Beyond the MHC: A canine model of dermatomyositis shows a complex pattern of genetic risk involving novel loci
Juvenile dermatomyositis (JDM) is a chronic inflammatory myopathy and vasculopathy driven by genetic and environmental influences. Here, we investigated the genetic underpinnings of an analogous, spontaneous disease of dogs also termed dermatomyositis (DMS). As in JDM, we observed a significant asso...
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| Published in | PLoS genetics Vol. 13; no. 2; p. e1006604 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
03.02.2017
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7404 1553-7390 1553-7404 |
| DOI | 10.1371/journal.pgen.1006604 |
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| Abstract | Juvenile dermatomyositis (JDM) is a chronic inflammatory myopathy and vasculopathy driven by genetic and environmental influences. Here, we investigated the genetic underpinnings of an analogous, spontaneous disease of dogs also termed dermatomyositis (DMS). As in JDM, we observed a significant association with a haplotype of the major histocompatibility complex (MHC) (DLA-DRB1*002:01/-DQA1*009:01/-DQB1*001:01), particularly in homozygosity (P-val = 0.0001). However, the high incidence of the haplotype among healthy dogs indicated that additional genetic risk factors are likely involved in disease progression. We conducted genome-wide association studies in two modern breeds having common ancestry and detected strong associations with novel loci on canine chromosomes 10 (P-val = 2.3X10-12) and 31 (P-val = 3.95X10-8). Through whole genome resequencing, we identified primary candidate polymorphisms in conserved regions of PAN2 (encoding p.Arg492Cys) and MAP3K7CL (c.383_392ACTCCACAAA>GACT) on chromosomes 10 and 31, respectively. Analyses of these polymorphisms and the MHC haplotypes revealed that nine of 27 genotypic combinations confer high or moderate probability of disease and explain 93% of cases studied. The pattern of disease risk across PAN2 and MAP3K7CL genotypes provided clear evidence for a significant epistatic foundation for this disease, a risk further impacted by MHC haplotypes. We also observed a genotype-phenotype correlation wherein an earlier age of onset is correlated with an increased number of risk alleles at PAN2 and MAP3K7CL. High frequencies of multiple genetic risk factors are unique to affected breeds and likely arose coincident with artificial selection for desirable phenotypes. Described herein is the first three-locus association with a complex canine disease and two novel loci that provide targets for exploration in JDM and related immunological dysfunction. |
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| AbstractList | Juvenile dermatomyositis (JDM) is a chronic inflammatory myopathy and vasculopathy driven by genetic and environmental influences. Here, we investigated the genetic underpinnings of an analogous, spontaneous disease of dogs also termed dermatomyositis (DMS). As in JDM, we observed a significant association with a haplotype of the major histocompatibility complex (MHC) (DLA-DRB1*002:01/-DQA1*009:01/-DQB1*001:01), particularly in homozygosity (P-val = 0.0001). However, the high incidence of the haplotype among healthy dogs indicated that additional genetic risk factors are likely involved in disease progression. We conducted genome-wide association studies in two modern breeds having common ancestry and detected strong associations with novel loci on canine chromosomes 10 (P-val = 2.3X10.sup.-12) and 31 (P-val = 3.95X10.sup.-8). Through whole genome resequencing, we identified primary candidate polymorphisms in conserved regions of PAN2 (encoding p.Arg492Cys) and MAP3K7CL (c.383_392ACTCCACAAA>GACT) on chromosomes 10 and 31, respectively. Analyses of these polymorphisms and the MHC haplotypes revealed that nine of 27 genotypic combinations confer high or moderate probability of disease and explain 93% of cases studied. The pattern of disease risk across PAN2 and MAP3K7CL genotypes provided clear evidence for a significant epistatic foundation for this disease, a risk further impacted by MHC haplotypes. We also observed a genotype-phenotype correlation wherein an earlier age of onset is correlated with an increased number of risk alleles at PAN2 and MAP3K7CL. High frequencies of multiple genetic risk factors are unique to affected breeds and likely arose coincident with artificial selection for desirable phenotypes. Described herein is the first three-locus association with a complex canine disease and two novel loci that provide targets for exploration in JDM and related immunological dysfunction. Juvenile dermatomyositis (JDM) is a chronic inflammatory myopathy and vasculopathy driven by genetic and environmental influences. Here, we investigated the genetic underpinnings of an analogous, spontaneous disease of dogs also termed dermatomyositis (DMS). As in JDM, we observed a significant association with a haplotype of the major histocompatibility complex (MHC) (DLA-DRB1*002:01/-DQA1*009:01/-DQB1*001:01), particularly in homozygosity (P-val = 0.0001). However, the high incidence of the haplotype among healthy dogs indicated that additional genetic risk factors are likely involved in disease progression. We conducted genome-wide association studies in two modern breeds having common ancestry and detected strong associations with novel loci on canine chromosomes 10 (P-val = 2.3X10-12) and 31 (P-val = 3.95X10-8). Through whole genome resequencing, we identified primary candidate polymorphisms in conserved regions of PAN2 (encoding p.Arg492Cys) and MAP3K7CL (c.383_392ACTCCACAAA>GACT) on chromosomes 10 and 31, respectively. Analyses of these polymorphisms and the MHC haplotypes revealed that nine of 27 genotypic combinations confer high or moderate probability of disease and explain 93% of cases studied. The pattern of disease risk across PAN2 and MAP3K7CL genotypes provided clear evidence for a significant epistatic foundation for this disease, a risk further impacted by MHC haplotypes. We also observed a genotype-phenotype correlation wherein an earlier age of onset is correlated with an increased number of risk alleles at PAN2 and MAP3K7CL. High frequencies of multiple genetic risk factors are unique to affected breeds and likely arose coincident with artificial selection for desirable phenotypes. Described herein is the first three-locus association with a complex canine disease and two novel loci that provide targets for exploration in JDM and related immunological dysfunction. Juvenile dermatomyositis (JDM) is a chronic inflammatory myopathy and vasculopathy driven by genetic and environmental influences. Here, we investigated the genetic underpinnings of an analogous, spontaneous disease of dogs also termed dermatomyositis (DMS). As in JDM, we observed a significant association with a haplotype of the major histocompatibility complex (MHC) (DLA-DRB1*002:01/-DQA1*009:01/-DQB1*001:01), particularly in homozygosity (P-val = 0.0001). However, the high incidence of the haplotype among healthy dogs indicated that additional genetic risk factors are likely involved in disease progression. We conducted genome-wide association studies in two modern breeds having common ancestry and detected strong associations with novel loci on canine chromosomes 10 (P-val = 2.3X10-12) and 31 (P-val = 3.95X10-8). Through whole genome resequencing, we identified primary candidate polymorphisms in conserved regions of PAN2 (encoding p.Arg492Cys) and MAP3K7CL (c.383_392ACTCCACAAA>GACT) on chromosomes 10 and 31, respectively. Analyses of these polymorphisms and the MHC haplotypes revealed that nine of 27 genotypic combinations confer high or moderate probability of disease and explain 93% of cases studied. The pattern of disease risk across PAN2 and MAP3K7CL genotypes provided clear evidence for a significant epistatic foundation for this disease, a risk further impacted by MHC haplotypes. We also observed a genotype-phenotype correlation wherein an earlier age of onset is correlated with an increased number of risk alleles at PAN2 and MAP3K7CL. High frequencies of multiple genetic risk factors are unique to affected breeds and likely arose coincident with artificial selection for desirable phenotypes. Described herein is the first three-locus association with a complex canine disease and two novel loci that provide targets for exploration in JDM and related immunological dysfunction.Juvenile dermatomyositis (JDM) is a chronic inflammatory myopathy and vasculopathy driven by genetic and environmental influences. Here, we investigated the genetic underpinnings of an analogous, spontaneous disease of dogs also termed dermatomyositis (DMS). As in JDM, we observed a significant association with a haplotype of the major histocompatibility complex (MHC) (DLA-DRB1*002:01/-DQA1*009:01/-DQB1*001:01), particularly in homozygosity (P-val = 0.0001). However, the high incidence of the haplotype among healthy dogs indicated that additional genetic risk factors are likely involved in disease progression. We conducted genome-wide association studies in two modern breeds having common ancestry and detected strong associations with novel loci on canine chromosomes 10 (P-val = 2.3X10-12) and 31 (P-val = 3.95X10-8). Through whole genome resequencing, we identified primary candidate polymorphisms in conserved regions of PAN2 (encoding p.Arg492Cys) and MAP3K7CL (c.383_392ACTCCACAAA>GACT) on chromosomes 10 and 31, respectively. Analyses of these polymorphisms and the MHC haplotypes revealed that nine of 27 genotypic combinations confer high or moderate probability of disease and explain 93% of cases studied. The pattern of disease risk across PAN2 and MAP3K7CL genotypes provided clear evidence for a significant epistatic foundation for this disease, a risk further impacted by MHC haplotypes. We also observed a genotype-phenotype correlation wherein an earlier age of onset is correlated with an increased number of risk alleles at PAN2 and MAP3K7CL. High frequencies of multiple genetic risk factors are unique to affected breeds and likely arose coincident with artificial selection for desirable phenotypes. Described herein is the first three-locus association with a complex canine disease and two novel loci that provide targets for exploration in JDM and related immunological dysfunction. Juvenile dermatomyositis (JDM) is a chronic inflammatory myopathy and vasculopathy driven by genetic and environmental influences. Here, we investigated the genetic underpinnings of an analogous, spontaneous disease of dogs also termed dermatomyositis (DMS). As in JDM, we observed a significant association with a haplotype of the major histocompatibility complex (MHC) (DLA-DRB1*002:01/-DQA1*009:01/-DQB1*001:01), particularly in homozygosity (P-val = 0.0001). However, the high incidence of the haplotype among healthy dogs indicated that additional genetic risk factors are likely involved in disease progression. We conducted genome-wide association studies in two modern breeds having common ancestry and detected strong associations with novel loci on canine chromosomes 10 (P-val = 2.3X10-12) and 31 (P-val = 3.95X10-8). Through whole genome resequencing, we identified primary candidate polymorphisms in conserved regions of PAN2 (encoding p.Arg492Cys) and MAP3K7CL (c.383_392ACTCCACAAA>GACT) on chromosomes 10 and 31, respectively. Analyses of these polymorphisms and the MHC haplotypes revealed that nine of 27 genotypic combinations confer high or moderate probability of disease and explain 93% of cases studied. The pattern of disease risk across PAN2 and MAP3K7CL genotypes provided clear evidence for a significant epistatic foundation for this disease, a risk further impacted by MHC haplotypes. We also observed a genotype-phenotype correlation wherein an earlier age of onset is correlated with an increased number of risk alleles at PAN2 and MAP3K7CL. High frequencies of multiple genetic risk factors are unique to affected breeds and likely arose coincident with artificial selection for desirable phenotypes. Described herein is the first three-locus association with a complex canine disease and two novel loci that provide targets for exploration in JDM and related immunological dysfunction. Juvenile dermatomyositis (JDM) is an autoimmune disease of the skin and muscle influenced by both genetic and environmental components. Although genes independent of the MHC are thought to contribute to disease pathogenesis, their identification has been complicated by a paucity of biological samples, disease heterogeneity, and genetically diverse subjects. A naturally occurring inflammatory disease of domestic dogs, also termed dermatomyositis (DMS), is analogous to JDM and is the only animal model available for genetic study. We first determined that, as in JDM, a particular MHC haplotype confers susceptibility to DMS. Capitalizing on the genetic isolation of dog breeds and extremely low MHC diversity within affected breeds, we used multibreed genome-wide association studies to identify two novel loci. Through genome resequencing and additional genotyping, we uncovered highly associated polymorphisms in conserved positions of PAN2 and MAP3K7CL. Analysis of three-locus genotypes revealed uniquely high frequencies among affected breeds and nine allelic combinations that confer moderate or high risk for DMS. The pattern of disease probability illustrates the presence of gene-gene interaction, as well as an inverse correlation between age of onset and number of risk alleles. This study highlights the utility of canine models for mapping susceptibility loci in complex diseases and detecting patterns of genetic interactions obscured in diverse human populations. Juvenile dermatomyositis (JDM) is a chronic inflammatory myopathy and vasculopathy driven by genetic and environmental influences. Here, we investigated the genetic underpinnings of an analogous, spontaneous disease of dogs also termed dermatomyositis (DMS). As in JDM, we observed a significant association with a haplotype of the major histocompatibility complex (MHC) (DLA-DRB1*002:01/-DQA1*009:01/-DQB1*001:01), particularly in homozygosity (P-val = 0.0001). However, the high incidence of the haplotype among healthy dogs indicated that additional genetic risk factors are likely involved in disease progression. We conducted genome-wide association studies in two modern breeds having common ancestry and detected strong associations with novel loci on canine chromosomes 10 (P-val = 2.3X10-12) and 31 (P-val = 3.95X10-8). Through whole genome resequencing, we identified primary candidate polymorphisms in conserved regions of PAN2 (encoding p.Arg492Cys) and MAP3K7CL (c.383_392ACTCCACAAA>GACT) on chromosomes 10 and 31, respectively. Analyses of these polymorphisms and the MHC haplotypes revealed that nine of 27 genotypic combinations confer high or moderate probability of disease and explain 93% of cases studied. The pattern of disease risk across PAN2 and MAP3K7CL genotypes provided clear evidence for a significant epistatic foundation for this disease, a risk further impacted by MHC haplotypes. We also observed a genotype-phenotype correlation wherein an earlier age of onset is correlated with an increased number of risk alleles at PAN2 and MAP3K7CL. High frequencies of multiple genetic risk factors are unique to affected breeds and likely arose coincident with artificial selection for desirable phenotypes. Described herein is the first three-locus association with a complex canine disease and two novel loci that provide targets for exploration in JDM and related immunological dysfunction. |
| Audience | Academic |
| Author | Hill, Cody M. Anderson, Kendall J. Noorai, Rooksana E. Tsai, Kate L. Clark, Leigh Anne Evans, Jacquelyn M. Starr-Moss, Alison N. Famula, Thomas R. |
| AuthorAffiliation | 2 Genomics and Computational Laboratory, Clemson University, Clemson, South Carolina, United States of America Stanford University School of Medicine, UNITED STATES 3 Department of Animal Science, University of California, Davis, California, United States of America 1 Department of Genetics and Biochemistry, Clemson University, Clemson, South Carolina, United States of America |
| AuthorAffiliation_xml | – name: Stanford University School of Medicine, UNITED STATES – name: 1 Department of Genetics and Biochemistry, Clemson University, Clemson, South Carolina, United States of America – name: 2 Genomics and Computational Laboratory, Clemson University, Clemson, South Carolina, United States of America – name: 3 Department of Animal Science, University of California, Davis, California, United States of America |
| Author_xml | – sequence: 1 givenname: Jacquelyn M. surname: Evans fullname: Evans, Jacquelyn M. – sequence: 2 givenname: Rooksana E. orcidid: 0000-0002-9992-5198 surname: Noorai fullname: Noorai, Rooksana E. – sequence: 3 givenname: Kate L. orcidid: 0000-0002-7946-0522 surname: Tsai fullname: Tsai, Kate L. – sequence: 4 givenname: Alison N. orcidid: 0000-0001-9908-4491 surname: Starr-Moss fullname: Starr-Moss, Alison N. – sequence: 5 givenname: Cody M. surname: Hill fullname: Hill, Cody M. – sequence: 6 givenname: Kendall J. surname: Anderson fullname: Anderson, Kendall J. – sequence: 7 givenname: Thomas R. orcidid: 0000-0002-3139-9849 surname: Famula fullname: Famula, Thomas R. – sequence: 8 givenname: Leigh Anne orcidid: 0000-0001-6621-9660 surname: Clark fullname: Clark, Leigh Anne |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28158183$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1038_s41698_024_00591_0 crossref_primary_10_1292_jvms_22_0116 crossref_primary_10_1007_s00335_023_09991_2 crossref_primary_10_1186_s13100_018_0131_6 crossref_primary_10_1111_vde_12772 crossref_primary_10_1146_annurev_animal_030117_014523 crossref_primary_10_1016_j_jtauto_2019_100018 crossref_primary_10_1371_journal_pgen_1011538 crossref_primary_10_1111_vde_12743 crossref_primary_10_3233_JND_190394 crossref_primary_10_1016_j_cca_2018_03_042 crossref_primary_10_1007_s00251_019_01113_0 crossref_primary_10_1016_j_ygeno_2018_11_028 |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2017 Public Library of Science 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Evans JM, Noorai RE, Tsai KL, Starr-Moss AN, Hill CM, Anderson KJ, et al. (2017) Beyond the MHC: A canine model of dermatomyositis shows a complex pattern of genetic risk involving novel loci. PLoS Genet 13(2): e1006604. doi:10.1371/journal.pgen.1006604 2017 Evans et al 2017 Evans et al 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Evans JM, Noorai RE, Tsai KL, Starr-Moss AN, Hill CM, Anderson KJ, et al. (2017) Beyond the MHC: A canine model of dermatomyositis shows a complex pattern of genetic risk involving novel loci. PLoS Genet 13(2): e1006604. doi:10.1371/journal.pgen.1006604 |
| Copyright_xml | – notice: COPYRIGHT 2017 Public Library of Science – notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Evans JM, Noorai RE, Tsai KL, Starr-Moss AN, Hill CM, Anderson KJ, et al. (2017) Beyond the MHC: A canine model of dermatomyositis shows a complex pattern of genetic risk involving novel loci. PLoS Genet 13(2): e1006604. doi:10.1371/journal.pgen.1006604 – notice: 2017 Evans et al 2017 Evans et al – notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Evans JM, Noorai RE, Tsai KL, Starr-Moss AN, Hill CM, Anderson KJ, et al. (2017) Beyond the MHC: A canine model of dermatomyositis shows a complex pattern of genetic risk involving novel loci. PLoS Genet 13(2): e1006604. doi:10.1371/journal.pgen.1006604 |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceptualization: LAC KLT JME.Data curation: REN KLT JME.Formal analysis: JME TRF ANSM.Funding acquisition: LAC KLT.Investigation: JME REN CMH KJA.Project administration: LAC.Supervision: JME LAC.Validation: JME LAC REN TRF KLT ANSM.Visualization: LAC JME REN TRF.Writing – original draft: JME LAC TRF REN.Writing – review & editing: JME LAC ANSM KJA KLT. The authors have declared that no competing interests exist. |
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| Snippet | Juvenile dermatomyositis (JDM) is a chronic inflammatory myopathy and vasculopathy driven by genetic and environmental influences. Here, we investigated the... Juvenile dermatomyositis (JDM) is a chronic inflammatory myopathy and vasculopathy driven by genetic and environmental influences. Here, we investigated the... |
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| SubjectTerms | Adaptor Proteins, Signal Transducing - genetics Age Analysis Animals Biology and Life Sciences Breeding Chromosomes Dermatomyositis Dermatomyositis - epidemiology Dermatomyositis - genetics Dermatomyositis - veterinary Disease Disease Models, Animal Dog Diseases - epidemiology Dog Diseases - genetics Dogs Epidemiology Exoribonucleases - genetics Funding Genetic aspects Genetic Association Studies Genetic Predisposition to Disease Genetics Genome-Wide Association Study Genomes Genomics Haplotypes Health aspects Histocompatibility Antigens Class I - genetics Homozygote Major histocompatibility complex Medicine and Health Sciences Polymorphism, Genetic - genetics Polymorphism, Single Nucleotide Probability Risk Factors |
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| Title | Beyond the MHC: A canine model of dermatomyositis shows a complex pattern of genetic risk involving novel loci |
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