Enzyme-mediated depletion of serum l-Met abrogates prostate cancer growth via multiple mechanisms without evidence of systemic toxicity

Proc Natl Acad Sci U S A. 2020 Jun 9;117(23):13000-13011. doi: 10.1073/pnas.1917362117. Epub 2020 May 20.

Abstract

Extensive studies in prostate cancer and other malignancies have revealed that l-methionine (l-Met) and its metabolites play a critical role in tumorigenesis. Preclinical and clinical studies have demonstrated that systemic restriction of serum l-Met, either via partial dietary restriction or with bacterial l-Met-degrading enzymes exerts potent antitumor effects. However, administration of bacterial l-Met-degrading enzymes has not proven practical for human therapy because of problems with immunogenicity. As the human genome does not encode l-Met-degrading enzymes, we engineered the human cystathionine-γ-lyase (hMGL-4.0) to catalyze the selective degradation of l-Met. At therapeutically relevant dosing, hMGL-4.0 reduces serum l-Met levels to >75% for >72 h and significantly inhibits the growth of multiple prostate cancer allografts/xenografts without weight loss or toxicity. We demonstrate that in vitro, hMGL-4.0 causes tumor cell death, associated with increased reactive oxygen species, S-adenosyl-methionine depletion, global hypomethylation, induction of autophagy, and robust poly(ADP-ribose) polymerase (PARP) cleavage indicative of DNA damage and apoptosis.

Keywords: hMGL; l-methionine depletion; prostate cancer.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Autophagy / drug effects
  • Cell Line, Tumor
  • Cystathionine gamma-Lyase / genetics
  • Cystathionine gamma-Lyase / isolation & purification
  • Cystathionine gamma-Lyase / pharmacology*
  • Cystathionine gamma-Lyase / therapeutic use
  • DNA Damage / drug effects
  • Enzyme Assays
  • Humans
  • Male
  • Methionine / antagonists & inhibitors*
  • Methionine / blood
  • Methionine / metabolism
  • Mice
  • Mutagenesis, Site-Directed*
  • Poly(ADP-ribose) Polymerases / metabolism
  • Prostatic Neoplasms / blood
  • Prostatic Neoplasms / drug therapy*
  • Reactive Oxygen Species / metabolism
  • Recombinant Proteins / genetics
  • Recombinant Proteins / isolation & purification
  • Recombinant Proteins / pharmacology
  • Recombinant Proteins / therapeutic use
  • Toxicity Tests, Acute
  • Xenograft Model Antitumor Assays

Substances

  • Reactive Oxygen Species
  • Recombinant Proteins
  • Methionine
  • Poly(ADP-ribose) Polymerases
  • Cystathionine gamma-Lyase