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Parent-of-origin-specific allelic associations among 106 genomic loci for age at menarche
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Here 106 genomic loci associated with age at menarche, a marker of puberty timing in females, are identified; these loci show enrichment for genes involved in nuclear hormone receptor function, body mass index, and rare disorders of puberty, and for genes located in imprinted regions, with parent-of-origin specific effects at several loci. The age at which females first experience menstruation, called menarche, is a heritable trait associated with risks for obesity, type 2 diabetes, cardiovascular disease, breast cancer and general mortality. This large-scale genome-wide association study identifies 123 signals at 106 genomic loci associated with age at menarche. New findings include parent-of-origin-specific allelic associations (both maternally and paternally driven) at three imprinted loci and the implication of retinoic acid and GABAB receptor II signalling and lysine-specific histone demethylation. These data bring new insights into the genetic architecture of puberty timing and suggest a model involving thousands of genetic variants. Age at menarche is a marker of timing of puberty in females. It varies widely between individuals, is a heritable trait and is associated with risks for obesity, type 2 diabetes, cardiovascular disease, breast cancer and all-cause mortality1. Studies of rare human disorders of puberty and animal models point to a complex hypothalamic-pituitary-hormonal regulation2,3, but the mechanisms that determine pubertal timing and underlie its links to disease risk remain unclear. Here, using genome-wide and custom-genotyping arrays in up to 182,416 women of European descent from 57 studies, we found robust evidence (P < 5 × 10−8) for 123 signals at 106 genomic loci associated with age at menarche. Many loci were associated with other pubertal traits in both sexes, and there was substantial overlap with genes implicated in body mass index and various diseases, including rare disorders of puberty. Menarche signals were enriched in imprinted regions, with three loci (DLK1-WDR25, MKRN3-MAGEL2 and KCNK9) demonstrating parent-of-origin-specific associations concordant with known parental expression patterns. Pathway analyses implicated nuclear hormone receptors, particularly retinoic acid and γ-aminobutyric acid-B2 receptor signalling, among novel mechanisms that regulate pubertal timing in humans. Our findings suggest a genetic architecture involving at least hundreds of common variants in the coordinated timing of the pubertal transition.
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“In a recent meta-analysis of genome-wide association and custom-genotyping array studies of age at menarche in up to 182 416 women of European descent, a variant downstream of MKRN3 had the largest effect size for association with menarche when the variant was paternally inherited.80”
From Pubertal development and regulation (2016) · cites this paper as [80]
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“After identification of the association of MKRN3 with puberty regulation, single nucleotide polymorphisms in imprinted gene regions were linked to the age of menarche, supporting puberty timing as a selective trait.80”
From Pubertal development and regulation (2016) · cites this paper as [80]
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Metadata
- Authors
- Study, A. O. C., Perry, J. R. B., The GENICA Network, kConFab, Study, T. L. C., The InterAct Consortium, Early Growth Genetics (EGG) Consortium, Day, F., Elks, C. E., Sulem, P., Thompson, D. J., Ferreira, T., He, C., Chasman, D. I., Esko, T., Thorleifsson, G., Albrecht, E., Ang, W. Q., Corre, T., Cousminer, D. L., Feenstra, B., Franceschini, N., Ganna, A., Johnson, A. D., Kjellqvist, S., Lunetta, K. L., McMahon, G., Nolte, I. M., Paternoster, L., Porcu, E., Smith, A. V., Stolk, L., Teumer, A., Tšernikova, N., Tikkanen, E., Ulivi, S., Wagner, E. K., Amin, N., Bierut, L. J., Byrne, E. M., Hottenga, J.-J., Koller, D. L., Mangino, M., Pers, T. H., Yerges-Armstrong, L. M., Hua Zhao, J., Andrulis, I. L., Anton-Culver, H., Atsma, F., Bandinelli, S., Beckmann, M. W., Benitez, J., Blomqvist, C., Bojesen, S. E., Bolla, M. K., Bonanni, B., Brauch, H., Brenner, H., Buring, J. E., Chang-Claude, J., Chanock, S., Chen, J., Chenevix-Trench, G., Collée, J. M., Couch, F. J., Couper, D., Coviello, A. D., Cox, A., Czene, K., D’adamo, A. P., Davey Smith, G., De Vivo, I., Demerath, E. W., Dennis, J., Devilee, P., Dieffenbach, A. K., Dunning, A. M., Eiriksdottir, G., Eriksson, J. G., Fasching, P. A., Ferrucci, L., Flesch-Janys, D., Flyger, H., Foroud, T., Franke, L., Garcia, M. E., García-Closas, M., Geller, F., de Geus, E. E. J., Giles, G. G., Gudbjartsson, D. F., Gudnason, V., Guénel, P., Guo, S., Hall, P., Hamann, U., Haring, R., Hartman, C. A., Heath, A. C., Hofman, A., Hooning, M. J., Hopper, J. L., Hu, F. B., Hunter, D. J., Karasik, D., Kiel, D. P., Knight, J. A., Kosma, V.-M., Kutalik, Z., Lai, S., Lambrechts, D., Lindblom, A., Mägi, R., Magnusson, P. K., Mannermaa, A., Martin, N. G., Masson, G., McArdle, P. F., McArdle, W. L., Melbye, M., Michailidou, K., Mihailov, E., Milani, L., Milne, R. L., Nevanlinna, H., Neven, P., Nohr, E. A., Oldehinkel, A. J., Oostra, B. A., Palotie, A., Peacock, M., Pedersen, N. L., Peterlongo, P., Peto, J., Pharoah, P. D. P., Postma, D. S., Pouta, A., Pylkäs, K., Radice, P., Ring, S., Rivadeneira, F., Robino, A., Rose, L. M., Rudolph, A., Salomaa, V., Sanna, S., Schlessinger, D., Schmidt, M. K., Southey, M. C., Sovio, U., Stampfer, M. J., Stöckl, D., Storniolo, A. M., Timpson, N. J., Tyrer, J., Visser, J. A., Vollenweider, P., Völzke, H., Waeber, G., Waldenberger, M., Wallaschofski, H., Wang, Q., Willemsen, G., Winqvist, R., Wolffenbuttel, B. H. R., Wright, M. J., Boomsma, D. I., Econs, M. J., Khaw, K.-T., Loos, R. J. F., McCarthy, M. I., Montgomery, G. W., Rice, J. P., Streeten, E. A., Thorsteinsdottir, U., van Duijn, C. M., Alizadeh, B. Z., Bergmann, S., Boerwinkle, E., Boyd, H. A., Crisponi, L., Gasparini, P., Gieger, C., Harris, T. B., Ingelsson, E., Järvelin, M.-R., Kraft, P., Lawlor, D., Metspalu, A., Pennell, C. E., Ridker, P. M., Snieder, H., Sørensen, T. I. A., Spector, T. D., Strachan, D. P., Uitterlinden, A. G., Wareham, N. J., Widen, E., Zygmunt, M., Murray, A., Easton, D. F., Stefansson, K., Murabito, J. M., & Ong, K. K.
- Affiliations
- Centre for Human Genetics (GB)
- University of Bonn (DE)
- deCODE Genetics (Iceland) (IS)
- University of Cambridge (GB)
- Indiana University Health (US)
- Brigham and Women's Hospital (US)
- Broad Institute (US)
- Statens Serum Institut (DK)
- University of North Carolina at Chapel Hill (US)
- SIB Swiss Institute of Bioinformatics (CH)
- Boston University (US)
- Karolinska Institutet (SE)
- Science for Life Laboratory (SE)
- University of Bristol (GB)
- University Medical Center Groningen (NL)
- Universitätsmedizin Greifswald (DE)
- University of Sassari (IT)
- University of Helsinki (FI)
- IRCCS Materno Infantile Burlo Garofolo (IT)
- Erasmus MC (NL)
- The University of Queensland (AU)
- King's College London (GB)
- University of Maryland, Baltimore (US)
- Mount Sinai Hospital (CA)
- University of Copenhagen (DK)
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- Spanish National Cancer Research Centre (ES)
- German Cancer Research Center (DE)
- Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology (DE)
- Mayo Clinic (US)
- University of Minnesota (US)
- Institute of Cancer Research (GB)
- National Institutes of Health (US)
- The University of Melbourne (AU)
- University of Iceland (IS)
- Université Paris-Sud (FR)
- Washington University in St. Louis (US)
- Harvard University (US)
- Beth Israel Deaconess Medical Center (US)
- University of Eastern Finland (FI)
- QIMR Berghofer Medical Research Institute (AU)
- University of Tartu (EE)
- University of Southern Denmark (DK)
- Finnish Institute for Health and Welfare (FI)
- Oulu University Hospital (FI)
- University of Trieste (IT)
- National Research Council (IT)
- The Netherlands Cancer Institute (NL)
- Centre Hospitalier Universitaire Vaudois (CH)
- Vrije Universiteit Amsterdam (NL)
- Icahn School of Medicine at Mount Sinai (US)
- Churchill Hospital (GB)
- Centre for Medical Systems Biology (NL)
- Helmholtz Munich (DE)
- Uppsala University (SE)
- The University of Western Australia (AU)
- St George's, University of London (GB)
- University of Exeter (GB)
- Corresponding author
- Perry, John R. B.
- Murabito, Joanne M.
- ORCID
- Perry, John R. B.
- Day, Felix
- Sulem, Patrick
- Thompson, Deborah J.
- Ferreira, Teresa
- He, Chunyan
- Chasman, Daniel I.
- Esko, Tõnu
- Corre, Tanguy
- Feenstra, Bjarke
- Franceschini, Nora
- Ganna, Andrea
- Johnson, Andrew D.
- Lunetta, Kathryn L.
- Nolte, Ilja M.
- Paternoster, Lavinia
- Porcu, Eleonora
- Smith, Albert V.
- Teumer, Alexander
- Tikkanen, Emmi
- Ulivi, Sheila
- Amin, Najaf
- Bierut, Laura J.
- Byrne, Enda M.
- Hottenga, Jouke-Jan
- Mangino, Massimo
- Pers, Tune H.
- Yerges-Armstrong, Laura M.
- Andrulis, Irene L.
- Atsma, Femke
- Bandinelli, Stefania
- Beckmann, Matthias W.
- Benitez, Javier
- Blomqvist, Carl
- Bojesen, Stig E.
- Bolla, Manjeet K.
- Bonanni, Bernardo
- Brauch, Hiltrud
- Brenner, Hermann
- Buring, Julie E.
- Chang-Claude, Jenny
- Chanock, Stephen
- Chen, Jinhui
- Couch, Fergus J.
- Couper, David
- Coviello, Andrea D.
- Cox, Angela
- Czene, Kamila
- Demerath, Ellen W.
- Dennis, Joe
- Devilee, Peter
- Dunning, Alison M.
- Eriksson, Johan G.
- Fasching, Peter A.
- Ferrucci, Luigi
- Foroud, Tatiana
- Franke, Lude
- Geller, Frank
- Giles, Graham G.
- Gudbjartsson, Daniel F.
- Gudnason, Vilmundur
- Guénel, Pascal
- Guo, Suiqun
- Hall, Per
- Hamann, Ute
- Haring, Robin
- Hartman, Catharina A.
- Heath, Andrew C.
- Hooning, Maartje J.
- Hopper, John L.
- Hu, Frank B.
- Karasik, David
- Kiel, Douglas P.
- Knight, Julia A.
- Lai, Sandra
- Lambrechts, Diether
- Lindblom, Annika
- Mägi, Reedik
- Magnusson, Patrik K.
- Martin, Nicholas G.
- McArdle, Patrick F.
- McArdle, Wendy L.
- Melbye, Mads
- Michailidou, Kyriaki
- Milani, Lili
- Milne, Roger L.
- Nevanlinna, Heli
- Neven, Patrick
- Nohr, Ellen A.
- Oldehinkel, Albertine J.
- Palotie, Aarno
- Peacock, Munro
- Pedersen, Nancy L.
- Peterlongo, Paolo
- Peto, Julian
- Pharoah, Paul D. P.
- Postma, Dirkje S.
- Pylkäs, Katri
- Radice, Paolo
- Ring, Susan
- Rivadeneira, Fernando
- Robino, Antonietta
- Rose, Lynda M.
- Rudolph, Anja
- Salomaa, Veikko
- Sanna, Serena
- Schmidt, Marjanka K.
- Sovio, Ulla
- Stampfer, Meir J.
- Storniolo, Anna M.
- Timpson, Nicholas J.
- Tyrer, Jonathan
- Völzke, Henry
- Wang, Qin
- Willemsen, Gonneke
- Winqvist, Robert
- Wolffenbuttel, Bruce H. R.
- Wright, Margaret J.
- Boomsma, Dorret I.
- Econs, Michael J.
- Khaw, Kay-Tee
- Loos, Ruth J. F.
- McCarthy, Mark I.
- Montgomery, Grant W.
- Rice, John P.
- Streeten, Elizabeth A.
- Alizadeh, Behrooz Z.
- Bergmann, Sven
- Boerwinkle, Eric
- Boyd, Heather A.
- Crisponi, Laura
- Gasparini, Paolo
- Gieger, Christian
- Harris, Tamara B.
- Ingelsson, Erik
- Järvelin, Marjo-Riitta
- Kraft, Peter
- Lawlor, Debbie
- Metspalu, Andres
- Pennell, Craig E.
- Ridker, Paul M.
- Snieder, Harold
- Sørensen, Thorkild I. A.
- Spector, Tim D.
- Strachan, David P.
- Uitterlinden, André G.
- Wareham, Nicholas J.
- Zygmunt, Marek
- Murray, Anna
- Easton, Douglas F.
- Murabito, Joanne M.
- Ong, Ken K.
- Venue
- Nature
- Published
- 2014-07-23
- Volume
- 514
- Issue
- 7520
- Pages
- 92-97
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4185210
- OpenAlex
- W2155441570
- Cited by
- 604
- References
- 78
- Citations by year
- 2026: 13 · 2025: 35 · 2024: 55 · 2023: 42 · 2022: 45 · 2021: 41 · 2020: 49 · 2019: 81 · 2018: 69 · 2017: 58 · 2016: 59 · 2015: 50 · 2014: 5
- FWCI
- 69.48
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- other-oa
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion, other-oa)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, other-oa)
- VU Research Portal (publishedVersion, other-oa)
- University of Southern Denmark Research Portal (University of Southern Denmark) (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- St George's Online Research Archive (St George's University of London) (acceptedVersion)
- Open Research Exeter (University of Exeter) (acceptedVersion)
- LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
- IRIS (submittedVersion)
- Lirias (KU Leuven) (submittedVersion, other-oa)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Leiden Repository (Leiden University) (submittedVersion)
- ArTS Archivio della ricerca di Trieste (University of Trieste https://www.units.it/) (submittedVersion)
- Minerva Access (University of Melbourne) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Site cant be reached (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- IUScholarWorks (Indiana University) (submittedVersion)
- Purdue University Indianapolis (Indiana University) (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion, other-oa)
- Spiral (Imperial College London) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Brigham and Women's Hospital
- University of Minnesota
- School of Medicine, Boston University
- Helsingin Yliopisto
- Helsingin ja Uudenmaan Sairaanhoitopiiri
- Deutsches Krebsforschungszentrum
- Wellcome Trust (098381, 102215)
- QIMR Berghofer Medical Research Institute
- Cancer Research UK (10119, 16561, 16565, 10118, 16563, 11022, 10124)
- National Institute for Health and Care Research (NF-SI-0512-10114)
- Universiteit Leiden
- Rijksuniversiteit Groningen
- Eberhard Karls Universität Tübingen
- Gentofte Hospital
- Herlev Hospital
- Novo Nordisk
- Leids Universitair Medisch Centrum
- Oulun Yliopisto
- Uppsala Universitet
- Science for Life Laboratory
- Faculty of Health and Medical Sciences, University of Western Australia
- Novo Nordisk Foundation Center for Basic Metabolic Research
- Deutschen Konsortium für Translationale Krebsforschung
- Terveyden ja hyvinvoinnin laitos
- National Institutes of Health (UL1TR001108, 20892, MD 20892)
- University of North Carolina at Chapel Hill
- School of Medicine, Indiana University
- Geriatric Research Education and Clinical Center
- Medical Research Council (MR/J012165/1, MC_UU_12015/2, MC_PC_15018, MC_UU_12015/1)
- Det Sundhedsvidenskabelige Fakultet, Københavns Universitet
- Erasmus Universitair Medisch Centrum Rotterdam
- Biocenter, University of Oulu
- National Institute on Aging (U01AG049505, R01AG041517)
- National Cancer Institute (MD 20892, 20892, P50CA116201)
- National Institute of Neurological Disorders and Stroke (R01NS017950)
- NIH Clinical Center
- National Center for Advancing Translational Sciences
- Division of Cancer Epidemiology and Genetics, National Cancer Institute
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Keywords
- age at menarche, puberty timing, parent-of-origin effects, genomic imprinting, nuclear receptors, retinoic acid signaling, body mass index, KCNK9, genetic architecture, European women
- MeSH terms
- Adolescent, Age Factors, Alleles, Breast Neoplasms, Calcium-Binding Proteins, Cardiovascular Diseases, Child, Diabetes Mellitus, Type 2, Europe, Female, Humans, Hypothalamo-Hypophyseal System, Male, Membrane Proteins, Menarche, Obesity, Ovary, Parents, Proteins, Ribonucleoproteins, Body Mass Index, Receptors, GABA-B, Receptors, Retinoic Acid, Genomic Imprinting, Polymorphism, Single Nucleotide, Potassium Channels, Tandem Pore Domain, Intercellular Signaling Peptides and Proteins, Quantitative Trait Loci, Ubiquitin-Protein Ligases, Intracellular Signaling Peptides and Proteins, Genome-Wide Association Study, Genetic Loci, Intrinsically Disordered Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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