Short-term high-fat feeding induces islet macrophage infiltration and β-cell replication independently of insulin resistance in mice

Am J Physiol Endocrinol Metab. 2016 Oct 1;311(4):E763-E771. doi: 10.1152/ajpendo.00092.2016. Epub 2016 Aug 30.

Abstract

Short-term high-fat consumption stimulates mouse islet β-cell replication through unknown mechanisms. Resident macrophages (MΦs) are capable of secreting various factors involved in islet development and tissue remodeling. We hypothesized that a short-term high-fat diet (HFD) promotes MΦ infiltration in pancreatic islets and that MΦs serve as a regulator of β-cell replication. To test these hypotheses and dissect mechanisms involved in HFD-induced β-cell replication, adult C57BL/6J mice were fed a HFD for 7 days with or without administration of clodronate-containing liposomes, an MΦ-depleting agent. Mouse body and epididymal fat pad weights, and nonfasting blood glucose and fasting serum insulin levels were measured, and pancreatic islet β-cell replication, oxidative stress, and MΦ infiltration were examined. Short-term HFD promoted an increase in body and epididymal fat pad weight and blood glucose levels, along with an increased fasting serum insulin concentration. β-Cell replication, islet MΦ infiltration, and the percentage of inducible NO synthase positive MΦs in the islets increased significantly in mice fed the HFD. Immunofluorescence staining for 8-oxo-2'-deoxyguanosine or activated caspase-3 revealed no significant induction of DNA damage or apoptosis, respectively. In addition, no change in stromal-derived factor 1-expressing cells was found induced by HFD. Despite continuous elevation of nonfasting blood glucose and fasting serum insulin levels, depletion of MΦs through treatments of clodronate abrogated HFD-induced β-cell replication. These findings demonstrated that HFD-induced MΦ infiltration is responsible for β-cell replication. This study suggests the existence of MΦ-mediated mechanisms in β-cell replication that are independent of insulin resistance.

Keywords: HFD; macrophage; β-cell replication.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipose Tissue / cytology
  • Adipose Tissue / drug effects
  • Animals
  • Blood Glucose / metabolism
  • Cell Division
  • Clodronic Acid / pharmacology
  • Diet, High-Fat / adverse effects*
  • Epididymis / cytology
  • Epididymis / drug effects
  • Insulin / blood
  • Insulin Resistance*
  • Insulin-Secreting Cells / drug effects*
  • Islets of Langerhans / cytology*
  • Islets of Langerhans / drug effects
  • Macrophages / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Nitric Oxide Synthase Type II / biosynthesis
  • Oxidative Stress / drug effects

Substances

  • Blood Glucose
  • Insulin
  • Clodronic Acid
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse