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The human peripheral B-cell compartment displays a large population of immunoglobulin M–positive, immunoglobulin D–positive CD27⁺ (IgM⁺IgD⁺CD27⁺) “memory” B cells carrying a mutated immunoglobulin receptor. By means of phenotypic analysis, complementarity-determining region 3 (CDR3) spectratyping during a T-independent response, and gene-expression profiling of the different blood and splenic B-cell subsets, we show here that blood IgM⁺IgD⁺CD27⁺ cells correspond to circulating splenic marginal zone B cells. Furthermore, analysis of this peripheral subset in healthy children younger than 2 years shows that these B cells develop and mutate their immunoglobulin receptor during ontogeny, prior to their differentiation into T-independent antigen-responsive cells. It is therefore proposed that these IgM⁺IgD⁺CD27⁺ B cells provide the splenic marginal zone with a diversified and protective …