Small molecular weight epigenetic inhibitors modulate the extracellular matrix during pancreatic acinar ductal metaplasia

Biochem Biophys Res Commun. 2024 Dec 3:736:150496. doi: 10.1016/j.bbrc.2024.150496. Epub 2024 Aug 3.

Abstract

The pancreatic ductal adenocarcinoma (PDAC) tumor microenvironment is distinguished by a high degree of fibrosis and inflammation, known as desmoplasia. Desmoplasia increases the stromal deposition and extracellular matrix (ECM) stiffness observed in the tumor microenvironment, contributing to the dampened penetration of pharmacological agents. The molecular and biophysical composition of the ECM during the earliest cellular changes in the development of PDAC, i.e. acinar ductal metaplasia (ADM), has not been extensively explored. We report that the mRNA expression of key protein components of the ECM increases during ADM in p48Cre/+;LSL-KrasG12D (KC) mouse acinar organoids cultured in Matrigel. Treatment of the organoids with small molecular weight epigenetic modulating compounds that inhibit or reverse ADM (largazole, FK228 and chaetocin) dramatically reduced the tissue mRNA expression of collagens, hyaluronan synthase, laminin and fibronectin. The storage moduli, determined by video tracking of fluorescent nanoparticles embedded into the Matrigel, increased during ADM and was reduced following treatment with the epigenetic modulating compounds. We report that the ECM of mouse organoids stiffens during ADM and is further enhanced by the presence of mutant Kras. Moreover, select HDAC and HMT inhibitors reduced the mRNA expression of ECM components and ECM stiffness during inhibition and reversal of ADM, suggesting that these compounds may be useful as adjuvants to enhance the tumor penetration of agents used to treat PDAC.

Keywords: Acinar ductal metaplasia; Biomechanics; Microrheology; Pancreas plasticity; Pancreatic cancer.

MeSH terms

  • Acinar Cells / drug effects
  • Acinar Cells / metabolism
  • Acinar Cells / pathology
  • Animals
  • Carcinoma, Pancreatic Ductal* / drug therapy
  • Carcinoma, Pancreatic Ductal* / genetics
  • Carcinoma, Pancreatic Ductal* / metabolism
  • Carcinoma, Pancreatic Ductal* / pathology
  • Depsipeptides
  • Epigenesis, Genetic* / drug effects
  • Extracellular Matrix* / drug effects
  • Extracellular Matrix* / metabolism
  • Histone Deacetylase Inhibitors / pharmacology
  • Metaplasia* / metabolism
  • Mice
  • Organoids / drug effects
  • Organoids / metabolism
  • Organoids / pathology
  • Pancreatic Ducts / drug effects
  • Pancreatic Ducts / metabolism
  • Pancreatic Ducts / pathology
  • Pancreatic Neoplasms / drug therapy
  • Pancreatic Neoplasms / genetics
  • Pancreatic Neoplasms / metabolism
  • Pancreatic Neoplasms / pathology
  • Tumor Microenvironment / drug effects

Substances

  • romidepsin
  • Histone Deacetylase Inhibitors
  • Depsipeptides