journal article·2024-12Open access

Lactylation‐Driven IGF2BP3‐Mediated Serine Metabolism Reprogramming and RNA m6A—Modification Promotes Lenvatinib Resistance in HCC

Yuanxiang Lu, Jinghan Zhu, Yuxin Zhang, Wentao Li, Yixiao Xiong, Yunhui Fan, Yang Wu, Jianping Zhao, Changzhen Shang, Huifang Liang, Wanguang Zhang

Advanced Science· Volume 11· Issue 46

Abstract

Abstract Acquired resistance remains a bottleneck for molecular‐targeted therapy in advanced hepatocellular carcinoma (HCC). Metabolic adaptation and epigenetic remodeling are recognized as hallmarks of cancer that may contribute to acquired resistance. In various lenvatinib‐resistant models, increased glycolysis leads to lactate accumulation and lysine lactylation of IGF2BP3. This lactylation is crucial for capturing PCK2 and NRF2 mRNAs, thereby enhancing their expression. This process reprograms serine metabolism and strengthens the antioxidant defense system. Additionally, altered serine metabolism increases the availability of methylated substrates, such as S‐adenosylmethionine (SAM), for N6‐methyladenosine (m6A) methylation of PCK2 and NRF2 mRNAs. The lactylated IGF2BP3‐PCK2‐SAM‐m6A loop maintains elevated PCK2 and NRF2 levels, enhancing the antioxidant system and promoting lenvatinib resistance in HCC. Treatment with liposomes carrying siRNAs targeting IGF2BP3 or the glycolysis inhibitor 2‐DG restored lenvatinib sensitivity in vivo. These findings highlight the connection between metabolic reprogramming and epigenetic regulation and suggest that targeting metabolic pathways may offer new strategies to overcome lenvatinib resistance in HCC.
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Research context

OpenAlex topics: RNA modifications and cancer · Cancer-related gene regulation · Epigenetics and DNA Methylation

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

Affiliations

Hepatic Surgery Center Tongji Hospital Tongji Medical College Huazhong University of Science and Technology 1095 Jiefang Avenue Wuhan Hubei 430030 China

Department of Breast Surgery Zhengzhou University People's Hospital Henan Provincial People's Hospital Zhengzhou 450003 China

Hubei Key Laboratory of Hepato‐Pancreato‐Biliary Diseases Wuhan Hubei 430030 China

Department of Dermatology Tongji Hospital Tongji Medical College Huazhong University of Science and Technology Wuhan Hubei 430030 China

Key Laboratory of Organ Transplantation Ministry of Education NHC Key Laboratory of Organ Transplantation Key Laboratory of Organ Transplantation Chinese Academy of Medical Sciences Wuhan Hubei 430030 China

Department of Hepatobiliary Surgery Sun Yat‐sen Memorial Hospital of Sun Yat‐sen University Yanjiang West Road Guangzhou 510120 China

Funding

National Natural Science Foundation of China

References (74)

Show source-provided references
1. 10.3322/caac.2166010.3322/caac.21660 ↗
2. 10.1016/S1470-2045(23)00469-210.1016/S1470-2045(23)00469-2 ↗
3. 10.1038/s41586-021-03741-710.1038/s41586-021-03741-7 ↗
4. 10.1016/j.molcel.2022.01.02910.1016/j.molcel.2022.01.029 ↗
5. 10.1158/0008-5472.CAN-18-050510.1158/0008-5472.CAN-18-0505 ↗
6. 10.15252/emmm.20170831310.15252/emmm.201708313 ↗
7. 10.1186/s13059-021-02308-z10.1186/s13059-021-02308-z ↗
8. 10.1038/s42255-022-00710-w10.1038/s42255-022-00710-w ↗
9. Li W. · Autophagy · 2023 · 1
10. 10.1038/s41467-023-42025-810.1038/s41467-023-42025-8 ↗
11. 10.1126/science.aaw547310.1126/science.aaw5473 ↗
12. 10.1038/s41467-022-32101-w10.1038/s41467-022-32101-w ↗
13. 10.1016/j.drup.2023.10097610.1016/j.drup.2023.100976 ↗
14. 10.1016/j.cmet.2018.08.00610.1016/j.cmet.2018.08.006 ↗
15. 10.1038/nrc355710.1038/nrc3557 ↗
16. 10.1038/s41467-020-20223-y10.1038/s41467-020-20223-y ↗
17. 10.1172/JCI16171310.1172/JCI161713 ↗
18. 10.1038/s41467-023-36708-510.1038/s41467-023-36708-5 ↗
19. 10.1038/nrd400210.1038/nrd4002 ↗
20. 10.1016/j.bbrc.2022.08.04010.1016/j.bbrc.2022.08.040 ↗
21. 10.1158/0008-5472.CAN-13-203710.1158/0008-5472.CAN-13-2037 ↗
22. 10.1016/j.canlet.2023.21640510.1016/j.canlet.2023.216405 ↗
23. 10.1007/s13238-021-00846-710.1007/s13238-021-00846-7 ↗
24. 10.1158/0008-5472.CAN-21-075310.1158/0008-5472.CAN-21-0753 ↗
25. 10.1016/j.trecan.2018.11.00310.1016/j.trecan.2018.11.003 ↗
26. 10.1016/j.molcel.2015.08.01310.1016/j.molcel.2015.08.013 ↗
27. 10.1016/j.immuni.2020.09.01410.1016/j.immuni.2020.09.014 ↗
28. 10.1038/s41467-021-26842-310.1038/s41467-021-26842-3 ↗
29. 10.1016/j.molcel.2022.02.03310.1016/j.molcel.2022.02.033 ↗
30. 10.1038/s41556-018-0045-z10.1038/s41556-018-0045-z ↗
31. 10.1158/0008-5472.CAN-20-154110.1158/0008-5472.CAN-20-1541 ↗
32. 10.1038/s41467-019-12606-710.1038/s41467-019-12606-7 ↗
33. 10.1038/s41467-020-20223-y10.1038/s41467-020-20223-y ↗
34. 10.1016/j.molcel.2019.06.03910.1016/j.molcel.2019.06.039 ↗
35. 10.1111/nyas.1295610.1111/nyas.12956 ↗
36. 10.1136/gutjnl‐2022‐32692810.1136/gutjnl‐2022‐326928 ↗
37. 10.1016/j.molcel.2015.09.02510.1016/j.molcel.2015.09.025 ↗
38. 10.1038/onc.2014.4710.1038/onc.2014.47 ↗
39. 10.1158/2159-8290.CD-21-105910.1158/2159-8290.CD-21-1059 ↗
40. 10.1158/0008‐5472.Can‐22‐305910.1158/0008‐5472.Can‐22‐3059 ↗
41. 10.1038/s41586-019-1678-110.1038/s41586-019-1678-1 ↗
42. 10.1038/srep4591310.1038/srep45913 ↗
43. 10.1038/s41388-017-0070-610.1038/s41388-017-0070-6 ↗
44. 10.1016/j.canlet.2021.06.01610.1016/j.canlet.2021.06.016 ↗
45. Chen Y. · Am. J. Cancer Res. · 2023 · 13 · 886
46. b)S.‐F.Wang C.‐H.Wung M.‐S.Chen C.‐F.Chen P.‐H.Yin T.‐S.Yeh Y.‐L.Chang Y.‐C.Chou H.‐H.Hung H.‐C.Lee 2018 19 3389.10.3390/ijms19113389 ↗
47. 10.1074/jbc.M114.56692710.1074/jbc.M114.566927 ↗
48. 10.1073/pnas.171987111510.1073/pnas.1719871115 ↗
49. 10.1158/0008-5472.CAN-21-293410.1158/0008-5472.CAN-21-2934 ↗
50. 10.1016/j.jhep.2020.11.00810.1016/j.jhep.2020.11.008 ↗
51. 10.1038/s41467-019-10427-210.1038/s41467-019-10427-2 ↗
52. 10.1038/nchembio.207010.1038/nchembio.2070 ↗
53. 10.1038/s41467-022-30217-710.1038/s41467-022-30217-7 ↗
54. 10.1158/0008-5472.CAN-21-407410.1158/0008-5472.CAN-21-4074 ↗
55. 10.1053/j.gastro.2023.01.04110.1053/j.gastro.2023.01.041 ↗
56. 10.1186/s13046-018-0909-x10.1186/s13046-018-0909-x ↗
57. 10.1038/s41392-021-00594-410.1038/s41392-021-00594-4 ↗
58. 10.1073/pnas.162043311410.1073/pnas.1620433114 ↗
59. 10.1016/j.drup.2018.11.00110.1016/j.drup.2018.11.001 ↗
60. 10.1074/jbc.M114.63158010.1074/jbc.M114.631580 ↗
61. 10.1186/s13046-018-0728-010.1186/s13046-018-0728-0 ↗
62. 10.1186/s13045-020-01029-310.1186/s13045-020-01029-3 ↗
63. 10.1016/j.freeradbiomed.2012.07.02110.1016/j.freeradbiomed.2012.07.021 ↗
64. 10.1186/s13045-020-01029-310.1186/s13045-020-01029-3 ↗
65. Zhou S. · Am. J. Transl. Res. · 2016 · 8 · 2992
66. 10.1038/s41392-024-01772-w10.1038/s41392-024-01772-w ↗
67. 10.1158/0008-5472.CAN-22-260510.1158/0008-5472.CAN-22-2605 ↗
68. 10.1055/s-0030-124713210.1055/s-0030-1247132 ↗
69. 10.1158/0008-5472.CAN-21-414010.1158/0008-5472.CAN-21-4140 ↗
70. 10.1038/nm0202-12810.1038/nm0202-128 ↗
71. 10.7150/thno.4815210.7150/thno.48152 ↗
72. 10.1007/978-1-0716-1920-9_1410.1007/978-1-0716-1920-9_14 ↗
73. 10.1158/0008-5472.CAN-14-261510.1158/0008-5472.CAN-14-2615 ↗
74. 10.1038/s41418-023-01166-510.1038/s41418-023-01166-5 ↗