An infection-induced oxidation site regulates legumain processing and tumor growth

Nat Chem Biol. 2022 Jul;18(7):698-705. doi: 10.1038/s41589-022-00992-x. Epub 2022 Mar 24.

Abstract

Oxidative stress is a defining feature of most cancers, including those that stem from carcinogenic infections. Reactive oxygen species can drive tumor formation, yet the molecular oxidation events that contribute to tumorigenesis are largely unknown. Here we show that inactivation of a single, redox-sensitive cysteine in the host protease legumain, which is oxidized during infection with the gastric cancer-causing bacterium Helicobacter pylori, accelerates tumor growth. By using chemical proteomics to map cysteine reactivity in human gastric cells, we determined that H. pylori infection induces oxidation of legumain at Cys219. Legumain oxidation dysregulates intracellular legumain processing and decreases the activity of the enzyme in H. pylori-infected cells. We further show that the site-specific loss of Cys219 reactivity increases tumor growth and mortality in a xenograft model. Our findings establish a link between an infection-induced oxidation site and tumorigenesis while underscoring the importance of cysteine reactivity in tumor growth.

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

  • Cell Transformation, Neoplastic / metabolism
  • Cysteine / metabolism
  • Cysteine Endopeptidases* / metabolism
  • Helicobacter Infections*
  • Helicobacter pylori*
  • Humans
  • Oxidation-Reduction
  • Stomach Neoplasms* / metabolism
  • Stomach Neoplasms* / microbiology
  • Stomach Neoplasms* / pathology

Substances

  • Cysteine Endopeptidases
  • asparaginylendopeptidase
  • Cysteine