Pancreatic neuroendocrine tumor progression and resistance to everolimus: the crucial role of NF-kB and STAT3 interplay

J Endocrinol Invest. 2024 May;47(5):1101-1117. doi: 10.1007/s40618-023-02221-1. Epub 2023 Oct 26.

Abstract

Purpose: The finding of mTOR overactivation in patients affected by pancreatic neuroendocrine tumors (Pa-NETs) led to their treatment with the mTOR inhibitor everolimus. Unfortunately, the efficacy of everolimus is restricted by the occurrence of resistance. The mechanisms leading to Pa-NETs' progression and resistance are not well understood. Notably, chronic inflammation is implicated in NET development. NF-kB is involved in inflammation and drug resistance mechanisms through the activation of several mediators, including STAT3. In this respect, NF-κB and STAT3 interaction is implicated in the crosstalk between inflammatory and tumor cells.

Methods: We investigated the expression of NF-kB in different Pa-NETs by RT-qPCR and immunohistochemistry. Then, we studied the role of NF-κB and STAT3 interplay in QGP-1 cells. Subsequently, we assessed the impact of NF-κB and STAT3 inhibitors in QGP-1 cell proliferation and spheroids growth. Finally, we evaluated the implication of the NF-kB pathway in everolimus-resistant Pa-NET cells.

Results: We found that the increased NF-kB expression correlates with a higher grade in Pa-NETs. The activation of the STAT3 pathway induced by TNFα is mediated by NF-kB p65. NF-kB p65 and STAT3 inhibitors decrease QGP-1 viability, spheroids growth, and Pa-NETs cell proliferation. These effects are maintained in everolimus-resistant QGP-1R cells. Interestingly, we found that NF-kB, STAT3, IL-8, and SOCS3 are overexpressed in QGP-1R compared to QGP-1.

Conclusion: Since the NF-kB pathway is implicated in Pa-NETs' progression and resistance to everolimus, these data could explain the potential use of NF-kB as a novel therapeutic target in Pa-NET patients.

Keywords: Everolimus; NF-kB; Pancreatic neuroendocrine tumors; Resistance; STAT3.

MeSH terms

  • Antineoplastic Agents / pharmacology
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Drug Resistance, Neoplasm* / genetics
  • Everolimus* / pharmacology
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Interleukin-8 / genetics
  • NF-kappa B* / antagonists & inhibitors
  • NF-kappa B* / genetics
  • NF-kappa B* / metabolism
  • Neoplasm Grading
  • Neuroendocrine Tumors* / genetics
  • Pancreatic Neoplasms* / genetics
  • STAT3 Transcription Factor* / antagonists & inhibitors
  • STAT3 Transcription Factor* / metabolism
  • Spheroids, Cellular / drug effects
  • Transcriptional Activation / genetics
  • Tumor Cells, Cultured
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Tumor Necrosis Factor-alpha
  • NF-kappa B
  • STAT3 protein, human
  • STAT3 Transcription Factor
  • 4-methyl-N1-(3-phenylpropyl)benzene-1,2-diamine
  • AZD 1480
  • Antineoplastic Agents
  • Interleukin-8
  • Everolimus