Cell-cycle dependence on the biological effects of boron neutron capture therapy and its modification by polyvinyl alcohol.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
19 Jul 2024
Historique:
received: 15 04 2024
accepted: 08 07 2024
medline: 20 7 2024
pubmed: 20 7 2024
entrez: 19 7 2024
Statut: epublish

Résumé

Boron neutron capture therapy (BNCT) is a unique radiotherapy of selectively eradicating tumor cells using boron compounds (e.g., 4-borono-L-phenylalanine [BPA]) that are heterogeneously taken up at the cellular level. Such heterogenicity potentially reduces the curative efficiency. However, the effects of temporospatial heterogenicity on cell killing remain unclear. With the technical combination of radiation track detector and biophysical simulations, this study revealed the cell cycle-dependent heterogenicity of BPA uptake and subsequent biological effects of BNCT on HeLa cells expressing fluorescent ubiquitination-based cell cycle indicators, as well as the modification effects of polyvinyl alcohol (PVA). The results showed that the BPA concentration in the S/G

Identifiants

pubmed: 39030350
doi: 10.1038/s41598-024-67041-6
pii: 10.1038/s41598-024-67041-6
doi:

Substances chimiques

Polyvinyl Alcohol 9002-89-5
Boron Compounds 0
Phenylalanine 47E5O17Y3R

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

16696

Informations de copyright

© 2024. The Author(s).

Références

Locher, G. L. Biological effects and therapeutic possibilities of neutrons. Am. J. Roentgenol. Radium. Ther. 36(1), 1–13 (1936).
Coderre, J. A. et al. Derivations of relative biological effectiveness for the high-let radiations produced during boron neutron capture irradiations of the 9l rat gliosarcoma in vitro and in vivo. Int. J. Radiat. Oncol. Biol. Phys. 27, 1121–1129 (1993).
pubmed: 8262837 doi: 10.1016/0360-3016(93)90533-2
Fukunaga, H., Matsuya, Y., Tokuuye, K. & Omura, M. Implications of radiation microdosimetry for accelerator-based boron neutron capture therapy: A radiobiological perspective. Br. J. Radiol. 93, 20200311 (2020).
pubmed: 32374629 pmcid: 7336073 doi: 10.1259/bjr.20200311
Farr, L. E., Sweet, W. H., Locksley, H. B. & Robertson, J. S. Neutron capture therapy of gliomas using boron-10. Trans. Am. Neurol. Assoc. 79, 110–113 (1954).
Archambeau, J. O. The effect of increasing exposures of the
doi: 10.1148/10.1148/94.1.179
Mishima, Y. et al. Treatment of malignant melanoma by single thermal neutron capture therapy with melanoma-seeking
doi: 10.1016/S0140-6736(89)90567-9
Nomoto, T. et al. Poly(vinyl alcohol) boosting therapeutic potential of p-boronophenylalanine in neutron capture therapy by modulating metabolism. Sci. Adv. 6, eaaz1722 (2020).
pubmed: 32010792 pmcid: 6976296 doi: 10.1126/sciadv.aaz1722
International Atomic Energy Agency. Current status of neutron capture therapy. IAEA-TECDOC-1223. Vienna, Austria: IAEA (2001).
Suzuki, M. Boron neutron capture therapy (BNCT): A unique role in radiotherapy with a view to entering the accelerator-based BNCT era. Int. J. Clin. Oncol. 25, 43–50 (2020).
pubmed: 31168726 doi: 10.1007/s10147-019-01480-4
Yoshino, K. et al. Improvement of solubility of p-boronophenylalanine by complex formation with monosaccharides. Strahlenther. Onkol. 165, 127–129 (1989).
pubmed: 2928932
Fukuda, H. & Hiratsuka, J. Pharmacokinetics of
pubmed: 32823081 doi: 10.1016/j.apradiso.2020.109308
Matsuya, Y., Fukunaga, H., Omura, M. & Date, H. A model for estimating dose-rate effects on cell-killing of human melanoma after boron neutron capture therapy. Cells. 9, 1117 (2020).
pubmed: 32365916 pmcid: 7290789 doi: 10.3390/cells9051117
Sato, T., Masunaga, S., Kumada, H. & Hamada, N. Microdosimetric modeling of biological effectiveness for boron neutron capture therapy considering intra- and intercellular heterogeneity in
pubmed: 29343841 pmcid: 5772701 doi: 10.1038/s41598-017-18871-0
Yoshida, F. et al. Cell cycle dependence of boron uptake from two boron compounds used for clinical neutron capture therapy. Cancer Lett. 187, 135–141 (2002).
pubmed: 12359361 doi: 10.1016/S0304-3835(02)00380-4
Somogyi, G., Grabisch, K., Scherzer, R. & Enge, W. Revision of the concept of registration threshold in plastic track detector. Nucl. Instrum. Methods. 134, 129–141 (1976).
doi: 10.1016/0029-554X(76)90133-6
Kusumoto, T. & Ogawara, R. Radiation chemical yield of hydroxyl radicals for accelerator-based boron neutron capture therapy: Dose assessment of
pubmed: 30896280 doi: 10.1667/RR15318.1
Hihara, T. et al. Discriminative detection of laser-accelerated multi-MeV carbon ions utilizing solid state nuclear track detectors. Sci. Rep. 11, 16283 (2021).
pubmed: 34381072 pmcid: 8358032 doi: 10.1038/s41598-021-92300-1
Matsuya, Y. et al. Features of accelerator-based neutron source for boron neutron capture therapy calculated by particle and heavy ion transport code system (PHITS). AIP Adv. 12, 025013 (2022).
doi: 10.1063/5.0077782
Sakaue-Sawano, A. et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell. 132, 487–498 (2008).
pubmed: 18267078 doi: 10.1016/j.cell.2007.12.033
Sakaue-Sawano, A. & Miyawaki, A. Visualizing spatiotemporal dynamics of multicellular cell-cycle progressions with Fucci technology. Cold Spring Harb. Protoc. 2014(5), 080408 (2014).
doi: 10.1101/pdb.prot080408
Saga, R. et al. Translational study for stereotactic body radiotherapy against non-small cell lung cancer, including oligometastases, considering cancer stem-like cells enable predicting clinical outcome from in vitro data. Radiother. Oncol. 181, 109444 (2023).
pubmed: 37011969 doi: 10.1016/j.radonc.2022.109444
Morita, N. Marked low skin reaction of boron neutron capture therapy in melanoma-bearing hamster in comparison with single-dose electron beam at a tumor control dose. Kawasaki Med. J. 1–2, 9–17 (2004).
Baba, M. et al. Development of monoenergetic neutron calibration fields between 8 keV and 15 MeV. Nucl. Instrum. Methods Phys. Res. Sect. A 376, 115–123 (1996).
doi: 10.1016/0168-9002(96)00190-8
Ishikawa, M., Tanaka, K., Endo, S. & Hoshi, M. Application of an ultraminiature thermal neutron monitor for irradiation field study of accelerator-based neutron capture therapy. J. Radiat. Res. 2015(56), 391–396 (2015).
doi: 10.1093/jrr/rru112
Sato, T. et al. Recent improvements of the particle and Heavy Ion transport code system—PHITS version 3.33. J. Nucl. Sci. Technol. 61(1), 127–135 (2023).
doi: 10.1080/00223131.2023.2275736
Ohnish, S. Gxsview: Geometry and cross section viewer for calculating radiation transport. SoftwareX. 14, 100681 (2021).
doi: 10.1016/j.softx.2021.100681
Kunieda, S. et al. Overview of JENDL-40/HE and benchmark calculation. In JAEA-Conf. 2016-004, vol. 4 41–46 (2016).
Matsuda, N., Kunieda, S., Okamoto, T., Tada, K. & Konno, C. ACE library of JENDL-4.0/HE. Prog. Nucl. Sci. Technol. 6, 225–229 (2019).
doi: 10.15669/pnst.6.225
Hirayama, H. et al. The EGS5 Code System; Office of Scientific and Technical Information (OSTI): Oak Ridge, TN (2005).
Ogawa, T., Sato, T., Hashimoto, S. & Niita, K. Development of a reaction ejectile sampling algorithm to recover kinematic correlations from inclusive cross-section data in Monte-Carlo particle transport simulations. Nucl. Instrum. Methods Phys. Res. Sect. A 763, 575–590 (2014).
doi: 10.1016/j.nima.2014.06.088
Ogawara, R., Kusumoto, T., Konishi, T., Hamano, T. & Kodaira, S. Detection of alpha and
doi: 10.1016/j.nimb.2020.01.030
Rasband, W. S. ImageJ. U.S. National Institutes of Health, Bethesda, MD, 1997–2007. http://rsb.info.nih.gov/ij/ (2022).
Abramoff, M. D., Magelhaes, P. J. & Ram, S. J. Image processing with ImageJ. Biophoton. Int. 11(7), 36–42 (2004).
Kase, Y. et al. Microdosimetric calculation of relative biological effectiveness for design of therapeutic proton beams. J. Radiat. Res. 54, 485–493 (2013).
pubmed: 23179376 doi: 10.1093/jrr/rrs110
ICRU. Microdosimetry; Report 36; International Commission on Radiation Units and Measurements: Rockville, MD, USA (1983).
Fertil, B., Dertinger, H., Courdi, A. & Malaise, E. P. Mean inactivation dose: A useful concept for intercomparison of human cell survival curves. Radiat. Res. 178, 237–243 (2012).
doi: 10.1667/RRAV20.1
ICRU, Quantitative concepts and dosimetry in radobiology, Report No. 30, International Commission on Radiation Units and Measurements, Washington, DC (1979).
Sato, T., Watanabe, R. & Niita, K. Development of a calculation method for estimating specific energy distribution in complex radiation fields. Radiat. Prot. Dosim. 122, 41–45 (2006).
doi: 10.1093/rpd/ncl407
Sato, T., Kase, Y., Watanabe, R., Niita, K. & Sihver, L. Biological dose estimation for charged-particle therapy using an improved PHITS code coupled with a microdosimetric kinetic model. Radiat. Res. 171, 107–117 (2009).
pubmed: 19138056 doi: 10.1667/RR1510.1
Seino, R., Uno, H., Prise, K. M. & Fukunaga, H. Cell cycle dependence of cell survival following exposure to X-rays in synchronous HeLa cells expressing fluorescent ubiquitination-based cell cycle indicators. Biomed. Res. 45(1), 25–31 (2023).
doi: 10.2220/biomedres.45.25
Matsuya, Y., Kimura, T. & Date, H. Markov chain Monte Carlo analysis for the selection of a cell-killing model under high-dose rate irradiation. Med. Phys. 44, 5522–5532 (2017).
pubmed: 28786486 doi: 10.1002/mp.12508
Fantidis, J. G. Beam shaping assembly study for BNCT facility based on a 2.5 MeV proton accelerator on Li target. J. Theo. Appl. Phys. 12, 249–256 (2018).
doi: 10.1007/s40094-018-0312-1
Butterworth, K. T. et al. Out-of-field cell survival following exposure to intensity modulated radiation fields. Int. J. Radiat. Oncol. Biol. Phys. 79(5), 1516–1522 (2011).
pubmed: 21277116 pmcid: 3061203 doi: 10.1016/j.ijrobp.2010.11.034
Sato, S., Rancourt, A., Sato, Y. & Satoh, M. S. Single-cell lineage tracking analysis reveals that an established cell line comprises putative cancer stem cells and their heterogeneous progeny. Sci. Rep. 6, 23328 (2016).
pubmed: 27003384 pmcid: 4802345 doi: 10.1038/srep23328
LaHann, T. R. et al. Bioavailability of intravenous formulations of p-boronophenylalanine in dog and rat. In Advances in Neutron Capture Therapy (eds Soloway, A. H. et al.) 585–589 (Springer, 1993).
doi: 10.1007/978-1-4615-2978-1_118
Wongthai, P. et al. Boronophenylalanine, a boron delivery agent for boron neutron capture therapy, is transported by ATB
pubmed: 25580517 pmcid: 4376436 doi: 10.1111/cas.12602
Nomoto, T. et al. Fructose-functionalized polymers to enhance therapeutic potential of p-boronophenylalanine for neutron capture therapy. J. Controlled Release 332, 184–193 (2021).
doi: 10.1016/j.jconrel.2021.02.021
Parisi, A. et al. Development of a new microdosimetric biological weighting function for the RBE
pubmed: 33274727 doi: 10.1088/1361-6560/abbf96
Chen, Y., Li, J., Li, C., Qiu, R. & Wu, Z. A modified microdosimetric kinetic model for relative biological effectiveness calculation. Phys. Med. Biol. 63, 015008 (2018).
doi: 10.1088/1361-6560/aa9a68
Parisi, A., Furutani, K. M. & Beltran, C. J. The Mayo Clinic Florida microdosimetric kinetic model of clonogenic survival: Formalism and first benchmark against in vitro and in silico data. Phys. Med. Biol. 67, 185013 (2022).
doi: 10.1088/1361-6560/ac7375
Kato, A. T. et al. In vitro characterization of cells derived from chordoma cell line U-CH1 following treatment with X-rays, heavy ions and chemotherapeutic drugs. Radiat. Oncol. 6, 116 (2011).
pubmed: 21914223 pmcid: 3182904 doi: 10.1186/1748-717X-6-116
Goodhead, D. T. et al. Direct comparison between protons and alpha-particles of the same LET. I: Irradiation methods and inactivation of asynchronous V79, HeLa and C3HT1/2 cells. Int. J. Radiat. Biol. 61, 611–624 (1992).
pubmed: 1349625 doi: 10.1080/09553009214551421
Deering, R. A. & Rice, R. Heavy ion irradiation of HeLa cells. Radiat. Res. 17, 774–786 (1962).
pubmed: 14026388 doi: 10.2307/3571225
Ito, H. et al. Carbon beam irradiation of monolayer cells. Nippon Acta. Radiol. 53, 321–328 (1993).
pubmed: 8474866
Li, W.-J. et al. RBE of cells irradiated by carbon ions. High Ener. Phys. Nucl. Phys. 26(7), 742–746 (2002).
Kaur, H., Pujari, G., Semwal, M. K., Sarma, A. & Avasthi, D. K. In vitro studies on radiosensitization effect of glucose capped gold nanoparticles in photon and ion irradiation of HeLa cells. Nucl. Instr. Methods Phys. Res. Sect. B 301, 7–11 (2013).
doi: 10.1016/j.nimb.2013.02.015
Friedrich, T., Scholz, U., Elsässer, T., Durante, M. & Scholz, M. Systematic analysis of RBE and related quantities using a database of cell survival experiments with ion beam irradiation. J. Radiat. Res. 54(3), 494–514 (2013).
pubmed: 23266948 doi: 10.1093/jrr/rrs114
Davis, M. A. & Little, J. B. Relative biological effectiveness of the
pubmed: 5460394 doi: 10.2307/3573228
Sinclair, W. K. & Morton, R. A. X-ray sensitivity during the cell generation cycle of cultured Chinese Hamster cells. Radiat. Res. 29, 450–474 (1966).
pubmed: 5924188 doi: 10.2307/3572025
Matsuya, Y. et al. Investigation of dose-rate effects and cell-cycle distribution under protracted exposure to ionizing radiation for various dose-rates. Sci. Rep. 8, 8287 (2018).
pubmed: 29844494 pmcid: 5974424 doi: 10.1038/s41598-018-26556-5
Mori, R., Matsuya, Y., Yoshii, Y. & Date, H. Estimation of the radiation-induced DNA double-strand breaks number by considering cell cycle and absorbed dose per cell nucleus. J. Radiat. Res. 59(3), 253–260 (2018).
pubmed: 29800455 pmcid: 5967466 doi: 10.1093/jrr/rrx097
Matsuya, Y., Sato, T., Nakamura, R., Naijo, S. & Date, H. A theoretical cell-killing model to evaluate oxygen enhancement ratios at DNA damage and cell survival endpoints in radiation therapy. Phys. Med. Biol. 65, 095006 (2020).
pubmed: 32135526 doi: 10.1088/1361-6560/ab7d14
Brandsma, I. & van Gent, D. C. Pathway choice in DNA double strand break repair: Observations of a balancing act. Genome Integrity. 3, 9 (2012).
pubmed: 23181949 pmcid: 3557175 doi: 10.1186/2041-9414-3-9
Mao, Z., Bozzella, M., Seluanov, A. & Gorbunova, V. DNA repair by nonhomologous end joining and homologous recombination during cell cycle in human cells. Cell Cycle. 7(18), 2902–2906 (2008).
pubmed: 18769152 doi: 10.4161/cc.7.18.6679
Fukuda, H. et al. Boron neutron capture therapy of malignant melanoma using
pubmed: 8184019 doi: 10.2307/3578693

Auteurs

Yusuke Matsuya (Y)

Nuclear Science and Engineering Center, Japan Atomic Energy Agency, Tokai, 319-1195, Japan. matsuya.yusuke@hs.hokudai.ac.jp.
Faculty of Health Sciences, Hokkaido University, Sapporo, 060-0812, Japan. matsuya.yusuke@hs.hokudai.ac.jp.

Tatsuhiko Sato (T)

Nuclear Science and Engineering Center, Japan Atomic Energy Agency, Tokai, 319-1195, Japan.

Tamon Kusumoto (T)

National Institutes for Quantum and Radiological Science and Technology, Chiba, 263-8555, Japan.

Yoshie Yachi (Y)

Graduate School of Health Sciences, Hokkaido University, Sapporo, 060-0812, Japan.

Ryosuke Seino (R)

Graduate School of Health Sciences, Hokkaido University, Sapporo, 060-0812, Japan.

Misako Miwa (M)

Department of Quantum Science and Energy Engineering, Graduate School of Engineering, Tohoku University, Sendai, 980-8579, Japan.

Masayori Ishikawa (M)

Faculty of Health Sciences, Hokkaido University, Sapporo, 060-0812, Japan.

Shigeo Matsuyama (S)

Department of Quantum Science and Energy Engineering, Graduate School of Engineering, Tohoku University, Sendai, 980-8579, Japan.

Hisanori Fukunaga (H)

Faculty of Health Sciences, Hokkaido University, Sapporo, 060-0812, Japan. hisanori.fukunaga@hs.hokudai.ac.jp.
Center for Environmental and Health Sciences, Hokkaido University, Sapporo, 060-0812, Japan. hisanori.fukunaga@hs.hokudai.ac.jp.
Institute of Development, Aging and Cancer, Tohoku University, Sendai, 980-8575, Japan. hisanori.fukunaga@hs.hokudai.ac.jp.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH