Targeting NPM1 inhibits proliferation and promotes apoptosis of hepatic progenitor cells via suppression of mTOR signalling pathway

  • Stem Cell Res Ther. 2024 Sep 11;15(1):292. doi: 10.1186/s13287-024-03898-8.
Ping Wang  1  2  3 Min Wang  4  5  6 Lin Liu  4  5  6 Hongyi Li  4  5  6 Helin Liu  4  5  6 Jiangbo Ren  4  5  6 Tianhui Liu  4  5  6 Min Cong  4  5  6 Zhijun Zhu  6  7  8 Xinyan Zhao  4  5  6 Liying Sun  9  10  11 Jidong Jia  12  13  14
Affiliations
  • 1. Liver Research Center, Beijing Friendship Hospital, Capital Medical University, Beijing, 100050, China. [email protected].
  • 2. Beijing Key Laboratory On Translational Medicine On Liver Cirrhosis, Beijing, 100050, China. [email protected].
  • 3. National Clinical Research Center for Digestive Disease, Beijing, 100069, China. [email protected].
  • 4. Liver Research Center, Beijing Friendship Hospital, Capital Medical University, Beijing, 100050, China.
  • 5. Beijing Key Laboratory On Translational Medicine On Liver Cirrhosis, Beijing, 100050, China.
  • 6. National Clinical Research Center for Digestive Disease, Beijing, 100069, China.
  • 7. Liver Transplantation Center, Beijing Friendship Hospital, Capital Medical University, Beijing, 100050, China.
  • 8. Clinical Center for Paediatric Liver Transplantation, Capital Medical University, Beijing, 100069, China.
  • 9. Liver Research Center, Beijing Friendship Hospital, Capital Medical University, Beijing, 100050, China. [email protected].
  • 10. Beijing Key Laboratory On Translational Medicine On Liver Cirrhosis, Beijing, 100050, China. [email protected].
  • 11. National Clinical Research Center for Digestive Disease, Beijing, 100069, China. [email protected].
  • 12. Liver Research Center, Beijing Friendship Hospital, Capital Medical University, Beijing, 100050, China. [email protected].
  • 13. Beijing Key Laboratory On Translational Medicine On Liver Cirrhosis, Beijing, 100050, China. [email protected].
  • 14. National Clinical Research Center for Digestive Disease, Beijing, 100069, China. [email protected].
Abstract

Background: Hepatic progenitor cells serve not only as the origin of combined hepatocellular cholangiocarcinoma (cHCC-CCA) but are also responsible for malignancy recurrence after surgical resection. Nucleophosmin 1 (NPM1) has been implicated in Cancer metastasis and poor prognosis. This study aimed to determine the expression of NPM1 by hepatic progenitor cells in cHCC-CCA and the effects of targeting NPM1 on hepatic progenitor cells and BEL-7402 cells with characteristics of both progenitor cells and cHCC-CCA.

Methods: First, NPM1 was detected by RT‒PCR, western blotting, and double-immunofluorescence staining in cHCC-CCA tissues. NPM1 expression was subsequently analysed in rat hepatic progenitor cells cultured in vitro and in interleukin 6 (IL6)-treated cells. The effects and mechanism of NPM1 on hepatic progenitor cells were determined by knocking down NPM1 and performing RNA Sequencing analysis. Finally, NSC348884, a small-molecule inhibitor that disrupts NPM1 dimer formation, was used to confirm the function of NPM1 in BEL-7402 cells.

Results: Both human hepatic progenitor cells in cHCC-CCA tissues and rat in vitro cultured hepatic progenitor cells highly expressed NPM1. IL6, a cytokine involved in the malignant transformation of hepatic progenitor cells, dose-dependently increased NPM1 and PCNA expression. Knocking down NPM1 reduced IL6R transcription (P < 0.0001) and inhibited the proliferation (P = 0.0065) of hepatic progenitor cells by suppressing the mTOR signalling pathway and activating the Apoptosis pathway. Furthermore, knocking down NPM1 in hepatic progenitor cells resulted in more apoptotic cells (7.33 ± 0.09% vs. 3.76 ± 0.13%, P < 0.0001) but fewer apoptotic cells in the presence of NSC348884 (47.57 ± 0.49% vs. 63.40 ± 0.05%, P = 0.0008) than in the control cells, suggesting that low-NPM1-expressing cells are more resistant to NSC348884. In addition, NSC348884 induced the Apoptosis of BEL-7402 cells with an IC50 of 2.77 μmol/L via the downregulation of the IL-6R and mTOR signalling pathways and inhibited the growth of BEL-7402 cells in a subcutaneous xenograft tumour model (P = 0.0457).

Conclusions: Targeting NPM1 inhibits proliferation and induces Apoptosis in hepatic progenitor cells and BEL-7402 cells, thus serving as a potential therapy for cHCC-CCA.

Keywords
Apoptosis; Liver progenitor cells; Nucleophosmin 1; mTOR signalling pathway.
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