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Experimental Autoimmune Encephalomyelitis Phenotype HLA Class II Polymorphisms Modulate Gut Microbiota

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Experimental Autoimmune Encephalomyelitis Phenotype HLA Class II Polymorphisms Modulate Gut Microbiota HLA Class II Polymorphisms Modulate Gut Microbiota and Experimental Autoimmune Encephalomyelitis Phenotype Shailesh K. Shahi, Soham Ali, Camille M. Jaime, Natalya V. Guseva and Ashutosh K. Mangalam Downloaded from ImmunoHorizons 2021, 5 (8) 627-646 doi: https://doi.org/10.4049/immunohorizons.2100024 http://www.immunohorizons.org/content/5/8/627 http://www.immunohorizons.org/ This information is current as of September 26, 2021. http://www.immunohorizons.org/ Supplementary http://www.immunohorizons.org/content/suppl/2021/08/11/immunohorizon Material s.2100024.DCSupplemental References This article cites 98 articles, 14 of which you can access for free at: http://www.immunohorizons.org/content/5/8/627.full#ref-list-1 by guest on September 26, 2021 Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: by guest on September 26, 2021 http://www.immunohorizons.org/alerts ImmunoHorizons is an open access journal published by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 All rights reserved. ISSN 2573-7732. RESEARCH ARTICLE Adaptive Immunity HLA Class II Polymorphisms Modulate Gut Microbiota and Experimental Autoimmune Encephalomyelitis Phenotype Shailesh K. Shahi,*,1 Soham Ali,*,†,1 Camille M. Jaime,* Natalya V. Guseva,* and Ashutosh K. Mangalam*,‡,§ *Department of Pathology, University of Iowa, Iowa City, IA; †Roy J. and Lucille A. Carver College of Medicine, University of Iowa, Iowa City, IA; ‡Graduate § Program in Immunology, University of Iowa, Iowa City, IA; and Graduate Program in Molecular Medicine, University of Iowa, Iowa City, IA Downloaded from ABSTRACT Multiple sclerosis (MS) is an autoimmune disease of the CNS in which the interaction between genetic and environmental factors plays http://www.immunohorizons.org/ an important role in disease pathogenesis. Although environmental factors account for 70% of disease risk, the exact environmental factors associated with MS are unknown. Recently, gut microbiota has emerged as a potential missing environmental factor linked with the pathobiology of MS. Yet, how genetic factors, such as HLA class II gene(s), interact with gut microbiota and influence MS is unclear. In the current study, we investigated whether HLA class II genes that regulate experimental autoimmune encephalomyelitis (EAE) and MS susceptibility also influence gut microbiota. Previously, we have shown that HLA-DR3 transgenic mice lacking endogenous mouse class II genes (AE-KO) were susceptible to myelin proteolipid protein (91–110)–induced EAE, an animal model of MS, whereas AE-KO.HLA-DQ8 transgenic mice were resistant. Surprisingly, HLA-DR3.DQ8 double transgenic mice showed higher disease prevalence and severity compared with HLA-DR3 mice. Gut microbiota analysis showed that HLA-DR3, HLA-DQ8, and HLA- DR3.DQ8 double transgenic mice microbiota are compositionally different from AE-KO mice. Within HLA class II transgenic mice, the microbiota of HLA-DQ8 mice were more similar to HLA-DR3.DQ8 than HLA-DR3. As the presence of DQ8 on an HLA-DR3 background by guest on September 26, 2021 increases disease severity, our data suggests that HLA-DQ8–specific microbiota may contribute to disease severity in HLA-DR3.DQ8 mice. Altogether, our study provides evidence that the HLA-DR and -DQ genes linked to specific gut microbiota contribute to EAE susceptibility or resistance in a transgenic animal model of MS. ImmunoHorizons, 2021, 5: 627–646. INTRODUCTION T cell immune response to a number of myelin Ags, including proteolipid protein (PLP), and myelin oligodendrocyte glyco- Multiple sclerosis (MS) is a chronic, autoimmune inflammatory protein (1, 2). The cause of MS is poorly understood, but collec- demyelinating disease of the CNS resulting from aberrant CD4 tive evidence suggests that the interaction of both genetic and Received for publication March 16, 2021. Accepted for publication July 20, 2021. Address correspondence and reprint requests to: Dr. Ashutosh K. Mangalam, Department of Pathology, University of Iowa, 25 S. Grand Avenue, 1080A Medical Laboratory, Iowa City, IA 52246. E-mail address: [email protected] ORCIDs: 0000-0002-8506-7655 (S.K.S.); 0000-0002-6797-8842 (C.M.J.); 0000-0002-9926-2531 (A.K.M.). 1S.K.S. and S.A. contributed equally. The sequences presented in this article have been submitted to the Sequence Read Archives (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA738522/) under accession number PRJNA738522. This work was supported by a National Multiple Sclerosis Society grant (RG 5138A1/1T), a National Institutes of Health, National Institute of Allergy and Infectious Diseases grant (1R01AI137075-01), a National Institute of Environmental Health Sciences career development award (P30 ES005605), a Carver Trust Medical Research Initiative Grant, and a University of Iowa Environmental Health Sciences Research Center pilot grant. S.A. was supported by the Roy J. and Lucille A. Carver College of Medicine Emory Warner Fellowship, which provides medical students the opportunity to take a full year out of their medical school curriculum to work in a laboratory in the University of Iowa Department of Pathology. C.M.J. was supported by a scholarship from the Iowa Biosciences Academy and a National Institutes of Health Initiative for Maximizing Student Development R25 training grant (5R25GM058939). Abbreviations used in this article: AE-KO, MHC class II gene knockout; DSS, dextran sulfate sodium; EAE, experimental autoimmune encephalomyelitis; FDR, false discovery rate; GxE, gene–environment interaction; IBD, inflammatory bowel disease; LDA, linear discriminant analysis; LEfSe, LDA effect size; MS, multiple sclerosis; padj, adjusted p value; PCA, principal component for analysis; PLP, proteolipid protein; SCFA, short-chain fatty acid. The online version of this article contains supplemental material. This article is distributed under the terms of the CC BY 4.0 Unported license. Copyright © 2021 The Authors https://doi.org/10.4049/immunohorizons.2100024 627 ImmunoHorizons is published by The American Association of Immunologists, Inc. 628 HLA CLASS II POLYMORPHISM AND GUT MICROBIOTA ImmunoHorizons environmental factors plays an important role (3). Furthermore, Although prior studies have reported a role of MHC genes recent studies showed a greater consensus on the contribution of in gut microbiota dysbiosis (3032), the importance of HLA- geneenvironment interactions (GxE) in the pathogenesis of MS DQ8 gene in modulating HLA-DR3 microbiome has not been (46). Genetic factors account for 30% of disease risk as deter- studied previously. In the current study, we investigated mined from studies of identical twins (7). In addition, environ- whether changes in HLA class II molecules from HLA-DQ8 to mental factors account for 70% of disease risk (8). However, how HLA-DR3 influences gut microbiota. Additionally, we ask genetic and environmental factors are linked with a predisposi- whether the HLA-DQ8 gene can modulate gut microbiota of tion to induce MS or protect from it is unknown. HLA-DR3 transgenic mice and modulate disease severity. We Among all the genetic factors associated with MS suscepti- found that the gut microbiota of MHC class II genes knockout bility, the strongest association has been found with MHC (AE-KO) mice differ from HLA-DR3, HLA-DQ8, and HLA- genes. MHC genes are among the most polymorphic genes in DR3.DQ8 double transgenic mice. We also further observed vertebrates (9), also known in humans as the HLA genes. Previ- that the gut microbiota of HLA-DR3 mice are different from ous studies have reported that individuals with HLA-DR2/ that of HLA-DQ8. Furthermore, our results showed that HLA-DQ6, HLA-DR3/HLA-DQ2, and HLA-DR4/HLA-DQ8 although HLA-DQ8 confers resistance to EAE, its shared Downloaded from class II haplotypes have an increased frequency of MS (10, 11). microbiota with HLA-DR3/HLA-DQ8 double transgenic mice Although a direct role of HLA-DR alleles in MS has been eluci- increase disease severity. Therefore, our study demonstrates an dated, the contribution of HLA-DQ alleles in disease pathogen- important role of the HLA-DQ8 and HLA-DR3 genes in shap- esis is not known. Human studies have shown that HLA-DQ ing gut microbiota and the HLA-DQ8 genes influence on the alleles may play a modulatory role in MS progression (12, 13). gut microbiota of HLA-DR3 transgenic mice. Using single transgenic mice expressing HLA class II genes, we http://www.immunohorizons.org/ showed that although both HLA-DR3 and HLA-DQ8 were able MATERIALS AND METHODS to recognize and mount a CD4 T cell response to PLP91110, only HLA-DR3 transgenic mice were susceptible to myelin Generation of single and double transgenic mice and PLP91110induced experimental autoimmune encephalomyelitis (EAE), whereas HLA-DQ8 (DQB1*0302) transgenic mice were breeding scheme resistant (14, 15). The CD4 T cells from HLA-DR3/HLA-DQ8 AE-KO mice. AE-KO mice were originally generated by Mathis double transgenic mice also recognized and proliferated to and Benoist (33). Briefly, AE-KO mice lack all four conventional PLP91110 peptide. However, the HLA-DR3/HLA-DQ8 double MHC class II genes (Aa,Ab,Ea,andEb) because of a large transgenic mice showed higher disease prevalence and severity (80 kb) deletion of the entire mouse class II region. Embryonic (14, 15), suggesting that the disease-resistant HLA-DQ8 allele stem cells with deleted MHC class II locus were injected into by guest on September 26, 2021 may synergize with HLA-DR3 to modulate the disease severity C57BL/6 blastocysts following standard procedures (34). Chi- and progression. We have also shown that HLA-DQ8induced meras were then crossed with C57BL/6 mice to generate AE- IL-17playsaroleinmodulatingdiseaseHLA-DR3.DQ8trans- KO mice, which were then interbred to generate homozygous genic mice. As gut microbiota has been shown to play a central AE-KO mice and maintained in homozygous conditions for a role in the development of IL-17producing CD4 T cells (16), it prolonged period by interbreeding. is possible that HLA-DQ8 modulate disease through its influ- ence on gut microbiota.
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