Citation: Wenjia Wang, Xingyue He, Xiaojie Wang, Tiantian Zhao, Osamu Muraoka, Genzoh Tanabe, Weijia Xie, Tianjiao Zhou, Lei Xing, Qingri Jin, Hulin Jiang. Glutathione-depleted cyclodextrin pseudo-polyrotaxane nanoparticles for anti-inflammatory oxaliplatin (Ⅳ) prodrug delivery and enhanced colorectal cancer therapy[J]. Chinese Chemical Letters, ;2024, 35(4): 108656. doi: 10.1016/j.cclet.2023.108656 shu

Glutathione-depleted cyclodextrin pseudo-polyrotaxane nanoparticles for anti-inflammatory oxaliplatin (Ⅳ) prodrug delivery and enhanced colorectal cancer therapy

Wenjia Wang ^{a, 1} ,
Xingyue He ^{a, 1} ,
Xiaojie Wang ^{a, 1} ,
Tiantian Zhao ^a ,
Osamu Muraoka ^b ,
Genzoh Tanabe ^b ,
Weijia Xie ^c ,
Tianjiao Zhou ^a ,
Lei Xing ^{a, *,} ,
Qingri Jin ^{d, *,} ,
Hulin Jiang ^{a, e, *,}

a.
State Key Laboratory of Natural Medicines, China Pharmaceutical University, Nanjing 210009, China
b.
Faculty of Pharmacy Kinki University, Higashiosaka, Osaka 577-8502, Japan
c.
State Key Laboratory of Natural Medicines (SKLNM) and Department of Medicinal Chemistry, School of Pharmacy, China Pharmaceutical University, Nanjing 210009, China
d.
School of Pharmacy, Hangzhou Medical College, Hangzhou 311399, China
e.
College of Pharmacy, Yanbian University, Yanji 133002, China

xinglei6xl@163.com

jinqr@hmc.edu.cn

jianghulin3@163.com

Received Date: 5 May 2023
Revised Date: 1 June 2023
Accepted Date: 4 June 2023
Available Online: 7 June 2023

Figures(6)

Oxaliplatin (Oxa) is the first-line chemotherapeutic drug for the treatment of colorectal cancer (CRC). However, long-term Oxa chemotherapy can induce inflammation and increase the levels of cyclooxygenase-2 (COX-2) and prostaglandin E2 (PGE2), which can promote tumor metastasis. Moreover, high glutathione (GSH) levels in CRC cells significantly reduce Oxa sensitivity and seriously restrict the clinical application of Oxa. Herein, an Oxa(Ⅳ) prodrug with anti-inflammatory properties (desmethyl naproxe, DN) and GSH-depleting cyclodextrin pseudo-polyrotaxane carriers were prepared and further self-assembled into micellar nanoparticles (designated DNPt@PPRI). The relesae of DN from DNPt@PPRI can reduce the level of PGE2 to inhibit inflammation and tumor metastasis by decreasing COX-2 protein, and also synergize with Oxa to inhibit tumor. More importantly, GSH depletion can reduce the detoxification of Oxa and further enhance chemotherapy-induced apoptosis. DNPt@PPRI have a good GSH depletion ability to enhance the sensitivity of Oxa, indicating a potential in the synergistic chemotherapy and chemo-sensitization of colorectal cancer.
- Oxaliplatin,
- Glutathione depletion,
- Tetravalent platinum prodrug,
- Synergistic therapy,
- Colorectal cancer
1. [1]
  R.L. Siegel, K.D. Miller, N.S. Wagle, et al., CA Cancer J. Clin. 73 (2023) 17–48. doi: 10.3322/caac.21763
2. [2]
  N. Altoom, S.M. Ibrahim, S.I. Othman, et al., Colloids Surface A 648 (2022) 129144. doi: 10.1016/j.colsurfa.2022.129144
3. [3]
  R.L. Siegel, N.S. Wagle, A. Cercek, et al., CA Cancer J. Clin. 73 (2023) 233–254. doi: 10.3322/caac.21772
4. [4]
  L.H. Biller, D. Schrag, JAMA 325 (2021) 669–685. doi: 10.1001/jama.2021.0106
5. [5]
  X.L. Chen, J. Chen, W.B. Feng, et al., Theranostics 13 (2023) 1401–1418. doi: 10.7150/thno.82269
6. [6]
  T. Alcindor, N. Beauger, Curr. Oncol. 18 (2011) 18–25.
7. [7]
  O.M. Alian, A.S. Azmi, R.M. Mohammad, Clin. Transl. Med. 1 (2012) 26. doi: 10.1186/2001-1326-1-26
8. [8]
  T. Xia, J.Z. Zhang, L.Y. Han, et al., Phytother. Res. 33 (2019) 1161–1172. doi: 10.1002/ptr.6311
9. [9]
  Q.H. Chen, X.Y. Lu, X.Y. Zhang, J. Clin. Transl. Hepatol. 9 (2021) 81–89.
10. [10]
  A. Lasry, A. Zinger, Y. Ben-Neriah, Nat. Immunol. 17 (2016) 230–240. doi: 10.1038/ni.3384
11. [11]
  J.H. Park, D.C. McMillan, P.G. Horgan, et al., Cancer Treat. Rev. 40 (2014) 68–77. doi: 10.1016/j.ctrv.2013.05.006
12. [12]
  A.A. Bhat, S. Nisar, M. Singh, et al., Cancer Commun. 42 (2022) 689–715. doi: 10.1002/cac2.12295
13. [13]
  C.W. Su, Y. Zhang, Y.T. Zhu, Crit. Rev. Oncol. Hematol. 107 (2016) 33–38. doi: 10.1109/CPE.2016.7544154
14. [14]
  W.K. Chia, R. Ali, H.C. Toh, Nat. Rev. Clin. Oncol. 9 (2012) 561–570. doi: 10.1038/nrclinonc.2012.137
15. [15]
  C.R. Bell, V.S. Pelly, A. Moeini, et al., Nat. Commun. 13 (2022) 2063. doi: 10.1038/s41467-022-29606-9
16. [16]
  L. Xing, C.X. Yang, D. Zhao, et al., J. Control. Release 331 (2021) 460–471. doi: 10.1016/j.jconrel.2021.01.037
17. [17]
  E. Martinez-Balibrea, A. Martinez-Cardus, A. Gines, et al., Mol. Cancer Ther. 14 (2015) 1767–1776. doi: 10.1158/1535-7163.MCT-14-0636
18. [18]
  A. Bansal, M.C. Simon, J. Cell Biol. 217 (2018) 2291–2298. doi: 10.1083/jcb.201804161
19. [19]
  Q. Jin, S.Q. Yan, H. Hu, et al., Small Methods 5 (2021) e2101047. doi: 10.1002/smtd.202101047
20. [20]
  D.C. Qi, L. Xing, L.J. Shen, et al., Chin. Chem. Lett. 33 (2022) 4595–4599. doi: 10.1016/j.cclet.2022.03.105
21. [21]
  T. Sun, G.P. Zhang, T. Ning, et al., Adv. Sci. 8 (2021) e2102256. doi: 10.1002/advs.202102256
22. [22]
  X.D. Qian, Y.Q. Wang, H.L. Xie, et al., J. Control. Release 353 (2023) 447–461. doi: 10.1016/j.jconrel.2022.11.044
23. [23]
  M. Bambouskova, L. Gorvel, V. Lampropoulou, et al., Nature 556 (2018) 501–504. doi: 10.1038/s41586-018-0052-z
24. [24]
  Y.Y. Deng, F. Jia, X.H. Chen, et al., Small 16 (2020) e2001747. doi: 10.1002/smll.202001747
25. [25]
  R. Liu, C. Luo, Z.Q. Pang, et al., Chin. Chem. Lett. 34 (2023) 107518. doi: 10.1016/j.cclet.2022.05.032
26. [26]
  F. Li, X. Zhao, H. Wang, et al., Adv. Funct. Mater. 25 (2015) 788–798. doi: 10.1002/adfm.201401583
27. [27]
  H. Huang, C.H. Dong, M.Q. Chang, et al., Exploration 1 (2021) 50–60. doi: 10.1002/exp.20210149
28. [28]
  Y. Kang, X.M. Zhang, S. Zhang, et al., Polym. Chem. 6 (2015) 2098–2107. doi: 10.1039/C4PY01431F
29. [29]
  T. Martinez-Bernabe, J. Oliver, J. Sastre-Serra, et al., Int. J. Mol. Sci. 24 (2023) 3821. doi: 10.3390/ijms24043821
30. [30]
  V. Banerjee, N. Sharda, J. Huse, et al., Eur. J. Pharmacol. 897 (2021) 173919. doi: 10.1016/j.ejphar.2021.173919
31. [31]
  L.N. Wang, Y.J. Yu, D.S. Wei, et al., Adv. Mater. 33 (2021) e2100599. doi: 10.1002/adma.202100599
32. [32]
  F.Y. Shen, L. Feng, Y.J. Zhu, et al., Biomaterials 255 (2020) 120190. doi: 10.1016/j.biomaterials.2020.120190
33. [33]
  S. Jin, N. Muhammad, Y. Sun, et al., Angew. Chem. Int. Ed. 59 (2020) 23313–23321. doi: 10.1002/anie.202011273
34. [34]
  X.J. Gao, G.X. Lei, B. Wang, et al., Adv. Sci. 10 (2023) e2205241. doi: 10.1002/advs.202205241
35. [35]
  D.S. Wei, Y. Huang, B. Wang, et al., Angew. Chem. Int. Ed. 61 (2022) e202201486. doi: 10.1002/anie.202201486
36. [36]
  X. Wang, X. Wang, Z. Guo, Acc. Chem. Res. 48 (2015) 2622–2631. doi: 10.1021/acs.accounts.5b00203
37. [37]
  Y.Q. Wang, H.L. Xie, Y. Wu, et al., Adv. Mater. 34 (2022) e2110614. doi: 10.1002/adma.202110614
38. [38]
  C. Peptu, D.A. Blaj, M. Balan-Porcarasu, et al., Polymers 14 (2022) 1436. doi: 10.3390/polym14071436
39. [39]
  X.H. Chen, H.Q. Gao, Y.Y. Deng, et al., ACS Nano 14 (2020) 5121–5134. doi: 10.1021/acsnano.0c02197
40. [40]
  J. Choi, T. Takata, H. Ajiro, Macromolecules 54 (2021) 5087–5093. doi: 10.1021/acs.macromol.1c00220
41. [41]
  C.T. Zhang, J. Li, C.X. Yang, et al., Nanomedicine 23 (2020) 102071. doi: 10.1016/j.nano.2019.102071
42. [42]
  J. Chang, Y. Li, G. Wang, et al., Nanoscale 5 (2013) 813–820. doi: 10.1039/C2NR32927A
43. [43]
  P. Zhang, Y. Zhang, X.Y. Ding, et al., Adv. Mater. 32 (2020) e2000013. doi: 10.1002/adma.202000013
44. [44]
  T.J. Zhou, Y. Xu, L. Xing, et al., Adv. Mater 33 (2021) e2100114. doi: 10.1002/adma.202100114
45. [45]
  S. Goschl, E. Schreiber-Brynzak, V. Pichler, et al., Metallomics 9 (2017) 309–322. doi: 10.1039/C6MT00226A
46. [46]
  Y. Xu, L.L. Huang, Y.Y. Bi, et al., Chin. Chem. Lett. 34 (2023) 107719. doi: 10.1016/j.cclet.2022.07.062
47. [47]
  Y.J. He, L. Xing, P.F. Cui, et al., Biomaterials 113 (2017) 266–278. doi: 10.1016/j.biomaterials.2016.11.001
48. [48]
  T.J. Zhou, L. Xing, Y.T. Fan, et al., J. Control. Release 307 (2019) 44–54. doi: 10.1016/j.jconrel.2019.06.016
49. [49]
  T.J. Zhou, L. Xing, Y.T. Fan, et al., J. Control. Release 309 (2019) 82–93. doi: 10.1016/j.jconrel.2019.07.028
50. [50]
  J. Wan, X.H. Zhang, Z.H. Li, et al., Adv. Healthc. Mater. (2022) e2202710.
51. [51]
  Y. Wang, L.F. Hu, P.F. Cui, et al., Adv. Mater. 33 (2021) e2103307. doi: 10.1002/adma.202103307
52. [52]
  D. Brenner, T.W. Mak, Curr. Opin. Cell Biol. 21 (2009) 871–877. doi: 10.1016/j.ceb.2009.09.004
53. [53]
  D.F. Suen, K.L. Norris, R.J. Youle, Genes Dev. 22 (2008) 1577–1590. doi: 10.1101/gad.1658508
54. [54]
  L.A. Pradelli, M. Beneteau, J.E. Ricci, Cell Mol. Life Sci. 67 (2010) 1589–1597. doi: 10.1007/s00018-010-0285-y
55. [55]
  G.Y. Zhu, M. Myint, W.H. Ang, et al., Cancer Res. 72 (2012) 790–800.
56. [56]
  Y. Xu, X.X. Han, Y.Y. Li, et al., ACS Nano 13 (2019) 13445–13455. doi: 10.1021/acsnano.9b07032
57. [57]
  Y. Zhu, L. Xing, X. Zheng, et al., Int. J. Pharm. 573 (2020) 118736. doi: 10.1016/j.ijpharm.2019.118736
58. [58]
  L.H. Xu, J. Stevens, M.B. Hilton, et al., Sci. Transl. Med. 6 (2014) 242ra284.
59. [59]
  D.B. Vendramini-Costa, J.E. Carvalho, Curr. Pharm. Des. 18 (2012) 3831–3852. doi: 10.2174/138161212802083707
60. [60]
  X.L. Fu, Y.B. Shi, H.C. Zang, et al., J. Control. Release 347 (2022) 1–13. doi: 10.1155/2022/3100892
61. [61]
  B. Zhang, T.Q. Wang, S.M. Yang, et al., J. Control. Release 238 (2016) 10–21. doi: 10.1016/j.jconrel.2016.07.022
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