The Investigation of Efficiency of Pheophorbide-A Mediated Sonodynamic Therapy on Prostate Cancer 3D Cell Culture Model
Year 2024,
Volume: 10 Issue: 1, 47 - 56, 30.06.2024
Mehran Aksel
,
Ömer Erdoğan
,
Mehmet Bilgin
Abstract
The aim of this study is to investigate the effectiveness of fjorbid-a-mediated sono-dynamic therapy in a 3D prostate cancer cell model. The effect of fjorbid-a-mediated sonodynamic therapy was examined by crystal violet staining in a 3D cell culture model created using human PC3 cells. Furthermore, apoptosis mechanisms were an-alyzed using Hoechst and propidium iodide staining (HOPI), and the levels of total oxidant (TOS) and total antioxidant (TAS) were assessed biochemically using cor-responding kits. Crystal violet staining was employed to assess the effectiveness of sonodynamic therapy facilitated by pheophorbide-a, revealing a substantial 75% re-duction in the viability of cancer cells. HOPI staining results indicated that there was no noteworthy increment in the count of apoptotic cells in the control, drug-only, or ultrasound-only groups. However, a remarkable 80% increase in apoptotic cell count was observed following pheophorbide-a-mediated sonodynamic treatment. Addi-tionally, biochemical measurements demonstrated elevated levels of Total Oxidant Status (TOS) and decreased levels of Total Antioxidant Status (TAS) in the treatment groups in comparison to the control groups. Based on the acquired data, it was estab-lished that pheophorbide-a-induced sonodynamic therapy for prostate cancer treat-ment diminishes cell viability by inducing apoptosis through oxidative stress in a 3D cell culture system.
Ethical Statement
Etik kurul onayına ihtiyaç yoktur.
Supporting Institution
Adnan Menderes Üniversitesi
References
- Siegel, R. L., Miller, K. D. and Jemal, A. (2020), Cancer statistics, 2020. CA A Cancer J Clin, 70(1), 7-30.
- Šrajer Gajdošik, M., Hixson, D. C., Brilliant, K. E., Yang, D., De Paepe, M. E., Josić, D., and Mills, D. R. (2018). Soft agar-based selection of spontaneously transformed rat prostate epi-thelial cells with highly tumorigenic characteristics. Experimental and molecular pathology, 105(1), 89–97.
- Abe-Fukasawa, N., Otsuka, K., Aihara, A. et al. (2018). Novel 3D Liquid Cell Culture Method for Anchorage-independent Cell Growth, Cell Imaging and Automated Drug Screening. Sci Rep 8, 3627.
- Erdoğan, Ö., Paşa, S., and Cevik, O. (2021). Green Synthesis and Characterization of Anti-cancer Effected Silver Nanoparticles with Silverberry (Elaeagnus angustifolia) Fruit Aqueous Extract. International Journal of Pure and Applied Sciences, 7(3), 391-400.
- Demir, S., Pekdemir, S., Keser, S., Karatepe, A., Koparir, M. and Karatepe, M. (2021). An-tioxidant and antiproliferative properties of some 2- (4h- [1,2,4] Triazol-3-Yl-sulfanyl) -acetamide derivatives. International Journal of Pure and Applied Sciences, 7(3), 472-479.
- Umemura, K., Yumita, N., Nishigaki, R., Umemura, S.I. (1996). Sonodynamically induced antitumor effect of pheophorbide a. Cancer Lett. 1996, 102, 151-157.
- Yumita, N., Sasaki, K., Umemura, S., and Nishigaki, R. (1996). Sonodynamically induced antitumor effect of a gallium-porphyrin complex, ATX-70. Japanese journal of cancer research: Gann, 87(3), 310–316.
- Baker, K. G., Robertson, V. J., and Duck, F. A. (2001). A review of therapeutic ultrasound: biophysical effects. Physical therapy, 81(7), 1351–1358.
- Pang X., Xu C., Jiang Y., Xiao Q., Leung A.W. (2016). Natural products in the discovery of novel sonosensitizers. Pharmacol. Ther., 162, 144–151.
- Trendowski, M. (2014). The promise of sonodynamic therapy. Cancer and Metastasis Reviews, 33, 143–160.
- Shibaguchi, H., Tsuru, H., Kuroki, M., and Kuroki, M. (2011). Sonodynamic cancer therapy: a non-invasive and repeatable approach using low-intensity ultrasound with a sonosensitizer. Anticancer research, 31(7), 2425–2429.
- Patil, S.M. and Kunda, N.K. (2022). Nisin ZP, an Antimicrobial Peptide, Induces Cell Death and Inhibits Non-Small Cell Lung Cancer (NSCLC) Progression in vitro in 2D and 3D Cell Culture. Pharm Res., 39, 2859–2870.
- Jacks, T., and Weinberg, R. A. (2002). Taking the study of cancer cell survival to a new di-mension. Cell, 111(7), 923–925.
- Breslin, S., & O'Driscoll, L. (2013). Three-dimensional cell culture: the missing link in drug discovery. Drug discovery today, 18(5-6), 240–249.
- Atat, O. E., Farzaneh, Z., Pourhamzeh, M., Taki, F., Abi-Habib, R., Vosough, M., and El-Sibai, M. (2022). 3D modeling in cancer studies. Human cell, 35(1), 23–36.
- Grayson, K. A., Jyotsana, N., Ortiz-Otero, N., King, M. R. (2021). Overcoming TRAIL-resistance by sensitizing prostate cancer 3D spheroids with taxanes. PLoS One, 16(3), e0246733.
- Safari, F., Shakery, T. and Sayadamin, N. (2021). Evaluating the effect of secretome of human amniotic mesenchymal stromal cells on apoptosis induction and epithelial-mesenchymal tran-sition inhibition in LNCaP prostate cancer cells based on 2D and 3D cell culture models. Cell Biochem Funct, 39(6), 813-820.
- Di Donato, M., Zamagni, A., Galasso, G., Di Zazzo, E., Giovannelli, P., Barone, M.V., Zanoni, M., Gunelli, R., Costantini, M., Auricchio, F., Migliaccio, A., Tesei, A. and Castoria, G. (2021). Correction to: The androgen receptor/filamin A complex as a target in prostate cancer micro-environment. Cell Death Dis, 12(3), 272.
- Aizer, A. A., Gu, X., Chen, M. H., Choueiri, T. K., Martin, N. E., Efstathiou, J. A., Hyatt, A. S., Graham, P. L., Trinh, Q. D., Hu, J. C. and Nguyen, P. L. (2015). Cost implications and com-plications of overtreatment of low-risk prostate cancer in the United States. JNCCN Journal of the National Comprehensive Cancer Network, 13, 61–68.
- Collins, K., and Cheng, L. (2022). Morphologic spectrum of treatment-related changes in prostate tissue and prostate cancer: an updated review. Human pathology, 127, 56–66.
- Aksel, M., Kesmez, Ö., Yavaş, A. and Bilgin, M.D. (2021). Titaniumdioxide mediated sono-photodynamic therapy against prostate cancer. J Photochem Photobiol B, 225, 112333.
- Bilgin, M. D., Aksel, M., Degirmenci, E.H., Bozkurt Girit, O. and Ozmen, A. (2017). Efficacy of methylene blue and aliminium phthalocyanine mediated sonophotodynamic therapy on prostate cancer cell lines. Biophys J, 112, 282a–283a.
- Aksel, M., Bozkurt-Girit, O. and Bilgin, M. D. (2021). Pheophorbide a-mediated sonodynamic, photodynamic and sonophotodynamic therapies against prostate cancer. Photodiagnosis Pho-todyn Ther, 31, 101909.
- Yamaguchi, T., Kitahara, S., Kusuda, K., Okamoto, J., Horise, Y., Masamune, K., & Muragaki, Y. (2021). Current landscape of sonodynamic therapy for treating cancer. Cancers (Basel), 13(24), 6184.
- Costley, D., Mc Ewan, C., Fowley, C., McHale, A. P., Atchison, J., Nomikou, N. and Callan, J. F. (2015). Treating cancer with sonodynamic therapy: A review. International Journal of Hy-perthermia, 31(2), 107–117.
- Chen, H. J., Zhou, X. B., Wang, A. L., Zheng, B. Y., Yeh, C. K., and Huang, J. D. (2018). Synthesis and biological characterization of novel rose bengal derivatives with improved am-phiphilicity for sono-photodynamic therapy. European journal of medicinal chemistry, 145, 86–95.
- Bakhshizadeh, M., Moshirian, T., Esmaily, H., Rajabi, O., Nassirli, H., and Sazgarnia, A. (2017). Sonophotodynamic therapy mediated by liposomal zinc phthalocyanine in a colon carcinoma tumor model: Role of irradiating arrangement. Iranian journal of basic medical sciences, 20(10), 1088–1092.
- Wang, D., Wan, Z., Yang, Q., Chen, J., Liu Y., Lu, F. and Tang, J. (2022). Sonodynamical reversion of immunosuppressive microenvironment in prostate cancer via engineered exosomes. Drug Deliv, 29, 702-713.
- Jin, Z. H., Miyoshi, N., Ishiguro, K., Umemura, S., Kawabata, K., Yumita, N., Sakata, I., Takaoka, K., Udagawa, T., Nakajima, S., Tajiri, H., Ueda, K., Fukuda, M., and Kumakiri, M. (2000). Combination effect of photodynamic and sonodynamic therapy on experimental skin squamous cell carcinoma in C3H/HeN mice. The Journal of dermatology, 27(5), 294–306.
- Cho, M., Park, G. M., Kim, S. N., Amna, T., Lee, S., and Shin, W. S. (2014). Glioblasto-ma-specific anticancer activity of pheophorbide a from the edible red seaweed Grateloupia el-liptica. Journal of microbiology and biotechnology, 24(3), 346–353.
- Gheewala, T., Skwor, T., and Munirathinam, G. (2018). Photodynamic therapy using phe-ophorbide and 670nm LEDs exhibits anti-cancer effects in-vitro in androgen dependent prostate cancer. Photodiagnosis and photodynamic therapy, 21, 130–137.
- Xu, D. D., Lam, H. M., Hoeven, R., Xu, C. B., Leung, A. W. N., Cho, W. C. S. (2013). Photodynamic therapy induced cell death of hormone insensitive prostate cancer PC-3 cells with autophagic characteristics. Photodiagnosis and Photodynamic Therapy, 10, 278-287.
Year 2024,
Volume: 10 Issue: 1, 47 - 56, 30.06.2024
Mehran Aksel
,
Ömer Erdoğan
,
Mehmet Bilgin
References
- Siegel, R. L., Miller, K. D. and Jemal, A. (2020), Cancer statistics, 2020. CA A Cancer J Clin, 70(1), 7-30.
- Šrajer Gajdošik, M., Hixson, D. C., Brilliant, K. E., Yang, D., De Paepe, M. E., Josić, D., and Mills, D. R. (2018). Soft agar-based selection of spontaneously transformed rat prostate epi-thelial cells with highly tumorigenic characteristics. Experimental and molecular pathology, 105(1), 89–97.
- Abe-Fukasawa, N., Otsuka, K., Aihara, A. et al. (2018). Novel 3D Liquid Cell Culture Method for Anchorage-independent Cell Growth, Cell Imaging and Automated Drug Screening. Sci Rep 8, 3627.
- Erdoğan, Ö., Paşa, S., and Cevik, O. (2021). Green Synthesis and Characterization of Anti-cancer Effected Silver Nanoparticles with Silverberry (Elaeagnus angustifolia) Fruit Aqueous Extract. International Journal of Pure and Applied Sciences, 7(3), 391-400.
- Demir, S., Pekdemir, S., Keser, S., Karatepe, A., Koparir, M. and Karatepe, M. (2021). An-tioxidant and antiproliferative properties of some 2- (4h- [1,2,4] Triazol-3-Yl-sulfanyl) -acetamide derivatives. International Journal of Pure and Applied Sciences, 7(3), 472-479.
- Umemura, K., Yumita, N., Nishigaki, R., Umemura, S.I. (1996). Sonodynamically induced antitumor effect of pheophorbide a. Cancer Lett. 1996, 102, 151-157.
- Yumita, N., Sasaki, K., Umemura, S., and Nishigaki, R. (1996). Sonodynamically induced antitumor effect of a gallium-porphyrin complex, ATX-70. Japanese journal of cancer research: Gann, 87(3), 310–316.
- Baker, K. G., Robertson, V. J., and Duck, F. A. (2001). A review of therapeutic ultrasound: biophysical effects. Physical therapy, 81(7), 1351–1358.
- Pang X., Xu C., Jiang Y., Xiao Q., Leung A.W. (2016). Natural products in the discovery of novel sonosensitizers. Pharmacol. Ther., 162, 144–151.
- Trendowski, M. (2014). The promise of sonodynamic therapy. Cancer and Metastasis Reviews, 33, 143–160.
- Shibaguchi, H., Tsuru, H., Kuroki, M., and Kuroki, M. (2011). Sonodynamic cancer therapy: a non-invasive and repeatable approach using low-intensity ultrasound with a sonosensitizer. Anticancer research, 31(7), 2425–2429.
- Patil, S.M. and Kunda, N.K. (2022). Nisin ZP, an Antimicrobial Peptide, Induces Cell Death and Inhibits Non-Small Cell Lung Cancer (NSCLC) Progression in vitro in 2D and 3D Cell Culture. Pharm Res., 39, 2859–2870.
- Jacks, T., and Weinberg, R. A. (2002). Taking the study of cancer cell survival to a new di-mension. Cell, 111(7), 923–925.
- Breslin, S., & O'Driscoll, L. (2013). Three-dimensional cell culture: the missing link in drug discovery. Drug discovery today, 18(5-6), 240–249.
- Atat, O. E., Farzaneh, Z., Pourhamzeh, M., Taki, F., Abi-Habib, R., Vosough, M., and El-Sibai, M. (2022). 3D modeling in cancer studies. Human cell, 35(1), 23–36.
- Grayson, K. A., Jyotsana, N., Ortiz-Otero, N., King, M. R. (2021). Overcoming TRAIL-resistance by sensitizing prostate cancer 3D spheroids with taxanes. PLoS One, 16(3), e0246733.
- Safari, F., Shakery, T. and Sayadamin, N. (2021). Evaluating the effect of secretome of human amniotic mesenchymal stromal cells on apoptosis induction and epithelial-mesenchymal tran-sition inhibition in LNCaP prostate cancer cells based on 2D and 3D cell culture models. Cell Biochem Funct, 39(6), 813-820.
- Di Donato, M., Zamagni, A., Galasso, G., Di Zazzo, E., Giovannelli, P., Barone, M.V., Zanoni, M., Gunelli, R., Costantini, M., Auricchio, F., Migliaccio, A., Tesei, A. and Castoria, G. (2021). Correction to: The androgen receptor/filamin A complex as a target in prostate cancer micro-environment. Cell Death Dis, 12(3), 272.
- Aizer, A. A., Gu, X., Chen, M. H., Choueiri, T. K., Martin, N. E., Efstathiou, J. A., Hyatt, A. S., Graham, P. L., Trinh, Q. D., Hu, J. C. and Nguyen, P. L. (2015). Cost implications and com-plications of overtreatment of low-risk prostate cancer in the United States. JNCCN Journal of the National Comprehensive Cancer Network, 13, 61–68.
- Collins, K., and Cheng, L. (2022). Morphologic spectrum of treatment-related changes in prostate tissue and prostate cancer: an updated review. Human pathology, 127, 56–66.
- Aksel, M., Kesmez, Ö., Yavaş, A. and Bilgin, M.D. (2021). Titaniumdioxide mediated sono-photodynamic therapy against prostate cancer. J Photochem Photobiol B, 225, 112333.
- Bilgin, M. D., Aksel, M., Degirmenci, E.H., Bozkurt Girit, O. and Ozmen, A. (2017). Efficacy of methylene blue and aliminium phthalocyanine mediated sonophotodynamic therapy on prostate cancer cell lines. Biophys J, 112, 282a–283a.
- Aksel, M., Bozkurt-Girit, O. and Bilgin, M. D. (2021). Pheophorbide a-mediated sonodynamic, photodynamic and sonophotodynamic therapies against prostate cancer. Photodiagnosis Pho-todyn Ther, 31, 101909.
- Yamaguchi, T., Kitahara, S., Kusuda, K., Okamoto, J., Horise, Y., Masamune, K., & Muragaki, Y. (2021). Current landscape of sonodynamic therapy for treating cancer. Cancers (Basel), 13(24), 6184.
- Costley, D., Mc Ewan, C., Fowley, C., McHale, A. P., Atchison, J., Nomikou, N. and Callan, J. F. (2015). Treating cancer with sonodynamic therapy: A review. International Journal of Hy-perthermia, 31(2), 107–117.
- Chen, H. J., Zhou, X. B., Wang, A. L., Zheng, B. Y., Yeh, C. K., and Huang, J. D. (2018). Synthesis and biological characterization of novel rose bengal derivatives with improved am-phiphilicity for sono-photodynamic therapy. European journal of medicinal chemistry, 145, 86–95.
- Bakhshizadeh, M., Moshirian, T., Esmaily, H., Rajabi, O., Nassirli, H., and Sazgarnia, A. (2017). Sonophotodynamic therapy mediated by liposomal zinc phthalocyanine in a colon carcinoma tumor model: Role of irradiating arrangement. Iranian journal of basic medical sciences, 20(10), 1088–1092.
- Wang, D., Wan, Z., Yang, Q., Chen, J., Liu Y., Lu, F. and Tang, J. (2022). Sonodynamical reversion of immunosuppressive microenvironment in prostate cancer via engineered exosomes. Drug Deliv, 29, 702-713.
- Jin, Z. H., Miyoshi, N., Ishiguro, K., Umemura, S., Kawabata, K., Yumita, N., Sakata, I., Takaoka, K., Udagawa, T., Nakajima, S., Tajiri, H., Ueda, K., Fukuda, M., and Kumakiri, M. (2000). Combination effect of photodynamic and sonodynamic therapy on experimental skin squamous cell carcinoma in C3H/HeN mice. The Journal of dermatology, 27(5), 294–306.
- Cho, M., Park, G. M., Kim, S. N., Amna, T., Lee, S., and Shin, W. S. (2014). Glioblasto-ma-specific anticancer activity of pheophorbide a from the edible red seaweed Grateloupia el-liptica. Journal of microbiology and biotechnology, 24(3), 346–353.
- Gheewala, T., Skwor, T., and Munirathinam, G. (2018). Photodynamic therapy using phe-ophorbide and 670nm LEDs exhibits anti-cancer effects in-vitro in androgen dependent prostate cancer. Photodiagnosis and photodynamic therapy, 21, 130–137.
- Xu, D. D., Lam, H. M., Hoeven, R., Xu, C. B., Leung, A. W. N., Cho, W. C. S. (2013). Photodynamic therapy induced cell death of hormone insensitive prostate cancer PC-3 cells with autophagic characteristics. Photodiagnosis and Photodynamic Therapy, 10, 278-287.