Latent-Transforming Growth Factor β-Binding Protein 1/Transforming Growth Factor β1 Complex Drives Antitumoral Effects upon ERK5 Targeting in Melanoma

Am J Pathol. 2024 Aug;194(8):1581-1591. doi: 10.1016/j.ajpath.2024.03.015. Epub 2024 May 3.

Abstract

Melanoma is the deadliest skin cancer, with a poor prognosis in advanced stages. While available treatments have improved survival, long-term benefits are still unsatisfactory. The mitogen-activated protein kinase extracellular signal-regulated kinase 5 (ERK5) promotes melanoma growth, and ERK5 inhibition determines cellular senescence and the senescence-associated secretory phenotype. Here, latent-transforming growth factor β-binding protein 1 (LTBP1) mRNA was found to be up-regulated in A375 and SK-Mel-5 BRAF V600E melanoma cells after ERK5 inhibition. In keeping with a key role of LTBP1 in regulating transforming growth factor β (TGF-β), TGF-β1 protein levels were increased in lysates and conditioned media of ERK5-knockdown (KD) cells, and were reduced upon LTBP1 KD. Both LTBP1 and TGF-β1 proteins were increased in melanoma xenografts in mice treated with the ERK5 inhibitor XMD8-92. Moreover, treatment with conditioned media from ERK5-KD melanoma cells reduced cell proliferation and invasiveness, and TGF-β1-neutralizing antibodies impaired these effects. In silico data sets revealed that higher expression levels of both LTBP1 and TGF-β1 mRNA were associated with better overall survival of melanoma patients. Increased LTBP1 or TGF-β1 expression played a beneficial role in patients treated with anti-PD1 immunotherapy, making a possible immunosuppressive role of LTBP1/TGF-β1 unlikely upon ERK5 inhibition. This study, therefore, identifies additional desirable effects of ERK5 targeting, providing evidence of an ERK5-dependent tumor-suppressive role of TGF-β in melanoma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Proliferation*
  • Humans
  • Latent TGF-beta Binding Proteins* / genetics
  • Latent TGF-beta Binding Proteins* / metabolism
  • Melanoma* / drug therapy
  • Melanoma* / genetics
  • Melanoma* / metabolism
  • Melanoma* / pathology
  • Mice
  • Mitogen-Activated Protein Kinase 7* / genetics
  • Mitogen-Activated Protein Kinase 7* / metabolism
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / pathology
  • Transforming Growth Factor beta1* / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Latent TGF-beta Binding Proteins
  • Mitogen-Activated Protein Kinase 7
  • Transforming Growth Factor beta1
  • LTBP1 protein, human
  • MAPK7 protein, human
  • TGFB1 protein, human