Evolutionary and Functional Relationships of B Cells from Fish and Mammals: Insights into their Novel Roles in Phagocytosis and Presentation of Particulate Antigen
J. Oriol Sunyer.
The evolutionary origins of Ig-producing B cells appear to be linked to the emergence of fish in this planet.
There are three major classes of living fish species, which from most primitive to modern they are referred to as agnathan
(e.g., lampreys), Chondrichthyes (e.g., sharks), and teleost fish (e.g., rainbow trout). Agnathans do not have immunoglobulin-
producing B cells, however these fish contain a subset of lymphocytes-like cells producing type B variable lymphocyte
receptors (VLRBs) that appear to act as functional analogs of immunoglobulins. Chondrichthyes fish represent
the most primitive living species containing bona-fide immunoglobulin-producing B cells. Their B cells are known to secrete
three types of antibodies, IgM, IgW and IgNAR. Teleost fish are also called bony fish since they represent the most
ancient living species containing true bones. Teleost B cells produce three different immunoglobulin isotypes, IgM, IgD
and the recently described IgT. While teleost IgM is the principal player in systemic immunity, IgT appears to be a teleost
immunoglobulin class specialized in mucosal immune responses. Thus far, three major B cell lineages have been described
in teleost, those expressing either IgT or IgD, and the most common lineage which co-expresses IgD and IgM. A
few years ago, the study of teleost fish B cells revealed for the first time in vertebrates the existence of B cell subsets with
phagocytic and intracellular bactericidal capacities. This finding represented a paradigm shift as professional phagocytosis
was believed to be exclusively performed by some cells of the myeloid lineage (i.e., macrophages, monocytes, neutrophils).
This phagocytic capacity was also found in amphibians and reptiles, suggesting that this innate capacity was evolutionarily
conserved in certain B cell subsets of vertebrates. Recently, the existence of subsets of B cells with phagocytic
and bactericidal abilities have also been confirmed in mammals. Moreover, it has been shown that phagocytic B-1 B cells
have a potent ability to present particulate antigen to CD4+ T cells. Thus, studies carried out originally on fish B cells have
lead to the discovery of new innate and adaptive roles of B cells in mammals. This review will concentrate on the evolutionary
and functional relationships of fish and mammalian B cells, focusing mainly on the newly discovered roles of
these cells in phagocytosis, intracellular killing and presentation of particulate antigen.
Keywords: Evolution, fish, mammals, phagocytosis, B cells, antigen presentation, intracellular killing, agnathan, Teleost fish, variable lymphocyte receptors (VLRBs), immunoglobulin-producing B cells, antibodies, immunoglobulin isotypes, mucosal immune responses, particulate antigen
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