Differential expression and ligand binding indicate alternative functions for zebrafish polymeric immunoglobulin receptor (pIgR) and a family of pIgR-like (PIGRL) proteins

Abstract

The polymeric immunoglobulin (Ig) receptor (pIgR) is an integral transmembrane glycoprotein that plays an important role in the mammalian immune response by transporting soluble polymeric Igs across mucosal epithelial cells. Single pIgR genes, which are expressed in lymphoid organs including mucosal tissues, have been identified in several teleost species. A single pigr gene has been identified on zebrafish chromosome 2 along with a large multigene family consisting of 29 pigr-like (PIGRL) genes. Full length transcripts from 10 different PIGRL genes that encode secreted and putative inhibitory membrane bound receptors have been characterized. Although PIGRL and pigr transcripts are detected in immune tissues, only PIGRL transcripts can be detected in lymphoid and myeloid cells. In contrast to pIgR which binds Igs, certain PIGRL proteins bind phospholipids. PIGRL transcript levels are increased after infection with Streptococcus iniae, suggesting a role for PIGRL genes during bacterial challenge. Transcript levels of PIGRL genes are decreased after infection with Snakehead rhabdovirus, suggesting that viral infection may suppress PIGRL function.

Adaptive immune responses at mucosal surfaces of teleost fish

“…Ten pigr-like genes are present on chromosome 2 of zebrafish, and they encode secreted and putative inhibitory membrane-bound receptors. Immune tissues express pigr-like genes as well as pigr transcripts, while lymphoid and myeloid cells have only pigr-like gene transcripts [62]. The pigr gene expression was significantly upregulated in the mucosa of infected fish; after an ectoparasite (Lepeophtheirus salmonis) infection on the skin of Atlantic salmon [63] or a bacterial (Vibrio anguillarum) infection in the gut of carp (G. Yang, unpublished).…”

“…The pigr gene expression was significantly upregulated in the mucosa of infected fish; after an ectoparasite (Lepeophtheirus salmonis) infection on the skin of Atlantic salmon [63] or a bacterial (Vibrio anguillarum) infection in the gut of carp (G. Yang, unpublished). In zebrafish, pigr-like gene expression was elevated during a bacterial (Streptococcus iniae) infection while the transcripts were down-regulated after viral (Snakehead rhabdovirus) infection [62]. Up-regulation of pIgR expression is an accepted phenomenon in mammals and seems to be infection-, inflammation-or cytokine-driven [64,65], although it also can be down-regulated, for instance, in the case of inflammatory bowel disease [64].…”

“…Upon release to the apical plasma membrane domain, the extracellular part of the receptor is cleaved off by a proteinase and co-secreted with the IgA or IgM as a protective secretory component (SC) [20,21]. The pIgR amino acid sequences of seven teleosts were published in the past decade: fugu [59], carp [60], orange-spotted grouper Epinephelus coioides [61], rainbow trout [35], zebrafish [62], Atlantic salmon [63] and olive flounder Paralichthys olivaceus [55]. The seven pIgR sequences were aligned along with the sequence of the Atlantic cod Gadus morhua pIgR.…”

Putting J Chain Back on the Map: How Might Its Expression Define Plasma Cell Development?

“…placoderms and cartilaginous fish, see below; note, one study suggesting J chain’s presence in earthworms could not be verified in any other invertebrate or agnathan species (41)), but surprisingly was lost from teleosts, although it has been described in a lobed-fin fish, the lungfish (34). Secretory B cells and B cell-specific transcription factors have been well studied in teleosts, and despite their lack of J-chain, plasma cells nevertheless produce multimerized IgM and IgT that can be transported across epithelia via pIgR (39, 42–44) (Table I). Interestingly, Xenopus mucosal IgX also multimerizes in the absence of J-chain, although unlike teleosts, J-chain is present in frogs and associates with IgM heavy chains (37) (Table I).…”

Neutralization of Mitochondrial Superoxide by Superoxide Dismutase 2 Promotes Bacterial Clearance and Regulates Phagocyte Numbers in Zebrafish

“…Tissues were dissected from five zebrafish (EkkWill Waterlife Resources), and total RNA was purified with TRIzol reagent (Life Technologies). Lymphoid and myeloid cell populations were isolated from pooled kidneys of five zebrafish as described previously (35). In brief, kidneys from adult zebrafish were dissected and homogenized with a 40-m nylon mesh filter in ice-cold PBS plus 5% FBS.…”