B-cell outgrowth and ligand-specific production of IL-10 correlate with Th2 dominance in certain parasitic diseases

Exp Parasitol. 1996 Nov;84(2):168-77. doi: 10.1006/expr.1996.0102.

Abstract

In many parasitic infections, dominant T helper cell (Th) type-2 CD4+ T cell responses exacerbate the disease. We have previously demonstrated that lacto-N-fucopentaose-III (LNFPIII), a sugar found on soluble egg antigens (SEA) of Schistosoma mansoni, stimulates splenic B cells from parasite-infected mice to proliferate and produce IL-10, a cytokine that promotes the generation of Th2 immune responses. In the present study, we extend our observations on ligand-specific activation of IL-10 producing B cells to leishmaniasis and lymphatic filariasis. We report here that infection with Leishmania major increases the splenic B220+ B cell subset in BALB/c mice, but not BALB/c. xid (lacking B-1 cells and carrying defective B-2 cells). In addition, these B cells secrete large amounts of IL-10 in vitro in response to stimulation with soluble leishmanial extract (LSE), LNFPIII, or SO4-Lewis(x). We also observed that injection of LSE increased the level of peritoneal exudate (PeC) B-1 cells (CD5+B220+) in BALB/c mice, but not C57BL/6, as compared to buffer-injected controls. Further, LSE elicited PeC B cells secreted IL-10 in response to LSE as well as to the sugars tested. A similar differential secretion of IL-10 by splenic B cells from BALB/c and BALB/c.xid was seen after S. mansoni infection. Likewise, injection of soluble microfilarial extract (MFX) resulted in an increase in percentage of PeC B-1 cells in BALB/c mice, but not C57BL/6, and these cells secreted IL-10 in response to stimulation with MFX or phosphorylcholine (PC). Collectively, these results suggest a correlation between expansion of ligand-specific IL-10 producing B and B-1 cells with dominance of Th2-type T cells in mice with the susceptible phenotype for these diseases.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Antigens, Helminth / immunology
  • Antigens, Protozoan / immunology
  • B-Lymphocytes / immunology*
  • Brugia malayi / immunology
  • Female
  • Interleukin-10 / biosynthesis*
  • Leishmania major / immunology*
  • Leishmaniasis, Cutaneous / immunology*
  • Ligands
  • Lymphocyte Activation
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Schistosomiasis mansoni / immunology*
  • Th2 Cells / immunology*

Substances

  • Antigens, Helminth
  • Antigens, Protozoan
  • Ligands
  • Interleukin-10