Prebiotic stachyose inhibits PRDX5 activity and castration-resistant prostate cancer development

Int J Biol Macromol. 2024 Oct;278(Pt 3):134844. doi: 10.1016/j.ijbiomac.2024.134844. Epub 2024 Aug 19.

Abstract

Stachyose (STA) is a prebiotic with poor oral bioavailability. In this study, we developed stachyose caproate (C6-STA), as a novel STA derivative, to demonstrate its high adsorption rate via oral administration. Pharmacokinetic analysis reveals that after absorption, the STA derived from C6-STA reaches its highest peak in the blood, liver, and kidney at 20 min, 30 min, and 12-24 h, with approximate levels of 1200 μg/mL, 0.14 μg/mL, and 0.2-0.3 μg/mL, respectively. In addition, the accumulation of STA in prostate tissues of mice with castration-resistant prostate cancer (CRPC) (1.75 μg/mg) is 10-fold higher than that in normal prostate tissues (0.14 μg/mg). The analysis also reveals that C6-STA has t1/2 of 12.8 h and Tmax of 0.25 h, indicating that it has the potential to be used as a promising drug in clinical practice. The toxicological evaluation shows no obvious side effects of C6-STA in mice administered with a 0.2 g/kg intragastric dose. Pharmacodynamic analysis and mechanism investigation of C6-STA show its ability to inhibit peroxiredoxin 5 (PRDX5) enzyme activity, disrupt PRDX5-nuclear factor erythroid 2-related factor 2 (NRF2) interaction, and decrease NAD(P)H quinone dehydrogenase 1 (NQO1) levels. NQO1 decrease further causes the accumulation of quinone radicals, which ultimately leads to the apoptosis of LNCaP cell-derived drug-tolerant persister (DTP) cells and slows CRPC progression. Our study discovered the anti-tumor activity of stachyose and shows that prebiotics have biological functions in vivo besides in the gut. Further investigation of C6-STA, especially in CRPC patients, is warranted.

Keywords: Castration-resistant prostate cancer; Drug-tolerant persister; Nuclear factor erythroid 2-related factor 2; Peroxiredoxin 5; Stachyose; Stachyose caproate.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Humans
  • Male
  • Mice
  • NAD(P)H Dehydrogenase (Quinone) / metabolism
  • NF-E2-Related Factor 2 / metabolism
  • Oligosaccharides / chemistry
  • Oligosaccharides / pharmacology
  • Peroxiredoxins* / metabolism
  • Prebiotics*
  • Prostatic Neoplasms, Castration-Resistant* / drug therapy
  • Prostatic Neoplasms, Castration-Resistant* / metabolism
  • Prostatic Neoplasms, Castration-Resistant* / pathology

Substances

  • Peroxiredoxins
  • Prebiotics
  • stachyose
  • Oligosaccharides
  • NAD(P)H Dehydrogenase (Quinone)
  • NF-E2-Related Factor 2