Sequence data and association statistics from 12,940 type 2 diabetes cases and controls

Jason Flannick 1 2, Christian Fuchsberger 3, Anubha Mahajan 4, Tanya M Teslovich 3, Vineeta Agarwala 2 5, Kyle J Gaulton 4, Lizz Caulkins 2, Ryan Koesterer 2, Clement Ma 3, Loukas Moutsianas 4, Davis J McCarthy 4 6, Manuel A Rivas 4, John R B Perry 4 7 8 9, Xueling Sim 3, Thomas W Blackwell 3, Neil R Robertson 4 10, N William Rayner 4 10 11, Pablo Cingolani 12 13, Adam E Locke 3, Juan Fernandez Tajes 4, Heather M Highland 14, Josee Dupuis 15 16, Peter S Chines 17, Cecilia M Lindgren 2 4, Christopher Hartl 2, Anne U Jackson 3, Han Chen 15 18, Jeroen R Huyghe 3, Martijn van de Bunt 4 10, Richard D Pearson 4, Ashish Kumar 4 19, Martina Müller-Nurasyid 20 21 22 23, Niels Grarup 24, Heather M Stringham 3, Eric R Gamazon 25, Jaehoon Lee 26, Yuhui Chen 4, Robert A Scott 8, Jennifer E Below 27, Peng Chen 28, Jinyan Huang 29, Min Jin Go 30, Michael L Stitzel 31, Dorota Pasko 7, Stephen C J Parker 32, Tibor V Varga 33, Todd Green 2, Nicola L Beer 10, Aaron G Day-Williams 11, Teresa Ferreira 4, Tasha Fingerlin 34, Momoko Horikoshi 4 10, Cheng Hu 35, Iksoo Huh 26, Mohammad Kamran Ikram 36 37 38, Bong-Jo Kim 30, Yongkang Kim 26, Young Jin Kim 30, Min-Seok Kwon 39, Juyoung Lee 30, Selyeong Lee 26, Keng-Han Lin 3, Taylor J Maxwell 27, Yoshihiko Nagai 13 40 41, Xu Wang 28, Ryan P Welch 3, Joon Yoon 39, Weihua Zhang 42 43, Nir Barzilai 44, Benjamin F Voight 45 46, Bok-Ghee Han 30, Christopher P Jenkinson 47 48, Teemu Kuulasmaa 49, Johanna Kuusisto 49 50, Alisa Manning 2, Maggie C Y Ng 51 52, Nicholette D Palmer 51 52 53, Beverley Balkau 54, Alena Stančáková 49, Hanna E Abboud 47, Heiner Boeing 55, Vilmantas Giedraitis 56, Dorairaj Prabhakaran 57, Omri Gottesman 58, James Scott 59, Jason Carey 2, Phoenix Kwan 3, George Grant 2, Joshua D Smith 60, Benjamin M Neale 2 61, Shaun Purcell 2 62 63, Adam S Butterworth 64, Joanna M M Howson 64, Heung Man Lee 65, Yingchang Lu 58, Soo-Heon Kwak 66, Wei Zhao 67, John Danesh 11 64 68, Vincent K L Lam 65, Kyong Soo Park 69, Danish Saleheen 70 71, Wing Yee So 65, Claudia H T Tam 65, Uzma Afzal 42, David Aguilar 72, Rector Arya 73, Tin Aung 36 37 38, Edmund Chan 74, Carmen Navarro 75 76 77, Ching-Yu Cheng 28 36 37 38, Domenico Palli 78, Adolfo Correa 79, Joanne E Curran 80, Dennis Rybin 15, Vidya S Farook 81, Sharon P Fowler 47, Barry I Freedman 82, Michael Griswold 83, Daniel Esten Hale 73, Pamela J Hicks 51 52 53, Chiea-Chuen Khor 28 36 37 84 85, Satish Kumar 80, Benjamin Lehne 42, Dorothée Thuillier 86, Wei Yen Lim 28, Jianjun Liu 28 85, Marie Loh 42 87 88, Solomon K Musani 89, Sobha Puppala 81, William R Scott 42, Loïc Yengo 86, Sian-Tsung Tan 43 59, Herman A Taylor 79, Farook Thameem 47, Gregory Wilson 90, Tien Yin Wong 36 37 38, Pål Rasmus Njølstad 91 92, Jonathan C Levy 10, Massimo Mangino 9 93, Lori L Bonnycastle 17, Thomas Schwarzmayr 94, João Fadista 95, Gabriela L Surdulescu 9, Christian Herder 96 97, Christopher J Groves 10, Thomas Wieland 94, Jette Bork-Jensen 24, Ivan Brandslund 98 99, Cramer Christensen 100, Heikki A Koistinen 101 102 103 104, Alex S F Doney 105, Leena Kinnunen 101, Tõnu Esko 2 106 107 108, Andrew J Farmer 109, Liisa Hakaste 102 110 111, Dylan Hodgkiss 9, Jasmina Kravic 95, Valeri Lyssenko 95, Mette Hollensted 24, Marit E Jørgensen 112, Torben Jørgensen 113 114 115, Claes Ladenvall 95, Johanne Marie Justesen 24, Annemari Käräjämäki 116 117, Jennifer Kriebel 97 118 119, Wolfgang Rathmann 97 120, Lars Lannfelt 56, Torsten Lauritzen 121, Narisu Narisu 17, Allan Linneberg 113 122 123, Olle Melander 124, Lili Milani 106, Matt Neville 10 125, Marju Orho-Melander 126, Lu Qi 127 128, Qibin Qi 127 129, Michael Roden 96 97 130, Olov Rolandsson 131, Amy Swift 17, Anders H Rosengren 95, Kathleen Stirrups 11, Andrew R Wood 7, Evelin Mihailov 106, Christine Blancher 132, Mauricio O Carneiro 2, Jared Maguire 2, Ryan Poplin 2, Khalid Shakir 2, Timothy Fennell 2, Mark DePristo 2, Martin Hrabé de Angelis 97 133 134, Panos Deloukas 11 135 136, Anette P Gjesing 24, Goo Jun 3 27, Peter Nilsson 137, Jacquelyn Murphy 2, Robert Onofrio 2, Barbara Thorand 97 118, Torben Hansen 24 138, Christa Meisinger 97 118, Frank B Hu 29 127, Bo Isomaa 110 139, Fredrik Karpe 10 125, Liming Liang 18 29, Annette Peters 23 97 118, Cornelia Huth 97 118, Stephen P O'Rahilly 140, Colin N A Palmer 141, Oluf Pedersen 24, Rainer Rauramaa 142, Jaakko Tuomilehto 143 144 145 146, Veikko Salomaa 146, Richard M Watanabe 147 148 149, Ann-Christine Syvänen 150, Richard N Bergman 151, Dwaipayan Bharadwaj 152, Erwin P Bottinger 58, Yoon Shin Cho 153, Giriraj R Chandak 154, Juliana Cn Chan 65 155 156, Kee Seng Chia 28, Mark J Daly 61, Shah B Ebrahim 57, Claudia Langenberg 8, Paul Elliott 42 157, Kathleen A Jablonski 158, Donna M Lehman 47, Weiping Jia 35, Ronald C W Ma 65 155 156, Toni I Pollin 159, Manjinder Sandhu 11 64, Nikhil Tandon 160, Philippe Froguel 86 161, Inês Barroso 11 140, Yik Ying Teo 28 162 163, Eleftheria Zeggini 11, Ruth J F Loos 58, Kerrin S Small 9, Janina S Ried 20, Ralph A DeFronzo 47, Harald Grallert 97 118 119, Benjamin Glaser 164, Andres Metspalu 106, Nicholas J Wareham 8, Mark Walker 165, Eric Banks 2, Christian Gieger 20 118 119, Erik Ingelsson 4 166, Hae Kyung Im 25, Thomas Illig 119 167 168, Paul W Franks 33 127 131, Gemma Buck 132, Joseph Trakalo 132, David Buck 132, Inga Prokopenko 4 10 161, Reedik Mägi 106, Lars Lind 169, Yossi Farjoun 170, Katharine R Owen 10 125, Anna L Gloyn 4 10 125, Konstantin Strauch 20 22, Tiinamaija Tuomi 102 110 111 171, Jaspal Singh Kooner 43 59 172, Jong-Young Lee 30, Taesung Park 26 39, Peter Donnelly 4 6, Andrew D Morris 173 174, Andrew T Hattersley 175, Donald W Bowden 51 52 53, Francis S Collins 17, Gil Atzmon 44 176, John C Chambers 42 43 172, Timothy D Spector 9, Markku Laakso 49 50, Tim M Strom 94 177, Graeme I Bell 178, John Blangero 80, Ravindranath Duggirala 81, E Shyong Tai 28 74 179, Gilean McVean 4 180, Craig L Hanis 27, James G Wilson 181, Mark Seielstad 182 183, Timothy M Frayling 7, James B Meigs 184, Nancy J Cox 25, Rob Sladek 13 40 185, Eric S Lander 186, Stacey Gabriel 2, Karen L Mohlke 187, Thomas Meitinger 94 177, Leif Groop 95 171, Goncalo Abecasis 3, Laura J Scott 3, Andrew P Morris 4 106 188, Hyun Min Kang 1, David Altshuler 1 2 107 189 190 191, Noël P Burtt 2, Jose C Florez 2 62 189 190, Michael Boehnke 3, Mark I McCarthy 4 10 125

Affiliations

19 December 2017

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doi: 10.1038/sdata.2017.179


Abstract

To investigate the genetic basis of type 2 diabetes (T2D) to high resolution, the GoT2D and T2D-GENES consortia catalogued variation from whole-genome sequencing of 2,657 European individuals and exome sequencing of 12,940 individuals of multiple ancestries. Over 27M SNPs, indels, and structural variants were identified, including 99% of low-frequency (minor allele frequency [MAF] 0.1-5%) non-coding variants in the whole-genome sequenced individuals and 99.7% of low-frequency coding variants in the whole-exome sequenced individuals. Each variant was tested for association with T2D in the sequenced individuals, and, to increase power, most were tested in larger numbers of individuals (>80% of low-frequency coding variants in ~82 K Europeans via the exome chip, and ~90% of low-frequency non-coding variants in ~44 K Europeans via genotype imputation). The variants, genotypes, and association statistics from these analyses provide the largest reference to date of human genetic information relevant to T2D, for use in activities such as T2D-focused genotype imputation, functional characterization of variants or genes, and other novel analyses to detect associations between sequence variation and T2D.

Conflict of interest statement

Ralph A DeFronzo has been a member of advisory boards for Astra Zeneca, Novo Nordisk, Janssen, Lexicon, Boehringer-Ingelheim, received research support from Bristol Myers Squibb, Boehringer- Ingelheim, Takeda and Astra Zeneca, and is a member of speaker’s bureaus for Novo-Nordisk and Astra Zeneca. Jose C Florez has received consulting honoraria from Pfizer and PanGenX. Erik Ingelsson is an advisor and consultant for Precision Wellness, Inc., and advisor for Cellink for work unrelated to the present project. Mark McCarthy has received consulting and advisory board honoraria from Pfizer, Lilly, and NovoNordisk. Gilean McVean and Peter Donnelly are co-founders of Genomics PLC, which provides genome analytics.


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KMEL References


References

  1.  
    1. 2016. The European Genome-phenome Archive. EGAS00001001459
  2.  
    1. 2016. The European Genome-phenome Archive. EGAS00001001460
  3.  
    1. Altshuler D., Boehnke M., McCarthy M., Florez J. 2016. dbGAP. phs001097.v1.p1
  4.  
    1. Altshuler D., Boehnke M., McCarthy M., Florez J. 2016. dbGAP. phs001099.v1.p1
  5.  
    1. Altshuler D., Boehnke M., McCarthy M., Florez J. 2016. dbGAP. phs001098.v1.p1
  6.  
    1. Duggirala R. 2016. dbGAP. phs000849.v1.p1
  7.  
    1. Altshuler D., Boehnke M., McCarthy M., Florez J. 2016. dbGAP. phs001096.v1.p1
  8.  
    1. Altshuler D., Boehnke M., McCarthy M., Florez J. 2016. dbGAP. phs001095.v1.p1
  9.  
    1. Altshuler D., Boehnke M., McCarthy M., Florez J. 2016. dbGAP. phs001093.v1.p1
  10.  
    1. Altshuler D., Boehnke M., McCarthy M., Florez J. 2016. dbGAP. phs001100.v1.p1
  11.  
    1. Altshuler D., Boehnke M., McCarthy M., Florez J. 2016. dbGAP. phs001102.v1.p1
  12.  
    1. Altshuler D., Boehnke M., McCarthy M., Florez J. 2016. dbGAP. phs000840.v1.p1