Reduced S-nitrosylation of TGFβ1 elevates its binding affinity toward the receptor and promotes fibrogenic signaling in the breast

J Biol Chem. 2024 Dec;300(12):108011. doi: 10.1016/j.jbc.2024.108011. Epub 2024 Nov 20.

Abstract

Transforming Growth Factor β (TGFβ) is a pleiotropic cytokine closely linked to tumors. Previously, we pharmacologically inhibited basal nitric oxide (NO) production in healthy mammary glands and found that this induced precancerous progression accompanied by upregulation of TGFβ and desmoplasia. In the present study, we tested whether NO directly S-nitrosylates (forms an NO-adduct at a cysteine residue) TGFβ for inhibition, whereas reduction of NO denitrosylates TGFβ for de-repression. We introduced mutations to 3 C-terminal cysteines of TGFβ1 which were predicted to be S-nitrosylated. We found that these mutations indeed impaired S-nitrosylation of TGFβ1 and shifted the binding affinity towards the receptor from the latent complex. Furthermore, in silico structural analyses predicted that these S-nitrosylation-defective mutations strengthen the dimerization of mature protein, whereas S-nitrosylation-mimetic mutations weaken the dimerization. Such differences in dimerization dynamics of TGFβ1 by denitrosylation/S-nitrosylation likely account for the shift of the binding affinities toward the receptor versus latent complex. Our findings, for the first time, unravel a novel mode of TGFβ regulation based on S-nitrosylation or denitrosylation of the protein.

Keywords: S-nitrosylation; TGFβ1; breast cancer; mammary epithelia; nitric oxide.

MeSH terms

  • Animals
  • Breast / metabolism
  • Breast / pathology
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Cysteine / metabolism
  • Female
  • Humans
  • Mutation
  • Nitric Oxide* / metabolism
  • Protein Binding
  • Protein Multimerization
  • Receptors, Transforming Growth Factor beta / genetics
  • Receptors, Transforming Growth Factor beta / metabolism
  • Signal Transduction*
  • Transforming Growth Factor beta1* / genetics
  • Transforming Growth Factor beta1* / metabolism

Substances

  • Transforming Growth Factor beta1
  • Nitric Oxide
  • TGFB1 protein, human
  • Cysteine
  • Receptors, Transforming Growth Factor beta