Thymoquinone Inhibits Renal Cell Cancer Metastasis Through AMPK/mTOR-Mediated Autophagy

Key Findings

Primary Discovery: Thymoquinone (TQ), extracted from Nigella sativa seeds, effectively inhibits renal cell carcinoma (RCC) metastasis by inducing autophagy through the AMPK/mTOR signaling pathway.

Mechanism of Action: TQ activates AMPK phosphorylation while decreasing mTOR phosphorylation, leading to autophagy induction that subsequently inhibits cancer cell migration, invasion, and epithelial-mesenchymal transition (EMT).

Experimental Results

Cell Viability and Dosing

  • IC50 values: 55 μmol/L in 786-O cells and 72 μmol/L in ACHN cells at 24 hours
  • 40 μmol/L concentration showed <20% inhibition of cell proliferation
  • No significant toxicity to normal renal tubular epithelial cells (HK-2) at doses <60 μmol/L

Anti-Metastatic Effects

  • Migration: TQ reduced cell migration in time- and concentration-dependent manner
  • Invasion: Decreased number of invaded cells correlated with increasing TQ concentration
  • EMT Reversal:
    • Upregulated epithelial marker E-cadherin
    • Downregulated mesenchymal markers (N-cadherin, vimentin)
    • Induced mesenchymal-epithelial transition (MET)

Autophagy Induction

  • Cytoplasmic vacuole accumulation observed via microscopy
  • Increased LC3-II expression in concentration-dependent manner
  • Enhanced autophagosome (yellow puncta) and autolysosome (red puncta) formation
  • Autophagy inhibitor 3-MA attenuated TQ’s anti-tumor effects

AMPK/mTOR Pathway Involvement

  • Pathway Activation: TQ elevated p-AMPK while reducing p-mTOR and p-S6K expression
  • Mechanistic Validation: AMPK inhibitor (compound C) blocked TQ-induced autophagy and anti-metastatic effects
  • Comparison: Everolimus (mTOR inhibitor) showed greater anti-tumor effects than TQ

In Vivo Validation

Xenograft Model Results

  • Tumor volume reduction: Control group reached ~500 mm³ vs TQ group ~270 mm³ after 4 weeks
  • Confirmed EMT reversal: increased E-cadherin, decreased N-cadherin expression
  • Metastasis Model: TQ significantly inhibited lung metastasis formation

Clinical Context

RCC Treatment Challenges

  • RCC accounts for 80% of kidney cancers
  • 30% of patients diagnosed with metastasis; one-third experience recurrence
  • Resistance to radiotherapy and chemotherapy
  • Current targeted therapies have limited efficiency and significant side effects

TQ Therapeutic Potential

  • Multi-cancer efficacy: Previously demonstrated against breast, gastric, cervical, colon, prostate, and bladder cancers
  • Safety profile: Plant-derived compound with established anti-inflammatory, anti-oxidant properties
  • Cost advantage: Potentially less expensive than current targeted therapies

Mechanistic Insights

Autophagy’s Dual Role in Cancer

  • Early stages: Suppresses cancer initiation by eliminating inflammation and genome instability
  • Advanced stages: Can promote tumor growth by providing metabolic substrates
  • Metastasis: Complex relationship where autophagy can both support and inhibit metastatic processes

AMPK/mTOR Pathway Significance

  • mTOR signaling activated in nearly 100% of RCC cases
  • mTORC1 inhibition increases autophagy
  • AMPK acts as cellular energy sensor regulating homeostatic balance
  • Direct phosphorylation of mTOR regulatory proteins by AMPK

Study Limitations and Future Directions

Drug Resistance Considerations

  • Current mTOR inhibitors face clinical resistance issues
  • TQ’s multi-pathway targeting approach may overcome single-target limitations
  • Combination therapy with autophagy modulators suggested

Comparative Efficacy

  • Everolimus demonstrated superior anti-tumor effects compared to TQ
  • However, TQ offers potential advantages in resistance prevention
  • Multi-component pathway targeting urgently needed

TL;DR: Thymoquinone from black seeds inhibits renal cell cancer metastasis by activating the AMPK/mTOR pathway to induce autophagy, which reverses epithelial-mesenchymal transition and reduces cancer cell migration/invasion. In vivo studies confirmed 46% tumor volume reduction and significant metastasis inhibition, suggesting TQ as a promising, cost-effective therapeutic alternative to current targeted therapies that face resistance issues.

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