Genome-wide association and longitudinal analyses reveal genetic loci linking pubertal height growth, pubertal timing and childhood adiposity
Open accessAbstract
The pubertal height growth spurt is a distinctive feature of childhood growth reflecting both the central onset of puberty and local growth factors. Although little is known about the underlying genetics, growth variability during puberty correlates with adult risks for hormone-dependent cancer and adverse cardiometabolic health. The only gene so far associated with pubertal height growth, LIN28B, pleiotropically influences childhood growth, puberty and cancer progression, pointing to shared underlying mechanisms. To discover genetic loci influencing pubertal height and growth and to place them in context of overall growth and maturation, we performed genome-wide association meta-analyses in 18 737 European samples utilizing longitudinally collected height measurements. We found significant associations (P < 1.67 × 10(-8)) at 10 loci, including LIN28B. Five loci associated with pubertal timing, all impacting multiple aspects of growth. In particular, a novel variant correlated with expression of MAPK3, and associated both with increased prepubertal growth and earlier menarche. Another variant near ADCY3-POMC associated with increased body mass index, reduced pubertal growth and earlier puberty. Whereas epidemiological correlations suggest that early puberty marks a pathway from rapid prepubertal growth to reduced final height and adult obesity, our study shows that individual loci associating with pubertal growth have variable longitudinal growth patterns that may differ from epidemiological observations. Overall, this study uncovers part of the complex genetic architecture linking pubertal height growth, the timing of puberty and childhood obesity and provides new information to pinpoint processes linking these traits.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A female-specific SNP in LIN28B is associated with late pubertal growth.
“Another interesting association of the study by Cousminer et al. is the identification of a female-specific SNP in LIN28B associated with late pubertal growth (23).”
From The Hippo signal transduction network for exercise physiologists (2016) · cites this paper as [23]
The Results (p. 4) identify rs7759938 near LIN28B as a variant associated with pubertal growth. The paper defines late pubertal growth separately in Phenotypes and study subjects (p. 11), but the retrieved passages do not establish that this LIN28B association is female-specific or specifically concerns late pubertal growth. (LLM, conf=0.83)
Experimental — accuracy not yet measuredSNPs in genes encoding LATS2, TEAD1, YAP1, VGLL2, VGLL3, and VGLL4 are associated with body height.
“Indeed, SNPs associated with genes encoding for LATS2, TEAD1, YAP1, VGLL2, VGLL3, and VGLL4 are associated with body height (23, 57, 78, 152).”
From The Hippo signal transduction network for exercise physiologists (2016) · cites this paper as [23]
The Discussion (p. 10) links a variant near VGLL3 to taller prepubertal stature, supporting the height association for that locus. The passages from our copy do not establish height associations for LATS2, TEAD1, YAP1, VGLL2, or VGLL4, so they do not support the full six-gene claim. (LLM, conf=0.88)
Experimental — accuracy not yet measuredSNPs in YAP1 (rs11225148) and VGLL3 (rs7628864) were individually associated with shorter stature during pubertal growth in a longitudinal meta-analysis of 18,737 European individuals.
“Also, SNPs in YAP1 (rs11225148) and in VGLL3 (rs7628864) were individually associated with a shorter stature during pubertal growth in a longitudinal metaanalysis involving 18,737 European individuals (23).”
From The Hippo signal transduction network for exercise physiologists (2016) · cites this paper as [23]
The paper states that its genome-wide meta-analyses used 18,737 European samples (p. 3), and its longitudinal results identify rs7628864 in VGLL3 (p. 7). The Discussion (p. 10) describes VGLL3 as linked to taller prepubertal stature and reduced overall pubertal height growth, rather than simply shorter stature throughout puberty. Searches for rs11225148 and YAP1 found no corresponding association in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe SNP in VGLL3 was only significantly associated with the trait in females.
“Interestingly, the SNP in VGLL3 was only significantly associated with the trait in females.”
From The Hippo signal transduction network for exercise physiologists (2016) · cites this paper as [23]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
PLINK: a tool set for whole-genome association and population-based linkage analyses.
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., et al. (2007) · The American Journal of Human Genetics · doi:10.1086/519795 · Cited by 34,089 · see citing works
Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls
The Wellcome Trust Case Control Consortium, Management Committee, Burton, P. R., Clayton, D. G., Cardon, L. R., Craddock, N., Deloukas, P., Duncanson, A., Kwiatkowski, D. P., McCarthy, M. I., et al. (2007) · Nature · doi:10.1038/nature05911 · Cited by 9,442 · see citing works
Self-citationGenetics of Food Intake Self-Regulation in Childhood: Literature Review and Research Opportunities
Faith, M. S., Carnell, S., & Kral, T. V. E. (2013) · Human Heredity · doi:10.1159/000353879 · Cited by 7,628 · see citing works
Boyd, A., Golding, J., Macleod, J., Lawlor, D. A., Fraser, A., Henderson, J., Molloy, L., Ness, A., Ring, S., & Davey Smith, G. (2013) · International Journal of Epidemiology · doi:10.1093/ije/dys064 · Cited by 2,996 · see citing works
Self-citationAssociation analyses of 249,796 individuals reveal 18 new loci associated with body mass index
MAGIC, Speliotes, E. K., on behalf of Procardis Consortium, Willer, C. J., Berndt, S. I., Monda, K. L., Thorleifsson, G., Jackson, A. U., Allen, H. L., Lindgren, C. M., et al. (2010) · Nature Genetics · doi:10.1038/ng.686 · Cited by 2,912 · see citing works
Self-citationThe Wellcome Trust Case Control Consortium, U.K.
Mossman, K. (2008) · Scientific American · doi:10.1038/scientificamerican0108-42a · Cited by 2,714 · see citing works
Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis
The International Multiple Sclerosis Genetics Consortium & The Wellcome Trust Case Control Consortium 2 (2011) · Nature · doi:10.1038/nature10251 · Cited by 2,697 · see citing works
A new multipoint method for genome-wide association studies by imputation of genotypes
Marchini, J., Howie, B., Myers, S., McVean, G., & Donnelly, P. (2007) · Nature Genetics · doi:10.1038/ng2088 · Cited by 2,609 · see citing works
Hundreds of variants clustered in genomic loci and biological pathways affect human height
Lango Allen, H., Estrada, K., Lettre, G., Berndt, S. I., Weedon, M. N., Rivadeneira, F., Willer, C. J., Jackson, A. U., Vedantam, S., Raychaudhuri, S., et al. (2010) · Nature · doi:10.1038/nature09410 · Cited by 1,945 · see citing works
Self-citationMaCH: using sequence and genotype data to estimate haplotypes and unobserved genotypes
Li, Y., Willer, C. J., Ding, J., Scheet, P., & Abecasis, G. R. (2010) · Genetic Epidemiology · doi:10.1002/gepi.20533 · Cited by 1,843 · see citing works
GenABEL: an R library for genome-wide association analysis
Aulchenko, Y. S., Ripke, S., Isaacs, A., & van Duijn, C. M. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm108 · Cited by 1,836 · see citing works
Wang, K., Li, M., Hadley, D., Liu, R., Glessner, J., Grant, S. F. A., Hakonarson, H., & Bucan, M. (2007) · Genome Research · doi:10.1101/gr.6861907 · Cited by 1,792 · see citing works
Self-citationThe Type 1 Diabetes Genetics Consortium, Barrett, J. C., Clayton, D. G., Concannon, P., Akolkar, B., Cooper, J. D., Erlich, H. A., Julier, C., Morahan, G., Nerup, J., et al. (2009) · Nature Genetics · doi:10.1038/ng.381 · Cited by 1,746 · see citing works
Self-citationg:Profiler—a web-based toolset for functional profiling of gene lists from large-scale experiments
Reimand, J., Kull, M., Peterson, H., Hansen, J., & Vilo, J. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm226 · Cited by 1,525 · see citing works
Shiang, R., Thompson, L., Zhu, Y.-Z., Church, D., Fielder, T., Bocian, M., Winokur, S., & Wasmuth, J. (1994) · Cell · doi:10.1016/0092-8674(94)90302-6 · Cited by 1,291 · see citing works
Continuing Positive Secular Growth Change in the Netherlands 1955–1997
Fredriks, A. M., van Buuren, S., Burgmeijer, R. J. F., Meulmeester, J. F., Beuker, R. J., Brugman, E., Roede, M. J., Verloove-Vanhorick, S. P., & Wit, J.-M. (2000) · Pediatric Research · doi:10.1203/00006450-200003000-00006 · Cited by 1,138 · see citing works
The Generation R Study: design and cohort update 2010
Jaddoe, V. W. V., van Duijn, C. M., van der Heijden, A. J., Mackenbach, J. P., Moll, H. A., Steegers, E. A. P., Tiemeier, H., Uitterlinden, A. G., Verhulst, F. C., & Hofman, A. (2010) · European Journal of Epidemiology · doi:10.1007/s10654-010-9516-7 · Cited by 1,027 · see citing works
Self-citationChildhood Asthma after Bacterial Colonization of the Airway in Neonates
Bisgaard, H. F., Hermansen, M. N., Buchvald, F. F., Loland, L., Halkjær, L. B., Bønnelykke, K., Brasholt, M., Heltberg, A., Vissing, N. H., Thorsen, S. V., et al. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa052632 · Cited by 1,005 · see citing works
Self-citationEarly growth and coronary heart disease in later life: longitudinal study
Eriksson, J. G., Forsén, T., Tuomilehto, J., Osmond, C., & Barker, D. J. P. (2001) · BMJ · doi:10.1136/bmj.322.7292.949 · Cited by 1,004 · see citing works
Self-citationCohort profile: 1958 British birth cohort (National Child Development Study)
Power, C., & Elliott, J. (2005) · International Journal of Epidemiology · doi:10.1093/ije/dyi183 · Cited by 978 · see citing works
Self-citationMutations in the gene encoding fibroblast growth factor receptor-3 in achondroplasia
Rousseau, F., Bonaventure, J., Legeai-Mallet, L., Pelet, A., Rozet, J., Maroteaux, P., Merrer, M. L., & Munnich, A. (1994) · Nature · doi:10.1038/371252a0 · Cited by 920 · see citing works
Cohort Profile: The Cardiovascular Risk in Young Finns Study
Raitakari, O. T., Juonala, M., Rönnemaa, T., Keltikangas‐Järvinen, L., Räsänen, L., Pietikainen, M., Hutri‐Kähönen, N., Taittonen, L. M., Jokinen, E. V., Marniemi, J., et al. (2008) · International Journal of Epidemiology · doi:10.1093/ije/dym225 · Cited by 754 · see citing works
Self-citationGermline mutations in HRAS proto-oncogene cause Costello syndrome
Aoki, Y., Niihori, T., Kawame, H., Kurosawa, K., Ohashi, H., Tanaka, Y., Filocamo, M., Kato, K., Suzuki, Y., Kure, S., et al. (2005) · Nature Genetics · doi:10.1038/ng1641 · Cited by 678 · see citing works
Effects of frequent ultrasound during pregnancy: a randomised controlled trial
Newnham, J. P., Evans, S. F., Michael, C. A., Stanley, F. J., & Landau, L. I. (1993) · The Lancet · doi:10.1016/0140-6736(93)91944-h · Cited by 640 · see citing works
Cohort Profile: The INMA—INfancia y Medio Ambiente—(Environment and Childhood) Project
Guxens, M., Ballester, F., Espada, M., Fernández, M. F., Grimalt, J. O., Ibarluzea, J. M., Olea, N., Rebagliato, M., Tardón, A., Torrent, M., et al. (2011) · International Journal of Epidemiology · doi:10.1093/ije/dyr054 · Cited by 637 · see citing works
Self-citationIntermittent Inhaled Corticosteroids in Infants with Episodic Wheezing
Bisgaard, H. F., Hermansen, M. N., Loland, L., Halkjær, L. B., & Buchvald, F. F. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa054692 · Cited by 555 · see citing works
Self-citationA new highly penetrant form of obesity due to deletions on chromosome 16p11.2
Walters, R. G., Jacquemont, S., Valsesia, A., de Smith, A. J., Martinet, D., Andersson, J., Falchi, M., Chen, F., Andrieux, J., Lobbens, S., et al. (2010) · Nature · doi:10.1038/nature08727 · Cited by 543 · see citing works
Self-citationA genome-wide association study identifies KIAA0350 as a type 1 diabetes gene
Hakonarson, H., Grant, S. F. A., Bradfield, J. P., Marchand, L., Kim, C. E., Glessner, J. T., Grabs, R., Casalunovo, T., Taback, S. P., Frackelton, E. C., et al. (2007) · Nature · doi:10.1038/nature06010 · Cited by 542 · see citing works
Self-citationThirty new loci for age at menarche identified by a meta-analysis of genome-wide association studies
The GIANT Consortium, Elks, C. E., Perry, J. R. B., Sulem, P., Chasman, D. I., Franceschini, N., He, C., Lunetta, K. L., Visser, J. A., Byrne, E. M., et al. (2010) · Nature Genetics · doi:10.1038/ng.714 · Cited by 504 · see citing works
Self-citationThe adolescent growth spurt of boys and girls of the Harpenden Growth Study
Tanner, J. M., Whitehouse, R. H., Marubini, E., & Resele, L. (1976) · Annals of Human Biology · doi:10.1080/03014467600001231 · Cited by 466 · see citing works
Segrè, A. V., DIAGRAM Consortium, MAGIC investigators, Groop, L., Mootha, V. K., Daly, M. J., & Altshuler, D. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001058 · Cited by 463 · see citing works
Mirror extreme BMI phenotypes associated with gene dosage at the chromosome 16p11.2 locus
Jacquemont, S., Reymond, A., Zufferey, F., Harewood, L., Walters, R. G., Kutalik, Z., Martinet, D., Shen, Y., Valsesia, A., Beckmann, N. D., et al. (2011) · Nature · doi:10.1038/nature10406 · Cited by 462 · see citing works
Self-citationBellus, G., McIntosh, I., Smith, E., Aylsworth, A., Kaitila, I., Horton, W., Greenhaw, G. A., Hecht, J., & Francomano, C. (1995) · Nature Genetics · doi:10.1038/ng0795-357 · Cited by 460 · see citing works
Laitinen, J. H., Power, C., & Järvelin, M. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/74.3.287 · Cited by 453 · see citing works
Self-citationBMI in Childhood and Its Association with Height Gain, Timing of Puberty, and Final Height
He, Q., & KARLBERG, J. P. E. (2001) · Pediatric Research · doi:10.1203/00006450-200102000-00019 · Cited by 450 · see citing works
A genome-wide association meta-analysis identifies new childhood obesity loci
Bradfield, J. P., Abou‐Sleiman, P. M., Hakonarson, H. H., Grant, S. F. A., Taal, H. R., Mook‐Kanamori, D. O., Albert Hofman, D., van der Valk, R. J. P., de Jongste, J. C., Jaddoe, V. W. V., et al. (2012) · Nature Genetics · doi:10.1038/ng.2247 · Cited by 428 · see citing works
Self-citationHill, O. W. (1968) · The British Journal of Psychiatry · doi:10.1192/bjp.114.507.175 · Cited by 405 · see citing works
Netherlands Twin Register: From Twins to Twin Families
Boomsma, D. I., de Geus, E. J. C., Vink, J. M., Stubbe, J. H., Distel, M. A., Hottenga, J., Danielle Posthuma, B., van Beijsterveldt, T. C. E. M., Hudziak, J. J., Bartels, M., et al. (2006) · Twin Research and Human Genetics · doi:10.1375/183242706779462426 · Cited by 401 · see citing works
Self-citationProbABEL package for genome-wide association analysis of imputed data
Aulchenko, Y. S., Struchalin, M. V., & van Duijn, C. M. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-134 · Cited by 396 · see citing works
Adjustment of genomic waves in signal intensities from whole-genome SNP genotyping platforms
Diskin, S. J., Li, M., Hou, C., Yang, S., Glessner, J., Hakonarson, H. H., Bućan, M., Maris, J. M., & Wang, K. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn556 · Cited by 350 · see citing works
Self-citationBrunekreef, B., Smit, J., de Jongste, J. C., Neijens, H. J., Gerritsen, J., Postma, D. S., Aalberse, R. C., Koopman, L. P., Kerkhof, M., Wijga, A. H., et al. (2002) · Pediatric Allergy and Immunology · doi:10.1034/j.1399-3038.13.s.15.1.x · Cited by 300 · see citing works
Self-citationKaprio, J. A., Pulkkinen, L., & Rose, R. J. (2002) · Twin Research · doi:10.1375/136905202320906101 · Cited by 293 · see citing works
Self-citationZutavern, A., Brockow, I., Schaaf, B., Bolte, G., Berg, A. V., Diez, U., Borte, M., Herbarth, O., Wichmann, H. ‐., Heinrich, J., et al. (2006) · PEDIATRICS · doi:10.1542/peds.2004-2521 · Cited by 290 · see citing works
Self-citationBrisbane Adolescent Twin Study: Outline of study methods and research projects
Wright, M., & Martin, N. (2004) · Australian Journal of Psychology · doi:10.1080/00049530410001734865 · Cited by 288 · see citing works
Self-citationAge at Puberty and the Emerging Obesity Epidemic
Aksglæde, L., Juul, A., Olsen, L. W., & Sørensen, T. I. A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008450 · Cited by 269 · see citing works
Self-citationVariants in ADCY5 and near CCNL1 are associated with fetal growth and birth weight
Freathy, R. M., Mook‐Kanamori, D. O., Sovio, U., Prokopenko, I., Timpson, N. J., Berry, D. J., Warrington, N. M., Widén, E., Hottenga, J., Kaakinen, M., et al. (2010) · Nature Genetics · doi:10.1038/ng.567 · Cited by 255 · see citing works
Self-citationChildhood growth and age at menarche
Cooper, C. C., Kuh, D. J., Egger, P., Wadsworth, M. E. J., & Barker, D. J. P. (1996) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1996.tb09879.x · Cited by 254 · see citing works
The Generation R Study Biobank: a resource for epidemiological studies in children and their parents
Jaddoe, V. W. V., Bakker, R., van Duijn, C. M., van der Heijden, A. J., Lindemans, J. W., Mackenbach, J. P., Moll, H. A., Steegers, E. A. P., Tiemeier, H. W., Uitterlinden, A. G., et al. (2007) · European Journal of Epidemiology · doi:10.1007/s10654-007-9209-z · Cited by 248 · see citing works
Self-citationMetabonomic, transcriptomic, and genomic variation of a population cohort
Inouye, M., Kettunen, J., Soininen, P., Silander, K., Ripatti, S., Kumpula, L. S., Hämäläinen, E., Jousilahti, P., Kangas, A. J., Männistö, S., et al. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.93 · Cited by 247 · see citing works
Self-citationBisgaard, H. F. (2004) · Annals of Allergy Asthma & Immunology · doi:10.1016/s1081-1206(10)61398-1 · Cited by 232 · see citing works
Self-citationLakshman, R., Forouhi, N. G., Luben, R., Bingham, S. A., Khaw, K., Wareham, N. J., & Ong, K. K. (2008) · Diabetologia · doi:10.1007/s00125-008-0948-5 · Cited by 203 · see citing works
GnRH Activates ERK1/2 Leading to the Induction of c-fos and LH Protein Expression in L T2 Cells
Liu, F., Austin, D. A., Mellon, P. L., Olefsky, J. M., & Webster, N. J. G. (2002) · Molecular Endocrinology · doi:10.1210/mend.16.3.0791 · Cited by 186 · see citing works
Williams, L. A., Evans, S. F., & Newnham, J. P. (1997) · BMJ · doi:10.1136/bmj.314.7098.1864 · Cited by 185 · see citing works
Sovio, U., Bennett, A. J., Millwood, I. Y., Molitor, J., O’Reilly, P. F., Timpson, N. J., Kaakinen, M., Laitinen, J. H., Haukka, J. K., Pillas, D., et al. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000409 · Cited by 153 · see citing works
Self-citationAge at menarche: secular trends and association with adult anthropometric measures
Okasha, P. M. M. (2001) · Annals of Human Biology · doi:10.1080/03014460150201896 · Cited by 150 · see citing works
Kivimèki, M., Lawlor, D. A., Smith, G. D., Elovainio, M. J., Jokela, M. M., Keltikangas‐Järvinen, L., Vahtera, J., Taittonen, L. M., Juonala, M., Viikari, J. S. A., et al. (2008) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/87.6.1876 · Cited by 149 · see citing works
Self-citationPubertal Timing and Growth Influences Cardiometabolic Risk Factors in Adult Males and Females
Widén, E., Silventoinen, K., Sovio, U., Ripatti, S., Cousminer, D. L., Hartikainen, A., Laitinen, J. H., Pouta, A. M., Kaprio, J. A., Järvelin, M., et al. (2012) · Diabetes Care · doi:10.2337/dc11-1365 · Cited by 133 · see citing works
Self-citationThe role of sex steroids in controlling pubertal growth
Perry, R., Farquharson, C., & Ahmed, S. F. (2007) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2007.02960.x · Cited by 122 · see citing works
Familial concordance for age at menarche: analyses from the Breakthrough Generations Study
Morris, D. H., Jones, M. E., Schoemaker, M. J., Ashworth, A., & Swerdlow, A. J. (2011) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2010.01183.x · Cited by 120 · see citing works
Body mass index during childhood and adult body composition in men and women aged 56–70 y
Ylihèrsilè, H., Kajantie, E., Osmond, C., Forsén, T., Barker, D. J. P., & Eriksson, J. G. (2008) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/87.6.1769 · Cited by 116 · see citing works
Self-citationTaponen, S., Martikainen, H. K., Järvelin, M., Sovio, U., Laitinen, J. H., Pouta, A. M., Hartikainen, A., McCarthy, M. I., Franks, S., Paldanius, M., et al. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031720 · Cited by 111 · see citing works
Self-citationDistinct Variants at LIN28B Influence Growth in Height from Birth to Adulthood
Widén, E., Ripatti, S., Cousminer, D. L., Surakka, I., Lappalainen, T., Järvelin, M.-R., Eriksson, J. G., Raitakari, O., Salomaa, V., Sovio, U., et al. (2010) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2010.03.010 · Cited by 88 · see citing works
Self-citationGenetic and environmental influences on pubertal timing assessed by height growth
Wehkalampi, K., Silventoinen, K., Kaprio, J. A., Dick, D. M., Rose, R. J., Pulkkinen, L., & Dunkel, L. (2008) · American Journal of Human Biology · doi:10.1002/ajhb.20748 · Cited by 87 · see citing works
Self-citationSilventoinen, K., Bartels, M., Posthuma, D., Burk, G. F. E.-V., Willemsen, G. A. H. M., van Beijsterveldt, T. C. E. M., & Boomsma, D. I. (2007) · Twin Research and Human Genetics · doi:10.1375/twin.10.2.354 · Cited by 79 · see citing works
Self-citationWood, A. R., Hernandez, D. G., Nalls, M. A., Yaghootkar, H., Gibbs, J. R., Harries, L. W., Chong, S., Moore, M., Weedon, M. N., Guralnik, J. M., et al. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr328 · Cited by 65 · see citing works
Genetic regulation of growth from birth to 18 years of age: The Swedish young male twins study
Silventoinen, K., Pietiläinen, K. H., Tynelius, P., Sørensen, T. I. A., Kaprio, J. A., & Rasmussen, F. E. (2008) · American Journal of Human Biology · doi:10.1002/ajhb.20717 · Cited by 64 · see citing works
Self-citationEstrada, K., Abuseiris, A., Grosveld, F. G., Uitterlinden, A. G., Knoch, T., & Rivadeneira, F. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp497 · Cited by 58 · see citing works
Evans, S. F., Newnham, J. P., MacDonald, W. K., & Hall, C. (1996) · Early Human Development · doi:10.1016/0378-3782(96)01728-8 · Cited by 57 · see citing works
Sharma, J. C. (1983) · Annals of Human Biology · doi:10.1080/03014468300006301 · Cited by 54 · see citing works
Critical Growth Phases for Adult Shortness
Luo, Z., & KARLBERG, J. P. E. (2000) · American Journal of Epidemiology · doi:10.1093/aje/152.2.125 · Cited by 52 · see citing works
Sebastian, A. S., Matsushita, T., Kawanami, A., et al. (2010) · Journal of Orthopaedic Research® · doi:10.1002/jor.21262 · Cited by 44 · see citing works
Rzehak, P., Scherag, A., Grallert, H., Sausenthaler, S., Koletzko, S., Bauer, C. P., Schaaf, B., Berg, A. V., Berdel, D., Borte, M., et al. (2010) · Obesity Facts · doi:10.1159/000314612 · Cited by 42 · see citing works
Self-citationGenetic Influences on Physical Activity in Young Adults
Mustelin, L., JOUTSI, J., Latvala, A., Pietiläinen, K. H., Rissanen, A., & Kaprio, J. A. (2012) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3182479747 · Cited by 29 · see citing works
Self-citationA System for Information Management in BioMedical Studies—SIMBioMS
Krestyaninova, M., Zarins, A., Vīksna, J., Kurbatova, N., Ručevskis, P., Neogi, S. G., Gostev, M., Perheentupa, T., Knuuttila, J. S., Barrett, A., et al. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp420 · Cited by 29 · see citing works
Self-citationGrowth in Height in Childhood and Risk of Coronary Heart Disease in Adult Men and Women
Silventoinen, K., Baker, J. L., & Sørensen, T. I. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030476 · Cited by 22 · see citing works
Self-citationPhenotype mining in CNV carriers from a population cohort †
Pietiläinen, O. P. H., Rehnström, K., Jakkula, E., Service, S. K., Congdon, E. L., Tilgmann, C., Hartikainen, A., Taanila, A. M., Heikura, U., Paunio, T., et al. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr162 · Cited by 18 · see citing works
Self-citationVrieze, S. I., McGue, M. K., Miller, M. B., Legrand, L. N., Schork, N. J., & Iacono, W. G. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002413 · Cited by 13 · see citing works
Cardiorespiratory Fitness of Finnish Adolescents
Tammelin, T., Remes, J., Kujala, V. M., et al. (2007) · International Journal of Sports Medicine · doi:10.1055/s-2007-964911 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Verbanck, M., Chen, C.-Y., Neale, B., & Do, R. (2018) · Nature Genetics · doi:10.1038/s41588-018-0099-7 · Cited by 8,591 · see citing works
Jelenkovic, A., Sund, R., Hur, Y.-M., Yokoyama, Y., Hjelmborg, J. V. B., Möller, S., Honda, C., Magnusson, P. K. E., Pedersen, N. L., Ooki, S., et al. (2016) · Scientific Reports · doi:10.1038/srep28496 · Cited by 202 · see citing works
Self-citationEpigenetic regulation of female puberty
Lomniczi, A., Wright, H., & Ojeda, S. R. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.08.003 · Cited by 136 · see citing works
Dissection of genetic variation and evidence for pleiotropy in male pattern baldness
Yap, C. X., Sidorenko, J., Wu, Y., Kemper, K. E., Yang, J., Wray, N. R., Robinson, M. R., & Visscher, P. M. (2018) · Nature Communications · doi:10.1038/s41467-018-07862-y · Cited by 124 · see citing works
Neuronal and astrocytic primary cilia in the mature brain
Sterpka, A., & Chen, X. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.10.002 · Cited by 80 · see citing works
Jordan, D. M., Verbanck, M., & Do, R. (2019) · Genome Biology · doi:10.1186/s13059-019-1844-7 · Cited by 73 · see citing works
A Gain-of-Function Mutation in Adenylate Cyclase 3 Protects Mice from Diet-Induced Obesity
Pitman, J. L., Wheeler, M. C., Lloyd, D. J., Walker, J. R., Glynne, R. J., & Gekakis, N. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110226 · Cited by 63 · see citing works
The Hippo signal transduction network for exercise physiologists
Gabriel, B. M., Hamilton, D. L., Tremblay, A. M., & Wackerhage, H. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01076.2015 · Cited by 48 · see citing works
Temporal ablation of the ciliary protein IFT88 alters normal brainwave patterns
Strobel, M. R., Zhou, Y., Qiu, L., Hofer, A. M., & Chen, X. (2025) · Scientific Reports · doi:10.1038/s41598-024-83432-1 · Cited by 9 · see citing works
- Authors
- Cousminer, D. L., Berry, D. J., Timpson, N. J., Ang, W., Thiering, E., Byrne, E. M., Taal, H. R., Huikari, V., Bradfield, J. P., Kerkhof, M., Groen-Blokhuis, M. M., Kreiner-Møller, E., Marinelli, M., Holst, C., Leinonen, J. T., Perry, J. R. B., Surakka, I., Pietiläinen, O., Kettunen, J., Anttila, V., Kaakinen, M., Sovio, U., Pouta, A., Das, S., Lagou, V., Power, C., Prokopenko, I., Evans, D. M., Kemp, J. P., St Pourcain, B., Ring, S., Palotie, A., Kajantie, E., Osmond, C., Lehtimäki, T., Viikari, J. S., Kähönen, M., Warrington, N. M., Lye, S. J., Palmer, L. J., Tiesler, C. M. T., Flexeder, C., Montgomery, G. W., Medland, S. E., Hofman, A., Hakonarson, H., Guxens, M., Bartels, M., Salomaa, V., The ReproGen Consortium, Murabito, J. M., Kaprio, J., Sørensen, T. I. A., Ballester, F., Bisgaard, H., Boomsma, D. I., Koppelman, G. H., Grant, S. F. A., Jaddoe, V. W. V., Martin, N. G., Heinrich, J., Pennell, C. E., Raitakari, O. T., Eriksson, J. G., Smith, G. D., Hyppönen, E., Järvelin, M.-R., McCarthy, M. I., Ripatti, S., Widén, E., & for the Early Growth Genetics (EGG) Consortium
- Affiliations
- Institute for Molecular Medicine Finland (FI)
- University College London (GB)
- Medical Research Council (GB)
- The University of Western Australia (AU)
- Helmholtz Munich (DE)
- QIMR Berghofer Medical Research Institute (AU)
- Erasmus MC (NL)
- Institute of Health Sciences,
- Centre for Applied Genomics (CA)
- Department of Epidemiology,
- Netherlands Twin Register, Department of Biological Psychology, VU University, Amsterdam, The Netherlands,
- Copenhagen Prospective Studies on Asthma in Childhood, Health Sciences, University of Copenhagen, Copenhagen University Hospital, Gentofte, Denmark,
- Center for Research in Environmental Epidemiology (ES)
- Copenhagen University Hospital (DK)
- Centre for Human Genetics (GB)
- Wellcome Sanger Institute (GB)
- Broad Institute (US)
- University of Oulu (FI)
- London School of Hygiene & Tropical Medicine (GB)
- Department of Epidemiology and Biostatistics, School of Public Health,
- University of Bristol (GB)
- School of Social and Community Medicine, University of Bristol, Bristol, UK
- University of Helsinki (FI)
- MRC Lifecourse Epidemiology Unit (GB)
- Tampere University Hospital (FI)
- Department of Medicine,
- University of Turku (FI)
- Mount Sinai Hospital (CA)
- Ontario Institute for Cancer Research (CA)
- The Generation R Study Group,
- Children's Hospital of Philadelphia (US)
- Vrije Universiteit Amsterdam (NL)
- Department of Chronic Disease Prevention,
- Boston University (US)
- Finnish Institute for Health and Welfare (FI)
- University of Copenhagen (DK)
- CIBER Epidemiologia y Salud Pública (CIBERESP), Barcelona, Catalonia, Spain,
- University Medical Center Groningen (NL)
- Oulu University Hospital (FI)
- Corresponding author
- Widén, Elisabeth
- ORCID
- Timpson, Nicholas J.
- Thiering, Elisabeth
- Byrne, Enda M.
- Taal, H. Rob
- Kerkhof, Marjan
- Leinonen, Jaakko T.
- Perry, John R.B.
- Surakka, Ida
- Pietiläinen, Olli
- Kettunen, Johannes
- Anttila, Verneri
- Kaakinen, Marika
- Sovio, Ulla
- Lagou, Vasiliki
- Power, Chris
- Prokopenko, Inga
- Evans, David M.
- Kemp, John P.
- Ring, Susan
- Palotie, Aarno
- Kajantie, Eero
- Osmond, Clive
- Lehtimäki, Terho
- Viikari, Jorma S.
- Kähönen, Mika
- Warrington, Nicole M.
- Lye, Stephen J.
- Palmer, Lyle J.
- Flexeder, Claudia
- Montgomery, Grant W.
- Medland, Sarah E.
- Hakonarson, Hakon
- Guxens, Mònica
- Bartels, Meike
- Salomaa, Veikko
- Murabito, Joanne M.
- Kaprio, Jaakko
- Bisgaard, Hans
- Boomsma, Dorret I.
- Koppelman, Gerard H.
- Grant, Struan F.A.
- Jaddoe, Vincent W.V.
- Martin, Nicholas G.
- Heinrich, Joachim
- Pennell, Craig E.
- Raitakari, Olli T.
- Eriksson, Johan G.
- Smith, George Davey
- Hyppönen, Elina
- Järvelin, Marjo-Riitta
- McCarthy, Mark I.
- Ripatti, Samuli
- Widén, Elisabeth
- Venue
- Human Molecular Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-02-27
- Volume
- 22
- Issue
- 13
- Pages
- 2735-2747
- ISSN
- 0964-6906 (ISSN-L)
- 1460-2083
- PMC
- PMC3674797
- OpenAlex
- W2130767371
- Cited by
- 209
- References
- 78
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 22 · 2023: 11 · 2022: 13 · 2021: 18 · 2020: 12 · 2019: 28 · 2018: 19 · 2017: 15 · 2016: 21 · 2015: 16 · 2014: 14 · 2013: 3
- FWCI
- 2.92
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Human Molecular Genetics (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
- ePrints Soton (University of Southampton) (acceptedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- ArTS Archivio della ricerca di Trieste (University of Trieste https://www.units.it/) (submittedVersion)
- Universitätsbibliographie, Universität Duisburg-Essen (submittedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- IRIS (submittedVersion)
- Site cant be reached (submittedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Bristol Research (University of Bristol) (submittedVersion)
- VU Research Portal (submittedVersion, other-oa)
- LSHTM Research Online (London School of Hygiene and Tropical Medicine) (submittedVersion)
- Repository of Digital Objects for Teaching Research and Culture (University of Valencia) (submittedVersion, cc-by-nc)
- SERVAL (Université de Lausanne) (submittedVersion)
- STM:n Hallinnonalan avoin julkaisuarkisto (Julkari) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Wellcome Trust (068545/Z/02), FP7/2007–2013, 076467, 092731, WT083431MA, 068545, 084762MA, 090532, 092447/Z/10/Z)
- National Institute for Health and Care Research (NF-SI-0508-10082, NF-SI-0611-10099, NF-SI-0611-10219)
- British Heart Foundation
- European Commission
- Raine Medical Research Foundation
- ZonMw (907.00303, 2100.0074, 916.10159)
- Erasmus Universiteit Rotterdam
- Generalitat de Catalunya
- Nierstichting (C08.2251)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (14192, 480-04-004)
- Ministerio de Ciencia e Innovación
- Oulun Yliopisto
- Tampereen Tuberkuloosisäätiö
- Paavo Nurmen Säätiö
- Novo Nordisk Fonden (NNF12OC1016374)
- Turun Yliopistollinen Keskussairaala (9N035, 9M048)
- National Institutes of Health (5u01hg004423-02, 6r01hl087679-03, 5rl1mh083268-05)
- Canadian Institutes of Health Research (MOP82893)
- Medical Research Council (MC_UU_12011/4, MC_PC_15018, MC_UU_12011/1)
- National Health and Medical Research Council (496739, 403981, 389927, 389891, 552498, 613608, 389938, 241944, 442915, 389875, 389892)
- National Institute on Alcohol Abuse and Alcoholism (AA-09203, AA12502, K05AA017688, R01AA008315, R01AA012502, R01AA009203, R37AA012502, AA08315)
- National Institute on Aging (R01AG041517)
- National Heart, Lung, and Blood Institute (5R01 HL087679-02, R01 HL087679)
- National Institute of Mental Health (R01MH063706, RC2MH089995, RL1-MH083268, 1RL1MH083268-01, 5R01 MH63706:02)
- National Human Genome Research Institute (U01-HG004423, U01HG006830)
- National Institute of Diabetes and Digestive and Kidney Diseases (U01DK062418)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD056465)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
- Keywords
- pubertal timing, childhood adiposity, puberty onset, LIN28B, ERK1, body mass index, menarche, prepubertal growth, adult height, genetic loci, linear growth, cardiometabolic risk
- MeSH terms
- Adolescent, Age Factors, Body Height, Child, Female, Follow-Up Studies, Humans, Genetic Linkage, Male, Menarche, Neoplasms, Phenotype, Puberty, Signal Transduction, Gene Expression, Body Mass Index, Transforming Growth Factor beta, Quantitative Trait Loci, Mitogen-Activated Protein Kinase 3, Adiposity, Genome-Wide Association Study, Young Adult
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review