Dataset Information

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 ten 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.

SUBMITTER: Kortum AN

PROVIDER: S-EPMC3962068 | biostudies-literature | 2014 Apr

REPOSITORIES: biostudies-literature

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

Kortum Amanda N AN Rodriguez-Nunez Ivan I Yang Jibing J Shim Juyoung J Runft Donna D O'Driscoll Marci L ML Haire Robert N RN Cannon John P JP Turner Poem M PM Litman Ronda T RT Kim Carol H CH Neely Melody N MN Litman Gary W GW Yoder Jeffrey A JA

Immunogenetics 20140128 4

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 ...[more]

PMID: 24469064

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Project description:To date few studies have addressed the development and function of the porcine gastric mucosal immune system and this is a major limitation to understanding the immunopathogenesis of infections occurring in young pigs. The polymeric immunoglobulin receptor (pIgR) mediates the transport of secretory immunoglobulins until luminal surface of the gut mucosa and the aim of this study was to investigate the time course of pIgR expression and to determine its localization in three functionally different porcine gastric sites during the suckling period and after weaning. An additional goal was to investigate the time course expression of toll-like receptors (TLRs) in relation to pIgR expression. Gastric samples were collected from the cardiac-to-oxyntic transition (Cd), the oxyntic (Ox), and the pyloric (Py) regions in 84 pigs, slaughtered before weaning (14, 21 and 28 days of age; 23, 23 and 19 pigs, respectively) and 14 days post-weaning (42 days of age, 23 pigs). PIgR was expressed in the mucosa of all the three gastric sites, and its transcript levels were modulated during suckling and after weaning, with regional differences. PIgR expression increased linearly during suckling (P=0.019) and also increased post-weaning (P=0.001) in Cd, it increased post-weaning in Py (P=0.049) and increased linearly during suckling in Ox (P=0.036). TLRs expression was also modulated during development: in Cd, TLR2 increased linearly during suckling (P=0.003); in Ox, TLR2 decreased after weaning (P=0.038) while TLR4 increased linearly during suckling(P=0.008). The expression of TLR2, 3 and 4 in Ox was positively correlated with pIgR expression (P<0.001). Importantly, both pIgR protein and mRNA were localized, by immunohistochemistry and in situ hybridization, respectively, in the gastric glands of the lamina propria. These results indicate that pIgR is actively synthesized in the gastric mucosa and suggest that pIgR could play a crucial role in gastric mucosal immune defense of growing pigs.

Project description:The retention of particular genes after the whole genome duplication in zebrafish has given insights into how genes may evolve through partitioning of ancestral functions. We examine the partitioning of expression patterns and functions of two zebrafish kit ligands, kit ligand a (kitla) and kit ligand b (kitlb), and discuss their possible coevolution with the duplicated zebrafish kit receptors (kita and kitb). In situ hybridizations show that kitla mRNA is expressed in the trunk adjacent to the notochord in the middle of each somite during stages of melanocyte migration and later expressed in the skin, when the receptor is required for melanocyte survival. kitla is also expressed in other regions complementary to kita receptor expression, including the pineal gland, tail bud, and ear. In contrast, kitlb mRNA is expressed in brain ventricles, ear, and cardinal vein plexus, in regions generally not complementary to either zebrafish kit receptor ortholog. However, like kitla, kitlb is expressed in the skin during stages consistent with melanocyte survival. Thus, it appears that kita and kitla have maintained congruent expression patterns, while kitb and kitlb have evolved divergent expression patterns. We demonstrate the interaction of kita and kitla by morpholino knockdown analysis. kitla morphants, but not kitlb morphants, phenocopy the null allele of kita, with defects for both melanocyte migration and survival. Furthermore, kitla morpholino, but not kitlb morpholino, interacts genetically with a sensitized allele of kita, confirming that kitla is the functional ligand to kita. Last, we examine kitla overexpression in embryos, which results in hyperpigmentation caused by an increase in the number and size of melanocytes. This hyperpigmentation is dependent on kita function. We conclude that following genome duplication, kita and kitla have maintained their receptor-ligand relationship, coevolved complementary expression patterns, and that functional analysis reveals that most or all of the kita receptor's function in the embryo are promoted by its interaction with kitla.

Dataset Information

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

Publications

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

Similar Datasets

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