Wireless sequential dual light delivery for programmed PDT in vivo

Jiayi Liu; Bowen Sun; Wenkai Li; Han-Joon Kim; Shu Uin Gan; John S. Ho; Juwita Norasmara Bte Rahmat; Yong Zhang

doi:10.1038/s41377-024-01437-x

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Wireless sequential dual light delivery for programmed PDT in vivo

Original Articles

- Wireless sequential dual light delivery for programmed PDT in vivo
- Wireless sequential dual light delivery for programmed PDT in vivo
- LSA 2024年13卷第6期页码：1047-1061
- Affiliations：
  
  1.Department of Oncology, The Second Xiangya Hospital, Central South University, Changsha, Hunan 410011, China
  2.Department of Biomedical Engineering, College of Design and Engineering, National University of Singapore, Singapore 117585, Singapore
  3.Department of Mechanical Engineering, College of Design and Engineering, National University of Singapore, Singapore 117576, Singapore
  4.Department of Electrical and Computer Engineering, College of Design and Engineering, National University of Singapore, Singapore 117583, Singapore
  5.Department of Medical IT Convergence Engineering, Kumoh National Institute of Technology, Gumi 39253, Republic of Korea
  6.Department of Surgery, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228, Singapore
  7.The N.1 Institute for Health, National University of Singapore, Singapore 117456, Singapore
  8.Institute for Health Innovation and Technology, National University of Singapore, Singapore 119276, Singapore
  9.Department of Biomedical Engineering, College of Engineering, City University of Hong Kong, Kowloon, Hong Kong SAR, China
- Author bio：
  
  Juwita Norasmara Bte Rahmat (biejnr@nus.edu.sg)
  Yong Zhang (yozhang@cityu.edu.hk)
- Funds：
- DOI：10.1038/s41377-024-01437-x
  中图分类号：
- 收稿：2024-01-04，
  
  修回：2024-03-05，
  
  录用：2024-03-21，
  
  网络出版：2024-05-15，
  
  纸质出版：2024-06-30
- Accepted：
Scan QR Code
Wireless sequential dual light delivery for programmed PDT in vivo[J]. LSA, 2024,13(6):1047-1061.

Liu, J. Y. et al. Wireless sequential dual light delivery for programmed PDT in vivo. Light: Science & Applications, 13, 1047-1061 (2024).
Wireless sequential dual light delivery for programmed PDT in vivo[J]. LSA, 2024,13(6):1047-1061. DOI： 10.1038/s41377-024-01437-x.

Liu, J. Y. et al. Wireless sequential dual light delivery for programmed PDT in vivo. Light: Science & Applications, 13, 1047-1061 (2024). DOI： 10.1038/s41377-024-01437-x.

摘要

Abstract

Using photodynamic therapy (PDT) to treat deep-seated cancers is limited due to inefficient delivery of photosensitizers and low tissue penetration of light. Polymeric nanocarriers are widely used for photosensitizer delivery

while the self-quenching of the encapsulated photosensitizers would impair the PDT efficacy. Furthermore

the generated short-lived reactive oxygen spieces (ROS) can hardly diffuse out of nanocarriers

resulting in low PDT efficacy. Therefore

a smart nanocarrier system which can be degraded by light

followed by photosensitizer activation can potentially overcome these limitations and enhance the PDT efficacy. A light-sensitive polymer nanocarrier encapsulating photosensitizer (RB-M) was synthesized. An implantable wireless dual wavelength microLED device which delivers the two light wavelengths sequentially was developed to programmatically control the release and activation of the loaded photosensitizer. Two transmitter coils with matching resonant frequencies allow activation of the connected LEDs to emit different wavelengths independently. Optimal irradiation time

dose

and RB-M concentration were determined using an agent-based digital simulation method. In vitro and in vivo validation experiments in an orthotopic rat liver hepatocellular carcinoma disease model confirmed that the nanocarrier rupture and sequential low dose light irradiation strategy resulted in successful PDT at reduced photosensitizer and irradiation dose

which is a clinically significant event that enhances treatment safety.

关键词

Keywords

references

Castano, A. P. et al. Mechanisms in photodynamic therapy: part one-photosensitizers, photochemistry and cellular localization. Photodiagnosis Photodyn. Ther. 1 , 279–293 (2004)..

Castano, A. P., Demidova, T. N. & Hamblin, M. R. Mechanisms in photodynamic therapy: part two-cellular signaling, cell metabolism and modes of cell death. Photodiagnosis Photodyn. Ther. 2 , 1–23 (2005)..

Stolik, S. et al. Measurement of the penetration depths of red and near infrared light in human "ex vivo" tissues. J. Photochem. Photobiol. B Biol. 57 , 90–93 (2000)..

Ismail, M. S. et al. Pharmacokinetic analysis of octa-α-butyloxy-zinc phthalocyanine in mice bearing Lewis lung carcinoma. J. Clin. Laser Med. Surg. 15 , 157–161 (1997)..

Sun, B. W. et al. Wirelessly activated nanotherapeutics for in vivo programmable photodynamic-chemotherapy of orthotopic bladder cancer. Adv. Sci. 9 , 2200731 (2022)..

Teh, D. B. L. et al. A flexi-PEGDA upconversion implant for wireless brain photodynamic therapy. Adv. Mater. 32 , 2001459 (2020)..

Bansal, A. et al. In vivo wireless photonic photodynamic therapy. Proc. Natl Acad. Sci. USA 115 , 1469–1474 (2018)..

Zhang, Z. et al. Upconversion superballs for programmable photoactivation of therapeutics. Nat. Commun. 10 , 4586 (2019)..

Zhang, Z. et al. Controllable assembly of upconversion nanoparticles enhanced tumor cell penetration and killing efficiency. Adv. Sci. 7 , 2001831 (2020)..

Choi, J. et al. Implantable micro-scale LED device guided photodynamic therapy to potentiate antitumor immunity with mild visible light. Biomater. Res. 26 , 56 (2022)..

Kirino, I. et al. Metronomic photodynamic therapy using an implantable LED device and orally administered 5-aminolevulinic acid. Sci. Rep. 10 , 22017 (2020)..

Yamagishi, K. et al. Tissue-adhesive wirelessly powered optoelectronic device for metronomic photodynamic cancer therapy. Nat. Biomed. Eng. 3 , 27–36 (2019)..

Deng, K. et al. Dual-step irradiation strategy to sequentially destroy singlet oxygen-responsive polymeric micelles and boost photodynamic cancer therapy. Biomaterials 275 , 120959 (2021)..

Guo, H. et al. Dual-responsive nano-prodrug micelles for MRI-guided tumor PDT and immune synergistic therapy. J. Mater. Chem. B 10 , 4261–4273 (2022)..

Cheng, R. et al. Dual and multi-stimuli responsive polymeric nanoparticles for programmed site-specific drug delivery. Biomaterials 34 , 3647–3657 (2013)..

Fathi, M. et al. Stimuli-responsive chitosan-based nanocarriers for cancer therapy. Bioimpacts 7 , 269–277 (2017)..

Fleige, E., Quadir, M. A. & Haag, R. Stimuli-responsive polymeric nanocarriers for the controlled transport of active compounds: concepts and applications. Adv. Drug Deliv. Rev. 64 , 866–884 (2012)..

Sun, B. W., Bte Rahmat, J. N. & Zhang, Y. Advanced techniques for performing photodynamic therapy in deep-seated tissues. Biomaterials 291 , 121875 (2022)..

Pogue, B. W. et al. Revisiting photodynamic therapy dosimetry: reductionist & surrogate approaches to facilitate clinical success. Phys. Med. Biol. 61 , R57–R89 (2016)..

Gunaydin, G., Gedik, M. E. & Ayan, S. Photodynamic therapy for the treatment and diagnosis of cancer-a review of the current clinical status. Front. Chem. 9 , 686303 (2021)..

Sun, X. Q. et al. Multi-scale agent-based brain cancer modeling and prediction of TKI treatment response: incorporating EGFR signaling pathway and angiogenesis. BMC Bioinform. 13 , 218 (2012)..

Rahbar, S. et al. Agent-based modeling of tumor and immune system interactions in combinational therapy with low-dose 5-fluorouracil and dendritic cell vaccine in melanoma B16F10. Iran. J. Allergy Asthma Immunol. 21 , 151–166 (2022)..

Jiang, J. Q. et al. Toward photocontrolled release using light-dissociable block copolymer micelles. Macromolecules 39 , 4633–4640 (2006)..

Chen, G. J. et al. Neuroendocrine tumor-targeted upconversion nanoparticle-based micelles for simultaneous nir-controlled combination chemotherapy and photodynamic therapy, and fluorescence imaging. Adv. Funct. Mater. 27 , 1604671 (2017)..

Ding, F. et al. Chlorin e6-encapsulated polyphosphoester based nanocarriers with viscous flow core for effective treatment of pancreatic cancer. ACS Appl. Mater. Interfaces 7 , 18856–18865 (2015)..

Steffen-Heins, A. & Steffens, B. EPR spectroscopy and its use in planta —a promising technique to disentangle the origin of specific ROS. Front. Environ. Sci. 3 , 15 (2015)..

Mahalingam, S. M., Ordaz, J. D. & Low, P. S. Targeting of a photosensitizer to the mitochondrion enhances the potency of photodynamic therapy. ACS Omega 3 , 6066–6074 (2018)..

Ludvíková, L. et al. Photochemistry of rose bengal in water and acetonitrile: a comprehensive kinetic analysis. Phys. Chem. Chem. Phys. 18 , 16266–16273 (2016)..

Yarmolenko, P. S. et al. Thresholds for thermal damage to normal tissues: an update. Int. J. Hyperth. 27 , 320–343 (2011) ..

Chau, G. Y., Lui, W. Y. & Wu, C. W. Spectrum and significance of microscopic vascular invasion in hepatocellular carcinoma. Surg. Oncol. Clin. N. Am. 12 , 25–34 (2003)..

Wu, Q. et al. Exosome-mediated communication in the tumor microenvironment contributes to hepatocellular carcinoma development and progression. J. Hematol. Oncol. 12 , 53 (2019)..

Deng, Z. et al. Comprehensive understanding of anchorage-independent survival and its implication in cancer metastasis. Cell Death Dis. 12 , 629 (2021)..

Workman, P. et al. Guidelines for the welfare and use of animals in cancer research. Br. J. Cancer 102 , 1555–1577 (2010)..

Mendonsa, A. M., Na, T. Y. & Gumbiner, B. M. E-cadherin in contact inhibition and cancer. Oncogene 37 , 4769–4780 (2018)..

Chen, J. et al. Prognostic significance of E-cadherin expression in hepatocellular carcinoma: a meta-analysis. PLoS One 9 , e103952 (2014)..

Park, J. S. et al. Synergistic effects of concurrent photodynamic therapy with indocyanine green and chemotherapy in hepatocellular carcinoma cell lines and mouse models. J. Photochem. Photobiol. B: Biol. 239 , 112642 (2023)..

Hu, J. et al. Bimodal treatment of hepatocellular carcinoma by targeted minimally interventional photodynamic/chemotherapy using glyco-covalent-organic frameworks-guided porphyrin/sorafenib. Acta Biomater. 148 , 206–217 (2022)..

Qi, S. et al. Targeted multifunctional nanoplatform for imaging-guided precision diagnosis and photothermal/photodynamic therapy of orthotopic hepatocellular carcinoma. Int. J. Nanomed. 17 , 3777–3792 (2022)..

Ikeda, M. et al. Chemotherapy for hepatocellular carcinoma: current status and future perspectives. Jpn. J. Clin. Oncol. 48 , 103–114 (2018)..

Fan, Y. J., Xue, H. & Zheng, H. C. Systemic therapy for hepatocellular carcinoma: current updates and outlook. J. Hepatocell. Carcinoma 9 , 233–263 (2022)..

Qi, D. P. et al. Stretchable electronics based on PDMS substrates. Adv. Mater. 33 , 2003155 (2021)..

González-Alonso, J. Human thermoregulation and the cardiovascular system. Exp. Physiol. 97 , 340–346 (2012)..

Chu, K. F. & Dupuy, D. E. Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat. Rev. Cancer 14 , 199–208 (2014)..

Hannon, G. et al. The effects of localized heat on the hallmarks of cancer. Adv. Therapeutics 4 , 2000267 (2021)..

Bienia, A. et al. Photodynamic therapy and hyperthermia in combination treatment—neglected forces in the fight against cancer. Pharmaceutics 13 , 1147 (2021)..

Smith, S. A. et al. The endosomal escape of nanoparticles: toward more efficient cellular delivery. Bioconjugate Chem. 30 , 263–272 (2019)..

Moreno-Echeverri, A. M. et al. Pitfalls in methods to study colocalization of nanoparticles in mouse macrophage lysosomes. J. Nanobiotechnol. 20 , 464 (2022)..

Sun, Y. et al. Phase-separating peptides for direct cytosolic delivery and redox -activated release of macromolecular therapeutics. Nat. Chem. 14 , 274–283 (2022)..

Chen, X. Y. et al. Study of copper-cysteamine based X-ray induced photodynamic therapy and its effects on cancer cell proliferation and migration in a clinical mimic setting. Bioact. Mater. 7 , 504–514 (2022)..

Shao, W. et al. Molecular design of conjugated small molecule nanoparticles for synergistically enhanced PTT/PDT. Nano-Micro Lett. 12 , 147 (2020)..

Bharate, G. Y., Qin, H. B. & Fang, J. Poly(styrene- co -maleic acid) micelle of photosensitizers for targeted photodynamic therapy, exhibits prolonged singlet oxygen generating capacity and superior intracellular uptake. J. Pers. Med. 12 , 493 (2022)..

Sztandera, K. et al. pH-stable polymersome as nanocarrier for post-loaded rose bengal in photodynamic therapy. Colloids Surf. B: Biointerfaces 217 , 112662 (2022)..

Ceballos, M. P. et al. ABC transporters: regulation and association with multidrug resistance in hepatocellular carcinoma and colorectal carcinoma. Curr. Med. Chem. 26 , 1224–1250 (2019)..

Brito, A. F. et al. Positron emission tomography diagnostic imaging in multidrug-resistant hepatocellular carcinoma: focus on 2-deoxy-2-(18F)Fluoro-D-Glucose. Mol. Diagn. Ther. 18 , 495–504 (2014)..

Kanda, T. et al. Molecular mechanisms driving progression of liver cirrhosis towards hepatocellular carcinoma in chronic hepatitis B and C infections: a review. Int. J. Mol. Sci. 20 , 1358 (2019)..

Cao, L. et al. Engineering nanotheranostic strategies for liver cancer. World J. Gastrointest. Oncol. 13 , 1213–1228 (2021)..

Yang, S. S. et al. Drug delivery strategy in hepatocellular carcinoma therapy. Cell Commun. Signal. 20 , 26 (2022)..

Khorobrykh, S. et al. Oxygen and ROS in photosynthesis. Plants 9 , 91 (2020)..

Sutherland, R. M. Cell and environment interactions in tumor microregions: the multicell spheroid model. Science 240 , 177–184 (1988)..

Fang, Y. & Eglen, R. M. Three-dimensional cell cultures in drug discovery and developmen t. SLAS Discov. 22 , 456–472 (2017)..

Langhans, S. A. Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front. Pharmacol. 9 , 6 (2018)..

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