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. 2013 Jan;45(1):76-82.
doi: 10.1038/ng.2477. Epub 2012 Dec 2.

New loci associated with birth weight identify genetic links between intrauterine growth and adult height and metabolism

Momoko Horikoshi  1 , Hanieh Yaghootkar, Dennis O Mook-Kanamori, Ulla Sovio, H Rob Taal, Branwen J Hennig, Jonathan P Bradfield, Beate St Pourcain, David M Evans, Pimphen Charoen, Marika Kaakinen, Diana L Cousminer, Terho Lehtimäki, Eskil Kreiner-Møller, Nicole M Warrington, Mariona Bustamante, Bjarke Feenstra, Diane J Berry, Elisabeth Thiering, Thiemo Pfab, Sheila J Barton, Beverley M Shields, Marjan Kerkhof, Elisabeth M van Leeuwen, Anthony J Fulford, Zoltán Kutalik, Jing Hua Zhao, Marcel den Hoed, Anubha Mahajan, Virpi Lindi, Liang-Kee Goh, Jouke-Jan Hottenga, Ying Wu, Olli T Raitakari, Marie N Harder, Aline Meirhaeghe, Ioanna Ntalla, Rany M Salem, Karen A Jameson, Kaixin Zhou, Dorota M Monies, Vasiliki Lagou, Mirna Kirin, Jani Heikkinen, Linda S Adair, Fowzan S Alkuraya, Ali Al-Odaib, Philippe Amouyel, Ehm Astrid Andersson, Amanda J Bennett, Alexandra I F Blakemore, Jessica L Buxton, Jean Dallongeville, Shikta Das, Eco J C de Geus, Xavier Estivill, Claudia Flexeder, Philippe Froguel, Frank Geller, Keith M Godfrey, Frédéric Gottrand, Christopher J Groves, Torben Hansen, Joel N Hirschhorn, Albert Hofman, Mads V Hollegaard, David M Hougaard, Elina Hyppönen, Hazel M Inskip, Aaron Isaacs, Torben Jørgensen, Christina Kanaka-Gantenbein, John P Kemp, Wieland Kiess, Tuomas O Kilpeläinen, Norman Klopp, Bridget A Knight, Christopher W Kuzawa, George McMahon, John P Newnham, Harri Niinikoski, Ben A Oostra, Louise Pedersen, Dirkje S Postma, Susan M Ring, Fernando Rivadeneira, Neil R Robertson, Sylvain Sebert, Olli Simell, Torsten Slowinski, Carla M T Tiesler, Anke Tönjes, Allan Vaag, Jorma S Viikari, Jacqueline M Vink, Nadja Hawwa Vissing, Nicholas J Wareham, Gonneke Willemsen, Daniel R Witte, Haitao Zhang, Jianhua Zhao; Meta-Analyses of Glucose- and Insulin-related traits Consortium (MAGIC); James F Wilson, Michael Stumvoll, Andrew M Prentice, Brian F Meyer, Ewan R Pearson, Colin A G Boreham, Cyrus Cooper, Matthew W Gillman, George V Dedoussis, Luis A Moreno, Oluf Pedersen, Maiju Saarinen, Karen L Mohlke, Dorret I Boomsma, Seang-Mei Saw, Timo A Lakka, Antje Körner, Ruth J F Loos, Ken K Ong, Peter Vollenweider, Cornelia M van Duijn, Gerard H Koppelman, Andrew T Hattersley, John W Holloway, Berthold Hocher, Joachim Heinrich, Chris Power, Mads Melbye, Mònica Guxens, Craig E Pennell, Klaus Bønnelykke, Hans Bisgaard, Johan G Eriksson, Elisabeth Widén, Hakon Hakonarson, André G Uitterlinden, Anneli Pouta, Debbie A Lawlor, George Davey Smith, Timothy M Frayling, Mark I McCarthy, Struan F A Grant, Vincent W V Jaddoe, Marjo-Riitta Jarvelin, Nicholas J Timpson, Inga Prokopenko, Rachel M Freathy; Early Growth Genetics (EGG) Consortium
Affiliations

New loci associated with birth weight identify genetic links between intrauterine growth and adult height and metabolism

Momoko Horikoshi et al. Nat Genet. 2013 Jan.

Abstract

Birth weight within the normal range is associated with a variety of adult-onset diseases, but the mechanisms behind these associations are poorly understood. Previous genome-wide association studies of birth weight identified a variant in the ADCY5 gene associated both with birth weight and type 2 diabetes and a second variant, near CCNL1, with no obvious link to adult traits. In an expanded genome-wide association meta-analysis and follow-up study of birth weight (of up to 69,308 individuals of European descent from 43 studies), we have now extended the number of loci associated at genome-wide significance to 7, accounting for a similar proportion of variance as maternal smoking. Five of the loci are known to be associated with other phenotypes: ADCY5 and CDKAL1 with type 2 diabetes, ADRB1 with adult blood pressure and HMGA2 and LCORL with adult height. Our findings highlight genetic links between fetal growth and postnatal growth and metabolism.

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Figures

Figure 1
Figure 1
Regional plots of seven loci associated with birth weight at P<5×10−8. For each of the CCNL1 (a), ADCY5 (b), HMGA2 (c), CDKAL1 (d), 5q11.2 (e), LCORL (f), and ADRB1 (g) regions, SNPs are plotted with their meta-analysis P values (as –log10 values) as a function of genomic position (NCBI Build 36). In each panel, the European discovery stage SNP taken forward for follow-up is represented by a purple circle (with global [discovery + follow-up] meta-analysis P value), with its discovery P value denoted by a purple diamond. Estimated recombination rates (taken from HapMap) are plotted to reflect the local LD structure around the associated SNPs and their correlated proxies (according to a blue to red scale from r2 = 0 to 1, based on pairwise r2 values from HapMap CEU). Gene annotations were taken from the University of California Santa Cruz genome browser.
Figure 1
Figure 1
Regional plots of seven loci associated with birth weight at P<5×10−8. For each of the CCNL1 (a), ADCY5 (b), HMGA2 (c), CDKAL1 (d), 5q11.2 (e), LCORL (f), and ADRB1 (g) regions, SNPs are plotted with their meta-analysis P values (as –log10 values) as a function of genomic position (NCBI Build 36). In each panel, the European discovery stage SNP taken forward for follow-up is represented by a purple circle (with global [discovery + follow-up] meta-analysis P value), with its discovery P value denoted by a purple diamond. Estimated recombination rates (taken from HapMap) are plotted to reflect the local LD structure around the associated SNPs and their correlated proxies (according to a blue to red scale from r2 = 0 to 1, based on pairwise r2 values from HapMap CEU). Gene annotations were taken from the University of California Santa Cruz genome browser.
Figure 1
Figure 1
Regional plots of seven loci associated with birth weight at P<5×10−8. For each of the CCNL1 (a), ADCY5 (b), HMGA2 (c), CDKAL1 (d), 5q11.2 (e), LCORL (f), and ADRB1 (g) regions, SNPs are plotted with their meta-analysis P values (as –log10 values) as a function of genomic position (NCBI Build 36). In each panel, the European discovery stage SNP taken forward for follow-up is represented by a purple circle (with global [discovery + follow-up] meta-analysis P value), with its discovery P value denoted by a purple diamond. Estimated recombination rates (taken from HapMap) are plotted to reflect the local LD structure around the associated SNPs and their correlated proxies (according to a blue to red scale from r2 = 0 to 1, based on pairwise r2 values from HapMap CEU). Gene annotations were taken from the University of California Santa Cruz genome browser.
Figure 1
Figure 1
Regional plots of seven loci associated with birth weight at P<5×10−8. For each of the CCNL1 (a), ADCY5 (b), HMGA2 (c), CDKAL1 (d), 5q11.2 (e), LCORL (f), and ADRB1 (g) regions, SNPs are plotted with their meta-analysis P values (as –log10 values) as a function of genomic position (NCBI Build 36). In each panel, the European discovery stage SNP taken forward for follow-up is represented by a purple circle (with global [discovery + follow-up] meta-analysis P value), with its discovery P value denoted by a purple diamond. Estimated recombination rates (taken from HapMap) are plotted to reflect the local LD structure around the associated SNPs and their correlated proxies (according to a blue to red scale from r2 = 0 to 1, based on pairwise r2 values from HapMap CEU). Gene annotations were taken from the University of California Santa Cruz genome browser.
Figure 1
Figure 1
Regional plots of seven loci associated with birth weight at P<5×10−8. For each of the CCNL1 (a), ADCY5 (b), HMGA2 (c), CDKAL1 (d), 5q11.2 (e), LCORL (f), and ADRB1 (g) regions, SNPs are plotted with their meta-analysis P values (as –log10 values) as a function of genomic position (NCBI Build 36). In each panel, the European discovery stage SNP taken forward for follow-up is represented by a purple circle (with global [discovery + follow-up] meta-analysis P value), with its discovery P value denoted by a purple diamond. Estimated recombination rates (taken from HapMap) are plotted to reflect the local LD structure around the associated SNPs and their correlated proxies (according to a blue to red scale from r2 = 0 to 1, based on pairwise r2 values from HapMap CEU). Gene annotations were taken from the University of California Santa Cruz genome browser.
Figure 1
Figure 1
Regional plots of seven loci associated with birth weight at P<5×10−8. For each of the CCNL1 (a), ADCY5 (b), HMGA2 (c), CDKAL1 (d), 5q11.2 (e), LCORL (f), and ADRB1 (g) regions, SNPs are plotted with their meta-analysis P values (as –log10 values) as a function of genomic position (NCBI Build 36). In each panel, the European discovery stage SNP taken forward for follow-up is represented by a purple circle (with global [discovery + follow-up] meta-analysis P value), with its discovery P value denoted by a purple diamond. Estimated recombination rates (taken from HapMap) are plotted to reflect the local LD structure around the associated SNPs and their correlated proxies (according to a blue to red scale from r2 = 0 to 1, based on pairwise r2 values from HapMap CEU). Gene annotations were taken from the University of California Santa Cruz genome browser.
Figure 1
Figure 1
Regional plots of seven loci associated with birth weight at P<5×10−8. For each of the CCNL1 (a), ADCY5 (b), HMGA2 (c), CDKAL1 (d), 5q11.2 (e), LCORL (f), and ADRB1 (g) regions, SNPs are plotted with their meta-analysis P values (as –log10 values) as a function of genomic position (NCBI Build 36). In each panel, the European discovery stage SNP taken forward for follow-up is represented by a purple circle (with global [discovery + follow-up] meta-analysis P value), with its discovery P value denoted by a purple diamond. Estimated recombination rates (taken from HapMap) are plotted to reflect the local LD structure around the associated SNPs and their correlated proxies (according to a blue to red scale from r2 = 0 to 1, based on pairwise r2 values from HapMap CEU). Gene annotations were taken from the University of California Santa Cruz genome browser.
Figure 2
Figure 2
Associations between birth weight and known type 2 diabetes (T2D; a and b), systolic blood pressure (SBP, c and d) or height (e and f) loci from the discovery meta-analysis of N=26,836 individuals. Plots a, c and e are quantile-quantile plots: the black triangles (associated with lower birth weight) and circles (associated with higher birth weight) represent observed P-values after removing the loci that achieved P < 5×10−8 in the overall meta-analysis, and the black line represents expected P-values under the null. The grey area defines the approximate 95% confidence interval around the expected line. Plots b, d and f show, respectively, the T2D, SBP or height effect size (left-hand y-axis), taken from published meta-analyses,,,, against the birth weight effect size (x-axis), with a superimposed frequency histogram showing the number of SNPs in each category of birth weight effect size (right-hand y-axis). The odds ratios for type 2 diabetes are all obtained from the published DIAGRAM+ Consortium meta-analysis, the largest available reference sample of European descent, and while they do not necessarily reach genome-wide significance in that sample, all loci have shown associations with type 2 diabetes at P < 5×10−8 (see Online Methods for details of published studies). Effect sizes are aligned to the T2D risk allele or the SBP- or height-increasing allele. Colours indicate birth weight association P-values: P<5e-08 (red); P>=5e-08 and P<0.001 (orange); P>=0.001 and P<0.01 (yellow); P>0.01 (white). The triangles in plot f are SNPs known to be associated with age at menarche. There were more associations between height loci and higher birth weight than expected under the null, and a slight excess of associations between T2D or SBP loci and lower birth weight (binomial sign test P = 0.02, 0.09 and 3×10−10 for b, d and f, respectively).
Figure 2
Figure 2
Associations between birth weight and known type 2 diabetes (T2D; a and b), systolic blood pressure (SBP, c and d) or height (e and f) loci from the discovery meta-analysis of N=26,836 individuals. Plots a, c and e are quantile-quantile plots: the black triangles (associated with lower birth weight) and circles (associated with higher birth weight) represent observed P-values after removing the loci that achieved P < 5×10−8 in the overall meta-analysis, and the black line represents expected P-values under the null. The grey area defines the approximate 95% confidence interval around the expected line. Plots b, d and f show, respectively, the T2D, SBP or height effect size (left-hand y-axis), taken from published meta-analyses,,,, against the birth weight effect size (x-axis), with a superimposed frequency histogram showing the number of SNPs in each category of birth weight effect size (right-hand y-axis). The odds ratios for type 2 diabetes are all obtained from the published DIAGRAM+ Consortium meta-analysis, the largest available reference sample of European descent, and while they do not necessarily reach genome-wide significance in that sample, all loci have shown associations with type 2 diabetes at P < 5×10−8 (see Online Methods for details of published studies). Effect sizes are aligned to the T2D risk allele or the SBP- or height-increasing allele. Colours indicate birth weight association P-values: P<5e-08 (red); P>=5e-08 and P<0.001 (orange); P>=0.001 and P<0.01 (yellow); P>0.01 (white). The triangles in plot f are SNPs known to be associated with age at menarche. There were more associations between height loci and higher birth weight than expected under the null, and a slight excess of associations between T2D or SBP loci and lower birth weight (binomial sign test P = 0.02, 0.09 and 3×10−10 for b, d and f, respectively).
Figure 2
Figure 2
Associations between birth weight and known type 2 diabetes (T2D; a and b), systolic blood pressure (SBP, c and d) or height (e and f) loci from the discovery meta-analysis of N=26,836 individuals. Plots a, c and e are quantile-quantile plots: the black triangles (associated with lower birth weight) and circles (associated with higher birth weight) represent observed P-values after removing the loci that achieved P < 5×10−8 in the overall meta-analysis, and the black line represents expected P-values under the null. The grey area defines the approximate 95% confidence interval around the expected line. Plots b, d and f show, respectively, the T2D, SBP or height effect size (left-hand y-axis), taken from published meta-analyses,,,, against the birth weight effect size (x-axis), with a superimposed frequency histogram showing the number of SNPs in each category of birth weight effect size (right-hand y-axis). The odds ratios for type 2 diabetes are all obtained from the published DIAGRAM+ Consortium meta-analysis, the largest available reference sample of European descent, and while they do not necessarily reach genome-wide significance in that sample, all loci have shown associations with type 2 diabetes at P < 5×10−8 (see Online Methods for details of published studies). Effect sizes are aligned to the T2D risk allele or the SBP- or height-increasing allele. Colours indicate birth weight association P-values: P<5e-08 (red); P>=5e-08 and P<0.001 (orange); P>=0.001 and P<0.01 (yellow); P>0.01 (white). The triangles in plot f are SNPs known to be associated with age at menarche. There were more associations between height loci and higher birth weight than expected under the null, and a slight excess of associations between T2D or SBP loci and lower birth weight (binomial sign test P = 0.02, 0.09 and 3×10−10 for b, d and f, respectively).
Figure 2
Figure 2
Associations between birth weight and known type 2 diabetes (T2D; a and b), systolic blood pressure (SBP, c and d) or height (e and f) loci from the discovery meta-analysis of N=26,836 individuals. Plots a, c and e are quantile-quantile plots: the black triangles (associated with lower birth weight) and circles (associated with higher birth weight) represent observed P-values after removing the loci that achieved P < 5×10−8 in the overall meta-analysis, and the black line represents expected P-values under the null. The grey area defines the approximate 95% confidence interval around the expected line. Plots b, d and f show, respectively, the T2D, SBP or height effect size (left-hand y-axis), taken from published meta-analyses,,,, against the birth weight effect size (x-axis), with a superimposed frequency histogram showing the number of SNPs in each category of birth weight effect size (right-hand y-axis). The odds ratios for type 2 diabetes are all obtained from the published DIAGRAM+ Consortium meta-analysis, the largest available reference sample of European descent, and while they do not necessarily reach genome-wide significance in that sample, all loci have shown associations with type 2 diabetes at P < 5×10−8 (see Online Methods for details of published studies). Effect sizes are aligned to the T2D risk allele or the SBP- or height-increasing allele. Colours indicate birth weight association P-values: P<5e-08 (red); P>=5e-08 and P<0.001 (orange); P>=0.001 and P<0.01 (yellow); P>0.01 (white). The triangles in plot f are SNPs known to be associated with age at menarche. There were more associations between height loci and higher birth weight than expected under the null, and a slight excess of associations between T2D or SBP loci and lower birth weight (binomial sign test P = 0.02, 0.09 and 3×10−10 for b, d and f, respectively).
Figure 2
Figure 2
Associations between birth weight and known type 2 diabetes (T2D; a and b), systolic blood pressure (SBP, c and d) or height (e and f) loci from the discovery meta-analysis of N=26,836 individuals. Plots a, c and e are quantile-quantile plots: the black triangles (associated with lower birth weight) and circles (associated with higher birth weight) represent observed P-values after removing the loci that achieved P < 5×10−8 in the overall meta-analysis, and the black line represents expected P-values under the null. The grey area defines the approximate 95% confidence interval around the expected line. Plots b, d and f show, respectively, the T2D, SBP or height effect size (left-hand y-axis), taken from published meta-analyses,,,, against the birth weight effect size (x-axis), with a superimposed frequency histogram showing the number of SNPs in each category of birth weight effect size (right-hand y-axis). The odds ratios for type 2 diabetes are all obtained from the published DIAGRAM+ Consortium meta-analysis, the largest available reference sample of European descent, and while they do not necessarily reach genome-wide significance in that sample, all loci have shown associations with type 2 diabetes at P < 5×10−8 (see Online Methods for details of published studies). Effect sizes are aligned to the T2D risk allele or the SBP- or height-increasing allele. Colours indicate birth weight association P-values: P<5e-08 (red); P>=5e-08 and P<0.001 (orange); P>=0.001 and P<0.01 (yellow); P>0.01 (white). The triangles in plot f are SNPs known to be associated with age at menarche. There were more associations between height loci and higher birth weight than expected under the null, and a slight excess of associations between T2D or SBP loci and lower birth weight (binomial sign test P = 0.02, 0.09 and 3×10−10 for b, d and f, respectively).
Figure 2
Figure 2
Associations between birth weight and known type 2 diabetes (T2D; a and b), systolic blood pressure (SBP, c and d) or height (e and f) loci from the discovery meta-analysis of N=26,836 individuals. Plots a, c and e are quantile-quantile plots: the black triangles (associated with lower birth weight) and circles (associated with higher birth weight) represent observed P-values after removing the loci that achieved P < 5×10−8 in the overall meta-analysis, and the black line represents expected P-values under the null. The grey area defines the approximate 95% confidence interval around the expected line. Plots b, d and f show, respectively, the T2D, SBP or height effect size (left-hand y-axis), taken from published meta-analyses,,,, against the birth weight effect size (x-axis), with a superimposed frequency histogram showing the number of SNPs in each category of birth weight effect size (right-hand y-axis). The odds ratios for type 2 diabetes are all obtained from the published DIAGRAM+ Consortium meta-analysis, the largest available reference sample of European descent, and while they do not necessarily reach genome-wide significance in that sample, all loci have shown associations with type 2 diabetes at P < 5×10−8 (see Online Methods for details of published studies). Effect sizes are aligned to the T2D risk allele or the SBP- or height-increasing allele. Colours indicate birth weight association P-values: P<5e-08 (red); P>=5e-08 and P<0.001 (orange); P>=0.001 and P<0.01 (yellow); P>0.01 (white). The triangles in plot f are SNPs known to be associated with age at menarche. There were more associations between height loci and higher birth weight than expected under the null, and a slight excess of associations between T2D or SBP loci and lower birth weight (binomial sign test P = 0.02, 0.09 and 3×10−10 for b, d and f, respectively).
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