Nanodiamond Effects on Cancer Cell Radiosensitivity: The Interplay between Their Chemical/Physical Characteristics and the Irradiation Energy

Varzi, Veronica; Fratini, Emiliano; Falconieri, Mauro; Giovannini, Daniela; Cemmi, Alessia; Scifo, Jessica; Di Sarcina, Ilaria; Aprà, Pietro; Sturari, Sofia; Mino, Lorenzo; Tomagra, Giulia; Infusino, Erminia; Landoni, Valeria; Marino, Carmela; Mancuso, Mariateresa; Picollo, Federico; Pazzaglia, Simonetta

doi:10.3390/ijms242316622

Open AccessArticle

Nanodiamond Effects on Cancer Cell Radiosensitivity: The Interplay between Their Chemical/Physical Characteristics and the Irradiation Energy

by

Veronica Varzi

^1,2,3,†

,

Emiliano Fratini

^2,†

,

Mauro Falconieri

⁴

,

Daniela Giovannini

²,

Alessia Cemmi

⁵

,

Jessica Scifo

⁵

,

Ilaria Di Sarcina

⁵,

Pietro Aprà

^1,3,

Sofia Sturari

^1,3,

Lorenzo Mino

^3,6

,

Giulia Tomagra

⁷

,

Erminia Infusino

⁸,

Valeria Landoni

⁸

,

Carmela Marino

²,

Mariateresa Mancuso

²

,

Federico Picollo

^1,3,*

and

Simonetta Pazzaglia

^2,*

¹

Physics Department, National Institute of Nuclear Physics, Section of Turin, University of Turin, Via P. Giuria 1, 10125 Turin, Italy

²

Laboratory of Biomedical Technologies, Italian National Agency for New Technologies, Energy and Sustainable Economic Development (ENEA), Casaccia Research Centre, Via Anguillarese 301, 00123 Rome, Italy

³

Nanomaterials for Industry and Sustainability (NIS) Inter-Departmental Centre, University of Turin, Via Quarello 15/A, 10125 Turin, Italy

⁴

Fusion and Technology for Nuclear Safety and Security Department, Italian National Agency for New Technologies, Energy and Sustainable Economic Development (ENEA), Casaccia Research Centre, Via Anguillarese 301, 00123 Rome, Italy

⁵

Innovative Nuclear Systems Laboratory, Italian National Agency for New Technologies, Energy and Sustainable Economic Development (ENEA), Casaccia Research Centre, Via Anguillarese 301, 00123 Rome, Italy

⁶

Chemistry Department, University of Turin, Via P. Giuria 7, 10125 Turin, Italy

⁷

Drug Science and Technology Department, University of Turin, Corso Raffaello 30, 10125 Turin, Italy

⁸

Medical Physics Laboratory, IRCCS Istituto Nazionale Tumori Regina Elena, Via Elio Chianesi 53, 00144 Rome, Italy

^*

Authors to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Int. J. Mol. Sci. 2023, 24(23), 16622; https://doi.org/10.3390/ijms242316622

Submission received: 29 September 2023 / Revised: 6 November 2023 / Accepted: 15 November 2023 / Published: 22 November 2023

(This article belongs to the Special Issue Nanomaterial-Based Radiosensitization 3.0)

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Abstract

Nanoparticles are being increasingly studied to enhance radiation effects. Among them, nanodiamonds (NDs) are taken into great consideration due to their low toxicity, inertness, chemical stability, and the possibility of surface functionalization. The objective of this study is to explore the influence of the chemical/physical properties of NDs on cellular radiosensitivity to combined treatments with radiation beams of different energies. DAOY, a human radioresistant medulloblastoma cell line was treated with NDs—differing for surface modifications [hydrogenated (H-NDs) and oxidized (OX-NDs)], size, and concentration—and analysed for (i) ND internalization and intracellular localization, (ii) clonogenic survival after combined treatment with different radiation beam energies and (iii) DNA damage and apoptosis, to explore the nature of ND–radiation biological interactions. Results show that chemical/physical characteristics of NDs are crucial in determining cell toxicity, with hydrogenated NDs (H-NDs) decreasing either cellular viability when administered alone, or cell survival when combined with radiation, depending on ND size and concentration, while OX-NDs do not. Also, irradiation at high energy (γ-rays at 1.25 MeV), in combination with H-NDs, is more efficient in eliciting radiosensitisation when compared to irradiation at lower energy (X-rays at 250 kVp). Finally, the molecular mechanisms of ND radiosensitisation was addressed, demonstrating that cell killing is mediated by the induction of Caspase-3-dependent apoptosis that is independent to DNA damage. Identifying the optimal combination of ND characteristics and radiation energy has the potential to offer a promising therapeutic strategy for tackling radioresistant cancers using H-NDs in conjunction with high-energy radiation.

Keywords: nanodiamonds; radiation sensitizer; medulloblastoma; radiation therapy; DNA damage; apoptosis

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MDPI and ACS Style

Varzi, V.; Fratini, E.; Falconieri, M.; Giovannini, D.; Cemmi, A.; Scifo, J.; Di Sarcina, I.; Aprà, P.; Sturari, S.; Mino, L.; et al. Nanodiamond Effects on Cancer Cell Radiosensitivity: The Interplay between Their Chemical/Physical Characteristics and the Irradiation Energy. Int. J. Mol. Sci. 2023, 24, 16622. https://doi.org/10.3390/ijms242316622

AMA Style

Varzi V, Fratini E, Falconieri M, Giovannini D, Cemmi A, Scifo J, Di Sarcina I, Aprà P, Sturari S, Mino L, et al. Nanodiamond Effects on Cancer Cell Radiosensitivity: The Interplay between Their Chemical/Physical Characteristics and the Irradiation Energy. International Journal of Molecular Sciences. 2023; 24(23):16622. https://doi.org/10.3390/ijms242316622

Chicago/Turabian Style

Varzi, Veronica, Emiliano Fratini, Mauro Falconieri, Daniela Giovannini, Alessia Cemmi, Jessica Scifo, Ilaria Di Sarcina, Pietro Aprà, Sofia Sturari, Lorenzo Mino, and et al. 2023. "Nanodiamond Effects on Cancer Cell Radiosensitivity: The Interplay between Their Chemical/Physical Characteristics and the Irradiation Energy" International Journal of Molecular Sciences 24, no. 23: 16622. https://doi.org/10.3390/ijms242316622

APA Style

Varzi, V., Fratini, E., Falconieri, M., Giovannini, D., Cemmi, A., Scifo, J., Di Sarcina, I., Aprà, P., Sturari, S., Mino, L., Tomagra, G., Infusino, E., Landoni, V., Marino, C., Mancuso, M., Picollo, F., & Pazzaglia, S. (2023). Nanodiamond Effects on Cancer Cell Radiosensitivity: The Interplay between Their Chemical/Physical Characteristics and the Irradiation Energy. International Journal of Molecular Sciences, 24(23), 16622. https://doi.org/10.3390/ijms242316622

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Nanodiamond Effects on Cancer Cell Radiosensitivity: The Interplay between Their Chemical/Physical Characteristics and the Irradiation Energy

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