Abstract
The leukocyte receptor complex (LRC) encodes numerous immunoglobulin (Ig)-like receptors involved in innate immunity. These include the killer-cell Ig-like receptors (KIR) and the leukocyte Ig-like receptors (LILR) which can be polymorphic and vary greatly in number between species. Using the recent long-read genome assembly, Sscrofa11.1, we have characterized the porcine LRC on chromosome 6. We identified a ~ 197-kb region containing numerous LILR genes that were missing in previous assemblies. Out of 17 such LILR genes and fragments, six encode functional proteins, of which three are inhibitory and three are activating, while the majority of pseudogenes had the potential to encode activating receptors. Elsewhere in the LRC, between FCAR and GP6, we identified a novel gene that encodes two Ig-like domains and a long inhibitory intracellular tail. Comparison with two other porcine assemblies revealed a second, nearly identical, non-functional gene encoding a short intracellular tail with ambiguous function. These novel genes were found in a diverse range of mammalian species, including a pseudogene in humans, and typically consist of a single long-tailed receptor and a variable number of short-tailed receptors. Using porcine transcriptome data, both the novel inhibitory gene and the LILR were highly expressed in peripheral blood, while the single KIR gene, KIR2DL1, was either very poorly expressed or not at all. These observations are a prerequisite for improved understanding of immune cell functions in the pig and other species.
Highlights
The leukocyte receptor complex (LRC) encodes a diverse array of immunoglobulin (Ig)-like genes crucially involved in innate and cell-mediated immune responses against intracellular pathogens and neoplasms
As previous work identified a D1-like Ig domain fragment encoded within the KIR2DL1 gene (Hammond et al 2009), we investigated KIR2DL1 mRNA splicing using PCR and cDNA from six animals leveraged from a recent major histocompatibility complex (MHC) genotyping study (Schwartz et al 2018)
The porcine LRC is typically organized as in other species; compared to the human LRC, the centrally positioned LAIR1-TTYH1-LENG8-LENG9-CDC42EP5 gene cluster is inverted in the pig, with LAIR1 and the killer-cell Ig-like receptors (KIR)-proximal leukocyte Ig-like receptors (LILR) being juxtaposed (Fig. 1c)
Summary
The leukocyte receptor complex (LRC) encodes a diverse array of immunoglobulin (Ig)-like genes crucially involved in innate and cell-mediated immune responses against intracellular pathogens and neoplasms. Two known subgroups of LRC-encoded receptors are variably expanded in mammals: the killer-cell Ig-like receptors (KIR) and the leukocyte Ig-like receptors (LILR). Cell lectin-like receptors (KLR) mediate natural killer (NK) cell functions through their interactions with polymorphic major histocompatibility complex (MHC) class I or class I-like ligands. Mice (Mus musculus) have a highly expanded and polymorphic repertoire of KLRA genes, but possess only two KIR-like genes outside the LRC and which are thought to have alternative functions (Bryceson et al 2005; Hoelsbrekken et al 2003). The paired Ig-like receptors (PIR) are orthologous to human LILR, and some of these interact with MHC class I ligands (Kelley et al 2005; Liang et al 2002; Takai 2005)
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