Single-cell immunophenotyping of the skin lesion erythema migrans identifies IgM memory B cells

JCI Insight. 2021 Jun 22;6(12):e148035. doi: 10.1172/jci.insight.148035.

Abstract

The skin lesion erythema migrans (EM) is an initial sign of the Ixodes tick-transmitted Borreliella spirochetal infection known as Lyme disease. T cells and innate immune cells have previously been shown to predominate the EM lesion and promote the reaction. Despite the established importance of B cells and antibodies in preventing infection, the role of B cells in the skin immune response to Borreliella is unknown. Here, we used single-cell RNA-Seq in conjunction with B cell receptor (BCR) sequencing to immunophenotype EM lesions and their associated B cells and BCR repertoires. We found that B cells were more abundant in EM in comparison with autologous uninvolved skin; many were clonally expanded and had circulating relatives. EM-associated B cells upregulated the expression of MHC class II genes and exhibited preferential IgM isotype usage. A subset also exhibited low levels of somatic hypermutation despite a gene expression profile consistent with memory B cells. Our study demonstrates that single-cell gene expression with paired BCR sequencing can be used to interrogate the sparse B cell populations in human skin and reveals that B cells in the skin infection site in early Lyme disease expressed a phenotype consistent with local antigen presentation and antibody production.

Keywords: Adaptive immunity; Bacterial infections; Immunology; Infectious disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • B-Lymphocytes* / cytology
  • B-Lymphocytes* / immunology
  • B-Lymphocytes* / metabolism
  • Erythema Chronicum Migrans* / immunology
  • Erythema Chronicum Migrans* / pathology
  • Female
  • Histocompatibility Antigens Class II / genetics
  • Histocompatibility Antigens Class II / immunology
  • Histocompatibility Antigens Class II / metabolism
  • Humans
  • Immunoglobulin M / genetics
  • Immunoglobulin M / metabolism
  • Immunophenotyping / methods*
  • Lyme Disease
  • Male
  • Middle Aged
  • RNA-Seq
  • Single-Cell Analysis / methods*
  • Skin / cytology
  • Transcriptome / genetics
  • Transcriptome / immunology

Substances

  • Histocompatibility Antigens Class II
  • Immunoglobulin M