B cell depletion increases sphingosine-1-phosphate-dependent airway inflammation in mice

Am J Respir Cell Mol Biol. 2015 May;52(5):571-83. doi: 10.1165/rcmb.2014-0207OC.

Abstract

Sphingosine-1-phosphate (S1P) has been widely associated with inflammation-based lung pathologies. Because B cells play a critical role as antigen-presenting and/or Ig-producing cells during asthmatic conditions, we wanted to dissect the role of these cells in S1P-dependent airway hyperreactivity and inflammation. Mice were sensitized to ovalbumin or exposed to S1P. Ovalbumin sensitization caused airway hyperreactivity coupled to an increased lung infiltration of B cells, which was significantly reduced after the inhibition of sphingosine kinases I/II. Similarly, the sole administration of S1P increased bronchial reactivity compared with vehicle and was accompanied by a higher influx of B cells in a time-dependent manner. This effect was associated with higher levels of IL-13, transforming growth factor-β, IL-10, and T regulatory cells. In addition, isolated S1P-derived lung B cells increased CD4(+) and CD8(+) T cell proliferation in vitro, and their suppressive nature at Day 14 was associated with the higher release of transforming growth factor-β and IL-10 when they were cocultured. Therefore, to prove the role of B cells in S1P-mediated airway inflammation, and because CD20 expression, contrary to major hystocompatibility complex I and major hystocompatibility complex II, was up-regulated at Day 14, CD20(+) B cells were depleted by means of a specific monoclonal antibody. The absence of CD20(+) B cells increased airway reactivity and inflammation in S1P-treated mice compared with control mice. These data imply that sphingosine kinase/S1P-mediated airway inflammation is countered by B cells via the induction of an immune-suppressive environment to reduce asthma-like outcomes in mice.

Keywords: B cells; asthma; immunosuppression; lung inflammation; sphingosine-1-phosphate.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Antigens, CD20 / immunology
  • Antigens, CD20 / metabolism
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism
  • Bronchial Hyperreactivity / chemically induced
  • Bronchial Hyperreactivity / immunology
  • Bronchial Hyperreactivity / physiopathology
  • Bronchoconstriction
  • Cell Proliferation
  • Chemotaxis, Leukocyte
  • Disease Models, Animal
  • Female
  • Inflammation Mediators / immunology
  • Inflammation Mediators / metabolism
  • Interleukin-10 / immunology
  • Interleukin-10 / metabolism
  • Interleukin-13 / immunology
  • Interleukin-13 / metabolism
  • Lung / drug effects
  • Lung / immunology*
  • Lung / metabolism
  • Lung / pathology
  • Lung / physiopathology
  • Lymphocyte Activation
  • Lysophospholipids*
  • Mice, Inbred BALB C
  • Ovalbumin
  • Phosphotransferases (Alcohol Group Acceptor) / antagonists & inhibitors
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Pneumonia / chemically induced*
  • Pneumonia / immunology*
  • Pneumonia / metabolism
  • Pneumonia / pathology
  • Pneumonia / physiopathology
  • Protein Kinase Inhibitors / pharmacology
  • Sphingosine / analogs & derivatives*
  • T-Lymphocytes, Regulatory / immunology
  • Time Factors
  • Transforming Growth Factor beta / immunology
  • Transforming Growth Factor beta / metabolism

Substances

  • Antibodies, Monoclonal
  • Antigens, CD20
  • IL10 protein, human
  • Inflammation Mediators
  • Interleukin-13
  • Lysophospholipids
  • Protein Kinase Inhibitors
  • Transforming Growth Factor beta
  • Interleukin-10
  • sphingosine 1-phosphate
  • Ovalbumin
  • Phosphotransferases (Alcohol Group Acceptor)
  • sphingosine kinase
  • Sphingosine