010;143:274–9.

    Article  CAS  PubMed  Google Scholar 

  22. Agarwal A, Mackey MA, El-Sayed MA, Bellamkonda RV. Remote triggered release of doxorubicin in tumors by synergistic application of thermosensitive liposomes and gold nanorods. ACS Nano. 2011;5:4919–26.

    Article  CAS  PubMed  Google Scholar 

  23. Park JH, von Maltzahn G, Ong LL, Centrone A, Hatton TA, Ruoslahti E, et al. Cooperative nanoparticles for tumor detection and photothermally triggered drug delivery. Adv Mater. 2010;22:880–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Leungand SJ, Romanowski M. NIR-activated content release from plasmon resonant liposomes for probing single-cell responses. ACS Nano. 2012;6:9383–91.

    Article  Google Scholar 

  25. S.J. Leung, M.C. Bobnick, and M. Romanowski. Plasmon resonant gold-coated liposomes for spectrally controlled content release. Proc Soc Photo Opt Instrum Eng. 2010;7577.

  26. Schwartzberg AM, Oshiro TY, Zhang JZ, Huser T, Talley CE. Improving nanoprobes using surface-enhanced Raman scattering from 30-nm hollow gold particles. Anal Chem. 2006;78:4732–6.

    Article  CAS  PubMed  Google Scholar 

  27. Lu W, Huang Q, Ku G, Wen X, Zhou M, Guzatov D, et al. Photoacoustic imaging of living mouse brain vasculature using hollow gold nanospheres. Biomaterials. 2010;31:2617–26.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Lu W, Xiong C, Zhang G, Huang Q, Zhang R, Zhang JZ, et al. Targeted photothermal ablation of murine melanomas with melanocyte-stimulating hormone analog-conjugated hollow gold nanospheres. Clin Cancer Res. 2009;15:876–86.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. You J, Zhang G, Li C. Exceptionally high payload of doxorubicin in hollow gold nanospheres for near-infrared light-triggered drug release. ACS Nano. 2010;4:1033–41.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. You J, Shao R, Wei X, Gupta S, Li C. Near-infrared light triggers release of Paclitaxel from biodegradable microspheres: photothermal effect and enhanced antitumor activity. Small. 2010;6:1022–31.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. You J, Zhang R, Zhang G, Zhong M, Liu Y, Van Pelt CS, et al. Photothermal-chemotherapy with doxorubicin-loaded hollow gold nanospheres: A platform for near-infrared light-trigged drug release. J Control Release. 2012;158:319–28.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. de Smet M, Langereis S. S.v. den Bosch, and H. Grüll. Temperature-sensitive liposomes for doxorubicin delivery under MRI guidance. J Control Release. 2010;143:120–7.

    Article  PubMed  Google Scholar 

  33. Noble RP, Hatch FT, Mazrimas JA, Lindgren FT, Jensen LC, Adamson GL. Comparison of lipoprotein analysis by agarose gel and paper electrophoresis with analytical ultracentrifugation. Lipids. 1969;4:55–9.

    Article  CAS  PubMed  Google Scholar 

  34. Wu G, Mikhailovsky A, Khant HA, Fu C, Chiu W, Zasadzinski JA. Remotely triggered liposome release by near-infrared light absorption via hollow gold nanoshells. J Am Chem Soc. 2008;130:8175–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Hahnand GM, Shiu EC. Effect of pH and elevated temperatures on the cytotoxicity of some chemotherapeutic agents on Chinese hamster cells in vitro. Cancer Res. 1983;43:5789–91.

    Google Scholar 

  36. Yooand J, Lee YJ. Effect of hyperthermia and chemotherapeutic agents on TRAIL-induced cell death in human colon cancer cells. J Cell Biochem. 2008;103:98–109.

    Article  Google Scholar 

  37. Adachi S, Kokura S, Okayama T, Ishikawa T, Takagi T, Handa O, et al. Effect of hyperthermia combined with gemcitabine on apoptotic cell death in cultured human pancreatic cancer cell lines. Int J Hyperth. 2009;25:210–9.

    Article  CAS  Google Scholar 

  38. Ko SH, Ueno T, Yoshimoto Y, Yoo JS, Abdel-Wahab OI, Abdel-Wahab Z, et al. Optimizing a novel regional chemotherapeutic agent against melanoma: hyperthermia-induced enhancement of temozolomide cytotoxicity. Clin Cancer Res. 2006;12:289–97.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments and disclosures

This work was supported by the National Nature Science Foundation of China (81001411), Qianjiang Talent Plan Program of Zhejiang Province (2013R10043), the National Basic Research Program of China (973 Program) under Contract 2009CB930300, National Nature Science Foundation of China (81072583), and part by the National Cancer Institute (U54CA151668).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jian You or Jiang Zhu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 363 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

You, J., Zhang, P., Hu, F. et al. Near-Infrared Light-Sensitive Liposomes for the Enhanced Photothermal Tumor Treatment by the Combination with Chemotherapy. Pharm Res 31, 554–565 (2014). https://doi.org/10.1007/s11095-013-1180-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11095-013-1180-7

KEY WORDS

Navigation