Genome-wide interaction study of smoking behavior and non-small cell lung cancer risk in Caucasian population

Yafang Li; Xiangjun Xiao; Younghun Han; Olga Gorlova; David Qian; Natasha Leighl; Jakob S. Johansen; Matt Barnett; Chu Chen; Gary Goodman; Angela Cox; Fiona Taylor; Penella Woll; H. Erich Wichmann; Judith Manz; Thomas Muley; Angela Risch; Albert Rosenberger; Susanne M. Arnold; Eric B. Haura; Ciprian Bolca; Ivana Holcatova; Vladimir Janout; Milica Kontic; Jolanta Lissowska; Anush Mukeria; Simona Ognjanovic; Tadeusz M. Orlowski; Ghislaine Scelo; Beata Swiatkowska; David Zaridze; Per Bakke; Vidar Skaug; Shanbeh Zienolddiny; Eric J. Duell; Lesley M. Butler; Richard Houlston; María Soler Artigas; Kjell Grankvist; Mikael Johansson; Frances A. Shepherd; Michael W. Marcus; Hans Brunnström; Jonas Manjer; Olle Melander; David C. Muller; Kim Overvad; Antonia Trichopoulou; Rosario Tumino; Geoffrey Liu; Stig E. Bojesen; Xifeng Wu; Loic Le Marchand; Demetrios Albanes; Heike Bickeböller; Melinda C. Aldrich; William S. Bush; Adonina Tardon; Gad Rennert; M. Dawn Teare; John K. Field; Lambertus A. Kiemeney; Philip Lazarus; Aage Haugen; Stephen Lam; Matthew B. Schabath; Angeline S. Andrew; Pier Alberto Bertazzi; Angela C. Pesatori; David C. Christiani; Neil Caporaso; Mattias Johansson; James D. McKay; Paul Brennan; Rayjean J. Hung; Christopher I. Amos

doi:10.1093/carcin/bgx113

Genome-wide interaction study of smoking behavior and non-small cell lung cancer risk in Caucasian population

Yafang Li
, Xiangjun Xiao
, Younghun Han
, Olga Gorlova
, David Qian
, Natasha Leighl
, Jakob S. Johansen
, Matt Barnett
, Chu Chen
, Gary Goodman
, Angela Cox
, Fiona Taylor
, Penella Woll
, H. Erich Wichmann
, Judith Manz
, Thomas Muley
, Angela Risch
, Albert Rosenberger
, Susanne M. Arnold
, Eric B. Haura

Ciprian Bolca, Ivana Holcatova, Vladimir Janout, Milica Kontic, Jolanta Lissowska, Anush Mukeria, Simona Ognjanovic, Tadeusz M. Orlowski, Ghislaine Scelo, Beata Swiatkowska, David Zaridze, Per Bakke, Vidar Skaug, Shanbeh Zienolddiny, Eric J. Duell, Lesley M. Butler, Richard Houlston, María Soler Artigas, Kjell Grankvist, Mikael Johansson, Frances A. Shepherd, Michael W. Marcus, Hans Brunnström, Jonas Manjer, Olle Melander, David C. Muller, Kim Overvad, Antonia Trichopoulou, Rosario Tumino, Geoffrey Liu, Stig E. Bojesen, Xifeng Wu, Loic Le Marchand, Demetrios Albanes, Heike Bickeböller, Melinda C. Aldrich, William S. Bush, Adonina Tardon, Gad Rennert, M. Dawn Teare, John K. Field, Lambertus A. Kiemeney, Philip Lazarus, Aage Haugen, Stephen Lam, Matthew B. Schabath, Angeline S. Andrew, Pier Alberto Bertazzi, Angela C. Pesatori, David C. Christiani, Neil Caporaso, Mattias Johansson, James D. McKay, Paul Brennan, Rayjean J. Hung, Christopher I. Amos

Pharmaceutical Sciences

Dartmouth College
University Health Network
University of Copenhagen
Fred Hutchinson Cancer Research Center
Swedish Medical Center
University of Sheffield
Helmholtz Zentrum München - German Research Center for Environmental Health
Heidelberg University
Member of the German Center for Lung Research (DZL)
University of Salzburg
University of Göttingen
University of Kentucky
Moffitt Cancer Center
Marius Nasta National Institute of Pneumology
University of Ostrava
University of Belgrade
Maria Sklodowska-Curie Institute of Oncology
Russian N.N. Blokhin Cancer Research Centre
International Organization for Cancer Prevention and Research
National Institute of Tuberculosis and Lung Diseases
International Agency for Research on Cancer
Nofer Institute of Occupational Medicine
University of Bergen
National Institute of Occupational Health
Institute Catala Oncologia
University of Pittsburgh
The Institute of Cancer Research
University of Leicester
University Hospitals of Leicester NHS Trust
Umeå University
University of Liverpool
Lund University
Imperial College London
Aarhus University
National and Kapodistrian University of Athens
Centro Per Lo Studio E La Prevenzione Oncologica
University of Texas MD Anderson Cancer Center
University of Hawai'i at Mānoa
National Institutes of Health
Vanderbilt University
Case Western Reserve University
University of Oviedo
Technion-Israel Institute of Technology
Radboud University Nijmegen
Provincial Health Services Authority
University of Milan
Harvard University
University of Toronto

Research output: Contribution to journal › Article › peer-review

32 Scopus citations

Abstract

Non-small cell lung cancer is the most common type of lung cancer. Both environmental and genetic risk factors contribute to lung carcinogenesis. We conducted a genome-wide interaction analysis between single nucleotide polymorphisms (SNPs) and smoking status (never- versus ever-smokers) in a European-descent population. We adopted a two-step analysis strategy in the discovery stage: we first conducted a case-only interaction analysis to assess the relationship between SNPs and smoking behavior using 13 336 non-small cell lung cancer cases. Candidate SNPs with P-value <0.001 were further analyzed using a standard case-control interaction analysis including 13 970 controls. The significant SNPs with P-value <3.5 × 10^-5 (correcting for multiple tests) from the case-control analysis in the discovery stage were further validated using an independent replication dataset comprising 5377 controls and 3054 non-small cell lung cancer cases. We further stratified the analysis by histological subtypes. Two novel SNPs, rs6441286 and rs17723637, were identified for overall lung cancer risk. The interaction odds ratio and meta-analysis P-value for these two SNPs were 1.24 with 6.96 × 10^-7 and 1.37 with 3.49 × 10^-7, respectively. In addition, interaction of smoking with rs4751674 was identified in squamous cell lung carcinoma with an odds ratio of 0.58 and P-value of 8.12 × 10^-7. This study is by far the largest genome-wide SNP-smoking interaction analysis reported for lung cancer. The three identified novel SNPs provide potential candidate biomarkers for lung cancer risk screening and intervention. The results from our study reinforce that gene-smoking interactions play important roles in the etiology of lung cancer and account for part of the missing heritability of this disease.

Original language	English
Pages (from-to)	336-346
Number of pages	11
Journal	Carcinogenesis
Volume	39
Issue number	3
DOIs	https://doi.org/10.1093/carcin/bgx113
State	Published - Mar 8 2018

Access to Document

10.1093/carcin/bgx113

Cite this

Li, Y., Xiao, X., Han, Y., Gorlova, O., Qian, D., Leighl, N., Johansen, J. S., Barnett, M., Chen, C., Goodman, G., Cox, A., Taylor, F., Woll, P., Wichmann, H. E., Manz, J., Muley, T., Risch, A., Rosenberger, A., Arnold, S. M., ... Amos, C. I. (2018). Genome-wide interaction study of smoking behavior and non-small cell lung cancer risk in Caucasian population. Carcinogenesis, 39(3), 336-346. https://doi.org/10.1093/carcin/bgx113

@article{68620627c6a441c3bd9ef44122aafa8e,

title = "Genome-wide interaction study of smoking behavior and non-small cell lung cancer risk in Caucasian population",

abstract = "Non-small cell lung cancer is the most common type of lung cancer. Both environmental and genetic risk factors contribute to lung carcinogenesis. We conducted a genome-wide interaction analysis between single nucleotide polymorphisms (SNPs) and smoking status (never- versus ever-smokers) in a European-descent population. We adopted a two-step analysis strategy in the discovery stage: we first conducted a case-only interaction analysis to assess the relationship between SNPs and smoking behavior using 13 336 non-small cell lung cancer cases. Candidate SNPs with P-value <0.001 were further analyzed using a standard case-control interaction analysis including 13 970 controls. The significant SNPs with P-value <3.5 × 10-5 (correcting for multiple tests) from the case-control analysis in the discovery stage were further validated using an independent replication dataset comprising 5377 controls and 3054 non-small cell lung cancer cases. We further stratified the analysis by histological subtypes. Two novel SNPs, rs6441286 and rs17723637, were identified for overall lung cancer risk. The interaction odds ratio and meta-analysis P-value for these two SNPs were 1.24 with 6.96 × 10-7 and 1.37 with 3.49 × 10-7, respectively. In addition, interaction of smoking with rs4751674 was identified in squamous cell lung carcinoma with an odds ratio of 0.58 and P-value of 8.12 × 10-7. This study is by far the largest genome-wide SNP-smoking interaction analysis reported for lung cancer. The three identified novel SNPs provide potential candidate biomarkers for lung cancer risk screening and intervention. The results from our study reinforce that gene-smoking interactions play important roles in the etiology of lung cancer and account for part of the missing heritability of this disease.",

author = "Yafang Li and Xiangjun Xiao and Younghun Han and Olga Gorlova and David Qian and Natasha Leighl and Johansen, \{Jakob S.\} and Matt Barnett and Chu Chen and Gary Goodman and Angela Cox and Fiona Taylor and Penella Woll and Wichmann, \{H. Erich\} and Judith Manz and Thomas Muley and Angela Risch and Albert Rosenberger and Arnold, \{Susanne M.\} and Haura, \{Eric B.\} and Ciprian Bolca and Ivana Holcatova and Vladimir Janout and Milica Kontic and Jolanta Lissowska and Anush Mukeria and Simona Ognjanovic and Orlowski, \{Tadeusz M.\} and Ghislaine Scelo and Beata Swiatkowska and David Zaridze and Per Bakke and Vidar Skaug and Shanbeh Zienolddiny and Duell, \{Eric J.\} and Butler, \{Lesley M.\} and Richard Houlston and Artigas, \{Mar{\'i}a Soler\} and Kjell Grankvist and Mikael Johansson and Shepherd, \{Frances A.\} and Marcus, \{Michael W.\} and Hans Brunnstr{\"o}m and Jonas Manjer and Olle Melander and Muller, \{David C.\} and Kim Overvad and Antonia Trichopoulou and Rosario Tumino and Geoffrey Liu and Bojesen, \{Stig E.\} and Xifeng Wu and Marchand, \{Loic Le\} and Demetrios Albanes and Heike Bickeb{\"o}ller and Aldrich, \{Melinda C.\} and Bush, \{William S.\} and Adonina Tardon and Gad Rennert and \{Dawn Teare\}, M. and Field, \{John K.\} and Kiemeney, \{Lambertus A.\} and Philip Lazarus and Aage Haugen and Stephen Lam and Schabath, \{Matthew B.\} and Andrew, \{Angeline S.\} and Bertazzi, \{Pier Alberto\} and Pesatori, \{Angela C.\} and Christiani, \{David C.\} and Neil Caporaso and Mattias Johansson and McKay, \{James D.\} and Paul Brennan and Hung, \{Rayjean J.\} and Amos, \{Christopher I.\}",

year = "2018",

month = mar,

day = "8",

doi = "10.1093/carcin/bgx113",

language = "English",

volume = "39",

pages = "336--346",

journal = "Carcinogenesis",

issn = "0143-3334",

publisher = "Oxford University Press",

number = "3",

}

Li, Y, Xiao, X, Han, Y, Gorlova, O, Qian, D, Leighl, N, Johansen, JS, Barnett, M, Chen, C, Goodman, G, Cox, A, Taylor, F, Woll, P, Wichmann, HE, Manz, J, Muley, T, Risch, A, Rosenberger, A, Arnold, SM, Haura, EB, Bolca, C, Holcatova, I, Janout, V, Kontic, M, Lissowska, J, Mukeria, A, Ognjanovic, S, Orlowski, TM, Scelo, G, Swiatkowska, B, Zaridze, D, Bakke, P, Skaug, V, Zienolddiny, S, Duell, EJ, Butler, LM, Houlston, R, Artigas, MS, Grankvist, K, Johansson, M, Shepherd, FA, Marcus, MW, Brunnström, H, Manjer, J, Melander, O, Muller, DC, Overvad, K, Trichopoulou, A, Tumino, R, Liu, G, Bojesen, SE, Wu, X, Marchand, LL, Albanes, D, Bickeböller, H, Aldrich, MC, Bush, WS, Tardon, A, Rennert, G, Dawn Teare, M, Field, JK, Kiemeney, LA, Lazarus, P, Haugen, A, Lam, S, Schabath, MB, Andrew, AS, Bertazzi, PA, Pesatori, AC, Christiani, DC, Caporaso, N, Johansson, M, McKay, JD, Brennan, P, Hung, RJ & Amos, CI 2018, 'Genome-wide interaction study of smoking behavior and non-small cell lung cancer risk in Caucasian population', Carcinogenesis, vol. 39, no. 3, pp. 336-346. https://doi.org/10.1093/carcin/bgx113

TY - JOUR

T1 - Genome-wide interaction study of smoking behavior and non-small cell lung cancer risk in Caucasian population

AU - Li, Yafang

AU - Xiao, Xiangjun

AU - Han, Younghun

AU - Gorlova, Olga

AU - Qian, David

AU - Leighl, Natasha

AU - Johansen, Jakob S.

AU - Barnett, Matt

AU - Chen, Chu

AU - Goodman, Gary

AU - Cox, Angela

AU - Taylor, Fiona

AU - Woll, Penella

AU - Wichmann, H. Erich

AU - Manz, Judith

AU - Muley, Thomas

AU - Risch, Angela

AU - Rosenberger, Albert

AU - Arnold, Susanne M.

AU - Haura, Eric B.

AU - Bolca, Ciprian

AU - Holcatova, Ivana

AU - Janout, Vladimir

AU - Kontic, Milica

AU - Lissowska, Jolanta

AU - Mukeria, Anush

AU - Ognjanovic, Simona

AU - Orlowski, Tadeusz M.

AU - Scelo, Ghislaine

AU - Swiatkowska, Beata

AU - Zaridze, David

AU - Bakke, Per

AU - Skaug, Vidar

AU - Zienolddiny, Shanbeh

AU - Duell, Eric J.

AU - Butler, Lesley M.

AU - Houlston, Richard

AU - Artigas, María Soler

AU - Grankvist, Kjell

AU - Johansson, Mikael

AU - Shepherd, Frances A.

AU - Marcus, Michael W.

AU - Brunnström, Hans

AU - Manjer, Jonas

AU - Melander, Olle

AU - Muller, David C.

AU - Overvad, Kim

AU - Trichopoulou, Antonia

AU - Tumino, Rosario

AU - Liu, Geoffrey

AU - Bojesen, Stig E.

AU - Wu, Xifeng

AU - Marchand, Loic Le

AU - Albanes, Demetrios

AU - Bickeböller, Heike

AU - Aldrich, Melinda C.

AU - Bush, William S.

AU - Tardon, Adonina

AU - Rennert, Gad

AU - Dawn Teare, M.

AU - Field, John K.

AU - Kiemeney, Lambertus A.

AU - Lazarus, Philip

AU - Haugen, Aage

AU - Lam, Stephen

AU - Schabath, Matthew B.

AU - Andrew, Angeline S.

AU - Bertazzi, Pier Alberto

AU - Pesatori, Angela C.

AU - Christiani, David C.

AU - Caporaso, Neil

AU - Johansson, Mattias

AU - McKay, James D.

AU - Brennan, Paul

AU - Hung, Rayjean J.

AU - Amos, Christopher I.

PY - 2018/3/8

Y1 - 2018/3/8

N2 - Non-small cell lung cancer is the most common type of lung cancer. Both environmental and genetic risk factors contribute to lung carcinogenesis. We conducted a genome-wide interaction analysis between single nucleotide polymorphisms (SNPs) and smoking status (never- versus ever-smokers) in a European-descent population. We adopted a two-step analysis strategy in the discovery stage: we first conducted a case-only interaction analysis to assess the relationship between SNPs and smoking behavior using 13 336 non-small cell lung cancer cases. Candidate SNPs with P-value <0.001 were further analyzed using a standard case-control interaction analysis including 13 970 controls. The significant SNPs with P-value <3.5 × 10-5 (correcting for multiple tests) from the case-control analysis in the discovery stage were further validated using an independent replication dataset comprising 5377 controls and 3054 non-small cell lung cancer cases. We further stratified the analysis by histological subtypes. Two novel SNPs, rs6441286 and rs17723637, were identified for overall lung cancer risk. The interaction odds ratio and meta-analysis P-value for these two SNPs were 1.24 with 6.96 × 10-7 and 1.37 with 3.49 × 10-7, respectively. In addition, interaction of smoking with rs4751674 was identified in squamous cell lung carcinoma with an odds ratio of 0.58 and P-value of 8.12 × 10-7. This study is by far the largest genome-wide SNP-smoking interaction analysis reported for lung cancer. The three identified novel SNPs provide potential candidate biomarkers for lung cancer risk screening and intervention. The results from our study reinforce that gene-smoking interactions play important roles in the etiology of lung cancer and account for part of the missing heritability of this disease.

AB - Non-small cell lung cancer is the most common type of lung cancer. Both environmental and genetic risk factors contribute to lung carcinogenesis. We conducted a genome-wide interaction analysis between single nucleotide polymorphisms (SNPs) and smoking status (never- versus ever-smokers) in a European-descent population. We adopted a two-step analysis strategy in the discovery stage: we first conducted a case-only interaction analysis to assess the relationship between SNPs and smoking behavior using 13 336 non-small cell lung cancer cases. Candidate SNPs with P-value <0.001 were further analyzed using a standard case-control interaction analysis including 13 970 controls. The significant SNPs with P-value <3.5 × 10-5 (correcting for multiple tests) from the case-control analysis in the discovery stage were further validated using an independent replication dataset comprising 5377 controls and 3054 non-small cell lung cancer cases. We further stratified the analysis by histological subtypes. Two novel SNPs, rs6441286 and rs17723637, were identified for overall lung cancer risk. The interaction odds ratio and meta-analysis P-value for these two SNPs were 1.24 with 6.96 × 10-7 and 1.37 with 3.49 × 10-7, respectively. In addition, interaction of smoking with rs4751674 was identified in squamous cell lung carcinoma with an odds ratio of 0.58 and P-value of 8.12 × 10-7. This study is by far the largest genome-wide SNP-smoking interaction analysis reported for lung cancer. The three identified novel SNPs provide potential candidate biomarkers for lung cancer risk screening and intervention. The results from our study reinforce that gene-smoking interactions play important roles in the etiology of lung cancer and account for part of the missing heritability of this disease.

UR - https://www.scopus.com/pages/publications/85043592947

U2 - 10.1093/carcin/bgx113

DO - 10.1093/carcin/bgx113

M3 - Article

C2 - 29059373

AN - SCOPUS:85043592947

SN - 0143-3334

VL - 39

SP - 336

EP - 346

JO - Carcinogenesis

JF - Carcinogenesis

IS - 3

ER -

Genome-wide interaction study of smoking behavior and non-small cell lung cancer risk in Caucasian population

Abstract

Access to Document

Other files and links

Fingerprint

Cite this