Frontline Science: A reduction in DHA-derived mediators in male obesity contributes toward defects in select B cell subsets and circulating antibody

J Leukoc Biol. 2019 Aug;106(2):241-257. doi: 10.1002/JLB.3HI1017-405RR. Epub 2018 Dec 21.

Abstract

Obesity dysregulates B cell populations, which contributes toward poor immunological outcomes. We previously reported that differing B cell subsets are lowered in the bone marrow of obese male mice. Here, we focused on how lipid metabolites synthesized from docosahexaenoic acid (DHA) known as specialized pro-resolving lipid mediators (SPMs) influence specific B cell populations in obese male mice. Metabololipidomics revealed that splenic SPM precursors 14-hydroxydocosahexaenoic acid (14-HDHA), 17-hydroxydocosahexaenoic acid (17-HDHA), and downstream protectin DX (PDX) were decreased in obese male C57BL/6J mice. Simultaneous administration of these mediators to obese mice rescued major decrements in bone marrow B cells, modest impairments in the spleen, and circulating IgG2c, which is pro-inflammatory in obesity. In vitro studies with B cells, flow cytometry experiments with ALOX5-/- mice, and lipidomic analyses revealed the lowering of 14-HDHA/17-HDHA/PDX and dysregulation of B cell populations in obesity was driven indirectly via B cell extrinsic mechanisms. Notably, the lowering of lipid mediators was associated with an increase in the abundance of n-6 polyunsaturated fatty acids, which have a high affinity for SPM-generating enzymes. Subsequent experiments revealed female obese mice generally maintained the levels of SPM precursors, B cell subsets, and antibody levels. Finally, obese human females had increased circulating plasma cells accompanied by ex vivo B cell TNFα and IL-10 secretion. Collectively, the data demonstrate that DHA-derived mediators of the SPM pathway control the number of B cell subsets and pro-inflammatory antibody levels in obese male but not female mice through a defect that is extrinsic to B cells.

Keywords: 14-HDHA; 17-HDHA; PDX; n-3 polyunsaturated fatty acids.

Publication types

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

MeSH terms

  • Animals
  • Antibodies / blood
  • Antibodies / immunology*
  • B-Lymphocyte Subsets / drug effects
  • B-Lymphocyte Subsets / immunology*
  • B-Lymphocyte Subsets / metabolism*
  • Biomarkers
  • Bone Marrow Cells / drug effects
  • Diet, High-Fat / adverse effects
  • Disease Models, Animal
  • Disease Susceptibility
  • Docosahexaenoic Acids / analogs & derivatives
  • Docosahexaenoic Acids / metabolism*
  • Docosahexaenoic Acids / pharmacology
  • Female
  • Germinal Center / cytology
  • Germinal Center / immunology
  • Germinal Center / metabolism
  • Humans
  • Immunophenotyping
  • Inflammation Mediators / metabolism*
  • Lipid Metabolism
  • Lymphocyte Activation
  • Lymphocyte Count
  • Male
  • Metabolomics / methods
  • Mice
  • Mice, Knockout
  • Mice, Obese
  • Obesity / etiology*
  • Obesity / metabolism*
  • Obesity / pathology
  • Phenotype
  • Sex Factors

Substances

  • Antibodies
  • Biomarkers
  • Inflammation Mediators
  • Docosahexaenoic Acids
  • 14-hydroxydocosahexaenoic acid
  • 17-hydroxy-4,7,10,13,15,19-docosahexaenoic acid