Human Ascaris infection is associated with higher frequencies of IL-10 producing B cells

PLoS Negl Trop Dis. 2024 Sep 23;18(9):e0012520. doi: 10.1371/journal.pntd.0012520. eCollection 2024 Sep.

Abstract

Introduction: Ascaris lumbricoides has dual effects on the immune system of infected hosts. The IgE response to this parasite has been thoroughly studied, but little is known about cellular responses induced by infection. This study aims to explore the interplay between A. lumbricoides infection and B cell responses, especially B regulatory cells.

Methods: Participants from Santa Catalina, Bolívar, Colombia, a helminth-endemic town, were screened for soil-transmitted helminthiasis (STH) using stool examinations. Eighteen A. lumbricoides-infected and 11 non-infected subjects were selected. Blood samples were analyzed for Breg cells and related cytokines, and immunoglobulins specific to the A. lumbricoides excretory/secretory product, ABA-1.

Results: Infected subjects exhibited higher frequencies of Breg cells, especially those with a higher A. lumbricoides egg burden. Higher frequencies of different Breg subsets were observed in infected individuals, with CD25+CD71+CD73- B cells being notably increased in strongly infected individuals. Additionally, A. lumbricoides infection was associated with reduced levels of circulating ABA-1-specific IgG1 and IgE. IL-10+ B cell frequencies correlated inversely with ABA-1-specific IgE.

Conclusions: A. lumbricoides infection has a significant impact on the immune response, particularly on Breg cell populations and antibody responses. Our findings suggest that A. lumbricoides infection mediates a dose-dependent immunosuppressive response characterized by an increase in Breg cells and concomitant suppression of ABA-1-specific humoral responses.

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Antibodies, Helminth* / blood
  • Antibodies, Helminth* / immunology
  • Ascariasis* / immunology
  • Ascariasis* / parasitology
  • Ascaris lumbricoides* / immunology
  • B-Lymphocytes / immunology
  • B-Lymphocytes, Regulatory / immunology
  • Colombia
  • Female
  • Humans
  • Immunoglobulin E* / blood
  • Immunoglobulin G / blood
  • Interleukin-10* / immunology
  • Male
  • Middle Aged
  • Young Adult

Substances

  • Interleukin-10
  • Antibodies, Helminth
  • Immunoglobulin E
  • IL10 protein, human
  • Immunoglobulin G

Grants and funding

This research was funded by MinCiencias and the University of Cartagena (Grant 699-2017 to JZ, https://minciencias.gov.co), Minciencias/SGR (Grant Number BPIN2020000100405 to LC, https://minciencias.gov.co), SIAF/University of Zürich, The Christine Kühne – Center for Allergy Research and Education (CK-CARE) Care (to MA, https://ck-care.ch/en/), and the Leading House for the Latin American Region, University of St. Gallen (Grant Agreement No. SMG1929 to MA, https://latinamerica.unisg.ch/en/leading-house). No salaries were paid by any of these funders. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.