Detection of IgE anti-parvovirus B19 and increased CD23+ B cells in parvovirus B19 infection: relation to Th2 cytokines

doi:10.1016/S1521-6616(03)00098-6

Clinical Immunology

Volume 108, Issue 2, August 2003, Pages 152-158

https://doi.org/10.1016/S1521-6616(03)00098-6 Get rights and content

Abstract

The immune profile of a parvovirus B19-infected patient (male, 8 years old) was studied on day 0 (initial presentation) and on days 14 and 210 post symptom presentation (psp). Before infection, the patient was skin test positive to various allergens, including ragweed and tree and grass pollens, and had a serum IgE level of 150 IU/mL. On day 0, the patient was diagnosed as parvovirus B19 infected, as judged by the presence of IgG anti-parvovirus Abs in serum (EIA) and presentation of “slap cheek” rash. The patient’s serum IgE level increased from 150 IU/mL before infection to 256 IU/mL on day 0, was 233 IU/mL on day 14, and returned to preinfection levels on day 210. In contrast, there was little change in the levels of serum IgM, IgG, or IgA (nephelometry). IgE anti-parvovirus B19 protein (VP-N) was detected in serum (Western blot) on days 0, 14, and 210, despite the decrease in total IgE on day 210. Although there was no increase in total numbers of blood CD23+ B cells on day 0, by day 14 the numbers of these cells increased dramatically (93%), remaining high on day 210. In contrast, there were virtually no changes in total numbers of CD4+ and CD8+ T cells or CD16/56+ NK precursor cells on days 0–210. On day 0, when IgG and IgE anti-parvovirus were detected in serum, patient’s peripheral blood mononuclear cells (PBMC) expressed mRNA for the Th2 cytokines IL-4 and IL-10, but not for the Th1 cytokines IFN-γ or IL-2. However, by day 14 psp, PBMC expressed mRNA for the Th1 cytokines IFN-γ and IL-2, as well as for IL-4 and IL-10. This is the first demonstration of the existence of IgE anti-parvovirus B19 Ab. The presence of IgE anti-parvovirus B19 Ab in serum on day 0 and its persistence in serum 7 months psp suggests that IgE anti-parvovirus may be useful in prognosis of parvovirus B19 infection. Our results reinforce the idea that IgE, in general, may play a major role in anti-viral immunity, perhaps in conjunction with CD23+ cells. The results further suggest that clearance of this infection is accompanied by a switch to Th1 cytokines.

Introduction

Previous studies in our laboratory were the first to identify the presence and function of IgE anti-HIV in serum of a subset of HIV-1 seropositive, nonprogressor pediatric patients who remained relatively healthy, despite decreased numbers of peripheral blood CD4+ T cells [1], [2]. Further, it has been demonstrated that specific IgE anti-HIV-1 antibodies may protect against HIV-1 disease progression by promoting cytotoxic responses or by suppressing virus production [1], [2], [3].

Studies by others [4], [5], [6] have identified immunoglobulin (Ig)E anti-parainfluenza virus [6] and IgE anti-respiratory syncytial virus (RSV) [4], [5] in sera from pediatric patients [6]. However, studies of De Alarcon et al. [7] were unable to detect IgE anti-RSV-F(a) and -G(a) antibodies in nasal washes and sera from infants [7].

In the present study, we determined the presence of IgE anti-parvovirus B19 Ab in serum obtained from a parvovirus B19-infected pediatric patient and its relationship to Th1 or Th2 cytokines. The exact role of IgE in parvovirus infection is not known; however, the presence of IgE anti-parvovirus B19 Ab in serum on day 0 and its persistence 7 months post symptom presentation (psp) suggest that IgE anti-parvovirus may be useful in prognosis of parvovirus B19 infection and that IgE may play a major role in anti-viral immunity.

Section snippets

Patient specimens

Peripheral blood (5 ml total) was obtained from a pediatric parvovirus (B19) patient (male, 8 years old, Caucasian), with an elevated serum IgE level (>100 IU/ml). The patient had positive skin prick to various allergens, including tree and grass pollens and ragweed. Parvovirus B19 infection was established by: (1) EIA and (2) positive pattern on Western blots. The patient presented with a “slap cheek” rash over his face and with a diffuse erythematous rash over his neck, ears, hands, elbows,

Symptoms

Clinical symptoms of parvovirus B19 patient included “slap cheek” rash over facial area, diffuse erythematous rash over body regions (neck, ears, hands, elbows, and knees), and arthralgias.

a. Total IgM, IgG, and IgA

Serum obtained from parvovirus B19-infected patient contained similar levels of total IgM (45 and 49 mg/dL, respectively). IgG₁ (621 and 507 mg/dL, respectively), IgG₂ (87 and 109 mg/dL, respectively), IgG₃ (52 and 54 mg/dL, respectively), IgG₄ (13 and 13 mg/dL, respectively), and IgA (37 and 58 mg/dL,

Discussion

Several findings stand out from the results reported here. The present study is the first to demonstrate that (1) IgE anti-parvovirus B19 is produced by a parvovirus B19-infected child. (2) Th2 cytokine responses predominate early in IgE anti-parvovirus B19 infection, whereas late in parvovirus B19 infection Th1 and Th2 cytokine responses both are prevalent. (3) CD23 surface expression on B cells is increased on peripheral blood lymphocytes from a parvovirus B19-infected child.

This is the first

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Parvovirus B19 in pregnancy
2006, Reproductive Toxicology
Parvovirus B19 is a widespread infection that may affects 1–5% of pregnant women, mainly with normal pregnancy outcome. The prevalence of infection is higher during epidemics – between 3 and 20% with sero-conversion rate of 3–34%. Infection during pregnancy can cause a variety of other signs of fetal damage. The risk of adverse fetal outcome is increased if maternal infection occurs during the first two trimesters of pregnancy but may also happen during the third trimester. It is a significant cause of fetal loss throughout pregnancy, but has a higher impact in the second half of pregnancy when spontaneous fetal loss from other causes is relatively rare. Parvovirus infection can cause severe fetal anemia as a result of fetal erythroid progenitor cells infection with shortened half life of erythrocytes, causing high output cardiac failure and therefore nonimmune hydrops fetalis (NIHF). The P antigen expressed on fetal cardiac myocytes enables the Parvovirus B19 to infect myocardial cells and produce myocarditis that aggravates the cardiac failure. Although there are several reports of major congenital anomalies among offspring of mothers infected by Parvovirus, the virus does not seem to be a significant teratogen. Since Parvovirus B19 infection can cause severe morbidity and mortality, it should be part of the routine work up of complicated pregnancies. Risk assessment for maternal infection during pregnancy is especially important during epidemics when sero-conversion rates are high.
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Although IgE is implicated in viral immunity, its role in parvovirus B19 immunity and its relationship to other immunological states has not been studied. Total serum immunoglobulin levels, IgG and IgE anti–parvovirus B19, blood lymphocyte numbers, and epsilon and cytokine specific mRNA were determined in pediatric patients with normal serum IgA levels (IgA+) and selective IgA deficiency (IgA−) on days 0 (initial diagnosis) and 14, and 3 years after recovery (nephelometry, Western blot test, flow cytometry, reverse transcriptase–polymerase chain reaction). We found that both patients had serum IgM, IgG, IgE, and IgA levels within normal ranges on day 0 to 3 years, excluding IgG₁ and IgA in the IgA− patient, which were elevated and negative, respectively, and IgE in the IgA+ patient, which was elevated (>100 IU/ml). The serum IgA+ and IgA− patients made IgE (and IgG) anti–parvovirus B19 at all time points. Excluding CD8⁺CD60⁺ T cells, determinations of T, B, and NK lymphocyte subsets always were within normal ranges. In both patients, CD8⁺CD60⁺ T-cell numbers were within normal ranges on day 0, but dramatically increased on day 14 (more than fivefold). At 3 years, they had returned to normal in the IgA+ patient, but remained high in the IgA− patient. On day 0 to 3 years, peripheral blood mononuclear cells of both patients expressed epsilon- and interferon (IFN)-α–specific mRNA. On day 0, the IgA+ patient expressed interleukin (IL)-4 and IL-10, but not IL-2, IFN-γ, or IL-6 mRNA; the IgA− patient expressed IL-6 and IL-10 mRNA, but not IL-4, IL-2, or IFN-γ mRNA. At 3 years, the IgA+ patient expressed mRNA for all cytokines, but the IgA− patient did not express mRNA for any of these cytokines. Our results suggest that IgE is important in parvovirus B19 immunity, and that IFN-α and CD8⁺CD60⁺ T cells may regulate IgE memory responses and isotype switching.
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Regular articleDetection of IgE anti-parvovirus B19 and increased CD23+ B cells in parvovirus B19 infection: relation to Th2 cytokines

Abstract

Introduction

Section snippets

Patient specimens

Symptoms

a. Total IgM, IgG, and IgA

Discussion

J. Allergy Clin. Immunol.

J Allergy Clin. Immunol.

J.Pediatr.

J Pediatr.

Clin. Immunol. Immunopathol.

Clin. Immunol. Immunopathol.

Immunol. Today.

Clin. Immunol.

Clin. Immunol. Immunopathol.

Clin. Diagn. Virol.

HIV-1 specific IgE in serum of long-term surviving children inhibits HIV-1 production in vitro

AIDS Res. Hum. Retroviruses

The development of respiratory syncytial virus-specific IgE and the release of histamine in nasopharyngeal secretions after infection

N.Engl. J.Med.

Evaluation of immunoglobulin E-specific antibodies and viral antigens in nasopharyngeal secretions of children with respiratory syncytial virus infection

J.Clin. Microbiol.

Single step method of RNA isolation by acid guanadium thiocyanate–phenol chloroform extraction

Anal. Biochem.

The absence of IgE antibody-mediated augmentation of immune responses in CD23-deficient mice

Proc. Natl. Acad. Sci. USA

Expression of the C3d/EBV receptor and other membrane surface markers is altered upon HIV-1 infection of myeloid, T, and B cells

J Acquired Immune Defic. Syndr.

Formation of IgE-binding factors by T cells of patients infected with human immunodeficiency virus type I

Proc. Natl. Acad. Sci. USA

Formation of IgE-binding factors by lymphocytes of HIV-infected patients

Int Arch. Allergy Appl. Immunol.

The low affinity receptor for IgE (CD23) in humana multifunctional receptor/cytokine?

Eur. Cytokine Network

Regulation of IgE synthesis by CD23/CD21 interaction

Int. Arch Allergy Immunol.

Regular article
Detection of IgE anti-parvovirus B19 and increased CD23+ B cells in parvovirus B19 infection: relation to Th₂ cytokines