The positive feedback loop between SP1 and MAP2K2 significantly drives resistance to VEGFR inhibitors in clear cell renal cell carcinoma

Int J Biol Sci. 2025 Jan 1;21(2):860-873. doi: 10.7150/ijbs.104591. eCollection 2025.

Abstract

Clear cell renal cell carcinoma (ccRCC) is one of the most common and aggressive malignancies of the urinary system. Despite being the first-line treatment for advanced ccRCC, vascular endothelial growth factor receptor inhibitors (VEGFRis) face significant limitations due to both initial and acquired resistance, which impede complete tumor eradication. Using a CRISPR/Cas9 library screening approach, MAP2K2 was identified as a resistance-associated gene for three prevalent VEGFRis (Sunitinib, Axitinib, and Sorafenib). A strong positive correlation was observed between MAP2K2 expression and resistance to these VEGFRis. Drug-resistant cell lines established through dose-escalation consistently exhibited elevated MAP2K2 expression and activation of the MEK/ERK signaling pathway. Notably, combining MEK inhibitors (MEKis) with VEGFRis significantly enhanced the sensitivity of these resistant cells, leading to pronounced cell death. Additionally, a positive feedback regulatory mechanism was discovered between SP1 and MAP2K2, wherein SP1 and MAP2K2 could enhance mutual expression, thereby maintaining MEK/ERK pathway activation. This study reveals that MEKis can effectively re-sensitize VEGFRi-resistant cells, offering a promising therapeutic strategy for overcoming VEGFRi resistance in ccRCC.

Keywords: Clear cell renal cell carcinoma; Drug resistance; MAP2K2; Vascular endothelial growth factor receptor inhibitors.

MeSH terms

  • Axitinib / pharmacology
  • Axitinib / therapeutic use
  • Carcinoma, Renal Cell* / drug therapy
  • Carcinoma, Renal Cell* / genetics
  • Carcinoma, Renal Cell* / metabolism
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm* / genetics
  • Humans
  • Kidney Neoplasms* / drug therapy
  • Kidney Neoplasms* / genetics
  • Kidney Neoplasms* / metabolism
  • MAP Kinase Kinase 2 / antagonists & inhibitors
  • MAP Kinase Kinase 2 / metabolism
  • MAP Kinase Signaling System
  • Protein Kinase Inhibitors / pharmacology
  • Protein Kinase Inhibitors / therapeutic use
  • Receptors, Vascular Endothelial Growth Factor / metabolism
  • Sorafenib / pharmacology
  • Sorafenib / therapeutic use
  • Sp1 Transcription Factor* / metabolism
  • Sunitinib / pharmacology
  • Sunitinib / therapeutic use

Substances

  • Sp1 Transcription Factor
  • MAP Kinase Kinase 2
  • Receptors, Vascular Endothelial Growth Factor
  • Protein Kinase Inhibitors
  • Sorafenib
  • MAP2K2 protein, human
  • SP1 protein, human
  • Sunitinib
  • Axitinib