Cleavage of periostin by MMP9 protects mice from kidney cystic disease

PLoS One. 2023 Dec 1;18(12):e0294922. doi: 10.1371/journal.pone.0294922. eCollection 2023.

Abstract

The matrix metalloproteinase MMP9 influences cellular morphology and function, and plays important roles in organogenesis and disease. It exerts both protective and deleterious effects in renal pathology, depending upon its specific substrates. To explore new functions for MMP9 in kidney cysts formation and disease progression, we generated a mouse model by breeding juvenile cystic kidney (jck) mice with MMP9 deficient mice. Specifically, we provide evidence that MMP9 is overexpressed in cystic tissue where its enzymatic activity is increased 7-fold. MMP9 deficiency in cystic kidney worsen cystic kidney diseases by decreasing renal function, favoring cyst expansion and fibrosis. In addition, we find that periostin is a new critical substrate for MMP9 and in its absence periostin accumulates in cystic lining cells. As periostin promotes renal cyst growth and interstitial fibrosis in polycystic kidney diseases, we propose that the control of periostin by MMP9 and its associated intracellular signaling pathways including integrins, integrin-linked kinase and focal adhesion kinase confers to MMP9 a protective effect on the severity of the disease.

MeSH terms

  • Animals
  • Fibrosis
  • Kidney / pathology
  • Matrix Metalloproteinase 9* / genetics
  • Matrix Metalloproteinase 9* / metabolism
  • Mice
  • Polycystic Kidney Diseases* / pathology
  • Signal Transduction

Substances

  • Matrix Metalloproteinase 9

Grants and funding

These studies were supported by institutional funding from Institut National de la Santé et de la Recherche Médicale (INSERM) and Sorbonne Université to the laboratory INSERM U1155, grant from the Association pour l'Information et la Recherche sur les maladies Rénales Génétiques (AIRG) to BL and grants from the Agence Nationale de la Recherche (ANR) (grant Renalcyst, and grant AnBiCyst) to BL. The funders have no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.