Synergistic celecoxib and dimethyl-celecoxib combinations block cervix cancer growth through multiple mechanisms

PLoS One. 2024 Sep 26;19(9):e0308233. doi: 10.1371/journal.pone.0308233. eCollection 2024.

Abstract

Objective: The synergistic inhibitory effect of celecoxib (CXB) and dimethyl-celecoxib (DMC) plus paclitaxel (PA) or cisplatin (CP) on human cervix HeLa and SiHa cells was assessed at multiple cellular levels in order to elucidate the biochemical mechanisms triggered by the synergistic drug combinations.

Methods: The effect of CXB (5 μM)/CP (2 μM) or CXB (5 μM)/PA (15 μM) and DMC (15 μM)/CP (5 μM) or DMC (15 μM)/PA (20 μM) for 24 h was assayed on cancer cell proliferation, energy metabolism, mitophagy, ROS production, glycoprotein-P activity, DNA stability and apoptosis/necrosis.

Results: Drug combinations synergistically decreased HeLa and SiHa cell proliferation (>75%) and arrested cellular cycle by decreasing S and G2/M phases as well as the Ki67 content (HeLa) by 7.5-30 times. Cell viability was preserved (>90%) and no apparent effects on non-cancer cell growth were observed. Mitochondrial and glycolytic protein contents (44-95%) and ΔΨm (45-50%) in HeLa cells and oxidative phosphorylation and glycolysis fluxes (70-90%) in HeLa and SiHa cells were severely decreased, which in turn promoted a drastic fall in the ATP supply (85-88%). High levels of mitophagy proteins in HeLa cells and active mitochondrial digestion in HeLa and SiHa cells was observed. Mitochondrial fission and microtubule proteins were also affected. Intracellular ROS content (2-2.3-fold) and ROS production was stimulated (2.3-4 times), whereas content and activity of glycoprotein-P (45-85%) were diminished. DNA fragmentation was not observed and apoptosis/necrosis was not detected suggesting that cell death could be mainly associated to mitophagy induction.

Conclusions: CXB or DMC combination with canonical chemotherapy may be a promising chemotherapy strategy against cervical cancer growth, because it can selectively block multiple cell processes including inhibition of energy pathways and in consequence ATP-dependent processes such as cell proliferation, glycoprotein-P activity, ROS production and mitophagy, with no apparent effects on non-cancer cells.

MeSH terms

  • Antineoplastic Agents / pharmacology
  • Apoptosis* / drug effects
  • Celecoxib* / pharmacology
  • Cell Line, Tumor
  • Cell Proliferation* / drug effects
  • Cell Survival / drug effects
  • Cisplatin / pharmacology
  • Drug Synergism*
  • Female
  • Glycolysis / drug effects
  • HeLa Cells
  • Humans
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Mitophagy* / drug effects
  • Paclitaxel / pharmacology
  • Reactive Oxygen Species* / metabolism
  • Uterine Cervical Neoplasms* / drug therapy
  • Uterine Cervical Neoplasms* / metabolism
  • Uterine Cervical Neoplasms* / pathology

Substances

  • Celecoxib
  • Reactive Oxygen Species
  • Cisplatin
  • Paclitaxel
  • Antineoplastic Agents

Grants and funding

The present work was partially supported by grants from CONAHCyT-México to DXRC (No. 814560), CONAHCyT-México (No. 283144) and PAPIIT, DGAPA-UNAM, México to SRE (No. IA201823), and CONAHCyT-México (No. 6379) and National Institute of Chemical Physics and Biophysics (NICPB), Tallinn, Estonia Institutional Development Fund to RMS. There was no additional external funding received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.