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Multicenter Study
. 2019 Aug 1;28(15):2615-2633.
doi: 10.1093/hmg/ddz070.

A multi-ancestry genome-wide study incorporating gene-smoking interactions identifies multiple new loci for pulse pressure and mean arterial pressure

Yun Ju Sung  1 , Lisa de las Fuentes  1   2 , Thomas W Winkler  3 , Daniel I Chasman  4 , Amy R Bentley  5 , Aldi T Kraja  6 , Ioanna Ntalla  7 , Helen R Warren  7   8 , Xiuqing Guo  9 , Karen Schwander  1 , Alisa K Manning  10   11 , Michael R Brown  12 , Hugues Aschard  13   14 , Mary F Feitosa  6 , Nora Franceschini  15 , Yingchang Lu  16 , Ching-Yu Cheng  17   18   19 , Xueling Sim  20 , Dina Vojinovic  21 , Jonathan Marten  22 , Solomon K Musani  23 , Tuomas O Kilpeläinen  24   25 , Melissa A Richard  26 , Stella Aslibekyan  27 , Traci M Bartz  28 , Rajkumar Dorajoo  29 , Changwei Li  30 , Yongmei Liu  31 , Tuomo Rankinen  32 , Albert Vernon Smith  33   34 , Salman M Tajuddin  35 , Bamidele O Tayo  36 , Wei Zhao  37 , Yanhua Zhou  38 , Nana Matoba  39 , Tamar Sofer  40   41 , Maris Alver  42 , Marzyeh Amini  43 , Mathilde Boissel  44 , Jin Fang Chai  20 , Xu Chen  45 , Jasmin Divers  46 , Ilaria Gandin  47 , Chuan Gao  48 , Franco Giulianini  4 , Anuj Goel  49   50 , Sarah E Harris  51   52 , Fernando P Hartwig  53   54 , Meian He  55 , Andrea R V R Horimoto  56 , Fang-Chi Hsu  46 , Anne U Jackson  57 , Candace M Kammerer  58 , Anuradhani Kasturiratne  59 , Pirjo Komulainen  60 , Brigitte Kühnel  61   62 , Karin Leander  63 , Wen-Jane Lee  64 , Keng-Hung Lin  65 , Jian'an Luan  66 , Leo-Pekka Lyytikäinen  67   68 , Colin A McKenzie  69 , Christopher P Nelson  70   71 , Raymond Noordam  72 , Robert A Scott  66 , Wayne H H Sheu  73   74   75   76 , Alena Stančáková  77 , Fumihiko Takeuchi  78 , Peter J van der Most  43 , Tibor V Varga  79 , Robert J Waken  1 , Heming Wang  40   41 , Yajuan Wang  80 , Erin B Ware  37   81 , Stefan Weiss  82   83 , Wanqing Wen  84 , Lisa R Yanek  85 , Weihua Zhang  86   87 , Jing Hua Zhao  66 , Saima Afaq  86 , Tamuno Alfred  16 , Najaf Amin  21 , Dan E Arking  88 , Tin Aung  17   18   19 , R Graham Barr  89 , Lawrence F Bielak  37 , Eric Boerwinkle  12   90 , Erwin P Bottinger  16 , Peter S Braund  70   71 , Jennifer A Brody  91 , Ulrich Broeckel  92 , Brian Cade  41 , Archie Campbell  93 , Mickaël Canouil  44 , Aravinda Chakravarti  88 , Massimiliano Cocca  47 , Francis S Collins  94 , John M Connell  95 , Renée de Mutsert  96 , H Janaka de Silva  97 , Marcus Dörr  83   98 , Qing Duan  99 , Charles B Eaton  100 , Georg Ehret  88   101 , Evangelos Evangelou  86   102 , Jessica D Faul  81 , Nita G Forouhi  66 , Oscar H Franco  21 , Yechiel Friedlander  103 , He Gao  86 , Bruna Gigante  63 , C Charles Gu  1 , Preeti Gupta  17 , Saskia P Hagenaars  51   104 , Tamara B Harris  105 , Jiang He  106   107 , Sami Heikkinen  77   108 , Chew-Kiat Heng  109   110 , Albert Hofman  21 , Barbara V Howard  111   112 , Steven C Hunt  113   114 , Marguerite R Irvin  115 , Yucheng Jia  9 , Tomohiro Katsuya  116   117 , Joel Kaufman  118 , Nicola D Kerrison  66 , Chiea Chuen Khor  29   119 , Woon-Puay Koh  20   120 , Heikki A Koistinen  121   122   123 , Charles B Kooperberg  124 , Jose E Krieger  56 , Michiaki Kubo  125 , Zoltan Kutalik  126   127 , Johanna Kuusisto  77 , Timo A Lakka  60   108   128 , Carl D Langefeld  46 , Claudia Langenberg  66 , Lenore J Launer  105 , Joseph H Lee  129 , Benjamin Lehne  86 , Daniel Levy  130   131 , Cora E Lewis  132 , Yize Li  1 ; Lifelines Cohort Study; Sing Hui Lim  17 , Ching-Ti Liu  38 , Jianjun Liu  20   29 , Jingmin Liu  133 , Yeheng Liu  9 , Marie Loh  86   134 , Kurt K Lohman  46 , Tin Louie  135 , Reedik Mägi  42 , Koichi Matsuda  136 , Thomas Meitinger  137   138 , Andres Metspalu  42 , Lili Milani  2 , Yukihide Momozawa  139 , Thomas H Mosley Jr  140 , Mike A Nalls  141 , Ubaydah Nasri  9 , Jeff R O'Connell  142   143 , Adesola Ogunniyi  144 , Walter R Palmas  145 , Nicholette D Palmer  146 , James S Pankow  147 , Nancy L Pedersen  45 , Annette Peters  61   148 , Patricia A Peyser  37 , Ozren Polasek  149   150   151 , David Porteous  93 , Olli T Raitakari  152   153 , Frida Renström  79   154 , Treva K Rice  1 , Paul M Ridker  4 , Antonietta Robino  155 , Jennifer G Robinson  156 , Lynda M Rose  4 , Igor Rudan  157 , Charumathi Sabanayagam  17   18 , Babatunde L Salako  144 , Kevin Sandow  9 , Carsten O Schmidt  83   158 , Pamela J Schreiner  147 , William R Scott  86   159 , Peter Sever  160 , Mario Sims  23 , Colleen M Sitlani  91 , Blair H Smith  161 , Jennifer A Smith  37   81 , Harold Snieder  43 , John M Starr  51   162 , Konstantin Strauch  163   164 , Hua Tang  165 , Kent D Taylor  9 , Yik Ying Teo  20   29   166   167   168 , Yih Chung Tham  17 , André G Uitterlinden  169 , Melanie Waldenberger  60   61   65 , Lihua Wang  6 , Ya Xing Wang  170 , Wen Bin Wei  171 , Gregory Wilson  172 , Mary K Wojczynski  6 , Yong-Bing Xiang  173 , Jie Yao  9 , Jian-Min Yuan  174   175 , Alan B Zonderman  176 , Diane M Becker  85 , Michael Boehnke  56 , Donald W Bowden  146 , John C Chambers  86   87 , Yii-Der Ida Chen  9 , David R Weir  81 , Ulf de Faire  62 , Ian J Deary  51   104 , Tõnu Esko  42   177 , Martin Farrall  49   50 , Terrence Forrester  68 , Barry I Freedman  178 , Philippe Froguel  44   179 , Paolo Gasparini  47   114 , Christian Gieger  60   61   180 , Bernardo Lessa Horta  53 , Yi-Jen Hung  181 , Jost Bruno Jonas  171   182 , Norihiro Kato  78 , Jaspal S Kooner  87   159 , Markku Laakso  77 , Terho Lehtimäki  66   67 , Kae-Woei Liang  74   183   184 , Patrik K E Magnusson  45 , Albertine J Oldehinkel  185 , Alexandre C Pereira  55   186 , Thomas Perls  187 , Rainer Rauramaa  59 , Susan Redline  41 , Rainer Rettig  83   188 , Nilesh J Samani  70   71 , James Scott  159 , Xiao-Ou Shu  84 , Pim van der Harst  189 , Lynne E Wagenknecht  190 , Nicholas J Wareham  65 , Hugh Watkins  49   50 , Ananda R Wickremasinghe  58 , Tangchun Wu  69 , Yoichiro Kamatani  39 , Cathy C Laurie  135 , Claude Bouchard  32 , Richard S Cooper  36 , Michele K Evans  35 , Vilmundur Gudnason  33   34 , James Hixson  12 , Sharon L R Kardia  37 , Stephen B Kritchevsky  191 , Bruce M Psaty  192   193 , Rob M van Dam  20   194 , Donna K Arnett  195 , Dennis O Mook-Kanamori  96   196 , Myriam Fornage  26 , Ervin R Fox  197 , Caroline Hayward  22 , Cornelia M van Duijn  21 , E Shyong Tai  20   120   194 , Tien Yin Wong  17   18   19 , Ruth J F Loos  16   198 , Alex P Reiner  124 , Charles N Rotimi  5 , Laura J Bierut  199 , Xiaofeng Zhu  80 , L Adrienne Cupples  38 , Michael A Province  6 , Jerome I Rotter  9 , Paul W Franks  79   200   201 , Kenneth Rice  135 , Paul Elliott  86 , Mark J Caulfield  7   8 , W James Gauderman  202 , Patricia B Munroe  7   8 , Dabeeru C Rao  1 , Alanna C Morrison  12
Affiliations
Multicenter Study

A multi-ancestry genome-wide study incorporating gene-smoking interactions identifies multiple new loci for pulse pressure and mean arterial pressure

Yun Ju Sung et al. Hum Mol Genet. .

Abstract

Elevated blood pressure (BP), a leading cause of global morbidity and mortality, is influenced by both genetic and lifestyle factors. Cigarette smoking is one such lifestyle factor. Across five ancestries, we performed a genome-wide gene-smoking interaction study of mean arterial pressure (MAP) and pulse pressure (PP) in 129 913 individuals in stage 1 and follow-up analysis in 480 178 additional individuals in stage 2. We report here 136 loci significantly associated with MAP and/or PP. Of these, 61 were previously published through main-effect analysis of BP traits, 37 were recently reported by us for systolic BP and/or diastolic BP through gene-smoking interaction analysis and 38 were newly identified (P < 5 × 10-8, false discovery rate < 0.05). We also identified nine new signals near known loci. Of the 136 loci, 8 showed significant interaction with smoking status. They include CSMD1 previously reported for insulin resistance and BP in the spontaneously hypertensive rats. Many of the 38 new loci show biologic plausibility for a role in BP regulation. SLC26A7 encodes a chloride/bicarbonate exchanger expressed in the renal outer medullary collecting duct. AVPR1A is widely expressed, including in vascular smooth muscle cells, kidney, myocardium and brain. FHAD1 is a long non-coding RNA overexpressed in heart failure. TMEM51 was associated with contractile function in cardiomyocytes. CASP9 plays a central role in cardiomyocyte apoptosis. Identified only in African ancestry were 30 novel loci. Our findings highlight the value of multi-ancestry investigations, particularly in studies of interaction with lifestyle factors, where genomic and lifestyle differences may contribute to novel findings.

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Figures

Figure 1
Figure 1
Study design. Summary of data included in this study. Smk: smoking status (considering either current smoking or ever smoking status separately); PC: principal component; EUR: European; AFR: African; ASN: Asian; HIS: Hispanic; BRZ: Brazilian; TRANS; trans-ancestry (i.e. combining all ancestry groups through meta-analysis).
Figure 2
Figure 2
Venn diagram of loci/signals associated with the four BP traits. The diagram shows 133 loci and/or signals that were identified through gene–smoking interactions. In this paper, we newly identified 38 loci (Table 2) and 9 signals near known BP loci (Table 3) that are unique to MAP and/or PP (to a total of 49 new loci/signals). We had reported 81 loci associated with SBP/DBP (16), among which 37 showed association with MAP or PP. SBP: systolic blood pressure; DBP, diastolic blood pressure; MAP: mean arterial pressure; PP: pulse pressure.
Figure 3
Figure 3
Smoking-specific genetic effect sizes in African ancestry for MAP or PP. Among the 138 loci significantly associated with MAP and/or PP, 8 loci show significant interactions with smoking exposure status in African ancestry. Smoking-specific effect estimates and 95% confidence intervals for variants associated with BP traits are shown as red and blue squares for current-smokers and non-current smokers, respectively. SNP effects between two strata are significantly different (one DF interaction P < 5 × 10−8). These results were based on African-specific results in stage 1. MAP: mean arterial pressure; PP: pulse pressure; CS: current-smoking.
Figure 4
Figure 4
Smoking-specific estimates of variance explained in European ancestry. The variants with P ≤ 5 × 10-8 explained 1.9% of variance in MAP and 0.5% of variance in PP, whereas variants with P ≤ 10-4 explained 16% of variance in MAP and 11% of variance in PP. The vertical line corresponds to FDR = 0.1.
Figure 5
Figure 5
LocusZoom plots for four selected loci associated with MAP and/or PP. (A) rs140881076 (chr1:15364113) was identified in an analysis of individuals of African ancestry and is intronic to KAZN; neighboring genes have been implicated in cardiovascular traits. FHAD1 is a long non-coding RNA overexpressed in heart failure, TMEM51 has been associated with contractile function in cardiomyocytes and CASP9 plays a central role in cardiomyocyte apoptosis. (B) rs140994551 (chr8:4449086), intronic to CSMD1, shows interaction with current smoking in individuals of African ancestry. CSMD1 are shown to be associated with insulin resistance and BP in the spontaneously hypertensive rats. CSMD1 is also suggestively associated with studies of addiction and related disorders. (C) rs11991823 (chr8:92188440) was associated with PP in trans-ancestry analyses and in intronic to LRRC69. The nearby gene SLC26A7 encodes a chloride/bicarbonate exchanger expressed specifically in the renal outer medullary collecting duct. (D) rs146924684 (chr12:63437286) was associated with MAP in individuals of African ancestry. The nearby gene AVPR1A is widely expressed including in vascular smooth muscle cells, kidney, myocardium and brain. CurSmk: current smoking status; EverSmk: ever smoking status; MAP: mean arterial pressure; PP: pulse pressure. The plots were created using LocusZoom (http://locuszoom.sph.umich.edu/).
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