Identification of a novel susceptibility locus at 13q34 and refinement of the 20p12.2 region as a multi-signal locus associated with bladder cancer risk in individuals of european ancestry

Jonine D. Figueroa; Candace D. Middlebrooks; A. Rouf Banday; Yuanqing Ye; Montserrat Garcia-Closas; Nilanjan Chatterjee; Stella Koutros; Lambertus A. Kiemeney; Thorunn Rafnar; Timothy Bishop; Helena Furberg; Giuseppe Matullo; Klaus Golka; Manuela Gago-Dominguez; Jack A. Taylor; Tony Fletcher; Afshan Siddiq; Victoria K. Cortessis; Charles Kooperberg; Olivier Cussenot; Simone Benhamou; Jennifer Prescott; Stefano Porru; Colin P. Dinney; Núria Malats; Dalsu Baris; Mark P. Purdue; Eric J. Jacobs; Demetrius Albanes; Zhaoming Wang; Charles C. Chung; Sita H. Vermeulen; Katja K. Aben; Tessel E. Galesloot; Gudmar Thorleifsson; Patrick Sulem; Kari Stefansson; Anne E. Kiltie; Mark Harland; Mark Teo; Kenneth Offit; Joseph Vijai; Dean Bajorin; Ryan Kopp; Giovanni Fiorito; Simonetta Guarrera; Carlotta Sacerdote; Silvia Selinski; Jan G. Hengstler; Holger Gerullis

doi:10.1093/hmg/ddv492

Identification of a novel susceptibility locus at 13q34 and refinement of the 20p12.2 region as a multi-signal locus associated with bladder cancer risk in individuals of european ancestry

Jonine D. Figueroa^*, Candace D. Middlebrooks, A. Rouf Banday, Yuanqing Ye, Montserrat Garcia-Closas, Nilanjan Chatterjee, Stella Koutros, Lambertus A. Kiemeney, Thorunn Rafnar, Timothy Bishop, Helena Furberg, Giuseppe Matullo, Klaus Golka, Manuela Gago-Dominguez, Jack A. Taylor, Tony Fletcher, Afshan Siddiq, Victoria K. Cortessis, Charles Kooperberg, Olivier CussenotSimone Benhamou, Jennifer Prescott, Stefano Porru, Colin P. Dinney, Núria Malats, Dalsu Baris, Mark P. Purdue, Eric J. Jacobs, Demetrius Albanes, Zhaoming Wang, Charles C. Chung, Sita H. Vermeulen, Katja K. Aben, Tessel E. Galesloot, Gudmar Thorleifsson, Patrick Sulem, Kari Stefansson, Anne E. Kiltie, Mark Harland, Mark Teo, Kenneth Offit, Joseph Vijai, Dean Bajorin, Ryan Kopp, Giovanni Fiorito, Simonetta Guarrera, Carlotta Sacerdote, Silvia Selinski, Jan G. Hengstler, Holger Gerullis

^*Corresponding author for this work

The Rowett Institute of Nutrition and Health

University of Oxford

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

33 Citations (Scopus)

Abstract

Candidate gene and genome-wide association studies (GWAS) have identified 15 independent genomic regions associated with bladder cancer risk. In search for additional susceptibility variants, we followed up on four promising single-nucleotide polymorphisms (SNPs) that had not achieved genome-wide significance in 6911 cases and 11 814 controls (rs6104690, rs4510656, rs5003154 and rs4907479, P < 1 × 10^-6), using additional data from existing GWAS datasets and targeted genotyping for studies that did not have GWAS data. In a combined analysis, which included data on up to 15 058 cases and 286 270 controls, two SNPs achieved genome-wide statistical significance: Rs6104690 in a gene desert at 20p12.2 (P = 2.19 × 10^-11) and rs4907479 within the MCF2L gene at 13q34 (P = 3.3 × 10-10). Imputation and fine-mapping analyses were performed in these two regions for a subset of 5551 bladder cancer cases and 10 242 controls. Analyses at the 13q34 region suggest a single signal marked by rs4907479. In contrast, we detected two signals in the 20p12.2 region-the first signal is marked by rs6104690, and the second signal is marked by two moderately correlated SNPs (r² = 0.53), rs6108803 and the previously reported rs62185668. The second 20p12.2 signal is more strongly associated with the risk of muscle-invasive (T2-T4 stage) compared with non-muscle-invasive (Ta, T1 stage) bladder cancer (case-case P ≤ 0.02 for both rs62185668 and rs6108803). Functional analyses are needed to explore the biological mechanisms underlying these novel genetic associations with risk for bladder cancer. Published by Oxford University Press 2016. This work is written by (a) US Government employee(s) and is in the public domain in the US.

Original language	English
Pages (from-to)	1203-1214
Number of pages	12
Journal	Human Molecular Genetics
Volume	25
Issue number	6
DOIs	https://doi.org/10.1093/hmg/ddv492
Publication status	Published - 17 Aug 2015

Bibliographical note

Funding Information:
See Supplementary Material for funding details. The authors acknowledge the following: Marie Audouin, Cécile Gaffory, Valérie Ondet; Leslie Carroll (Information Management Services, Silver Spring, MD, USA); Gemma Castaño-Vinyals (Institut Municipal d’Investigació Mèdica, Barcelona, Spain); Francisco Fernández (Institut Municipal d’Investigació Mèdica, Barcelona, Spain); Anna McIntosh (Westat, Inc., Rockville, MD, USA); Robert Saal (Westat, Rockville, MD, USA); Francisco Real [Spanish National Cancer Research Centre (CNIO), Madrid, Spain]; Maria Sala (Institut Municipal d’Investigació Mèdica, Barcelona, Spain); Kirk Snyder (Information Management Services, Inc., Silver Spring, MD); Anne Taylor (Information Management Services, Inc., Silver Spring, MD); Montserrat Torà (Institut Municipal d’Investigació Mèdica, Barcelona, Spain); JaneWang (Information Management Services, Silver Spring, MD, USA). WHI Program Office: (National Heart, Lung, and Blood Institute, Bethesda, Maryland) Jacques Rossouw, Shari Ludlam, Dale Burwen, Joan McGowan, Leslie Ford, and Nancy Geller. Clinical Coordinating Center: Clinical Coordinating Center: (Fred Hutchinson Cancer Research Center, Seattle, WA) Garnet Anderson, Ross Prentice, Andrea LaCroix, and Charles Kooperberg. Investigators and Academic Centers: (Brigham and Women’s Hospital, Harvard Medical School, Boston, MA) JoAnn E. Manson; (MedStar Health Research Institute/Howard University, Washington, DC) Barbara V. Howard; (Stanford Prevention Research Center, Stanford, CA) Marcia L. Stefanick; (The Ohio State University, Columbus, OH) Rebecca Jackson; (University of Arizona, Tucson/ Phoenix, AZ) Cynthia A. Thomson; (University at Buffalo, Buffalo, NY) Jean Wactawski-Wende; (University of Florida, Gainesville/ Jacksonville, FL) Marian Limacher; (University of Iowa, Iowa City/Davenport, IA) Robert Wallace; (University of Pittsburgh, Pittsburgh, PA) Lewis Kuller; (Wake Forest University School of Medicine, Winston-Salem, NC) Sally Shumaker. Women’s Health Initiative Memory Study: (Wake Forest University School of Medicine, Winston-Salem, NC) Sally Shumaker. For a list of all the investigators who have contributed to WHI science, please visit: https://cleo.whi.org/researchers/SitePages/ Write%20a%20Paper.aspx. The Memorial Sloan Kettering investigators gratefully acknowledge the MSK Cancer Center Support Grant/Core Grant (P30 CA008748).

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10.1093/hmg/ddv492

Cite this

Figueroa, J. D., Middlebrooks, C. D., Banday, A. R., Ye, Y., Garcia-Closas, M., Chatterjee, N., Koutros, S., Kiemeney, L. A., Rafnar, T., Bishop, T., Furberg, H., Matullo, G., Golka, K., Gago-Dominguez, M., Taylor, J. A., Fletcher, T., Siddiq, A., Cortessis, V. K., Kooperberg, C., ... Gerullis, H. (2015). Identification of a novel susceptibility locus at 13q34 and refinement of the 20p12.2 region as a multi-signal locus associated with bladder cancer risk in individuals of european ancestry. Human Molecular Genetics, 25(6), 1203-1214. https://doi.org/10.1093/hmg/ddv492

Identification of a novel susceptibility locus at 13q34 and refinement of the 20p12.2 region as a multi-signal locus associated with bladder cancer risk in individuals of european ancestry. / Figueroa, Jonine D.; Middlebrooks, Candace D.; Banday, A. Rouf et al.
In: Human Molecular Genetics, Vol. 25, No. 6, 17.08.2015, p. 1203-1214.

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

Figueroa, JD, Middlebrooks, CD, Banday, AR, Ye, Y, Garcia-Closas, M, Chatterjee, N, Koutros, S, Kiemeney, LA, Rafnar, T, Bishop, T, Furberg, H, Matullo, G, Golka, K, Gago-Dominguez, M, Taylor, JA, Fletcher, T, Siddiq, A, Cortessis, VK, Kooperberg, C, Cussenot, O, Benhamou, S, Prescott, J, Porru, S, Dinney, CP, Malats, N, Baris, D, Purdue, MP, Jacobs, EJ, Albanes, D, Wang, Z, Chung, CC, Vermeulen, SH, Aben, KK, Galesloot, TE, Thorleifsson, G, Sulem, P, Stefansson, K, Kiltie, AE, Harland, M, Teo, M, Offit, K, Vijai, J, Bajorin, D, Kopp, R, Fiorito, G, Guarrera, S, Sacerdote, C, Selinski, S, Hengstler, JG & Gerullis, H 2015, 'Identification of a novel susceptibility locus at 13q34 and refinement of the 20p12.2 region as a multi-signal locus associated with bladder cancer risk in individuals of european ancestry', Human Molecular Genetics, vol. 25, no. 6, pp. 1203-1214. https://doi.org/10.1093/hmg/ddv492

@article{00a27c10899a4ffebfb69b2296fc941a,

title = "Identification of a novel susceptibility locus at 13q34 and refinement of the 20p12.2 region as a multi-signal locus associated with bladder cancer risk in individuals of european ancestry",

abstract = "Candidate gene and genome-wide association studies (GWAS) have identified 15 independent genomic regions associated with bladder cancer risk. In search for additional susceptibility variants, we followed up on four promising single-nucleotide polymorphisms (SNPs) that had not achieved genome-wide significance in 6911 cases and 11 814 controls (rs6104690, rs4510656, rs5003154 and rs4907479, P < 1 × 10-6), using additional data from existing GWAS datasets and targeted genotyping for studies that did not have GWAS data. In a combined analysis, which included data on up to 15 058 cases and 286 270 controls, two SNPs achieved genome-wide statistical significance: Rs6104690 in a gene desert at 20p12.2 (P = 2.19 × 10-11) and rs4907479 within the MCF2L gene at 13q34 (P = 3.3 × 10-10). Imputation and fine-mapping analyses were performed in these two regions for a subset of 5551 bladder cancer cases and 10 242 controls. Analyses at the 13q34 region suggest a single signal marked by rs4907479. In contrast, we detected two signals in the 20p12.2 region-the first signal is marked by rs6104690, and the second signal is marked by two moderately correlated SNPs (r2 = 0.53), rs6108803 and the previously reported rs62185668. The second 20p12.2 signal is more strongly associated with the risk of muscle-invasive (T2-T4 stage) compared with non-muscle-invasive (Ta, T1 stage) bladder cancer (case-case P ≤ 0.02 for both rs62185668 and rs6108803). Functional analyses are needed to explore the biological mechanisms underlying these novel genetic associations with risk for bladder cancer. Published by Oxford University Press 2016. This work is written by (a) US Government employee(s) and is in the public domain in the US.",

author = "Figueroa, {Jonine D.} and Middlebrooks, {Candace D.} and Banday, {A. Rouf} and Yuanqing Ye and Montserrat Garcia-Closas and Nilanjan Chatterjee and Stella Koutros and Kiemeney, {Lambertus A.} and Thorunn Rafnar and Timothy Bishop and Helena Furberg and Giuseppe Matullo and Klaus Golka and Manuela Gago-Dominguez and Taylor, {Jack A.} and Tony Fletcher and Afshan Siddiq and Cortessis, {Victoria K.} and Charles Kooperberg and Olivier Cussenot and Simone Benhamou and Jennifer Prescott and Stefano Porru and Dinney, {Colin P.} and N{\'u}ria Malats and Dalsu Baris and Purdue, {Mark P.} and Jacobs, {Eric J.} and Demetrius Albanes and Zhaoming Wang and Chung, {Charles C.} and Vermeulen, {Sita H.} and Aben, {Katja K.} and Galesloot, {Tessel E.} and Gudmar Thorleifsson and Patrick Sulem and Kari Stefansson and Kiltie, {Anne E.} and Mark Harland and Mark Teo and Kenneth Offit and Joseph Vijai and Dean Bajorin and Ryan Kopp and Giovanni Fiorito and Simonetta Guarrera and Carlotta Sacerdote and Silvia Selinski and Hengstler, {Jan G.} and Holger Gerullis",

note = "Funding Information: See Supplementary Material for funding details. The authors acknowledge the following: Marie Audouin, C{\'e}cile Gaffory, Val{\'e}rie Ondet; Leslie Carroll (Information Management Services, Silver Spring, MD, USA); Gemma Casta{\~n}o-Vinyals (Institut Municipal d{\textquoteright}Investigaci{\'o} M{\`e}dica, Barcelona, Spain); Francisco Fern{\'a}ndez (Institut Municipal d{\textquoteright}Investigaci{\'o} M{\`e}dica, Barcelona, Spain); Anna McIntosh (Westat, Inc., Rockville, MD, USA); Robert Saal (Westat, Rockville, MD, USA); Francisco Real [Spanish National Cancer Research Centre (CNIO), Madrid, Spain]; Maria Sala (Institut Municipal d{\textquoteright}Investigaci{\'o} M{\`e}dica, Barcelona, Spain); Kirk Snyder (Information Management Services, Inc., Silver Spring, MD); Anne Taylor (Information Management Services, Inc., Silver Spring, MD); Montserrat Tor{\`a} (Institut Municipal d{\textquoteright}Investigaci{\'o} M{\`e}dica, Barcelona, Spain); JaneWang (Information Management Services, Silver Spring, MD, USA). WHI Program Office: (National Heart, Lung, and Blood Institute, Bethesda, Maryland) Jacques Rossouw, Shari Ludlam, Dale Burwen, Joan McGowan, Leslie Ford, and Nancy Geller. Clinical Coordinating Center: Clinical Coordinating Center: (Fred Hutchinson Cancer Research Center, Seattle, WA) Garnet Anderson, Ross Prentice, Andrea LaCroix, and Charles Kooperberg. Investigators and Academic Centers: (Brigham and Women{\textquoteright}s Hospital, Harvard Medical School, Boston, MA) JoAnn E. Manson; (MedStar Health Research Institute/Howard University, Washington, DC) Barbara V. Howard; (Stanford Prevention Research Center, Stanford, CA) Marcia L. Stefanick; (The Ohio State University, Columbus, OH) Rebecca Jackson; (University of Arizona, Tucson/ Phoenix, AZ) Cynthia A. Thomson; (University at Buffalo, Buffalo, NY) Jean Wactawski-Wende; (University of Florida, Gainesville/ Jacksonville, FL) Marian Limacher; (University of Iowa, Iowa City/Davenport, IA) Robert Wallace; (University of Pittsburgh, Pittsburgh, PA) Lewis Kuller; (Wake Forest University School of Medicine, Winston-Salem, NC) Sally Shumaker. Women{\textquoteright}s Health Initiative Memory Study: (Wake Forest University School of Medicine, Winston-Salem, NC) Sally Shumaker. For a list of all the investigators who have contributed to WHI science, please visit: https://cleo.whi.org/researchers/SitePages/ Write%20a%20Paper.aspx. The Memorial Sloan Kettering investigators gratefully acknowledge the MSK Cancer Center Support Grant/Core Grant (P30 CA008748).",

year = "2015",

month = aug,

day = "17",

doi = "10.1093/hmg/ddv492",

language = "English",

volume = "25",

pages = "1203--1214",

journal = "Human Molecular Genetics",

issn = "0964-6906",

publisher = "Oxford University Press",

number = "6",

}

TY - JOUR

T1 - Identification of a novel susceptibility locus at 13q34 and refinement of the 20p12.2 region as a multi-signal locus associated with bladder cancer risk in individuals of european ancestry

AU - Figueroa, Jonine D.

AU - Middlebrooks, Candace D.

AU - Banday, A. Rouf

AU - Ye, Yuanqing

AU - Garcia-Closas, Montserrat

AU - Chatterjee, Nilanjan

AU - Koutros, Stella

AU - Kiemeney, Lambertus A.

AU - Rafnar, Thorunn

AU - Bishop, Timothy

AU - Furberg, Helena

AU - Matullo, Giuseppe

AU - Golka, Klaus

AU - Gago-Dominguez, Manuela

AU - Taylor, Jack A.

AU - Fletcher, Tony

AU - Siddiq, Afshan

AU - Cortessis, Victoria K.

AU - Kooperberg, Charles

AU - Cussenot, Olivier

AU - Benhamou, Simone

AU - Prescott, Jennifer

AU - Porru, Stefano

AU - Dinney, Colin P.

AU - Malats, Núria

AU - Baris, Dalsu

AU - Purdue, Mark P.

AU - Jacobs, Eric J.

AU - Albanes, Demetrius

AU - Wang, Zhaoming

AU - Chung, Charles C.

AU - Vermeulen, Sita H.

AU - Aben, Katja K.

AU - Galesloot, Tessel E.

AU - Thorleifsson, Gudmar

AU - Sulem, Patrick

AU - Stefansson, Kari

AU - Kiltie, Anne E.

AU - Harland, Mark

AU - Teo, Mark

AU - Offit, Kenneth

AU - Vijai, Joseph

AU - Bajorin, Dean

AU - Kopp, Ryan

AU - Fiorito, Giovanni

AU - Guarrera, Simonetta

AU - Sacerdote, Carlotta

AU - Selinski, Silvia

AU - Hengstler, Jan G.

AU - Gerullis, Holger

N1 - Funding Information: See Supplementary Material for funding details. The authors acknowledge the following: Marie Audouin, Cécile Gaffory, Valérie Ondet; Leslie Carroll (Information Management Services, Silver Spring, MD, USA); Gemma Castaño-Vinyals (Institut Municipal d’Investigació Mèdica, Barcelona, Spain); Francisco Fernández (Institut Municipal d’Investigació Mèdica, Barcelona, Spain); Anna McIntosh (Westat, Inc., Rockville, MD, USA); Robert Saal (Westat, Rockville, MD, USA); Francisco Real [Spanish National Cancer Research Centre (CNIO), Madrid, Spain]; Maria Sala (Institut Municipal d’Investigació Mèdica, Barcelona, Spain); Kirk Snyder (Information Management Services, Inc., Silver Spring, MD); Anne Taylor (Information Management Services, Inc., Silver Spring, MD); Montserrat Torà (Institut Municipal d’Investigació Mèdica, Barcelona, Spain); JaneWang (Information Management Services, Silver Spring, MD, USA). WHI Program Office: (National Heart, Lung, and Blood Institute, Bethesda, Maryland) Jacques Rossouw, Shari Ludlam, Dale Burwen, Joan McGowan, Leslie Ford, and Nancy Geller. Clinical Coordinating Center: Clinical Coordinating Center: (Fred Hutchinson Cancer Research Center, Seattle, WA) Garnet Anderson, Ross Prentice, Andrea LaCroix, and Charles Kooperberg. Investigators and Academic Centers: (Brigham and Women’s Hospital, Harvard Medical School, Boston, MA) JoAnn E. Manson; (MedStar Health Research Institute/Howard University, Washington, DC) Barbara V. Howard; (Stanford Prevention Research Center, Stanford, CA) Marcia L. Stefanick; (The Ohio State University, Columbus, OH) Rebecca Jackson; (University of Arizona, Tucson/ Phoenix, AZ) Cynthia A. Thomson; (University at Buffalo, Buffalo, NY) Jean Wactawski-Wende; (University of Florida, Gainesville/ Jacksonville, FL) Marian Limacher; (University of Iowa, Iowa City/Davenport, IA) Robert Wallace; (University of Pittsburgh, Pittsburgh, PA) Lewis Kuller; (Wake Forest University School of Medicine, Winston-Salem, NC) Sally Shumaker. Women’s Health Initiative Memory Study: (Wake Forest University School of Medicine, Winston-Salem, NC) Sally Shumaker. For a list of all the investigators who have contributed to WHI science, please visit: https://cleo.whi.org/researchers/SitePages/ Write%20a%20Paper.aspx. The Memorial Sloan Kettering investigators gratefully acknowledge the MSK Cancer Center Support Grant/Core Grant (P30 CA008748).

PY - 2015/8/17

Y1 - 2015/8/17

N2 - Candidate gene and genome-wide association studies (GWAS) have identified 15 independent genomic regions associated with bladder cancer risk. In search for additional susceptibility variants, we followed up on four promising single-nucleotide polymorphisms (SNPs) that had not achieved genome-wide significance in 6911 cases and 11 814 controls (rs6104690, rs4510656, rs5003154 and rs4907479, P < 1 × 10-6), using additional data from existing GWAS datasets and targeted genotyping for studies that did not have GWAS data. In a combined analysis, which included data on up to 15 058 cases and 286 270 controls, two SNPs achieved genome-wide statistical significance: Rs6104690 in a gene desert at 20p12.2 (P = 2.19 × 10-11) and rs4907479 within the MCF2L gene at 13q34 (P = 3.3 × 10-10). Imputation and fine-mapping analyses were performed in these two regions for a subset of 5551 bladder cancer cases and 10 242 controls. Analyses at the 13q34 region suggest a single signal marked by rs4907479. In contrast, we detected two signals in the 20p12.2 region-the first signal is marked by rs6104690, and the second signal is marked by two moderately correlated SNPs (r2 = 0.53), rs6108803 and the previously reported rs62185668. The second 20p12.2 signal is more strongly associated with the risk of muscle-invasive (T2-T4 stage) compared with non-muscle-invasive (Ta, T1 stage) bladder cancer (case-case P ≤ 0.02 for both rs62185668 and rs6108803). Functional analyses are needed to explore the biological mechanisms underlying these novel genetic associations with risk for bladder cancer. Published by Oxford University Press 2016. This work is written by (a) US Government employee(s) and is in the public domain in the US.

AB - Candidate gene and genome-wide association studies (GWAS) have identified 15 independent genomic regions associated with bladder cancer risk. In search for additional susceptibility variants, we followed up on four promising single-nucleotide polymorphisms (SNPs) that had not achieved genome-wide significance in 6911 cases and 11 814 controls (rs6104690, rs4510656, rs5003154 and rs4907479, P < 1 × 10-6), using additional data from existing GWAS datasets and targeted genotyping for studies that did not have GWAS data. In a combined analysis, which included data on up to 15 058 cases and 286 270 controls, two SNPs achieved genome-wide statistical significance: Rs6104690 in a gene desert at 20p12.2 (P = 2.19 × 10-11) and rs4907479 within the MCF2L gene at 13q34 (P = 3.3 × 10-10). Imputation and fine-mapping analyses were performed in these two regions for a subset of 5551 bladder cancer cases and 10 242 controls. Analyses at the 13q34 region suggest a single signal marked by rs4907479. In contrast, we detected two signals in the 20p12.2 region-the first signal is marked by rs6104690, and the second signal is marked by two moderately correlated SNPs (r2 = 0.53), rs6108803 and the previously reported rs62185668. The second 20p12.2 signal is more strongly associated with the risk of muscle-invasive (T2-T4 stage) compared with non-muscle-invasive (Ta, T1 stage) bladder cancer (case-case P ≤ 0.02 for both rs62185668 and rs6108803). Functional analyses are needed to explore the biological mechanisms underlying these novel genetic associations with risk for bladder cancer. Published by Oxford University Press 2016. This work is written by (a) US Government employee(s) and is in the public domain in the US.

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DO - 10.1093/hmg/ddv492

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AN - SCOPUS:84960105525

SN - 0964-6906

VL - 25

SP - 1203

EP - 1214

JO - Human Molecular Genetics

JF - Human Molecular Genetics

IS - 6

ER -

Identification of a novel susceptibility locus at 13q34 and refinement of the 20p12.2 region as a multi-signal locus associated with bladder cancer risk in individuals of european ancestry

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