A missense variant in FTCD is associated with arsenic metabolism and toxicity phenotypes in Bangladesh
Inorganic arsenic (iAs) is a carcinogen, and exposure to iAs via food and water is a global public health problem. iAs-contaminated drinking water alone affects >100 million people worldwide, including ~50 million in Bangladesh. Once absorbed into the blood stream, most iAs is converted to mono-m...
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| Published in | PLoS genetics Vol. 15; no. 3; p. e1007984 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
20.03.2019
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7404 1553-7390 1553-7404 |
| DOI | 10.1371/journal.pgen.1007984 |
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| Abstract | Inorganic arsenic (iAs) is a carcinogen, and exposure to iAs via food and water is a global public health problem. iAs-contaminated drinking water alone affects >100 million people worldwide, including ~50 million in Bangladesh. Once absorbed into the blood stream, most iAs is converted to mono-methylated (MMA) and then di-methylated (DMA) forms, facilitating excretion in urine. Arsenic metabolism efficiency varies among individuals, in part due to genetic variation near AS3MT (arsenite methyltransferase; 10q24.32). To identify additional arsenic metabolism loci, we measured protein-coding variants across the human exome for 1,660 Bangladeshi individuals participating in the Health Effects of Arsenic Longitudinal Study (HEALS). Among the 19,992 coding variants analyzed exome-wide, the minor allele (A) of rs61735836 (p.Val101Met) in exon 3 of FTCD (formiminotransferase cyclodeaminase) was associated with increased urinary iAs% (P = 8x10-13), increased MMA% (P = 2x10-16) and decreased DMA% (P = 6x10-23). Among 2,401 individuals with arsenic-induced skin lesions (an indicator of arsenic toxicity and cancer risk) and 2,472 controls, carrying the low-efficiency A allele (frequency = 7%) was associated with increased skin lesion risk (odds ratio = 1.35; P = 1x10-5). rs61735836 is in weak linkage disequilibrium with all nearby variants. The high-efficiency/major allele (G/Valine) is human-specific and eliminates a start codon at the first 5´-proximal Kozak sequence in FTCD, suggesting selection against an alternative translation start site. FTCD is critical for catabolism of histidine, a process that generates one-carbon units that can enter the one-carbon/folate cycle, which provides methyl groups for arsenic metabolism. In our study population, FTCD and AS3MT SNPs together explain ~10% of the variation in DMA% and support a causal effect of arsenic metabolism efficiency on arsenic toxicity (i.e., skin lesions). In summary, this work identifies a coding variant in FTCD associated with arsenic metabolism efficiency, providing new evidence supporting the established link between one-carbon/folate metabolism and arsenic toxicity. |
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| AbstractList | Inorganic arsenic (iAs) is a carcinogen, and exposure to iAs via food and water is a global public health problem. iAs-contaminated drinking water alone affects >100 million people worldwide, including ~50 million in Bangladesh. Once absorbed into the blood stream, most iAs is converted to mono-methylated (MMA) and then di-methylated (DMA) forms, facilitating excretion in urine. Arsenic metabolism efficiency varies among individuals, in part due to genetic variation near AS3MT (arsenite methyltransferase; 10q24.32). To identify additional arsenic metabolism loci, we measured protein-coding variants across the human exome for 1,660 Bangladeshi individuals participating in the Health Effects of Arsenic Longitudinal Study (HEALS). Among the 19,992 coding variants analyzed exome-wide, the minor allele (A) of rs61735836 (p.Val101Met) in exon 3 of FTCD (formiminotransferase cyclodeaminase) was associated with increased urinary iAs% (P = 8x10-13), increased MMA% (P = 2x10-16) and decreased DMA% (P = 6x10-23). Among 2,401 individuals with arsenic-induced skin lesions (an indicator of arsenic toxicity and cancer risk) and 2,472 controls, carrying the low-efficiency A allele (frequency = 7%) was associated with increased skin lesion risk (odds ratio = 1.35; P = 1x10-5). rs61735836 is in weak linkage disequilibrium with all nearby variants. The high-efficiency/major allele (G/Valine) is human-specific and eliminates a start codon at the first 5´-proximal Kozak sequence in FTCD, suggesting selection against an alternative translation start site. FTCD is critical for catabolism of histidine, a process that generates one-carbon units that can enter the one-carbon/folate cycle, which provides methyl groups for arsenic metabolism. In our study population, FTCD and AS3MT SNPs together explain ~10% of the variation in DMA% and support a causal effect of arsenic metabolism efficiency on arsenic toxicity (i.e., skin lesions). In summary, this work identifies a coding variant in FTCD associated with arsenic metabolism efficiency, providing new evidence supporting the established link between one-carbon/folate metabolism and arsenic toxicity. Inorganic arsenic (iAs) is a carcinogen, and exposure to iAs via food and water is a global public health problem. iAs-contaminated drinking water alone affects >100 million people worldwide, including ~50 million in Bangladesh. Once absorbed into the blood stream, most iAs is converted to mono-methylated (MMA) and then di-methylated (DMA) forms, facilitating excretion in urine. Arsenic metabolism efficiency varies among individuals, in part due to genetic variation near AS3MT (arsenite methyltransferase; 10q24.32). To identify additional arsenic metabolism loci, we measured protein-coding variants across the human exome for 1,660 Bangladeshi individuals participating in the Health Effects of Arsenic Longitudinal Study (HEALS). Among the 19,992 coding variants analyzed exome-wide, the minor allele (A) of rs61735836 (p.Val101Met) in exon 3 of FTCD (formiminotransferase cyclodeaminase) was associated with increased urinary iAs% (P = 8x10.sup.-13 ), increased MMA% (P = 2x10.sup.-16) and decreased DMA% (P = 6x10.sup.-23). Among 2,401 individuals with arsenic-induced skin lesions (an indicator of arsenic toxicity and cancer risk) and 2,472 controls, carrying the low-efficiency A allele (frequency = 7%) was associated with increased skin lesion risk (odds ratio = 1.35; P = 1x10.sup.-5). rs61735836 is in weak linkage disequilibrium with all nearby variants. The high-efficiency/major allele (G/Valine) is human-specific and eliminates a start codon at the first 5'-proximal Kozak sequence in FTCD, suggesting selection against an alternative translation start site. FTCD is critical for catabolism of histidine, a process that generates one-carbon units that can enter the one-carbon/folate cycle, which provides methyl groups for arsenic metabolism. In our study population, FTCD and AS3MT SNPs together explain ~10% of the variation in DMA% and support a causal effect of arsenic metabolism efficiency on arsenic toxicity (i.e., skin lesions). In summary, this work identifies a coding variant in FTCD associated with arsenic metabolism efficiency, providing new evidence supporting the established link between one-carbon/folate metabolism and arsenic toxicity. Inorganic arsenic (iAs) is a carcinogen, and exposure to iAs via food and water is a global public health problem. iAs-contaminated drinking water alone affects >100 million people worldwide, including ~50 million in Bangladesh. Once absorbed into the blood stream, most iAs is converted to mono-methylated (MMA) and then di-methylated (DMA) forms, facilitating excretion in urine. Arsenic metabolism efficiency varies among individuals, in part due to genetic variation near AS3MT (arsenite methyltransferase; 10q24.32). To identify additional arsenic metabolism loci, we measured protein-coding variants across the human exome for 1,660 Bangladeshi individuals participating in the Health Effects of Arsenic Longitudinal Study (HEALS). Among the 19,992 coding variants analyzed exome-wide, the minor allele (A) of rs61735836 (p.Val101Met) in exon 3 of FTCD (formiminotransferase cyclodeaminase) was associated with increased urinary iAs% (P = 8x10 -13 ), increased MMA% (P = 2x10 -16 ) and decreased DMA% (P = 6x10 -23 ). Among 2,401 individuals with arsenic-induced skin lesions (an indicator of arsenic toxicity and cancer risk) and 2,472 controls, carrying the low-efficiency A allele (frequency = 7%) was associated with increased skin lesion risk (odds ratio = 1.35; P = 1x10 -5 ). rs61735836 is in weak linkage disequilibrium with all nearby variants. The high-efficiency/major allele (G/Valine) is human-specific and eliminates a start codon at the first 5´-proximal Kozak sequence in FTCD , suggesting selection against an alternative translation start site. FTCD is critical for catabolism of histidine, a process that generates one-carbon units that can enter the one-carbon/folate cycle, which provides methyl groups for arsenic metabolism. In our study population, FTCD and AS3MT SNPs together explain ~10% of the variation in DMA% and support a causal effect of arsenic metabolism efficiency on arsenic toxicity (i.e., skin lesions). In summary, this work identifies a coding variant in FTCD associated with arsenic metabolism efficiency, providing new evidence supporting the established link between one-carbon/folate metabolism and arsenic toxicity. Chronic exposure to arsenic through food and drinking water is a serious global health issue, as arsenic can increase risk for cancer, cardiorespiratory diseases, and other chronic conditions. Ingested arsenic absorbed into the blood stream is metabolized (through reduction and methylation reactions) in order to facilitate excretion in urine and removal from the body. Individuals differ with respect to the efficiency of this metabolism, in part due to inherited genetic variation. The only region of the genome known to contain variation that impacts arsenic metabolism efficiency is 10q24.32, and these variants likely alter the function of the nearby gene AS3MT (arsenite methyltransferase). In order to identify new genetic variants that affect arsenic metabolism, we measured variation in protein-coding regions across the entire genome for >4,800 individuals with varying levels of exposure to arsenic through naturally-contaminated drinking water in Bangladesh. Using this data, we identified a variant in the FTCD gene (formiminotransferase cyclodeaminase) that is associated with arsenic metabolism efficiency and risk for arsenic-induced skin lesions. This genetic variant alters the FTCD amino acid sequence, potentially disrupting a cryptic protein translation start site in exon 3. FTCD codes for an enzyme involved in histidine catabolism and one-carbon/folate metabolism; thus, our result provides new evidence supporting the well-established hypothesis that the folate/one-carbon cycle plays an important role in arsenic-related disease. Inorganic arsenic (iAs) is a carcinogen, and exposure to iAs via food and water is a global public health problem. iAs-contaminated drinking water alone affects >100 million people worldwide, including ~50 million in Bangladesh. Once absorbed into the blood stream, most iAs is converted to mono-methylated (MMA) and then di-methylated (DMA) forms, facilitating excretion in urine. Arsenic metabolism efficiency varies among individuals, in part due to genetic variation near AS3MT (arsenite methyltransferase; 10q24.32). To identify additional arsenic metabolism loci, we measured protein-coding variants across the human exome for 1,660 Bangladeshi individuals participating in the Health Effects of Arsenic Longitudinal Study (HEALS). Among the 19,992 coding variants analyzed exome-wide, the minor allele (A) of rs61735836 (p.Val101Met) in exon 3 of FTCD (formiminotransferase cyclodeaminase) was associated with increased urinary iAs% (P = 8x10-13), increased MMA% (P = 2x10-16) and decreased DMA% (P = 6x10-23). Among 2,401 individuals with arsenic-induced skin lesions (an indicator of arsenic toxicity and cancer risk) and 2,472 controls, carrying the low-efficiency A allele (frequency = 7%) was associated with increased skin lesion risk (odds ratio = 1.35; P = 1x10-5). rs61735836 is in weak linkage disequilibrium with all nearby variants. The high-efficiency/major allele (G/Valine) is human-specific and eliminates a start codon at the first 5´-proximal Kozak sequence in FTCD, suggesting selection against an alternative translation start site. FTCD is critical for catabolism of histidine, a process that generates one-carbon units that can enter the one-carbon/folate cycle, which provides methyl groups for arsenic metabolism. In our study population, FTCD and AS3MT SNPs together explain ~10% of the variation in DMA% and support a causal effect of arsenic metabolism efficiency on arsenic toxicity (i.e., skin lesions). In summary, this work identifies a coding variant in FTCD associated with arsenic metabolism efficiency, providing new evidence supporting the established link between one-carbon/folate metabolism and arsenic toxicity.Inorganic arsenic (iAs) is a carcinogen, and exposure to iAs via food and water is a global public health problem. iAs-contaminated drinking water alone affects >100 million people worldwide, including ~50 million in Bangladesh. Once absorbed into the blood stream, most iAs is converted to mono-methylated (MMA) and then di-methylated (DMA) forms, facilitating excretion in urine. Arsenic metabolism efficiency varies among individuals, in part due to genetic variation near AS3MT (arsenite methyltransferase; 10q24.32). To identify additional arsenic metabolism loci, we measured protein-coding variants across the human exome for 1,660 Bangladeshi individuals participating in the Health Effects of Arsenic Longitudinal Study (HEALS). Among the 19,992 coding variants analyzed exome-wide, the minor allele (A) of rs61735836 (p.Val101Met) in exon 3 of FTCD (formiminotransferase cyclodeaminase) was associated with increased urinary iAs% (P = 8x10-13), increased MMA% (P = 2x10-16) and decreased DMA% (P = 6x10-23). Among 2,401 individuals with arsenic-induced skin lesions (an indicator of arsenic toxicity and cancer risk) and 2,472 controls, carrying the low-efficiency A allele (frequency = 7%) was associated with increased skin lesion risk (odds ratio = 1.35; P = 1x10-5). rs61735836 is in weak linkage disequilibrium with all nearby variants. The high-efficiency/major allele (G/Valine) is human-specific and eliminates a start codon at the first 5´-proximal Kozak sequence in FTCD, suggesting selection against an alternative translation start site. FTCD is critical for catabolism of histidine, a process that generates one-carbon units that can enter the one-carbon/folate cycle, which provides methyl groups for arsenic metabolism. In our study population, FTCD and AS3MT SNPs together explain ~10% of the variation in DMA% and support a causal effect of arsenic metabolism efficiency on arsenic toxicity (i.e., skin lesions). In summary, this work identifies a coding variant in FTCD associated with arsenic metabolism efficiency, providing new evidence supporting the established link between one-carbon/folate metabolism and arsenic toxicity. |
| Audience | Academic |
| Author | Argos, Maria Shahriar, Hasan Dean, Samantha Islam, Tariqul Tong, Lin Yunus, Md Islam, Md. Tariqul Pierce, Brandon L. Rakibuz-Zaman, Muhammad Lynch, Vincent J. Gamble, Mary V. Kibriya, Muhammad G. Jasmine, Farzana Rahman, Mahfuzar Ahsan, Habibul Sarwar, Golam Oglesbee, Devin Graziano, Joseph H. |
| AuthorAffiliation | 3 Comprehensive Cancer Center, The University of Chicago, Chicago, IL United States of America 8 Department of Laboratory Medicine and Pathology, Mayo Clinic College of Medicine, Rochester, MN, United States of America 7 International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh 1 Department of Public Health Sciences, The University of Chicago, Chicago, IL, United States of America 6 Research and Evaluation Division, BRAC, Dhaka, Bangladesh 4 Division of Epidemiology and Biostatistics, University of Illinois at Chicago, Chicago, IL, United States of America 10 Department of Medicine, The University of Chicago, Chicago, IL, United States of America 5 UChicago Research Bangladesh, Mohakhali, Dhaka, Bangladesh 11 Institute for Population and Precision Health, The University of Chicago, Chicago, IL, United States of America 9 Department of Environmental Health Sciences, Mailman School of Public Health, Columbia University, New York, NY, United States of America 2 Department |
| AuthorAffiliation_xml | – name: 9 Department of Environmental Health Sciences, Mailman School of Public Health, Columbia University, New York, NY, United States of America – name: 5 UChicago Research Bangladesh, Mohakhali, Dhaka, Bangladesh – name: 10 Department of Medicine, The University of Chicago, Chicago, IL, United States of America – name: 2 Department of Human Genetics, The University of Chicago, Chicago, IL, United States of America – name: Stanford University School of Medicine, UNITED STATES – name: 3 Comprehensive Cancer Center, The University of Chicago, Chicago, IL United States of America – name: 7 International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh – name: 4 Division of Epidemiology and Biostatistics, University of Illinois at Chicago, Chicago, IL, United States of America – name: 6 Research and Evaluation Division, BRAC, Dhaka, Bangladesh – name: 8 Department of Laboratory Medicine and Pathology, Mayo Clinic College of Medicine, Rochester, MN, United States of America – name: 1 Department of Public Health Sciences, The University of Chicago, Chicago, IL, United States of America – name: 11 Institute for Population and Precision Health, The University of Chicago, Chicago, IL, United States of America |
| Author_xml | – sequence: 1 givenname: Brandon L. orcidid: 0000-0002-7829-952X surname: Pierce fullname: Pierce, Brandon L. – sequence: 2 givenname: Lin surname: Tong fullname: Tong, Lin – sequence: 3 givenname: Samantha orcidid: 0000-0003-1517-3118 surname: Dean fullname: Dean, Samantha – sequence: 4 givenname: Maria orcidid: 0000-0003-4234-252X surname: Argos fullname: Argos, Maria – sequence: 5 givenname: Farzana surname: Jasmine fullname: Jasmine, Farzana – sequence: 6 givenname: Muhammad surname: Rakibuz-Zaman fullname: Rakibuz-Zaman, Muhammad – sequence: 7 givenname: Golam surname: Sarwar fullname: Sarwar, Golam – sequence: 8 givenname: Md. Tariqul surname: Islam fullname: Islam, Md. Tariqul – sequence: 9 givenname: Hasan orcidid: 0000-0002-1625-0229 surname: Shahriar fullname: Shahriar, Hasan – sequence: 10 givenname: Tariqul surname: Islam fullname: Islam, Tariqul – sequence: 11 givenname: Mahfuzar surname: Rahman fullname: Rahman, Mahfuzar – sequence: 12 givenname: Md surname: Yunus fullname: Yunus, Md – sequence: 13 givenname: Vincent J. orcidid: 0000-0001-5311-3824 surname: Lynch fullname: Lynch, Vincent J. – sequence: 14 givenname: Devin orcidid: 0000-0002-7147-5527 surname: Oglesbee fullname: Oglesbee, Devin – sequence: 15 givenname: Joseph H. surname: Graziano fullname: Graziano, Joseph H. – sequence: 16 givenname: Muhammad G. surname: Kibriya fullname: Kibriya, Muhammad G. – sequence: 17 givenname: Mary V. surname: Gamble fullname: Gamble, Mary V. – sequence: 18 givenname: Habibul surname: Ahsan fullname: Ahsan, Habibul |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30893314$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2019 Public Library of Science 2019 Pierce 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. 2019 Pierce et al 2019 Pierce et al |
| Copyright_xml | – notice: COPYRIGHT 2019 Public Library of Science – notice: 2019 Pierce 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: 2019 Pierce et al 2019 Pierce et al |
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| DOI | 10.1371/journal.pgen.1007984 |
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| Snippet | Inorganic arsenic (iAs) is a carcinogen, and exposure to iAs via food and water is a global public health problem. iAs-contaminated drinking water alone... |
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| SubjectTerms | Adult Alleles Amino acids Ammonia-Lyases - genetics Ammonia-Lyases - physiology Arsenic Arsenic - metabolism Arsenic - toxicity Arsenic compounds Arsenic Poisoning Arsenite Arsenite methyltransferase Bangladesh Biology and Life Sciences Cancer Carbon Carbon cycle Carcinogens Cardiovascular disease Codons Diabetes Drinking behavior Drinking water Efficiency Environmental Exposure Environmental health Enzymes Epidemiology Excretion Female Folic acid Folic Acid - metabolism Funding Gene frequency Gene Frequency - genetics Genetic aspects Genetic diversity Genetic variation Genetics Genomes Glutamate Formimidoyltransferase - genetics Glutamate Formimidoyltransferase - physiology Health sciences Histidine Humans Linkage disequilibrium Longitudinal studies Male Medicine and Health Sciences Metabolism Metabolites Methylation Methyltransferases - genetics Methyltransferases - metabolism Multifunctional Enzymes Mutation, Missense Odds Ratio Phenotype Phenotypes Physical Sciences Physiological aspects Polymorphism, Single Nucleotide - genetics Population studies Protein turnover Public health Risk Factors Single-nucleotide polymorphism Skin Skin diseases Skin Diseases - chemically induced Skin Diseases - genetics Toxicity Transferases Urine Valine Vitamin B Water Water Pollutants, Chemical |
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| Title | A missense variant in FTCD is associated with arsenic metabolism and toxicity phenotypes in Bangladesh |
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