Postprandial activation of leukocyte-endothelium interaction by fatty acids in the visceral adipose tissue microcirculation

FASEB J. 2019 Nov;33(11):11993-12007. doi: 10.1096/fj.201802637RR. Epub 2019 Aug 8.

Abstract

High-fat diet (HFD)-induced obesity is associated with accumulation of inflammatory cells predominantly in visceral adipose depots [visceral adipose tissue (VAT)] rather than in subcutaneous ones [subcutaneous adipose tissue (SAT)]. The cellular and molecular mechanisms responsible for this phenotypic difference remain poorly understood. Controversy also exists on the overall impact that adipose tissue inflammation has on metabolic health in diet-induced obesity. The endothelium of the microcirculation regulates both the transport of lipids and the trafficking of leukocytes into organ tissue. We hypothesized that the VAT and SAT microcirculations respond differently to postprandial processing of dietary fat. We also tested whether inhibition of endothelial postprandial responses to high-fat meals (HFMs) preserves metabolic health in chronic obesity. We demonstrate that administration of a single HFM or ad libitum access to a HFD for 24 h quickly induces a transient P-selectin-dependent inflammatory phenotype in the VAT but not the SAT microcirculation of lean wild-type mice. Studies in P-selectin-deficient mice confirmed a mechanistic role for P-selectin in the initiation of leukocyte trafficking, myeloperoxidase accumulation, and acute reduction in adiponectin mRNA expression by HFMs. Despite reduced VAT inflammation in response to HFMs, P-selectin-deficient mice still developed glucose intolerance and insulin resistance when chronically fed an HFD. Our data uncover a novel nutrient-sensing role of the vascular endothelium that instigates postprandial VAT inflammation. They also demonstrate that inhibition of this transient postprandial inflammatory response fails to correct metabolic dysfunction in diet-induced obesity.-Preston, K. J., Rom, I., Vrakas, C., Landesberg, G., Etwebe, Z., Muraoka, S., Autieri, M., Eguchi, S., Scalia, R. Postprandial activation of leukocyte-endothelium interaction by fatty acids in the visceral adipose tissue microcirculation.

Keywords: adipocyte; free fatty acids; inflammation; insulin resistance.

Publication types

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

MeSH terms

  • Animals
  • Blood Glucose / metabolism
  • Diet, High-Fat / adverse effects
  • Endothelium / metabolism*
  • Fatty Acids / metabolism*
  • Glucose Tolerance Test
  • Intra-Abdominal Fat / blood supply
  • Intra-Abdominal Fat / metabolism*
  • Leukocytes / metabolism*
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microcirculation*
  • Obesity / etiology
  • Obesity / metabolism
  • P-Selectin / genetics
  • P-Selectin / metabolism
  • Peroxidase / genetics
  • Peroxidase / metabolism
  • Postprandial Period
  • Subcutaneous Fat / metabolism

Substances

  • Blood Glucose
  • Fatty Acids
  • P-Selectin
  • Peroxidase