Plasma endocannabinoid levels in lean, overweight, and obese humans: relationships to intestinal permeability markers, inflammation, and incretin secretion

Am J Physiol Endocrinol Metab. 2018 Oct 1;315(4):E489-E495. doi: 10.1152/ajpendo.00355.2017. Epub 2018 Feb 13.

Abstract

Intestinal production of endocannabinoid and oleoylethanolamide (OEA) is impaired in high-fat diet/obese rodents, leading to reduced satiety. Such diets also alter the intestinal microbiome in association with enhanced intestinal permeability and inflammation; however, little is known of these effects in humans. This study aimed to 1) evaluate effects of lipid on plasma anandamide (AEA), 2-arachidonyl- sn-glycerol (2-AG), and OEA in humans; and 2) examine relationships to intestinal permeability, inflammation markers, and incretin hormone secretion. Twenty lean, 18 overweight, and 19 obese participants underwent intraduodenal Intralipid infusion (2 kcal/min) with collection of endoscopic duodenal biopsies and blood. Plasma AEA, 2-AG, and OEA (HPLC/tandem mass spectrometry), tumor necrosis factor-α (TNFα), glucagon-like peptide-1 (GLP-1), and glucose-dependent insulinotropic peptide (GIP) (multiplex), and duodenal expression of occludin, zona-occludin-1 (ZO-1), intestinal-alkaline-phosphatase (IAP), and Toll-like receptor 4 (TLR4) (by RT-PCR) were assessed. Fasting plasma AEA was increased in obese compared with lean and overweight patients ( P < 0.05), with no effect of BMI group or ID lipid infusion on plasma 2-AG or OEA. Duodenal expression of IAP and ZO-1 was reduced in obese compared with lean ( P < 0.05), and these levels related negatively to plasma AEA ( P < 0.05). The iAUC for AEA was positively related to iAUC GIP ( r = 0.384, P = 0.005). Obese individuals have increased plasma AEA and decreased duodenal expression of ZO-1 and IAP compared with lean and overweight subjects. The relationships between plasma AEA with duodenal ZO-1, IAP, and GIP suggest that altered endocannabinoid signaling may contribute to changes in intestinal permeability, inflammation, and incretin release in human obesity.

Keywords: 2-arachidonylglycerol; anandamide; inflammation tight-junction proteins; intestinal fat sensors; n-acylethanolamines.

Publication types

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

MeSH terms

  • Adult
  • Alkaline Phosphatase / genetics
  • Arachidonic Acids / blood
  • Dietary Fats / metabolism*
  • Duodenum / metabolism*
  • Endocannabinoids / blood*
  • Female
  • GPI-Linked Proteins / genetics
  • Gastric Inhibitory Polypeptide / blood
  • Gene Expression
  • Glucagon-Like Peptide 1 / blood
  • Glycerides / blood
  • Humans
  • Incretins / metabolism*
  • Inflammation / immunology*
  • Male
  • Obesity / blood*
  • Obesity / immunology
  • Obesity / metabolism
  • Occludin / genetics
  • Oleic Acids / blood
  • Overweight / blood
  • Overweight / immunology
  • Overweight / metabolism
  • Permeability
  • Polyunsaturated Alkamides / blood
  • Thinness / blood
  • Thinness / immunology
  • Thinness / metabolism
  • Toll-Like Receptor 4 / genetics
  • Tumor Necrosis Factor-alpha / immunology
  • Zonula Occludens-1 Protein / genetics

Substances

  • Arachidonic Acids
  • Dietary Fats
  • Endocannabinoids
  • GPI-Linked Proteins
  • Glycerides
  • Incretins
  • OCLN protein, human
  • Occludin
  • Oleic Acids
  • Polyunsaturated Alkamides
  • TJP1 protein, human
  • TLR4 protein, human
  • TNF protein, human
  • Toll-Like Receptor 4
  • Tumor Necrosis Factor-alpha
  • Zonula Occludens-1 Protein
  • oleoylethanolamide
  • Gastric Inhibitory Polypeptide
  • Glucagon-Like Peptide 1
  • glyceryl 2-arachidonate
  • ALPI protein, human
  • Alkaline Phosphatase
  • anandamide