Citation: Jiangshan Xu, Weifei Zhang, Zhengwen Cai, Yong Li, Long Bai, Shaojingya Gao, Qiang Sun, Yunfeng Lin. Tetrahedron DNA nanostructure/iron-based nanomaterials for combined tumor therapy[J]. Chinese Chemical Letters, ;2024, 35(11): 109620. doi: 10.1016/j.cclet.2024.109620 shu

Tetrahedron DNA nanostructure/iron-based nanomaterials for combined tumor therapy

Jiangshan Xu ^{a, b} ,
Weifei Zhang ^c ,
Zhengwen Cai ^b ,
Yong Li ^d ,
Long Bai ^d ,
Shaojingya Gao ^b ,
Qiang Sun ^{b, e, *,} ,
Yunfeng Lin ^{a, b, e, *,}

a.
College of Biomedical Engineering, Sichuan University, Chengdu 610065, China
b.
State Key Laboratory of Oral Diseases, National Center for Stomatology, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Chengdu 610041, China
c.
Department of Orthopedics, Orthopedic Research Institute, West China Hospital, Sichuan University, Chengdu 610041, China
d.
Department of Oral Implantology, The Affiliated Stomatological Hospital of Southwest Medical University, Luzhou 646000, China
e.
Sichuan Provincial Engineering Research Center of Oral Biomaterials, Chengdu 610041, China

qiangsun@scu.edu.cn

yunfenglin@scu.edu.cn

Received Date: 9 December 2023
Revised Date: 1 February 2024
Accepted Date: 3 February 2024
Available Online: 13 February 2024

Figures(5)

Triple-negative breast cancer, due to its aggressive nature and lack of targeted treatment, faces serious challenges in breast cancer treatment. Conventional therapies, such as chemotherapy, are encumbered by a range of limitations, and there is an urgent need for more effective treatment strategies. Ferroptosis, as an iron-dependent form of cell death, has exhibited promising potential in cancer treatment. Combining ferroptosis with other cancer therapies offers new avenues for treatment. Tetrahedral DNA nanostructure (TDN), a novel DNA-based three-dimensional (3D) nanomaterial, is promising drug delivery vehicle and can be utilized for functionalizing inorganic nanomaterials. In this work, we have demonstrated the preparation of Fe₃O₄-PEI@TDN-DOX nanocomposites and elucidated their antitumor mechanism. The TDN facilitated the enhanced cellular uptake of polyetherimide (PEI)-modified Fe₃O₄, and the delivery of the chemotherapeutic drug doxorubicin (DOX) further augmented their anti-tumor effect. This novel strategy can destroy the tumor redox homeostasis and produce overwhelming lipid peroxides, consequently sensitizing the tumor to ferroptosis. The integration of ferroptosis with other cancer therapies opens up new possibilities for treatment. This research provides valuable mechanistic insights and practical strategies for leveraging nanotechnology to induce ferroptosis and amplify its impact on tumor cells.
- Tetrahedron DNA nanostructure,
- Ferroptosis,
- Doxorubicin,
- Breast cancer,
- Combined cancer therapy
1. [1]
  O. Ginsburg, F. Bray, M.P. Coleman, et al., Lancet 389 (2017) 847–860. doi: 10.1016/S0140-6736(16)31392-7
2. [2]
  E. Nolan, G.J. Lindeman, J.E. Visvader, Cell 186 (2023) 1708–1728. doi: 10.1016/j.cell.2023.01.040
3. [3]
  S. Loibl, P. Poortmans, M. Morrow, et al., Lancet 397 (2021) 1750–1769. doi: 10.1016/S0140-6736(20)32381-3
4. [4]
  N. Harbeck, M. Gnant, Lancet 389 (2017) 1134–1150. doi: 10.1016/S0140-6736(16)31891-8
5. [5]
  F.J. Esteva, V.M. Hubbard-Lucey, J. Tang, L. Pusztai, Lancet Oncol. 20 (2019) E175–E186. doi: 10.1016/S1470-2045(19)30026-9
6. [6]
  S. Nagata, M. Tanaka, Nat. Rev. Immunol. 17 (2017) 333–340. doi: 10.1038/nri.2016.153
7. [7]
  D. Bertheloot, E. Latz, B.S. Franklin, Cell. Mol. Immunol. 18 (2021) 1106–1121. doi: 10.1038/s41423-020-00630-3
8. [8]
  B. Zhou, J. Liu, R. Kang, et al., Semin. Cancer Biol. 66 (2020) 89–100. doi: 10.1016/j.semcancer.2019.03.002
9. [9]
  D. Tang, X. Chen, R. Kang, G. Kroemer, Cell Res. 31 (2021) 107–125. doi: 10.1038/s41422-020-00441-1
10. [10]
  J.Y. Cao, S.J. Dixon, Cell. Mol. Life Sci. 73 (2016) 2195–2209. doi: 10.1007/s00018-016-2194-1
11. [11]
  X. Jiang, B.R. Stockwell, M. Conrad, Nat. Rev. Mol. Cell Biol. 22 (2021) 266–282. doi: 10.1038/s41580-020-00324-8
12. [12]
  Q. Nie, Y. Hu, X. Yu, et al., Cancer Cell Int. 22 (2022) 12. doi: 10.1186/s12935-021-02366-0
13. [13]
  Y. Li, X. Zeng, D. Lu, et al., Hum. Reprod. 36 (2021) 951–964. doi: 10.1093/humrep/deaa363
14. [14]
  Y. Zhao, Y. Li, R. Zhang, et al., OncoTargets Ther. 13 (2020) 5429–5441. doi: 10.2147/ott.s254995
15. [15]
  P. Koppula, L. Zhuang, B. Gan, Protein Cell 12 (2021) 599–620. doi: 10.1007/s13238-020-00789-5
16. [16]
  Y. Wang, T. Sun, C. Jiang, J. Control. Release 344 (2022) 289–301. doi: 10.3390/jfb13040289
17. [17]
  S. Xie, W. Sun, C. Zhang, et al., ACS Nano 15 (2021) 7179–7194. doi: 10.1021/acsnano.1c00380
18. [18]
  Q. Chen, X. Ma, L. Xie, et al., Nanoscale 13 (2021) 4855–4870. doi: 10.1039/d0nr08757b
19. [19]
  R. Yue, C. Zhang, L. Xu, et al., Chem 8 (2022) 1956–1981. doi: 10.1016/j.chempr.2022.03.009
20. [20]
  H. Peng, X. Zhang, P. Yang, et al., Bioact. Mater. 19 (2023) 1–11.
21. [21]
  F. Zeng, L. Tang, Q. Zhang, et al., Angew. Chem. Int. Ed. 61 (2022) e202112925. doi: 10.1002/anie.202112925
22. [22]
  R. Xu, J. Yang, Y. Qian, et al., Nanoscale Horiz. 6 (2021) 348–356. doi: 10.1039/d0nh00674b
23. [23]
  F.S. Carvalho, A. Burgeiro, R. Garcia, et al., Med. Res. Rev. 34 (2014) 106–135. doi: 10.1002/med.21280
24. [24]
  R.E. Nicoletto, C.M. Ofner Ⅲ, Cancer Chemother. Pharmacol. 89 (2022) 285–311. doi: 10.1007/s00280-022-04400-y
25. [25]
  A. Shafei, W. El-Bakly, A. Sobhy, et al., Biomed. Pharmacother. 95 (2017) 1209–1218. doi: 10.1016/j.biopha.2017.09.059
26. [26]
  P. Arivalagan, T.N.J.I. Edison, B.K. Velmurugan, et al., Life Sci. 200 (2018) 26–30. doi: 10.1016/j.lfs.2018.03.023
27. [27]
  H. Liang, X. -B. Zhang, Y. Lv, et al., Acc. Chem. Res. 47 (2014) 1891–1901. doi: 10.1021/ar500078f
28. [28]
  X. Yang, F. Zhang, Y. Du, et al., Chin. Chem. Lett. 33 (2022) 1901–1906. doi: 10.1016/j.cclet.2021.10.029
29. [29]
  S. Lin, Q. Zhang, S. Li, et al., Cell Proliferat. 55 (2022) e13279. doi: 10.1111/cpr.13279
30. [30]
  T. Zhang, H. Ma, X. Zhang, et al., Adv. Funct. Mater. 33 (2023) 2213401. doi: 10.1002/adfm.202213401
31. [31]
  Y. Zhao, S. Li, M. Feng, et al., Small 19 (2023) e2302326. doi: 10.1002/smll.202302326
32. [32]
  R. Chen, D. Wen, W. Fu, et al., Cell Proliferat. 55 (2022) e13206. doi: 10.1111/cpr.13206
33. [33]
  H. Ijas, B. Shen, A. Heuer-Jungemann, et al., Nucleic Acids Res. 49 (2021) 3048–3062. doi: 10.1093/nar/gkab097
34. [34]
  M. Liu, L. Hao, D. Zhao, et al., ACS Appl. Mater. Interfaces 14 (2022) 38506–38514. doi: 10.1021/acsami.2c09462
35. [35]
  Y. Liu, S. Li, S. Lin, et al., Chin. Chem. Lett. 34 (2023) 107987. doi: 10.1016/j.cclet.2022.107987
36. [36]
  Y. Wang, W. Jia, J. Zhu, et al., Chin. Chem. Lett. 34 (2023) 107746. doi: 10.1016/j.cclet.2022.107746
37. [37]
  X. Shao, Z. Hu, Y. Zhan, et al., Cell Proliferat. 55 (2022) e13272. doi: 10.1111/cpr.13272
38. [38]
  M. Liu, W. Ma, D. Zhao, et al., ACS Appl. Mater. Interfaces 13 (2021) 25825–25835. doi: 10.1021/acsami.1c07297
39. [39]
  N. Wenningmann, M. Knapp, A. Ande, et al., Mol. Pharmacol. 96 (2019) 219–232. doi: 10.1124/mol.119.115725
40. [40]
  N. Kajarabille, G.O. Latunde-Dada, Int. J. Mol. Sci. 20 (2019) 4968. doi: 10.3390/ijms20194968
41. [41]
  T. Ganz, Physiol. Rev. 93 (2013) 1721–1741. doi: 10.1152/physrev.00008.2013
42. [42]
  E. Nemeth, T. Ganz, Annu. Rev. Med. 74 (2023) 261–277. doi: 10.1146/annurev-med-043021-032816
43. [43]
  J. Li, F. Cao, H.L. Yin, et al., Cell Death Dis. 11 (2020) 88. doi: 10.1038/s41419-020-2298-2
44. [44]
  X. Chen, J. Li, R. Kang, et al., Autophagy 17 (2021) 2054–2081. doi: 10.1080/15548627.2020.1810918
45. [45]
  M. Maiorino, M. Conrad, F. Ursini, Antioxid. Redox Signal. 29 (2018) 61–74. doi: 10.1089/ars.2017.7115
46. [46]
  M. Liu, W. Zhu, D. Pei, Invest. New Drugs 39 (2021) 1123–1131. doi: 10.1007/s10637-021-01070-0
47. [47]
  J. Liu, R. Kang, D. Tang, FEBS J. 289 (2022) 7038–7050. doi: 10.1111/febs.16059
48. [48]
  E. Gammella, P. Buratti, G. Cairo, S. Recalcati, Metallomics 9 (2017) 1367–1375. doi: 10.1039/C7MT00143F
49. [49]
  Y. Shen, X. Li, D. Dong, et al., Am. J. Cancer Res. 8 (2018) 916–931.
50. [50]
  D. Tsikas, Anal. Biochem. 524 (2017) 13–30. doi: 10.1016/j.ab.2016.10.021
51. [51]
  W.S. Yang, B.R. Stockwell, Trends Cell Biol. 26 (2016) 165–176. doi: 10.1016/j.tcb.2015.10.014
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  Zhendong Liu , Sainan Liu , Bin Liu , Qi Meng , Meng Yuan , Chunzheng Yang , Yulong Bian , Ping'an Ma , Jun Lin . Fe(Ⅲ)-juglone nanoscale coordination polymers for cascade chemodynamic therapy through synergistic ferroptosis and apoptosis strategy. Chinese Chemical Letters, 2024, 35(11): 109626-. doi: 10.1016/j.cclet.2024.109626
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  Jialin Xie , Qing Feng , Zhen Li , Jinyi Yang , Min Liu , Wei Qi . Life’s Guardian Angel: Progesterone. University Chemistry, 2024, 39(10): 416-419. doi: 10.12461/PKU.DXHX202403068
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