Searching for Protein Off-Targets of Prostate-Specific Membrane Antigen-Targeting Radioligands in the Salivary Glands

Cancer Biother Radiopharm. 2024 Dec;39(10):721-732. doi: 10.1089/cbr.2024.0066. Epub 2024 Sep 13.

Abstract

Background: Prostate specific membrane antigen (PSMA)-targeted radioligand therapies represent a highly effective treatment for metastatic prostate cancer. However, high and sustain uptake of PSMA-ligands in the salivary glands led to dose limiting dry mouth (xerostomia), especially with α-emitters. The expression of PSMA and histologic analysis couldn't directly explain the toxicity, suggesting a potential off-target mediator for uptake. In this study, we searched for possible off-target non-PSMA protein(s) in the salivary glands. Methods: A machine-learning based quantitative structure activity relationship (QSAR) model was built for seeking the possible off-target(s). The resulting target candidates from the model prediction were subjected to further analysis for salivary protein expression and structural homology at key regions required for PSMA-ligand binding. Furthermore, cellular binding assays were performed utilizing multiple cell lines with high expression of the candidate proteins and low expression of PSMA. Finally, PSMA knockout (PSMA-/-) mice were scanned by small animal PET/MR using [68Ga]Ga-PSMA-11 for in-vivo validation. Results: The screening of the trained QSAR model did not yield a solid off-target protein, which was corroborated in part by cellular binding assays. Imaging using PSMA-/- mice further demonstrated markedly reduced PSMA-radioligand uptake in the salivary glands. Conclusion: Uptake of the PSMA-targeted radioligands in the salivary glands remains primarily PSMA-mediated. Further investigations are needed to illustrate a seemingly different process of uptake and retention in the salivary glands than that in prostate cancer.

Keywords: PSMA; QSAR; off-targets; targeted radioligand therapy.

MeSH terms

  • Animals
  • Antigens, Surface / genetics
  • Antigens, Surface / metabolism
  • Cell Line, Tumor
  • Gallium Isotopes
  • Gallium Radioisotopes
  • Glutamate Carboxypeptidase II* / genetics
  • Glutamate Carboxypeptidase II* / metabolism
  • Humans
  • Ligands
  • Machine Learning
  • Male
  • Mice
  • Mice, Knockout
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology
  • Quantitative Structure-Activity Relationship
  • Radiopharmaceuticals* / pharmacokinetics
  • Radiopharmaceuticals* / pharmacology
  • Salivary Glands* / metabolism

Substances

  • Glutamate Carboxypeptidase II
  • FOLH1 protein, human
  • Radiopharmaceuticals
  • Antigens, Surface
  • Ligands
  • Gallium Radioisotopes
  • gallium 68 PSMA-11
  • Gallium Isotopes