Genome-wide interaction study of smoking and bladder cancer risk

Jonine D. Figueroa; Summer S. Han; Montserrat Garcia-Closas; Dalsu Baris; Eric J. Jacobs; Manolis Kogevinas; Molly Schwenn; Nuria Malats; Alison Johnson; Mark P. Purdue; Neil Caporaso; Maria Teresa Landi; Ludmila Prokunina-Olsson; Zhaoming Wang; Amy Hutchinson; Laurie Burdette; William Wheeler; Paolo Vineis; Afshan Siddiq; Victoria K. Cortessis; Charles Kooperberg; Olivier Cussenot; Simone Benhamou; Jennifer Prescott; Stefano Porru; H. Bas Bueno-de-Mesquita; Dimitrios Trichopoulos; Börje Ljungberg; Françoise Clavel-Chapelon; Elisabete Weiderpass; Vittorio Krogh; Miren Dorronsoro; Ruth Travis; Anne Tjønneland; Paul Brenan; Jenny Chang-Claude; Elio Riboli; David Conti; Manuela Gago-Dominguez; Mariana C. Stern; Malcolm C. Pike; David van den Berg; Jian Min Yuan; Chancellor Hohensee; Rebecca Rodabough; Geraldine Cancel-Tassin; Morgan Roupret; Eva Comperat; Constance Chen; Immaculata de Vivo; Edward Giovannucci; David J. Hunter; Peter Kraft; Sara Lindstrom; Angela Carta; Sofia Pavanello; Cecilia Arici; Giuseppe Mastrangelo; Margaret R. Karagas; Alan Schned; Karla R. Armenti; G. M. Monawar Hosain; Chris A. Haiman; Joseph F. Fraumeni; Stephen J. Chanock; Nilanjan Chatterjee; Nathaniel Rothman; Debra T. Silverman

doi:10.1093/carcin/bgu064

Genome-wide interaction study of smoking and bladder cancer risk

Jonine D. Figueroa, Summer S. Han, Montserrat Garcia-Closas, Dalsu Baris, Eric J. Jacobs, Manolis Kogevinas, Molly Schwenn, Nuria Malats, Alison Johnson, Mark P. Purdue, Neil Caporaso, Maria Teresa Landi, Ludmila Prokunina-Olsson, Zhaoming Wang, Amy Hutchinson, Laurie Burdette, William Wheeler, Paolo Vineis, Afshan Siddiq, Victoria K. CortessisCharles Kooperberg, Olivier Cussenot, Simone Benhamou, Jennifer Prescott, Stefano Porru, H. Bas Bueno-de-Mesquita, Dimitrios Trichopoulos, Börje Ljungberg, Françoise Clavel-Chapelon, Elisabete Weiderpass, Vittorio Krogh, Miren Dorronsoro, Ruth Travis, Anne Tjønneland, Paul Brenan, Jenny Chang-Claude, Elio Riboli, David Conti, Manuela Gago-Dominguez, Mariana C. Stern, Malcolm C. Pike, David van den Berg, Jian Min Yuan, Chancellor Hohensee, Rebecca Rodabough, Geraldine Cancel-Tassin, Morgan Roupret, Eva Comperat, Constance Chen, Immaculata de Vivo, Edward Giovannucci, David J. Hunter, Peter Kraft, Sara Lindstrom, Angela Carta, Sofia Pavanello, Cecilia Arici, Giuseppe Mastrangelo, Margaret R. Karagas, Alan Schned, Karla R. Armenti, G. M. Monawar Hosain, Chris A. Haiman, Joseph F. Fraumeni, Stephen J. Chanock, Nilanjan Chatterjee, Nathaniel Rothman, Debra T. Silverman

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

36 Scopus citations

Abstract

Bladder cancer is a complex disease with known environmental and genetic risk factors. We performed a genome-wide interaction study of smoking and bladder cancer risk based on primary scan data from 3,002 cases and 4,411 controls from the NCI Bladder Cancer Genome-Wide Association Study (GWAS). Alternative methods were used to evaluate both additive and multiplicative interactions between individual single nucleotide polymorphisms (SNPs) and smoking exposure. SNPs with interaction P-values <5x10^-5 were evaluated further in an independent dataset of 2,422 bladder cancer cases and 5,751 controls. We identified 10 SNPs that showed association in a consistent manner with the initial data set and in the combined data set, providing evidence of interaction with tobacco use. Further, two of these novel SNPs showed strong evidence of association with bladder cancer in tobacco use subgroups that approached genome-wide significance. Specifically, rs1711973 (FOXF2) on 6p25.3 was a susceptibility SNP for never smokers (combined OR=1.34, 95% CI=1.20-1.50, P-value=5.18x10^-7); and rs12216499 (RSPH3-TAGAP-EZR) on 6q25.3 was a susceptibility SNP for ever smokers (combined OR=0.75, 95% CI=0.67-0.84, P-value=6.35x10^-7). In our analysis of smoking and bladder cancer, the tests for multiplicative interaction seemed to more commonly identify susceptibility loci with associations in never smokers, while the additive interaction analysis identified more loci with associations among smokers-including the known smoking and NAT2 acetylation interaction. Our findings provide additional evidence of gene-environment interactions for tobacco and bladder cancer.

Original language	English (US)
Pages (from-to)	1737-1744
Number of pages	8
Journal	Carcinogenesis
Volume	35
Issue number	8
DOIs	https://doi.org/10.1093/carcin/bgu064
State	Published - Aug 2014
Externally published	Yes

Keywords

Bladder cancer
Gene-environment interaction

ASJC Scopus subject areas

Cancer Research

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10.1093/carcin/bgu064

Cite this

Figueroa, J. D., Han, S. S., Garcia-Closas, M., Baris, D., Jacobs, E. J., Kogevinas, M., Schwenn, M., Malats, N., Johnson, A., Purdue, M. P., Caporaso, N., Landi, M. T., Prokunina-Olsson, L., Wang, Z., Hutchinson, A., Burdette, L., Wheeler, W., Vineis, P., Siddiq, A., ... Silverman, D. T. (2014). Genome-wide interaction study of smoking and bladder cancer risk. Carcinogenesis, 35(8), 1737-1744. https://doi.org/10.1093/carcin/bgu064

Figueroa, JD, Han, SS, Garcia-Closas, M, Baris, D, Jacobs, EJ, Kogevinas, M, Schwenn, M, Malats, N, Johnson, A, Purdue, MP, Caporaso, N, Landi, MT, Prokunina-Olsson, L, Wang, Z, Hutchinson, A, Burdette, L, Wheeler, W, Vineis, P, Siddiq, A, Cortessis, VK, Kooperberg, C, Cussenot, O, Benhamou, S, Prescott, J, Porru, S, Bas Bueno-de-Mesquita, H, Trichopoulos, D, Ljungberg, B, Clavel-Chapelon, F, Weiderpass, E, Krogh, V, Dorronsoro, M, Travis, R, Tjønneland, A, Brenan, P, Chang-Claude, J, Riboli, E, Conti, D, Gago-Dominguez, M, Stern, MC, Pike, MC, van den Berg, D, Yuan, JM, Hohensee, C, Rodabough, R, Cancel-Tassin, G, Roupret, M, Comperat, E, Chen, C, de Vivo, I, Giovannucci, E, Hunter, DJ, Kraft, P, Lindstrom, S, Carta, A, Pavanello, S, Arici, C, Mastrangelo, G, Karagas, MR, Schned, A, Armenti, KR, Monawar Hosain, GM, Haiman, CA, Fraumeni, JF, Chanock, SJ, Chatterjee, N, Rothman, N & Silverman, DT 2014, 'Genome-wide interaction study of smoking and bladder cancer risk', Carcinogenesis, vol. 35, no. 8, pp. 1737-1744. https://doi.org/10.1093/carcin/bgu064

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title = "Genome-wide interaction study of smoking and bladder cancer risk",

abstract = "Bladder cancer is a complex disease with known environmental and genetic risk factors. We performed a genome-wide interaction study of smoking and bladder cancer risk based on primary scan data from 3,002 cases and 4,411 controls from the NCI Bladder Cancer Genome-Wide Association Study (GWAS). Alternative methods were used to evaluate both additive and multiplicative interactions between individual single nucleotide polymorphisms (SNPs) and smoking exposure. SNPs with interaction P-values <5x10-5 were evaluated further in an independent dataset of 2,422 bladder cancer cases and 5,751 controls. We identified 10 SNPs that showed association in a consistent manner with the initial data set and in the combined data set, providing evidence of interaction with tobacco use. Further, two of these novel SNPs showed strong evidence of association with bladder cancer in tobacco use subgroups that approached genome-wide significance. Specifically, rs1711973 (FOXF2) on 6p25.3 was a susceptibility SNP for never smokers (combined OR=1.34, 95% CI=1.20-1.50, P-value=5.18x10-7); and rs12216499 (RSPH3-TAGAP-EZR) on 6q25.3 was a susceptibility SNP for ever smokers (combined OR=0.75, 95% CI=0.67-0.84, P-value=6.35x10-7). In our analysis of smoking and bladder cancer, the tests for multiplicative interaction seemed to more commonly identify susceptibility loci with associations in never smokers, while the additive interaction analysis identified more loci with associations among smokers-including the known smoking and NAT2 acetylation interaction. Our findings provide additional evidence of gene-environment interactions for tobacco and bladder cancer.",

keywords = "Bladder cancer, Gene-environment interaction",

author = "Figueroa, {Jonine D.} and Han, {Summer S.} and Montserrat Garcia-Closas and Dalsu Baris and Jacobs, {Eric J.} and Manolis Kogevinas and Molly Schwenn and Nuria Malats and Alison Johnson and Purdue, {Mark P.} and Neil Caporaso and Landi, {Maria Teresa} and Ludmila Prokunina-Olsson and Zhaoming Wang and Amy Hutchinson and Laurie Burdette and William Wheeler and Paolo Vineis and Afshan Siddiq and Cortessis, {Victoria K.} and Charles Kooperberg and Olivier Cussenot and Simone Benhamou and Jennifer Prescott and Stefano Porru and {Bas Bueno-de-Mesquita}, H. and Dimitrios Trichopoulos and B{\"o}rje Ljungberg and Fran{\c c}oise Clavel-Chapelon and Elisabete Weiderpass and Vittorio Krogh and Miren Dorronsoro and Ruth Travis and Anne Tj{\o}nneland and Paul Brenan and Jenny Chang-Claude and Elio Riboli and David Conti and Manuela Gago-Dominguez and Stern, {Mariana C.} and Pike, {Malcolm C.} and {van den Berg}, David and Yuan, {Jian Min} and Chancellor Hohensee and Rebecca Rodabough and Geraldine Cancel-Tassin and Morgan Roupret and Eva Comperat and Constance Chen and {de Vivo}, Immaculata and Edward Giovannucci and Hunter, {David J.} and Peter Kraft and Sara Lindstrom and Angela Carta and Sofia Pavanello and Cecilia Arici and Giuseppe Mastrangelo and Karagas, {Margaret R.} and Alan Schned and Armenti, {Karla R.} and {Monawar Hosain}, {G. M.} and Haiman, {Chris A.} and Fraumeni, {Joseph F.} and Chanock, {Stephen J.} and Nilanjan Chatterjee and Nathaniel Rothman and Silverman, {Debra T.}",

year = "2014",

month = aug,

doi = "10.1093/carcin/bgu064",

language = "English (US)",

volume = "35",

pages = "1737--1744",

journal = "Carcinogenesis",

issn = "0143-3334",

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number = "8",

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T1 - Genome-wide interaction study of smoking and bladder cancer risk

AU - Figueroa, Jonine D.

AU - Han, Summer S.

AU - Garcia-Closas, Montserrat

AU - Baris, Dalsu

AU - Jacobs, Eric J.

AU - Kogevinas, Manolis

AU - Schwenn, Molly

AU - Malats, Nuria

AU - Johnson, Alison

AU - Purdue, Mark P.

AU - Caporaso, Neil

AU - Landi, Maria Teresa

AU - Prokunina-Olsson, Ludmila

AU - Wang, Zhaoming

AU - Hutchinson, Amy

AU - Burdette, Laurie

AU - Wheeler, William

AU - Vineis, Paolo

AU - Siddiq, Afshan

AU - Cortessis, Victoria K.

AU - Kooperberg, Charles

AU - Cussenot, Olivier

AU - Benhamou, Simone

AU - Prescott, Jennifer

AU - Porru, Stefano

AU - Bas Bueno-de-Mesquita, H.

AU - Trichopoulos, Dimitrios

AU - Ljungberg, Börje

AU - Clavel-Chapelon, Françoise

AU - Weiderpass, Elisabete

AU - Krogh, Vittorio

AU - Dorronsoro, Miren

AU - Travis, Ruth

AU - Tjønneland, Anne

AU - Brenan, Paul

AU - Chang-Claude, Jenny

AU - Riboli, Elio

AU - Conti, David

AU - Gago-Dominguez, Manuela

AU - Stern, Mariana C.

AU - Pike, Malcolm C.

AU - van den Berg, David

AU - Yuan, Jian Min

AU - Hohensee, Chancellor

AU - Rodabough, Rebecca

AU - Cancel-Tassin, Geraldine

AU - Roupret, Morgan

AU - Comperat, Eva

AU - Chen, Constance

AU - de Vivo, Immaculata

AU - Giovannucci, Edward

AU - Hunter, David J.

AU - Kraft, Peter

AU - Lindstrom, Sara

AU - Carta, Angela

AU - Pavanello, Sofia

AU - Arici, Cecilia

AU - Mastrangelo, Giuseppe

AU - Karagas, Margaret R.

AU - Schned, Alan

AU - Armenti, Karla R.

AU - Monawar Hosain, G. M.

AU - Haiman, Chris A.

AU - Fraumeni, Joseph F.

AU - Chanock, Stephen J.

AU - Chatterjee, Nilanjan

AU - Rothman, Nathaniel

AU - Silverman, Debra T.

PY - 2014/8

Y1 - 2014/8

N2 - Bladder cancer is a complex disease with known environmental and genetic risk factors. We performed a genome-wide interaction study of smoking and bladder cancer risk based on primary scan data from 3,002 cases and 4,411 controls from the NCI Bladder Cancer Genome-Wide Association Study (GWAS). Alternative methods were used to evaluate both additive and multiplicative interactions between individual single nucleotide polymorphisms (SNPs) and smoking exposure. SNPs with interaction P-values <5x10-5 were evaluated further in an independent dataset of 2,422 bladder cancer cases and 5,751 controls. We identified 10 SNPs that showed association in a consistent manner with the initial data set and in the combined data set, providing evidence of interaction with tobacco use. Further, two of these novel SNPs showed strong evidence of association with bladder cancer in tobacco use subgroups that approached genome-wide significance. Specifically, rs1711973 (FOXF2) on 6p25.3 was a susceptibility SNP for never smokers (combined OR=1.34, 95% CI=1.20-1.50, P-value=5.18x10-7); and rs12216499 (RSPH3-TAGAP-EZR) on 6q25.3 was a susceptibility SNP for ever smokers (combined OR=0.75, 95% CI=0.67-0.84, P-value=6.35x10-7). In our analysis of smoking and bladder cancer, the tests for multiplicative interaction seemed to more commonly identify susceptibility loci with associations in never smokers, while the additive interaction analysis identified more loci with associations among smokers-including the known smoking and NAT2 acetylation interaction. Our findings provide additional evidence of gene-environment interactions for tobacco and bladder cancer.

AB - Bladder cancer is a complex disease with known environmental and genetic risk factors. We performed a genome-wide interaction study of smoking and bladder cancer risk based on primary scan data from 3,002 cases and 4,411 controls from the NCI Bladder Cancer Genome-Wide Association Study (GWAS). Alternative methods were used to evaluate both additive and multiplicative interactions between individual single nucleotide polymorphisms (SNPs) and smoking exposure. SNPs with interaction P-values <5x10-5 were evaluated further in an independent dataset of 2,422 bladder cancer cases and 5,751 controls. We identified 10 SNPs that showed association in a consistent manner with the initial data set and in the combined data set, providing evidence of interaction with tobacco use. Further, two of these novel SNPs showed strong evidence of association with bladder cancer in tobacco use subgroups that approached genome-wide significance. Specifically, rs1711973 (FOXF2) on 6p25.3 was a susceptibility SNP for never smokers (combined OR=1.34, 95% CI=1.20-1.50, P-value=5.18x10-7); and rs12216499 (RSPH3-TAGAP-EZR) on 6q25.3 was a susceptibility SNP for ever smokers (combined OR=0.75, 95% CI=0.67-0.84, P-value=6.35x10-7). In our analysis of smoking and bladder cancer, the tests for multiplicative interaction seemed to more commonly identify susceptibility loci with associations in never smokers, while the additive interaction analysis identified more loci with associations among smokers-including the known smoking and NAT2 acetylation interaction. Our findings provide additional evidence of gene-environment interactions for tobacco and bladder cancer.

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KW - Gene-environment interaction

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VL - 35

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JO - Carcinogenesis

JF - Carcinogenesis

IS - 8

ER -

Genome-wide interaction study of smoking and bladder cancer risk

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