Large-scale GWAS of food liking reveals genetic determinants and genetic correlations with distinct neurophysiological traits

TY - JOUR

T1 - Large-scale GWAS of food liking reveals genetic determinants and genetic correlations with distinct neurophysiological traits

AU - May-Wilson, Sebastian

AU - Matoba, Nana

AU - Wade, Kaitlin H.

AU - Hottenga, Jouke Jan

AU - Concas, Maria Pina

AU - Mangino, Massimo

AU - Grzeszkowiak, Eryk J.

AU - Menni, Cristina

AU - Gasparini, Paolo

AU - Timpson, Nicholas J.

AU - Veldhuizen, Maria G.

AU - de Geus, Eco

AU - Wilson, James F.

AU - Pirastu, Nicola

N1 - Funding Information: We would like to thank all the study participants without whom this study would not have been possible. We would like to thank, Prof Catherine Sudlow for her support to this project, Dr. Jo Holliday for all the work during the final questionnaire definition and roll out. We would further like to thank Dr. Michel Nivard and Dr. Yakov A. Tsepilov for the advice and the great methods they have produced. This research has been conducted using the UK Biobank Resource under Application Number 19655. The Viking Health Study—Shetland (VIKING): DNA extractions and genotyping were performed at the Edinburgh Clinical Research Facility, University of Edinburgh. We would like to acknowledge the invaluable contributions of the research nurses in Shetland, the administrative team in Edinburgh and the people of Shetland. We are extremely grateful to all the families who took part in this study, the midwives for their help in recruiting them, and the whole ALSPAC team, which includes interviewers, computer and laboratory technicians, clerical workers, research scientists, volunteers, managers, receptionists and nurses. Genome-wide association data were generated by Sample Logistics and Genotyping Facilities at Wellcome Sanger Institute and LabCorp (Laboratory Corporation of America) using support from 23andMe. We are very grateful to the municipal administrators of all INGI cohorts, for their collaboration on the project and for logistic support. We would like to thank all participants to this study. J.F.W. acknowledges support from the MRC Human Genetics Unit programme grant, “Quantitative traits in health and disease” (U. MC_UU_00007/10). M.G.V. is supported by the 2232 International Fellowship for Outstanding Researchers Program of TÜBİTAK under award number 118C299. This work was supported by IRCCS Burlo Garofalo of Trieste, funding 5 per mille 2015 senses “Genetics of senses and related diseases” to P.G. Funding was obtained from the Netherlands Organization for Scientific Research (NWO) and The Netherlands Organisation for Health Research and Development (ZonMW) grants 904-61-090, 985-10-002, 904-61-193,480-04-004, 400-05-717, Addiction-31160008, 016-115-035, 400-07-080, Middelgroot-911-09-032, NWO-Groot 480-15-001/674, Center for Medical Systems Biology (CSMB, NWO Genomics), NBIC/BioAssist/RK(2008.024), Biobanking and Biomolecular Resources Research Infrastructure (BBMRI –NL, 184.021.007 and 184.033.111), X-Omics 184-034-019; Spinozapremie (NWO- 56-464-14192) and KNAW Academy Professor Award (PAH/6635) to D.I.B.; Amsterdam Public Health research institute (former EMGO+); the European Community’s Fifth and Seventh Framework Program (FP5- LIFE QUALITY-CT-2002-2006, FP7- HEALTH-F4-2007-2013, grant 01254: GenomEUtwin, grant 01413: ENGAGE); the European Research Council (ERC Starting 284167, ERC Consolidator 771057, ERC Advanced 230374), Rutgers University Cell and DNA Repository (NIMH U24 MH068457-06), the National Institutes of Health (NIH, R01D0042157-01A1, MH081802, DA018673, R01 DK092127-04, Grand Opportunity grants 1RC2 MH089951); the Avera Institute for Human Genetics, Sioux Falls, South Dakota (USA). ALSPAC: The UK Medical Research Council and Wellcome (Grant ref: 102215/2/13/2) and the University of Bristol provide core support for ALS TwinsUK receives funding from the Wellcome Trust (212904/Z/18/Z), Medical Research Council (AIMHY; MR/M016560/1) and European Union (H2020 contract #733100). TwinsUK and M.M. are supported by the National Institute for Health Research (NIHR)-funded BioResource, Clinical Research Facility and Biomedical Research Centre based at Guy’s and St Thomas’ NHS Foundation Trust in partnership with King’s College London. O.M. is supported by Chronic Disease Research Foundation (CDRF). C.M. is funded by the Chronic Disease Research Foundation and by the Medical Research Council (MRC)/British Heart Foundation Ancestry and Biological Informative Markers for Stratification of Hypertension (AIMHY; MR/M016560/1). NJT is a Wellcome Trust Investigator (202802/Z/16/Z), is the PI of the Avon Longitudinal Study of Parents and Children (MRC & WT 217065/Z/19/Z), is supported by the University of Bristol NIHR Biomedical Research Centre (BRC-1215-2001), the MRC Integrative Epidemiology Unit (MC_UU_00011/1) and works within the CRUK Integrative Cancer Epidemiology Programme (C18281/A29019). Funding Information: We would like to thank all the study participants without whom this study would not have been possible. We would like to thank, Prof Catherine Sudlow for her support to this project, Dr. Jo Holliday for all the work during the final questionnaire definition and roll out. We would further like to thank Dr. Michel Nivard and Dr. Yakov A. Tsepilov for the advice and the great methods they have produced. This research has been conducted using the UK Biobank Resource under Application Number 19655. The Viking Health Study—Shetland (VIKING): DNA extractions and genotyping were performed at the Edinburgh Clinical Research Facility, University of Edinburgh. We would like to acknowledge the invaluable contributions of the research nurses in Shetland, the administrative team in Edinburgh and the people of Shetland. We are extremely grateful to all the families who took part in this study, the midwives for their help in recruiting them, and the whole ALSPAC team, which includes interviewers, computer and laboratory technicians, clerical workers, research scientists, volunteers, managers, receptionists and nurses. Genome-wide association data were generated by Sample Logistics and Genotyping Facilities at Wellcome Sanger Institute and LabCorp (Laboratory Corporation of America) using support from 23andMe. We are very grateful to the municipal administrators of all INGI cohorts, for their collaboration on the project and for logistic support. We would like to thank all participants to this study. J.F.W. acknowledges support from the MRC Human Genetics Unit programme grant, “Quantitative traits in health and disease” (U. MC_UU_00007/10). M.G.V. is supported by the 2232 International Fellowship for Outstanding Researchers Program of TÜBİTAK under award number 118C299. This work was supported by IRCCS Burlo Garofalo of Trieste, funding 5 per mille 2015 senses “Genetics of senses and related diseases” to P.G. Funding was obtained from the Netherlands Organization for Scientific Research (NWO) and The Netherlands Organisation for Health Research and Development (ZonMW) grants 904-61-090, 985-10-002, 904-61-193,480-04-004, 400-05-717, Addiction-31160008, 016-115-035, 400-07-080, Middelgroot-911-09-032, NWO-Groot 480-15-001/674, Center for Medical Systems Biology (CSMB, NWO Genomics), NBIC/BioAssist/RK(2008.024), Biobanking and Biomolecular Resources Research Infrastructure (BBMRI –NL, 184.021.007 and 184.033.111), X-Omics 184-034-019; Spinozapremie (NWO- 56-464-14192) and KNAW Academy Professor Award (PAH/6635) to D.I.B.; Amsterdam Public Health research institute (former EMGO+); the European Community’s Fifth and Seventh Framework Program (FP5- LIFE QUALITY-CT-2002-2006, FP7- HEALTH-F4-2007-2013, grant 01254: GenomEUtwin, grant 01413: ENGAGE); the European Research Council (ERC Starting 284167, ERC Consolidator 771057, ERC Advanced 230374), Rutgers University Cell and DNA Repository (NIMH U24 MH068457-06), the National Institutes of Health (NIH, R01D0042157-01A1, MH081802, DA018673, R01 DK092127-04, Grand Opportunity grants 1RC2 MH089951); the Avera Institute for Human Genetics, Sioux Falls, South Dakota (USA). ALSPAC: The UK Medical Research Council and Wellcome (Grant ref: 102215/2/13/2) and the University of Bristol provide core support for ALS TwinsUK receives funding from the Wellcome Trust (212904/Z/18/Z), Medical Research Council (AIMHY; MR/M016560/1) and European Union (H2020 contract #733100). TwinsUK and M.M. are supported by the National Institute for Health Research (NIHR)-funded BioResource, Clinical Research Facility and Biomedical Research Centre based at Guy’s and St Thomas’ NHS Foundation Trust in partnership with King’s College London. O.M. is supported by Chronic Disease Research Foundation (CDRF). C.M. is funded by the Chronic Disease Research Foundation and by the Medical Research Council (MRC)/British Heart Foundation Ancestry and Biological Informative Markers for Stratification of Hypertension (AIMHY; MR/M016560/1). NJT is a Wellcome Trust Investigator (202802/Z/16/Z), is the PI of the Avon Longitudinal Study of Parents and Children (MRC & WT 217065/Z/19/Z), is supported by the University of Bristol NIHR Biomedical Research Centre (BRC-1215-2001), the MRC Integrative Epidemiology Unit (MC_UU_00011/1) and works within the CRUK Integrative Cancer Epidemiology Programme (C18281/A29019). Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - We present the results of a GWAS of food liking conducted on 161,625 participants from the UK-Biobank. Liking was assessed over 139 specific foods using a 9-point scale. Genetic correlations coupled with structural equation modelling identified a multi-level hierarchical map of food-liking with three main dimensions: “Highly-palatable”, “Acquired” and “Low-caloric”. The Highly-palatable dimension is genetically uncorrelated from the other two, suggesting that independent processes underlie liking high reward foods. This is confirmed by genetic correlations with MRI brain traits which show with distinct associations. Comparison with the corresponding food consumption traits shows a high genetic correlation, while liking exhibits twice the heritability. GWAS analysis identified 1,401 significant food-liking associations which showed substantial agreement in the direction of effects with 11 independent cohorts. In conclusion, we created a comprehensive map of the genetic determinants and associated neurophysiological factors of food-liking.

AB - We present the results of a GWAS of food liking conducted on 161,625 participants from the UK-Biobank. Liking was assessed over 139 specific foods using a 9-point scale. Genetic correlations coupled with structural equation modelling identified a multi-level hierarchical map of food-liking with three main dimensions: “Highly-palatable”, “Acquired” and “Low-caloric”. The Highly-palatable dimension is genetically uncorrelated from the other two, suggesting that independent processes underlie liking high reward foods. This is confirmed by genetic correlations with MRI brain traits which show with distinct associations. Comparison with the corresponding food consumption traits shows a high genetic correlation, while liking exhibits twice the heritability. GWAS analysis identified 1,401 significant food-liking associations which showed substantial agreement in the direction of effects with 11 independent cohorts. In conclusion, we created a comprehensive map of the genetic determinants and associated neurophysiological factors of food-liking.

UR - http://www.scopus.com/inward/record.url?scp=85130293053&partnerID=8YFLogxK

U2 - 10.1038/s41467-022-30187-w

DO - 10.1038/s41467-022-30187-w

M3 - Article

C2 - 35585065

AN - SCOPUS:85130293053

SN - 2041-1723

VL - 13

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 2743

ER -