journal article·2023-07Open access

IGFBP1 Sustains Cell Survival during Spatially‐Confined Migration and Promotes Tumor Metastasis

Guoqing Cai, Yijun Qi, Ping Wei, Hong Gao, Chenqi Xu, Yun Zhao, Xiujuan Qu, Feng Yao, Weiwei Yang

Advanced Science· Volume 10· Issue 21

Abstract

Abstract Cell migration is a pivotal step in metastatic process, which requires cancer cells to navigate a complex spatially‐confined environment, including tracks within blood vessels and in the vasculature of target organs. Here it is shown that during spatially‐confined migration, the expression of insulin‐like growth factor‐binding protein 1 (IGFBP1) is upregulated in tumor cells. Secreted IGFBP1 inhibits AKT1‐mediated phosphorylation of mitochondrial superoxide dismutase (SOD2) serine (S) 27 and enhances SOD2 activity. Enhanced SOD2 attenuates mitochondrial reactive oxygen species (ROS) accumulation in confined cells, which supports tumor cell survival in blood vessels of lung tissues, thereby accelerating tumor metastasis in mice. The levels of blood IGFBP1 correlate with metastatic recurrence of lung cancer patients. This finding reveals a unique mechanism by which IGFBP1 sustains cell survival during confined migration by enhancing mitochondrial ROS detoxification, thereby promoting tumor metastasis.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Cancer, Hypoxia, and Metabolism · Growth Hormone and Insulin-like Growth Factors · Cancer Cells and Metastasis

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

Affiliations

State Key Laboratory of Cell Biology Shanghai Key Laboratory of Molecular Andrology Shanghai Institute of Biochemistry and Cell Biology Center for Excellence in Molecular Cell Science Chinese Academy of Sciences University of Chinese Academy of Sciences Shanghai 200031 China

Key Laboratory of Systems Health Science of Zhejiang Province School of Life Science Hangzhou Institute for Advanced Study University of Chinese Academy of Sciences Hangzhou 310024 China

Department of Pathology Fudan University Shanghai Cancer Center Shanghai 200032 China

State Key Laboratory of Molecular Biology, Shanghai Science Research Center, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology Chinese Academy of Sciences shanghai 200031 China

Department of Medical Oncology The First Hospital of China Medical University Shenyang 110001 China

Department of Thoracic Surgery Shanghai Chest Hospital, Shanghai Jiao Tong University School of Medicine Shanghai 200031 China

Funding

National Natural Science Foundation of China · Program of Shanghai Academic Research Leader

References (56)

Show source-provided references
1. 10.1016/j.cell.2006.11.00110.1016/j.cell.2006.11.001 ↗
2. 10.1126/science.120354310.1126/science.1203543 ↗
3. 10.1093/intbio/zyz01610.1093/intbio/zyz016 ↗
4. 10.1016/j.semcdb.2009.08.00510.1016/j.semcdb.2009.08.005 ↗
5. 10.1007/s00418-008-0529-110.1007/s00418-008-0529-1 ↗
6. 10.4161/intv.2122310.4161/intv.21223 ↗
7. 10.1038/srep2383410.1038/srep23834 ↗
8. 10.1242/jcs.112.12.183510.1242/jcs.112.12.1835 ↗
9. 10.1038/nrc.2016.12310.1038/nrc.2016.123 ↗
10. 10.1038/s41580-019-0123-510.1038/s41580-019-0123-5 ↗
11. 10.7554/eLife.1937510.7554/eLife.19375 ↗
12. 10.1038/ncb303910.1038/ncb3039 ↗
13. 10.1007/s10585-011-9405-910.1007/s10585-011-9405-9 ↗
14. 10.1038/srep1475210.1038/srep14752 ↗
15. 10.1038/s41586-019-1847-210.1038/s41586-019-1847-2 ↗
16. 10.1210/er.2001-003310.1210/er.2001-0033 ↗
17. 10.1021/acs.chemrev.8b0004210.1021/acs.chemrev.8b00042 ↗
18. 10.1016/j.neuron.2018.09.04610.1016/j.neuron.2018.09.046 ↗
19. 10.1038/nature2140710.1038/nature21407 ↗
20. 10.1016/j.jphotobiol.2014.04.02510.1016/j.jphotobiol.2014.04.025 ↗
21. 10.1089/ars.2013.550710.1089/ars.2013.5507 ↗
22. 10.1007/s00392005024110.1007/s003920050241 ↗
23. 10.1161/CIRCRESAHA.109.20633410.1161/CIRCRESAHA.109.206334 ↗
24. 10.1038/nrc380310.1038/nrc3803 ↗
25. 10.1016/j.cbi.2005.12.00910.1016/j.cbi.2005.12.009 ↗
26. 10.1007/s12032-013-0805-310.1007/s12032-013-0805-3 ↗
27. 10.1046/j.1471-4159.2003.02113.x10.1046/j.1471-4159.2003.02113.x ↗
28. 10.1038/nrc372010.1038/nrc3720 ↗
29. 10.1002/jcp.104157020410.1002/jcp.1041570204 ↗
30. 10.1210/jcem.80.12.853058610.1210/jcem.80.12.8530586 ↗
31. Zhang X. · Cancer Res. · 2002 · 62 · 4369
32. 10.1073/pnas.90.22.1055310.1073/pnas.90.22.10553 ↗
33. 10.3389/fendo.2020.0023310.3389/fendo.2020.00233 ↗
34. 10.1038/s12276-020-0384-210.1038/s12276-020-0384-2 ↗
35. 10.1371/journal.pone.006489710.1371/journal.pone.0064897 ↗
36. 10.1016/j.yjmcc.2012.11.01110.1016/j.yjmcc.2012.11.011 ↗
37. 10.1002/(SICI)1097-4652(199805)175:2<156::AID-JCP5>3.0.CO;2-N10.1002/(SICI)1097-4652(199805)175:2<156::AID-JCP5>3.0.CO;2-N ↗
38. 10.1016/j.neuroscience.2019.08.00710.1016/j.neuroscience.2019.08.007 ↗
39. 10.3390/antiox604008610.3390/antiox6040086 ↗
40. 10.1089/10445499931505110.1089/104454999315051 ↗
41. Oberley L. W. · Cancer Res. · 1979 · 39 · 1141
42. Cobbs C. S. · Cancer Res. · 1996 · 15 · 3192
43. 10.1007/s00535005018110.1007/s005350050181 ↗
44. 10.1007/s00384-010-1041-310.1007/s00384-010-1041-3 ↗
45. 10.1158/0008-5472.CAN-07-120410.1158/0008-5472.CAN-07-1204 ↗
46. 10.1038/cddis.2013.2010.1038/cddis.2013.20 ↗
47. 10.1038/onc.2014.44910.1038/onc.2014.449 ↗
48. 10.1186/s12964-019-0450-310.1186/s12964-019-0450-3 ↗
49. 10.1016/j.celrep.2015.09.05710.1016/j.celrep.2015.09.057 ↗
50. 10.1016/j.molcel.2005.10.03310.1016/j.molcel.2005.10.033 ↗
51. 10.1158/1541-7786.MCR-20-062310.1158/1541-7786.MCR-20-0623 ↗
52. 10.1038/s41598-017-06128-910.1038/s41598-017-06128-9 ↗
53. 10.1158/0008-5472.CAN-03-346510.1158/0008-5472.CAN-03-3465 ↗
54. 10.1016/j.compbiomed.2015.05.02410.1016/j.compbiomed.2015.05.024 ↗
55. 10.1126/science.aba289410.1126/science.aba2894 ↗
56. 10.1038/cr.2016.15910.1038/cr.2016.159 ↗