Evolution of B Cell Immunity

Abstract

Two types of adaptive immune strategies are known to have evolved in vertebrates: the VLR-based system, which is present in jawless organisms and is mediated by VLRA and VLRB lymphocytes, and the BCR/TCR-based system, which is present in jawed species and is provided by B and T cell receptors expressed on B and T cells, respectively. Here we summarize features of B cells and their predecessors in the different animal phyla, focusing the review on B cells from jawed vertebrates. We point out the critical role of nonclassical species and comparative immunology studies in the understanding of B cell immunity. Because nonclassical models include species relevant to veterinary medicine, basic science research performed in these animals contributes to the knowledge required for the development of more efficacious vaccines against emerging pathogens.

B Cells in Teleost Fish Act as Pivotal Initiating APCs in Priming Adaptive Immunity: An Evolutionary Perspective on the Origin of the B-1 Cell Subset and B7 Molecules

“…In contrast, B-2 cells are a major B cell population circulating throughout the entire body and producing highaffinity Ag-specific Abs in a T cell-dependent manner (51,52). As one of the most important cellular components in the immune system, the origin and evolution of B cells have received considerable attention (53,54). However, this topic has long been challenged in immunology given the limited information about B cells in phylogenetically older species.…”

“…Importantly, this finding led to the recent identification of a similar feature shared by B-1 cells in mammals, which points to the innate-like nature of B-1 cells, as well as the existence of a close evolutionary relationship between the ancient B cell lineage and the B-1 subset (10,11). Given the central function of an innate-like cell in nonspecific Ag presentation, this innate feature has been examined in detail in B-1 cells (53). However, it remains undetermined whether fish B cells have such a function.…”

B cells and their role in the teleost gut

“…Teleost fish possess three major types of immunoglobulins: IgM and IgD, that have been identified in all teleost fish examined, as in almost all jawed vertebrates (Parra et al, 2013); and IgT (named as IgZ in cyprinids) which was identified in rainbow trout and zebrafish in 2005 (Danilova et al, 2005; Hansen et al, 2005), and has been found to be a specialized mucosal-dedicated immunoglobulin, akin to IgA and IgX in tetrapods and amphibians respectively (Zhang et al, 2010). The teleost igh locus encoding these three isotypes is arranged in a translocon organization (Flajnik and Kasahara, 2010).…”

“…However, minor modifications of this archetypal structure of the genomic igh locus occurred in various teleost species (Bengtén and Wilson, 2015; Fillatreau et al, 2013). Importantly, in sharp contrast to tetrapod igh locus that is regulated by an AID-mediated class switch recombination, the genomic structure of teleost igh locus rules out a possible class switch recombination between ighτ/ζ and ighμ , leading to the development of mutually exclusive B-cell lineages expressing IgT or IgM/D (Parra et al, 2013; Zhang et al, 2010). In support of this, B cells uniquely expressing surface IgT or IgM have been described in rainbow trout (Zhang et al, 2010).…”

“…Similar to IgM, IgD is an ancient immunoglobulin isotype that has been found in most jawed vertebrates, although birds and some mammals are devoid of the ighδ gene (Edholm et al, 2011; Parra et al, 2013; Sun et al, 2011) [i.e. examined birds (Huang et al, 2012; Magor et al, 2013), rabbit (Lanning et al, 2003), opossum (Wang et al, 2009), elephant (Guo et al, 2011)].…”