Genome-wide association study of resistance to Mycobacterium tuberculosis infection identifies a locus at 10q26.2 in three distinct populations
The natural history of tuberculosis (TB) is characterized by a large inter-individual outcome variability after exposure to Mycobacterium tuberculosis . Specifically, some highly exposed individuals remain resistant to M . tuberculosis infection, as inferred by tuberculin skin test (TST) or interfer...
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| Published in | PLoS genetics Vol. 17; no. 3; p. e1009392 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
04.03.2021
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7404 1553-7390 1553-7404 |
| DOI | 10.1371/journal.pgen.1009392 |
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| Abstract | The natural history of tuberculosis (TB) is characterized by a large inter-individual outcome variability after exposure to
Mycobacterium tuberculosis
. Specifically, some highly exposed individuals remain resistant to
M
.
tuberculosis
infection, as inferred by tuberculin skin test (TST) or interferon-gamma release assays (IGRAs). We performed a genome-wide association study of resistance to
M
.
tuberculosis
infection in an endemic region of Southern Vietnam. We enrolled household contacts (HHC) of pulmonary TB cases and compared subjects who were negative for both TST and IGRA (n = 185) with infected individuals (n = 353) who were either positive for both TST and IGRA or had a diagnosis of TB. We found a genome-wide significant locus on chromosome 10q26.2 with a cluster of variants associated with strong protection against
M
.
tuberculosis
infection (OR = 0.42, 95%CI 0.35–0.49,
P
= 3.71×10
−8
, for the genotyped variant rs17155120). The locus was replicated in a French multi-ethnic HHC cohort and a familial admixed cohort from a hyper-endemic area of South Africa, with an overall OR for rs17155120 estimated at 0.50 (95%CI 0.45–0.55,
P
= 1.26×10
−9
). The variants are located in intronic regions and upstream of
C10orf90
, a tumor suppressor gene which encodes an ubiquitin ligase activating the transcription factor p53.
In silico
analysis showed that the protective alleles were associated with a decreased expression in monocytes of the nearby gene
ADAM12
which could lead to an enhanced response of Th17 lymphocytes. Our results reveal a novel locus controlling resistance to
M
.
tuberculosis
infection across different populations. |
|---|---|
| AbstractList | Infection is inferred from the presence of anti-mycobacterial immunoreactivity, as shown by a positive result in tuberculin skin test (TST) and/or interferon-gamma (IFN-γ) release assay (IGRA).
The intensity cluster plot for rs17155120 showed that the genotype calling was of high quality and separated clearly into 3 genotype groups (S2 Fig).
Since all 18 variants in the locus were in high LD (S3 Fig), the imputed variants were likely to have a high imputation quality as suggested by their info score (S1 Table).
A) Manhattan plot showing results from a genome-wide association study between 185 uninfected subjects (negative for both tuberculin skin test and QuantiFERON-TB Gold In-Tube test) and 353 infected subjects (201 infected individuals positive for both tests and 152 patients with a history of pulmonary tuberculosis) for 5,591,951 variants (minor allele frequency > 5% and info > 0.8) with an unadjusted additive genetic model.
Odds ratios and 95% confidence intervals derived from a linear mixed model, P values, sample sizes and frequency of the effect allele (EAF) are reported by individual cohort and for the random effects meta-analysis. The natural history of tuberculosis (TB) is characterized by a large inter-individual outcome variability after exposure to Mycobacterium tuberculosis . Specifically, some highly exposed individuals remain resistant to M . tuberculosis infection, as inferred by tuberculin skin test (TST) or interferon-gamma release assays (IGRAs). We performed a genome-wide association study of resistance to M . tuberculosis infection in an endemic region of Southern Vietnam. We enrolled household contacts (HHC) of pulmonary TB cases and compared subjects who were negative for both TST and IGRA (n = 185) with infected individuals (n = 353) who were either positive for both TST and IGRA or had a diagnosis of TB. We found a genome-wide significant locus on chromosome 10q26.2 with a cluster of variants associated with strong protection against M . tuberculosis infection (OR = 0.42, 95%CI 0.35–0.49, P = 3.71×10 −8 , for the genotyped variant rs17155120). The locus was replicated in a French multi-ethnic HHC cohort and a familial admixed cohort from a hyper-endemic area of South Africa, with an overall OR for rs17155120 estimated at 0.50 (95%CI 0.45–0.55, P = 1.26×10 −9 ). The variants are located in intronic regions and upstream of C10orf90 , a tumor suppressor gene which encodes an ubiquitin ligase activating the transcription factor p53. In silico analysis showed that the protective alleles were associated with a decreased expression in monocytes of the nearby gene ADAM12 which could lead to an enhanced response of Th17 lymphocytes. Our results reveal a novel locus controlling resistance to M . tuberculosis infection across different populations. The natural history of tuberculosis (TB) is characterized by a large inter-individual outcome variability after exposure to Mycobacterium tuberculosis. Specifically, some highly exposed individuals remain resistant to M. tuberculosis infection, as inferred by tuberculin skin test (TST) or interferon-gamma release assays (IGRAs). We performed a genome-wide association study of resistance to M. tuberculosis infection in an endemic region of Southern Vietnam. We enrolled household contacts (HHC) of pulmonary TB cases and compared subjects who were negative for both TST and IGRA (n = 185) with infected individuals (n = 353) who were either positive for both TST and IGRA or had a diagnosis of TB. We found a genome-wide significant locus on chromosome 10q26.2 with a cluster of variants associated with strong protection against M. tuberculosis infection (OR = 0.42, 95%CI 0.35-0.49, P = 3.71×10-8, for the genotyped variant rs17155120). The locus was replicated in a French multi-ethnic HHC cohort and a familial admixed cohort from a hyper-endemic area of South Africa, with an overall OR for rs17155120 estimated at 0.50 (95%CI 0.45-0.55, P = 1.26×10-9). The variants are located in intronic regions and upstream of C10orf90, a tumor suppressor gene which encodes an ubiquitin ligase activating the transcription factor p53. In silico analysis showed that the protective alleles were associated with a decreased expression in monocytes of the nearby gene ADAM12 which could lead to an enhanced response of Th17 lymphocytes. Our results reveal a novel locus controlling resistance to M. tuberculosis infection across different populations.The natural history of tuberculosis (TB) is characterized by a large inter-individual outcome variability after exposure to Mycobacterium tuberculosis. Specifically, some highly exposed individuals remain resistant to M. tuberculosis infection, as inferred by tuberculin skin test (TST) or interferon-gamma release assays (IGRAs). We performed a genome-wide association study of resistance to M. tuberculosis infection in an endemic region of Southern Vietnam. We enrolled household contacts (HHC) of pulmonary TB cases and compared subjects who were negative for both TST and IGRA (n = 185) with infected individuals (n = 353) who were either positive for both TST and IGRA or had a diagnosis of TB. We found a genome-wide significant locus on chromosome 10q26.2 with a cluster of variants associated with strong protection against M. tuberculosis infection (OR = 0.42, 95%CI 0.35-0.49, P = 3.71×10-8, for the genotyped variant rs17155120). The locus was replicated in a French multi-ethnic HHC cohort and a familial admixed cohort from a hyper-endemic area of South Africa, with an overall OR for rs17155120 estimated at 0.50 (95%CI 0.45-0.55, P = 1.26×10-9). The variants are located in intronic regions and upstream of C10orf90, a tumor suppressor gene which encodes an ubiquitin ligase activating the transcription factor p53. In silico analysis showed that the protective alleles were associated with a decreased expression in monocytes of the nearby gene ADAM12 which could lead to an enhanced response of Th17 lymphocytes. Our results reveal a novel locus controlling resistance to M. tuberculosis infection across different populations. The natural history of tuberculosis (TB) is characterized by a large inter-individual outcome variability after exposure to Mycobacterium tuberculosis. Specifically, some highly exposed individuals remain resistant to M. tuberculosis infection, as inferred by tuberculin skin test (TST) or interferon-gamma release assays (IGRAs). We performed a genome-wide association study of resistance to M. tuberculosis infection in an endemic region of Southern Vietnam. We enrolled household contacts (HHC) of pulmonary TB cases and compared subjects who were negative for both TST and IGRA (n = 185) with infected individuals (n = 353) who were either positive for both TST and IGRA or had a diagnosis of TB. We found a genome-wide significant locus on chromosome 10q26.2 with a cluster of variants associated with strong protection against M. tuberculosis infection (OR = 0.42, 95%CI 0.35-0.49, P = 3.71x10.sup.-8, for the genotyped variant rs17155120). The locus was replicated in a French multi-ethnic HHC cohort and a familial admixed cohort from a hyper-endemic area of South Africa, with an overall OR for rs17155120 estimated at 0.50 (95%CI 0.45-0.55, P = 1.26x10.sup.-9). The variants are located in intronic regions and upstream of C10orf90, a tumor suppressor gene which encodes an ubiquitin ligase activating the transcription factor p53. In silico analysis showed that the protective alleles were associated with a decreased expression in monocytes of the nearby gene ADAM12 which could lead to an enhanced response of Th17 lymphocytes. Our results reveal a novel locus controlling resistance to M. tuberculosis infection across different populations. Infection is inferred from the presence of anti-mycobacterial immunoreactivity, as shown by a positive result in tuberculin skin test (TST) and/or interferon-gamma (IFN-γ) release assay (IGRA). The intensity cluster plot for rs17155120 showed that the genotype calling was of high quality and separated clearly into 3 genotype groups (S2 Fig). Since all 18 variants in the locus were in high LD (S3 Fig), the imputed variants were likely to have a high imputation quality as suggested by their info score (S1 Table). A) Manhattan plot showing results from a genome-wide association study between 185 uninfected subjects (negative for both tuberculin skin test and QuantiFERON-TB Gold In-Tube test) and 353 infected subjects (201 infected individuals positive for both tests and 152 patients with a history of pulmonary tuberculosis) for 5,591,951 variants (minor allele frequency > 5% and info > 0.8) with an unadjusted additive genetic model. Odds ratios and 95% confidence intervals derived from a linear mixed model, P values, sample sizes and frequency of the effect allele (EAF) are reported by individual cohort and for the random effects meta-analysis. The natural history of tuberculosis (TB) is characterized by a large inter-individual outcome variability after exposure to Mycobacterium tuberculosis. Specifically, some highly exposed individuals remain resistant to M. tuberculosis infection, as inferred by tuberculin skin test (TST) or interferon-gamma release assays (IGRAs). We performed a genome-wide association study of resistance to M. tuberculosis infection in an endemic region of Southern Vietnam. We enrolled household contacts (HHC) of pulmonary TB cases and compared subjects who were negative for both TST and IGRA (n = 185) with infected individuals (n = 353) who were either positive for both TST and IGRA or had a diagnosis of TB. We found a genome-wide significant locus on chromosome 10q26.2 with a cluster of variants associated with strong protection against M. tuberculosis infection (OR = 0.42, 95%CI 0.35-0.49, P = 3.71×10-8, for the genotyped variant rs17155120). The locus was replicated in a French multi-ethnic HHC cohort and a familial admixed cohort from a hyper-endemic area of South Africa, with an overall OR for rs17155120 estimated at 0.50 (95%CI 0.45-0.55, P = 1.26×10-9). The variants are located in intronic regions and upstream of C10orf90, a tumor suppressor gene which encodes an ubiquitin ligase activating the transcription factor p53. In silico analysis showed that the protective alleles were associated with a decreased expression in monocytes of the nearby gene ADAM12 which could lead to an enhanced response of Th17 lymphocytes. Our results reveal a novel locus controlling resistance to M. tuberculosis infection across different populations. The natural history of tuberculosis (TB) is characterized by a large inter-individual outcome variability after exposure to Mycobacterium tuberculosis . Specifically, some highly exposed individuals remain resistant to M . tuberculosis infection, as inferred by tuberculin skin test (TST) or interferon-gamma release assays (IGRAs). We performed a genome-wide association study of resistance to M . tuberculosis infection in an endemic region of Southern Vietnam. We enrolled household contacts (HHC) of pulmonary TB cases and compared subjects who were negative for both TST and IGRA (n = 185) with infected individuals (n = 353) who were either positive for both TST and IGRA or had a diagnosis of TB. We found a genome-wide significant locus on chromosome 10q26.2 with a cluster of variants associated with strong protection against M . tuberculosis infection (OR = 0.42, 95%CI 0.35–0.49, P = 3.71×10 −8 , for the genotyped variant rs17155120). The locus was replicated in a French multi-ethnic HHC cohort and a familial admixed cohort from a hyper-endemic area of South Africa, with an overall OR for rs17155120 estimated at 0.50 (95%CI 0.45–0.55, P = 1.26×10 −9 ). The variants are located in intronic regions and upstream of C10orf90 , a tumor suppressor gene which encodes an ubiquitin ligase activating the transcription factor p53. In silico analysis showed that the protective alleles were associated with a decreased expression in monocytes of the nearby gene ADAM12 which could lead to an enhanced response of Th17 lymphocytes. Our results reveal a novel locus controlling resistance to M . tuberculosis infection across different populations. There is strong epidemiological evidence that a proportion of highly exposed individuals remain resistant to M . tuberculosis infection, as shown by a negative result for Tuberculin Skin Test (TST) or IFN-γ Release Assays (IGRAs). We performed a genome-wide association study between resistant and infected individuals, which were carefully selected employing a household contact design to maximize exposure by infectious index patients. We employed stringently defined concordant results for both TST and IGRA assays to avoid misclassifications. We discovered a locus at 10q26.2 associated with resistance to M . tuberculosis infection in a Vietnamese discovery cohort. This locus could be replicated in two independent cohorts from different epidemiological settings and of diverse ancestries enrolled in France and South Africa. |
| Audience | Academic |
| Author | Ton, Le Thi Ba, Nguyen Ngoc Cobat, Aurélie Bustamante, Jacinta Huong, Nguyen Thu Danh, Nguyễn Thanh Hoal, Eileen G. Thành, Lai The Schurr, Erwin Thai, Vu Hong Seeleuthner, Yoann Delacourt, Christophe Quistrebert, Jocelyn Jabot-Hanin, Fabienne Luong, Nguyễn Trong Kerner, Gaspard Orlova, Marianna Casanova, Jean-Laurent Abel, Laurent Alcaïs, Alexandre Boisson-Dupuis, Stéphanie Vincent, Quentin B. |
| AuthorAffiliation | 1 Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Paris, France 10 Necker Federative Research Structure, INSERM US24, CNRS UMS3633, Paris, France 6 Human Evolutionary Genetics Unit, Institut Pasteur, UMR2000, CNRS, Paris, France 7 Center for Social Disease Control, Binh Duong, Vietnam 15 Paediatric Pulmonology and Allergology Department, Necker Hospital for Sick Children, Paris, France 3 Infectious Diseases and Immunity in Global Health Program, Research Institute of the McGill University Health Centre, Montreal, Canada Case Western Reserve University School of Medicine, UNITED STATES 8 Bioinformatics Core Facility, Paris Descartes University, Paris, France 13 Hospital for Dermato-Venereology, Ho Chi Minh City, Vietnam 12 St Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York City, New York, United States of America 16 South African Medical Research Council Centre for Tuberculosis Research, DST-NRF Cent |
| AuthorAffiliation_xml | – name: 5 Departments of Medicine and Human Genetics, McGill University, Montreal, Canada – name: 15 Paediatric Pulmonology and Allergology Department, Necker Hospital for Sick Children, Paris, France – name: 7 Center for Social Disease Control, Binh Duong, Vietnam – name: 4 McGill International TB Centre, McGill University, Montreal, Canada – name: 8 Bioinformatics Core Facility, Paris Descartes University, Paris, France – name: 9 Bioinformatics Platform, INSERM UMR U1163, Imagine Institute, Paris, France – name: 11 Study Center of Immunodeficiencies, Necker Hospital for Sick Children, Paris, France – name: 1 Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Paris, France – name: 16 South African Medical Research Council Centre for Tuberculosis Research, DST-NRF Centre of Excellence for Biomedical Tuberculosis Research, Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa – name: Case Western Reserve University School of Medicine, UNITED STATES – name: 6 Human Evolutionary Genetics Unit, Institut Pasteur, UMR2000, CNRS, Paris, France – name: 12 St Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, Rockefeller University, New York City, New York, United States of America – name: 13 Hospital for Dermato-Venereology, Ho Chi Minh City, Vietnam – name: 10 Necker Federative Research Structure, INSERM US24, CNRS UMS3633, Paris, France – name: 14 Howard Hughes Medical Institute, New YorkCity, New York, United States of America – name: 3 Infectious Diseases and Immunity in Global Health Program, Research Institute of the McGill University Health Centre, Montreal, Canada – name: 2 University of Paris, Imagine Institute, Paris, France |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33661925$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2021 Public Library of Science 2021 Quistrebert 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/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2021 Quistrebert et al 2021 Quistrebert et al |
| Copyright_xml | – notice: COPYRIGHT 2021 Public Library of Science – notice: 2021 Quistrebert 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/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2021 Quistrebert et al 2021 Quistrebert et al |
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| DOI | 10.1371/journal.pgen.1009392 |
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| DocumentTitleAlternate | Genetics of resistance to Mycobacterium tuberculosis infection |
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| Snippet | The natural history of tuberculosis (TB) is characterized by a large inter-individual outcome variability after exposure to
Mycobacterium tuberculosis
.... The natural history of tuberculosis (TB) is characterized by a large inter-individual outcome variability after exposure to Mycobacterium tuberculosis.... Infection is inferred from the presence of anti-mycobacterial immunoreactivity, as shown by a positive result in tuberculin skin test (TST) and/or... |
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| SubjectTerms | Alleles Analysis Biology and Life Sciences Chromosome 10 Chromosomes Diagnosis Drug therapy Extensively drug-resistant tuberculosis Gene frequency Genetic aspects Genome-wide association studies Genomes Genotype & phenotype Genotypes Identification and classification Immunoreactivity Infections Medicine and Health Sciences Mycobacterium tuberculosis Natural history Patient outcomes People and Places Population Quantitative trait loci Skin tests Tuberculin Tuberculosis γ-Interferon |
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| Title | Genome-wide association study of resistance to Mycobacterium tuberculosis infection identifies a locus at 10q26.2 in three distinct populations |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/33661925 https://www.proquest.com/docview/2513685723 https://www.proquest.com/docview/2498501934 https://pubmed.ncbi.nlm.nih.gov/PMC7963100 https://doaj.org/article/4f7beee9588e480d8337e49640f11266 http://dx.doi.org/10.1371/journal.pgen.1009392 |
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