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PLoS genetics2016; 12(12); e1006467; doi: 10.1371/journal.pgen.1006467

Allelic Variation in CXCL16 Determines CD3+ T Lymphocyte Susceptibility to Equine Arteritis Virus Infection and Establishment of Long-Term Carrier State in the Stallion.

Abstract: Equine arteritis virus (EAV) is the causative agent of equine viral arteritis (EVA), a respiratory, systemic, and reproductive disease of horses and other equid species. Following natural infection, 10-70% of the infected stallions can become persistently infected and continue to shed EAV in their semen for periods ranging from several months to life. Recently, we reported that some stallions possess a subpopulation(s) of CD3+ T lymphocytes that are susceptible to in vitro EAV infection and that this phenotypic trait is associated with long-term carrier status following exposure to the virus. In contrast, stallions not possessing the CD3+ T lymphocyte susceptible phenotype are at less risk of becoming long-term virus carriers. A genome wide association study (GWAS) using the Illumina Equine SNP50 chip revealed that the ability of EAV to infect CD3+ T lymphocytes and establish long-term carrier status in stallions correlated with a region within equine chromosome 11. Here we identified the gene and mutations responsible for these phenotypes. Specifically, the work implicated three allelic variants of the equine orthologue of CXCL16 (EqCXCL16) that differ by four non-synonymous nucleotide substitutions (XM_00154756; c.715 A → T, c.801 G → C, c.804 T → A/G, c.810 G → A) within exon 1. This resulted in four amino acid changes with EqCXCL16S (XP_001504806.1) having Phe, His, Ile and Lys as compared to EqCXL16R having Tyr, Asp, Phe, and Glu at 40, 49, 50, and 52, respectively. Two alleles (EqCXCL16Sa, EqCXCL16Sb) encoded identical protein products that correlated strongly with long-term EAV persistence in stallions (P<0.000001) and are required for in vitro CD3+ T lymphocyte susceptibility to EAV infection. The third (EqCXCL16R) was associated with in vitro CD3+ T lymphocyte resistance to EAV infection and a significantly lower probability for establishment of the long-term carrier state (viral persistence) in the male reproductive tract. EqCXCL16Sa and EqCXCL16Sb exert a dominant mode of inheritance. Most importantly, the protein isoform EqCXCL16S but not EqCXCL16R can function as an EAV cellular receptor. Although both molecules have equal chemoattractant potential, EqCXCL16S has significantly higher scavenger receptor and adhesion properties compared to EqCXCL16R.
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Publication Date: 2016-12-08 PubMed ID: 27930647PubMed Central: PMC5145142DOI: 10.1371/journal.pgen.1006467Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research paper is about how difference in genetic makeup, specifically variations in the CXCL16 gene, affects the susceptibility of horse T-cells to equine arteritis virus (EAV) infection, influencing the long-term carrier status in stallions.

Objective of the Research

  • The primary goal of this study was to identify and understand the genetic factors that enable some stallions to become long-term carriers of equine arteritis virus (EAV) after exposure. Additionally, the researchers aimed to shed light on the mechanism behind the susceptibility of certain T-lymphocytes to EAV infection.

Methodology and Findings

  • The study used a genome-wide association study (GWAS) and found that the ability of EAV to infect CD3+ T-cells and establish long-term carriage in stallions was linked with a region in chromosome 11 of equines.
  • Researchers pinpointed the equine orthologue of the CXCL16 gene (EqCXCL16), identifying three allelic variants with four non-synonymous nucleotide substitutions within exon 1. These changes caused four amino acid differences.
  • The two alleles (EqCXCL16Sa, EqCXCL16Sb) produced identical proteins and were heavily associated with persistent EAV infection in stallions. These alleles also enabled CD3+ T-cell susceptibility to EAV infection in vitro.
  • The third allele variant (EqCXCL16R) was linked with resistance to EAV infection in CD3+ T-cells in vitro and a significantly lower chance of establishing a long-term carrier state in the male reproductive tract.

Implications and Significance

  • These results indicate that the allele variants of the EqCXCL16 gene function in a dominant manner and have a significant role in dictating the long-term carrier state of EAV in stallions.
  • The researchers established that the protein isoform EqCXCL16S can serve as a cellular receptor for EAV, unlike EqCXCL16R.
  • Between the two variants, EqCXCL16S exhibited a greater scavenger receptor and adhesive capacity compared to EqCXCL16R, despite having equivalent chemoattraction potential. This suggests that differences in the allelic variants of the EqCXCL16 gene can influence the physiological responses of CD3+ T-cells to EAV infection.

Cite This Article

APA
Sarkar S, Bailey E, Go YY, Cook RF, Kalbfleisch T, Eberth J, Chelvarajan RL, Shuck KM, Artiushin S, Timoney PJ, Balasuriya UB. (2016). Allelic Variation in CXCL16 Determines CD3+ T Lymphocyte Susceptibility to Equine Arteritis Virus Infection and Establishment of Long-Term Carrier State in the Stallion. PLoS Genet, 12(12), e1006467. https://doi.org/10.1371/journal.pgen.1006467

Publication

PLoS genetics
ISSN: 1553-7404
NlmUniqueID: 101239074
Country: United States
Language: English
Volume: 12
Issue: 12
Pages: e1006467

Researcher Affiliations

Sarkar, Sanjay
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America.
Bailey, Ernest
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America.
Go, Yun Young
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America.
Cook, R Frank
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America.
Kalbfleisch, Ted
  • Department of Biochemistry and Molecular Genetics, School of Medicine, University of Louisville, Louisville, Kentucky, United States of America.
Eberth, John
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America.
Chelvarajan, R Lakshman
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America.
Shuck, Kathleen M
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America.
Artiushin, Sergey
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America.
Timoney, Peter J
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America.
Balasuriya, Udeni B R
  • Maxwell H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America.

MeSH Terms

  • Alleles
  • Amino Acid Sequence / genetics
  • Animals
  • Arterivirus Infections / genetics
  • Arterivirus Infections / veterinary
  • Arterivirus Infections / virology
  • CD3 Complex / genetics
  • CD3 Complex / immunology
  • Chemokines, CXC / genetics
  • Equartevirus / genetics
  • Equartevirus / pathogenicity
  • Genetic Predisposition to Disease
  • Genome-Wide Association Study
  • Horse Diseases / genetics
  • Horse Diseases / virology
  • Horses / genetics
  • Horses / virology
  • Male
  • Phylogeny
  • Semen / metabolism
  • T-Lymphocytes / immunology
  • T-Lymphocytes / pathology

Conflict of Interest Statement

The authors have declared that no competing interests exist.

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Citations

This article has been cited 9 times.
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