Genome-wide meta-analysis of 241,258 adults accounting for smoking behaviour identifies novel loci for obesity traits

Anne E. Justice, Thomas W. Winkler, Mary F. Feitosa, Misa Graff, Virginia A. Fisher, Kristin Young, Llilda Barata, Xuan Deng, Jacek Czajkowski, David Hadley, Julius S. Ngwa, Tarunveer S. Ahluwalia, Audrey Y. Chu, Nancy L. Heard-Costa, Elise Lim, Jeremiah Perez, John D. Eicher, Zolta'n Kutalik, Luting Xue, Anubha Mahajan & 297 others Frida Renström, Joseph Wu, Qibin Qi, Shafqat Ahmad, Tamuno Alfred, Najaf Amin, Lawrence F. Bielak, Amelie Bonnefond, Jennifer Bragg, Gemma Cadby, Martina Chittani, Scott Coggeshall, Tanguy Corre, Nese Direk, Joel Eriksson, Krista Fischer, Mathias Gorski, Marie Neergaard Harder, Momoko Horikoshi, Tao Huang, Jennifer E. Huffman, Anne U. Jackson, Johanne Marie Justesen, Stavroula Kanoni, Leena Kinnunen, Marcus E. Kleber, Pirjo Komulainen, Meena Kumari, Unhee Lim, Jian'an Luan, Leo Pekka Lyytikäinen, Massimo Mangino, Ani Manichaikul, Jonathan Marten, Rita P.S. Middelberg, Martina Müller-Nurasyid, Pau Navarro, Louis Pe'russe, Natalia Pervjakova, Cinzia Sarti, Albert Vernon Smith, Jennifer A. Smith, Alena Stanča'kova, Rona J. Strawbridge, Heather M. Stringham, Yun Ju Sung, Toshiko Tanaka, Alexander Teumer, Stella Trompet, Sander W. Van Der Laan, Peter J. Van Der Most, Jana V. Van Vliet-Ostaptchouk, Sailaja L. Vedantam, Niek Verweij, Jacqueline M. Vink, Veronique Vitart, Ying Wu, Loic Yengo, Weihua Zhang, Jing Hua Zhao, Martina E. Zimmermann, Niha Zubair, Gonçalo R. Abecasis, Linda S. Adair, Saima Afaq, Uzma Afzal, Stephan J.L. Bakker, Traci M. Bartz, John Beilby, Richard N. Bergman, Sven Bergmann, Reiner Biffar, John Blangero, Eric Boerwinkle, Lori L. Bonnycastle, Erwin Bottinger, Daniele Braga, Brendan M. Buckley, Steve Buyske, Harry Campbell, John C. Chambers, Francis S. Collins, Joanne E. Curran, Gert J. De Borst, Anton J.M. De Craen, Eco J.C. De Geus, George Dedoussis, Graciela E. Delgado, Hester M. Den Ruijter, Gudny Eiriksdottir, Anna L. Eriksson, Toñu Esko, Jessica D. Faul, Ian Ford, Terrence Forrester, Karl Gertow, Bruna Gigante, Nicola Glorioso, Jian Gong, Harald Grallert, Tanja B. Grammer, Niels Grarup, Saskia Haitjema, Göran Hallmans, Anders Hamsten, Torben Hansen, Tamara B. Harris, Catharina A. Hartman, Maija Hassinen, Nicholas D. Hastie, Andrew C. Heath, Dena Hernandez, Lucia Hindorff, Lynne J. Hocking, Mette Hollensted, Oddgeir L. Holmen, Georg Homuth, Jouke Jan Hottenga, Jie Huang, Joseph Hung, Nina Hutri-Kähönen, Erik Ingelsson, Alan L. James, John Olov Jansson, Marjo Riitta Jarvelin, Min A. Jhun, Marit E. Jorgensen, Markus Juonala, Mika Kähönen, Magnus Karlsson, Heikki A. Koistinen, Ivana Kolcic, Genovefa Kolovou, Charles Kooperberg, Bernhard K. Krämer, Johanna Kuusisto, Kirsti Kvaloy, Timo A. Lakka, Claudia Langenberg, Lenore J. Launer, Karin Leander, Nanette R. Lee, Lars Lind, Cecilia M. Lindgren, Allan Linneberg, Stephane Lobbens, Marie Loh, Mattias Lorentzon, Robert Luben, Gitta Lubke, Anja Ludolph-Donislawski, Sara Lupoli, Pamela A.F. Madden, Reija Männikkö, Pedro Marques-Vidal, Nicholas G. Martin, Colin A. McKenzie, Barbara McKnight, Dan Mellström, Cristina Menni, Grant W. Montgomery, A. W. Musk, Narisu Narisu, Matthias Nauck, Ilja M. Nolte, Albertine J. Oldehinkel, Matthias Olden, Ken K. Ong, Sandosh Padmanabhan, Patricia A. Peyser, Charlotta Pisinger, David J. Porteous, Olli T. Raitakari, Tuomo Rankinen, D. C. Rao, Laura J. Rasmussen-Torvik, Rajesh Rawal, Treva Rice, Paul M. Ridker, Lynda M. Rose, Stephanie A. Bien, Igor Rudan, Serena Sanna, Mark A. Sarzynski, Naveed Sattar, Kai Savonen, David Schlessinger, Salome Scholtens, Claudia Schurmann, Robert A. Scott, Bengt Sennblad, Marten A. Siemelink, Günther Silbernagel, P. Eline Slagboom, Harold Snieder, Jan A. Staessen, David J. Stott, Morris A. Swertz, Amy J. Swift, Kent D. Taylor, Bamidele O. Tayo, Barbara Thorand, Dorothee Thuillier, Jaakko Tuomilehto, Andre G. Uitterlinden, Liesbeth Vandenput, Marie Claude Vohl, Henry Völzke, Judith M. Vonk, Ge'rard Waeber, Melanie Waldenberger, R. G.J. Westendorp, Sarah Wild, Gonneke Willemsen, Bruce H.R. Wolffenbuttel, Andrew Wong, Alan F. Wright, Wei Zhao, M. Carola Zillikens, Damiano Baldassarre, Beverley Balkau, Stefania Bandinelli, Carsten A. Böger, Dorret I. Boomsma, Claude Bouchard, Marcel Bruinenberg, Daniel I. Chasman, Yii Der Ida Chen, Peter S. Chines, Richard S. Cooper, Francesco Cucca, Daniele Cusi, Ulf De Faire, Luigi Ferrucci, Paul W. Franks, Philippe Froguel, Penny Gordon-Larsen, Hans Jörgen Grabe, Vilmundur Gudnason, Christopher A. Haiman, Caroline Hayward, Kristian Hveem, Andrew D. Johnson, J. Wouter Jukema, Sharon L.R. Kardia, Mika Kivimaki, Jaspal S. Kooner, Diana Kuh, Markku Laakso, Terho Lehtimäki, Loic Le Marchand, Winfried März, Mark I. McCarthy, Andres Metspalu, Andrew P. Morris, Claes Ohlsson, Lyle J. Palmer, Gerard Pasterkamp, Oluf Pedersen, Annette Peters, Ulrike Peters, Ozren Polasek, Bruce M. Psaty, Lu Qi, Rainer Rauramaa, Blair H. Smith, Thorkild I.A. Sorensen, Konstantin Strauch, Henning Tiemeier, Elena Tremoli, Pim Van Der Harst, Henrik Vestergaard, Peter Vollenweider, Nicholas J. Wareham, David R. Weir, John B. Whitfield, James F. Wilson, Jessica Tyrrell, Timothy M. Frayling, Inês Barroso, Michael Boehnke, Panagiotis Deloukas, Caroline S. Fox, Joel N. Hirschhorn, David J. Hunter, Tim D. Spector, David P. Strachan, Cornelia M. Van Duijn, Iris M. Heid, Karen L. Mohlke, Jonathan Marchini, Ruth J.F. Loos, Tuomas O. Kilpeläinen, Ching Ti Liu, Ingrid B. Borecki, Kari E. North, L. Adrienne Cupples

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Abstract

Few genome-wide association studies (GWAS) account for environmental exposures, like smoking, potentially impacting the overall trait variance when investigating the genetic contribution to obesity-related traits. Here, we use GWAS data from 51,080 current smokers and 190,178 nonsmokers (87% European descent) to identify loci influencing BMI and central adiposity, measured as waist circumference and waist-to-hip ratio both adjusted for BMI. We identify 23 novel genetic loci, and 9 loci with convincing evidence of gene-smoking interaction (GxSMK) on obesity-related traits. We show consistent direction of effect for all identified loci and significance for 18 novel and for 5 interaction loci in an independent study sample. These loci highlight novel biological functions, including response to oxidative stress, addictive behaviour, and regulatory functions emphasizing the importance of accounting for environment in genetic analyses. Our results suggest that tobacco smoking may alter the genetic susceptibility to overall adiposity and body fat distribution.

LanguageEnglish
Article number14977
JournalNature Communications
Volume8
DOIs
StatePublished - 26 Apr 2017

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obesity
genome
loci
Meta-Analysis
Obesity
Genes
Genome-Wide Association Study
Smoking
Adiposity
Genome
Association reactions
Addictive Behavior
Body Fat Distribution
Genetic Loci
Oxidative stress
Waist-Hip Ratio
Tobacco
Environmental Exposure
Waist Circumference
Genetic Predisposition to Disease

Cite this

Justice, A. E., Winkler, T. W., Feitosa, M. F., Graff, M., Fisher, V. A., Young, K., ... Cupples, L. A. (2017). Genome-wide meta-analysis of 241,258 adults accounting for smoking behaviour identifies novel loci for obesity traits. Nature Communications, 8, [14977]. DOI: 10.1038/ncomms14977
Justice, Anne E. ; Winkler, Thomas W. ; Feitosa, Mary F. ; Graff, Misa ; Fisher, Virginia A. ; Young, Kristin ; Barata, Llilda ; Deng, Xuan ; Czajkowski, Jacek ; Hadley, David ; Ngwa, Julius S. ; Ahluwalia, Tarunveer S. ; Chu, Audrey Y. ; Heard-Costa, Nancy L. ; Lim, Elise ; Perez, Jeremiah ; Eicher, John D. ; Kutalik, Zolta'n ; Xue, Luting ; Mahajan, Anubha ; Renström, Frida ; Wu, Joseph ; Qi, Qibin ; Ahmad, Shafqat ; Alfred, Tamuno ; Amin, Najaf ; Bielak, Lawrence F. ; Bonnefond, Amelie ; Bragg, Jennifer ; Cadby, Gemma ; Chittani, Martina ; Coggeshall, Scott ; Corre, Tanguy ; Direk, Nese ; Eriksson, Joel ; Fischer, Krista ; Gorski, Mathias ; Harder, Marie Neergaard ; Horikoshi, Momoko ; Huang, Tao ; Huffman, Jennifer E. ; Jackson, Anne U. ; Justesen, Johanne Marie ; Kanoni, Stavroula ; Kinnunen, Leena ; Kleber, Marcus E. ; Komulainen, Pirjo ; Kumari, Meena ; Lim, Unhee ; Luan, Jian'an ; Lyytikäinen, Leo Pekka ; Mangino, Massimo ; Manichaikul, Ani ; Marten, Jonathan ; Middelberg, Rita P.S. ; Müller-Nurasyid, Martina ; Navarro, Pau ; Pe'russe, Louis ; Pervjakova, Natalia ; Sarti, Cinzia ; Smith, Albert Vernon ; Smith, Jennifer A. ; Stanča'kova, Alena ; Strawbridge, Rona J. ; Stringham, Heather M. ; Sung, Yun Ju ; Tanaka, Toshiko ; Teumer, Alexander ; Trompet, Stella ; Van Der Laan, Sander W. ; Van Der Most, Peter J. ; Van Vliet-Ostaptchouk, Jana V. ; Vedantam, Sailaja L. ; Verweij, Niek ; Vink, Jacqueline M. ; Vitart, Veronique ; Wu, Ying ; Yengo, Loic ; Zhang, Weihua ; Zhao, Jing Hua ; Zimmermann, Martina E. ; Zubair, Niha ; Abecasis, Gonçalo R. ; Adair, Linda S. ; Afaq, Saima ; Afzal, Uzma ; Bakker, Stephan J.L. ; Bartz, Traci M. ; Beilby, John ; Bergman, Richard N. ; Bergmann, Sven ; Biffar, Reiner ; Blangero, John ; Boerwinkle, Eric ; Bonnycastle, Lori L. ; Bottinger, Erwin ; Braga, Daniele ; Buckley, Brendan M. ; Buyske, Steve ; Campbell, Harry ; Chambers, John C. ; Collins, Francis S. ; Curran, Joanne E. ; De Borst, Gert J. ; De Craen, Anton J.M. ; De Geus, Eco J.C. ; Dedoussis, George ; Delgado, Graciela E. ; Den Ruijter, Hester M. ; Eiriksdottir, Gudny ; Eriksson, Anna L. ; Esko, Toñu ; Faul, Jessica D. ; Ford, Ian ; Forrester, Terrence ; Gertow, Karl ; Gigante, Bruna ; Glorioso, Nicola ; Gong, Jian ; Grallert, Harald ; Grammer, Tanja B. ; Grarup, Niels ; Haitjema, Saskia ; Hallmans, Göran ; Hamsten, Anders ; Hansen, Torben ; Harris, Tamara B. ; Hartman, Catharina A. ; Hassinen, Maija ; Hastie, Nicholas D. ; Heath, Andrew C. ; Hernandez, Dena ; Hindorff, Lucia ; Hocking, Lynne J. ; Hollensted, Mette ; Holmen, Oddgeir L. ; Homuth, Georg ; Hottenga, Jouke Jan ; Huang, Jie ; Hung, Joseph ; Hutri-Kähönen, Nina ; Ingelsson, Erik ; James, Alan L. ; Jansson, John Olov ; Jarvelin, Marjo Riitta ; Jhun, Min A. ; Jorgensen, Marit E. ; Juonala, Markus ; Kähönen, Mika ; Karlsson, Magnus ; Koistinen, Heikki A. ; Kolcic, Ivana ; Kolovou, Genovefa ; Kooperberg, Charles ; Krämer, Bernhard K. ; Kuusisto, Johanna ; Kvaloy, Kirsti ; Lakka, Timo A. ; Langenberg, Claudia ; Launer, Lenore J. ; Leander, Karin ; Lee, Nanette R. ; Lind, Lars ; Lindgren, Cecilia M. ; Linneberg, Allan ; Lobbens, Stephane ; Loh, Marie ; Lorentzon, Mattias ; Luben, Robert ; Lubke, Gitta ; Ludolph-Donislawski, Anja ; Lupoli, Sara ; Madden, Pamela A.F. ; Männikkö, Reija ; Marques-Vidal, Pedro ; Martin, Nicholas G. ; McKenzie, Colin A. ; McKnight, Barbara ; Mellström, Dan ; Menni, Cristina ; Montgomery, Grant W. ; Musk, A. W. ; Narisu, Narisu ; Nauck, Matthias ; Nolte, Ilja M. ; Oldehinkel, Albertine J. ; Olden, Matthias ; Ong, Ken K. ; Padmanabhan, Sandosh ; Peyser, Patricia A. ; Pisinger, Charlotta ; Porteous, David J. ; Raitakari, Olli T. ; Rankinen, Tuomo ; Rao, D. C. ; Rasmussen-Torvik, Laura J. ; Rawal, Rajesh ; Rice, Treva ; Ridker, Paul M. ; Rose, Lynda M. ; Bien, Stephanie A. ; Rudan, Igor ; Sanna, Serena ; Sarzynski, Mark A. ; Sattar, Naveed ; Savonen, Kai ; Schlessinger, David ; Scholtens, Salome ; Schurmann, Claudia ; Scott, Robert A. ; Sennblad, Bengt ; Siemelink, Marten A. ; Silbernagel, Günther ; Slagboom, P. Eline ; Snieder, Harold ; Staessen, Jan A. ; Stott, David J. ; Swertz, Morris A. ; Swift, Amy J. ; Taylor, Kent D. ; Tayo, Bamidele O. ; Thorand, Barbara ; Thuillier, Dorothee ; Tuomilehto, Jaakko ; Uitterlinden, Andre G. ; Vandenput, Liesbeth ; Vohl, Marie Claude ; Völzke, Henry ; Vonk, Judith M. ; Waeber, Ge'rard ; Waldenberger, Melanie ; Westendorp, R. G.J. ; Wild, Sarah ; Willemsen, Gonneke ; Wolffenbuttel, Bruce H.R. ; Wong, Andrew ; Wright, Alan F. ; Zhao, Wei ; Zillikens, M. Carola ; Baldassarre, Damiano ; Balkau, Beverley ; Bandinelli, Stefania ; Böger, Carsten A. ; Boomsma, Dorret I. ; Bouchard, Claude ; Bruinenberg, Marcel ; Chasman, Daniel I. ; Ida Chen, Yii Der ; Chines, Peter S. ; Cooper, Richard S. ; Cucca, Francesco ; Cusi, Daniele ; De Faire, Ulf ; Ferrucci, Luigi ; Franks, Paul W. ; Froguel, Philippe ; Gordon-Larsen, Penny ; Grabe, Hans Jörgen ; Gudnason, Vilmundur ; Haiman, Christopher A. ; Hayward, Caroline ; Hveem, Kristian ; Johnson, Andrew D. ; Jukema, J. Wouter ; Kardia, Sharon L.R. ; Kivimaki, Mika ; Kooner, Jaspal S. ; Kuh, Diana ; Laakso, Markku ; Lehtimäki, Terho ; Le Marchand, Loic ; März, Winfried ; McCarthy, Mark I. ; Metspalu, Andres ; Morris, Andrew P. ; Ohlsson, Claes ; Palmer, Lyle J. ; Pasterkamp, Gerard ; Pedersen, Oluf ; Peters, Annette ; Peters, Ulrike ; Polasek, Ozren ; Psaty, Bruce M. ; Qi, Lu ; Rauramaa, Rainer ; Smith, Blair H. ; Sorensen, Thorkild I.A. ; Strauch, Konstantin ; Tiemeier, Henning ; Tremoli, Elena ; Van Der Harst, Pim ; Vestergaard, Henrik ; Vollenweider, Peter ; Wareham, Nicholas J. ; Weir, David R. ; Whitfield, John B. ; Wilson, James F. ; Tyrrell, Jessica ; Frayling, Timothy M. ; Barroso, Inês ; Boehnke, Michael ; Deloukas, Panagiotis ; Fox, Caroline S. ; Hirschhorn, Joel N. ; Hunter, David J. ; Spector, Tim D. ; Strachan, David P. ; Van Duijn, Cornelia M. ; Heid, Iris M. ; Mohlke, Karen L. ; Marchini, Jonathan ; Loos, Ruth J.F. ; Kilpeläinen, Tuomas O. ; Liu, Ching Ti ; Borecki, Ingrid B. ; North, Kari E. ; Cupples, L. Adrienne. / Genome-wide meta-analysis of 241,258 adults accounting for smoking behaviour identifies novel loci for obesity traits. In: Nature Communications. 2017 ; Vol. 8.
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W.} and Narisu Narisu and Matthias Nauck and Nolte, {Ilja M.} and Oldehinkel, {Albertine J.} and Matthias Olden and Ong, {Ken K.} and Sandosh Padmanabhan and Peyser, {Patricia A.} and Charlotta Pisinger and Porteous, {David J.} and Raitakari, {Olli T.} and Tuomo Rankinen and Rao, {D. C.} and Rasmussen-Torvik, {Laura J.} and Rajesh Rawal and Treva Rice and Ridker, {Paul M.} and Rose, {Lynda M.} and Bien, {Stephanie A.} and Igor Rudan and Serena Sanna and Sarzynski, {Mark A.} and Naveed Sattar and Kai Savonen and David Schlessinger and Salome Scholtens and Claudia Schurmann and Scott, {Robert A.} and Bengt Sennblad and Siemelink, {Marten A.} and G{\"u}nther Silbernagel and Slagboom, {P. 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Adrienne}",
year = "2017",
month = "4",
day = "26",
doi = "10.1038/ncomms14977",
language = "English",
volume = "8",
journal = "NATURE COMMUNICATIONS",
issn = "2041-1723",
publisher = "Nature Publishing Group",

}

Justice, AE, Winkler, TW, Feitosa, MF, Graff, M, Fisher, VA, Young, K, Barata, L, Deng, X, Czajkowski, J, Hadley, D, Ngwa, JS, Ahluwalia, TS, Chu, AY, Heard-Costa, NL, Lim, E, Perez, J, Eicher, JD, Kutalik, Z, Xue, L, Mahajan, A, Renström, F, Wu, J, Qi, Q, Ahmad, S, Alfred, T, Amin, N, Bielak, LF, Bonnefond, A, Bragg, J, Cadby, G, Chittani, M, Coggeshall, S, Corre, T, Direk, N, Eriksson, J, Fischer, K, Gorski, M, Harder, MN, Horikoshi, M, Huang, T, Huffman, JE, Jackson, AU, Justesen, JM, Kanoni, S, Kinnunen, L, Kleber, ME, Komulainen, P, Kumari, M, Lim, U, Luan, J, Lyytikäinen, LP, Mangino, M, Manichaikul, A, Marten, J, Middelberg, RPS, Müller-Nurasyid, M, Navarro, P, Pe'russe, L, Pervjakova, N, Sarti, C, Smith, AV, Smith, JA, Stanča'kova, A, Strawbridge, RJ, Stringham, HM, Sung, YJ, Tanaka, T, Teumer, A, Trompet, S, Van Der Laan, SW, Van Der Most, PJ, Van Vliet-Ostaptchouk, JV, Vedantam, SL, Verweij, N, Vink, JM, Vitart, V, Wu, Y, Yengo, L, Zhang, W, Zhao, JH, Zimmermann, ME, Zubair, N, Abecasis, GR, Adair, LS, Afaq, S, Afzal, U, Bakker, SJL, Bartz, TM, Beilby, J, Bergman, RN, Bergmann, S, Biffar, R, Blangero, J, Boerwinkle, E, Bonnycastle, LL, Bottinger, E, Braga, D, Buckley, BM, Buyske, S, Campbell, H, Chambers, JC, Collins, FS, Curran, JE, De Borst, GJ, De Craen, AJM, De Geus, EJC, Dedoussis, G, Delgado, GE, Den Ruijter, HM, Eiriksdottir, G, Eriksson, AL, Esko, T, Faul, JD, Ford, I, Forrester, T, Gertow, K, Gigante, B, Glorioso, N, Gong, J, Grallert, H, Grammer, TB, Grarup, N, Haitjema, S, Hallmans, G, Hamsten, A, Hansen, T, Harris, TB, Hartman, CA, Hassinen, M, Hastie, ND, Heath, AC, Hernandez, D, Hindorff, L, Hocking, LJ, Hollensted, M, Holmen, OL, Homuth, G, Hottenga, JJ, Huang, J, Hung, J, Hutri-Kähönen, N, Ingelsson, E, James, AL, Jansson, JO, Jarvelin, MR, Jhun, MA, Jorgensen, ME, Juonala, M, Kähönen, M, Karlsson, M, Koistinen, HA, Kolcic, I, Kolovou, G, Kooperberg, C, Krämer, BK, Kuusisto, J, Kvaloy, K, Lakka, TA, Langenberg, C, Launer, LJ, Leander, K, Lee, NR, Lind, L, Lindgren, CM, Linneberg, A, Lobbens, S, Loh, M, Lorentzon, M, Luben, R, Lubke, G, Ludolph-Donislawski, A, Lupoli, S, Madden, PAF, Männikkö, R, Marques-Vidal, P, Martin, NG, McKenzie, CA, McKnight, B, Mellström, D, Menni, C, Montgomery, GW, Musk, AW, Narisu, N, Nauck, M, Nolte, IM, Oldehinkel, AJ, Olden, M, Ong, KK, Padmanabhan, S, Peyser, PA, Pisinger, C, Porteous, DJ, Raitakari, OT, Rankinen, T, Rao, DC, Rasmussen-Torvik, LJ, Rawal, R, Rice, T, Ridker, PM, Rose, LM, Bien, SA, Rudan, I, Sanna, S, Sarzynski, MA, Sattar, N, Savonen, K, Schlessinger, D, Scholtens, S, Schurmann, C, Scott, RA, Sennblad, B, Siemelink, MA, Silbernagel, G, Slagboom, PE, Snieder, H, Staessen, JA, Stott, DJ, Swertz, MA, Swift, AJ, Taylor, KD, Tayo, BO, Thorand, B, Thuillier, D, Tuomilehto, J, Uitterlinden, AG, Vandenput, L, Vohl, MC, Völzke, H, Vonk, JM, Waeber, G, Waldenberger, M, Westendorp, RGJ, Wild, S, Willemsen, G, Wolffenbuttel, BHR, Wong, A, Wright, AF, Zhao, W, Zillikens, MC, Baldassarre, D, Balkau, B, Bandinelli, S, Böger, CA, Boomsma, DI, Bouchard, C, Bruinenberg, M, Chasman, DI, Ida Chen, YD, Chines, PS, Cooper, RS, Cucca, F, Cusi, D, De Faire, U, Ferrucci, L, Franks, PW, Froguel, P, Gordon-Larsen, P, Grabe, HJ, Gudnason, V, Haiman, CA, Hayward, C, Hveem, K, Johnson, AD, Jukema, JW, Kardia, SLR, Kivimaki, M, Kooner, JS, Kuh, D, Laakso, M, Lehtimäki, T, Le Marchand, L, März, W, McCarthy, MI, Metspalu, A, Morris, AP, Ohlsson, C, Palmer, LJ, Pasterkamp, G, Pedersen, O, Peters, A, Peters, U, Polasek, O, Psaty, BM, Qi, L, Rauramaa, R, Smith, BH, Sorensen, TIA, Strauch, K, Tiemeier, H, Tremoli, E, Van Der Harst, P, Vestergaard, H, Vollenweider, P, Wareham, NJ, Weir, DR, Whitfield, JB, Wilson, JF, Tyrrell, J, Frayling, TM, Barroso, I, Boehnke, M, Deloukas, P, Fox, CS, Hirschhorn, JN, Hunter, DJ, Spector, TD, Strachan, DP, Van Duijn, CM, Heid, IM, Mohlke, KL, Marchini, J, Loos, RJF, Kilpeläinen, TO, Liu, CT, Borecki, IB, North, KE & Cupples, LA 2017, 'Genome-wide meta-analysis of 241,258 adults accounting for smoking behaviour identifies novel loci for obesity traits' Nature Communications, vol 8, 14977. DOI: 10.1038/ncomms14977

Genome-wide meta-analysis of 241,258 adults accounting for smoking behaviour identifies novel loci for obesity traits. / Justice, Anne E.; Winkler, Thomas W.; Feitosa, Mary F.; Graff, Misa; Fisher, Virginia A.; Young, Kristin; Barata, Llilda; Deng, Xuan; Czajkowski, Jacek; Hadley, David; Ngwa, Julius S.; Ahluwalia, Tarunveer S.; Chu, Audrey Y.; Heard-Costa, Nancy L.; Lim, Elise; Perez, Jeremiah; Eicher, John D.; Kutalik, Zolta'n; Xue, Luting; Mahajan, Anubha; Renström, Frida; Wu, Joseph; Qi, Qibin; Ahmad, Shafqat; Alfred, Tamuno; Amin, Najaf; Bielak, Lawrence F.; Bonnefond, Amelie; Bragg, Jennifer; Cadby, Gemma; Chittani, Martina; Coggeshall, Scott; Corre, Tanguy; Direk, Nese; Eriksson, Joel; Fischer, Krista; Gorski, Mathias; Harder, Marie Neergaard; Horikoshi, Momoko; Huang, Tao; Huffman, Jennifer E.; Jackson, Anne U.; Justesen, Johanne Marie; Kanoni, Stavroula; Kinnunen, Leena; Kleber, Marcus E.; Komulainen, Pirjo; Kumari, Meena; Lim, Unhee; Luan, Jian'an; Lyytikäinen, Leo Pekka; Mangino, Massimo; Manichaikul, Ani; Marten, Jonathan; Middelberg, Rita P.S.; Müller-Nurasyid, Martina; Navarro, Pau; Pe'russe, Louis; Pervjakova, Natalia; Sarti, Cinzia; Smith, Albert Vernon; Smith, Jennifer A.; Stanča'kova, Alena; Strawbridge, Rona J.; Stringham, Heather M.; Sung, Yun Ju; Tanaka, Toshiko; Teumer, Alexander; Trompet, Stella; Van Der Laan, Sander W.; Van Der Most, Peter J.; Van Vliet-Ostaptchouk, Jana V.; Vedantam, Sailaja L.; Verweij, Niek; Vink, Jacqueline M.; Vitart, Veronique; Wu, Ying; Yengo, Loic; Zhang, Weihua; Zhao, Jing Hua; Zimmermann, Martina E.; Zubair, Niha; Abecasis, Gonçalo R.; Adair, Linda S.; Afaq, Saima; Afzal, Uzma; Bakker, Stephan J.L.; Bartz, Traci M.; Beilby, John; Bergman, Richard N.; Bergmann, Sven; Biffar, Reiner; Blangero, John; Boerwinkle, Eric; Bonnycastle, Lori L.; Bottinger, Erwin; Braga, Daniele; Buckley, Brendan M.; Buyske, Steve; Campbell, Harry; Chambers, John C.; Collins, Francis S.; Curran, Joanne E.; De Borst, Gert J.; De Craen, Anton J.M.; De Geus, Eco J.C.; Dedoussis, George; Delgado, Graciela E.; Den Ruijter, Hester M.; Eiriksdottir, Gudny; Eriksson, Anna L.; Esko, Toñu; Faul, Jessica D.; Ford, Ian; Forrester, Terrence; Gertow, Karl; Gigante, Bruna; Glorioso, Nicola; Gong, Jian; Grallert, Harald; Grammer, Tanja B.; Grarup, Niels; Haitjema, Saskia; Hallmans, Göran; Hamsten, Anders; Hansen, Torben; Harris, Tamara B.; Hartman, Catharina A.; Hassinen, Maija; Hastie, Nicholas D.; Heath, Andrew C.; Hernandez, Dena; Hindorff, Lucia; Hocking, Lynne J.; Hollensted, Mette; Holmen, Oddgeir L.; Homuth, Georg; Hottenga, Jouke Jan; Huang, Jie; Hung, Joseph; Hutri-Kähönen, Nina; Ingelsson, Erik; James, Alan L.; Jansson, John Olov; Jarvelin, Marjo Riitta; Jhun, Min A.; Jorgensen, Marit E.; Juonala, Markus; Kähönen, Mika; Karlsson, Magnus; Koistinen, Heikki A.; Kolcic, Ivana; Kolovou, Genovefa; Kooperberg, Charles; Krämer, Bernhard K.; Kuusisto, Johanna; Kvaloy, Kirsti; Lakka, Timo A.; Langenberg, Claudia; Launer, Lenore J.; Leander, Karin; Lee, Nanette R.; Lind, Lars; Lindgren, Cecilia M.; Linneberg, Allan; Lobbens, Stephane; Loh, Marie; Lorentzon, Mattias; Luben, Robert; Lubke, Gitta; Ludolph-Donislawski, Anja; Lupoli, Sara; Madden, Pamela A.F.; Männikkö, Reija; Marques-Vidal, Pedro; Martin, Nicholas G.; McKenzie, Colin A.; McKnight, Barbara; Mellström, Dan; Menni, Cristina; Montgomery, Grant W.; Musk, A. W.; Narisu, Narisu; Nauck, Matthias; Nolte, Ilja M.; Oldehinkel, Albertine J.; Olden, Matthias; Ong, Ken K.; Padmanabhan, Sandosh; Peyser, Patricia A.; Pisinger, Charlotta; Porteous, David J.; Raitakari, Olli T.; Rankinen, Tuomo; Rao, D. C.; Rasmussen-Torvik, Laura J.; Rawal, Rajesh; Rice, Treva; Ridker, Paul M.; Rose, Lynda M.; Bien, Stephanie A.; Rudan, Igor; Sanna, Serena; Sarzynski, Mark A.; Sattar, Naveed; Savonen, Kai; Schlessinger, David; Scholtens, Salome; Schurmann, Claudia; Scott, Robert A.; Sennblad, Bengt; Siemelink, Marten A.; Silbernagel, Günther; Slagboom, P. Eline; Snieder, Harold; Staessen, Jan A.; Stott, David J.; Swertz, Morris A.; Swift, Amy J.; Taylor, Kent D.; Tayo, Bamidele O.; Thorand, Barbara; Thuillier, Dorothee; Tuomilehto, Jaakko; Uitterlinden, Andre G.; Vandenput, Liesbeth; Vohl, Marie Claude; Völzke, Henry; Vonk, Judith M.; Waeber, Ge'rard; Waldenberger, Melanie; Westendorp, R. G.J.; Wild, Sarah; Willemsen, Gonneke; Wolffenbuttel, Bruce H.R.; Wong, Andrew; Wright, Alan F.; Zhao, Wei; Zillikens, M. Carola; Baldassarre, Damiano; Balkau, Beverley; Bandinelli, Stefania; Böger, Carsten A.; Boomsma, Dorret I.; Bouchard, Claude; Bruinenberg, Marcel; Chasman, Daniel I.; Ida Chen, Yii Der; Chines, Peter S.; Cooper, Richard S.; Cucca, Francesco; Cusi, Daniele; De Faire, Ulf; Ferrucci, Luigi; Franks, Paul W.; Froguel, Philippe; Gordon-Larsen, Penny; Grabe, Hans Jörgen; Gudnason, Vilmundur; Haiman, Christopher A.; Hayward, Caroline; Hveem, Kristian; Johnson, Andrew D.; Jukema, J. Wouter; Kardia, Sharon L.R.; Kivimaki, Mika; Kooner, Jaspal S.; Kuh, Diana; Laakso, Markku; Lehtimäki, Terho; Le Marchand, Loic; März, Winfried; McCarthy, Mark I.; Metspalu, Andres; Morris, Andrew P.; Ohlsson, Claes; Palmer, Lyle J.; Pasterkamp, Gerard; Pedersen, Oluf; Peters, Annette; Peters, Ulrike; Polasek, Ozren; Psaty, Bruce M.; Qi, Lu; Rauramaa, Rainer; Smith, Blair H.; Sorensen, Thorkild I.A.; Strauch, Konstantin; Tiemeier, Henning; Tremoli, Elena; Van Der Harst, Pim; Vestergaard, Henrik; Vollenweider, Peter; Wareham, Nicholas J.; Weir, David R.; Whitfield, John B.; Wilson, James F.; Tyrrell, Jessica; Frayling, Timothy M.; Barroso, Inês; Boehnke, Michael; Deloukas, Panagiotis; Fox, Caroline S.; Hirschhorn, Joel N.; Hunter, David J.; Spector, Tim D.; Strachan, David P.; Van Duijn, Cornelia M.; Heid, Iris M.; Mohlke, Karen L.; Marchini, Jonathan; Loos, Ruth J.F.; Kilpeläinen, Tuomas O.; Liu, Ching Ti; Borecki, Ingrid B.; North, Kari E.; Cupples, L. Adrienne.

In: Nature Communications, Vol. 8, 14977, 26.04.2017.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Genome-wide meta-analysis of 241,258 adults accounting for smoking behaviour identifies novel loci for obesity traits

AU - Justice,Anne E.

AU - Winkler,Thomas W.

AU - Feitosa,Mary F.

AU - Graff,Misa

AU - Fisher,Virginia A.

AU - Young,Kristin

AU - Barata,Llilda

AU - Deng,Xuan

AU - Czajkowski,Jacek

AU - Hadley,David

AU - Ngwa,Julius S.

AU - Ahluwalia,Tarunveer S.

AU - Chu,Audrey Y.

AU - Heard-Costa,Nancy L.

AU - Lim,Elise

AU - Perez,Jeremiah

AU - Eicher,John D.

AU - Kutalik,Zolta'n

AU - Xue,Luting

AU - Mahajan,Anubha

AU - Renström,Frida

AU - Wu,Joseph

AU - Qi,Qibin

AU - Ahmad,Shafqat

AU - Alfred,Tamuno

AU - Amin,Najaf

AU - Bielak,Lawrence F.

AU - Bonnefond,Amelie

AU - Bragg,Jennifer

AU - Cadby,Gemma

AU - Chittani,Martina

AU - Coggeshall,Scott

AU - Corre,Tanguy

AU - Direk,Nese

AU - Eriksson,Joel

AU - Fischer,Krista

AU - Gorski,Mathias

AU - Harder,Marie Neergaard

AU - Horikoshi,Momoko

AU - Huang,Tao

AU - Huffman,Jennifer E.

AU - Jackson,Anne U.

AU - Justesen,Johanne Marie

AU - Kanoni,Stavroula

AU - Kinnunen,Leena

AU - Kleber,Marcus E.

AU - Komulainen,Pirjo

AU - Kumari,Meena

AU - Lim,Unhee

AU - Luan,Jian'an

AU - Lyytikäinen,Leo Pekka

AU - Mangino,Massimo

AU - Manichaikul,Ani

AU - Marten,Jonathan

AU - Middelberg,Rita P.S.

AU - Müller-Nurasyid,Martina

AU - Navarro,Pau

AU - Pe'russe,Louis

AU - Pervjakova,Natalia

AU - Sarti,Cinzia

AU - Smith,Albert Vernon

AU - Smith,Jennifer A.

AU - Stanča'kova,Alena

AU - Strawbridge,Rona J.

AU - Stringham,Heather M.

AU - Sung,Yun Ju

AU - Tanaka,Toshiko

AU - Teumer,Alexander

AU - Trompet,Stella

AU - Van Der Laan,Sander W.

AU - Van Der Most,Peter J.

AU - Van Vliet-Ostaptchouk,Jana V.

AU - Vedantam,Sailaja L.

AU - Verweij,Niek

AU - Vink,Jacqueline M.

AU - Vitart,Veronique

AU - Wu,Ying

AU - Yengo,Loic

AU - Zhang,Weihua

AU - Zhao,Jing Hua

AU - Zimmermann,Martina E.

AU - Zubair,Niha

AU - Abecasis,Gonçalo R.

AU - Adair,Linda S.

AU - Afaq,Saima

AU - Afzal,Uzma

AU - Bakker,Stephan J.L.

AU - Bartz,Traci M.

AU - Beilby,John

AU - Bergman,Richard N.

AU - Bergmann,Sven

AU - Biffar,Reiner

AU - Blangero,John

AU - Boerwinkle,Eric

AU - Bonnycastle,Lori L.

AU - Bottinger,Erwin

AU - Braga,Daniele

AU - Buckley,Brendan M.

AU - Buyske,Steve

AU - Campbell,Harry

AU - Chambers,John C.

AU - Collins,Francis S.

AU - Curran,Joanne E.

AU - De Borst,Gert J.

AU - De Craen,Anton J.M.

AU - De Geus,Eco J.C.

AU - Dedoussis,George

AU - Delgado,Graciela E.

AU - Den Ruijter,Hester M.

AU - Eiriksdottir,Gudny

AU - Eriksson,Anna L.

AU - Esko,Toñu

AU - Faul,Jessica D.

AU - Ford,Ian

AU - Forrester,Terrence

AU - Gertow,Karl

AU - Gigante,Bruna

AU - Glorioso,Nicola

AU - Gong,Jian

AU - Grallert,Harald

AU - Grammer,Tanja B.

AU - Grarup,Niels

AU - Haitjema,Saskia

AU - Hallmans,Göran

AU - Hamsten,Anders

AU - Hansen,Torben

AU - Harris,Tamara B.

AU - Hartman,Catharina A.

AU - Hassinen,Maija

AU - Hastie,Nicholas D.

AU - Heath,Andrew C.

AU - Hernandez,Dena

AU - Hindorff,Lucia

AU - Hocking,Lynne J.

AU - Hollensted,Mette

AU - Holmen,Oddgeir L.

AU - Homuth,Georg

AU - Hottenga,Jouke Jan

AU - Huang,Jie

AU - Hung,Joseph

AU - Hutri-Kähönen,Nina

AU - Ingelsson,Erik

AU - James,Alan L.

AU - Jansson,John Olov

AU - Jarvelin,Marjo Riitta

AU - Jhun,Min A.

AU - Jorgensen,Marit E.

AU - Juonala,Markus

AU - Kähönen,Mika

AU - Karlsson,Magnus

AU - Koistinen,Heikki A.

AU - Kolcic,Ivana

AU - Kolovou,Genovefa

AU - Kooperberg,Charles

AU - Krämer,Bernhard K.

AU - Kuusisto,Johanna

AU - Kvaloy,Kirsti

AU - Lakka,Timo A.

AU - Langenberg,Claudia

AU - Launer,Lenore J.

AU - Leander,Karin

AU - Lee,Nanette R.

AU - Lind,Lars

AU - Lindgren,Cecilia M.

AU - Linneberg,Allan

AU - Lobbens,Stephane

AU - Loh,Marie

AU - Lorentzon,Mattias

AU - Luben,Robert

AU - Lubke,Gitta

AU - Ludolph-Donislawski,Anja

AU - Lupoli,Sara

AU - Madden,Pamela A.F.

AU - Männikkö,Reija

AU - Marques-Vidal,Pedro

AU - Martin,Nicholas G.

AU - McKenzie,Colin A.

AU - McKnight,Barbara

AU - Mellström,Dan

AU - Menni,Cristina

AU - Montgomery,Grant W.

AU - Musk,A. W.

AU - Narisu,Narisu

AU - Nauck,Matthias

AU - Nolte,Ilja M.

AU - Oldehinkel,Albertine J.

AU - Olden,Matthias

AU - Ong,Ken K.

AU - Padmanabhan,Sandosh

AU - Peyser,Patricia A.

AU - Pisinger,Charlotta

AU - Porteous,David J.

AU - Raitakari,Olli T.

AU - Rankinen,Tuomo

AU - Rao,D. C.

AU - Rasmussen-Torvik,Laura J.

AU - Rawal,Rajesh

AU - Rice,Treva

AU - Ridker,Paul M.

AU - Rose,Lynda M.

AU - Bien,Stephanie A.

AU - Rudan,Igor

AU - Sanna,Serena

AU - Sarzynski,Mark A.

AU - Sattar,Naveed

AU - Savonen,Kai

AU - Schlessinger,David

AU - Scholtens,Salome

AU - Schurmann,Claudia

AU - Scott,Robert A.

AU - Sennblad,Bengt

AU - Siemelink,Marten A.

AU - Silbernagel,Günther

AU - Slagboom,P. Eline

AU - Snieder,Harold

AU - Staessen,Jan A.

AU - Stott,David J.

AU - Swertz,Morris A.

AU - Swift,Amy J.

AU - Taylor,Kent D.

AU - Tayo,Bamidele O.

AU - Thorand,Barbara

AU - Thuillier,Dorothee

AU - Tuomilehto,Jaakko

AU - Uitterlinden,Andre G.

AU - Vandenput,Liesbeth

AU - Vohl,Marie Claude

AU - Völzke,Henry

AU - Vonk,Judith M.

AU - Waeber,Ge'rard

AU - Waldenberger,Melanie

AU - Westendorp,R. G.J.

AU - Wild,Sarah

AU - Willemsen,Gonneke

AU - Wolffenbuttel,Bruce H.R.

AU - Wong,Andrew

AU - Wright,Alan F.

AU - Zhao,Wei

AU - Zillikens,M. Carola

AU - Baldassarre,Damiano

AU - Balkau,Beverley

AU - Bandinelli,Stefania

AU - Böger,Carsten A.

AU - Boomsma,Dorret I.

AU - Bouchard,Claude

AU - Bruinenberg,Marcel

AU - Chasman,Daniel I.

AU - Ida Chen,Yii Der

AU - Chines,Peter S.

AU - Cooper,Richard S.

AU - Cucca,Francesco

AU - Cusi,Daniele

AU - De Faire,Ulf

AU - Ferrucci,Luigi

AU - Franks,Paul W.

AU - Froguel,Philippe

AU - Gordon-Larsen,Penny

AU - Grabe,Hans Jörgen

AU - Gudnason,Vilmundur

AU - Haiman,Christopher A.

AU - Hayward,Caroline

AU - Hveem,Kristian

AU - Johnson,Andrew D.

AU - Jukema,J. Wouter

AU - Kardia,Sharon L.R.

AU - Kivimaki,Mika

AU - Kooner,Jaspal S.

AU - Kuh,Diana

AU - Laakso,Markku

AU - Lehtimäki,Terho

AU - Le Marchand,Loic

AU - März,Winfried

AU - McCarthy,Mark I.

AU - Metspalu,Andres

AU - Morris,Andrew P.

AU - Ohlsson,Claes

AU - Palmer,Lyle J.

AU - Pasterkamp,Gerard

AU - Pedersen,Oluf

AU - Peters,Annette

AU - Peters,Ulrike

AU - Polasek,Ozren

AU - Psaty,Bruce M.

AU - Qi,Lu

AU - Rauramaa,Rainer

AU - Smith,Blair H.

AU - Sorensen,Thorkild I.A.

AU - Strauch,Konstantin

AU - Tiemeier,Henning

AU - Tremoli,Elena

AU - Van Der Harst,Pim

AU - Vestergaard,Henrik

AU - Vollenweider,Peter

AU - Wareham,Nicholas J.

AU - Weir,David R.

AU - Whitfield,John B.

AU - Wilson,James F.

AU - Tyrrell,Jessica

AU - Frayling,Timothy M.

AU - Barroso,Inês

AU - Boehnke,Michael

AU - Deloukas,Panagiotis

AU - Fox,Caroline S.

AU - Hirschhorn,Joel N.

AU - Hunter,David J.

AU - Spector,Tim D.

AU - Strachan,David P.

AU - Van Duijn,Cornelia M.

AU - Heid,Iris M.

AU - Mohlke,Karen L.

AU - Marchini,Jonathan

AU - Loos,Ruth J.F.

AU - Kilpeläinen,Tuomas O.

AU - Liu,Ching Ti

AU - Borecki,Ingrid B.

AU - North,Kari E.

AU - Cupples,L. Adrienne

PY - 2017/4/26

Y1 - 2017/4/26

N2 - Few genome-wide association studies (GWAS) account for environmental exposures, like smoking, potentially impacting the overall trait variance when investigating the genetic contribution to obesity-related traits. Here, we use GWAS data from 51,080 current smokers and 190,178 nonsmokers (87% European descent) to identify loci influencing BMI and central adiposity, measured as waist circumference and waist-to-hip ratio both adjusted for BMI. We identify 23 novel genetic loci, and 9 loci with convincing evidence of gene-smoking interaction (GxSMK) on obesity-related traits. We show consistent direction of effect for all identified loci and significance for 18 novel and for 5 interaction loci in an independent study sample. These loci highlight novel biological functions, including response to oxidative stress, addictive behaviour, and regulatory functions emphasizing the importance of accounting for environment in genetic analyses. Our results suggest that tobacco smoking may alter the genetic susceptibility to overall adiposity and body fat distribution.

AB - Few genome-wide association studies (GWAS) account for environmental exposures, like smoking, potentially impacting the overall trait variance when investigating the genetic contribution to obesity-related traits. Here, we use GWAS data from 51,080 current smokers and 190,178 nonsmokers (87% European descent) to identify loci influencing BMI and central adiposity, measured as waist circumference and waist-to-hip ratio both adjusted for BMI. We identify 23 novel genetic loci, and 9 loci with convincing evidence of gene-smoking interaction (GxSMK) on obesity-related traits. We show consistent direction of effect for all identified loci and significance for 18 novel and for 5 interaction loci in an independent study sample. These loci highlight novel biological functions, including response to oxidative stress, addictive behaviour, and regulatory functions emphasizing the importance of accounting for environment in genetic analyses. Our results suggest that tobacco smoking may alter the genetic susceptibility to overall adiposity and body fat distribution.

UR - http://www.scopus.com/inward/record.url?scp=85019322396&partnerID=8YFLogxK

U2 - 10.1038/ncomms14977

DO - 10.1038/ncomms14977

M3 - Article

VL - 8

JO - NATURE COMMUNICATIONS

T2 - NATURE COMMUNICATIONS

JF - NATURE COMMUNICATIONS

SN - 2041-1723

M1 - 14977

ER -

Justice AE, Winkler TW, Feitosa MF, Graff M, Fisher VA, Young K et al. Genome-wide meta-analysis of 241,258 adults accounting for smoking behaviour identifies novel loci for obesity traits. Nature Communications. 2017 Apr 26;8. 14977. Available from, DOI: 10.1038/ncomms14977