BNIP3L/BNIP3-Mediated Mitophagy Contributes to the Maintenance of Ovarian Cancer Stem Cells.

Li Na; Pal Khaket Tejinder; Yang Yajing; Wang Linzhou; Cai Shurui; Li Aidan; Wani Elsa; Miao Jessica; Zhang Nan; Zheng Qingfei; Zhang Junran; Liu Xuefeng; Karuppaiyah Selvendiran; Pei Dehua; Wang Qi-En
Journal of cellular and molecular medicine 2025
Open on PubMed

Ovarian cancer remains the most lethal gynaecological malignancy, with tumour recurrence and chemoresistance posing significant therapeutic challenges. Emerging evidence suggests that cancer stem cells (CSCs), a rare subpopulation within tumours with self-renewal and differentiation capacities, contribute to these hurdles. Therefore, elucidating the mechanisms that sustain CSCs is critical for improving treatment strategies. Mitophagy, a selective process for eliminating damaged mitochondria, plays a key role in maintaining cellular homeostasis, including CSC survival. Our study demonstrates that ovarian CSCs exhibit enhanced mitophagy, accompanied by elevated expression of the mitochondrial outer membrane receptors BNIP3 and BNIP3L. Knockdown of BNIP3 or BNIP3L significantly reduces mitophagy and impairs CSC self-renewal, indicating that receptor-mediated mitophagy is essential for CSC maintenance. Mechanistically, we identify that hyperactivated NF-κB signalling drives the upregulation of BNIP3 and BNIP3L in ovarian CSCs. Inhibition of NF-κB signalling, either via p65 knockdown or pharmacological inhibitors, effectively suppresses mitophagy. Furthermore, we demonstrate that elevated DNA-PK expression contributes to the constitutive activation of NF-κB signalling, thereby promoting mitophagy in ovarian CSCs. In summary, our findings establish that BNIP3/BNIP3L-mediated mitophagy, driven by DNA-PK-dependent NF-κB hyperactivation, is essential for CSC maintenance. Targeting the DNA-PK/NF-κB/BNIP3L-BNIP3 axis to disrupt mitochondrial quality control in CSCs represents a promising therapeutic strategy to prevent ovarian cancer recurrence and metastasis.

6 Figures Extracted
FIGURE 1
FIGURE 1 PMC
Ovarian CSCs exhibit enhanced mitophagy. (A, B) Mitochondrial mass was evaluated in spheroid and adherent cultured ovarian cancer cells. OVCAR3 and OV...
FIGURE 2
FIGURE 2 PMC
BNIP3L and BNIP3 are critical to the enhanced mitophagy in ovarian CSCs. (A) Differential expression of BNIP3 and BNIP3L in spheroid and adherent cult...
FIGURE 3
FIGURE 3 PMC
BNIP3L and BNIP3 play important roles in the maintenance of ovarian CSCs. (A–D) Effect of BNIP3L knockdown on the sphere formation ability. Adherent c...
FIGURE 4
FIGURE 4 PMC
NF‐κB signalling upregulates expression of BNIP3L and BNIP3 in ovarian cancer cells. (A) Effect of RelA/p65 knockdown on BNIP3L and BNIP3 expression i...
FIGURE 5
FIGURE 5 PMC
Increased expression of DNA‐PKcs contributes to NF‐κB‐mediated mitophagy in ovarian CSCs. (A) Differentially expressed proteins identified by LC–MS in...
FIGURE 6
FIGURE 6 PMC
Schematic illustration of the DNA‐PK/NF‐κB/BNIP3L‐BNIP3 axis in regulating mitophagy in ovarian CSCs. Elevated DNA‐PKcs in ovarian CSCs enhances canon...