Dietary n-3 polyunsaturated fatty acids (PUFA) decrease obesity-associated Th17 cell-mediated inflammation during colitis

PLoS One. 2012;7(11):e49739. doi: 10.1371/journal.pone.0049739. Epub 2012 Nov 16.

Abstract

Clinical and experimental evidence suggests that obesity-associated inflammation increases disease activity during colitis, attributed in part to the effects of Th17 cells. Using a model of concurrent obesity and colitis, we monitored changes in critical immune cell subsets and inflammatory biomarker expression in three key tissues: visceral adipose tissue, colon (local inflammatory site) and spleen (systemic inflammatory site), and we hypothesized that n-3 PUFA would reduce the percentage of inflammatory immune cell subsets and suppress inflammatory gene expression, thereby improving the disease phenotype. Obesity was induced in C57BL/6 mice by feeding a high fat (HF) diet (59.2% kcal) alone or an isocaloric HF diet supplemented with fish oil (HF-FO) for 12 weeks. Colitis was induced via a 2.5% trinitrobenzene sulfonic acid (TNBS) enema. The HF-FO diet improved the obese phenotype by reducing i) serum hormone concentrations (leptin and resistin), ii) adipose tissue mRNA expression of inflammatory cytokines (MCP-1, IFNγ, IL-6, IL17F and IL-21) and iii) total (F4/80⁺ CD11b⁺) and inflammatory adipose tissue M1 (F4/80⁺ CD11c⁺) macrophage content compared to HF (P<0.05). In addition, the HF-FO diet reduced both colitis-associated disease severity and colonic mRNA expression of the Th17 cell master transcription factor (RORγτ) and critical cytokines (IL-6, IL-17A, IL-17F, IL-21, IL-23 and IFNγ) versus HF (P<0.05). Compared to HF, the percentage of both splenic Th17 and Th1 cells were reduced by the HF-FO group (P<0.05). Under ex vivo polarizing conditions, the percentage of HF-FO derived CD4⁺ T cells that reached Th17 cell effector status was suppressed (P = 0.05). Collectively, these results indicate that n-3 PUFA suppress Th1/Th17 cells and inflammatory macrophage subsets and reconfigure the inflammatory gene expression profile in diverse tissue sites in obese mice following the induction of colitis.

Publication types

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

MeSH terms

  • Adipose Tissue / drug effects
  • Adipose Tissue / immunology
  • Adipose Tissue / metabolism
  • Animals
  • Colitis / complications*
  • Colitis / diet therapy
  • Colitis / genetics
  • Colitis / immunology*
  • Colon / drug effects
  • Colon / immunology
  • Colon / pathology
  • Cytokines / immunology
  • Cytokines / metabolism
  • Diet, High-Fat
  • Dietary Fats
  • Dietary Supplements*
  • Disease Models, Animal
  • Fatty Acids, Omega-3 / administration & dosage
  • Fatty Acids, Omega-3 / pharmacology*
  • Gene Expression Profiling
  • Inflammation / complications
  • Inflammation / diet therapy
  • Inflammation / genetics
  • Inflammation / immunology
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / pathology
  • Lymphocyte Activation / immunology
  • Macrophages / immunology
  • Male
  • Mice
  • Obesity / complications*
  • Phenotype
  • Th1 Cells / drug effects
  • Th1 Cells / immunology
  • Th17 Cells / drug effects
  • Th17 Cells / immunology*

Substances

  • Cytokines
  • Dietary Fats
  • Fatty Acids, Omega-3