Abstract
The adaptive immune response in jawed vertebrates is marked by the ability to diversify somatically specific immune receptor genes. Somatic recombination and hypermutation of gene segments are used to generate extensive repertoires of T and B cell receptors. In contrast, jawless vertebrates utilize a distinct diversification system based on copy choice to assemble their variable lymphocyte receptors. To date, very little evidence for somatic immune gene diversification has been reported in invertebrate species. Here we show that the SpTransformer (SpTrf ; formerly Sp185/333) immune effector gene family members from individual coelomocytes from purple sea urchins undergo somatic diversification by means of gene deletions, duplications, and acquisitions of single nucleotide polymorphisms. While sperm cells from an individual sea urchin have identical SpTrf gene repertoires, single cells from two distinct coelomocyte subpopulations from the same sea urchin exhibit significant variation in the SpTrf gene repertoires. Moreover, the highly diverse gene sequences derived from single coelomocytes are all in-frame, suggesting that an unknown mechanism(s) driving these somatic changes involve stringent selection or correction processes for expression of productive SpTrf transcripts. Together, our findings infer somatic immune gene diversification strategy in an invertebrate.
Highlights
The Transformer (Trf, formerly known as 185/333) genes encode a family of highly diverse immune effector proteins in sea urchins [1,2,3]
We focused on two immune-relevant populations of sea urchin coelomocytes, (i) cells that expressed SpTrf proteins on their surface that likely consisted of small phagocytes [18]
These cells could be isolated by fluorescence activated cell sorting (FACS) based on anti-SpTrf antibodies. (ii) SpTrf-negative red spherule cells were isolated by FACS based on their farred auto-fluorescence
Summary
The Transformer (Trf, formerly known as 185/333) genes encode a family of highly diverse immune effector proteins in sea urchins [1,2,3]. The second exon has a mosaic structure composed of blocks of conserved sequences termed elements, that are either present or absent in different members of the gene family, creating defined element patterns (Figure 1) that are the major source of diversity in gene sequence and size [4, 5]. Different sea urchin genotypes express different subsets of SpTrf transcripts [8, 10] and protein repertoires [11]. The SpTrf transcript repertoire shows a broad range of transcript sizes in coelomocytes prior to immune challenge, which changes toward a single size in response to immune challenge [10], suggesting functional specificity of individual SpTrf variants to particular targets
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