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Meta-Analysis
. 2017 Apr 27;13(4):e1006528.
doi: 10.1371/journal.pgen.1006528. eCollection 2017 Apr.

Genome-wide Physical Activity Interactions in Adiposity - A Meta-Analysis of 200,452 Adults

Mariaelisa Graff  1 Robert A Scott  2 Anne E Justice  1 Kristin L Young  1   3 Mary F Feitosa  4 Llilda Barata  4 Thomas W Winkler  5 Audrey Y Chu  6   7 Anubha Mahajan  8 David Hadley  9 Luting Xue  6   10 Tsegaselassie Workalemahu  11 Nancy L Heard-Costa  6   12 Marcel den Hoed  2   13 Tarunveer S Ahluwalia  14   15 Qibin Qi  16 Julius S Ngwa  17 Frida Renström  18   19 Lydia Quaye  20 John D Eicher  21 James E Hayes  22   23 Marilyn Cornelis  11   24   25 Zoltan Kutalik  26   27 Elise Lim  10 Jian'an Luan  2 Jennifer E Huffman  6   28 Weihua Zhang  29   30 Wei Zhao  31 Paula J Griffin  10 Toomas Haller  32 Shafqat Ahmad  18 Pedro M Marques-Vidal  33 Stephanie Bien  34 Loic Yengo  35 Alexander Teumer  36   37 Albert Vernon Smith  38   39 Meena Kumari  40 Marie Neergaard Harder  14 Johanne Marie Justesen  14 Marcus E Kleber  41   42 Mette Hollensted  14 Kurt Lohman  43 Natalia V Rivera  44 John B Whitfield  45 Jing Hua Zhao  2 Heather M Stringham  46 Leo-Pekka Lyytikäinen  47   48 Charlotte Huppertz  49   50   51 Gonneke Willemsen  49   50 Wouter J Peyrot  52 Ying Wu  53 Kati Kristiansson  54   55 Ayse Demirkan  56   57 Myriam Fornage  58   59 Maija Hassinen  60 Lawrence F Bielak  31 Gemma Cadby  61 Toshiko Tanaka  62 Reedik Mägi  32 Peter J van der Most  63 Anne U Jackson  46 Jennifer L Bragg-Gresham  46 Veronique Vitart  28 Jonathan Marten  28 Pau Navarro  28 Claire Bellis  64   65 Dorota Pasko  66 Åsa Johansson  67 Søren Snitker  68 Yu-Ching Cheng  68   69 Joel Eriksson  70 Unhee Lim  71 Mette Aadahl  72   73 Linda S Adair  74 Najaf Amin  56 Beverley Balkau  75 Juha Auvinen  76   77 John Beilby  78   79   80 Richard N Bergman  81 Sven Bergmann  27   82 Alain G Bertoni  83   84 John Blangero  85 Amélie Bonnefond  35 Lori L Bonnycastle  86 Judith B Borja  87   88 Søren Brage  2 Fabio Busonero  89 Steve Buyske  90   91 Harry Campbell  92 Peter S Chines  86 Francis S Collins  86 Tanguy Corre  27   82 George Davey Smith  93 Graciela E Delgado  41 Nicole Dueker  94 Marcus Dörr  37   95 Tapani Ebeling  96   97 Gudny Eiriksdottir  38 Tõnu Esko  32   98   99   100 Jessica D Faul  101 Mao Fu  68 Kristine Færch  15 Christian Gieger  102   103   104 Sven Gläser  95 Jian Gong  34 Penny Gordon-Larsen  3   74 Harald Grallert  102   104   105 Tanja B Grammer  41 Niels Grarup  14 Gerard van Grootheest  52 Kennet Harald  54 Nicholas D Hastie  28 Aki S Havulinna  54 Dena Hernandez  106 Lucia Hindorff  107 Lynne J Hocking  108   109 Oddgeir L Holmens  110 Christina Holzapfel  102   111 Jouke Jan Hottenga  49   112 Jie Huang  113 Tao Huang  11 Jennie Hui  78   79   114 Cornelia Huth  104   105 Nina Hutri-Kähönen  115   116 Alan L James  78   117   118 John-Olov Jansson  119 Min A Jhun  31 Markus Juonala  120   121 Leena Kinnunen  54 Heikki A Koistinen  54   122   123 Ivana Kolcic  124 Pirjo Komulainen  60 Johanna Kuusisto  125 Kirsti Kvaløy  126 Mika Kähönen  127   128 Timo A Lakka  60   129 Lenore J Launer  130 Benjamin Lehne  29 Cecilia M Lindgren  8   131   132 Mattias Lorentzon  70   133 Robert Luben  134 Michel Marre  135   136 Yuri Milaneschi  52 Keri L Monda  1   137 Grant W Montgomery  45 Marleen H M De Moor  50   138 Antonella Mulas  89   139 Martina Müller-Nurasyid  103   140   141 A W Musk  78   114   142 Reija Männikkö  60 Satu Männistö  54 Narisu Narisu  86 Matthias Nauck  37   143 Jennifer A Nettleton  59 Ilja M Nolte  63 Albertine J Oldehinkel  144 Matthias Olden  5 Ken K Ong  2 Sandosh Padmanabhan  109   145 Lavinia Paternoster  93 Jeremiah Perez  10 Markus Perola  54   55   146 Annette Peters  104   105   141 Ulrike Peters  34 Patricia A Peyser  31 Inga Prokopenko  147 Hannu Puolijoki  148 Olli T Raitakari  149   150 Tuomo Rankinen  151 Laura J Rasmussen-Torvik  24 Rajesh Rawal  102   103   104 Paul M Ridker  7   152 Lynda M Rose  7 Igor Rudan  92 Cinzia Sarti  153 Mark A Sarzynski  151 Kai Savonen  60 William R Scott  29 Serena Sanna  89 Alan R Shuldiner  68   69 Steve Sidney  154 Günther Silbernagel  155 Blair H Smith  109   156 Jennifer A Smith  31 Harold Snieder  63 Alena Stančáková  125 Barbara Sternfeld  154 Amy J Swift  86 Tuija Tammelin  157 Sian-Tsung Tan  158 Barbara Thorand  104   105 Dorothée Thuillier  35 Liesbeth Vandenput  70 Henrik Vestergaard  14   15 Jana V van Vliet-Ostaptchouk  159 Marie-Claude Vohl  160   161 Uwe Völker  37   162 Gérard Waeber  33 Mark Walker  163 Sarah Wild  164 Andrew Wong  165 Alan F Wright  28 M Carola Zillikens  166 Niha Zubair  34 Christopher A Haiman  167 Loic Lemarchand  71 Ulf Gyllensten  67 Claes Ohlsson  70 Albert Hofman  168   169 Fernando Rivadeneira  166   168   169 André G Uitterlinden  166   168 Louis Pérusse  160   170 James F Wilson  28   92 Caroline Hayward  28 Ozren Polasek  92   124 Francesco Cucca  89   139 Kristian Hveem  126 Catharina A Hartman  171 Anke Tönjes  172 Stefania Bandinelli  173 Lyle J Palmer  174 Sharon L R Kardia  31 Rainer Rauramaa  60   175 Thorkild I A Sørensen  14   73   93   176 Jaakko Tuomilehto  54   177   178 Veikko Salomaa  54 Brenda W J H Penninx  52 Eco J C de Geus  49   50 Dorret I Boomsma  49   112 Terho Lehtimäki  47   48 Massimo Mangino  20   179 Markku Laakso  125 Claude Bouchard  151 Nicholas G Martin  45 Diana Kuh  165 Yongmei Liu  83 Allan Linneberg  72   180   181 Winfried März  41   182   183 Konstantin Strauch  103   184 Mika Kivimäki  185 Tamara B Harris  186 Vilmundur Gudnason  38   39 Henry Völzke  36   37 Lu Qi  11 Marjo-Riitta Järvelin  29   76   77   187   188 John C Chambers  29   30   189 Jaspal S Kooner  30   158   189 Philippe Froguel  35   190 Charles Kooperberg  34 Peter Vollenweider  33 Göran Hallmans  19 Torben Hansen  14 Oluf Pedersen  14 Andres Metspalu  32 Nicholas J Wareham  2 Claudia Langenberg  2 David R Weir  101 David J Porteous  109   191 Eric Boerwinkle  59 Daniel I Chasman  7   100   152 CHARGE ConsortiumEPIC-InterAct ConsortiumPAGE ConsortiumGonçalo R Abecasis  46 Inês Barroso  192   193   194 Mark I McCarthy  8   195   196 Timothy M Frayling  66 Jeffrey R O'Connell  68 Cornelia M van Duijn  56   169   197 Michael Boehnke  46 Iris M Heid  5 Karen L Mohlke  53 David P Strachan  198 Caroline S Fox  21 Ching-Ti Liu  10 Joel N Hirschhorn  99   100   199 Robert J Klein  23 Andrew D Johnson  6   21 Ingrid B Borecki  4 Paul W Franks  11   18   200 Kari E North  201 L Adrienne Cupples  6   10 Ruth J F Loos  2   202   203   204 Tuomas O Kilpeläinen  2   14   204
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Free PMC article
Meta-Analysis

Genome-wide Physical Activity Interactions in Adiposity - A Meta-Analysis of 200,452 Adults

Mariaelisa Graff et al. PLoS Genet. .
Free PMC article

Erratum in

  • Correction: Genome-wide physical activity interactions in adiposity - A meta-analysis of 200,452 adults.
    Graff M, Scott RA, Justice AE, Young KL, Feitosa MF, Barata L, Winkler TW, Chu AY, Mahajan A, Hadley D, Xue L, Workalemahu T, Heard-Costa NL, den Hoed M, Ahluwalia TS, Qi Q, Ngwa JS, Renström F, Quaye L, Eicher JD, Hayes JE, Cornelis M, Kutalik Z, Lim E, Luan J, Huffman JE, Zhang W, Zhao W, Griffin PJ, Haller T, Ahmad S, Marques-Vidal PM, Bien S, Yengo L, Teumer A, Smith AV, Kumari M, Harder MN, Justesen JM, Kleber ME, Hollensted M, Lohman K, Rivera NV, Whitfield JB, Zhao JH, Stringham HM, Lyytikäinen LP, Huppertz C, Willemsen G, Peyrot WJ, Wu Y, Kristiansson K, Demirkan A, Fornage M, Hassinen M, Bielak LF, Cadby G, Tanaka T, Mägi R, van der Most PJ, Jackson AU, Bragg-Gresham JL, Vitart V, Marten J, Navarro P, Bellis C, Pasko D, Johansson Å, Snitker S, Cheng YC, Eriksson J, Lim U, Aadahl M, Adair LS, Amin N, Balkau B, Auvinen J, Beilby J, Bergman RN, Bergmann S, Bertoni AG, Blangero J, Bonnefond A, Bonnycastle LL, Borja JB, Brage S, Busonero F, Buyske S, Campbell H, Chines PS, Collins FS, Corre T, Smith GD, Delgado GE, Dueker N, Dörr M, Ebeling T, Eiriksdottir G, Esko T, Faul JD, Fu M, Færch K, Gieger C, Gläser S, Gong J, Gordon-Larsen P, Grallert H, Grammer TB, Grarup N, van Grootheest G, Harald K, Hastie ND, Havulinna AS, Hernandez D, Hindorff L, Hocking LJ, Holmens OL, Holzapfel C, Hottenga JJ, Huang J, Huang T, Hui J, Huth C, Hutri-Kähönen N, James AL, Jansson JO, Jhun MA, Juonala M, Kinnunen L, Koistinen HA, Kolcic I, Komulainen P, Kuusisto J, Kvaløy K, Kähönen M, Lakka TA, Launer LJ, Lehne B, Lindgren CM, Lorentzon M, Luben R, Marre M, Milaneschi Y, Monda KL, Montgomery GW, De Moor MHM, Mulas A, Müller-Nurasyid M, Musk AW, Männikkö R, Männistö S, Narisu N, Nauck M, Nettleton JA, Nolte IM, Oldehinkel AJ, Olden M, Ong KK, Padmanabhan S, Paternoster L, Perez J, Perola M, Peters A, Peters U, Peyser PA, Prokopenko I, Puolijoki H, Raitakari OT, Rankinen T, Rasmussen-Torvik LJ, Rawal R, Ridker PM, Rose LM, Rudan I, Sarti C, Sarzynski MA, Savonen K, Scott WR, Sanna S, Shuldiner AR, Sidney S, Silbernagel G, Smith BH, Smith JA, Snieder H, Stančáková A, Sternfeld B, Swift AJ, Tammelin T, Tan ST, Thorand B, Thuillier D, Vandenput L, Vestergaard H, van Vliet-Ostaptchouk JV, Vohl MC, Völker U, Waeber G, Walker M, Wild S, Wong A, Wright AF, Zillikens MC, Zubair N, Haiman CA, Lemarchand L, Gyllensten U, Ohlsson C, Hofman A, Rivadeneira F, Uitterlinden AG, Pérusse L, Wilson JF, Hayward C, Polasek O, Cucca F, Hveem K, Hartman CA, Tönjes A, Bandinelli S, Palmer LJ, Kardia SLR, Rauramaa R, Sørensen TIA, Tuomilehto J, Salomaa V, Penninx BWJH, de Geus EJC, Boomsma DI, Lehtimäki T, Mangino M, Laakso M, Bouchard C, Martin NG, Kuh D, Liu Y, Linneberg A, März W, Strauch K, Kivimäki M, Harris TB, Gudnason V, Völzke H, Qi L, Järvelin MR, Chambers JC, Kooner JS, Froguel P, Kooperberg C, Vollenweider P, Hallmans G, Hansen T, Pedersen O, Metspalu A, Wareham NJ, Langenberg C, Weir DR, Porteous DJ, Boerwinkle E, Chasman DI; CHARGE Consortium; EPIC-InterAct Consortium; PAGE Consortium, Abecasis GR, Barroso I, McCarthy MI, Frayling TM, O'Connell JR, van Duijn CM, Boehnke M, Heid IM, Mohlke KL, Strachan DP, Fox CS, Liu CT, Hirschhorn JN, Klein RJ, Johnson AD, Borecki IB, Franks PW, North KE, Cupples LA, Loos RJF, Kilpeläinen TO. Graff M, et al. PLoS Genet. 2017 Aug 23;13(8):e1006972. doi: 10.1371/journal.pgen.1006972. eCollection 2017 Aug. PLoS Genet. 2017. PMID: 28832619 Free PMC article.

Abstract

Physical activity (PA) may modify the genetic effects that give rise to increased risk of obesity. To identify adiposity loci whose effects are modified by PA, we performed genome-wide interaction meta-analyses of BMI and BMI-adjusted waist circumference and waist-hip ratio from up to 200,452 adults of European (n = 180,423) or other ancestry (n = 20,029). We standardized PA by categorizing it into a dichotomous variable where, on average, 23% of participants were categorized as inactive and 77% as physically active. While we replicate the interaction with PA for the strongest known obesity-risk locus in the FTO gene, of which the effect is attenuated by ~30% in physically active individuals compared to inactive individuals, we do not identify additional loci that are sensitive to PA. In additional genome-wide meta-analyses adjusting for PA and interaction with PA, we identify 11 novel adiposity loci, suggesting that accounting for PA or other environmental factors that contribute to variation in adiposity may facilitate gene discovery.

Conflict of interest statement

We have read the journal's policy and the authors of this manuscript have the following competing interests: Genotyping in the Ely and Fenland studies was supported in part by an MRC-GlaxoSmithKline pilot programme grant (G0701863). The RISC Study was supported in part by AstraZeneca. The D.E.S.I.R. study has been supported in part by INSERM contracts with Lilly, Novartis Pharma, Sanofi-Aventis, Ardix Medical, Bayer Diagnostics, Becton Dickinson, Cardionics, Merck Santé, Novo Nordisk, Pierre Fabre, Roche, and Topcon. In SHIP, genome-wide data have been supported in part by a joint grant from Siemens Healthcare, Erlangen, Germany.

Figures

Fig 1
Fig 1. Power to identify PA-adjusted main, joint or GxPA interaction effects in 200,000 individuals (45,000 inactive, 155,000 active).
The plots compare power to identify genome-wide significant main effects (PadjPA<5x10-8, dashed black), joint effects (PJOINT<5x10-8, dotted green) or GxPA interaction effects (PINT<5x10-8, solid magenta) as well as the power to identify Bonferroni-corrected interaction effects (PINT<0.05/number of loci, solid orange) for the SNPs that reached a genome-wide significant PA-adjusted main effect association (PadjPA<5x10-8). The power computations were based on analytical power formulae provided elsewhere [50] and were conducted a-priori based on various types of known realistic BMI effect sizes [51]. Panels A, C, E: Assuming an effect in inactive individuals similar to a small (RINACT2=0.01%, comparable to the known BMI effect of the NUDT3 locus), medium (RINACT2=0.07%, comparable to the known BMI effect of the BDNF locus) and large (RINACT2=0.34%, comparable to the known BMI effect of the FTO locus) realistic effect on BMI and for various effects in physically active individuals (varied on the x axis); Panels B,D,F: Assuming an effect in physically active individuals similar to the small, medium and large realistic effects of the NUDT3, BDNF and FTO loci on BMI and for various effects in inactive individuals (varied on x axis).

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