Ageing is associated with molecular signatures of inflammation and type 2 diabetes in rat pancreatic islets

Diabetologia. 2016 Mar;59(3):502-11. doi: 10.1007/s00125-015-3837-8. Epub 2015 Dec 23.

Abstract

Aims/hypothesis: Ageing is a major risk factor for development of metabolic diseases such as type 2 diabetes. Identification of the mechanisms underlying this association could help to elucidate the relationship between age-associated progressive loss of metabolic health and development of type 2 diabetes. We aimed to determine molecular signatures during ageing in the endocrine pancreas.

Methods: Global gene transcription was measured in pancreatic islets isolated from young and old rats by Ilumina BeadChip arrays. Promoter DNA methylation was measured by Sequenom MassArray in 46 genes that showed differential expression with age, and correlations with expression were established. Alterations in morphological and cellular processes with age were determined by immunohistochemical methods.

Results: Age-related changes in gene expression were found at 623 loci (>1.5-fold, false discovery rate [FDR] <5%), with a significant (FDR < 0.05) enrichment in genes previously implicated in islet-cell function (Enpp1, Abcc8), type 2 diabetes (Tspan8, Kcnq1), inflammatory processes (Cxcl9, Il33) and extracellular matrix organisation (Col3a1, Dpt). Age-associated transcriptional differences negatively correlated with promoter DNA methylation at several loci related to inflammation, glucose homeostasis, cell proliferation and cell-matrix interactions (Il33, Cxcl9, Gpr119, Fbp2, Col3a1, Dpt, Spp1).

Conclusions/interpretation: Our findings suggest that a significant proportion of pancreatic islets develop a low-grade 'chronic' inflammatory status with ageing and this may trigger altered functional plasticity. Furthermore, we identified changes in expression of genes previously linked to type 2 diabetes and associated changes in DNA methylation that could explain their age-associated dysregulation. These findings provide new insights into key (epi)genetic signatures of the ageing process in islets.

Keywords: Ageing; DNA methylation; Epigenetics; Inflammageing; Pancreatic islets; Type 2 diabetes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging / genetics
  • Aging / physiology*
  • Animals
  • Chemokine CXCL9 / genetics
  • Collagen Type III / genetics
  • DNA Methylation / genetics
  • Diabetes Mellitus, Type 2 / etiology*
  • Diabetes Mellitus, Type 2 / metabolism
  • Epigenesis, Genetic / genetics
  • Inflammation / genetics*
  • Inflammation / metabolism
  • Islets of Langerhans / metabolism*
  • KCNQ1 Potassium Channel / genetics
  • Male
  • Phosphoric Diester Hydrolases / genetics
  • Pyrophosphatases / genetics
  • Rats
  • Sulfonylurea Receptors / genetics
  • Tetraspanins / genetics

Substances

  • Abcc8 protein, rat
  • COL3A1 protein, rat
  • CXCL9 protein, rat
  • Chemokine CXCL9
  • Collagen Type III
  • KCNQ1 Potassium Channel
  • Sulfonylurea Receptors
  • Tetraspanins
  • Tspan8 protein, rat
  • Phosphoric Diester Hydrolases
  • ectonucleotide pyrophosphatase phosphodiesterase 1
  • Pyrophosphatases