The effect of sodium nitroprusside in scaffolds for synergetic gas-photothermal therapy of osteosarcoma

Abstract

High recurrence rates and critical bone defects after surgical treatment seriously hinder the curing rate of malignant bone tumors. Thus, developing a multifunctional platform to achieve effective tumor elimination and bone regeneration is urgently needed. Recently, gas therapy combined with hyperthermia has shown an intriguing synergetic therapeutic effect on tumor, avoiding limited spot areas, insufficient heat in deep or surrounding regions, and other inherent limitations of photothermal therapy. Therefore, calcium alginate hydrogel was coated on the surface of 3D printing polycaprolactone (PCL) scaffold and loaded with sodium nitroprusside (SNP) to fabricate the PCLA-SNP composite scaffold. SNP can coordinately react with Fe³⁺ to form Prussian blue-like precipitates after ultraviolet irradiation to reduce the toxicity of SNP metabolites and improve the biocompatibility of materials. Hence, photothermal generated by a near-infrared laser and controlled release of nitric oxide (NO) were obtained to enhance ablation of bone tumors. Furthermore, the calcium and iron ions released from PCLA-SNP scaffolds can accelerate bone regeneration. With stable release of NO, efficient photothermal conversion, and promotion of bone regeneration, PCLA-SNP scaffolds have enlightened an interesting platform for synergistic gas-photothermal therapy for bone tumors.

Keywords

3D printing / gas therapy / hyperthermia / osteosarcoma / sodium nitroprusside

References

[1] M. S. Isakoff, S. S. Bielack, P. Meltzer, R. Gorlick, J. Clin. Oncol.2015, 33, 3029.

[2] A. Luetke, P. A. Meyers, I. Lewis, H. Juergens, Cancer Treat. Rev.2014, 40, 523.

[3] S. S. Bielack, B. Kempf-Bielack, G. Delling, G. U. Exner, S. Flege, K. Helmke, R. Kotz, M. Salzer-Kuntschik, M. Werner, W. Winkelmann, A. Zoubek, H. Jurgens, K. Winkler, J. Clin. Oncol.2002, 20, 776.

[4] H. Lin, S. S. Gao, C. Dai, Y. Chen, J. L. Shi, J. Am. Chem. Soc.2017, 139, 16235.

[5] Y. J. Lu, E. Y. Chuang, Y. H. Cheng, T. S. Anilkumar, H. A. Chen, J. P. Chen, Chem. Eng. J.2019, 373, 720.

[6] N. L. Yang, W. Li, F. Gong, L. Cheng, Z. L. Dong, S. Bai, Z. S. Xiao, C. F. Ni, Z. Liu, Small Methods2020, 4, 2000147.

[7] S. Monro, K. L. Colon, H. M. Yin, J. Roque, P. Konda, S. Gujar, R. P. Thummel, L. Lilge, C. G. Cameron, S. A. McFarland, Chem. Rev.2019, 119, 797.

[8] R. D. Issels, L. H. Lindner, J. Verweij, R. Wessalowski, P. Reichardt, P. Wust, P. Ghadjar, P. Hohenberger, M. Angele, C. Salat, Z. Vujaskovic, S. Daugaard, O. Mella, U. Mansmann, H. R. Durr, T. Knosel, S. Abdel-Rahman, M. Schmidt, W. Hiddemann, K. W. Jauch, C. Belka, A. Gronchi, JAMA Oncol.2018, 4, 483.

[9] M. W. Dewhirst, B. L. Viglianti, M. Lora-Michiels, M. Hanson, P. J. Hoopes, Int. J. Hyperthermia2003, 19, 267.

[10] N. Lu, Z. H. Deng, J. Gao, C. Liang, H. P. Xia, P. Y. Zhang, Nat. Commun.2022, 13, 2245.

[11] Y. R. Zhang, R. Lin, H. J. Li, W. L. He, J. Z. Du, J. Wang, WIREs Nanomed. Nanobiotechnol.2019, 11, e1519.

[12] Z. B. YangH, R. Chen, Nano Res.2023, 16, 3924.

[13] Y. Z. Jing, S. J. Li, Z. J. Sun, J. Mater. Chem. B2021, 9, 8541.

[14] F. Vannini, K. Kashfi, N. Nath, Redox Biol.2015, 6, 334.

[15] J. Kim, D. M. Francis, L. F. Sestito, P. A. Archer, M. P. Manspeaker, M. J. O'MeliaS, N. Thomas, Nat. Commun.2022, 13, 1479.

[16] T. Yang, A. N. Zelikin, R. Chandrawati, Adv. Sci.2018, 5, 1701043.

[17] X. Zhang, J. F. Du, Z. Guo, J. Yu, Q. Gao, W. Y. Yin, S. Zhu, Z. J. Gu, Y. L. Zhao, Adv. Sci.2019, 6, 1801122.

[18] A. J. Burke, F. J. Sullivan, F. J. Giles, S. A. Glynn, Carcinogenesis2013, 34, 503.

[19] S. X. Chen, J. Zhang, F. F. Xue, W. Liu, Y. C. Kuang, B. X. Gu, S. L. Song, H. R. Chen, Bioact. Mater.2023, 21, 86.

[20] S. J. Dong, Y. Chen, L. D. Yu, K. L. LinX, D. Wang, Adv. Funct. Mater.2020, 30, 1907071.

[21] J. Song, L. F. Li, L. Fang, E. S. Zhang, Y. Zhang, Z. X. Zhang, P. Vangari, Y. Q. Huang, F. Tian, Y. Zhao, W. Chen, J. J. Xue, BMEMat2023, 1, e12046.

[22] S. M. S. Shahriar, N. S. Polavoram, S. M. Andrabi, Y. Su, D. Lee, H. Q. Tran, S. J. Schindler, J. Xie, BMEMat2024, 2, e12065.

[23] H. Huang, L. Qiang, M. Fan, Y. Liu, A. Yang, D. Chang, J. Li, T. Sun, Y. Wang, R. Guo, H. Zhuang, X. Li, T. Guo, J. Wang, H. Tan, P. Zheng, J. Weng, Bioact. Mater.2024, 31, 18.

[24] F. C. Bin, M. Guo, T. Li, Y. C. Zheng, X. Z. Dong, J. Liu, F. Jin, M. L. Zheng, Adv. Funct. Mater.2023, 33, 2300293.

[25] S. Dong, Y. Zhang, Y. Zhang, Y. Mei, A. Sina, R. Zou, L. Niu, J. Nanobiotechnol.2024, 22, 199.

[26] B. Zegarska, K. Pietkun, W. Zegarski, P. Bolibok, M. Wiśniewski, K. Roszek, J. Czarnecka, M. Nowacki, Postepy Dermatol. Alergol.2017, 34, 6.

[27] U. Hauser, V. Oestreich, H. D. Rohrweck, Z. Physik. A1978, 284, 9.

[28] P. Gutlich, Y. Garcia, T. Woike, Coord. Chem. Rev.2001, 219, 839.

[29] T. Feng, J. Y. Wan, P. Li, H. T. Ran, H. L. Chen, Z. G. Wang, L. K. Zhang, Biomaterials2019, 214, 119213.

[30] M. Gautam, K. Poudel, C. S. Yong, J. O. Kim, Int. J. Pharm.2018, 549, 31.

[31] X. Lin, Y. B. Cao, Y. A. Xue, F. S. Wu, F. Q. Yu, M. Wu, X. J. Zhu, Nanotechnology2020, 31, 135101.

[32] C. C. Ren, Y. Cheng, W. Li, P. Liu, L. F. Yang, Q. L. Lu, M. Xu, F. P. Tan, J. Li, N. Li, Biomater. Sci.2020, 8, 1981.

[33] J. Yang, J. Choi, D. Bang, E. Kim, E. K. Lim, H. Park, J. S. Suh, K. Lee, K. H. Yoo, E. K. Kim, Y. M. Huh, S. Haam, Angew. Chem., Int. Ed.2011, 50, 441.

[34] Y. Tanaka, N. Tatewaki, H. Nishida, T. Eitsuka, N. Ikekawa, J. Nakayama, Cancer Sci.2012, 103, 1467.

[35] X. Q. Zhu, Y. N. Zhu, K. Jia, B. S. Abraha, Y. Li, W. C. Peng, F. B. Zhang, X. B. Fan, L. Zhang, Nanoscale2020, 12, 19129.

[36] G. Y. Chen, Y. H. Wu, K. Jin, H. F. Lu, M. Y. Tao, T. T. Wang, J. Zhang, X. H. Zhu, J. L. Liu, Y. Zhang, ACS Appl. Bio Mater.2021, 4, 7542.

[37] D. E. Chung, R. K. Lee, S. A. Kaplan, A. E. Te, J. Urol.2010, 184, 2434.

[38] D. K. Roper, W. Ahn, M. Hoepfner, J. Phys. Chem. C2007, 111, 3636.

[39] T. F. Hartley, J. C. Philcox, J. Willoughby, J. Pharm. Sci.1985, 74, 668.

[40] H. S. Ma, C. A. Jiang, D. Zhai, Y. X. Luo, Y. Chen, F. Lv, Z. F. Yi, Y. Deng, J. W. Wang, J. Chang, C. T. Wu, Adv. Funct. Mater.2016, 26, 1197.

[41] B. W. Yang, J. H. Yin, Y. Chen, S. S. Pan, H. L. Yao, Y. S. Gao, J. L. Shi, Adv. Mater.2018, 30, 1705611.

[42] X. Wang, D. Zhang, H. Peng, J. Yang, Y. Li, J. Xu, Biomater. Adv.2023, 154, 213638.

[43] J. Chapman, A. Elbourne, V. K. Truong, D. Cozzolino, Int. J. Food Sci. Technol.2020, 55, 935.

[44] J. G. Croissant, J. I. Zink, L. Raehm, J. O. Durand, Adv. Healthcare Mater.2018, 7, 1701248.

[45] D. Barolet, F. Christiaens, M. R. Hamblin, J. Photochem. Photobiol., B2016, 155, 78.

[46] B. Sanz, M. P. Calatayud, T. E. Torres, M. L. Fanarraga, M. R. Ibarra, G. F. Goya, Biomaterials2017, 114, 62.

[47] P. N. Coneski, M. H. Schoenfisch, Chem. Soc. Rev.2012, 41, 3753.

[48] V. Borutaite, G. C. Brown, Biochim. Biophys. Acta, Bioenerg. 2006, 1757, 562.

[49] D. D. Thomas, L. A. Ridnour, J. S. Isenberg, W. Flores-Santana, C. H. Switzer, S. Donzelli, P. Hussain, C. Vecoli, N. Paolocci, S. Ambs, C. A. Colton, C. C. Harris, D. D. Roberts, D. A. Wink, Free Radical Biol. Med.2008, 45, 18.

[50] Y. Feng, H. Zhang, X. Xie, Y. Chen, G. Yang, X. Wei, N. Li, M. Li, T. Li, X. Qin, S. Li, F. You, C. Wu, H. Yang, Y. Liu, Mater. Today Bio2022, 14, 100288.

[51] Z. Zhang, M. Ge, H. Lin, J. Shi, J. Inorg. Mater.2024, 39, 1114.

[52] X. Liu, Y. Zhang, Y. Wang, M. Yang, F. Hong, S. Yang, Biomolecules2021, 11, 1009.

[53] C. L. McGinity, E. M. Palmieri, V. Somasundaram, D. D. Bhattacharyya, L. A. Ridnour, R. Y. S. Cheng, A. E. Ryan, S. A. Glynn, D. D. Thomas, K. M. Miranda, S. K. Anderson, S. J. Lockett, D. W. McVicar, D. A. Wink, Int. J. Mol. Sci.2021, 22, 7068.

[54] E. Biscop, J. Baroen, J. De Backer, W. Vanden Berghe, E. Smits, A. Bogaerts, A. Lin, Cell Death Discovery2024, 10, 416.

[55] Q. He, W. Tang, B. Han, J. Wei, W. Lu, Z. Tang, J. Inorg. Mater.2024, 39, 90.

[56] E. Ooko, M. E. Saeed, O. Kadioglu, S. Sarvi, M. Colak, K. Elmasaoudi, R. Janah, H. J. Greten, T. Efferth, Phytomedicine2015, 22, 1045.

[57] B. R. Stockwell, X. Jiang, W. Gu, Trends Cell Biol.2020, 30, 478.

[58] F. E. Freeman, R. Burdis, O. R. Mahon, D. J. Kelly, N. Artzi, Adv. Healthcare Mater.2022, 11, 2101296.

[59] Q. H. Yang, H. H. Yin, T. M. Xu, D. Y. Zhu, J. H. Yin, Y. X. Chen, X. W. Yu, J. J. Gao, C. Q. Zhang, Y. Chen, Y. S. Gao, Small2020, 16, 1906814.

[60] Z. F. Zhou, T. W. Sun, F. Chen, D. Q. Zuo, H. S. Wang, Y. Q. Hua, Z. D. Cai, J. Tan, Biomaterials2017, 121, 1.

[61] X. C. Wang, T. Li, H. S. Ma, D. Zhai, C. Jiang, J. Chang, J. W. Wang, C. T. Wu, NPG Asia Mater.2017, 9, e376.

[62] K. J. Wu, C. S. WuJ, S. Chang, Process. Biochem.2007, 42, 669.

[63] Z. Gounani, S. Pourianejad, M. A. Asadollahi, R. L. Meyer, J. M. Rosenholm, A. Arpanaei, J. Mater. Sci.2020, 55, 17134.

[64] K. K. Rijin, P. Sagitha, G. S. Amitha, S. Vasudevan, A. Sujith, J. Mater. Sci.2019, 54, 13433.

[65] A. M. C. Barradas, H. A. M. Fernandes, N. Groen, Y. C. Chai, J. Schrooten, J. van de Peppel, J. van Leeuwen, C. A. van Blitterswijk, J. de Boer, Biomaterials2012, 33, 3205.

[66] Y. Q. Liu, T. Li, H. S. Ma, D. Zhai, C. J. Deng, J. W. Wang, S. J. Zhuo, J. Chang, C. T. Wu, Acta Biomater.2018, 73, 531.

[67] J. M. Kim, S. Choi, K. H. Kwack, S. Y. Kim, H. W. Lee, K. Park, Biomaterials2017, 127, 107.

[68] Y. Feng, S. Zhu, D. Mei, J. Li, J. Zhang, S. Yang, S. Guan, Curr. Drug Delivery2021, 18, 847.

[69] S. Wang, S. Zhao, J. Yu, Z. Gu, Y. Zhang, Small2022, 18, e2201869.

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