Journal of Radiopharmaceuticals and Molecular Probes (대한방사성의약품학회지)

Korean Society of Radiopharmaceuticals and Molecular Probes (대한방사성의약품학회)
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Photodynamic Therapy for Cancer without External Light Illumination by Utilizing Radioisotope-induced Cerenkov Luminescence as an Excitation Source

  • Chi Soo Kang (Division of Applied RI, Korea Institute of Radiological and Medical Sciences) ;
  • Md. Saidul Islam (Division of Applied RI, Korea Institute of Radiological and Medical Sciences) ;
  • Dohyeon Kim (Division of Applied RI, Korea Institute of Radiological and Medical Sciences) ;
  • Kyo Chul Lee (Division of Applied RI, Korea Institute of Radiological and Medical Sciences)
  • Received : 2023.04.25
  • Accepted : 2023.06.07
  • Published : 2023.06.30
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Abstract

Photodynamic therapy (PDT), in which a photosensitizer (PS), light, and molecular oxygen are essential components, is a non-invasive and highly effective cancer therapeutic method. However, PDT suffers from the penetration limit of light caused by attenuation and scattering of light through tissues constraining its use to skin and endoscopically accessible cancers. Cerenkov luminescence (CL) is defined as the light illuminated when charged particles move in a dielectric medium at a velocity greater than the phase velocity of light. It is known that medical radioisotopes in preclinical and clinical settings have enough energy to generate CL, and lately, CL has been exploited as an excitation source for PDT without external light illumination. This review introduces state of the art studies of radioisotope-based PDT for cancer, in which radioisotopes are utilized as a light source.

Keywords

Acknowledgement

This work was supported by a grant of the Korea Institute of Radiological and Medical Sciences (KIRAMS), funded by Ministry of Science and ICT (MSIT), Korea (No. 50461-2023).

References

  1. Santos AF dos, Almeida DRQ De, Terra LF, Baptista MS, Labriola L. Photodynamic therapy in cancer treatment - an update review. J Cancer Metastasis Treat 2019;5:25.
  2. Dolmans DE, Fukumura D, Jain RK. Photodynamic therapy for cancer. Nature reviews cancer 2003;3:380-7. https://doi.org/10.1038/nrc1071
  3. McCaughan JS. Photodynamic therapy: a review. Drugs Aging. 1999;15(1):49-68. https://doi.org/10.2165/00002512-199915010-00005
  4. Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, Moan J, Peng Q, Photodynamic therapy. Journal of the national cancer institute 1998;90(12):889-905. https://doi.org/10.1093/jnci/90.12.889
  5. Yanovsky RL, Bartenstein DW, Rogers GS, Isakoff SJ, Chen ST. Photodynamic therapy for solid tumors: A review of the literature. Photodermatology, Photoimmunology & Photomedicine 2019;35(5):295-303. https://doi.org/10.1111/phpp.12489
  6. Yoo JO, Ha KS. New Insights into the Mechanisms for Photodynamic Therapy-Induced Cancer Cell Death. In: Jeon KW, editor. International Review of Cell and Molecular Biology. Academic Press; 2012.p.139-74.
  7. Crous A, Abrahamse H. Photodynamic therapy of lung cancer, where are we? Frontiers in Pharmacology 2022;13:932098.
  8. Didamson OC, Abrahamse H. Targeted Photodynamic Diagnosis and Therapy for Esophageal Cancer: Potential Role of Functionalized Nanomedicine. Pharmaceutics 2021;13(11):1943.
  9. Lamberti MJ, Vittar NB, Rivarola VA. Breast cancer as photodynamic therapy target: Enhanced therapeutic efficiency by overview of tumor complexity. World J Clin Oncol 2014;5(5):901-7. https://doi.org/10.5306/wjco.v5.i5.901
  10. Mallidi S, Anbil S, Bulin A-L, Obaid G, Ichikawa M, Hasan T. Beyond the Barriers of Light Penetration: Strategies, Perspectives and Possibilities for Photodynamic Therapy. Theranostics 2016;6(13):2458-87. https://doi.org/10.7150/thno.16183
  11. Park J, Lee YK, Park I-K, Hwang SR. Current Limitations and Recent Progress in Nanomedicine for Clinically Available Photodynamic Therapy. Biomedicines 2021; 9(1):85.
  12. Ciarrocchi E, Belcari N. Cerenkov luminescence imaging: physics principles and potential applications in biomedical sciences. EJNMMI Physics 2017;4(1):14.
  13. Gill RK, Mitchell GS, Cherry SR. Computed Cerenkov luminescence yields for radionuclides used in biology and medicine. Phys Med Biol 2015;60(11):4263-80. https://doi.org/10.1088/0031-9155/60/11/4263
  14. Wang X, Li Lintao, Li J, Wang P, Lang J, Yang Y. Cherenkov Luminescence in Tumor Diagnosis and Treatment: A Review. Photonics 2022;9(6):390.
  15. Spinelli AE, Boschi F. Photodynamic Therapy Using Cerenkov and Radioluminescence Light. Frontiers in Physics 2021;9:637120.
  16. Jacobson O, Kiesewetter DO, Chen X. Fluorine-18 radiochemistry, labeling strategies and synthetic routes. Bioconjug Chem 2015;26(1):1-18. https://doi.org/10.1021/bc500475e
  17. Wang Y, Lin Q, Shi H, Cheng D. Fluorine-18: Radiochemistry and Target-Specific PET Molecular Probes Design. Frontiers in Chemistry 2022;10:884517.
  18. Nakamura Y, Nagaya T, Sato K, Okuyama S, Ogata F, Wong K, Adler S, Choyke PL, Kobayashi H. Cerenkov Radiation-Induced Photoimmunotherapy with 18F-FDG. J Nucl Med 2017;58(9):1395-1400. https://doi.org/10.2967/jnumed.116.188789
  19. Kotagiri N, Cooper ML, Rettig M, Egbulefu C, Prior J, Cui G, Karmakar P, Zhou M, Yang X, Sudlow G, Marsala L, ChanswangphuwanaC, Lu L, Habimana-Griffin L, Shokeen M, Xu X, Weilbaecher K, Tomasson M, Lanza G, DiPersio JF, Achilefu S. Radionuclides transform chemotherapeutics into phototherapeutics for precise treatment of disseminated cancer. Nature Communications 2018;9(1):275.
  20. Lioret V, Bellaye PD, Arnould C, Collin B, Decreau RA. Dual Cherenkov Radiation-Induced Near-Infrared Luminescence Imaging and Photodynamic Therapy toward Tumor Resection. Journal of Medicinal Chemistry 2020;63(17):9446-56. https://doi.org/10.1021/acs.jmedchem.0c00625
  21. Chen Y-A, Li J-J, Lin S-L, Lu C-H, Chiu S-J, Jeng F-S, Chang C-W, Yang B-H, Chang M-C, Ke C-C, Liu R-S. Effect of Cerenkov Radiation-Induced Photodynamic Therapy with (18)F-FDG in an Intraperitoneal Xenograft Mouse Model of Ovarian Cancer. Int J Mol Sic 2021;22(9):4934.
  22. Quintos-Meneses HA, Aranda-Lara L, Morales-Avila E, Torres-Garcia E, Camacho-Lopez MA, Sanchez-Holguin M, Luna-Gutierrez MA, Ramirez-Duran N, Isaac-Olive K. In vitro irradiation of doxorubicin with 18F-FDG Cerenkov radiation and its potential application as a theragnostic system. Journal of Photochemistry and Photobiology B: Biology 2020;210:111961.
  23. Gallaga-Gonzalez U, Morales-Avila E, Torres-Garcia E, Estrada JA, Diaz-Sanchez LE, Izquierdo G, Aranda-Lara L, Isaac-Olive K. Photoactivation of Chemotherapeutic Agents with Cerenkov Radiation for Chemo-Photodynamic Therapy. ACS Omega 2022;7(27):23591-604. https://doi.org/10.1021/acsomega.2c02153
  24. Zhou Y, Li J, Xu X, Zhao M, Zhang B, Deng S, Wu Y. 64Cu-based Radiopharmaceuticals in Molecular Imaging. Technol Cancer Res Treat 2019;18:1533033819830758.
  25. Kotagiri N, Sudlow GP, Akers WJ, Achilefu S. Breaking the depth dependency of phototherapy with Cerenkov radiation and low-radiance-responsive nanophotosensitizers. Nature Nanotechnology 2015;10(4):370-9. https://doi.org/10.1038/nnano.2015.17
  26. Lee W, Jeon M, Choi J, Oh C, Kim G, Jung S, Kim C, Ye S-J, Im H-J. Europium-Diethylenetriaminepentaacetic Acid Loaded Radioluminescence Liposome Nanoplatform for Effective Radioisotope-Mediated Photodynamic Therapy. ACS Nano 2020;4(10):13004-15. https://doi.org/10.1021/acsnano.0c04324
  27. Jo C, Ahn H, Kim JH, Lee YJ, KIM JY, Lee KC, Kang CS, Kim S. Cancer therapy by antibody-targeted Cerenkov light and metabolism-selective photosensitization. Journal of Controlled Release 2022;352:25-34. https://doi.org/10.1016/j.jconrel.2022.10.014
  28. Heskamp S, Raave R, Boerman O, Rijpkema M, Goncalves V, Denat F. 89Zr-Immuno-Positron Emission Tomography in Oncology: State-of-the-Art 89Zr Radiochemistry. Bioconju Chem 2017;28(9):2211-23. https://doi.org/10.1021/acs.bioconjchem.7b00325
  29. Kamkaew A, Cheng L, Geol S, Valdovinos HF, Barnhart TE, Liu Z, Cai W. Cerenkov Radiation Induced Photodynamic Therapy Using Chlorin e6-Loaded Hollow Mesoporous Silica Nanoparticles. ACS Applied Materials & Interfaces 2016;8(40):26630-7. https://doi.org/10.1021/acsami.6b10255
  30. Ni D, Ferreira CA, Barnhart TE, Quach V, Yu B, Jiang D, Wei W, Liu H, Engle JW, Hu P, Cai W. Magnetic Targeting of Nanotheranostics Enhances Cerenkov Radiation-Induced Photodynamic Therapy. J Am Chem Soc 2018;140(44):14971-9. https://doi.org/10.1021/jacs.8b09374
  31. Yu B, Ni D, Rosenkrans ZT, Barnhart TE, Wei H, Ferreira CA, Lan X, Engle JW, He Q, Yu F, Cai W. A "Missile-Detonation" Strategy to Precisely Supply and Efficiently Amplify Cerenkov Radiation Energy for Cancer Theranostics. Adv Mater 2019;31(52):e1904894.
  32. Morgat C, Hindie E, Mishra AK, Allard M, Fernandez P. Gallium-68: chemistry and radiolabeled peptides exploring different oncogenic pathways. Cancer Biother Radiopharm 2013;28(2):85-97. https://doi.org/10.1089/cbr.2012.1244
  33. Shaffer TM, Pratt EC, Grimm J. Utilizing the power of Cerenkov light with nanotechnology. Nature Nanotechnology 2017;12(2):106-17. https://doi.org/10.1038/nnano.2016.301
  34. Duan D, Liu H, Xu Y, Han Y, Xu M, Zhang Z, Liu Z. Activating TiO2 Nanoparticles: Gallium-68 Serves as a High-Yield Photon Emitter for Cerenkov-Induced Photodynamic Therapy. ACS Applied Materials & Interfaces 2018;10(6):5278-86. https://doi.org/10.1021/acsami.7b17902
  35. Wyszomirska A. Iodine-131 for therapy of thyroid diseases. Physical and biological basis. Nucl Med Rev Cent East Eur 2012;15(2):120-3.
  36. Mody VV, Singh AN, Deshmuk R, Shah S. Thyroid hormones, iodine and iodides, and antithyroid drugs. In: Ray SD, editor. Side Effects of Drugs Annual. Amsterdam:Elsevier; 2015;37:p. 513-9.
  37. Cai P, Yang W, He Z, Jia H, Wang H, Zhao W, Gao L, Zhang Z, Gao F, Gao X. A chlorin-lipid nanovesicle nucleus drug for amplified therapeutic effects of lung cancer by internal radiotherapy combined with the Cerenkov radiation-induced photodynamic therapy. Biomaterials Science 2020;8(17):4841-51. https://doi.org/10.1039/D0BM00778A
  38. Wang Q, Liu N, Hou Z, Shi J, Su X, Sun X. Radioiodinated Persistent Luminescence Nanoplatform for Radiation-Induced Photodynamic Therapy and Radiotherapy. Advanced Healthcare Materials 2021;10(5):2000802.
  39. Guo J, Feng K, Wu W, Ruan Y, Liu H, Han X, Shao G, Sun X. Smart 131I-Labeled Self-Illuminating Photosensitizers for Deep Tumor Therapy. Angew Chem Int Ed Engl 2021;60(40):21884-9. https://doi.org/10.1002/anie.202107231
  40. Qian R, Wang K, Guo Y, Li H, Zhu Z, Huang X, Gong C, Gao Y, Guo R, Yang B, Wang C, Jiang D, Lan X, An R, Gao Z. Minimizing adverse effects of Cerenkov radiation induced photodynamic therapy with transformable photosensitizer-loaded nanovesicles. Journal of Nanobiotechnology 2022;20(1):203.
  41. Khajornjiraphan N, Thu NA, Chow PKH. Yttrium-90 microspheres: a review of its emerging clinical indications. Liver Cancer 2015;4(1):6-15. https://doi.org/10.1159/000343876
  42. Witzig TE, Yttrium-90-ibritumomab tiuxetan radioimmunotherapy: a new treatment approach for B-cell non-Hodgkin's lymphoma. Drugs Today (Barc) 2004;40(2):111-9. https://doi.org/10.1358/dot.2004.40.2.799423
  43. Hartl BA, Hirschberg H, Marcu L, Cherry SR. Activating Photodynamic Therapy in vitro with Cerenkov Radiation Generated from Yttrium-90. J Environ Pathol Toxicol Oncol 2016;35(2):185-92. https://doi.org/10.1615/JEnvironPatholToxicolOncol.2016016903
  44. Malone CD, Egbulefu C, Zheleznyak Z, Polina J, Karmakar P, Black K, Shokeen M, Achilefu S. Activation of nano-photosensitizers by Y-90 microspheres to enhance oxidative stress and cell death in hepatocellular carcinoma. Scientific Reports 2022;12(1):12748.