journal article·2024-02Open access

The Interplay Between HIF‐1α and EZH2 in Lung Cancer and Dual‐Targeted Drug Therapy

Jianmin Wang, Cheng Yang, Huashen Xu, Xinyu Fan, Lina Jia, Yang Du, Shougeng Liu, Wenjing Wang, Jie Zhang, Yu Zhang, Xiaoxue Wang, Zhongbo Liu, Jie Bao, Songping Li, Jingyu Yang, Chunfu Wu, Jing Tang, Guoliang Chen, Lihui Wang

Advanced Science· Volume 11· Issue 7

Abstract

Abstract Interactions between oncogenic proteins contribute to the phenotype and drug resistance. Here, EZH2 (enhancer of zest homolog 2) is identified as a crucial factor that mediates HIF‐1 (hypoxia‐inducible factor) inhibitor resistance. Mechanistically, targeting HIF‐1 enhanced the activity of EZH2 through transcription activation of SUZ12 (suppressor of zest 12 protein homolog). Conversely, inhibiting EZH2 increased HIF‐1α transcription, but not the transcription of other HIF family members. Additionally, the negative feedback regulation between EZH2 and HIF‐1α is confirmed in lung cancer patient tissues and a database of cell lines. Moreover, molecular prediction showed that a newly screened dual‐target compound, DYB‐03, forms multiple hydrogen bonds with HIF‐1α and EZH2 to effectively inhibit the activity of both targets. Subsequent studies revealed that DYB‐03 could better inhibit migration, invasion, and angiogenesis of lung cancer cells and HUVECs in vitro and in vivo compared to single agent. DYB‐03 showed promising antitumor activity in a xenograft tumor model by promoting apoptosis and inhibiting angiogenesis, which could be almost abolished by the deletion of HIF‐1α and EZH2. Notably, DYB‐03 could reverse 2‐ME2 and GSK126‐resistance in lung cancer. These findings clarified the molecular mechanism of cross‐regulation of HIF‐1α and EZH2, and the potential of DYB‐03 for clinical combination target therapy.
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Research context

OpenAlex topics: Cancer, Hypoxia, and Metabolism · Epigenetics and DNA Methylation · RNA modifications and cancer

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

School of Life Science and Biopharmaceutics Shenyang Pharmaceutical University Shenyang 110016 P. R. China

Benxi Institute of Pharmaceutical Research Shenyang Pharmaceutical University Benxi 117004 P. R. China

Key Laboratory of Structure‐Based Drug Design & Discovery of Ministry of Education School of Pharmaceutical Engineering Shenyang Pharmaceutical University Shenyang 110016 P. R. China

Department of Pharmacy Shengjing Hospital of China Medical University Shenyang 110004 P. R. China

School of Pharmacy Shenyang Pharmaceutical University Shenyang 110016 P. R. China

Research Program in Systems Oncology Faculty of Medicine University of Helsinki Helsinki 00290 Finland

Funding

National Natural Science Foundation of China · China Postdoctoral Science Foundation · Academy of Finland

References (63)

Show source-provided references
1. 10.3322/caac.2166010.3322/caac.21660 ↗
2. 10.1080/07357907.2022.211947910.1080/07357907.2022.2119479 ↗
3. 10.1038/s41568-019-0179-810.1038/s41568-019-0179-8 ↗
4. 10.3389/fphar.2022.103734110.3389/fphar.2022.1037341 ↗
5. 10.1093/nar/gkw110010.1093/nar/gkw1100 ↗
6. 10.3389/fphar.2022.106466110.3389/fphar.2022.1064661 ↗
7. 10.1016/j.stem.2021.10.00910.1016/j.stem.2021.10.009 ↗
8. 10.3390/cells1009234010.3390/cells10092340 ↗
9. 10.1016/j.phymed.2021.15356510.1016/j.phymed.2021.153565 ↗
10. 10.1038/nrc318310.1038/nrc3183 ↗
11. 10.1016/j.ccr.2008.01.03410.1016/j.ccr.2008.01.034 ↗
12. 10.1038/nrc246810.1038/nrc2468 ↗
13. 10.1186/s12943-019-1089-910.1186/s12943-019-1089-9 ↗
14. 10.1016/j.pharmthera.2016.04.00910.1016/j.pharmthera.2016.04.009 ↗
15. 10.1007/s10637-010-9455-x10.1007/s10637-010-9455-x ↗
16. 10.1158/1078-0432.CCR-07-080710.1158/1078-0432.CCR-07-0807 ↗
17. 10.1007/s10637-006-9208-z10.1007/s10637-006-9208-z ↗
18. 10.3816/CGC.2005.n.02410.3816/CGC.2005.n.024 ↗
19. 10.1039/C6CS00599C10.1039/C6CS00599C ↗
20. 10.1007/s13238-021-00846-710.1007/s13238-021-00846-7 ↗
21. 10.1016/j.semcancer.2020.12.00610.1016/j.semcancer.2020.12.006 ↗
22. 10.1038/s41571-019-0267-410.1038/s41571-019-0267-4 ↗
23. 10.1186/s12943-022-01579-910.1186/s12943-022-01579-9 ↗
24. 10.1016/j.biocel.2015.10.01610.1016/j.biocel.2015.10.016 ↗
25. 10.1038/s41416-019-0473-y10.1038/s41416-019-0473-y ↗
26. 10.1158/1078-0432.CCR-14-282010.1158/1078-0432.CCR-14-2820 ↗
27. 10.1111/febs.1311010.1111/febs.13110 ↗
28. 10.1038/nprot.2010.610.1038/nprot.2010.6 ↗
29. Malinda K. M. · Methods Mol. Med. · 2003 · 78 · 329
30. 10.1038/nature0978410.1038/nature09784 ↗
31. 10.1002/pro.364710.1002/pro.3647 ↗
32. 10.1038/s41429-021-00451-010.1038/s41429-021-00451-0 ↗
33. 10.1158/0008-5472.605.65.210.1158/0008-5472.605.65.2 ↗
34. Tan C. · Neuro‐Oncology · 2004 · 6 · 335
35. 10.1002/tcr.20180009110.1002/tcr.201800091 ↗
36. 10.3389/fmolb.2022.86676410.3389/fmolb.2022.866764 ↗
37. 10.1186/s13046-018-0851-y10.1186/s13046-018-0851-y ↗
38. 10.1016/j.pediatrneurol.2014.06.00810.1016/j.pediatrneurol.2014.06.008 ↗
39. 10.1080/15548627.2021.187222710.1080/15548627.2021.1872227 ↗
40. 10.1093/carcin/bgp01410.1093/carcin/bgp014 ↗
41. 10.1038/s41598-021-02400-110.1038/s41598-021-02400-1 ↗
42. 10.1158/0008-5472.CAN-11-096110.1158/0008-5472.CAN-11-0961 ↗
43. 10.1016/j.bbrc.2014.09.09210.1016/j.bbrc.2014.09.092 ↗
44. 10.1016/j.gde.2009.10.00910.1016/j.gde.2009.10.009 ↗
45. 10.1186/s12885-020-07531-810.1186/s12885-020-07531-8 ↗
46. 10.1172/JCI12665510.1172/JCI126655 ↗
47. Figueiredo C. C. · Histology and Histopathology · 2019 · 34 · 257
48. 10.1038/nrc118710.1038/nrc1187 ↗
49. 10.1007/s10637-010-9618-910.1007/s10637-010-9618-9 ↗
50. 10.1038/nrc381910.1038/nrc3819 ↗
51. 10.1038/nrclinonc.2013.4210.1038/nrclinonc.2013.42 ↗
52. 10.1016/j.redox.2019.10119510.1016/j.redox.2019.101195 ↗
53. 10.3858/emm.2009.41.12.10310.3858/emm.2009.41.12.103 ↗
54. 10.1007/s10059-010-0067-210.1007/s10059-010-0067-2 ↗
55. 10.1016/j.molcel.2005.02.01510.1016/j.molcel.2005.02.015 ↗
56. 10.1073/pnas.201440811810.1073/pnas.2014408118 ↗
57. 10.1038/bjc.2014.11610.1038/bjc.2014.116 ↗
58. 10.1038/bjc.2016.12510.1038/bjc.2016.125 ↗
59. 10.1002/cncr.2917510.1002/cncr.29175 ↗
60. 10.1016/j.lungcan.2014.02.01110.1016/j.lungcan.2014.02.011 ↗
61. 10.1016/j.cell.2012.01.02110.1016/j.cell.2012.01.021 ↗
62. 10.1073/pnas.191950711710.1073/pnas.1919507117 ↗
63. 10.1002/hep.3119610.1002/hep.31196 ↗