High-fat meals induce systemic cytokine release without evidence of endotoxemia-mediated cytokine production from circulating monocytes or myeloid dendritic cells

Christopher L. Fogarty, Janne K. Nieminen, Lina Peräneva, Mariann I. Lassenius, Aila J. Ahola, Marja Riitta Taskinen, Matti Jauhiainen, Juha Kirveskari, Pirkko Pussinen, Sohvi Hörkkö, Ville Petteri Mäkinen, Daniel Gordin, Carol Forsblom, Per Henrik Groop, Outi Vaarala, Markku Lehto

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Aims: Dietary fats have been shown to promote the translocation of bacterial endotoxins from the gut into circulation, which may induce systemic inflammation and modulate the inflammatory response of circulating immune cells. The aim of this study was to determine the effect of the postprandial milieu on inflammation and the inflammatory response of antigen presenting cells in the context of type 1 diabetes (T1D). Materials and methods: Eleven patients with T1D and eleven nondiabetic controls were recruited as part of the FinnDiane study and given two fatty meals during 1 day. Cytokine responses in monocytes and myeloid dendritic cells (mDCs) as well as serum lipopolysaccharide activity levels, triglyceride concentrations and cytokine concentrations were measured from fasting and postprandial blood samples. Results: Postprandially, patients with T1D and controls showed significant increases in eight inflammatory cytokines (IL-6, TNF-α, IL-1β, IFN-α, IL-10, IFN-γ, IL-12 and MIP-1β) without concomitant increase in serum LPS activity. Serum cytokine production was similar in both groups. No postprandial change was seen in the IL-6, TNF-α or IL-1β production of mDCs or monocytes. At fasting, diabetic mDCs exhibited higher LPS-induced IL-6 and IL-1β production than controls. Conclusions: Acute high-fat meals increase circulating cytokines but have no effect on serum lipopolysaccharide activity levels or cytokine production in circulating mDCs or monocytes. Our results suggest that postprandial increase in serum cytokine levels is neither mediated by circulating endotoxins nor the activation of circulating innate cells. The production of high-fat meal-induced inflammatory markers is most likely regulated at the tissue level.

LanguageEnglish
Pages315-322
Number of pages8
JournalActa Diabetologica
Volume52
Issue number2
DOIs
Publication statusPublished - 3 Sep 2015

Keywords

  • Cytokines
  • Endotoxin
  • High-fat diet
  • Inflammation
  • Lipopolysaccharide
  • Type 1 diabetes

ASJC Scopus subject areas

  • Internal Medicine
  • Endocrinology, Diabetes and Metabolism
  • Endocrinology

Cite this

Fogarty, Christopher L. ; Nieminen, Janne K. ; Peräneva, Lina ; Lassenius, Mariann I. ; Ahola, Aila J. ; Taskinen, Marja Riitta ; Jauhiainen, Matti ; Kirveskari, Juha ; Pussinen, Pirkko ; Hörkkö, Sohvi ; Mäkinen, Ville Petteri ; Gordin, Daniel ; Forsblom, Carol ; Groop, Per Henrik ; Vaarala, Outi ; Lehto, Markku. / High-fat meals induce systemic cytokine release without evidence of endotoxemia-mediated cytokine production from circulating monocytes or myeloid dendritic cells. In: Acta Diabetologica. 2015 ; Vol. 52, No. 2. pp. 315-322.
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abstract = "Aims: Dietary fats have been shown to promote the translocation of bacterial endotoxins from the gut into circulation, which may induce systemic inflammation and modulate the inflammatory response of circulating immune cells. The aim of this study was to determine the effect of the postprandial milieu on inflammation and the inflammatory response of antigen presenting cells in the context of type 1 diabetes (T1D). Materials and methods: Eleven patients with T1D and eleven nondiabetic controls were recruited as part of the FinnDiane study and given two fatty meals during 1 day. Cytokine responses in monocytes and myeloid dendritic cells (mDCs) as well as serum lipopolysaccharide activity levels, triglyceride concentrations and cytokine concentrations were measured from fasting and postprandial blood samples. Results: Postprandially, patients with T1D and controls showed significant increases in eight inflammatory cytokines (IL-6, TNF-α, IL-1β, IFN-α, IL-10, IFN-γ, IL-12 and MIP-1β) without concomitant increase in serum LPS activity. Serum cytokine production was similar in both groups. No postprandial change was seen in the IL-6, TNF-α or IL-1β production of mDCs or monocytes. At fasting, diabetic mDCs exhibited higher LPS-induced IL-6 and IL-1β production than controls. Conclusions: Acute high-fat meals increase circulating cytokines but have no effect on serum lipopolysaccharide activity levels or cytokine production in circulating mDCs or monocytes. Our results suggest that postprandial increase in serum cytokine levels is neither mediated by circulating endotoxins nor the activation of circulating innate cells. The production of high-fat meal-induced inflammatory markers is most likely regulated at the tissue level.",
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Fogarty, CL, Nieminen, JK, Peräneva, L, Lassenius, MI, Ahola, AJ, Taskinen, MR, Jauhiainen, M, Kirveskari, J, Pussinen, P, Hörkkö, S, Mäkinen, VP, Gordin, D, Forsblom, C, Groop, PH, Vaarala, O & Lehto, M 2015, 'High-fat meals induce systemic cytokine release without evidence of endotoxemia-mediated cytokine production from circulating monocytes or myeloid dendritic cells', Acta Diabetologica, vol. 52, no. 2, pp. 315-322. https://doi.org/10.1007/s00592-014-0641-8

High-fat meals induce systemic cytokine release without evidence of endotoxemia-mediated cytokine production from circulating monocytes or myeloid dendritic cells. / Fogarty, Christopher L.; Nieminen, Janne K.; Peräneva, Lina; Lassenius, Mariann I.; Ahola, Aila J.; Taskinen, Marja Riitta; Jauhiainen, Matti; Kirveskari, Juha; Pussinen, Pirkko; Hörkkö, Sohvi; Mäkinen, Ville Petteri; Gordin, Daniel; Forsblom, Carol; Groop, Per Henrik; Vaarala, Outi; Lehto, Markku.

In: Acta Diabetologica, Vol. 52, No. 2, 03.09.2015, p. 315-322.

Research output: Contribution to journalArticle

TY - JOUR

T1 - High-fat meals induce systemic cytokine release without evidence of endotoxemia-mediated cytokine production from circulating monocytes or myeloid dendritic cells

AU - Fogarty, Christopher L.

AU - Nieminen, Janne K.

AU - Peräneva, Lina

AU - Lassenius, Mariann I.

AU - Ahola, Aila J.

AU - Taskinen, Marja Riitta

AU - Jauhiainen, Matti

AU - Kirveskari, Juha

AU - Pussinen, Pirkko

AU - Hörkkö, Sohvi

AU - Mäkinen, Ville Petteri

AU - Gordin, Daniel

AU - Forsblom, Carol

AU - Groop, Per Henrik

AU - Vaarala, Outi

AU - Lehto, Markku

PY - 2015/9/3

Y1 - 2015/9/3

N2 - Aims: Dietary fats have been shown to promote the translocation of bacterial endotoxins from the gut into circulation, which may induce systemic inflammation and modulate the inflammatory response of circulating immune cells. The aim of this study was to determine the effect of the postprandial milieu on inflammation and the inflammatory response of antigen presenting cells in the context of type 1 diabetes (T1D). Materials and methods: Eleven patients with T1D and eleven nondiabetic controls were recruited as part of the FinnDiane study and given two fatty meals during 1 day. Cytokine responses in monocytes and myeloid dendritic cells (mDCs) as well as serum lipopolysaccharide activity levels, triglyceride concentrations and cytokine concentrations were measured from fasting and postprandial blood samples. Results: Postprandially, patients with T1D and controls showed significant increases in eight inflammatory cytokines (IL-6, TNF-α, IL-1β, IFN-α, IL-10, IFN-γ, IL-12 and MIP-1β) without concomitant increase in serum LPS activity. Serum cytokine production was similar in both groups. No postprandial change was seen in the IL-6, TNF-α or IL-1β production of mDCs or monocytes. At fasting, diabetic mDCs exhibited higher LPS-induced IL-6 and IL-1β production than controls. Conclusions: Acute high-fat meals increase circulating cytokines but have no effect on serum lipopolysaccharide activity levels or cytokine production in circulating mDCs or monocytes. Our results suggest that postprandial increase in serum cytokine levels is neither mediated by circulating endotoxins nor the activation of circulating innate cells. The production of high-fat meal-induced inflammatory markers is most likely regulated at the tissue level.

AB - Aims: Dietary fats have been shown to promote the translocation of bacterial endotoxins from the gut into circulation, which may induce systemic inflammation and modulate the inflammatory response of circulating immune cells. The aim of this study was to determine the effect of the postprandial milieu on inflammation and the inflammatory response of antigen presenting cells in the context of type 1 diabetes (T1D). Materials and methods: Eleven patients with T1D and eleven nondiabetic controls were recruited as part of the FinnDiane study and given two fatty meals during 1 day. Cytokine responses in monocytes and myeloid dendritic cells (mDCs) as well as serum lipopolysaccharide activity levels, triglyceride concentrations and cytokine concentrations were measured from fasting and postprandial blood samples. Results: Postprandially, patients with T1D and controls showed significant increases in eight inflammatory cytokines (IL-6, TNF-α, IL-1β, IFN-α, IL-10, IFN-γ, IL-12 and MIP-1β) without concomitant increase in serum LPS activity. Serum cytokine production was similar in both groups. No postprandial change was seen in the IL-6, TNF-α or IL-1β production of mDCs or monocytes. At fasting, diabetic mDCs exhibited higher LPS-induced IL-6 and IL-1β production than controls. Conclusions: Acute high-fat meals increase circulating cytokines but have no effect on serum lipopolysaccharide activity levels or cytokine production in circulating mDCs or monocytes. Our results suggest that postprandial increase in serum cytokine levels is neither mediated by circulating endotoxins nor the activation of circulating innate cells. The production of high-fat meal-induced inflammatory markers is most likely regulated at the tissue level.

KW - Cytokines

KW - Endotoxin

KW - High-fat diet

KW - Inflammation

KW - Lipopolysaccharide

KW - Type 1 diabetes

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U2 - 10.1007/s00592-014-0641-8

DO - 10.1007/s00592-014-0641-8

M3 - Article

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SP - 315

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JO - Acta Diabetologica

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JF - Acta Diabetologica

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