Apoptosis inhibitor of macrophage (AIM) is required for obesity-associated recruitment of inflammatory macrophages into adipose tissue

Proc Natl Acad Sci U S A. 2011 Jul 19;108(29):12072-7. doi: 10.1073/pnas.1101841108. Epub 2011 Jul 5.

Abstract

Infiltration of inflammatory macrophages into adipose tissues with the progression of obesity triggers insulin resistance and obesity-related metabolic diseases. We recently reported that macrophage-derived apoptosis inhibitor of macrophage (AIM) protein is increased in blood in line with obesity progression and is incorporated into adipocytes, thereby inducing lipolysis in adipose tissue. Here we show that such a response is required for the recruitment of adipose tissue macrophages. In vitro, AIM-dependent lipolysis induced an efflux of palmitic and stearic acids from 3T3-L1 adipocytes, thereby stimulating chemokine production in adipocytes via activation of toll-like receptor 4 (TLR4). In vivo administration of recombinant AIM to TLR4-deficient (TLR4(-/-)) mice resulted in induction of lipolysis without chemokine production in adipose tissues. Consistently, mRNA levels for the chemokines that affect macrophages were far lower in AIM-deficient (AIM(-/-)) than in wild-type (AIM(+/+)) obese adipose tissue. This reduction in chemokine production resulted in a marked prevention of inflammatory macrophage infiltration into adipose tissue in obese AIM(-/-) mice, although these mice showed more advanced obesity than AIM(+/+) mice on a high-fat diet. Diminished macrophage infiltration resulted in decreased inflammation locally and systemically in obese AIM(-/-) mice, thereby protecting them from insulin resistance and glucose intolerance. These results indicate that the increase in blood AIM is a critical event for the initiation of macrophage recruitment into adipose tissue, which is followed by insulin resistance. Thus, AIM suppression might be therapeutically applicable for the prevention of obesity-related metabolic disorders.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipose Tissue / cytology*
  • Animals
  • Apoptosis Regulatory Proteins / blood
  • Apoptosis Regulatory Proteins / metabolism*
  • Chemokines / metabolism
  • Enzyme-Linked Immunosorbent Assay
  • Flow Cytometry
  • Insulin Resistance / physiology
  • Macrophages / metabolism*
  • Macrophages / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Obesity / metabolism*
  • Oligonucleotides / genetics
  • Polymerase Chain Reaction
  • RNA, Small Interfering / genetics
  • Receptors, Immunologic / blood
  • Receptors, Immunologic / metabolism*
  • Receptors, Scavenger
  • Statistics, Nonparametric
  • Toll-Like Receptor 4 / metabolism

Substances

  • Apoptosis Regulatory Proteins
  • Cd5l protein, mouse
  • Chemokines
  • Oligonucleotides
  • RNA, Small Interfering
  • Receptors, Immunologic
  • Receptors, Scavenger
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4