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. 2018 Jan;50(1):26-41.
doi: 10.1038/s41588-017-0011-x. Epub 2017 Dec 22.

Protein-altering variants associated with body mass index implicate pathways that control energy intake and expenditure in obesity

Valérie Turcot #  1 , Yingchang Lu #  2   3   4 , Heather M Highland #  5   6 , Claudia Schurmann #  3   4 , Anne E Justice #  5 , Rebecca S Fine #  7   8   9 , Jonathan P Bradfield  10   11 , Tõnu Esko  7   9   12 , Ayush Giri  13 , Mariaelisa Graff  5 , Xiuqing Guo  14 , Audrey E Hendricks  15   16 , Tugce Karaderi  17   18 , Adelheid Lempradl  19 , Adam E Locke  20   21 , Anubha Mahajan  17 , Eirini Marouli  22 , Suthesh Sivapalaratnam  23   24   25 , Kristin L Young  5 , Tamuno Alfred  3 , Mary F Feitosa  26 , Nicholas G D Masca  27   28 , Alisa K Manning  7   24   29   30 , Carolina Medina-Gomez  31   32 , Poorva Mudgal  33 , Maggie C Y Ng  33   34 , Alex P Reiner  35   36 , Sailaja Vedantam  7   8   9 , Sara M Willems  37 , Thomas W Winkler  38 , Gonçalo Abecasis  20 , Katja K Aben  39   40 , Dewan S Alam  41 , Sameer E Alharthi  22   42 , Matthew Allison  43 , Philippe Amouyel  44   45   46 , Folkert W Asselbergs  47   48   49 , Paul L Auer  50 , Beverley Balkau  51 , Lia E Bang  52 , Inês Barroso  15   53   54 , Lisa Bastarache  55 , Marianne Benn  56   57 , Sven Bergmann  58   59 , Lawrence F Bielak  60 , Matthias Blüher  61   62 , Michael Boehnke  20 , Heiner Boeing  63 , Eric Boerwinkle  64   65 , Carsten A Böger  66 , Jette Bork-Jensen  67 , Michiel L Bots  68 , Erwin P Bottinger  3 , Donald W Bowden  33   34   69 , Ivan Brandslund  70   71 , Gerome Breen  72   73 , Murray H Brilliant  74 , Linda Broer  32 , Marco Brumat  75 , Amber A Burt  76 , Adam S Butterworth  77   78 , Peter T Campbell  79 , Stefania Cappellani  80 , David J Carey  81 , Eulalia Catamo  80 , Mark J Caulfield  22   82 , John C Chambers  83   84   85 , Daniel I Chasman  7   86   87   88 , Yii-Der I Chen  14 , Rajiv Chowdhury  77 , Cramer Christensen  89 , Audrey Y Chu  90   91 , Massimiliano Cocca  92 , Francis S Collins  93 , James P Cook  94 , Janie Corley  95   96 , Jordi Corominas Galbany  97   98 , Amanda J Cox  33   34   99 , David S Crosslin  100 , Gabriel Cuellar-Partida  101   102 , Angela D'Eustacchio  80 , John Danesh  15   77   78   103 , Gail Davies  94   95 , Paul I W Bakker  68   104 , Mark C H Groot  105   106 , Renée Mutsert  107 , Ian J Deary  94   95 , George Dedoussis  108 , Ellen W Demerath  109 , Martin Heijer  110 , Anneke I Hollander  98 , Hester M Ruijter  111 , Joe G Dennis  112 , Josh C Denny  55 , Emanuele Di Angelantonio  77   78 , Fotios Drenos  113   114 , Mengmeng Du  36   115 , Marie-Pierre Dubé  1   116 , Alison M Dunning  117 , Douglas F Easton  112   117 , Todd L Edwards  13 , David Ellinghaus  118 , Patrick T Ellinor  7   24   30 , Paul Elliott  119 , Evangelos Evangelou  84   120 , Aliki-Eleni Farmaki  108   121 , I Sadaf Farooqi  53   54 , Jessica D Faul  122 , Sascha Fauser  123 , Shuang Feng  20 , Ele Ferrannini  124   125 , Jean Ferrieres  126 , Jose C Florez  7   24   29   30 , Ian Ford  127 , Myriam Fornage  128 , Oscar H Franco  31 , Andre Franke  118 , Paul W Franks  129   130   131 , Nele Friedrich  132 , Ruth Frikke-Schmidt  57   133 , Tessel E Galesloot  40 , Wei Gan  17 , Ilaria Gandin  134 , Paolo Gasparini  75   80 , Jane Gibson  135 , Vilmantas Giedraitis  136 , Anette P Gjesing  67 , Penny Gordon-Larsen  137   138 , Mathias Gorski  38   66 , Hans-Jörgen Grabe  139   140 , Struan F A Grant  10   141   142 , Niels Grarup  67 , Helen L Griffiths  143 , Megan L Grove  64 , Vilmundur Gudnason  144   145 , Stefan Gustafsson  146 , Jeff Haessler  36 , Hakon Hakonarson  10   141 , Anke R Hammerschlag  147 , Torben Hansen  67 , Kathleen Mullan Harris  137   148 , Tamara B Harris  149 , Andrew T Hattersley  150 , Christian T Have  67 , Caroline Hayward  151 , Liang He  152   153 , Nancy L Heard-Costa  90   154 , Andrew C Heath  155 , Iris M Heid  38   156 , Øyvind Helgeland  157   158 , Jussi Hernesniemi  159   160   161 , Alex W Hewitt  162   163   164 , Oddgeir L Holmen  165 , G Kees Hovingh  23 , Joanna M M Howson  77 , Yao Hu  166 , Paul L Huang  24 , Jennifer E Huffman  151 , M Arfan Ikram  31   167   168 , Erik Ingelsson  146   169 , Anne U Jackson  20 , Jan-Håkan Jansson  170   171 , Gail P Jarvik  76   172 , Gorm B Jensen  173 , Yucheng Jia  14 , Stefan Johansson  158   174 , Marit E Jørgensen  175   176 , Torben Jørgensen  57   177   178 , J Wouter Jukema  179   180 , Bratati Kahali  181   182   183   184 , René S Kahn  185 , Mika Kähönen  186   187 , Pia R Kamstrup  56 , Stavroula Kanoni  22 , Jaakko Kaprio  153   188   189 , Maria Karaleftheri  190 , Sharon L R Kardia  60 , Fredrik Karpe  191   192 , Sekar Kathiresan  7   24   88 , Frank Kee  193 , Lambertus A Kiemeney  40 , Eric Kim  14 , Hidetoshi Kitajima  17 , Pirjo Komulainen  194   195   196 , Jaspal S Kooner  83   85   197   198 , Charles Kooperberg  36 , Tellervo Korhonen  153   189   199 , Peter Kovacs  61 , Helena Kuivaniemi  81   200   201 , Zoltán Kutalik  59   202 , Kari Kuulasmaa  189 , Johanna Kuusisto  203 , Markku Laakso  203 , Timo A Lakka  194   195   196 , David Lamparter  58   59 , Ethan M Lange  204 , Leslie A Lange  204 , Claudia Langenberg  37 , Eric B Larson  76   205   206 , Nanette R Lee  207   208 , Terho Lehtimäki  160   161 , Cora E Lewis  209 , Huaixing Li  166 , Jin Li  169 , Ruifang Li-Gao  107 , Honghuang Lin  210 , Keng-Hung Lin  211 , Li-An Lin  128 , Xu Lin  166 , Lars Lind  212 , Jaana Lindström  189 , Allan Linneberg  178   213   214 , Ching-Ti Liu  215 , Dajiang J Liu  216 , Yongmei Liu  217 , Ken S Lo  1 , Artitaya Lophatananon  218 , Andrew J Lotery  143 , Anu Loukola  153   188 , Jian'an Luan  37 , Steven A Lubitz  7   24   30 , Leo-Pekka Lyytikäinen  160   161 , Satu Männistö  189 , Gaëlle Marenne  15 , Angela L Mazul  5 , Mark I McCarthy  17   191   192 , Roberta McKean-Cowdin  219 , Sarah E Medland  102 , Karina Meidtner  220   221 , Lili Milani  12 , Vanisha Mistry  53   54 , Paul Mitchell  222 , Karen L Mohlke  204 , Leena Moilanen  223 , Marie Moitry  224   225 , Grant W Montgomery  102   226 , Dennis O Mook-Kanamori  107   227 , Carmel Moore  78   228 , Trevor A Mori  229 , Andrew D Morris  230 , Andrew P Morris  17   94 , Martina Müller-Nurasyid  156   231   232 , Patricia B Munroe  22   82 , Mike A Nalls  233   234 , Narisu Narisu  93 , Christopher P Nelson  27   28 , Matt Neville  191   192 , Sune F Nielsen  56   57 , Kjell Nikus  159 , Pål R Njølstad  157   158 , Børge G Nordestgaard  56   57 , Dale R Nyholt  102   235 , Jeffrey R O'Connel  236 , Michelle L O'Donoghue  237 , Loes M Olde Loohuis  238 , Roel A Ophoff  185   238 , Katharine R Owen  191   192 , Chris J Packard  127 , Sandosh Padmanabhan  127 , Colin N A Palmer  239 , Nicholette D Palmer  69 , Gerard Pasterkamp  111   240 , Aniruddh P Patel  7   24   88 , Alison Pattie  96 , Oluf Pedersen  67 , Peggy L Peissig  74 , Gina M Peloso  215 , Craig E Pennell  241 , Markus Perola  12   188   189   242 , James A Perry  236 , John R B Perry  37 , Tune H Pers  67   243 , Thomas N Person  74 , Annette Peters  221   232   244 , Eva R B Petersen  245 , Patricia A Peyser  60 , Ailith Pirie  117 , Ozren Polasek  230   246 , Tinca J Polderman  147 , Hannu Puolijoki  247 , Olli T Raitakari  248   249 , Asif Rasheed  250 , Rainer Rauramaa  194   195 , Dermot F Reilly  91 , Frida Renström  129   251 , Myriam Rheinberger  66 , Paul M Ridker  87   88   237 , John D Rioux  1   116 , Manuel A Rivas  7   252 , David J Roberts  78   253   254 , Neil R Robertson  17   191 , Antonietta Robino  80 , Olov Rolandsson  170   255 , Igor Rudan  230 , Katherine S Ruth  256 , Danish Saleheen  250   257 , Veikko Salomaa  189 , Nilesh J Samani  27   28 , Yadav Sapkota  102 , Naveed Sattar  127 , Robert E Schoen  258 , Pamela J Schreiner  109 , Matthias B Schulze  220   221 , Robert A Scott  37 , Marcelo P Segura-Lepe  84 , Svati H Shah  259 , Wayne H-H Sheu  260   261   262 , Xueling Sim  20   263 , Andrew J Slater  264   265 , Kerrin S Small  266 , Albert V Smith  144   145 , Lorraine Southam  15   17 , Timothy D Spector  266 , Elizabeth K Speliotes  181   182   183 , John M Starr  95   267 , Kari Stefansson  144   268 , Valgerdur Steinthorsdottir  268 , Kathleen E Stirrups  22   25 , Konstantin Strauch  156   269 , Heather M Stringham  20 , Michael Stumvoll  61   62 , Liang Sun  152   153 , Praveen Surendran  77 , Amy J Swift  93 , Hayato Tada  237   270 , Katherine E Tansey  114   271 , Jean-Claude Tardif  1 , Kent D Taylor  14 , Alexander Teumer  272 , Deborah J Thompson  112 , Gudmar Thorleifsson  268 , Unnur Thorsteinsdottir  144   268 , Betina H Thuesen  178 , Anke Tönjes  273 , Gerard Tromp  81   201 , Stella Trompet  179   274 , Emmanouil Tsafantakis  275 , Jaakko Tuomilehto  189   276   277   278 , Anne Tybjaerg-Hansen  57   133 , Jonathan P Tyrer  117 , Rudolf Uher  279 , André G Uitterlinden  31   32 , Matti Uusitupa  280 , Sander W Laan  111 , Cornelia M Duijn  31 , Nienke Leeuwen  281   282 , Jessica van Setten  47 , Mauno Vanhala  283   284 , Anette Varbo  56   57 , Tibor V Varga  129 , Rohit Varma  285 , Digna R Velez Edwards  286 , Sita H Vermeulen  40 , Giovanni Veronesi  287 , Henrik Vestergaard  67   176 , Veronique Vitart  151 , Thomas F Vogt  288 , Uwe Völker  289   290 , Dragana Vuckovic  75   80 , Lynne E Wagenknecht  217 , Mark Walker  291 , Lars Wallentin  292 , Feijie Wang  166 , Carol A Wang  241 , Shuai Wang  215 , Yiqin Wang  166 , Erin B Ware  60   122 , Nicholas J Wareham  37 , Helen R Warren  22   82 , Dawn M Waterworth  293 , Jennifer Wessel  294 , Harvey D White  295 , Cristen J Willer  181   182   296 , James G Wilson  297 , Daniel R Witte  298   299 , Andrew R Wood  256 , Ying Wu  204 , Hanieh Yaghootkar  256 , Jie Yao  14 , Pang Yao  166 , Laura M Yerges-Armstrong  236   300 , Robin Young  77   127 , Eleftheria Zeggini  15 , Xiaowei Zhan  301 , Weihua Zhang  83   84 , Jing Hua Zhao  37 , Wei Zhao  257 , Wei Zhao  60 , Wei Zhou  181   182 , Krina T Zondervan  17   302 ; CHD Exome+ Consortium; EPIC-CVD Consortium; ExomeBP Consortium; Global Lipids Genetic Consortium; GoT2D Genes Consortium; EPIC InterAct Consortium; INTERVAL Study; ReproGen Consortium; T2D-Genes Consortium; MAGIC Investigators; Understanding Society Scientific Group; Jerome I Rotter  14 , John A Pospisilik  19 , Fernando Rivadeneira  31   32 , Ingrid B Borecki  26 , Panos Deloukas  22   42 , Timothy M Frayling  256 , Guillaume Lettre  1   116 , Kari E North  303 , Cecilia M Lindgren  17   304 , Joel N Hirschhorn  305   306   307   308 , Ruth J F Loos  309   310   311
Affiliations

Protein-altering variants associated with body mass index implicate pathways that control energy intake and expenditure in obesity

Valérie Turcot et al. Nat Genet. 2018 Jan.

Erratum in

  • Publisher Correction: Protein-altering variants associated with body mass index implicate pathways that control energy intake and expenditure in obesity.
    Turcot V, Lu Y, Highland HM, Schurmann C, Justice AE, Fine RS, Bradfield JP, Esko T, Giri A, Graff M, Guo X, Hendricks AE, Karaderi T, Lempradl A, Locke AE, Mahajan A, Marouli E, Sivapalaratnam S, Young KL, Alfred T, Feitosa MF, Masca NGD, Manning AK, Medina-Gomez C, Mudgal P, Ng MCY, Reiner AP, Vedantam S, Willems SM, Winkler TW, Abecasis G, Aben KK, Alam DS, Alharthi SE, Allison M, Amouyel P, Asselbergs FW, Auer PL, Balkau B, Bang LE, Barroso I, Bastarache L, Benn M, Bergmann S, Bielak LF, Blüher M, Boehnke M, Boeing H, Boerwinkle E, Böger CA, Bork-Jensen J, Bots ML, Bottinger EP, Bowden DW, Brandslund I, Breen G, Brilliant MH, Broer L, Brumat M, Burt AA, Butterworth AS, Campbell PT, Cappellani S, Carey DJ, Catamo E, Caulfield MJ, Chambers JC, Chasman DI, Chen YI, Chowdhury R, Christensen C, Chu AY, Cocca M, Collins FS, Cook JP, Corley J, Corominas Galbany J, Cox AJ, Crosslin DS, Cuellar-Partida G, D'Eustacchio A, Danesh J, Davies G, Bakker PIW, Groot MCH, Mutsert R, Deary IJ, Dedoussis G, Demerath EW, Heijer M, Hollander AI, Ruijter HM, Dennis JG, Denny JC, Angelantonio E, Drenos F, Du M, Dubé MP, Dunning AM, Easton DF, Edwards TL, Ellinghaus D, Ellinor PT, Elliott P, Evangelou… See abstract for full author list ➔ Turcot V, et al. Nat Genet. 2018 May;50(5):765-766. doi: 10.1038/s41588-018-0050-y. Nat Genet. 2018. PMID: 29549329
  • Publisher Correction: Protein-altering variants associated with body mass index implicate pathways that control energy intake and expenditure in obesity.
    Turcot V, Lu Y, Highland HM, Schurmann C, Justice AE, Fine RS, Bradfield JP, Esko T, Giri A, Graff M, Guo X, Hendricks AE, Karaderi T, Lempradl A, Locke AE, Mahajan A, Marouli E, Sivapalaratnam S, Young KL, Alfred T, Feitosa MF, Masca NGD, Manning AK, Medina-Gomez C, Mudgal P, Ng MCY, Reiner AP, Vedantam S, Willems SM, Winkler TW, Abecasis G, Aben KK, Alam DS, Alharthi SE, Allison M, Amouyel P, Asselbergs FW, Auer PL, Balkau B, Bang LE, Barroso I, Bastarache L, Benn M, Bergmann S, Bielak LF, Blüher M, Boehnke M, Boeing H, Boerwinkle E, Böger CA, Bork-Jensen J, Bots ML, Bottinger EP, Bowden DW, Brandslund I, Breen G, Brilliant MH, Broer L, Brumat M, Burt AA, Butterworth AS, Campbell PT, Cappellani S, Carey DJ, Catamo E, Caulfield MJ, Chambers JC, Chasman DI, Chen YI, Chowdhury R, Christensen C, Chu AY, Cocca M, Collins FS, Cook JP, Corley J, Corominas Galbany J, Cox AJ, Crosslin DS, Cuellar-Partida G, D'Eustacchio A, Danesh J, Davies G, Bakker PIW, Groot MCH, Mutsert R, Deary IJ, Dedoussis G, Demerath EW, Heijer M, Hollander AI, Ruijter HM, Dennis JG, Denny JC, Di Angelantonio E, Drenos F, Du M, Dubé MP, Dunning AM, Easton DF, Edwards TL, Ellinghaus D, Ellinor PT, Elliott P, Evange… See abstract for full author list ➔ Turcot V, et al. Nat Genet. 2018 May;50(5):766-767. doi: 10.1038/s41588-018-0082-3. Nat Genet. 2018. PMID: 29549330
  • Publisher Correction: Protein-altering variants associated with body mass index implicate pathways that control energy intake and expenditure in obesity.
    Turcot V, Lu Y, Highland HM, Schurmann C, Justice AE, Fine RS, Bradfield JP, Esko T, Giri A, Graff M, Guo X, Hendricks AE, Karaderi T, Lempradl A, Locke AE, Mahajan A, Marouli E, Sivapalaratnam S, Young KL, Alfred T, Feitosa MF, Masca NGD, Manning AK, Medina-Gomez C, Mudgal P, Ng MCY, Reiner AP, Vedantam S, Willems SM, Winkler TW, Abecasis G, Aben KK, Alam DS, Alharthi SE, Allison M, Amouyel P, Asselbergs FW, Auer PL, Balkau B, Bang LE, Barroso I, Bastarache L, Benn M, Bergmann S, Bielak LF, Blüher M, Boehnke M, Boeing H, Boerwinkle E, Böger CA, Bork-Jensen J, Bots ML, Bottinger EP, Bowden DW, Brandslund I, Breen G, Brilliant MH, Broer L, Brumat M, Burt AA, Butterworth AS, Campbell PT, Cappellani S, Carey DJ, Catamo E, Caulfield MJ, Chambers JC, Chasman DI, Chen YI, Chowdhury R, Christensen C, Chu AY, Cocca M, Collins FS, Cook JP, Corley J, Galbany JC, Cox AJ, Crosslin DS, Cuellar-Partida G, D'Eustacchio A, Danesh J, Davies G, Bakker PIW, Groot MCH, Mutsert R, Deary IJ, Dedoussis G, Demerath EW, Heijer M, Hollander AI, Ruijter HM, Dennis JG, Denny JC, Di Angelantonio E, Drenos F, Du M, Dubé MP, Dunning AM, Easton DF, Edwards TL, Ellinghaus D, Ellinor PT, Elliott P, Evangelou E, Fa… See abstract for full author list ➔ Turcot V, et al. Nat Genet. 2019 Jul;51(7):1191-1192. doi: 10.1038/s41588-019-0447-2. Nat Genet. 2019. PMID: 31160809

Abstract

Genome-wide association studies (GWAS) have identified >250 loci for body mass index (BMI), implicating pathways related to neuronal biology. Most GWAS loci represent clusters of common, noncoding variants from which pinpointing causal genes remains challenging. Here we combined data from 718,734 individuals to discover rare and low-frequency (minor allele frequency (MAF) < 5%) coding variants associated with BMI. We identified 14 coding variants in 13 genes, of which 8 variants were in genes (ZBTB7B, ACHE, RAPGEF3, RAB21, ZFHX3, ENTPD6, ZFR2 and ZNF169) newly implicated in human obesity, 2 variants were in genes (MC4R and KSR2) previously observed to be mutated in extreme obesity and 2 variants were in GIPR. The effect sizes of rare variants are ~10 times larger than those of common variants, with the largest effect observed in carriers of an MC4R mutation introducing a stop codon (p.Tyr35Ter, MAF = 0.01%), who weighed ~7 kg more than non-carriers. Pathway analyses based on the variants associated with BMI confirm enrichment of neuronal genes and provide new evidence for adipocyte and energy expenditure biology, widening the potential of genetically supported therapeutic targets in obesity.

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Figures

Figure 1
Figure 1. Effect sizes (y-axis) of the 14 BMI-associated R/LF coding variants by their minor allele frequency
Effect sizes are expressed in body weight (kg) per allele, assuming a SD of 4.5 kg and an average-sized person of 1.7m tall. Solid markers indicate that the minor allele is associated with higher BMI, and clear markers indicate that the minor allele is associated with lower BMI. Variants were identified in all-ancestry analyses (light blue diamonds), the European ancestry analyses (dark blue square) and women-only analyses (pink diamond). Effect sizes for previously identified GWAS loci are shown in navy blue diamonds. The dotted line represents 80% power, assuming α = 2×10−7 and N= 525,000 (discovery sample size).
Figure 2
Figure 2. Heatmap showing DEPICT gene set enrichment results for suggestive and significant rare and low-frequency coding SNVs
For any given square, the color indicates how strongly the corresponding gene (x-axis) is predicted to belong to the reconstituted gene set (y-axis), based on the gene’s Z-score for gene set inclusion in DEPICT’s reconstituted gene sets (red indicates a higher, blue a lower Z-score). To visually reduce redundancy and increase clarity, we chose one representative "meta-gene set" for each group of highly correlated gene sets based on affinity propagation clustering (Online Methods, Supplementary Note). Heatmap intensity and DEPICT P-values (Supplementary Table 17) correspond to the most significantly enriched gene set within the meta-gene set. Annotations for genes indicate (1) whether it has an OMIM annotation as underlying a monogenic obesity disorder (black/grey), (2) the MAF of the significant ExomeChip (EC) variant (blue), (3) whether the variant’s P-value reached array-wide significance (<2×10−7) or suggestive significance (<5×10−4) (purple), (4) whether the variant was novel, overlapping “relaxed” GWAS signals from Locke et al. (GWAS P<5×10−4), or overlapping “stringent” GWAS hits (GWAS P<5×10−8) (pink), and (5) whether the gene was included in the gene set enrichment analysis or excluded by filters (orange/brown) (Online Methods, Supplementary Note). Annotations for gene sets indicate if the meta-gene set was significant (green; FDR <0.01, <0.05, or not significant) in the DEPICT analysis of GWAS results. Here, two regions of particularly strong gene set membership are shown (see full heat map in Supplementary Figure 10a).
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