The proton-coupled oligopeptide transporters PEPT2, PHT1 and PHT2 mediate the uptake of carnosine in glioblastoma cells

Amino Acids. 2019 Jul;51(7):999-1008. doi: 10.1007/s00726-019-02739-w. Epub 2019 May 9.

Abstract

The previous studies demonstrated that carnosine (β-alanyl-L-histidine) inhibits the growth of tumor cells in vitro and in vivo. Considering carnosine for the treatment of glioblastoma, we investigated which proton-coupled oligopeptide transporters (POTs) are present in glioblastoma cells and how they contribute to the uptake of carnosine. Therefore, mRNA expression of the four known POTs (PEPT1, PEPT2, PHT1, and PHT2) was examined in three glioblastoma cell lines, ten primary tumor cell cultures, in freshly isolated tumor tissue and in healthy brain. Using high-performance liquid chromatography coupled to mass spectrometry, the uptake of carnosine was investigated in the presence of competitive inhibitors and after siRNA-mediated knockdown of POTs. Whereas PEPT1 mRNA was not detected in any sample, expression of the three other transporters was significantly increased in tumor tissue compared to healthy brain. In cell culture, PHT1 expression was comparable to expression in tumor tissue, PHT2 exhibited a slightly reduced expression, and PEPT2 expression was reduced to normal brain tissue levels. In the cell line LN405, the competitive inhibitors β-alanyl-L-alanine (inhibits all transporters) and L-histidine (inhibitor of PHT1/2) both inhibited the uptake of carnosine. SiRNA-mediated knockdown of PHT1 and PHT2 revealed a significantly reduced uptake of carnosine. Interestingly, despite its low expression at the level of mRNA, knockdown of PEPT2 also resulted in decreased uptake. In conclusion, our results demonstrate that the transporters PEPT2, PHT1, and PHT2 are responsible for the uptake of carnosine into glioblastoma cells and full function of all three transporters is required for maximum uptake.

Keywords: Carnosine; Glioblastoma; Peptide Transport; siRNA.

MeSH terms

  • Adult
  • Aged
  • Brain / metabolism
  • Brain Neoplasms / metabolism*
  • Carnosine / metabolism*
  • Cell Line, Tumor
  • Chromatography, High Pressure Liquid
  • Female
  • Glioblastoma / metabolism*
  • Histidine / metabolism
  • Humans
  • Male
  • Mass Spectrometry
  • Membrane Transport Proteins / genetics
  • Membrane Transport Proteins / metabolism*
  • Middle Aged
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Oligopeptides / metabolism
  • Peptide Transporter 1 / metabolism
  • RNA, Small Interfering / metabolism
  • Symporters / genetics
  • Symporters / metabolism*

Substances

  • Membrane Transport Proteins
  • Nerve Tissue Proteins
  • Oligopeptides
  • Peptide Transporter 1
  • RNA, Small Interfering
  • SLC15A1 protein, human
  • SLC15A3 protein, human
  • SLC15A4 protein, human
  • Symporters
  • hydrogen-coupled oligopeptide transporter PepT2
  • Histidine
  • Carnosine