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Radiosensitivity of Prostate Cancer Cell Lines for Irradiation from Beta Particle-Emitting Radionuclide 177Lu Compared to Alpha Particles and Gamma Rays

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Radiosensitivity of Prostate Cancer Cell Lines for Irradiation from Beta Particle-Emitting Radionuclide 177Lu Compared to Alpha Particles and Gamma Rays ANTICANCER RESEARCH 36: 103-110 (2016) Radiosensitivity of Prostate Cancer Cell Lines for Irradiation from Beta Particle-emitting Radionuclide 177Lu Compared to Alpha Particles and Gamma Rays JÖRGEN ELGQVIST1, OSKAR VILHELMSSON TIMMERMAND1, ERIK LARSSON2 and SVEN-ERIK STRAND1 1Department of Medical Radiation Physics, Institute of Clinical Sciences, Lund University, Lund, Sweden; 2Department of Radiation Physics, Skåne University Hospital, Lund, Sweden Abstract. Aim: The purpose of the present study was to Conclusion: The surviving fractions after irradiation using beta investigate the radiosensitivity of the prostate cancer cell lines particles or gamma rays did not differ significantly at the LNCaP, DU145, and PC3 when irradiated with beta particles absorbed dose levels and dose rates used. Irradiation using emitted from 177Lu, and to compare the effect with irradiation alpha particles led to a high level of cell killing. The results using alpha particles or gamma rays. Materials and Methods: show that the beta-particle emitter 177Lu as well as alpha- Cells were irradiated with beta particles emitted from 177Lu, particles are both good candidates for radionuclide-therapy alpha particles from 241Am, or gamma rays from 137Cs. A non- applications in the treatment of prostate cancer. specific polyclonal antibody was labeled with 177Lu and used to irradiate cells in suspension with beta particles. A previously Prostate cancer (PCa) is one of the most frequently described in-house developed alpha-particle irradiator based diagnosed type of cancer in men, at the same time being the on a 241Am source was used to irradiate cells with alpha second leading cause of cancer-related mortality in the USA. particles. External gamma-ray irradiation was achieved using According to the International Agency for Research on a standard 137Cs irradiator. Cells were irradiated to absorbed Cancer approximately 345,000 men were diagnosed with doses equal to 0, 0.5, 1, 2, 4, 6, 8, or 10 Gy. The absorbed PCa in Europe during 2012, and 72,000 men died of the doses were calculated as mean absorbed doses. For evaluation disease. The corresponding numbers for the USA for 2012 of cell survival, the tetrazolium-based WST-1 assay was used. were 233,000 and 30,000, respectively. The American Cancer After irradiation, WST-1 was added to the cell solutions, Society estimates that 221,000 men will be diagnosed with incubated, and then measured for level of absorbance at PCa during 2015 in the USA, and approximately 28,000 of 450 nm, indicating the live and viable cells. Results: LNCaP, them will die from the disease (1). In Europe, PCa is the DU145, and PC3 cell lines all had similar patterns of survival most commonly diagnosed cancer type. for the different radiation types. No significant difference in Therefore, improvement of already established therapies surviving fractions were observed between cells treated with and the development of new ones is of utmost importance. beta-particle and gamma-ray irradiation, represented for Prostate cancer is most often treated using radiotherapy example by the surviving fraction values (mean±SD) at 2, 6, (external irradiation or brachytherapy), chemotherapy or and 10 Gy (SF2, SF6, and SF10) for DU145 after beta-particle radical prostectomy, with or without androgen-deprivation irradiation: 0.700±0.090, 0.186±0.050 and 0.056±0.010, therapy (2). Regarding radiotherapy, almost 30% treated by respectively. A strong radiosensitivity to alpha particles was using potentially curative absorbed dose levels relapse at the observed, with SF2 values of 0.048±0.008, 0.018±0.006 and irradiation site (3, 4), and very little is known on how certain 0.015±0.005 for LNCaP, DU145, and PC3, respectively. prostate tumor cells seem to be more radioresistant than others. As death from PCa is most often the consequence of a metastatic spread of the disease, new targeted treatment strategies, such as radionuclide therapy (RNT) based on Correspondence to: Jörgen Elgqvist, Ph.D., Associate Professor, radiolabeled specific antibodies (radioimmunotherapy) or Department of Medical Radiation Physics, Institute of Clinical peptides (peptide radionuclidetherapy) are under development Sciences, LundUniversity, Barngatan 2B, SE-221 85 Lund, Sweden. E-mail: [email protected] and could be a way forward to cure or prolong survival. In the development of such new treatments, knowledge on Key Words: Radiosensitivity, prostate cancer, beta particles, alpha radiosensitivity, and the causes of radioresistance, is important. particles, gamma rays. The area of radioimmunotherapy is progressing and has so far 0250-7005/2016 $2.00+.40 103 ANTICANCER RESEARCH 36: 103-110 (2016) resulted in two Food and Drug Administration (FDA)- the radiosensitivity of cells in order to obtain as broad a picture approved drugs using beta-particle emitters: Zevalin® and as possible as to how specific cell types behave when irradiated. Bexxar® (90Y Ibritumomab and 131I Tositumomab, In the context of radiosensitivity, a comment on respectively), both used to treat refractory low-grade B-cell radiosensitizers and the determinants of the radiosensitivity of non-Hodgkin lymphomas (5-8). Another newly FDA-approved PCa is important. Examples of radiosensitizers of PCa are drug is Xofigo®, based on the alpha-particle emitter 223Ra, is baicalein and BMD122, both inhibitors of platelet-type 12- aimed for RNT of metastatic PCa (9). Another very intriguing lipoxygenases (12-LOX), which play an important role in the future therapy approach for avoiding normal organ toxicity progression of PCa (15). It was recently shown that both these and increasing the absorbed dose to the tumor is to combine sensitizers increase the radiosensitivity of PCa cells, without RNT with external beam therapy (10). Herein, knowledge of resulting in the same effect on normal cells (16). For the the tumor radiosensitivity will be of utmost importance in androgen-dependent LNCaP and androgen-independent PC3 cell calculating the prescribed absorbed doses (11). lines, it has been shown that these 12-LOX inhibitors, when Generally, radiosensitivity is related to the rate of cell division combined with radiation, have a synergistic inhibitory effect on and the level of cell differentiation. Cells that are most survival in vitro, and also resulted in a significantly reduced radiosensitive in general terms are those having a high metabolic tumor growth in vivo (16). Another interesting approach rate, good access to nutrients, and a relatively high division rate, regarding radiosensitizing relates to growth factors, which are i.e. highly proliferative, actively dividing cells (12). But also cells the basic regulators of differentiation, cellular proliferation, and not fully mature or less differentiated (e.g. stem cells or stem neoplastic transformation (17). Poor prognosis and advanced cell-like cells) have increased radiosensitivity (12). The part of PCa are often associated with expression of the epidermal the cell cycle that is least sensitive to radiation is the S-phase growth factor receptor (EGFR) (18, 19). It has been shown that (especially the latter part of the S-phase), at which the synthesis EGFR expression is high in many PCa cells, and that EGFR and replication of DNA occurs. The most radiosensitive parts of activation reduces the radiosensitivity of tumor cells in general the cell cycle are the G2- and M-phase, at which the chromatin (20-23). Besides being associated with resistance to radiation is condensed and the cell starts to divide, respectively. However, therapy, EGFR expression is also important for processes such these general statements on radiosensitivity cannot be made as angiogenesis, inhibition of apoptosis, and metastasis (17, 24, specific for certain cell types. Therefore, investigations, such as 25). Therefore, EGFR is a relevant candidate for targeted the present study, need to be performed in order to determine the therapies. A number of EGFR-blocking antibodies have been radiosensitivity of specific cells. Moreover, as radiosensitivity is developed, e.g. cetuximab (C225), which significantly enhances dependent not only on the cells, but also on which type of radiosensitivity and synergistically inhibits cell growth in radiation is being used, it is important to investigate the combination with radiation (17, 26-28). Regarding specific radiosensitivity to different types of radiation, e.g. beta particles, determinants of the radiosensitivity of PCa, the tumor-suppressor alpha-particles, or gamma rays, all used in this study. protein retinoblastoma (RB) should be mentioned. This protein Alpha particles differ, for example, from beta particles and regulates cell proliferation and has proven to be inactivated in gamma rays in their ability to create densely ionizing tracks 25-30% of all PCa, leading to a castration-resistant phenotype when passing through tissue (13). This characteristic is of PCa (29). Loss of RB also reduces the ability of the cell to expressed as the linear energy transfer (LET), which indicates repair DNA damage induced by radiation, by down-regulating the ability of radiation to transfer energy to the surrounding G1-S cell-cycle arrest, and might therefore be used as a media per unit travelled length (14). Typically, alpha particles biomarker for prediction regarding response to radiation (29). have an average LET of ~100 keV/μm, depending both on the Another determinant for the radiosensitivity of tumors in general, initial alpha-particle energy as well on where on the Bragg but also for PCa, is the TP53 gene or the p53 protein level, for curve the individual alpha-particle is along its ionization track. which a study has shown that the wild-type TP53 is a stronger Beta particles in comparison, emitted for example from determinant for radiosensitivity than mutant TP53 (30). radionuclides such as 177Lu, 131I, or 90Y, have an LET in range In the present study, we investigated the radiosensitivity of 0.2-0.3 keV/μm. The same LET range is also applicable of the PCa cell lines LNCaP, DU145, and PC3 when when considering gamma rays, e.g.
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