Genome-wide association identifies nine common variants associated with fasting proinsulin levels and provides new insights into the pathophysiology of type 2 diabetes

Rona J. Strawbridge, Josée Dupuis, Inga Prokopenko, Adam Barker, Emma Ahlqvist, John R. Petrie, George V. Dedoussis, Valeriya Lyssenko, James B. Meigs, Inês Barroso, Richard M. Watanabe, Erik Ingelsson, Claudia Langenberg, Anders Hamsten, Jose C. Florez, Leif Groop, Nicholas J. Wareham, Ruth J F Loos, Nicholas J. Wareham, James B. Meigs & 922 others Jose C. Florez, George V. Dedoussis, Tom J. Forsen, Cyrus C. Cooper, Mike Boehnke, Francis S. Collins, Markku Laakso, Erik Ingelsson, Lars Lind, Robert Clarke, Maria Grazia Franzosi, Anders Hamsten, Udo Seedorf, Hugh Watkins, Ele Ferrannini, Manuel Serrano Ríos, Claes Göran Östenson, Erik Ingelsson, Leif Groop, Bo Isomaa, Tiinamaija Tuomi, Leif Groop, Bo Isomaa, Tiinamaija Tuomi, Nicholas J. Wareham, Nicholas J. Wareham, Caroline S. Fox, James B. Meigs, Stavroula Kanoni, Konstantinos Makrilakis, Tom J. Forsen, Eero Kajantie, Clive Osmond, Cyrus C. Cooper, Elaine M. Dennison, Karen A. Jameson, Avan A. Sayer, Markku Laakso, Teemu Kuulasmaa, Johanna Kuusisto, Alena Stancakova, Lars Lind, Björn Zethelius, Maria Nastase Mannila, Angela Silveira, Mark Walker, Harvest Gu, Björn Zethelius, Emma Ahlqvist, Valeriya Lyssenko, Fabiola Turrini, Valeriya Lyssenko, Nicholas J. Wareham, Inês Barroso, Claudia Langenberg, Felicity Payne, Ruth J F Loos, Nicholas J. Wareham, Claudia Langenberg, James B. Meigs, Josée Dupuis, Caroline S. Fox, Panos Deloukas, Kathy Stirrups, Inês Barroso, Claudia Langenberg, Felicity Payne, Nicholas J. Wareham, Narisu Narisu, Amy J. Swift, Ann Christine Syvänen, Ann Christine Syvänen, Laura Pascoe, Mark Walker, Ann Christine Syvänen, Emma Ahlqvist, Valeriya Lyssenko, Valeriya Lyssenko, Emma Ahlqvist, Peter Almgren, Benjamin F. Voight, Claudia Langenberg, Adam Barker, Momoko Horikoshi, Inga Prokopenko, Claudia Langenberg, Daniel Barnes, Jian'an Luan, Caroline S. Fox, Josée Dupuis, Chen Han, Alisa K. Manning, Denis Rybin, Stavroula Kanoni, Claudia Langenberg, Adam Barker, Anne U. Jackson, Richard M. Watanabe, Erik Ingelsson, Stefan Gustafsson, Anuj Goel, John Öhrvik, John F. Peden, Bengt Sennblad, Rona J. Strawbridge, Timothy M. Frayling, Michael N. Weedon, Weijia Xie, Erik Ingelsson, Stefan Gustafsson, Nabila Bouatia-Naji, Elodie Eury, Philippe Froguel, Julie Kerr-Conte, François Pattou, Anna L. Gloyn, Paul Johnson, Mary Travers, Antigone S. Dimas, Alexandra C. Nica, Emmanouil T. Dermitzakis, Per Eriksson, Lasse Folkersen, Ferdinand M. van't Hooft, Benjamin F. Voight, Laura J. Scott, Valgerdur Steinthorsdottir, Andrew P. Morris, Christian Dina, Ryan P. Welch, Eleftheria Zeggini, Cornelia Huth, Yurii S. Aulchenko, Gudmar Thorleifsson, Laura J. McCulloch, Teresa Ferreira, Harald Grallert, Najaf Amin, Guanming Wu, Cristen J. Willer, Soumya Raychaudhuri, Steve A. McCarroll, Claudia Langenberg, Oliver M. Hofmann, Josée Dupuis, Lu Qi, Ayellet V. Segrè, Mandy van Hoek, Pau Navarro, Kristin Ardlie, Beverley Balkau, Rafn Benediktsson, Amanda J. Bennett, Roza Blagieva, Eric Boerwinkle, Lori L. Bonnycastle, Kristina Bengtsson Boström, Bert Bravenboer, Suzannah Bumpstead, Noisël P. Burtt, Guillaume Charpentier, Peter S. Chines, Marilyn Cornelis, David J. Couper, Gabe Crawford, Alex S F Doney, Katherine S. Elliott, Amanda L. Elliott, Michael R. Erdos, Caroline S. Fox, Christopher S. Franklin, Martha Ganser, Christian Gieger, Niels Grarup, Todd Green, Simon Griffin, Christopher J. Groves, Candace Guiducci, Samy Hadjadj, Neelam Hassanali, Christian Herder, Bo Isomaa, Anne U. Jackson, Paul R V Johnson, Torben Jørgensen, Wen H L Kao, Norman Klopp, Augustine Kong, Peter Kraft, Torsten Lauritzen, Man Li, Aloysius Lieverse, Cecilia M. Lindgren, Valeriya Lyssenko, Michel Marre, Thomas Meitinger, Kristian Midthjell, Mario A. Morken, Narisu Narisu, Peter Nilsson, Katharine R. Owen, Felicity Payne, John R B Perry, Ann Kristin Petersen, Carl Platou, Christine Proença, Inga Prokopenko, Wolfgang Rathmann, N. William Rayner, Neil R. Robertson, Ghislain Rocheleau, Michael Roden, Michael J. Sampson, Richa Saxena, Beverley M. Shields, Peter Shrader, Gunnar Sigurdsson, Thomas Sparsø, Klaus Strassburger, Heather M. Stringham, Qi Sun, Amy J. Swift, Barbara Thorand, Jean Tichet, Tiinamaija Tuomi, Rob M. van Dam, Timon W. van Haeften, Thijs van Herpt, Jana V. van Vliet-Ostaptchouk, G. Bragi Walters, Michael N. Weedon, Cisca Wijmenga, Jacqueline Witteman, Richard N. Bergman, Stephane Cauchi, Francis S. Collins, Anna L. Gloyn, Ulf Gyllensten, Torben Hansen, Winston A. Hide, Graham A. Hitman, Albert Hofman, David J. Hunter, Kristian Hveem, Markku Laakso, Karen L. Mohlke, Andrew D. Morris, Colin N A Palmer, Peter P. Pramstaller, Igor Rudan, Eric Sijbrands, Lincoln D. Stein, Jaakko Tuomilehto, Andre Uitterlinden, Mark Walker, Nicholas J. Wareham, Richard M. Watanabe, Gonçalo R. Abecasis, Bernhard O. Boehm, Harry Campbell, Mark J. Daly, Andrew T. Hattersley, Frank B. Hu, James B. Meigs, James S. Pankow, Oluf Pedersen, H. Erich Wichmann, Inês Barroso, Jose C. Florez, Leif Groop, Rob Sladek, Unnur Thorsteinsdottir, Unnur Thorsteinsdottir, Thomas Illig, Philippe Froguel, Cornelia M. van Duijn, Kari Stefansson, David Altshuler, Michael Boehnke, Mark I. McCarthy, Elizabeth K. Speliote, Cristen J. Wille, Sonja I. Bernd, Keri L. Mond, Gudmar Thorleifsso, Anne U. Jackso, Hana Lango Allen, Cecilia M. Lindgre, Jian'an Lua, Reedik Mäg, Joshua C. Randal, Sailaja Vedanta, Thomas W. Winkle, Lu Qi, Tsegaselassie Workalemah, Iris M. Hei, Valgerdur Steinthorsdotti, Heather M. Stringha, Michael N. Weedo, Eleanor Wheele, Andrew R. Woo, Teresa Ferreir, Robert J. Weyan, Ayellet V. Segrè, Karol Estrad, Liming Lian, James Nemes, Ju Hyun Par, Stefan Gustafsso, Tuomas O. Kilpeläine, Jian Yang, Nabila Bouatia-Naji, Tõnu Esko, Mary F. Feitosa, Zoltán Kutalik, Massimo Mangino, Soumya Raychaudhuri, Andre Scherag, Albert Vernon Smith, Ryan Welch, Jing Hua Zhao, Katja K. Aben, Devin M. Absher, Najaf Amin, Anna L. Dixon, Eva Fisher, Nicole L. Glazer, Michael E. Goddard, Nancy L. Heard-Costa, Volker Hoesel, Jouke Jan Hottenga, Åsa Johansson, Toby Johnson, Shamika Ketkar, Claudia Lamina, Shengxu Li, Miriam F. Moffatt, Richard H. Myers, Narisu Narisu, John R B Perry, Marjolein J. Peters, Michael Preuss, Samuli Ripatti, Fernando Rivadeneira, Camilla Sandholt, Laura J. Scott, Nicholas J. Timpson, Jonathan P. Tyrer, Sophie van Wingerden, Richard M. Watanabe, Charles C. White, Fredrik Wiklund, Christina Barlassina, Daniel I. Chasman, Matthew N. Cooper, John Olov Jansson, Robert W. Lawrence, Niina Pellikka, Inga Prokopenko, Jianxin Shi, Elisabeth Thiering, Helene Alavere, Maria T S Alibrandi, Peter Almgren, Alice M. Arnold, Thor Aspelund, Larry D. Atwood, Beverley Balkau, Anthony J. Balmforth, Amanda J. Bennett, Yoav Ben-Shlomo, Richard N. Bergman, Sven Bergmann, Heike Biebermann, Alexandra I F Blakemore, Tanja Boes, Lori L. Bonnycastle, Stefan R. Bornstein, Morris J. Brown, Thomas A. Buchanan, Fabio Busonero, Harry Campbell, Francesco P. Cappuccio, Christine Cavalcanti-Proença, Yii Der Ida Chen, Chih Mei Chen, Peter S. Chines, Robert Clarke, Lachlan Coin, John Connell, Ian N M Day, Martin den Heijer, Jubao Duan, Shah Ebrahim, Paul Elliott, Roberto Elosua, Gudny Eiriksdottir, Michael R. Erdos, Johan G. Eriksson, Maurizio F. Facheris, Stephan B. Felix, Pamela Fischer-Posovszky, Aaron R. Folsom, Nele Friedrich, Nelson B. Freimer, Mao Fu, Stefan Gaget, Pablo V. Gejman, Eco J C Geus, Christian Gieger, Anette P. Gjesing, Anuj Goel, Philippe Goyette, Harald Grallert, Jürgen Gräßler, Danielle M. Greenawalt, Christopher J. Groves, Vilmundur Gudnason, Candace Guiducci, Anna Liisa Hartikainen, Neelam Hassanali, Alistair S. Hall, Aki S. Havulinna, Caroline Hayward, Andrew C. Heath, Christian Hengstenberg, Andrew A. Hicks, Anke Hinney, Albert Hofman, Georg Homuth, Jennie Hui, Wilmar Igl, Carlos Iribarren, Bo Isomaa, Kevin B. Jacobs, Ivonne Jarick, Elizabeth Jewell, Ulrich John, Torben Jørgensen, Pekka Jousilahti, Antti Jula, Marika Kaakinen, Eero Kajantie, Lee M. Kaplan, Sekar Kathiresan, Johannes Kettunen, Leena Kinnunen, Joshua W. Knowles, Ivana Kolcic, Inke R. König, Seppo Koskinen, Peter Kovacs, Peter Kraft, Peter Kraft, Jaana Laitinen, Olivier Lantieri, Chiara Lanzani, Lenore J. Launer, Cecile Lecoeur, Terho Lehtimäki, Guillaume Lettre, Jianjun Liu, Marja Liisa Lokki, Mattias Lorentzon, Robert N. Luben, Paolo Manunta, Barbara Ludwig, Robert C. Kaplan, Michel Marre, Nicholas G. Martin, Wendy L. McArdle, Anne McCarthy, Barbara McKnight, Thomas Meitinger, Olle Melander, David Meyre, Kristian Midthjell, Grant W. Montgomery, Mario A. Morken, Andrew P. Morris, Rosanda Mulic, Julius S. Ngwa, Mari Nelis, Matt J. Neville, Dale R. Nyholt, Christopher J. O'Donnel, Stephen O'Rahilly, Ken K. Ong, Ben Oostra, Guillaume Paré, Alex N. Parker, Markus Perola, Irene Pichler, Kirsi H. Pietiläinen, Carl G P Platou, Ozren Polasek, Anneli Pouta, Suzanne Rafelt, Olli Raitakari, Nigel W. Rayner, Martin Ridderstråel, Winfried Rief, Aimo Ruokonen, Neil R. Robertson, Peter Rzehak, Veikko Salomaa, Alan R. Sanders, Manjinder S. Sandhu, Serena Sanna, Jouko Saramies, Markku J. Savolainen, Susann Scherag, Sabine Schipf, Stefan Schreiber, Heribert Schunkert, Kaisa Silander, Juha Sinisalo, David S. Siscovick, Jan H. Smit, Nicole Soranzo, Ulla Sovio, Jonathan Stephens, Ida Surakka, Amy J. Swift, Mari Liis Tammesoo, Jean Claude Tardif, Maris Teder-Laving, Tanya M. Teslovich, John R. Thompson, Brian Thomson, Anke Tönjes, Tiinamaija Tuomi, Joyce B. van Meurs, Gert Jan van Ommen, Vincent Vatin, Jorma Viikari, Sophie Visvikis-Siest, Veronique Vitart, Carla I G Vogel, Benjamin F. Voight, Lindsay L. Waite, Henri Wallaschofski, G. Bragi Walter, Elisabeth Widen, Susanna Wiegand, Sarah H. Wild, Gonneke Willemsen, Daniel R. Witte, Jacqueline C. Witteman, Jianfeng Xu, Qunyuan Zhang, Lina Zgaga, Andreas Ziegler, Paavo Zitting, John P. Beilby, I. Sadaf Farooqi, Johannes Hebebrand, Heikki V. Huikuri, Alan L. James, Mika Kähönen, Douglas F. Levinson, Fabio Macciardi, Markku S. Nieminen, Claes Ohlsson, Lyle J. Palmer, Paul M. Ridker, Michael Stumvoll, Jacques S. Beckmann, Heiner Boeing, Eric Boerwinkle, Dorret I. Boomsma, Mark J. Caulfield, Stephen J. Chanock, Francis S. Collins, L. Adrienne Cupples, George Davey Smith, Jeanette Erdmann, Philippe Froguel, Henrik Grönberg, Ulf Gyllensten, Per Hall, Torben Hansen, Tamara B. Harris, Andrew T. Hattersley, Richard B. Hayes, Joachim Heinrich, Frank B. Hu, Frank B. Hu, Thomas Illig, Marjo Riitta Jarvelin, Jaakko Kaprio, Fredrik Karpe, Kay Tee Khaw, Lambertus A. Kiemeney, Heiko Krude, Markku Laakso, Debbie A. Lawlor, Andres Metspalu, Patricia B. Munroe, Willem H. Ouwehand, Oluf Pedersen, Brenda W. Penninx, Annette Peters, Peter P. Pramstaller, Thomas Quertermous, Thomas Reinehr, Aila Rissanen, Igor Rudan, Nilesh J. Samani, Peter E H Schwarz, Alan R. Shuldiner, Timothy D. Spector, Jaakko Tuomilehto, Manuela Uda, André Uitterlinden, Timo T. Valle, Martin Wabitsch, Gérard Waeber, Nicholas J. Wareham, Hugh Watkins, James F. Wilson, Alan F. Wright, M. Carola Zillikens, Nilanjan Chatterjee, Steven A. McCarroll, Shaun Purcell, Eric E. Schadt, Peter M. Visscher, Themistocles L. Assimes, Ingrid B. Borecki, Panos Deloukas, Caroline S. Fox, Leif C. Groop, Talin Haritunians, David J. Hunter, Robert C. Kaplan, Karen L. Mohlke, Jeffrey R. O'Connell, Leena Peltonen, David Schlessinger, David P. Strachan, Cornelia M. van Duijn, H. Erich Wichmann, Unnur Thorsteinsdottir, Gonçalo R. Abecasis, Inês Barroso, Michael Boehnke, Kari Stefansson, Kari E. North, Mark I. McCarthy, Joel N. Hirschhorn, Erik Ingelsson, Ruth J F Loos, Alexandra C. Nica, Leopold Parts, Daniel Glass, James Nisbet, Amy Barrett, Magdalena Sekowska, Mary Travers, Simon Potter, Elin Grundberg, Kerrin Small, Åsa K. Hedman, Veronique Bataille, Jordana Tzenova Bell, Gabriela Surdulescu, Antigone S. Dimas, Catherine Ingle, Frank O. Nestle, Paola di Meglio, Josine L. Min, Alicja Wilk, Christopher J. Hammond, Neelam Hassanali, Tsun Po Yang, Stephen B. Montgomery, Steve O'Rahilly, Cecilia M. Lindgren, Krina T. Zondervan, Nicole Soranzo, Inês Barroso, Richard Durbin, Kourosh Ahmadi, Panos Deloukas, Mark I. McCarthy, Emmanouil T. Dermitzakis, Timothy D. Spector, Heribert Schunkert, Inke R. König, Sekar Kathiresan, Muredach P. Reilly, Themistocles L. Assimes, Hilma Holm, Michael Preuss, Alexandre F R Stewart, Maja Barbalic, Christian Gieger, Devin Absher, Zouhair Aherrahrou, Hooman Allayee, David Altshuler, Sonia S. Anand, Karl Andersen, Jeffrey L. Anderson, Diego Ardissino, Stephen G. Ball, Anthony J. Balmforth, Timothy A. Barnes, Diane M. Becker, Lewis C. 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Lotery, Pier M. Mannucci, Seraya Maouche, Nicola Martinelli, Pascal P. McKeown, Christa Meisinger, Thomas Meitinger, Olle Melander, Pier Angelica Merlini, Vincent Mooser, Thomas Morgan, Thomas W. Mühleisen, Joseph B. Muhlestein, Thomas Münzel, Kiran Musunuru, Janja Nahrstaedt, Christopher P. Nelson, Markus M. Nöthen, Oliviero Olivieri, Riyaz S. Patel, Chris C. Patterson, Annette Peters, Flora Peyvandi, Liming Qu, Arshed A. Quyyumi, Daniel J. Rader, Loukianos S. Rallidis, Catherine Rice, Frits R. Rosendaal, Diana Rubin, Veikko Salomaa, M. Lourdes Sampietro, Manj S. Sandhu, Eric Schadt, Arne Schäfer, Arne Schillert, Stefan Schreiber, Jürgen Schrezenmeir, Stephen M. Schwartz, David S. Siscovick, Mohan Sivananthan, Suthesh Sivapalaratnam, Albert Smith, Tamara B. Smith, Jaapjan D. Snoep, Nicole Soranzo, John A. Spertus, Klaus Stark, Kathy Stirrups, Monika Stoll, W. H Wilson Tang, Stephanie Tennstedt, Gudmundur Thorgeirsson, Gudmar Thorleifsson, Maciej Tomaszewski, Andre G. Uitterlinden, Andre M. van Rij, Benjamin F. Voight, Nick J. Wareham, George A. Wells, H. Erich Wichmann, Philipp S. Wild, Christina Willenborg, Jaqueline C M Witteman, Benjamin J. Wright, Shu Ye, Tanja Zeller, Andreas Ziegler, Francois Cambien, Alison H. Goodall, L. Adrienne Cupples, Thomas Quertermous, Winfried März, Christian Hengstenberg, Stefan Blankenberg, Willem H. Ouwehand, Alistair S. Hall, Panos Deloukas, John R. Thompson, Kari Stefansson, Robert Roberts, Unnur Thorsteinsdottir, Christopher J. O'Donnell, Ruth McPherson, Jeanette Erdmann, Nilesh J. Samani, Jemma C. Hopewell, Sarah Parish, Alison Offer, Robert Clarke, Louise Bowman, Peter Sleight, Jane Armitage, Richard Peto, Rory Collins, John C. Chambers, Goncalo Abecasis, Nabeel Ahmed, Mark Caulfield, Peter Donnelly, Paul Elliott, Philippe Froguel, Angad S. Kooner, Mark McCarthy, Nilesh Samani, James Scott, Joban Sehmi, Weihua Zhang, Jaspal S. Kooner, Rona Strawbridge, Maria Sabater-Lleal, Anders Mälarstig, Bengt Sennblad, John Öhrvik, Angela Silveira, Ferdinand van't Hooft, Per Eriksson, Anders Hamsten, Mai Lis Hellénius, Gunnar Olsson, Stephan Rust, Gerd Assmann, Udo Seedorf, Simona Barlera, Maria Grazia Franzosi, Gianni Tognoni, Robert Clarke, Pamela Linksted, Jemma C. Hopewell, Rory Collins, John F. Peden, Anuj Goel, Halit Ongen, Theodosios Kyriakou, Fiona Green, Martin Farrall, Hugh Watkins, Danish Saleheen, Asif Rasheed, Moazzam Zaidi, Nabi Shah, Maria Samuel, Nadeem Mallick, Muhammad Azhar, Khan Shah Zaman, Adbus Samad, Muhammad Ishaq, Ali Gardezi, Fazal ur Rehman Memon, Nilesh Samani, Philippe Frossard, Panos Deloukas, John Danesh

Research output: Contribution to journalArticle

201 Citations (Scopus)

Abstract

OBJECTIVE - Proinsulin is a precursor of mature insulin and C-peptide. Higher circulating proinsulin levels are associated with impaired b-cell function, raised glucose levels, insulin resistance, and type 2 diabetes (T2D). Studies of the insulin processing pathway could provide new insights about T2D pathophysiology. RESEARCH DESIGN AND METHODS - We have conducted a meta-analysis of genome-wide association tests of ;2.5 million genotyped or imputed single nucleotide polymorphisms (SNPs) and fasting proinsulin levels in 10,701 nondiabetic adults of European ancestry, with follow-up of 23 loci in up to 16,378 individuals, using additive genetic models adjusted for age, sex, fasting insulin, and study-specific covariates. RESULTS - Nine SNPs at eight loci were associated with proinsulin levels (P < 5 × 10<sup>-8</sup>). Two loci (LARP6 and SGSM2) have not been previously related to metabolic traits, one (MADD) has been associated with fasting glucose, one (PCSK1) has been implicated in obesity, and four (TCF7L2, SLC30A8, VPS13C/ C2CD4A/B, and ARAP1, formerly CENTD2) increase T2D risk. The proinsulin-raising allele of ARAP1 was associated with a lower fasting glucose (P = 1.7 3 10<sup>-4</sup>), improved b-cell function (P = 1.1 × 10<sup>-5</sup>), and lower risk of T2D (odds ratio 0.88; P = 7.8 × 10<sup>-6</sup>). Notably, PCSK1 encodes the protein prohormone convertase 1/3, the first enzyme in the insulin processing pathway. A genotype score composed of the nine proinsulin-raising alleles was not associated with coronary disease in two large case-control datasets. CONCLUSIONS - We have identified nine genetic variants associated with fasting proinsulin. Our findings illuminate the biology underlying glucose homeostasis and T2D development in humans and argue against a direct role of proinsulin in coronary artery disease pathogenesis.

Original languageEnglish (US)
Pages (from-to)2624-2634
Number of pages11
JournalDiabetes
Volume60
Issue number10
DOIs
StatePublished - Oct 1 2011

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Proinsulin
Type 2 Diabetes Mellitus
Fasting
Genome
Proprotein Convertase 1
Insulin
Glucose
Single Nucleotide Polymorphism
Alleles
C-Peptide
Genetic Models
Human Development
Coronary Disease
Insulin Resistance
Meta-Analysis
Coronary Artery Disease
Homeostasis
Research Design
Obesity
Odds Ratio

ASJC Scopus subject areas

  • Internal Medicine
  • Endocrinology, Diabetes and Metabolism

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Genome-wide association identifies nine common variants associated with fasting proinsulin levels and provides new insights into the pathophysiology of type 2 diabetes. / Strawbridge, Rona J.; Dupuis, Josée; Prokopenko, Inga; Barker, Adam; Ahlqvist, Emma; Petrie, John R.; Dedoussis, George V.; Lyssenko, Valeriya; Meigs, James B.; Barroso, Inês; Watanabe, Richard M.; Ingelsson, Erik; Langenberg, Claudia; Hamsten, Anders; Florez, Jose C.; Groop, Leif; Wareham, Nicholas J.; Loos, Ruth J F; Wareham, Nicholas J.; Meigs, James B.; Florez, Jose C.; Dedoussis, George V.; Forsen, Tom J.; Cooper, Cyrus C.; Boehnke, Mike; Collins, Francis S.; Laakso, Markku; Ingelsson, Erik; Lind, Lars; Clarke, Robert; Franzosi, Maria Grazia; Hamsten, Anders; Seedorf, Udo; Watkins, Hugh; Ferrannini, Ele; Ríos, Manuel Serrano; Östenson, Claes Göran; Ingelsson, Erik; Groop, Leif; Isomaa, Bo; Tuomi, Tiinamaija; Groop, Leif; Isomaa, Bo; Tuomi, Tiinamaija; Wareham, Nicholas J.; Wareham, Nicholas J.; Fox, Caroline S.; Meigs, James B.; Kanoni, Stavroula; Makrilakis, Konstantinos; Forsen, Tom J.; Kajantie, Eero; Osmond, Clive; Cooper, Cyrus C.; Dennison, Elaine M.; Jameson, Karen A.; Sayer, Avan A.; Laakso, Markku; Kuulasmaa, Teemu; Kuusisto, Johanna; Stancakova, Alena; Lind, Lars; Zethelius, Björn; Mannila, Maria Nastase; Silveira, Angela; Walker, Mark; Gu, Harvest; Zethelius, Björn; Ahlqvist, Emma; Lyssenko, Valeriya; Turrini, Fabiola; Lyssenko, Valeriya; Wareham, Nicholas J.; Barroso, Inês; Langenberg, Claudia; Payne, Felicity; Loos, Ruth J F; Wareham, Nicholas J.; Langenberg, Claudia; Meigs, James B.; Dupuis, Josée; Fox, Caroline S.; Deloukas, Panos; Stirrups, Kathy; Barroso, Inês; Langenberg, Claudia; Payne, Felicity; Wareham, Nicholas J.; Narisu, Narisu; Swift, Amy J.; Syvänen, Ann Christine; Syvänen, Ann Christine; Pascoe, Laura; Walker, Mark; Syvänen, Ann Christine; Ahlqvist, Emma; Lyssenko, Valeriya; Lyssenko, Valeriya; Ahlqvist, Emma; Almgren, Peter; Voight, Benjamin F.; Langenberg, Claudia; Barker, Adam; Horikoshi, Momoko; Prokopenko, Inga; Langenberg, Claudia; Barnes, Daniel; Luan, Jian'an; Fox, Caroline S.; Dupuis, Josée; Han, Chen; Manning, Alisa K.; Rybin, Denis; Kanoni, Stavroula; Langenberg, Claudia; Barker, Adam; Jackson, Anne U.; Watanabe, Richard M.; Ingelsson, Erik; Gustafsson, Stefan; Goel, Anuj; Öhrvik, John; Peden, John F.; Sennblad, Bengt; Strawbridge, Rona J.; Frayling, Timothy M.; Weedon, Michael N.; Xie, Weijia; Ingelsson, Erik; Gustafsson, Stefan; Bouatia-Naji, Nabila; Eury, Elodie; Froguel, Philippe; Kerr-Conte, Julie; Pattou, François; Gloyn, Anna L.; Johnson, Paul; Travers, Mary; Dimas, Antigone S.; Nica, Alexandra C.; Dermitzakis, Emmanouil T.; Eriksson, Per; Folkersen, Lasse; van't Hooft, Ferdinand M.; Voight, Benjamin F.; Scott, Laura J.; Steinthorsdottir, Valgerdur; Morris, Andrew P.; Dina, Christian; Welch, Ryan P.; Zeggini, Eleftheria; Huth, Cornelia; Aulchenko, Yurii S.; Thorleifsson, Gudmar; McCulloch, Laura J.; Ferreira, Teresa; Grallert, Harald; Amin, Najaf; Wu, Guanming; Willer, Cristen J.; Raychaudhuri, Soumya; McCarroll, Steve A.; Langenberg, Claudia; Hofmann, Oliver M.; Dupuis, Josée; Qi, Lu; Segrè, Ayellet V.; van Hoek, Mandy; Navarro, Pau; Ardlie, Kristin; Balkau, Beverley; Benediktsson, Rafn; Bennett, Amanda J.; Blagieva, Roza; Boerwinkle, Eric; Bonnycastle, Lori L.; Boström, Kristina Bengtsson; Bravenboer, Bert; Bumpstead, Suzannah; Burtt, Noisël P.; Charpentier, Guillaume; Chines, Peter S.; Cornelis, Marilyn; Couper, David J.; Crawford, Gabe; Doney, Alex S F; Elliott, Katherine S.; Elliott, Amanda L.; Erdos, Michael R.; Fox, Caroline S.; Franklin, Christopher S.; Ganser, Martha; Gieger, Christian; Grarup, Niels; Green, Todd; Griffin, Simon; Groves, Christopher J.; Guiducci, Candace; Hadjadj, Samy; Hassanali, Neelam; Herder, Christian; Isomaa, Bo; Jackson, Anne U.; Johnson, Paul R V; Jørgensen, Torben; Kao, Wen H L; Klopp, Norman; Kong, Augustine; Kraft, Peter; Lauritzen, Torsten; Li, Man; Lieverse, Aloysius; Lindgren, Cecilia M.; Lyssenko, Valeriya; Marre, Michel; Meitinger, Thomas; Midthjell, Kristian; Morken, Mario A.; Narisu, Narisu; Nilsson, Peter; Owen, Katharine R.; Payne, Felicity; Perry, John R B; Petersen, Ann Kristin; Platou, Carl; Proença, Christine; Prokopenko, Inga; Rathmann, Wolfgang; Rayner, N. William; Robertson, Neil R.; Rocheleau, Ghislain; Roden, Michael; Sampson, Michael J.; Saxena, Richa; Shields, Beverley M.; Shrader, Peter; Sigurdsson, Gunnar; Sparsø, Thomas; Strassburger, Klaus; Stringham, Heather M.; Sun, Qi; Swift, Amy J.; Thorand, Barbara; Tichet, Jean; Tuomi, Tiinamaija; van Dam, Rob M.; van Haeften, Timon W.; van Herpt, Thijs; van Vliet-Ostaptchouk, Jana V.; Bragi Walters, G.; Weedon, Michael N.; Wijmenga, Cisca; Witteman, Jacqueline; Bergman, Richard N.; Cauchi, Stephane; Collins, Francis S.; Gloyn, Anna L.; Gyllensten, Ulf; Hansen, Torben; Hide, Winston A.; Hitman, Graham A.; Hofman, Albert; Hunter, David J.; Hveem, Kristian; Laakso, Markku; Mohlke, Karen L.; Morris, Andrew D.; Palmer, Colin N A; Pramstaller, Peter P.; Rudan, Igor; Sijbrands, Eric; Stein, Lincoln D.; Tuomilehto, Jaakko; Uitterlinden, Andre; Walker, Mark; Wareham, Nicholas J.; Watanabe, Richard M.; Abecasis, Gonçalo R.; Boehm, Bernhard O.; Campbell, Harry; Daly, Mark J.; Hattersley, Andrew T.; Hu, Frank B.; Meigs, James B.; Pankow, James S.; Pedersen, Oluf; Wichmann, H. 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Bragi; Widen, Elisabeth; Wiegand, Susanna; Wild, Sarah H.; Willemsen, Gonneke; Witte, Daniel R.; Witteman, Jacqueline C.; Xu, Jianfeng; Zhang, Qunyuan; Zgaga, Lina; Ziegler, Andreas; Zitting, Paavo; Beilby, John P.; Farooqi, I. Sadaf; Hebebrand, Johannes; Huikuri, Heikki V.; James, Alan L.; Kähönen, Mika; Levinson, Douglas F.; Macciardi, Fabio; Nieminen, Markku S.; Ohlsson, Claes; Palmer, Lyle J.; Ridker, Paul M.; Stumvoll, Michael; Beckmann, Jacques S.; Boeing, Heiner; Boerwinkle, Eric; Boomsma, Dorret I.; Caulfield, Mark J.; Chanock, Stephen J.; Collins, Francis S.; Cupples, L. Adrienne; Smith, George Davey; Erdmann, Jeanette; Froguel, Philippe; Grönberg, Henrik; Gyllensten, Ulf; Hall, Per; Hansen, Torben; Harris, Tamara B.; Hattersley, Andrew T.; Hayes, Richard B.; Heinrich, Joachim; Hu, Frank B.; Hu, Frank B.; Illig, Thomas; Jarvelin, Marjo Riitta; Kaprio, Jaakko; Karpe, Fredrik; Khaw, Kay Tee; Kiemeney, Lambertus A.; Krude, Heiko; Laakso, Markku; Lawlor, Debbie A.; Metspalu, Andres; Munroe, Patricia B.; Ouwehand, Willem H.; Pedersen, Oluf; Penninx, Brenda W.; Peters, Annette; Pramstaller, Peter P.; Quertermous, Thomas; Reinehr, Thomas; Rissanen, Aila; Rudan, Igor; Samani, Nilesh J.; Schwarz, Peter E H; Shuldiner, Alan R.; Spector, Timothy D.; Tuomilehto, Jaakko; Uda, Manuela; Uitterlinden, André; Valle, Timo T.; Wabitsch, Martin; Waeber, Gérard; Wareham, Nicholas J.; Watkins, Hugh; Wilson, James F.; Wright, Alan F.; Zillikens, M. Carola; Chatterjee, Nilanjan; McCarroll, Steven A.; Purcell, Shaun; Schadt, Eric E.; Visscher, Peter M.; Assimes, Themistocles L.; Borecki, Ingrid B.; Deloukas, Panos; Fox, Caroline S.; Groop, Leif C.; Haritunians, Talin; Hunter, David J.; Kaplan, Robert C.; Mohlke, Karen L.; O'Connell, Jeffrey R.; Peltonen, Leena; Schlessinger, David; Strachan, David P.; van Duijn, Cornelia M.; Wichmann, H. Erich; Thorsteinsdottir, Unnur; Abecasis, Gonçalo R.; Barroso, Inês; Boehnke, Michael; Stefansson, Kari; North, Kari E.; McCarthy, Mark I.; Hirschhorn, Joel N.; Ingelsson, Erik; Loos, Ruth J F; Nica, Alexandra C.; Parts, Leopold; Glass, Daniel; Nisbet, James; Barrett, Amy; Sekowska, Magdalena; Travers, Mary; Potter, Simon; Grundberg, Elin; Small, Kerrin; Hedman, Åsa K.; Bataille, Veronique; Tzenova Bell, Jordana; Surdulescu, Gabriela; Dimas, Antigone S.; Ingle, Catherine; Nestle, Frank O.; di Meglio, Paola; Min, Josine L.; Wilk, Alicja; Hammond, Christopher J.; Hassanali, Neelam; Yang, Tsun Po; Montgomery, Stephen B.; O'Rahilly, Steve; Lindgren, Cecilia M.; Zondervan, Krina T.; Soranzo, Nicole; Barroso, Inês; Durbin, Richard; Ahmadi, Kourosh; Deloukas, Panos; McCarthy, Mark I.; Dermitzakis, Emmanouil T.; Spector, Timothy D.; Schunkert, Heribert; König, Inke R.; Kathiresan, Sekar; Reilly, Muredach P.; Assimes, Themistocles L.; Holm, Hilma; Preuss, Michael; Stewart, Alexandre F R; Barbalic, Maja; Gieger, Christian; Absher, Devin; Aherrahrou, Zouhair; Allayee, Hooman; Altshuler, David; Anand, Sonia S.; Andersen, Karl; Anderson, Jeffrey L.; Ardissino, Diego; Ball, Stephen G.; Balmforth, Anthony J.; Barnes, Timothy A.; Becker, Diane M.; Becker, Lewis C.; Berger, Klaus; Bis, Joshua C.; Boekholdt, S. Matthijs; Boerwinkle, Eric; Braund, Peter S.; Brown, Morris J.; Burnett, Mary Susan; Buysschaert, Ian; Carlquist, John F.; Chen, Li; Cichon, Sven; Codd, Veryan; Davies, Robert W.; Dedoussis, George; Dehghan, Abbas; Demissie, Serkalem; Devaney, Joseph M.; Diemert, Patrick; Do, Ron; Doering, Angela; Eifert, Sandra; El Mokhtari, Nour Eddine; Ellis, Stephen G.; Elosua, Roberto; Engert, James C.; Epstein, Stephen E.; de Faire, Ulf; Fischer, Marcus; Folsom, Aaron R.; Freyer, Jennifer; Gigante, Bruna; Girelli, Domenico; Gretarsdottir, Solveig; Gudnason, Vilmundur; Gulcher, Jeffrey R.; Halperin, Eran; Hammond, Naomi; Hazen, Stanley L.; Hofman, Albert; Horne, Benjamin D.; Illig, Thomas; Iribarren, Carlos; Jones, Gregory T.; Jukema, J. Wouter; Kaiser, Michael A.; Kaplan, Lee M.; Kastelein, John J P; Khaw, Kay Tee; Knowles, Joshua W.; Kolovou, Genovefa; Kong, Augustine; Laaksonen, Reijo; Lambrechts, Diether; Leander, Karin; Lettre, Guillaume; Li, Mingyao; Lieb, Wolfgang; Loley, Christina; Lotery, Andrew J.; Mannucci, Pier M.; Maouche, Seraya; Martinelli, Nicola; McKeown, Pascal P.; Meisinger, Christa; Meitinger, Thomas; Melander, Olle; Merlini, Pier Angelica; Mooser, Vincent; Morgan, Thomas; Mühleisen, Thomas W.; Muhlestein, Joseph B.; Münzel, Thomas; Musunuru, Kiran; Nahrstaedt, Janja; Nelson, Christopher P.; Nöthen, Markus M.; Olivieri, Oliviero; Patel, Riyaz S.; Patterson, Chris C.; Peters, Annette; Peyvandi, Flora; Qu, Liming; Quyyumi, Arshed A.; Rader, Daniel J.; Rallidis, Loukianos S.; Rice, Catherine; Rosendaal, Frits R.; Rubin, Diana; Salomaa, Veikko; Sampietro, M. Lourdes; Sandhu, Manj S.; Schadt, Eric; Schäfer, Arne; Schillert, Arne; Schreiber, Stefan; Schrezenmeir, Jürgen; Schwartz, Stephen M.; Siscovick, David S.; Sivananthan, Mohan; Sivapalaratnam, Suthesh; Smith, Albert; Smith, Tamara B.; Snoep, Jaapjan D.; Soranzo, Nicole; Spertus, John A.; Stark, Klaus; Stirrups, Kathy; Stoll, Monika; Tang, W. H Wilson; Tennstedt, Stephanie; Thorgeirsson, Gudmundur; Thorleifsson, Gudmar; Tomaszewski, Maciej; Uitterlinden, Andre G.; van Rij, Andre M.; Voight, Benjamin F.; Wareham, Nick J.; Wells, George A.; Wichmann, H. Erich; Wild, Philipp S.; Willenborg, Christina; Witteman, Jaqueline C M; Wright, Benjamin J.; Ye, Shu; Zeller, Tanja; Ziegler, Andreas; Cambien, Francois; Goodall, Alison H.; Cupples, L. Adrienne; Quertermous, Thomas; März, Winfried; Hengstenberg, Christian; Blankenberg, Stefan; Ouwehand, Willem H.; Hall, Alistair S.; Deloukas, Panos; Thompson, John R.; Stefansson, Kari; Roberts, Robert; Thorsteinsdottir, Unnur; O'Donnell, Christopher J.; McPherson, Ruth; Erdmann, Jeanette; Samani, Nilesh J.; Hopewell, Jemma C.; Parish, Sarah; Offer, Alison; Clarke, Robert; Bowman, Louise; Sleight, Peter; Armitage, Jane; Peto, Richard; Collins, Rory; Chambers, John C.; Abecasis, Goncalo; Ahmed, Nabeel; Caulfield, Mark; Donnelly, Peter; Elliott, Paul; Froguel, Philippe; Kooner, Angad S.; McCarthy, Mark; Samani, Nilesh; Scott, James; Sehmi, Joban; Zhang, Weihua; Kooner, Jaspal S.; Strawbridge, Rona; Sabater-Lleal, Maria; Mälarstig, Anders; Sennblad, Bengt; Öhrvik, John; Silveira, Angela; van't Hooft, Ferdinand; Eriksson, Per; Hamsten, Anders; Hellénius, Mai Lis; Olsson, Gunnar; Rust, Stephan; Assmann, Gerd; Seedorf, Udo; Barlera, Simona; Franzosi, Maria Grazia; Tognoni, Gianni; Clarke, Robert; Linksted, Pamela; Hopewell, Jemma C.; Collins, Rory; Peden, John F.; Goel, Anuj; Ongen, Halit; Kyriakou, Theodosios; Green, Fiona; Farrall, Martin; Watkins, Hugh; Saleheen, Danish; Rasheed, Asif; Zaidi, Moazzam; Shah, Nabi; Samuel, Maria; Mallick, Nadeem; Azhar, Muhammad; Zaman, Khan Shah; Samad, Adbus; Ishaq, Muhammad; Gardezi, Ali; Memon, Fazal ur Rehman; Samani, Nilesh; Frossard, Philippe; Deloukas, Panos; Danesh, John.

In: Diabetes, Vol. 60, No. 10, 01.10.2011, p. 2624-2634.

Research output: Contribution to journalArticle

Strawbridge, RJ, Dupuis, J, Prokopenko, I, Barker, A, Ahlqvist, E, Petrie, JR, Dedoussis, GV, Lyssenko, V, Meigs, JB, Barroso, I, Watanabe, RM, Ingelsson, E, Langenberg, C, Hamsten, A, Florez, JC, Groop, L, Wareham, NJ, Loos, RJF, Wareham, NJ, Meigs, JB, Florez, JC, Dedoussis, GV, Forsen, TJ, Cooper, CC, Boehnke, M, Collins, FS, Laakso, M, Ingelsson, E, Lind, L, Clarke, R, Franzosi, MG, Hamsten, A, Seedorf, U, Watkins, H, Ferrannini, E, Ríos, MS, Östenson, CG, Ingelsson, E, Groop, L, Isomaa, B, Tuomi, T, Groop, L, Isomaa, B, Tuomi, T, Wareham, NJ, Wareham, NJ, Fox, CS, Meigs, JB, Kanoni, S, Makrilakis, K, Forsen, TJ, Kajantie, E, Osmond, C, Cooper, CC, Dennison, EM, Jameson, KA, Sayer, AA, Laakso, M, Kuulasmaa, T, Kuusisto, J, Stancakova, A, Lind, L, Zethelius, B, Mannila, MN, Silveira, A, Walker, M, Gu, H, Zethelius, B, Ahlqvist, E, Lyssenko, V, Turrini, F, Lyssenko, V, Wareham, NJ, Barroso, I, Langenberg, C, Payne, F, Loos, RJF, Wareham, NJ, Langenberg, C, Meigs, JB, Dupuis, J, Fox, CS, Deloukas, P, Stirrups, K, Barroso, I, Langenberg, C, Payne, F, Wareham, NJ, Narisu, N, Swift, AJ, Syvänen, AC, Syvänen, AC, Pascoe, L, Walker, M, Syvänen, AC, Ahlqvist, E, Lyssenko, V, Lyssenko, V, Ahlqvist, E, Almgren, P, Voight, BF, Langenberg, C, Barker, A, Horikoshi, M, Prokopenko, I, Langenberg, C, Barnes, D, Luan, J, Fox, CS, Dupuis, J, Han, C, Manning, AK, Rybin, D, Kanoni, S, Langenberg, C, Barker, A, Jackson, AU, Watanabe, RM, Ingelsson, E, Gustafsson, S, Goel, A, Öhrvik, J, Peden, JF, Sennblad, B, Strawbridge, RJ, Frayling, TM, Weedon, MN, Xie, W, Ingelsson, E, Gustafsson, S, Bouatia-Naji, N, Eury, E, Froguel, P, Kerr-Conte, J, Pattou, F, Gloyn, AL, Johnson, P, Travers, M, Dimas, AS, Nica, AC, Dermitzakis, ET, Eriksson, P, Folkersen, L, van't Hooft, FM, Voight, BF, Scott, LJ, Steinthorsdottir, V, Morris, AP, Dina, C, Welch, RP, Zeggini, E, Huth, C, Aulchenko, YS, Thorleifsson, G, McCulloch, LJ, Ferreira, T, Grallert, H, Amin, N, Wu, G, Willer, CJ, Raychaudhuri, S, 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In: Diabetes. 2011 ; Vol. 60, No. 10. pp. 2624-2634.
@article{757f037bf5d94cb1adfa24fcca6494b0,
title = "Genome-wide association identifies nine common variants associated with fasting proinsulin levels and provides new insights into the pathophysiology of type 2 diabetes",
abstract = "OBJECTIVE - Proinsulin is a precursor of mature insulin and C-peptide. Higher circulating proinsulin levels are associated with impaired b-cell function, raised glucose levels, insulin resistance, and type 2 diabetes (T2D). Studies of the insulin processing pathway could provide new insights about T2D pathophysiology. RESEARCH DESIGN AND METHODS - We have conducted a meta-analysis of genome-wide association tests of ;2.5 million genotyped or imputed single nucleotide polymorphisms (SNPs) and fasting proinsulin levels in 10,701 nondiabetic adults of European ancestry, with follow-up of 23 loci in up to 16,378 individuals, using additive genetic models adjusted for age, sex, fasting insulin, and study-specific covariates. RESULTS - Nine SNPs at eight loci were associated with proinsulin levels (P < 5 × 10-8). Two loci (LARP6 and SGSM2) have not been previously related to metabolic traits, one (MADD) has been associated with fasting glucose, one (PCSK1) has been implicated in obesity, and four (TCF7L2, SLC30A8, VPS13C/ C2CD4A/B, and ARAP1, formerly CENTD2) increase T2D risk. The proinsulin-raising allele of ARAP1 was associated with a lower fasting glucose (P = 1.7 3 10-4), improved b-cell function (P = 1.1 × 10-5), and lower risk of T2D (odds ratio 0.88; P = 7.8 × 10-6). Notably, PCSK1 encodes the protein prohormone convertase 1/3, the first enzyme in the insulin processing pathway. A genotype score composed of the nine proinsulin-raising alleles was not associated with coronary disease in two large case-control datasets. CONCLUSIONS - We have identified nine genetic variants associated with fasting proinsulin. Our findings illuminate the biology underlying glucose homeostasis and T2D development in humans and argue against a direct role of proinsulin in coronary artery disease pathogenesis.",
author = "Strawbridge, {Rona J.} and Jos{\'e}e Dupuis and Inga Prokopenko and Adam Barker and Emma Ahlqvist and Petrie, {John R.} and Dedoussis, {George V.} and Valeriya Lyssenko and Meigs, {James B.} and In{\^e}s Barroso and Watanabe, {Richard M.} and Erik Ingelsson and Claudia Langenberg and Anders Hamsten and Florez, {Jose C.} and Leif Groop and Wareham, {Nicholas J.} and Loos, {Ruth J F} and Wareham, {Nicholas J.} and Meigs, {James B.} and Florez, {Jose C.} and Dedoussis, {George V.} and Forsen, {Tom J.} and Cooper, {Cyrus C.} and Mike Boehnke and Collins, {Francis S.} and Markku Laakso and Erik Ingelsson and Lars Lind and Robert Clarke and Franzosi, {Maria Grazia} and Anders Hamsten and Udo Seedorf and Hugh Watkins and Ele Ferrannini and R{\'i}os, {Manuel Serrano} and {\"O}stenson, {Claes G{\"o}ran} and Erik Ingelsson and Leif Groop and Bo Isomaa and Tiinamaija Tuomi and Leif Groop and Bo Isomaa and Tiinamaija Tuomi and Wareham, {Nicholas J.} and Wareham, {Nicholas J.} and Fox, {Caroline S.} and Meigs, {James B.} and Stavroula Kanoni and Konstantinos Makrilakis and Forsen, {Tom J.} and Eero Kajantie and Clive Osmond and Cooper, {Cyrus C.} and Dennison, {Elaine M.} and Jameson, {Karen A.} and Sayer, {Avan A.} and Markku Laakso and Teemu Kuulasmaa and Johanna Kuusisto and Alena Stancakova and Lars Lind and Bj{\"o}rn Zethelius and Mannila, {Maria Nastase} and Angela Silveira and Mark Walker and Harvest Gu and Bj{\"o}rn Zethelius and Emma Ahlqvist and Valeriya Lyssenko and Fabiola Turrini and Valeriya Lyssenko and Wareham, {Nicholas J.} and In{\^e}s Barroso and Claudia Langenberg and Felicity Payne and Loos, {Ruth J F} and Wareham, {Nicholas J.} and Claudia Langenberg and Meigs, {James B.} and Jos{\'e}e Dupuis and Fox, {Caroline S.} and Panos Deloukas and Kathy Stirrups and In{\^e}s Barroso and Claudia Langenberg and Felicity Payne and Wareham, {Nicholas J.} and Narisu Narisu and Swift, {Amy J.} and Syv{\"a}nen, {Ann Christine} and Syv{\"a}nen, {Ann Christine} and Laura Pascoe and Mark Walker and Syv{\"a}nen, {Ann Christine} and Emma Ahlqvist and Valeriya Lyssenko and Valeriya Lyssenko and Emma Ahlqvist and Peter Almgren and Voight, {Benjamin F.} and Claudia Langenberg and Adam Barker and Momoko Horikoshi and Inga Prokopenko and Claudia Langenberg and Daniel Barnes and Jian'an Luan and Fox, {Caroline S.} and Jos{\'e}e Dupuis and Chen Han and Manning, {Alisa K.} and Denis Rybin and Stavroula Kanoni and Claudia Langenberg and Adam Barker and Jackson, {Anne U.} and Watanabe, {Richard M.} and Erik Ingelsson and Stefan Gustafsson and Anuj Goel and John {\"O}hrvik and Peden, {John F.} and Bengt Sennblad and Strawbridge, {Rona J.} and Frayling, {Timothy M.} and Weedon, {Michael N.} and Weijia Xie and Erik Ingelsson and Stefan Gustafsson and Nabila Bouatia-Naji and Elodie Eury and Philippe Froguel and Julie Kerr-Conte and Fran{\cc}ois Pattou and Gloyn, {Anna L.} and Paul Johnson and Mary Travers and Dimas, {Antigone S.} and Nica, {Alexandra C.} and Dermitzakis, {Emmanouil T.} and Per Eriksson and Lasse Folkersen and {van't Hooft}, {Ferdinand M.} and Voight, {Benjamin F.} and Scott, {Laura J.} and Valgerdur Steinthorsdottir and Morris, {Andrew P.} and Christian Dina and Welch, {Ryan P.} and Eleftheria Zeggini and Cornelia Huth and Aulchenko, {Yurii S.} and Gudmar Thorleifsson and McCulloch, {Laura J.} and Teresa Ferreira and Harald Grallert and Najaf Amin and Guanming Wu and Willer, {Cristen J.} and Soumya Raychaudhuri and McCarroll, {Steve A.} and Claudia Langenberg and Hofmann, {Oliver M.} and Jos{\'e}e Dupuis and Lu Qi and Segr{\`e}, {Ayellet V.} and {van Hoek}, Mandy and Pau Navarro and Kristin Ardlie and Beverley Balkau and Rafn Benediktsson and Bennett, {Amanda J.} and Roza Blagieva and Eric Boerwinkle and Bonnycastle, {Lori L.} and Bostr{\"o}m, {Kristina Bengtsson} and Bert Bravenboer and Suzannah Bumpstead and Burtt, {Nois{\"e}l P.} and Guillaume Charpentier and Chines, {Peter S.} and Marilyn Cornelis and Couper, {David J.} and Gabe Crawford and Doney, {Alex S F} and Elliott, {Katherine S.} and Elliott, {Amanda L.} and Erdos, {Michael R.} and Fox, {Caroline S.} and Franklin, {Christopher S.} and Martha Ganser and Christian Gieger and Niels Grarup and Todd Green and Simon Griffin and Groves, {Christopher J.} and Candace Guiducci and Samy Hadjadj and Neelam Hassanali and Christian Herder and Bo Isomaa and Jackson, {Anne U.} and Johnson, {Paul R V} and Torben J{\o}rgensen and Kao, {Wen H L} and Norman Klopp and Augustine Kong and Peter Kraft and Torsten Lauritzen and Man Li and Aloysius Lieverse and Lindgren, {Cecilia M.} and Valeriya Lyssenko and Michel Marre and Thomas Meitinger and Kristian Midthjell and Morken, {Mario A.} and Narisu Narisu and Peter Nilsson and Owen, {Katharine R.} and Felicity Payne and Perry, {John R B} and Petersen, {Ann Kristin} and Carl Platou and Christine Proen{\cc}a and Inga Prokopenko and Wolfgang Rathmann and Rayner, {N. 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and Olli Raitakari and Rayner, {Nigel W.} and Martin Ridderstr{\aa}el and Winfried Rief and Aimo Ruokonen and Robertson, {Neil R.} and Peter Rzehak and Veikko Salomaa and Sanders, {Alan R.} and Sandhu, {Manjinder S.} and Serena Sanna and Jouko Saramies and Savolainen, {Markku J.} and Susann Scherag and Sabine Schipf and Stefan Schreiber and Heribert Schunkert and Kaisa Silander and Juha Sinisalo and Siscovick, {David S.} and Smit, {Jan H.} and Nicole Soranzo and Ulla Sovio and Jonathan Stephens and Ida Surakka and Swift, {Amy J.} and Tammesoo, {Mari Liis} and Tardif, {Jean Claude} and Maris Teder-Laving and Teslovich, {Tanya M.} and Thompson, {John R.} and Brian Thomson and Anke T{\"o}njes and Tiinamaija Tuomi and {van Meurs}, {Joyce B.} and {van Ommen}, {Gert Jan} and Vincent Vatin and Jorma Viikari and Sophie Visvikis-Siest and Veronique Vitart and Vogel, {Carla I G} and Voight, {Benjamin F.} and Waite, {Lindsay L.} and Henri Wallaschofski and Walter, {G. Bragi} and Elisabeth Widen and Susanna Wiegand and Wild, {Sarah H.} and Gonneke Willemsen and Witte, {Daniel R.} and Witteman, {Jacqueline C.} and Jianfeng Xu and Qunyuan Zhang and Lina Zgaga and Andreas Ziegler and Paavo Zitting and Beilby, {John P.} and Farooqi, {I. Sadaf} and Johannes Hebebrand and Huikuri, {Heikki V.} and James, {Alan L.} and Mika K{\"a}h{\"o}nen and Levinson, {Douglas F.} and Fabio Macciardi and Nieminen, {Markku S.} and Claes Ohlsson and Palmer, {Lyle J.} and Ridker, {Paul M.} and Michael Stumvoll and Beckmann, {Jacques S.} and Heiner Boeing and Eric Boerwinkle and Boomsma, {Dorret I.} and Caulfield, {Mark J.} and Chanock, {Stephen J.} and Collins, {Francis S.} and Cupples, {L. Adrienne} and Smith, {George Davey} and Jeanette Erdmann and Philippe Froguel and Henrik Gr{\"o}nberg and Ulf Gyllensten and Per Hall and Torben Hansen and Harris, {Tamara B.} and Hattersley, {Andrew T.} and Hayes, {Richard B.} and Joachim Heinrich and Hu, {Frank B.} and Hu, {Frank B.} and Thomas Illig and Jarvelin, {Marjo Riitta} and Jaakko Kaprio and Fredrik Karpe and Khaw, {Kay Tee} and Kiemeney, {Lambertus A.} and Heiko Krude and Markku Laakso and Lawlor, {Debbie A.} and Andres Metspalu and Munroe, {Patricia B.} and Ouwehand, {Willem H.} and Oluf Pedersen and Penninx, {Brenda W.} and Annette Peters and Pramstaller, {Peter P.} and Thomas Quertermous and Thomas Reinehr and Aila Rissanen and Igor Rudan and Samani, {Nilesh J.} and Schwarz, {Peter E H} and Shuldiner, {Alan R.} and Spector, {Timothy D.} and Jaakko Tuomilehto and Manuela Uda and Andr{\'e} Uitterlinden and Valle, {Timo T.} and Martin Wabitsch and G{\'e}rard Waeber and Wareham, {Nicholas J.} and Hugh Watkins and Wilson, {James F.} and Wright, {Alan F.} and Zillikens, {M. Carola} and Nilanjan Chatterjee and McCarroll, {Steven A.} and Shaun Purcell and Schadt, {Eric E.} and Visscher, {Peter M.} and Assimes, {Themistocles L.} and Borecki, {Ingrid B.} and Panos Deloukas and Fox, {Caroline S.} and Groop, {Leif C.} and Talin Haritunians and Hunter, {David J.} and Kaplan, {Robert C.} and Mohlke, {Karen L.} and O'Connell, {Jeffrey R.} and Leena Peltonen and David Schlessinger and Strachan, {David P.} and {van Duijn}, {Cornelia M.} and Wichmann, {H. Erich} and Unnur Thorsteinsdottir and Abecasis, {Gon{\cc}alo R.} and In{\^e}s Barroso and Michael Boehnke and Kari Stefansson and North, {Kari E.} and McCarthy, {Mark I.} and Hirschhorn, {Joel N.} and Erik Ingelsson and Loos, {Ruth J F} and Nica, {Alexandra C.} and Leopold Parts and Daniel Glass and James Nisbet and Amy Barrett and Magdalena Sekowska and Mary Travers and Simon Potter and Elin Grundberg and Kerrin Small and Hedman, {{\AA}sa K.} and Veronique Bataille and {Tzenova Bell}, Jordana and Gabriela Surdulescu and Dimas, {Antigone S.} and Catherine Ingle and Nestle, {Frank O.} and {di Meglio}, Paola and Min, {Josine L.} and Alicja Wilk and Hammond, {Christopher J.} and Neelam Hassanali and Yang, {Tsun Po} and Montgomery, {Stephen B.} and Steve O'Rahilly and Lindgren, {Cecilia M.} and Zondervan, {Krina T.} and Nicole Soranzo and In{\^e}s Barroso and Richard Durbin and Kourosh Ahmadi and Panos Deloukas and McCarthy, {Mark I.} and Dermitzakis, {Emmanouil T.} and Spector, {Timothy D.} and Heribert Schunkert and K{\"o}nig, {Inke R.} and Sekar Kathiresan and Reilly, {Muredach P.} and Assimes, {Themistocles L.} and Hilma Holm and Michael Preuss and Stewart, {Alexandre F R} and Maja Barbalic and Christian Gieger and Devin Absher and Zouhair Aherrahrou and Hooman Allayee and David Altshuler and Anand, {Sonia S.} and Karl Andersen and Anderson, {Jeffrey L.} and Diego Ardissino and Ball, {Stephen G.} and Balmforth, {Anthony J.} and Barnes, {Timothy A.} and Becker, {Diane M.} and Becker, {Lewis C.} and Klaus Berger and Bis, {Joshua C.} and Boekholdt, {S. Matthijs} and Eric Boerwinkle and Braund, {Peter S.} and Brown, {Morris J.} and Burnett, {Mary Susan} and Ian Buysschaert and Carlquist, {John F.} and Li Chen and Sven Cichon and Veryan Codd and Davies, {Robert W.} and George Dedoussis and Abbas Dehghan and Serkalem Demissie and Devaney, {Joseph M.} and Patrick Diemert and Ron Do and Angela Doering and Sandra Eifert and {El Mokhtari}, {Nour Eddine} and Ellis, {Stephen G.} and Roberto Elosua and Engert, {James C.} and Epstein, {Stephen E.} and {de Faire}, Ulf and Marcus Fischer and Folsom, {Aaron R.} and Jennifer Freyer and Bruna Gigante and Domenico Girelli and Solveig Gretarsdottir and Vilmundur Gudnason and Gulcher, {Jeffrey R.} and Eran Halperin and Naomi Hammond and Hazen, {Stanley L.} and Albert Hofman and Horne, {Benjamin D.} and Thomas Illig and Carlos Iribarren and Jones, {Gregory T.} and Jukema, {J. Wouter} and Kaiser, {Michael A.} and Kaplan, {Lee M.} and Kastelein, {John J P} and Khaw, {Kay Tee} and Knowles, {Joshua W.} and Genovefa Kolovou and Augustine Kong and Reijo Laaksonen and Diether Lambrechts and Karin Leander and Guillaume Lettre and Mingyao Li and Wolfgang Lieb and Christina Loley and Lotery, {Andrew J.} and Mannucci, {Pier M.} and Seraya Maouche and Nicola Martinelli and McKeown, {Pascal P.} and Christa Meisinger and Thomas Meitinger and Olle Melander and Merlini, {Pier Angelica} and Vincent Mooser and Thomas Morgan and M{\"u}hleisen, {Thomas W.} and Muhlestein, {Joseph B.} and Thomas M{\"u}nzel and Kiran Musunuru and Janja Nahrstaedt and Nelson, {Christopher P.} and N{\"o}then, {Markus M.} and Oliviero Olivieri and Patel, {Riyaz S.} and Patterson, {Chris C.} and Annette Peters and Flora Peyvandi and Liming Qu and Quyyumi, {Arshed A.} and Rader, {Daniel J.} and Rallidis, {Loukianos S.} and Catherine Rice and Rosendaal, {Frits R.} and Diana Rubin and Veikko Salomaa and Sampietro, {M. Lourdes} and Sandhu, {Manj S.} and Eric Schadt and Arne Sch{\"a}fer and Arne Schillert and Stefan Schreiber and J{\"u}rgen Schrezenmeir and Schwartz, {Stephen M.} and Siscovick, {David S.} and Mohan Sivananthan and Suthesh Sivapalaratnam and Albert Smith and Smith, {Tamara B.} and Snoep, {Jaapjan D.} and Nicole Soranzo and Spertus, {John A.} and Klaus Stark and Kathy Stirrups and Monika Stoll and Tang, {W. H Wilson} and Stephanie Tennstedt and Gudmundur Thorgeirsson and Gudmar Thorleifsson and Maciej Tomaszewski and Uitterlinden, {Andre G.} and {van Rij}, {Andre M.} and Voight, {Benjamin F.} and Wareham, {Nick J.} and Wells, {George A.} and Wichmann, {H. Erich} and Wild, {Philipp S.} and Christina Willenborg and Witteman, {Jaqueline C M} and Wright, {Benjamin J.} and Shu Ye and Tanja Zeller and Andreas Ziegler and Francois Cambien and Goodall, {Alison H.} and Cupples, {L. Adrienne} and Thomas Quertermous and Winfried M{\"a}rz and Christian Hengstenberg and Stefan Blankenberg and Ouwehand, {Willem H.} and Hall, {Alistair S.} and Panos Deloukas and Thompson, {John R.} and Kari Stefansson and Robert Roberts and Unnur Thorsteinsdottir and O'Donnell, {Christopher J.} and Ruth McPherson and Jeanette Erdmann and Samani, {Nilesh J.} and Hopewell, {Jemma C.} and Sarah Parish and Alison Offer and Robert Clarke and Louise Bowman and Peter Sleight and Jane Armitage and Richard Peto and Rory Collins and Chambers, {John C.} and Goncalo Abecasis and Nabeel Ahmed and Mark Caulfield and Peter Donnelly and Paul Elliott and Philippe Froguel and Kooner, {Angad S.} and Mark McCarthy and Nilesh Samani and James Scott and Joban Sehmi and Weihua Zhang and Kooner, {Jaspal S.} and Rona Strawbridge and Maria Sabater-Lleal and Anders M{\"a}larstig and Bengt Sennblad and John {\"O}hrvik and Angela Silveira and {van't Hooft}, Ferdinand and Per Eriksson and Anders Hamsten and Hell{\'e}nius, {Mai Lis} and Gunnar Olsson and Stephan Rust and Gerd Assmann and Udo Seedorf and Simona Barlera and Franzosi, {Maria Grazia} and Gianni Tognoni and Robert Clarke and Pamela Linksted and Hopewell, {Jemma C.} and Rory Collins and Peden, {John F.} and Anuj Goel and Halit Ongen and Theodosios Kyriakou and Fiona Green and Martin Farrall and Hugh Watkins and Danish Saleheen and Asif Rasheed and Moazzam Zaidi and Nabi Shah and Maria Samuel and Nadeem Mallick and Muhammad Azhar and Zaman, {Khan Shah} and Adbus Samad and Muhammad Ishaq and Ali Gardezi and Memon, {Fazal ur Rehman} and Nilesh Samani and Philippe Frossard and Panos Deloukas and John Danesh",
year = "2011",
month = "10",
day = "1",
doi = "10.2337/db11-0415",
language = "English (US)",
volume = "60",
pages = "2624--2634",
journal = "Diabetes",
issn = "0012-1797",
publisher = "American Diabetes Association Inc.",
number = "10",

}

TY - JOUR

T1 - Genome-wide association identifies nine common variants associated with fasting proinsulin levels and provides new insights into the pathophysiology of type 2 diabetes

AU - Strawbridge, Rona J.

AU - Dupuis, Josée

AU - Prokopenko, Inga

AU - Barker, Adam

AU - Ahlqvist, Emma

AU - Petrie, John R.

AU - Dedoussis, George V.

AU - Lyssenko, Valeriya

AU - Meigs, James B.

AU - Barroso, Inês

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AU - Hamsten, Anders

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AU - Watkins, Hugh

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AU - Marre, Michel

AU - Meitinger, Thomas

AU - Midthjell, Kristian

AU - Morken, Mario A.

AU - Narisu, Narisu

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AU - Payne, Felicity

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AU - Walker, Mark

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AU - Watanabe, Richard M.

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AU - Pankow, James S.

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AU - Barroso, Inês

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AU - Groop, Leif

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AU - Thorsteinsdottir, Unnur

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AU - Froguel, Philippe

AU - van Duijn, Cornelia M.

AU - Stefansson, Kari

AU - Altshuler, David

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AU - Facheris, Maurizio F.

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AU - Scott, James

AU - Sehmi, Joban

AU - Zhang, Weihua

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AU - Sabater-Lleal, Maria

AU - Mälarstig, Anders

AU - Sennblad, Bengt

AU - Öhrvik, John

AU - Silveira, Angela

AU - van't Hooft, Ferdinand

AU - Eriksson, Per

AU - Hamsten, Anders

AU - Hellénius, Mai Lis

AU - Olsson, Gunnar

AU - Rust, Stephan

AU - Assmann, Gerd

AU - Seedorf, Udo

AU - Barlera, Simona

AU - Franzosi, Maria Grazia

AU - Tognoni, Gianni

AU - Clarke, Robert

AU - Linksted, Pamela

AU - Hopewell, Jemma C.

AU - Collins, Rory

AU - Peden, John F.

AU - Goel, Anuj

AU - Ongen, Halit

AU - Kyriakou, Theodosios

AU - Green, Fiona

AU - Farrall, Martin

AU - Watkins, Hugh

AU - Saleheen, Danish

AU - Rasheed, Asif

AU - Zaidi, Moazzam

AU - Shah, Nabi

AU - Samuel, Maria

AU - Mallick, Nadeem

AU - Azhar, Muhammad

AU - Zaman, Khan Shah

AU - Samad, Adbus

AU - Ishaq, Muhammad

AU - Gardezi, Ali

AU - Memon, Fazal ur Rehman

AU - Samani, Nilesh

AU - Frossard, Philippe

AU - Deloukas, Panos

AU - Danesh, John

PY - 2011/10/1

Y1 - 2011/10/1

N2 - OBJECTIVE - Proinsulin is a precursor of mature insulin and C-peptide. Higher circulating proinsulin levels are associated with impaired b-cell function, raised glucose levels, insulin resistance, and type 2 diabetes (T2D). Studies of the insulin processing pathway could provide new insights about T2D pathophysiology. RESEARCH DESIGN AND METHODS - We have conducted a meta-analysis of genome-wide association tests of ;2.5 million genotyped or imputed single nucleotide polymorphisms (SNPs) and fasting proinsulin levels in 10,701 nondiabetic adults of European ancestry, with follow-up of 23 loci in up to 16,378 individuals, using additive genetic models adjusted for age, sex, fasting insulin, and study-specific covariates. RESULTS - Nine SNPs at eight loci were associated with proinsulin levels (P < 5 × 10-8). Two loci (LARP6 and SGSM2) have not been previously related to metabolic traits, one (MADD) has been associated with fasting glucose, one (PCSK1) has been implicated in obesity, and four (TCF7L2, SLC30A8, VPS13C/ C2CD4A/B, and ARAP1, formerly CENTD2) increase T2D risk. The proinsulin-raising allele of ARAP1 was associated with a lower fasting glucose (P = 1.7 3 10-4), improved b-cell function (P = 1.1 × 10-5), and lower risk of T2D (odds ratio 0.88; P = 7.8 × 10-6). Notably, PCSK1 encodes the protein prohormone convertase 1/3, the first enzyme in the insulin processing pathway. A genotype score composed of the nine proinsulin-raising alleles was not associated with coronary disease in two large case-control datasets. CONCLUSIONS - We have identified nine genetic variants associated with fasting proinsulin. Our findings illuminate the biology underlying glucose homeostasis and T2D development in humans and argue against a direct role of proinsulin in coronary artery disease pathogenesis.

AB - OBJECTIVE - Proinsulin is a precursor of mature insulin and C-peptide. Higher circulating proinsulin levels are associated with impaired b-cell function, raised glucose levels, insulin resistance, and type 2 diabetes (T2D). Studies of the insulin processing pathway could provide new insights about T2D pathophysiology. RESEARCH DESIGN AND METHODS - We have conducted a meta-analysis of genome-wide association tests of ;2.5 million genotyped or imputed single nucleotide polymorphisms (SNPs) and fasting proinsulin levels in 10,701 nondiabetic adults of European ancestry, with follow-up of 23 loci in up to 16,378 individuals, using additive genetic models adjusted for age, sex, fasting insulin, and study-specific covariates. RESULTS - Nine SNPs at eight loci were associated with proinsulin levels (P < 5 × 10-8). Two loci (LARP6 and SGSM2) have not been previously related to metabolic traits, one (MADD) has been associated with fasting glucose, one (PCSK1) has been implicated in obesity, and four (TCF7L2, SLC30A8, VPS13C/ C2CD4A/B, and ARAP1, formerly CENTD2) increase T2D risk. The proinsulin-raising allele of ARAP1 was associated with a lower fasting glucose (P = 1.7 3 10-4), improved b-cell function (P = 1.1 × 10-5), and lower risk of T2D (odds ratio 0.88; P = 7.8 × 10-6). Notably, PCSK1 encodes the protein prohormone convertase 1/3, the first enzyme in the insulin processing pathway. A genotype score composed of the nine proinsulin-raising alleles was not associated with coronary disease in two large case-control datasets. CONCLUSIONS - We have identified nine genetic variants associated with fasting proinsulin. Our findings illuminate the biology underlying glucose homeostasis and T2D development in humans and argue against a direct role of proinsulin in coronary artery disease pathogenesis.

UR - http://www.scopus.com/inward/record.url?scp=80053405321&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=80053405321&partnerID=8YFLogxK

U2 - 10.2337/db11-0415

DO - 10.2337/db11-0415

M3 - Article

VL - 60

SP - 2624

EP - 2634

JO - Diabetes

JF - Diabetes

SN - 0012-1797

IS - 10

ER -