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Meta-Analysis
. 2014 Nov;46(11):1173-86.
doi: 10.1038/ng.3097. Epub 2014 Oct 5.

Defining the role of common variation in the genomic and biological architecture of adult human height

Andrew R Wood  1 , Tonu Esko  2 , Jian Yang  3 , Sailaja Vedantam  4 , Tune H Pers  5 , Stefan Gustafsson  6 , Audrey Y Chu  7 , Karol Estrada  8 , Jian'an Luan  9 , Zoltán Kutalik  10 , Najaf Amin  11 , Martin L Buchkovich  12 , Damien C Croteau-Chonka  13 , Felix R Day  9 , Yanan Duan  14 , Tove Fall  15 , Rudolf Fehrmann  16 , Teresa Ferreira  17 , Anne U Jackson  18 , Juha Karjalainen  16 , Ken Sin Lo  19 , Adam E Locke  18 , Reedik Mägi  20 , Evelin Mihailov  21 , Eleonora Porcu  22 , Joshua C Randall  23 , André Scherag  24 , Anna A E Vinkhuyzen  25 , Harm-Jan Westra  16 , Thomas W Winkler  26 , Tsegaselassie Workalemahu  27 , Jing Hua Zhao  9 , Devin Absher  28 , Eva Albrecht  29 , Denise Anderson  30 , Jeffrey Baron  31 , Marian Beekman  32 , Ayse Demirkan  33 , Georg B Ehret  34 , Bjarke Feenstra  35 , Mary F Feitosa  36 , Krista Fischer  37 , Ross M Fraser  38 , Anuj Goel  39 , Jian Gong  40 , Anne E Justice  41 , Stavroula Kanoni  42 , Marcus E Kleber  43 , Kati Kristiansson  44 , Unhee Lim  45 , Vaneet Lotay  46 , Julian C Lui  31 , Massimo Mangino  47 , Irene Mateo Leach  48 , Carolina Medina-Gomez  49 , Michael A Nalls  50 , Dale R Nyholt  51 , Cameron D Palmer  4 , Dorota Pasko  1 , Sonali Pechlivanis  52 , Inga Prokopenko  53 , Janina S Ried  29 , Stephan Ripke  54 , Dmitry Shungin  55 , Alena Stancáková  56 , Rona J Strawbridge  57 , Yun Ju Sung  58 , Toshiko Tanaka  59 , Alexander Teumer  60 , Stella Trompet  61 , Sander W van der Laan  62 , Jessica van Setten  63 , Jana V Van Vliet-Ostaptchouk  64 , Zhaoming Wang  65 , Loïc Yengo  66 , Weihua Zhang  67 , Uzma Afzal  67 , Johan Arnlöv  68 , Gillian M Arscott  69 , Stefania Bandinelli  70 , Amy Barrett  71 , Claire Bellis  72 , Amanda J Bennett  71 , Christian Berne  73 , Matthias Blüher  74 , Jennifer L Bolton  38 , Yvonne Böttcher  75 , Heather A Boyd  35 , Marcel Bruinenberg  76 , Brendan M Buckley  77 , Steven Buyske  78 , Ida H Caspersen  79 , Peter S Chines  80 , Robert Clarke  81 , Simone Claudi-Boehm  82 , Matthew Cooper  30 , E Warwick Daw  36 , Pim A De Jong  83 , Joris Deelen  32 , Graciela Delgado  84 , Josh C Denny  85 , Rosalie Dhonukshe-Rutten  86 , Maria Dimitriou  87 , Alex S F Doney  88 , Marcus Dörr  89 , Niina Eklund  90 , Elodie Eury  66 , Lasse Folkersen  57 , Melissa E Garcia  91 , Frank Geller  35 , Vilmantas Giedraitis  92 , Alan S Go  93 , Harald Grallert  94 , Tanja B Grammer  84 , Jürgen Gräßler  95 , Henrik Grönberg  96 , Lisette C P G M de Groot  86 , Christopher J Groves  71 , Jeffrey Haessler  40 , Per Hall  96 , Toomas Haller  37 , Goran Hallmans  97 , Anke Hannemann  98 , Catharina A Hartman  99 , Maija Hassinen  100 , Caroline Hayward  101 , Nancy L Heard-Costa  102 , Quinta Helmer  103 , Gibran Hemani  3 , Anjali K Henders  51 , Hans L Hillege  104 , Mark A Hlatky  105 , Wolfgang Hoffmann  106 , Per Hoffmann  107 , Oddgeir Holmen  108 , Jeanine J Houwing-Duistermaat  109 , Thomas Illig  110 , Aaron Isaacs  111 , Alan L James  112 , Janina Jeff  46 , Berit Johansen  79 , Åsa Johansson  113 , Jennifer Jolley  114 , Thorhildur Juliusdottir  17 , Juhani Junttila  115 , Abel N Kho  116 , Leena Kinnunen  44 , Norman Klopp  110 , Thomas Kocher  117 , Wolfgang Kratzer  118 , Peter Lichtner  119 , Lars Lind  120 , Jaana Lindström  44 , Stéphane Lobbens  66 , Mattias Lorentzon  121 , Yingchang Lu  122 , Valeriya Lyssenko  123 , Patrik K E Magnusson  96 , Anubha Mahajan  17 , Marc Maillard  124 , Wendy L McArdle  125 , Colin A McKenzie  126 , Stela McLachlan  38 , Paul J McLaren  127 , Cristina Menni  47 , Sigrun Merger  82 , Lili Milani  37 , Alireza Moayyeri  47 , Keri L Monda  128 , Mario A Morken  80 , Gabriele Müller  129 , Martina Müller-Nurasyid  130 , Arthur W Musk  131 , Narisu Narisu  80 , Matthias Nauck  132 , Ilja M Nolte  133 , Markus M Nöthen  134 , Laticia Oozageer  135 , Stefan Pilz  136 , Nigel W Rayner  137 , Frida Renstrom  138 , Neil R Robertson  139 , Lynda M Rose  7 , Ronan Roussel  140 , Serena Sanna  22 , Hubert Scharnagl  141 , Salome Scholtens  133 , Fredrick R Schumacher  142 , Heribert Schunkert  143 , Robert A Scott  9 , Joban Sehmi  67 , Thomas Seufferlein  118 , Jianxin Shi  144 , Karri Silventoinen  145 , Johannes H Smit  146 , Albert Vernon Smith  147 , Joanna Smolonska  148 , Alice V Stanton  149 , Kathleen Stirrups  150 , David J Stott  151 , Heather M Stringham  18 , Johan Sundström  120 , Morris A Swertz  16 , Ann-Christine Syvänen  152 , Bamidele O Tayo  153 , Gudmar Thorleifsson  154 , Jonathan P Tyrer  155 , Suzanne van Dijk  156 , Natasja M van Schoor  157 , Nathalie van der Velde  158 , Diana van Heemst  159 , Floor V A van Oort  160 , Sita H Vermeulen  161 , Niek Verweij  48 , Judith M Vonk  133 , Lindsay L Waite  28 , Melanie Waldenberger  162 , Roman Wennauer  163 , Lynne R Wilkens  45 , Christina Willenborg  164 , Tom Wilsgaard  165 , Mary K Wojczynski  36 , Andrew Wong  166 , Alan F Wright  101 , Qunyuan Zhang  36 , Dominique Arveiler  167 , Stephan J L Bakker  168 , John Beilby  169 , Richard N Bergman  170 , Sven Bergmann  171 , Reiner Biffar  172 , John Blangero  72 , Dorret I Boomsma  173 , Stefan R Bornstein  95 , Pascal Bovet  174 , Paolo Brambilla  175 , Morris J Brown  176 , Harry Campbell  38 , Mark J Caulfield  177 , Aravinda Chakravarti  178 , Rory Collins  81 , Francis S Collins  80 , Dana C Crawford  179 , L Adrienne Cupples  180 , John Danesh  181 , Ulf de Faire  182 , Hester M den Ruijter  183 , Raimund Erbel  184 , Jeanette Erdmann  164 , Johan G Eriksson  185 , Martin Farrall  39 , Ele Ferrannini  186 , Jean Ferrières  187 , Ian Ford  188 , Nita G Forouhi  9 , Terrence Forrester  126 , Ron T Gansevoort  168 , Pablo V Gejman  189 , Christian Gieger  29 , Alain Golay  190 , Omri Gottesman  46 , Vilmundur Gudnason  147 , Ulf Gyllensten  113 , David W Haas  191 , Alistair S Hall  192 , Tamara B Harris  91 , Andrew T Hattersley  193 , Andrew C Heath  194 , Christian Hengstenberg  143 , Andrew A Hicks  195 , Lucia A Hindorff  196 , Aroon D Hingorani  197 , Albert Hofman  198 , G Kees Hovingh  199 , Steve E Humphries  200 , Steven C Hunt  201 , Elina Hypponen  202 , Kevin B Jacobs  203 , Marjo-Riitta Jarvelin  204 , Pekka Jousilahti  44 , Antti M Jula  44 , Jaakko Kaprio  205 , John J P Kastelein  199 , Manfred Kayser  206 , Frank Kee  207 , Sirkka M Keinanen-Kiukaanniemi  208 , Lambertus A Kiemeney  209 , Jaspal S Kooner  210 , Charles Kooperberg  40 , Seppo Koskinen  44 , Peter Kovacs  74 , Aldi T Kraja  36 , Meena Kumari  211 , Johanna Kuusisto  212 , Timo A Lakka  213 , Claudia Langenberg  214 , Loic Le Marchand  45 , Terho Lehtimäki  215 , Sara Lupoli  216 , Pamela A F Madden  194 , Satu Männistö  44 , Paolo Manunta  217 , André Marette  218 , Tara C Matise  219 , Barbara McKnight  220 , Thomas Meitinger  221 , Frans L Moll  222 , Grant W Montgomery  51 , Andrew D Morris  88 , Andrew P Morris  223 , Jeffrey C Murray  224 , Mari Nelis  37 , Claes Ohlsson  121 , Albertine J Oldehinkel  99 , Ken K Ong  225 , Willem H Ouwehand  114 , Gerard Pasterkamp  62 , Annette Peters  226 , Peter P Pramstaller  227 , Jackie F Price  38 , Lu Qi  228 , Olli T Raitakari  229 , Tuomo Rankinen  230 , D C Rao  231 , Treva K Rice  232 , Marylyn Ritchie  233 , Igor Rudan  234 , Veikko Salomaa  44 , Nilesh J Samani  235 , Jouko Saramies  236 , Mark A Sarzynski  230 , Peter E H Schwarz  237 , Sylvain Sebert  238 , Peter Sever  239 , Alan R Shuldiner  240 , Juha Sinisalo  241 , Valgerdur Steinthorsdottir  154 , Ronald P Stolk  133 , Jean-Claude Tardif  242 , Anke Tönjes  74 , Angelo Tremblay  243 , Elena Tremoli  244 , Jarmo Virtamo  44 , Marie-Claude Vohl  245 ; Electronic Medical Records and Genomics (eMEMERGEGE) Consortium; MIGen Consortium; PAGEGE Consortium; LifeLines Cohort Study; Philippe Amouyel  246 , Folkert W Asselbergs  247 , Themistocles L Assimes  105 , Murielle Bochud  174 , Bernhard O Boehm  248 , Eric Boerwinkle  249 , Erwin P Bottinger  46 , Claude Bouchard  230 , Stéphane Cauchi  66 , John C Chambers  250 , Stephen J Chanock  251 , Richard S Cooper  153 , Paul I W de Bakker  252 , George Dedoussis  87 , Luigi Ferrucci  59 , Paul W Franks  253 , Philippe Froguel  254 , Leif C Groop  255 , Christopher A Haiman  142 , Anders Hamsten  57 , M Geoffrey Hayes  116 , Jennie Hui  256 , David J Hunter  257 , Kristian Hveem  108 , J Wouter Jukema  258 , Robert C Kaplan  259 , Mika Kivimaki  211 , Diana Kuh  166 , Markku Laakso  212 , Yongmei Liu  260 , Nicholas G Martin  51 , Winfried März  261 , Mads Melbye  262 , Susanne Moebus  52 , Patricia B Munroe  177 , Inger Njølstad  165 , Ben A Oostra  263 , Colin N A Palmer  88 , Nancy L Pedersen  96 , Markus Perola  264 , Louis Pérusse  265 , Ulrike Peters  40 , Joseph E Powell  3 , Chris Power  266 , Thomas Quertermous  105 , Rainer Rauramaa  267 , Eva Reinmaa  37 , Paul M Ridker  268 , Fernando Rivadeneira  49 , Jerome I Rotter  269 , Timo E Saaristo  270 , Danish Saleheen  271 , David Schlessinger  272 , P Eline Slagboom  32 , Harold Snieder  133 , Tim D Spector  47 , Konstantin Strauch  273 , Michael Stumvoll  74 , Jaakko Tuomilehto  274 , Matti Uusitupa  275 , Pim van der Harst  276 , Henry Völzke  106 , Mark Walker  277 , Nicholas J Wareham  9 , Hugh Watkins  39 , H-Erich Wichmann  278 , James F Wilson  38 , Pieter Zanen  279 , Panos Deloukas  280 , Iris M Heid  281 , Cecilia M Lindgren  282 , Karen L Mohlke  12 , Elizabeth K Speliotes  283 , Unnur Thorsteinsdottir  284 , Inês Barroso  285 , Caroline S Fox  286 , Kari E North  287 , David P Strachan  288 , Jacques S Beckmann  289 , Sonja I Berndt  251 , Michael Boehnke  18 , Ingrid B Borecki  36 , Mark I McCarthy  290 , Andres Metspalu  21 , Kari Stefansson  284 , André G Uitterlinden  49 , Cornelia M van Duijn  291 , Lude Franke  16 , Cristen J Willer  292 , Alkes L Price  293 , Guillaume Lettre  242 , Ruth J F Loos  294 , Michael N Weedon  1 , Erik Ingelsson  295 , Jeffrey R O'Connell  296 , Goncalo R Abecasis  18 , Daniel I Chasman  268 , Michael E Goddard  297 , Peter M Visscher  3 , Joel N Hirschhorn  298 , Timothy M Frayling  1
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Meta-Analysis

Defining the role of common variation in the genomic and biological architecture of adult human height

Andrew R Wood et al. Nat Genet. 2014 Nov.

Abstract

Using genome-wide data from 253,288 individuals, we identified 697 variants at genome-wide significance that together explained one-fifth of the heritability for adult height. By testing different numbers of variants in independent studies, we show that the most strongly associated ∼2,000, ∼3,700 and ∼9,500 SNPs explained ∼21%, ∼24% and ∼29% of phenotypic variance. Furthermore, all common variants together captured 60% of heritability. The 697 variants clustered in 423 loci were enriched for genes, pathways and tissue types known to be involved in growth and together implicated genes and pathways not highlighted in earlier efforts, such as signaling by fibroblast growth factors, WNT/β-catenin and chondroitin sulfate-related genes. We identified several genes and pathways not previously connected with human skeletal growth, including mTOR, osteoglycin and binding of hyaluronic acid. Our results indicate a genetic architecture for human height that is characterized by a very large but finite number (thousands) of causal variants.

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Figures

Figure 1
Figure 1. Regional association plots for loci with multiple association signals
Panels a to d highlight examples of multiple signals after approximate conditional joint multiple-SNP analysis GCTA-COJO analysis. SNPs are shaded and shaped based on the index SNP with which they are in strongest LD (r2>0.4). Panels a–c show the majority of signals clustering in and around a single gene (ACAN, ADAMTS17, PTCH1, respectively) whereas panel d shows the multiple signals clustering through proximity.
Figure 2
Figure 2. Quantifying the variance explained by height associated SNPs at different levels of significance
The SNPs were selected from the approximate conditional and joint multiple SNPs association analysis using GCTA-COJO analysis with the target cohort being excluded from the meta-analysis. a, b, c, Partitioning the variance in the SNP-derived genetic predictor using a within-family analysis. The SNP-based predictor was adjusted by the first 20 PCs. The four variance-covariance components Vg, Ve, Cg and Ce are defined in Online Methods. d, Accuracy of predicting phenotype by the genetic predictor in unrelated individuals. The prediction R2 shown on the y-axis is the squared correlation between phenotype and predictor. The SNP-based predictor was adjusted by the first 20 PCs. The solid line is the average prediction R2 weighted by sample size over the five cohorts. The dashed line is the prediction accuracy inferred from the within-family prediction analysis (Equation 19 in Online Methods). e, The variance explained by the SNPs was estimated by the whole-genome estimation method in GCTA. The phenotype was adjusted by the first 20 PCs. Each error bar represents the standard error of the estimate. The estimates from all the five cohorts (B-PROOF, FRAM, QIMR, TwinGene and WTCCC-T2D) were averaged by the inverse-variance approach. The dashed line is the variance explained inferred from the within-family prediction analysis. In panels d and e, the number shown in each column is the number of SNPs used in the analysis.
Figure 3
Figure 3. Tissue enrichment combined with pruned gene set network
Genes within genome-wide significant height associated loci enriched for several relevant tissue annotations as well as gene sets. a, Genes in associated loci tended to be highly expressed in tissues related to chondrocytes and osteoblasts (cartilage, joints, and spine), and other musculoskeletal, cardiovascular and endocrine tissue-types. The analysis was conducted based on the DEPICT method and 37,427 human microarray samples. Tissue annotations are sorted by physiological system and significance. Significantly enriched (FDR<0.05) tissues are color-coded in black. b, Significantly enriched reconstituted gene sets (P-value<1×10−11, FDR<1×10−5) identified by DEPICT. Nodes represent reconstituted gene sets and are color-coded by statistical significance. Edge thickness between nodes is proportional to degree of gene overlap as measured by the Jaccard index. Nodes with gene overlap greater than 25% were collapsed into single meta nodes and marked by blue borders. c, reconstituted gene sets comprised by the Chordate Embryonic Development meta node, which represented several gene sets relevant to human height (e.g. ossification, embryonic skeletal system development, and limb development).
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