Evaluation the Effect of Sonodynamic Therapy with 5-Aminolevulinic Acid and Sodium Fluorescein by Preclinical Animal Study
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Cell Culture
2.2. Animal Preparation
2.3. FUS Sonication
2.4. Tumor Fluorescein Accumulation Imaging
2.5. Immunohistological Examination
2.6. Statistical Analysis
3. Results
3.1. SDT with Fluorescein in Rat Subcutaneous Tumors
3.2. Histological Examination of the Antitumor Effect of Fluorescein-SDT
3.3. SDT with 5-ALA in Rat Subcutaneous Tumors
3.4. SDT with 5-ALA in a Rat Brain Tumor Model
3.5. SDT with Fluorescein in a Rat Brain Tumor Model
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Ostrom, Q.T.; Gittleman, H.; Truitt, G.; Boscia, A.; Kruchko, C.; Barnholtz-Sloan, J.S. CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2011–2015. Neuro Oncol. 2018, 20, iv1–iv86. [Google Scholar] [CrossRef] [PubMed]
- Costley, D.; Mc Ewan, C.; Fowley, C.; McHale, A.P.; Atchison, J.; Nomikou, N.; Callan, J.F. Treating cancer with sonodynamic therapy: A review. Int. J. Hyperth. 2015, 31, 107–117. [Google Scholar] [CrossRef] [PubMed]
- McHale, A.P.; Callan, J.F.; Nomikou, N.; Fowley, C.; Callan, J.F. Sonodynamic Therapy: Concept, Mechanism and Application to Cancer Treatment. In Therapeutic Ultrasound; Springer Science and Business Media LLC: Cham, Switzerland, 2016; Volume 880, pp. 429–450. [Google Scholar]
- Redza-Dutordoir, M.; Averill-Bates, D.A. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim. Biophys. Acta 2016, 1863, 2977–2992. [Google Scholar] [CrossRef] [PubMed]
- Bunevicius, A.; Pikis, S.; Padilla, F.; Prada, F.; Sheehan, J. Sonodynamic therapy for gliomas. J. Neuro Oncol. 2021, 156, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Xing, X.; Zhao, S.; Xu, T.; Huang, L.; Zhang, Y.; Lan, M.; Lin, C.; Zheng, X.; Wang, P. Advances and perspectives in organic sonosensitizers for sonodynamic therapy. Coord. Chem. Rev. 2021, 445, 214087. [Google Scholar] [CrossRef]
- Prada, F.; Sheybani, N.; Franzini, A.; Moore, D.; Cordeiro, D.; Sheehan, J.; Timbie, K.; Xu, Z. Fluorescein-mediated sonodynamic therapy in a rat glioma model. J. Neuro Oncol. 2020, 148, 445–454. [Google Scholar] [CrossRef] [PubMed]
- Wu, S.-K.; Santos, M.A.; Marcus, S.L.; Hynynen, K. MR-guided Focused Ultrasound Facilitates Sonodynamic Therapy with 5-Aminolevulinic Acid in a Rat Glioma Model. Sci. Rep. 2019, 9, 10465. [Google Scholar] [CrossRef]
- Lipsman, N.; Meng, Y.; Bethune, A.J.; Huang, Y.; Lam, B.; Masellis, M.; Herrmann, N.; Heyn, C.; Aubert, I.; Boutet, A.; et al. Blood–brain barrier opening in Alzheimer’s disease using MR-guided focused ultrasound. Nat. Commun. 2018, 9, 2336. [Google Scholar] [CrossRef]
- Meng, Y.; Hynynen, K.; Lipsman, N. Applications of focused ultrasound in the brain: From thermoablation to drug delivery. Nat. Rev. Neurol. 2021, 17, 7–22. [Google Scholar] [CrossRef]
- Meng, Y.; Pople, C.B.; Lea-Banks, H.; Abrahao, A.; Davidson, B.; Suppiah, S.; Vecchio, L.M.; Samuel, N.; Mahmud, F.; Hynynen, K.; et al. Safety and efficacy of focused ultrasound induced blood-brain barrier opening, an integrative review of animal and human studies. J. Control. Release 2019, 309, 25–36. [Google Scholar] [CrossRef]
- Choi, J.J.; Pernot, M.; Small, S.A.; Konofagou, E.E. Noninvasive, transcranial and localized opening of the blood-brain barrier using focused ultrasound in mice. Ultrasound Med. Biol. 2007, 33, 95–104. [Google Scholar] [CrossRef] [PubMed]
- An, Y.; Liu, H.; Zhou, Z.; Wang, J.; Jiang, G.; Li, Z.; Wang, F.; Jin, H. Sinoporphyrin sodium is a promising sensitizer for photodynamic and sonodynamic therapy in glioma. Oncol. Rep. 2020, 44, 1596–1604. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, M.; Kobayashi, H.; Terasaka, S.; Endo, S.; Yamaguchi, S.; Motegi, H.; Itay, R.; Suzuki, S.; Brokman, O.; Shapira, Y.; et al. Sonodynamic Therapy for Malignant Glioma Using 220-kHz Transcranial Magnetic Resonance Imaging-Guided Focused Ultrasound and 5-Aminolevulinic acid. Ultrasound Med. Biol. 2019, 45, 526–538. [Google Scholar] [CrossRef] [PubMed]
- Ohmura, T.; Fukushima, T.; Shibaguchi, H.; Yoshizawa, S.; Inoue, T.; Kuroki, M.; Sasaki, K.; Umemura, S.-I. Sonodynamic therapy with 5-aminolevulinic acid and focused ultrasound for deep-seated intracranial glioma in rat. Anticancer Res. 2011, 31, 2527–2533. [Google Scholar] [PubMed]
- Chen, H.; Zhou, X.; Gao, Y.; Zheng, B.; Tang, F.; Huang, J. Recent progress in development of new sonosensitizers for sonodynamic cancer therapy. Drug Discov. Today 2014, 19, 502–509. [Google Scholar] [CrossRef] [PubMed]
- Shibaguchi, H.; Tsuru, H.; Kuroki, M.; Kuroki, M. Sonodynamic cancer therapy: A non-invasive and repeatable approach using low-intensity ultrasound with a sonosensitizer. Anticancer Res. 2011, 31, 2425–2429. [Google Scholar] [PubMed]
- Wan, G.-Y.; Liu, Y.; Chen, B.-W.; Liu, Y.-Y.; Wang, Y.; Zhang, N. Recent advances of sonodynamic therapy in cancer treatment. Cancer Biol. Med. 2016, 13, 325–338. [Google Scholar] [CrossRef]
- Acerbi, F.; Broggi, M.; Schebesch, K.-M.; Höhne, J.; Cavallo, C.; De Laurentis, C.; Eoli, M.; Anghileri, E.; Servida, M.; Boffano, C.; et al. Fluorescein-Guided Surgery for Resection of High-Grade Gliomas: A Multicentric Prospective Phase II Study (FLUOGLIO). Clin. Cancer Res. 2018, 24, 52–61. [Google Scholar] [CrossRef]
- Stummer, W.; Pichlmeier, U.; Meinel, T.; Wiestler, O.D.; Zanella, F.; Reulen, H.-J. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: A randomised controlled multicentre phase III trial. Lancet Oncol. 2006, 7, 392–401. [Google Scholar] [CrossRef]
- Mazurek, M.; Szczepanek, D.; Orzyłowska, A.; Rola, R. Analysis of Factors Affecting 5-ALA Fluorescence Intensity in Visualizing Glial Tumor Cells—Literature Review. Int. J. Mol. Sci. 2022, 23, 926. [Google Scholar] [CrossRef]
- Hadjipanayis, C.G.; Stummer, W. 5-ALA and FDA approval for glioma surgery. J. Neuro Oncol. 2019, 141, 479–486. [Google Scholar] [CrossRef] [PubMed]
- Hydrochloride, A.A. Known as ALA HCl (Gleolan, NX Development Corp.) as an Optical Imaging Agent Indicated in Patients with Gliomas; US Food and Drug Administration: Silver Spring, MD, USA, 2017.
- Teixidor, P.; Arráez, M.; Villalba, G.; Garcia, R.; Tardáguila, M.; González, J.J.; Rimbau, J.; Vidal, X.; Montané, E. Safety and Efficacy of 5-Aminolevulinic Acid for High Grade Glioma in Usual Clinical Practice: A Prospective Cohort Study. PLoS ONE 2016, 11, e0149244. [Google Scholar] [CrossRef] [PubMed]
- Bilmin, K.; Kujawska, T.; Grieb, P. Sonodynamic Therapy for Gliomas. Perspectives and Prospects of Selective Sonosensitization of Glioma Cells. Cells 2019, 8, 1428. [Google Scholar] [CrossRef] [PubMed]
- Traylor, J.I.; Pernik, M.N.; Sternisha, A.C.; McBrayer, S.K.; Abdullah, K.G. Molecular and Metabolic Mechanisms Underlying Selective 5-Aminolevulinic Acid-Induced Fluorescence in Gliomas. Cancers 2021, 13, 580. [Google Scholar] [CrossRef]
- Schebesch, K.-M.; Brawanski, A.; Hohenberger, C.; Hohne, J. Fluorescein sodium-guided surgery of malignant brain tumors: History, current concepts, and future projects. Turk. Neurosurg. 2016, 26, 185–194. [Google Scholar] [CrossRef] [PubMed]
- Diaz, R.J.; Dios, R.R.; Hattab, E.M.; Burrell, K.; Rakopoulos, P.; Sabha, N.; Hawkins, C.; Zadeh, G.; Rutka, J.T.; Cohen-Gadol, A.A. Study of the biodistribution of fluorescein in glioma-infiltrated mouse brain and histopathological correlation of intraoperative findings in high-grade gliomas resected under fluorescein fluorescence guidance. J. Neurosurg. 2015, 122, 1360–1369. [Google Scholar] [CrossRef] [PubMed]
- Schneider, S.W.; Ludwig, T.; Tatenhorst, L.; Braune, S.; Oberleithner, H.; Senner, V.; Paulus, W. Glioblastoma cells release factors that disrupt blood-brain barrier features. Acta Neuropathol. 2004, 107, 272–276. [Google Scholar] [CrossRef]
- Shinoda, J.; Yano, H.; Yoshimura, S.-I.; Okumura, A.; Kaku, Y.; Iwama, T.; Sakai, N. Fluorescence-guided resection of glioblastoma multiforme by using high-dose fluorescein sodium. J. Neurosurg. 2003, 99, 597–603. [Google Scholar] [CrossRef]
- Do, J.; Foster, D.; Renier, C.; Vogel, H.; Rosenblum, S.; Doyle, T.C.; Tse, V.; Wapnir, I. Ex vivo Evans blue assessment of the blood brain barrier in three breast cancer brain metastasis models. Breast Cancer Res. Treat. 2014, 144, 93–101. [Google Scholar] [CrossRef]
- McDannold, N.; Vykhodtseva, N.; Hynynen, K. Effects of acoustic parameters and ultrasound contrast agent dose on focused-ultrasound induced blood-brain barrier disruption. Ultrasound Med. Biol. 2008, 34, 930–937. [Google Scholar] [CrossRef]
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Huang, C.-Y.; Li, J.-C.; Chen, K.-T.; Lin, Y.-J.; Feng, L.-Y.; Liu, H.-L.; Wei, K.-C. Evaluation the Effect of Sonodynamic Therapy with 5-Aminolevulinic Acid and Sodium Fluorescein by Preclinical Animal Study. Cancers 2024, 16, 253. https://doi.org/10.3390/cancers16020253
Huang C-Y, Li J-C, Chen K-T, Lin Y-J, Feng L-Y, Liu H-L, Wei K-C. Evaluation the Effect of Sonodynamic Therapy with 5-Aminolevulinic Acid and Sodium Fluorescein by Preclinical Animal Study. Cancers. 2024; 16(2):253. https://doi.org/10.3390/cancers16020253
Chicago/Turabian StyleHuang, Chiung-Yin, Jui-Chin Li, Ko-Ting Chen, Ya-Jui Lin, Li-Ying Feng, Hao-Li Liu, and Kuo-Chen Wei. 2024. "Evaluation the Effect of Sonodynamic Therapy with 5-Aminolevulinic Acid and Sodium Fluorescein by Preclinical Animal Study" Cancers 16, no. 2: 253. https://doi.org/10.3390/cancers16020253