JC Polyomavirus Infection Is Strongly Controlled by Human Leucocyte Antigen Class II Variants
JC polyomavirus (JCV) carriers with a compromised immune system, such as in HIV, or subjects on immune-modulating therapies, such as anti VLA-4 therapy may develop progressive multifocal leukoencephalopathy (PML) which is a lytic infection of oligodendrocytes in the brain. Serum antibodies to JCV ma...
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| Published in | PLoS pathogens Vol. 10; no. 4; p. e1004084 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.04.2014
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | JC polyomavirus (JCV) carriers with a compromised immune system, such as in HIV, or subjects on immune-modulating therapies, such as anti VLA-4 therapy may develop progressive multifocal leukoencephalopathy (PML) which is a lytic infection of oligodendrocytes in the brain. Serum antibodies to JCV mark infection occur only in 50-60% of infected individuals, and high JCV-antibody titers seem to increase the risk of developing PML. We here investigated the role of human leukocyte antigen (HLA), instrumental in immune defense in JCV antibody response. Anti-JCV antibody status, as a surrogate for JCV infection, were compared to HLA class I and II alleles in 1621 Scandinavian persons with MS and 1064 population-based Swedish controls and associations were replicated in 718 German persons with MS. HLA-alleles were determined by SNP imputation, sequence specific (SSP) kits and a reverse PCR sequence-specific oligonucleotide (PCR-SSO) method. An initial GWAS screen displayed a strong HLA class II region signal. The HLA-DRB1*15 haplotype was strongly negatively associated to JCV sero-status in Scandinavian MS cases (OR = 0.42, p = 7×10(-15)) and controls (OR = 0.53, p = 2×10(-5)). In contrast, the DQB1*06:03 haplotype was positively associated with JCV sero-status, in Scandinavian MS cases (OR = 1.63, p = 0.006), and controls (OR = 2.69, p = 1×10(-5)). The German dataset confirmed these findings (OR = 0.54, p = 1×10(-4) and OR = 1.58, p = 0.03 respectively for these haplotypes). HLA class II restricted immune responses, and hence CD4+ T cell immunity is pivotal for JCV infection control. Alleles within the HLA-DR1*15 haplotype are associated with a protective effect on JCV infection. Alleles within the DQB1*06:03 haplotype show an opposite association. These associations between JC virus antibody response and human leucocyte antigens supports the notion that CD4+ T cells are crucial in the immune defence to JCV and lays the ground for risk stratification for PML and development of therapy and prevention. |
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| AbstractList | JC polyomavirus (JCV) carriers with a compromised immune system, such as in HIV, or subjects on immune-modulating therapies, such as anti VLA-4 therapy may develop progressive multifocal leukoencephalopathy (PML) which is a lytic infection of oligodendrocytes in the brain. Serum antibodies to JCV mark infection occur only in 50-60% of infected individuals, and high JCV-antibody titers seem to increase the risk of developing PML. We here investigated the role of human leukocyte antigen (HLA), instrumental in immune defense in JCV antibody response. Anti-JCV antibody status, as a surrogate for JCV infection, were compared to HLA class I and II alleles in 1621 Scandinavian persons with MS and 1064 population-based Swedish controls and associations were replicated in 718 German persons with MS. HLA-alleles were determined by SNP imputation, sequence specific (SSP) kits and a reverse PCR sequence-specific oligonucleotide (PCR-SSO) method. An initial GWAS screen displayed a strong HLA class II region signal. The HLA-DRB1*15 haplotype was strongly negatively associated to JCV sero-status in Scandinavian MS cases (OR = 0.42, p = 7×10(-15)) and controls (OR = 0.53, p = 2×10(-5)). In contrast, the DQB1*06:03 haplotype was positively associated with JCV sero-status, in Scandinavian MS cases (OR = 1.63, p = 0.006), and controls (OR = 2.69, p = 1×10(-5)). The German dataset confirmed these findings (OR = 0.54, p = 1×10(-4) and OR = 1.58, p = 0.03 respectively for these haplotypes). HLA class II restricted immune responses, and hence CD4+ T cell immunity is pivotal for JCV infection control. Alleles within the HLA-DR1*15 haplotype are associated with a protective effect on JCV infection. Alleles within the DQB1*06:03 haplotype show an opposite association. These associations between JC virus antibody response and human leucocyte antigens supports the notion that CD4+ T cells are crucial in the immune defence to JCV and lays the ground for risk stratification for PML and development of therapy and prevention. JC polyomavirus (JCV) carriers with a compromised immune system, such as in HIV, or subjects on immune-modulating therapies, such as anti VLA-4 therapy may develop progressive multifocal leukoencephalopathy (PML) which is a lytic infection of oligodendrocytes in the brain. Serum antibodies to JCV mark infection occur only in 50–60% of infected individuals, and high JCV-antibody titers seem to increase the risk of developing PML. We here investigated the role of human leukocyte antigen (HLA), instrumental in immune defense in JCV antibody response. Anti-JCV antibody status, as a surrogate for JCV infection, were compared to HLA class I and II alleles in 1621 Scandinavian persons with MS and 1064 population-based Swedish controls and associations were replicated in 718 German persons with MS. HLA -alleles were determined by SNP imputation, sequence specific (SSP) kits and a reverse PCR sequence-specific oligonucleotide (PCR-SSO) method. An initial GWAS screen displayed a strong HLA class II region signal. The HLA-DRB1*15 haplotype was strongly negatively associated to JCV sero-status in Scandinavian MS cases (OR = 0.42, p = 7×10 −15 ) and controls (OR = 0.53, p = 2×10 −5 ). In contrast, the DQB1*06:03 haplotype was positively associated with JCV sero-status, in Scandinavian MS cases (OR = 1.63, p = 0.006), and controls (OR = 2.69, p = 1×10 −5 ). The German dataset confirmed these findings (OR = 0.54, p = 1×10 −4 and OR = 1.58, p = 0.03 respectively for these haplotypes). HLA class II restricted immune responses, and hence CD4+ T cell immunity is pivotal for JCV infection control. Alleles within the HLA-DR1*15 haplotype are associated with a protective effect on JCV infection. Alleles within the DQB1*06:03 haplotype show an opposite association. These associations between JC virus antibody response and human leucocyte antigens supports the notion that CD4+ T cells are crucial in the immune defence to JCV and lays the ground for risk stratification for PML and development of therapy and prevention. JC virus infection can lead to progressive multifocal leukoencephalopathy in individuals with a compromised immune system, such as during HIV infections or when treated with immunosuppressive or immunomodulating therapies. Progressive multifocal leukoencephalopathy is a rare but potentially fatal disease characterized by progressive damage of the brain white matter at multiple locations. It is therefore of importance to understand the host genetic control of response to JC virus in order to identify patients that can be treated with immunomodulating therapies, common treatments for autoimmune diseases, without increased risk for progressive multifocal leukoencephalopathy. This may also lead to development of preventative or curative anti-JC virus therapies. We here identify genetic variants being associated with JC virus antibody development; a negative association with the human leucocyte antigen DRB1*15-DQA1*01:02-DQB1*06:02 haplotype and a positive association with the DRB1*13-DQA1*01:03-DQB1*06:03 haplotype among controls and patients with multiple sclerosis from Scandinavia. We confirmed the associations in patients with multiple sclerosis from Germany. These associations between JC virus antibody response and human leucocyte antigens imply that CD4+ T cells are crucial in the immune defence and lay the ground for development of therapy and prevention. JC polyomavirus (JCV) carriers with a compromised immune system, such as in HIV, or subjects on immune-modulating therapies, such as anti VLA-4 therapy may develop progressive multifocal leukoencephalopathy (PML) which is a lytic infection of oligodendrocytes in the brain. Serum antibodies to JCV mark infection occur only in 50-60% of infected individuals, and high JCV-antibody titers seem to increase the risk of developing PML. We here investigated the role of human leukocyte antigen (HLA), instrumental in immune defense in JCV antibody response. Anti-JCV antibody status, as a surrogate for JCV infection, were compared to HLA class I and II alleles in 1621 Scandinavian persons with MS and 1064 population-based Swedish controls and associations were replicated in 718 German persons with MS. HLA-alleles were determined by SNP imputation, sequence specific (SSP) kits and a reverse PCR sequence-specific oligonucleotide (PCR-SSO) method. An initial GWAS screen displayed a strong HLA class II region signal. The HLA-DRB1*15 haplotype was strongly negatively associated to JCV sero-status in Scandinavian MS cases (OR = 0.42, p = 7×10-15) and controls (OR = 0.53, p = 2×10-5). In contrast, the DQB1*06:03 haplotype was positively associated with JCV sero-status, in Scandinavian MS cases (OR = 1.63, p = 0.006), and controls (OR = 2.69, p = 1×10-5). The German dataset confirmed these findings (OR = 0.54, p = 1×10-4 and OR = 1.58, p = 0.03 respectively for these haplotypes). HLA class II restricted immune responses, and hence CD4+ T cell immunity is pivotal for JCV infection control. Alleles within the HLA-DR1*15 haplotype are associated with a protective effect on JCV infection. Alleles within the DQB1*06:03 haplotype show an opposite association. These associations between JC virus antibody response and human leucocyte antigens supports the notion that CD4+ T cells are crucial in the immune defence to JCV and lays the ground for risk stratification for PML and development of therapy and prevention. JC polyomavirus (JCV) carriers with a compromised immune system, such as in HIV, or subjects on immune-modulating therapies, such as anti VLA-4 therapy may develop progressive multifocal leukoencephalopathy (PML) which is a lytic infection of oligodendrocytes in the brain. Serum antibodies to JCV mark infection occur only in 50-60% of infected individuals, and high JCV-antibody titers seem to increase the risk of developing PML. We here investigated the role of human leukocyte antigen (HLA), instrumental in immune defense in JCV antibody response. Anti-JCV antibody status, as a surrogate for JCV infection, were compared to HLA class I and II alleles in 1621 Scandinavian persons with MS and 1064 population-based Swedish controls and associations were replicated in 718 German persons with MS. HLA-alleles were determined by SNP imputation, sequence specific (SSP) kits and a reverse PCR sequence-specific oligonucleotide (PCR-SSO) method. An initial GWAS screen displayed a strong HLA class II region signal. The HLA-DRB1*15 haplotype was strongly negatively associated to JCV sero-status in Scandinavian MS cases (OR = 0.42, p = 7 x [10.sup.-15]) and controls (OR = 0.53, p = 2 x [10.sup.-5]). In contrast, the DQB1*06:03 haplotype was positively associated with JCV sero-status, in Scandinavian MS cases (OR = 1.63, p = 0.006), and controls (OR = 2.69, p = 1 x [10.sup.-5]). The German dataset confirmed these findings (OR = 0.54, p = 1 x [10.sup.-4] and OR = 1.58, p = 0.03 respectively for these haplotypes). HLA class II restricted immune responses, and hence CD4+ T cell immunity is pivotal for JCV infection control. Alleles within the HLA-DR1*15 haplotype are associated with a protective effect on JCV infection. Alleles within the DQB1*06:03 haplotype show an opposite association. These associations between JC virus antibody response and human leucocyte antigens supports the notion that CD4+ T cells are crucial in the immune defence to JCV and lays the ground for risk stratification for PML and development of therapy and prevention. JC polyomavirus (JCV) carriers with a compromised immune system, such as in HIV, or subjects on immune-modulating therapies, such as anti VLA-4 therapy may develop progressive multifocal leukoencephalopathy (PML) which is a lytic infection of oligodendrocytes in the brain. Serum antibodies to JCV mark infection occur only in 50-60% of infected individuals, and high JCV-antibody titers seem to increase the risk of developing PML. We here investigated the role of human leukocyte antigen (HLA), instrumental in immune defense in JCV antibody response. Anti-JCV antibody status, as a surrogate for JCV infection, were compared to HLA class I and II alleles in 1621 Scandinavian persons with MS and 1064 population-based Swedish controls and associations were replicated in 718 German persons with MS. HLA-alleles were determined by SNP imputation, sequence specific (SSP) kits and a reverse PCR sequence-specific oligonucleotide (PCR-SSO) method. An initial GWAS screen displayed a strong HLA class II region signal. The HLA-DRB1*15 haplotype was strongly negatively associated to JCV sero-status in Scandinavian MS cases (OR = 0.42, p = 7×10(-15)) and controls (OR = 0.53, p = 2×10(-5)). In contrast, the DQB1*06:03 haplotype was positively associated with JCV sero-status, in Scandinavian MS cases (OR = 1.63, p = 0.006), and controls (OR = 2.69, p = 1×10(-5)). The German dataset confirmed these findings (OR = 0.54, p = 1×10(-4) and OR = 1.58, p = 0.03 respectively for these haplotypes). HLA class II restricted immune responses, and hence CD4+ T cell immunity is pivotal for JCV infection control. Alleles within the HLA-DR1*15 haplotype are associated with a protective effect on JCV infection. Alleles within the DQB1*06:03 haplotype show an opposite association. These associations between JC virus antibody response and human leucocyte antigens supports the notion that CD4+ T cells are crucial in the immune defence to JCV and lays the ground for risk stratification for PML and development of therapy and prevention.JC polyomavirus (JCV) carriers with a compromised immune system, such as in HIV, or subjects on immune-modulating therapies, such as anti VLA-4 therapy may develop progressive multifocal leukoencephalopathy (PML) which is a lytic infection of oligodendrocytes in the brain. Serum antibodies to JCV mark infection occur only in 50-60% of infected individuals, and high JCV-antibody titers seem to increase the risk of developing PML. We here investigated the role of human leukocyte antigen (HLA), instrumental in immune defense in JCV antibody response. Anti-JCV antibody status, as a surrogate for JCV infection, were compared to HLA class I and II alleles in 1621 Scandinavian persons with MS and 1064 population-based Swedish controls and associations were replicated in 718 German persons with MS. HLA-alleles were determined by SNP imputation, sequence specific (SSP) kits and a reverse PCR sequence-specific oligonucleotide (PCR-SSO) method. An initial GWAS screen displayed a strong HLA class II region signal. The HLA-DRB1*15 haplotype was strongly negatively associated to JCV sero-status in Scandinavian MS cases (OR = 0.42, p = 7×10(-15)) and controls (OR = 0.53, p = 2×10(-5)). In contrast, the DQB1*06:03 haplotype was positively associated with JCV sero-status, in Scandinavian MS cases (OR = 1.63, p = 0.006), and controls (OR = 2.69, p = 1×10(-5)). The German dataset confirmed these findings (OR = 0.54, p = 1×10(-4) and OR = 1.58, p = 0.03 respectively for these haplotypes). HLA class II restricted immune responses, and hence CD4+ T cell immunity is pivotal for JCV infection control. Alleles within the HLA-DR1*15 haplotype are associated with a protective effect on JCV infection. Alleles within the DQB1*06:03 haplotype show an opposite association. These associations between JC virus antibody response and human leucocyte antigens supports the notion that CD4+ T cells are crucial in the immune defence to JCV and lays the ground for risk stratification for PML and development of therapy and prevention. |
| Audience | Academic |
| Author | Khademi, Mohsen Buck, Dorothea Oturai, Annette B. Lima Bomfim, Izaura Link, Jenny Sundqvist, Emilie Kockum, Ingrid Fogdell-Hahn, Anna Hemme, Bernhard Hillert, Jan Warnke, Clemens Albrecht, Eva Søndergaard, Helle Bach Alfredsson, Lars Gieger, Christian Olsson, Tomas |
| AuthorAffiliation | 7 Munich Cluster for Systems Neurology (SyNergy), Munich, Germany 4 Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health, Neuherberg, Germany 1 Neuroimmunology Unit, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden 2 Department of Neurology, Technische Universität München, Munich, Germany 5 Institute for Environmental Medicine, Karolinska Institutet, Stockholm, Sweden Brown University, United States of America 3 The Multiple Sclerosis Research Group, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden 6 Danish Multiple Sclerosis Center, Department of Neurology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark |
| AuthorAffiliation_xml | – name: 4 Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health, Neuherberg, Germany – name: 2 Department of Neurology, Technische Universität München, Munich, Germany – name: 6 Danish Multiple Sclerosis Center, Department of Neurology, Copenhagen University Hospital, Rigshospitalet, Copenhagen, Denmark – name: 1 Neuroimmunology Unit, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden – name: 3 The Multiple Sclerosis Research Group, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden – name: 5 Institute for Environmental Medicine, Karolinska Institutet, Stockholm, Sweden – name: 7 Munich Cluster for Systems Neurology (SyNergy), Munich, Germany – name: Brown University, United States of America |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24763718$$D View this record in MEDLINE/PubMed http://kipublications.ki.se/Default.aspx?queryparsed=id:129853059$$DView record from Swedish Publication Index |
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| ContentType | Journal Article |
| Contributor | Martin, Roland Haines, Jonathan McCauley, Jacob L Zipp, Frauke Comabella, Manuel Ivinson, Adrian Kockum, Ingrid Sawcer, Stephen Oksenberg, Jorge Hawkins, Clive Stewart, Graeme Pericak-Vance, Margaret Martinelli Boneschi, Filippo Barcellos, Lisa Patsopoulos, Nikolaos Spurkland, Anne Fontaine, Bertrand Oturai, Annette Goris, An De Jager, Philip Hauser, Stephen L Booth, David DAlfonso, Sandra Harbo, Hanne F Compston, Alastair Hillert, Jan Saarela, Janna Hafler, David Hemmer, Bernhard Olsson, Tomas |
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| Copyright | COPYRIGHT 2014 Public Library of Science 2014 Sundqvist et al 2014 Sundqvist et al 2014 Sundqvist et al. 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: Sundqvist E, Buck D, Warnke C, Albrecht E, Gieger C, et al. (2014) JC Polyomavirus Infection Is Strongly Controlled by Human Leucocyte Antigen Class II Variants. PLoS Pathog 10(4): e1004084. doi:10.1371/journal.ppat.1004084 |
| Copyright_xml | – notice: COPYRIGHT 2014 Public Library of Science – notice: 2014 Sundqvist et al 2014 Sundqvist et al – notice: 2014 Sundqvist et al. 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: Sundqvist E, Buck D, Warnke C, Albrecht E, Gieger C, et al. (2014) JC Polyomavirus Infection Is Strongly Controlled by Human Leucocyte Antigen Class II Variants. PLoS Pathog 10(4): e1004084. doi:10.1371/journal.ppat.1004084 |
| CorporateAuthor | International Multiple Sclerosis Genetics Consortium |
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| DOI | 10.1371/journal.ppat.1004084 |
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| Notes | ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 23 Membership of International Multiple Sclerosis Genetics Consortium is provided in the Acknowledgments. Tomas Olsson has received lecture and or advisory board honoraria from BiogenIdec, Novartis, Genzyme and Merck. The same companies have provided unrestricted MS research grants. Bernard Hemmer has received lecture and advisory board honoraria from Biogenidec, Novartism Bayer, Teva, Roche, Glaxo-Smith-Kline, Chugai and Merck-Serono. Biogenidec, Novartis, Metanomics, 5Prime, Roche, Bayer and Merck-Serono have supported the Department of Neurology of the Technische Universität München with research grants. This does not alter our adherence to all PLOS policies on sharing data and materials. Conceived and designed the experiments: JH ABO BH IK TO LA. Performed the experiments: ES DB CW HBS JL MK. Analyzed the data: ES EA IK ILB CW CG. Contributed reagents/materials/analysis tools: LA JH TO AFH ABO BH. Wrote the paper: ES CW TO IK. |
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| SubjectTerms | Alleles Antigens Biology and Life Sciences Brain research CD4-Positive T-Lymphocytes - immunology Colleges & universities Disease Epidemiology Female Genetic aspects Genetic research Genetic variation Genetics Haplotypes Health aspects HLA-DQ beta-Chains - genetics HLA-DQ beta-Chains - immunology HLA-DRB1 Chains - genetics HLA-DRB1 Chains - immunology Hospitals Host-parasite relationships Humans Immune system Infections JC Virus Leukocytes Male Medicine Medicine and Health Sciences Microbiological research Multiple sclerosis Neurology Neurosciences Polyoma virus Polyomavirus Infections - genetics Polyomavirus Infections - immunology Scandinavian and Nordic Countries |
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| Title | JC Polyomavirus Infection Is Strongly Controlled by Human Leucocyte Antigen Class II Variants |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/24763718 https://www.proquest.com/docview/1519263174 https://pubmed.ncbi.nlm.nih.gov/PMC3999271 http://kipublications.ki.se/Default.aspx?queryparsed=id:129853059 https://doaj.org/article/9429a524df6b489ea87114c311c3e7c9 http://dx.doi.org/10.1371/journal.ppat.1004084 |
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