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Genetic Contribution to Multiple Sclerosis Risk Among Ashkenazi Jews

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Genetic Contribution to Multiple Sclerosis Risk Among Ashkenazi Jews UCSF UC San Francisco Previously Published Works Title Genetic contribution to multiple sclerosis risk among Ashkenazi Jews. Permalink https://escholarship.org/uc/item/0zw597hz Journal BMC medical genetics, 16(1) ISSN 1471-2350 Authors Khankhanian, Pouya Matsushita, Takuya Madireddy, Lohith et al. Publication Date 2015-07-28 DOI 10.1186/s12881-015-0201-2 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Khankhanian et al. BMC Medical Genetics (2015) 16:55 DOI 10.1186/s12881-015-0201-2 RESEARCH ARTICLE Open Access Genetic contribution to multiple sclerosis risk among Ashkenazi Jews Pouya Khankhanian1†, Takuya Matsushita1,2†, Lohith Madireddy1, Antoine Lizée1, Lennox Din1, Jayaji M Moré1, Pierre-Antoine Gourraud1, Stephen L Hauser1, Sergio E Baranzini1 and Jorge R Oksenberg1* Abstract Background: Multiple sclerosis (MS) is an autoimmune disease of the central nervous system, with a strong genetic component. Over 100 genetic loci have been implicated in susceptibility to MS in European populations, the most prominent being the 15:01 allele of the HLA-DRB1 gene. The prevalence of MS is high in European populations including those of Ashkenazi origin, and low in African and Asian populations including those of Jewish origin. Methods: Here we identified and extracted a total of 213 Ashkenazi MS cases and 546 ethnically matched healthy control individuals from two previous genome-wide case-control association analyses, and 72 trios (affected proband and two unaffected parents) from a previous genome-wide transmission disequilibrium association study, using genetic data to define Ashkenazi. We compared the pattern of genetic risk between Ashkenazi and non-Ashkenazi Europeans. We also sought to identify novel Ashkenazi-specific risk loci by performing association tests on the subset of Ashkenazi cases, controls, probands, and parents from each study. Results: The HLA-DRB1*15:01 allele and the non-HLA risk alleles were present at relatively low frequencies among Ashkenazi and explained a smaller fraction of the population-level risk when compared to non-Ashkenazi Europeans. Alternative HLA susceptibility alleles were identified in an Ashkenazi-only association study, including HLA-A*68:02 and one or both genes in the HLA-B*38:01-HLA-C*12:03 haplotype. The genome-wide screen in Ashkenazi did not reveal any loci associated with MS risk. Conclusion: These results suggest that genetic susceptibility to MS in Ashkenazi Jews has not been as well established as that of non-Ashkenazi Europeans. This implies value in studying large well-characterized Ashkenazi populations to accelerate gene discovery in complex genetic diseases. Keywords: Multiple sclerosis, Ashkenazi jews, Genome-wide association study, Population genetics Background frequency rates are found in Scandinavia, Iceland, the Multiple sclerosis (MS) is an autoimmune disease with British Isles and North America (about 1–2 in 1,000), central nervous system pathology [1] and the most com- but lower frequencies are observed in the Mediterranean mon cause of non-traumatic neurological disability in Basin (0.5 in 1000). young adults, affecting approximately 2.5 million people There are notable exceptions to the European preva- worldwide. The global burden of MS has increased over lence gradient, such as in Sardinia where the prevalence the past century but retains the well-known influence of of MS is among the highest in the world (1.4/1,000) [4]. gender, latitude, and ancestry on risk. This is reflected in Similarly, Ashkenazi Jews in Israel (and the Diaspora) the relatively high incidence in some population groups are at high risk for developing MS [5]. The distinctive (particularly those of European origin) compared with population histories of Sardinians and Ashkenazi Jews others (African and Asian groups) [2, 3]. Likewise, high include founder effects, admixture, and bottlenecks, sug- gesting that unique genetic signatures underlie their dif- * Correspondence: [email protected] ferential susceptibility. Unraveling these profiles may †Equal contributors 1Department of Neurology, University of California, San Francisco, 675 Nelson provide important insights into the genetics of MS and Rising Lane, San Francisco, CA 94158, USA interactions with non-genetic factors. Full list of author information is available at the end of the article © 2015 Khankhanian et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Khankhanian et al. BMC Medical Genetics (2015) 16:55 Page 2 of 10 Extensive empirical evidence confirms that genetic vari- genetic risk burden in Ashkenazi using previously identified ation is an important determinant of MS risk. Multiple MS susceptibility variants. Due to the unique properties of genome-wide association studies (GWAS) have been com- the HLA risk compared to the genome-wide risk, we assess pleted and reported, including a multi-center effort with the HLA risk before evaluating the genome-wide genetic nearly ten thousand cases [6]. The classic HLA-DRB1 risk burden at 110 non-HLA MS susceptibility SNPs en masse locus within the MHC, specifically the HLA-DRB1*15:01 (using a 110-SNP MS genetic burden score, termed the allele stood out in all GWAS with remarkably strong stat- MSGB). We compare Ashkenazi cases to Ashkenazi con- istical significance. In addition, 110 non-MHC variants trols to determine whether previously identified risk alleles were found to be associated with disease susceptibility apply to the Ashkenazi population. We compare MS risk (Additional file 1: Table S1) [7]. As expected, each identi- attributable to the previously identified genetic susceptibil- fied variant conferred only modest odds ratios. These ity loci between Ashkenazi and non-Ashkenazi Europeans. studies have focused on datasets ascertained in Europe, Finally, we seek to identify Ashkenazi-specific risk loci. Australia and North America and included affected We perform case–control analyses in Ashkenazi subsets Ashkenazi individuals. Jewish populations in the Diaspora of the GENEMSA and WTCCC2 studies and perform a can be grouped into distinct genetic clades shaped by ad- TD test of the Ashkenazi trios of the IMSGC study. mixture with local populations and social and cultural forces. Nevertheless, they all maintain the ancestral Defining the Ashkenazi subsets of previous studies Eastern Mediterranean and Middle Eastern genomic To extract individuals from case–control studies (GEN- identity, which contrasts significantly with central and EMSA and WTCCC2) who had genetic similarity to a northern European populations [8–12]. Here we seek well-defined Ashkenazi genetic reference dataset, we to clarify the genetic characteristics of MS in Ashkenazi built a hierarchy of clusters based on genome-wide IBD Jews. distances. In the GENEMSA study, hierarchical clustering Previous studies reported the HLA-DRB1*15:01 associ- revealed a large cluster of northern and western European ation with MS in Ashkenazi Jews living in Israel, albeit individuals (EUNW), a small cluster of eastern European with reduced odds ratios compared to Europeans [13]. Ashkenazi Jews, and a small cluster of southern Europeans The HLA-DRB1*13:03 allele was the strongest genetic bio- (EUS). In the WTCCC2 study, there was a large cluster of marker of risk in a study of non-Ashkenazi Israelis [13] EUNW, a small cluster of European Ashkenazi Jews, and but was not confirmed in Ashkenazi Israelis [13]. In our a small cluster of Finnish samples. Based on the hierarch- study, we use genomic signatures to identify and extract ical clustering, 97 Ashkenazi Jews and 1,541 EUNW in Ashkenazi Jewish individuals from three SNP-chip-based GENEMSA and 662 Ashkenazi Jews and 26,487 EUNW genome wide studies: a transmission disequilibrium (TD) in WTCCC2 were identified (Fig. 1a). Multidimensional study and two case control studies. We next illustrate the scaling of genome-wide IBD distances (Fig. 1b) revealed a genetic relationship of the Ashkenazi subsets to the other large main cluster of EUNW and a smaller outlying clus- European sub-populations. We then compare allelic risk ter of the well-characterized Ashkenazi controls in both at HLA-DRB1 and polygenic risk across the genome be- datasets. Structure-like analysis using FRAPPE [14] (a tween Ashkenazi Jews and non-Jewish western Europeans, maximum likelihood method to infer the genetic ancestry based on previously suggested risk alleles. To identify MS of each individual, where the individuals are assumed to susceptibility alleles that may be specific to the Ashkenazi have originated from K ancestral clusters) with K = 3 also population, we perform case–control and TD tests for demarcated the cluster of Ashkenazi individuals (Fig. 1a). SNPs across the genome and at classical HLA alleles in To extract individuals of Ashkenazi origin from the the Ashkenazi subset. IMSGC trio study, multi-dimensional scaling was per- formed as above. In this case, the first principal compo- Results nent (PC1) was used to define Ashkenazi individuals Overview (Additional file 5). For each trio, the value of PC1 for the We started by defining Ashkenazi
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