Cartilage-targeting and inflammatory-responsive nanocarriers for effective osteoarthritis treatment via reactive oxygen species scavenging and anti-angiogenesis

doi:10.1016/j.jmst.2022.08.048

Abstract

Abstract: Osteoarthritis (OA), a common disabling joint disease, is highly associated with microenvironmental changes in the cartilage and subchondral bone. Elevated reactive oxygen species (ROS) in the cartilage and subchondral bone angiogenesis accelerate articular cartilage erosion. New cartilage-targeting drug delivery systems that are aimed at preventing ROS production and angiogenesis may be of clinical significance for OA treatment. Herein, an ROS scavenger and an inflammatory-responsive nanocarrier are designed by immobilizing the natural polyphenol (curcumin) in chitosan-catechol nanoformulations (Cur-CS-C NPs) via boronate ester. The robust cartilage-targeting effects and ROS scavenging capacities of Cur-CS-C NPs were respectively determined in cartilage explants and chondrocytes. Intra-articular injection of Cur-CS-C NPs in OA rat models efficiently suppressed angiogenesis and cartilage degradation partially via the ROS-mediated NF-κB/PI3K-Akt signaling pathway. The developed curcumin-functionalized nanocarriers can significantly delay OA progression and provide a promising therapeutic strategy for other inflammatory diseases that are characterized by oxidative stress and angiogenesis.

Key words: Osteoarthritis, Reactive oxygen species, Angiogenesis, Cartilage-targeting, Drug delivery systems, Chitosan-catechol nanocarriers

Sixiang Wang, Yan Gao, Lili Dong, Peixing Chen, Wanqian Liu, Li Yang. Cartilage-targeting and inflammatory-responsive nanocarriers for effective osteoarthritis treatment via reactive oxygen species scavenging and anti-angiogenesis[J]. J. Mater. Sci. Technol., 2023, 143: 30-42.

References

[1] A. Mobasheri, M. Batt, Ann. Phys. Rehabil.Med. 59(2016) 333-339.
[2] M. Ishijima, T. Nakamura, K. Shimizu, K. Hayashi, H. Kikuchi, S. Soen, G. Omori, T. Yamashita, Y. Uchio, J. Chiba, Y. Ideno, M. Kubota, H. Kurosawa, K. Kaneko, Arthritis Res. Ther. 16(2014) R18.
[3] A.G. Bajpayee, A.J. Grodzinsky, Nat. Rev. Rheumatol. 13(2017) 183-193.
[4] Y. Hu, X. Chen, S.C. Wang, Y.Y. Jing, J.C. Su, Bone Res. 9(2021) 20.
[5] J. Soul, M.J. Barter, C.B. Little, D.A. Young, Ann. Rheum. Dis. 80(2021) 376-383.
[6] P.I. Mapp, D.A. Walsh, Nat. Rev. Rheumatol. 8(2012) 390-398.
[7] W.P. Su, G.Q. Liu, X.N. Liu, Y.Y. Zhou, Q. Sun, G.H. Zhen, X. Wang, Y.H. Hu, P.S. Gao, S. Demehri, X. Cao, M. Wan, JCI Insight 5 (2020) e135446.
[8] M.L.P.Lozano, Osteoarthr. Cartil. 25(2017) S144-S144.
[9] K. Takada, J. Hirose, K. Senba, S. Yamabe, Y. Oike, T. Gotoh, H. Mizuta, Int J. Exp. Pathol. 92(2011) 232-242.
[10] P. Lepetsos, A.G. Papavassiliou, Biochim. Biophys. Acta Mol.Basis Dis. 1862(2016) 576-591.
[11] D. Li, G.R. Xie, W.C. Wang, Am. J. Med. Sci. 344(2012) 486-490.
[12] W.B. Ye, S.Y. Zhu, C.R. Liao, J. Xiao, Q. Wu, Z. Lin, J.T. Chen, Fundam. Clin. Pharmacol. 31(2017) 64-74.
[13] L.H. Wu, H.Q. Liu, L.F. Li, H. Liu, Q.L. Cheng, H.L. Li, H. Huang, Curr. Drug Targets 15 (2014) 710-719.
[14] Y. Chen, B.J. Zhao, Y. Zhu, H.Q. Zhao, C. Ma, Am. J. Transl. Res. 11(2019) 2969-2982.
[15] P.R. Chiu, Y.C. Hu, T.C. Huang, B.S. Hsieh, J.P. Yeh, H.L. Cheng, L.W. Huang, K.L. Chang, Int. J. Mol. Sci. 18(2016) 38.
[16] H. Yao, J.K. Xu, J.L. Wang, Y.F. Zhang, N.Y. Zheng, J. Yue, J. Mi, L.Z. Zheng, B.Y. Dai, W.H. Huang, S.H. Yung, P.J. Hu, Y.C. Ruan, Q. Xue, K. Ho, L. Qin, Bioact. Mater. 6(2021) 1341-1352.
[17] S. Nakagawa, Y. Arai, O. Mazda, T. Kishida, K.A. Takahashi, K. Sakao, M. Saito, K. Honjo, J. Imanishi, T. Kubo, J. Orthop. Res. 28(2010) 156-163.
[18] J.A.Roman-Blas, M.A. Contreras-Blasco, R. Largo, M.A. Alvarez-Soria, S. Castaneda, G. Herrero-Beaumont, Eur. J. Pharmacol. 623(2009) 125-131.
[19] M.Y. Ansari, N. Ahmad, T.M. Haqqi, Biomed. Pharmacother. 129(2020) 110452.
[20] P. Yuce, H. Hosgor, S.F. Rencber, Y. Yazir, J. Oral Maxillofac.Surg. 79(2021) 344 e1.
[21] D. Slamenova, K. Kozics, L. Hunakova, M. Melusova, J. Navarova, E. Horvathova, Mutat. Res. Genet. Toxicol. Environ. Mutagen. 757(2013) 15-22.
[22] T. Shen, O. Alvarez-Garcia, Y. Li, M. Olmer, M.K.Lotz, in: World Congress of the Osteoarthritis-Research-Society-International (OARSI) on Osteoarthritis, Amsterdam, Netherlands, March 31-April 03, 2016.
[23] R.R. Yammani, R.F. Loeser, Arthritis Rheumatol. 66(2014) 1266-1271.
[24] Y.F. Ding, Z.M. Li, W.W. Hu, X.J. Feng, Y. Chen, G.H. Yan, Y.L. Wang, B. Zhu, W. Yao, L. Zheng, M.L. He, M. Gao, J.M. Zhao, Biomater. Sci. 9(2021) 6236-6250.
[25] J. Chu, B. Yan, J. Zhang, L.L. Peng, X. Ao, Z.Y. Zheng, T. Jiang, Z.M. Zhang, Inflammation 43 (2020) 810-820.
[26] B. Crivelli, E. Bari, S. Perteghella, L. Catenacci, M. Sorrenti, M. Mocchi, S. Farago, G. Tripodo, A. Prina-Mello, M.L. Torre, Eur. J. Pharm. Biopharm. 137(2019) 37-45.
[27] I. Rudnik-Jansen, S. Colen, J. Berard, S. Plomp, I. Que, M. van Rijen, N. Woike, A. Egas, G. van Osch, E. van Maarseveen, K. Messier, A. Chan, J. Thies, L. Creemers, J. Control. Release 253 (2017) 64-72.
[28] C.G. Lee, C.A.Da Silva, J.Y. Lee, D. Hartl, J.A. Elias, Curr. Opin. Immunol. 20(2008) 684-689.
[29] J.H. Ryu, S. Hong, H. Lee, Acta Biomater. 27(2015) 101-115.
[30] D. Liu, G.F. Shu, F.Y. Jin, J. Qi, X.L. Xu, Y. Du, H. Yu, J. Wang, M.C. Sun, Y.C. You, M.X. Zhu, M.X. Chen, L.W. Zhu, Q.Y. Shen, X.Y. Ying, X.F. Lou, S.P. Jiang, Y.Z. Du, Sci. Adv. 6 (2020) eabb7422.
[31] G.M. Soliman, Y.L. Zhang, G. Merle, M. Cerruti, J. Barralet, Eur. J. Pharm. Biopharm. 88(2014) 1026-1037.
[32] W.Z. Chen, X.K. Shen, Y. Hu, K. Xu, Q.C. Ran, Y.L. Yu, L.L. Dai, Z. Yuan, L. Huang, T.T. Shen, K. Cai, Biomaterials 114 (2017) 82-96.
[33] K.Y. Ju, Y. Lee, S. Lee, S.B. Park, J.K. Lee, Biomacromolecules 12 (2011) 625-632.
[34] J. Liu, C.G. Meng, Y.H. Yan, Y.N. Shan, J. Kan, C.H. Jin, Int. J. Biol. Macromol. 89(2016) 518-526.
[35] Z. Yi, G.C. Chen, X.Y. Chen, X.M. Ma, X.X. Cui, Z. Sun, W. Su, X.D. Li, ACS Appl. Mater. Interfaces 12 (2020) 33550-33563.
[36] L.Y. Rui, M.H. Xie, B. Hu, L. Zhou, M. Saeeduddin, X.X. Zeng, Carbohydr. Polym. 170(2017) 206-216.
[37] K. Xu, X. Pan, Y.J. Sun, W. Xu, L. Njunge, L. Yang, Pharm. Biol. 53(2015) 1010-1015.
[38] Q.Z. Zhang, D. Dehaini, Y. Zhang, J.L. Zhou, X. Chen, L.F. Zhang, R.H. Fang, W.W. Gao, L.F. Zhang, Nat. Nanotechnol. 13 (2018) 1182-+.
[39] X.F. Bao, J.H. Zhao, J. Sun, M. Hu, X.R. Yang, ACS Nano 12 (2018) 8882-8892.
[40] S.R. Shi, T.R. Tian, Y.J. Li, D.X. Xiao, T. Zhang, P. Gong, Y.F. Lin, ACS Appl. Mater. Interfaces 12 (2020) 56782-56791.
[41] T. Maerz, M.D. Newton, M.D. Kurdziel, P. Altman, K. Anderson, H.W. Matthew, K.C. Baker, Osteoarthr. Cartil. 24(2016) 1918-1927.
[42] K.P. Pritzker, S. Gay, S.A. Jimenez, K. Ostergaard, J.P. Pelletier, P.A. Revell, D. Salter, W.B. van den Berg, Osteoarthr.Cartil. 14(2006) 13-29.
[43] W.W. Zhao, H. Wang, Y. Han, H.M. Wang, Y.L. Sun, H.Y. Zhang, ACS Appl. Mater. Interfaces 12 (2020) 51236-51248.
[44] Y.J. Wang, M. Shen, S. Wang, X. Wen, X.R. Han, Z.F. Zhang, H. Li, F. Wang, D.M. Wu, J. Lu, Y.L. Zheng, Life Sci. 298(2022) 120531.
[45] W.B. Mu, B.Y. Xu, H.R. Ma, B.C. Ji, Z.D. Zhang, J. Li, A. Amat, L. Cao, Mol. Med. Rep. 16(2017) 7679-7684.
[46] Z. Cui, J. Crane, H. Xie, X. Jin, G.H. Zhen, C.J. Li, L. Xie, L. Wang, Q. Bian, T. Qiu, M. Wan, M. Xie, S. Ding, B. Yu, X. Cao, Ann. Rheum. Dis. 75(2016) 1714-1721.
[47] G. Zhen, C. Wen, X. Jia, Y. Li, J.L. Crane, S.C. Mears, F.B. Askin, F.J. Frassica, W. Chang, J. Yao, J.A. Carrino, A. Cosgarea, D. Artemov, Q. Chen, Z. Zhao, X. Zhou, L. Riley, P. Sponseller, M. Wan, W.W. Lu, X. Cao, Nat. Med. 19(2013) 704-712.
[48] C.H. Tsai, S.C. Liu, W.H. Chung, S.W. Wang, M.H. Wu, C.H. Tang, Cells 9 (2020) 1315.
[49] C.J. Zhao, Q.B. Liu, K.Z. Wang, Biomed. Pharmacother. 96(2017) 410-416.
[50] S. Basak, V. Srinivas, A. Mallepogu, A.K. Duttaroy, Cell Biol. Int. 44(2020) 1237-1251.
[51] S. Xu, Z.X. Xu, S. Yan, J. Le, H. Chen, L. Ming, S.G. Xu, T. Lin, Exp. Ther. Med. 18(2019) 1099-1106.
[52] D.A. Rothenfluh, H. Bermudez, C.P. ONeil, J.A. Hubbell, Nat. Mater. 7(2008) 248-254.
[53] P. Lepetsos, K.A. Papavassiliou, A.G. Papavassiliou, Free Radic, Biol. Med. 132(2019) 90-100.
[54] L.M. Zhu, M. Yang, Eur. Rev. Med. Pharmacol. Sci. 23(2019) 5567-5574.
[55] M. Zhang, R. Zhang, T.S. Zheng, Z.X. Chen, G.L. Ji, F. Peng, W. Wang, Front. Pharmacol. 12(2021) 680585.
[56] A. Abdurahman, X.L. Li, J. Li, D.Q. Liu, L.D. Zhai, X.T. Wang, Y.F. Zhang, Y. Meng, H. Yokota, P. Zhang, Bone 157 (2022) 116346.
[57] X.Y. Li, Z.J. Wei, H.T. Yu, Y.J. Xu, W.Y. He, X. Zhou, X. Gou, Cancer Lett. 523(2021) 10-28.
[58] G. Yang, S. Sun, J. Wang, W. Li, X.Q. Wang, L. Yuan, S. Li, Drug Des, Dev. Ther. 14(2020) 4533-4546.
[59] J. Saklatvala, Curr. Drug Targets 8 (2007) 305-313.