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The origin and function of blood IgM + IgD + CD27 +  B cells is controversial, and they are considered a heterogeneous population. Previous staining of circulating B cells of healthy donors with rotavirus fluorescent virus-like particles allowed us to differentiate two subsets of IgM + IgD + CD27 + : IgM hi  and IgM lo  B cells. Here, we confirmed this finding and compared the phenotype, transcriptome,  in vitro  function, and Ig gene repertoire of these two subsets. Eleven markers phenotypically discriminated both subsets (CD1c, CD69, IL21R, CD27, MTG, CD45RB, CD5, CD184, CD23, BAFFR, and CD38) with the IgM hi  phenotypically resembling previously reported marginal zone B cells and the IgM lo  resembling both naïve and memory B cells. Transcriptomic analysis showed that both subpopulations clustered close to germinal center-experienced IgM only B cells with a Principal Component Analysis, but differed in expression of 78 genes. Moreover, IgM hi  B cells expressed genes characteristic of previously reported marginal zone B cells. After stimulation with CpG and cytokines, significantly ( p  < 0.05) higher frequencies (62.5%) of IgM hi  B cells proliferated, compared with IgM lo  B cells (35.37%), and differentiated to antibody secreting cells (14.22% for IgM hi  and 7.19% for IgM lo ). IgM hi  B cells had significantly ( p  < 0.0007) higher frequencies of mutations in IGHV and IGKV regions, IgM lo  B cells had higher usage of  IGHJ6  genes ( p  < 0.0001), and both subsets differed in their HCDR3 properties. IgM hi  B cells shared most of their shared IGH clonotypes with IgM only memory B cells, and IgM lo  B cells with IgM hi  B cells. These results support the notion that differential expression of IgM and IgD discriminates two subpopulations of human circulating IgM + IgD + CD27 +  B cells, with the IgM hi  B cells having similarities with previously described marginal zone B cells that passed through germinal centers, and the IgM lo  B cells being the least differentiated amongst the IgM + CD27 +  subsets.

frontiers in immunology

Differential Expression of IgM and IgD Discriminates Two Subpopulations of Human Circulating IgM+IgD+CD27+ B Cells That Differ Phenotypically, Functionally, and Genetically