Nitric oxide regulates BAFF expression and T cell-independent antibody responses

J Immunol. 2014 Aug 1;193(3):1110-20. doi: 10.4049/jimmunol.1303158. Epub 2014 Jun 20.

Abstract

Whereas NO is known to regulate T cell responses, its role in regulating B cell responses remains unclear. Previous studies suggested that inducible NO synthase 2 (NOS2/iNOS) is required for normal IgA Ab responses but inhibits antiviral IgG2a Ab responses. In this study we used NOS2(-/-) mice to determine the role of NO in T cell-dependent and T cell-independent (TI)-2 Ab responses. Whereas T cell-dependent Ab responses were only modestly increased in NOS2(-/-) mice, IgM and IgG3 Ab responses as well as marginal zone B cell plasma cell numbers and peritoneal B1b B cells were significantly elevated after immunization with the TI-2 Ag 4-hydroxy-3-nitrophenyl acetyl (NP)-Ficoll. The elevated TI-2 responses in NOS2(-/-) mice were accompanied by significant increases in serum levels of BAFF/BLyS and by increases in BAFF-producing Ly6C(hi) inflammatory monocytes and monocyte-derived dendritic cells (DCs), suggesting that NO normally inhibits BAFF expression. Indeed, we found that NOS2(-/-) DCs produced more BAFF than did wild-type DCs, and addition of a NO donor to NOS2(-/-) DCs reduced BAFF production. Bone marrow chimeric mice that lack NOS2 in either nonhematopoietic or hematopoietic cells had intermediate IgM and IgG3 Ab responses after NP-Ficoll immunization, suggesting that NOS2 from both hematopoietic and nonhematopoietic sources regulates TI-2 Ab responses. Similar to NOS2(-/-) mice, depletion of Ly6C(hi) inflammatory monocytes and monocyte-derived DCs enhanced NP-specific IgM and IgG3 responses to NP-Ficoll. Thus, NO produced by inflammatory monocytes and their derivative DC subsets plays an important role in regulating BAFF production and TI-2 Ab responses.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antibody Formation / genetics
  • Antibody Formation / immunology*
  • B-Cell Activating Factor / biosynthesis*
  • B-Cell Activating Factor / genetics*
  • B-Cell Activating Factor / immunology
  • B-Lymphocyte Subsets / chemistry
  • B-Lymphocyte Subsets / immunology
  • B-Lymphocyte Subsets / metabolism
  • Ficoll / chemistry
  • Ficoll / immunology
  • Haptens / immunology
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Nitric Oxide / chemistry*
  • Nitric Oxide / immunology
  • Nitric Oxide Synthase Type II / deficiency
  • Nitric Oxide Synthase Type II / genetics
  • Nitric Oxide Synthase Type II / physiology*
  • Nitrophenols / immunology
  • Phenylacetates / immunology
  • T-Lymphocyte Subsets / chemistry
  • T-Lymphocyte Subsets / immunology*

Substances

  • B-Cell Activating Factor
  • Haptens
  • Nitrophenols
  • Phenylacetates
  • Tnfsf13b protein, mouse
  • 4-hydroxy-5-nitrophenyl acetic acid
  • Ficoll
  • Nitric Oxide
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse