Defective B-cell proliferation and maintenance of long-term memory in patients with chronic granulomatous disease

J Allergy Clin Immunol. 2015 Mar;135(3):753-61.e2. doi: 10.1016/j.jaci.2014.07.012. Epub 2014 Aug 29.

Abstract

Background: Chronic granulomatous disease (CGD) is a primary immune deficiency characterized by a defect in reactive oxygen species production. Although the effect of CGD mainly reflects on the phagocytic compartment, B-cell responses are also impaired in patients with CGD.

Objective: We sought to investigate how defective gp91(phox) expression in patients with CGD and CGD carriers might affect the B-cell compartment and maintenance of long-term memory.

Methods: We studied the B-cell compartment of patients with CGD in terms of phenotype and ability to produce reactive oxygen species and proliferate on stimuli differently directed to the B-cell receptor and Toll-like receptor 9. We further studied their capacity to maintain long-term memory by measuring cellular and serologic responses to measles.

Results: We show that the memory B-cell compartment is impaired among patients with CGD, as indicated by reduced total (CD19(+)CD27(+)) and resting (CD19(+)CD27(+)CD21(+)) memory B cells in parallel to increased naive (CD19(+)CD27(-)IgD(+)) B-cell frequencies. Data on CGD carriers reveal that such alterations are related to gp91(phox) expression. Moreover, proliferative capabilities of B cells on selective in vitro stimulation of B-cell receptor or Toll-like receptor 9 pathways were reduced in patients with CGD compared with those seen in age-matched healthy control subjects. Significantly lower measles-specific antibody levels and antibody-secreting cell numbers were also observed, indicating a poor ability to maintain long-term memory in these patients.

Conclusion: Altogether, our data suggest that patients with CGD present a defective B-cell compartment in terms of frequencies of memory B cells, response to in vitro stimulation, and maintenance of long-term antigen-specific memory.

Keywords: B cell; Chronic granulomatous disease; long-term memory; measles; memory B-cell compartment; proliferation; reactive oxygen species deficiency.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Antigens, CD / genetics
  • Antigens, CD / immunology
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / pathology
  • Case-Control Studies
  • Cell Proliferation / drug effects
  • Child, Preschool
  • Female
  • Gene Expression
  • Granulomatous Disease, Chronic / genetics
  • Granulomatous Disease, Chronic / immunology*
  • Granulomatous Disease, Chronic / pathology
  • Humans
  • Immunologic Memory / drug effects*
  • Immunophenotyping
  • Infant
  • Male
  • Measles / immunology
  • Measles / prevention & control*
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / immunology*
  • NADPH Oxidase 2
  • NADPH Oxidases / genetics
  • NADPH Oxidases / immunology*
  • Phenotype
  • Pokeweed Mitogens / pharmacology
  • Primary Cell Culture
  • Reactive Oxygen Species / immunology
  • Reactive Oxygen Species / metabolism
  • Receptors, Antigen, B-Cell / genetics
  • Receptors, Antigen, B-Cell / immunology
  • Toll-Like Receptor 9 / genetics
  • Toll-Like Receptor 9 / immunology
  • Vaccination
  • Viral Vaccines / administration & dosage
  • Young Adult

Substances

  • Antigens, CD
  • Membrane Glycoproteins
  • Pokeweed Mitogens
  • Reactive Oxygen Species
  • Receptors, Antigen, B-Cell
  • TLR9 protein, human
  • Toll-Like Receptor 9
  • Viral Vaccines
  • CYBB protein, human
  • NADPH Oxidase 2
  • NADPH Oxidases