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Published on: June 23, 2013
The Structure, Evolution, and Gene Expression Within the Caprine Leukocyte Receptor Complex
John C Schwartz1, Nicholas D Sanderson1,2, Derek M Bickhart3
1The Pirbright Institute, Woking, United Kingdom.
Insights
Goats and sheep possess unique killer cell Ig-like receptor (KIR) gene structures, differing from other mammals and lacking a functional 3DL-lineage KIR gene. This study details their leukocyte receptor complex evolution and gene expression.
Area of Science:
- Immunology
- Genomics
- Evolutionary Biology
Background:
- The leukocyte receptor complex (LRC) is crucial for immune responses, particularly natural killer (NK) cell function.
- Killer cell Ig-like receptors (KIR) and leukocyte Ig-like receptors (LILR) exhibit high interspecies variability, suggesting rapid evolution under pathogen pressure.
- Simians and bovids, including goats and cattle, possess expanded KIR gene complements, making them valuable models for studying KIR evolution.
Purpose of the Study:
- To describe the LRC and KIR region structure in goats and compare it to sheep using advanced genomic assemblies.
- To investigate the evolutionary relationships and gene expansion within the KIR region of goats and sheep.
- To analyze the expression patterns of LRC genes, including KIR, LILR, and novel Ig-like receptors, in various caprine and ovine tissues.
Main Methods:
- Utilized improved genome assemblies and bacterial artificial chromosome data for structural analysis of the LRC and KIR regions in goats and sheep.
- Performed comparative genomic analysis to identify conserved and novel KIR genes and subgroups.
- Analyzed available transcriptomic data to investigate LRC gene expression across different tissues in sheep and goats.
Main Results:
- Identified conserved KIR genes shared between goats and sheep, and a partial sheep haplotype common to Rambouillet and Texel breeds.
- Discovered independent expansion of two novel KIR subgroups in goats and sheep.
- Confirmed the absence of a functional 3DL-lineage KIR gene in goats and sheep, a unique finding among mammals.
- LRC gene expression analysis largely supported gene annotations, with a conserved caprinae-specific KIR subgroup expressed in macrophages.
- Demonstrated high expression of LILR and novel Ig-like receptors across diverse tissues in both species.
Conclusions:
- Goats and sheep exhibit distinct evolutionary trajectories in their KIR gene repertoire, including independent expansions and the absence of a 3DL-lineage gene.
- The identified KIR gene structures and expression patterns provide insights into the immune system's adaptation in these species.
- This research enhances understanding of the caprine and ovine LRC repertoire, facilitating future studies on immune response variations.
Abstract:
The leukocyte receptor complex (LRC) encodes a large number of immunoglobulin (Ig)-like receptors involved in the immune response, particularly in modulating natural killer (NK) cell function. The killer cell Ig-like receptors (KIR), the leukocyte Ig-like receptors (LILR), and a recently described novel Ig-like receptor family are highly variable between species, which is consistent with rapid evolution driven by selection pressure from pathogens. Among the species studied to date, only simians (such as humans) and bovids (such as cattle and goats) have an expanded complement of KIR genes and represent an interesting model to study KIR evolution. Using recently improved genome assemblies and an assembly of bacterial artificial chromosomes, we describe the structure of the LRC, and the KIR region in particular, in goats and compare this to sheep as the assemblies allow. These species diverged from a common ancestor ~10 million years ago and from cattle ~25 million years ago. We identified conserved KIR genes common to both goats and sheep and confirm a partial sheep haplotype shared between the Rambouillet and Texel breeds. Goats and sheep have independently expanded two novel KIR subgroups, and unlike cattle or any other mammal, they do not appear to possess a functional 3DL-lineage KIR gene. Investigation of LRC gene expression using available transcriptomic data for various sheep and goat tissues largely confirmed putative gene annotation and revealed that a relatively conserved caprinae-specific KIR subgroup is expressed in macrophages. The LILR and novel Ig-like receptors were also highly expressed across a diverse range of tissues. This further step toward our understanding of the LRC receptor repertoire will help inform future studies investigating immune response variation in these species.
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