journal article·2025-11Open access

5’‐Methylthioadenosine Metabolic Reprogramming Drives H3K79 Monomethylation‐Mediated PAK2 Upregulation to Promote Cadmium‐Induced Breast Cancer Progression by Impairing Autophagic Flux

Jingdian Li, Ping Deng, Tengfei Fan, Yuchen Qu, Miduo Tan, Yidan Liang, Peng Gao, Yongchun Peng, Mingke Qin, Sheng Jie, Rongrong Hao, Liting Wang, Lei Zhang, Chunhai Chen, Mindi He, Qinlong Ma, Yan Luo, Li Tian, Jia Xie, Mengyan Chen, Rui Tian, Min Li, Zhengping Yu, Zhou Zhou, Huifeng Pi

Advanced Science· Volume 12· Issue 44

Abstract

Abstract Cadmium (Cd) is a heavy metal that exhibits strong carcinogenic properties and promotes breast cancer (BC) progression. Autophagic flux dysfunction is involved in Cd‐induced BC progression, but the underlying molecular mechanisms remain unclear. Here, it is observed that impaired autophagic flux and metabolic reprogramming are notable features related to Cd‐induced proliferation, migration, and invasion in BC cell lines, including T‐47D and MCF‐7 cells. Through the integration of metabolomics, proteomics, and ingenuity pathway analysis, a metabolite–protein regulatory network is constructed, which revealed that 5′‐methylthioadenosine (MTA)‐mediated metabolic reprogramming plays a core regulatory role in the epigenetic‒autophagy axis involved in Cd‐induced autophagic flux impairment and BC progression. Mechanistically, Cd‐induced MTA depletion specifically increased DOT1L methyltransferase activity and H3K79me1 levels in the PAK2 promoter region, inducing the expression of PAK2 , which contributed to the autophagic flux blockade required for BC progression in Cd‐exposed BC cells and transgenic MMTV‐ErbB2 mice. Clinically, a significant negative correlation is also verified between MTA levels and TNM stage in BC patients; that is, advanced‐stage tumors exhibited notably lower MTA levels than early‐stage tumors. Thus, the study provides insights into metabolism‒epigenetic crosstalk in the context of Cd‐induced BC progression and highlights the importance of considering environmental factors in cancer healthcare.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Epigenetics and DNA Methylation · Autophagy in Disease and Therapy · Heavy Metal Exposure and Toxicity

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

Affiliations

Department of Occupational Health (Key Laboratory of Electromagnetic Radiation Protection Ministry of Education) Army Medical University (Third Military Medical University) Chongqing 400038 China

Department of Oral and Maxillofacial Surgery The Second Xiangya Hospital of Central South University Changsha Hunan 410007 China

Department of Breast Surgery Digestive Disease Medical Center Zhuzhou Hospital Affiliated to Xiangya School Medicine Central South University Zhuzhou Hunan 412000 China

School of Medicine Guangxi University Guangxi Zhuang Autonomous Region Nanning 530004 China

Biomedical Analysis Center Army Medical University Chongqing 400038 China

Center for Neurointelligence School of Medicine Chongqing University Chongqing 400030 China

State Key Laboratory of Trauma and Chemical Poisoning Army Medical University Chongqing 400038 China

Funding

National Natural Science Foundation of China

References (100+)

Show source-provided references
1. 10.1016/j.envint.2018.05.03010.1016/j.envint.2018.05.030 ↗
2. 10.1080/15548627.2015.105220810.1080/15548627.2015.1052208 ↗
3. 10.1289/EHP271610.1289/EHP2716 ↗
4. 10.1016/j.envres.2020.10978110.1016/j.envres.2020.109781 ↗
5. 10.1038/bjc.2017.14310.1038/bjc.2017.143 ↗
6. 10.1016/j.envres.2019.10863910.1016/j.envres.2019.108639 ↗
7. 10.1016/j.etap.2024.10449810.1016/j.etap.2024.104498 ↗
8. 10.3390/ijms2012302910.3390/ijms20123029 ↗
9. 10.1097/EDE.000000000000027710.1097/EDE.0000000000000277 ↗
10. 10.1007/s11356-017-0412-510.1007/s11356-017-0412-5 ↗
11. 10.1016/j.scitotenv.2024.17077310.1016/j.scitotenv.2024.170773 ↗
12. 10.1016/j.scitotenv.2023.16534810.1016/j.scitotenv.2023.165348 ↗
13. 10.1080/15548627.2020.172537810.1080/15548627.2020.1725378 ↗
14. 10.1038/s41467-020-17395-y10.1038/s41467-020-17395-y ↗
15. 10.1016/j.apsb.2020.12.01310.1016/j.apsb.2020.12.013 ↗
16. 10.1101/gad.156570710.1101/gad.1565707 ↗
17. 10.1080/15548627.2016.121738010.1080/15548627.2016.1217380 ↗
18. 10.1016/j.ecoenv.2021.11262610.1016/j.ecoenv.2021.112626 ↗
19. 10.15252/emmm.20191069810.15252/emmm.201910698 ↗
20. 10.7150/thno.5341710.7150/thno.53417 ↗
21. 10.1080/15548627.2015.105292810.1080/15548627.2015.1052928 ↗
22. 10.1158/0008-5472.CAN-22-356110.1158/0008-5472.CAN-22-3561 ↗
23. 10.1016/j.molcel.2017.01.02710.1016/j.molcel.2017.01.027 ↗
24. 10.1016/j.molcel.2021.03.00910.1016/j.molcel.2021.03.009 ↗
25. 10.1073/pnas.211038711810.1073/pnas.2110387118 ↗
26. 10.1126/science.aad521410.1126/science.aad5214 ↗
27. 10.1080/2162402X.2016.118480210.1080/2162402X.2016.1184802 ↗
28. Pascale R. M. · Anticancer Res. · 1991 · 11 · 1617
29. 10.1186/1471-2407-10-26510.1186/1471-2407-10-265 ↗
30. Ferra F. · Cancer Res. · 1984 · 44 · 2297
31. 10.18632/oncotarget.2023410.18632/oncotarget.20234 ↗
32. 10.1016/j.ebiom.2017.04.03110.1016/j.ebiom.2017.04.031 ↗
33. 10.1038/s41467-019-10486-510.1038/s41467-019-10486-5 ↗
34. 10.1016/j.biochi.2016.01.00510.1016/j.biochi.2016.01.005 ↗
35. 10.1126/sciadv.aav559010.1126/sciadv.aav5590 ↗
36. 10.1186/s13058-022-01547-710.1186/s13058-022-01547-7 ↗
37. 10.3390/biom1004053010.3390/biom10040530 ↗
38. 10.1158/1078-0432.CCR-21-129910.1158/1078-0432.CCR-21-1299 ↗
39. 10.1038/ncomms882110.1038/ncomms8821 ↗
40. 10.15252/embj.202010453210.15252/embj.2020104532 ↗
41. 10.1080/15548627.2017.142343910.1080/15548627.2017.1423439 ↗
42. 10.1080/15548627.2020.183928610.1080/15548627.2020.1839286 ↗
43. 10.1038/s41467-021-25572-w10.1038/s41467-021-25572-w ↗
44. 10.1080/15548627.2020.173944410.1080/15548627.2020.1739444 ↗
45. 10.1038/s41592-020-0781-410.1038/s41592-020-0781-4 ↗
46. 10.3390/cancers1320515710.3390/cancers13205157 ↗
47. 10.1038/s41467-019-10844-310.1038/s41467-019-10844-3 ↗
48. 10.3324/haematol.2018.19126210.3324/haematol.2018.191262 ↗
49. 10.1186/1476-4598-9-19610.1186/1476-4598-9-196 ↗
50. 10.1016/j.celrep.2016.05.01110.1016/j.celrep.2016.05.011 ↗
51. 10.2337/db15-031610.2337/db15-0316 ↗
52. 10.1007/s11356-015-5212-110.1007/s11356-015-5212-1 ↗
53. 10.1161/01.ATV.21.5.86310.1161/01.ATV.21.5.863 ↗
54. 10.1289/ehp.090099910.1289/ehp.0900999 ↗
55. 10.1016/j.ecoenv.2022.11427010.1016/j.ecoenv.2022.114270 ↗
56. 10.1016/j.envpol.2021.11650410.1016/j.envpol.2021.116504 ↗
57. 10.1016/j.marpolbul.2020.11104210.1016/j.marpolbul.2020.111042 ↗
58. 10.1016/j.jhazmat.2020.12378610.1016/j.jhazmat.2020.123786 ↗
59. 10.1002/ijc.3203910.1002/ijc.32039 ↗
60. 10.1093/toxsci/kfx20210.1093/toxsci/kfx202 ↗
61. 10.1080/15548627.2019.156994710.1080/15548627.2019.1569947 ↗
62. 10.1126/sciadv.abf914110.1126/sciadv.abf9141 ↗
63. 10.1016/j.redox.2021.10222710.1016/j.redox.2021.102227 ↗
64. 10.3390/cells103059710.3390/cells1030597 ↗
65. 10.1016/j.freeradbiomed.2023.02.00710.1016/j.freeradbiomed.2023.02.007 ↗
66. 10.3390/cancers1310249010.3390/cancers13102490 ↗
67. 10.1186/s13045-019-0773-y10.1186/s13045-019-0773-y ↗
68. 10.1038/cr.2016.10910.1038/cr.2016.109 ↗
69. 10.1073/pnas.240804912110.1073/pnas.2408049121 ↗
70. 10.1038/s42255-022-00553-510.1038/s42255-022-00553-5 ↗
71. 10.1126/sciadv.aav776910.1126/sciadv.aav7769 ↗
72. 10.1016/j.biocel.2024.10669410.1016/j.biocel.2024.106694 ↗
73. 10.1016/j.mce.2024.11241410.1016/j.mce.2024.112414 ↗
74. 10.31557/APJCP.2025.26.2.46510.31557/APJCP.2025.26.2.465 ↗
75. 10.1016/j.etap.2021.10368610.1016/j.etap.2021.103686 ↗
76. 10.1038/s41564-018-0272-x10.1038/s41564-018-0272-x ↗
77. 10.1073/pnas.211720911910.1073/pnas.2117209119 ↗
78. 10.1097/SHK.000000000000114110.1097/SHK.0000000000001141 ↗
79. 10.1186/s13578-022-00767-w10.1186/s13578-022-00767-w ↗
80. 10.1016/j.omto.2019.09.00510.1016/j.omto.2019.09.005 ↗
81. 10.1186/s13045-017-0400-810.1186/s13045-017-0400-8 ↗
82. 10.1016/j.immuni.2014.03.01010.1016/j.immuni.2014.03.010 ↗
83. 10.1186/s13045-019-0749-y10.1186/s13045-019-0749-y ↗
84. 10.1111/febs.1660510.1111/febs.16605 ↗
85. 10.1038/cr.2014.7110.1038/cr.2014.71 ↗
86. 10.1158/0008-5472.CAN-24-330410.1158/0008-5472.CAN-24-3304 ↗
87. 10.7150/thno.5865510.7150/thno.58655 ↗
88. 10.1186/s12885-024-12969-110.1186/s12885-024-12969-1 ↗
89. 10.3389/fimmu.2024.134768310.3389/fimmu.2024.1347683 ↗
90. 10.1186/1746-1596-9-5510.1186/1746-1596-9-55 ↗
91. 10.1016/j.cellsig.2005.12.00210.1016/j.cellsig.2005.12.002 ↗
92. 10.1016/j.bcp.2024.11620610.1016/j.bcp.2024.116206 ↗
93. 10.1155/2021/993615410.1155/2021/9936154 ↗
94. 10.1038/s41416-023-02523-410.1038/s41416-023-02523-4 ↗
95. 10.1002/advs.20240203010.1002/advs.202402030 ↗
96. 10.1038/s41420-020-00315-w10.1038/s41420-020-00315-w ↗
97. 10.1126/sciadv.abb877110.1126/sciadv.abb8771 ↗
98. 10.1016/j.ccr.2010.08.01210.1016/j.ccr.2010.08.012 ↗
99. 10.1093/nar/gkx61210.1093/nar/gkx612 ↗
100. 10.1016/j.envint.2022.10713910.1016/j.envint.2022.107139 ↗