Maternal immunization with ovalbumin prevents neonatal allergy development and up-regulates inhibitory receptor Fc gamma RIIB expression on B cells

BMC Immunol. 2010 Mar 11:11:11. doi: 10.1186/1471-2172-11-11.

Abstract

Background: Preconception allergen immunization prevents neonatal allergen sensitization in mice by a complex interaction between regulatory cells/factors and antibodies. The present study assessed the influence of maternal immunization with ovalbumin (OVA) on the immune response of 3 day-old and 3 week-old offspring immunized or non-immunized with OVA and evaluated the effect of IgG treatment during fetal development or neonatal period.

Results: Maternal immunization with OVA showed increased levels of Fc gamma RIIb expression in splenic B cells of neonates, which were maintained for up to 3 weeks and not affected by additional postnatal OVA immunization. Maternal immunization also exerted a down-modulatory effect on both IL-4 and IFN-gamma-secreting T cells and IL-4 and IL-12- secreting B cells. Furthermore, immunized neonates from immunized mothers showed a marked inhibition of antigen-specific IgE Ab production and lowered Th2/Th1 cytokine levels, whereas displaying enhanced Fc gamma RIIb expression on B cells. These offspring also showed reduced antigen-specific proliferative response and lowered B cell responsiveness. Moreover, in vitro evaluation revealed an impairment of B cell activation upon engagement of B cell antigen receptor by IgG from OVA-immunized mice. Finally, in vivo IgG transference during pregnancy or breastfeeding revealed that maternal Ab transference was able to increase regulatory cytokines, such as IL-10, in the prenatal stage; yet only the postnatal treatment prevented neonatal sensitization. None of the IgG treatments induced immunological changes in the offspring, as it was observed for those from OVA-immunized mothers.

Conclusion: Maternal immunization upregulates the inhibitory Fc gamma RIIb expression on offspring B cells, avoiding skewed Th2 response and development of allergy. These findings contribute to the advancement of prophylactic strategies to prevent allergic diseases in early life.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Allergens / immunology
  • Animals
  • Animals, Newborn
  • B-Lymphocytes / drug effects*
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • B-Lymphocytes / pathology
  • CD40 Antigens / genetics
  • CD40 Antigens / metabolism
  • Cytokines / metabolism
  • Female
  • Fetal Development / drug effects
  • Fetal Development / immunology
  • Humans
  • Hypersensitivity / etiology*
  • Hypersensitivity / prevention & control
  • Immunity, Maternally-Acquired
  • Immunization
  • Immunoglobulin E / biosynthesis
  • Immunoglobulin E / genetics
  • Infant, Newborn
  • Infant, Newborn, Diseases / etiology*
  • Infant, Newborn, Diseases / prevention & control
  • Lymphocyte Activation / drug effects
  • Maternal Exposure / adverse effects*
  • Mice
  • Mice, Inbred BALB C
  • Ovalbumin / immunology
  • Pregnancy
  • Prenatal Exposure Delayed Effects / prevention & control
  • Receptors, IgE / genetics
  • Receptors, IgE / metabolism
  • Receptors, IgG / genetics
  • Receptors, IgG / immunology
  • Receptors, IgG / metabolism*
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / pathology
  • Up-Regulation

Substances

  • Allergens
  • CD40 Antigens
  • Cytokines
  • Fcgr2b protein, mouse
  • Receptors, IgE
  • Receptors, IgG
  • Immunoglobulin E
  • Ovalbumin