Seven prostate cancer susceptibility loci identified by a multi-stage genome-wide association study

Zsofia Kote-Jarai; Ali Amin Al Olama; Graham G. Giles; Gianluca Severi; Johanna Schleutker; Maren Weischer; Daniele Campa; Elio Riboli; Tim Key; Henrik Gronberg; David J. Hunter; Peter Kraft; Michael J. Thun; Sue Ingles; Stephen Chanock; Demetrius Albanes; Richard B. Hayes; David E. Neal; Freddie C. Hamdy; Jenny L. Donovan; Paul Pharoah; Fredrick Schumacher; Brian E. Henderson; Janet L. Stanford; Elaine A. Ostrander; Karina Dalsgaard Sorensen; Thilo Dörk; Gerald Andriole; Joanne L. Dickinson; Cezary Cybulski; Jan Lubinski; Amanda Spurdle; Judith A. Clements; Suzanne Chambers; Joanne Aitken; R. A.Frank Gardiner; Stephen N. Thibodeau; Dan Schaid; Esther M. John; Christiane Maier; Walther Vogel; Kathleen A. Cooney; Jong Y. Park; Lisa Cannon-Albright; Hermann Brenner; Tomonori Habuchi; Hong Wei Zhang; Yong Jie Lu; Radka Kaneva; Ken Muir; Sara Benlloch; Daniel A. Leongamornlert; Edward J. Saunders; Malgorzata Tymrakiewicz; Nadiya Mahmud; Michelle Guy; Lynne T. O'Brien; Rosemary A. Wilkinson; Amanda L. Hall; Emma J. Sawyer; Tokhir Dadaev; Jonathan Morrison; David P. Dearnaley; Alan Horwich; Robert A. Huddart; Vincent S. Khoo; Christopher C. Parker; Nicholas Van As; Christopher J. Woodhouse; Alan Thompson; Tim Christmas; Chris Ogden; Colin S. Cooper; Aritaya Lophatonanon; Melissa C. Southey; John L. Hopper; Dallas R. English; Tiina Wahlfors; Teuvo L.J. Tammela; Peter Klarskov; Børge G. Nordestgaard; M. Andreas Røder; Anne Tybjarg-Hansen; Stig E. Bojesen; Ruth Travis; Federico Canzian; Rudolf Kaaks; Fredrik Wiklund; Markus Aly; Sara Lindstrom; W. Ryan Diver; Susan Gapstur; Mariana C. Stern; Roman Corral; Jarmo Virtamo; Angela Cox; Christopher A. Haiman; Loic Le Marchand; Liesel Fitzgerald; Suzanne Kolb; Erika M. Kwon; Danielle M. Karyadi; Torben Falck Ørntoft; Michael Borre; Andreas Meyer; Jürgen Serth; Meredith Yeager; Sonja I. Berndt; James R. Marthick; Briony Patterson; Dominika Wokolorczyk; Jyotsna Batra; Felicity Lose; Shannon K. McDonnell; Amit D. Joshi; Ahva Shahabi; Antje E. Rinckleb; Ana Ray; Thomas A. Sellers; Hui Yi Lin; Robert A. Stephenson; James Farnham; Heiko Muller; Dietrich Rothenbacher; Norihiko Tsuchiya; Shintaro Narita; Guang Wen Cao; Chavdar Slavov; Vanio Mitev; Douglas F. Easton; Rosalind A. Eeles

doi:10.1038/ng.882

Seven prostate cancer susceptibility loci identified by a multi-stage genome-wide association study

Zsofia Kote-Jarai, Ali Amin Al Olama, Graham G. Giles, Gianluca Severi, Johanna Schleutker, Maren Weischer, Daniele Campa, Elio Riboli, Tim Key, Henrik Gronberg, David J. Hunter, Peter Kraft, Michael J. Thun, Sue Ingles, Stephen Chanock, Demetrius Albanes, Richard B. Hayes, David E. Neal, Freddie C. Hamdy, Jenny L. DonovanPaul Pharoah, Fredrick Schumacher, Brian E. Henderson, Janet L. Stanford, Elaine A. Ostrander, Karina Dalsgaard Sorensen, Thilo Dörk, Gerald Andriole, Joanne L. Dickinson, Cezary Cybulski, Jan Lubinski, Amanda Spurdle, Judith A. Clements, Suzanne Chambers, Joanne Aitken, R. A.Frank Gardiner, Stephen N. Thibodeau, Dan Schaid, Esther M. John, Christiane Maier, Walther Vogel, Kathleen A. Cooney, Jong Y. Park, Lisa Cannon-Albright, Hermann Brenner, Tomonori Habuchi, Hong Wei Zhang, Yong Jie Lu, Radka Kaneva, Ken Muir, Sara Benlloch, Daniel A. Leongamornlert, Edward J. Saunders, Malgorzata Tymrakiewicz, Nadiya Mahmud, Michelle Guy, Lynne T. O'Brien, Rosemary A. Wilkinson, Amanda L. Hall, Emma J. Sawyer, Tokhir Dadaev, Jonathan Morrison, David P. Dearnaley, Alan Horwich, Robert A. Huddart, Vincent S. Khoo, Christopher C. Parker, Nicholas Van As, Christopher J. Woodhouse, Alan Thompson, Tim Christmas, Chris Ogden, Colin S. Cooper, Aritaya Lophatonanon, Melissa C. Southey, John L. Hopper, Dallas R. English, Tiina Wahlfors, Teuvo L.J. Tammela, Peter Klarskov, Børge G. Nordestgaard, M. Andreas Røder, Anne Tybjarg-Hansen, Stig E. Bojesen, Ruth Travis, Federico Canzian, Rudolf Kaaks, Fredrik Wiklund, Markus Aly, Sara Lindstrom, W. Ryan Diver, Susan Gapstur, Mariana C. Stern, Roman Corral, Jarmo Virtamo, Angela Cox, Christopher A. Haiman, Loic Le Marchand, Liesel Fitzgerald, Suzanne Kolb, Erika M. Kwon, Danielle M. Karyadi, Torben Falck Ørntoft, Michael Borre, Andreas Meyer, Jürgen Serth, Meredith Yeager, Sonja I. Berndt, James R. Marthick, Briony Patterson, Dominika Wokolorczyk, Jyotsna Batra, Felicity Lose, Shannon K. McDonnell, Amit D. Joshi, Ahva Shahabi, Antje E. Rinckleb, Ana Ray, Thomas A. Sellers, Hui Yi Lin, Robert A. Stephenson, James Farnham, Heiko Muller, Dietrich Rothenbacher, Norihiko Tsuchiya, Shintaro Narita, Guang Wen Cao, Chavdar Slavov, Vanio Mitev, Douglas F. Easton, Rosalind A. Eeles

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Abstract

Prostate cancer (PrCa) is the most frequently diagnosed male cancer in developed countries. We conducted a multi-stage genome-wide association study for PrCa and previously reported the results of the first two stages, which identified 16 PrCa susceptibility loci. We report here the results of stage 3, in which we evaluated 1,536 SNPs in 4,574 individuals with prostate cancer (cases) and 4,164 controls. We followed up ten new association signals through genotyping in 51,311 samples in 30 studies from the Prostate Cancer Association Group to Investigate Cancer Associated Alterations in the Genome (PRACTICAL) consortium. In addition to replicating previously reported loci, we identified seven new prostate cancer susceptibility loci on chromosomes 2p11, 3q23, 3q26, 5p12, 6p21, 12q13 and Xq12 (P = 4.0 × 10^-8 to P = 2.7 × 10^-24). We also identified a SNP in TERT more strongly associated with PrCa than that previously reported. More than 40 PrCa susceptibility loci, explaining 425% of the familial risk in this disease, have now been identified.

Original language	English
Pages (from-to)	785-791
Number of pages	7
Journal	Nature Genetics
Volume	43
Issue number	8
DOIs	https://doi.org/10.1038/ng.882
Publication status	Published - 1 Aug 2011
Externally published	Yes

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Kote-Jarai, Z., Olama, A. A. A., Giles, G. G., Severi, G., Schleutker, J., Weischer, M., Campa, D., Riboli, E., Key, T., Gronberg, H., Hunter, D. J., Kraft, P., Thun, M. J., Ingles, S., Chanock, S., Albanes, D., Hayes, R. B., Neal, D. E., Hamdy, F. C., ... Eeles, R. A. (2011). Seven prostate cancer susceptibility loci identified by a multi-stage genome-wide association study. Nature Genetics, 43(8), 785-791. https://doi.org/10.1038/ng.882

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title = "Seven prostate cancer susceptibility loci identified by a multi-stage genome-wide association study",

abstract = "Prostate cancer (PrCa) is the most frequently diagnosed male cancer in developed countries. We conducted a multi-stage genome-wide association study for PrCa and previously reported the results of the first two stages, which identified 16 PrCa susceptibility loci. We report here the results of stage 3, in which we evaluated 1,536 SNPs in 4,574 individuals with prostate cancer (cases) and 4,164 controls. We followed up ten new association signals through genotyping in 51,311 samples in 30 studies from the Prostate Cancer Association Group to Investigate Cancer Associated Alterations in the Genome (PRACTICAL) consortium. In addition to replicating previously reported loci, we identified seven new prostate cancer susceptibility loci on chromosomes 2p11, 3q23, 3q26, 5p12, 6p21, 12q13 and Xq12 (P = 4.0 × 10-8 to P = 2.7 × 10-24). We also identified a SNP in TERT more strongly associated with PrCa than that previously reported. More than 40 PrCa susceptibility loci, explaining 425% of the familial risk in this disease, have now been identified.",

author = "Zsofia Kote-Jarai and Olama, {Ali Amin Al} and Giles, {Graham G.} and Gianluca Severi and Johanna Schleutker and Maren Weischer and Daniele Campa and Elio Riboli and Tim Key and Henrik Gronberg and Hunter, {David J.} and Peter Kraft and Thun, {Michael J.} and Sue Ingles and Stephen Chanock and Demetrius Albanes and Hayes, {Richard B.} and Neal, {David E.} and Hamdy, {Freddie C.} and Donovan, {Jenny L.} and Paul Pharoah and Fredrick Schumacher and Henderson, {Brian E.} and Stanford, {Janet L.} and Ostrander, {Elaine A.} and Sorensen, {Karina Dalsgaard} and Thilo D{\"o}rk and Gerald Andriole and Dickinson, {Joanne L.} and Cezary Cybulski and Jan Lubinski and Amanda Spurdle and Clements, {Judith A.} and Suzanne Chambers and Joanne Aitken and Gardiner, {R. A.Frank} and Thibodeau, {Stephen N.} and Dan Schaid and John, {Esther M.} and Christiane Maier and Walther Vogel and Cooney, {Kathleen A.} and Park, {Jong Y.} and Lisa Cannon-Albright and Hermann Brenner and Tomonori Habuchi and Zhang, {Hong Wei} and Lu, {Yong Jie} and Radka Kaneva and Ken Muir and Sara Benlloch and Leongamornlert, {Daniel A.} and Saunders, {Edward J.} and Malgorzata Tymrakiewicz and Nadiya Mahmud and Michelle Guy and O'Brien, {Lynne T.} and Wilkinson, {Rosemary A.} and Hall, {Amanda L.} and Sawyer, {Emma J.} and Tokhir Dadaev and Jonathan Morrison and Dearnaley, {David P.} and Alan Horwich and Huddart, {Robert A.} and Khoo, {Vincent S.} and Parker, {Christopher C.} and {Van As}, Nicholas and Woodhouse, {Christopher J.} and Alan Thompson and Tim Christmas and Chris Ogden and Cooper, {Colin S.} and Aritaya Lophatonanon and Southey, {Melissa C.} and Hopper, {John L.} and English, {Dallas R.} and Tiina Wahlfors and Tammela, {Teuvo L.J.} and Peter Klarskov and Nordestgaard, {B{\o}rge G.} and R{\o}der, {M. Andreas} and Anne Tybjarg-Hansen and Bojesen, {Stig E.} and Ruth Travis and Federico Canzian and Rudolf Kaaks and Fredrik Wiklund and Markus Aly and Sara Lindstrom and Diver, {W. Ryan} and Susan Gapstur and Stern, {Mariana C.} and Roman Corral and Jarmo Virtamo and Angela Cox and Haiman, {Christopher A.} and {Le Marchand}, Loic and Liesel Fitzgerald and Suzanne Kolb and Kwon, {Erika M.} and Karyadi, {Danielle M.} and {\O}rntoft, {Torben Falck} and Michael Borre and Andreas Meyer and J{\"u}rgen Serth and Meredith Yeager and Berndt, {Sonja I.} and Marthick, {James R.} and Briony Patterson and Dominika Wokolorczyk and Jyotsna Batra and Felicity Lose and McDonnell, {Shannon K.} and Joshi, {Amit D.} and Ahva Shahabi and Rinckleb, {Antje E.} and Ana Ray and Sellers, {Thomas A.} and Lin, {Hui Yi} and Stephenson, {Robert A.} and James Farnham and Heiko Muller and Dietrich Rothenbacher and Norihiko Tsuchiya and Shintaro Narita and Cao, {Guang Wen} and Chavdar Slavov and Vanio Mitev and Easton, {Douglas F.} and Eeles, {Rosalind A.}",

year = "2011",

month = aug,

day = "1",

doi = "10.1038/ng.882",

language = "English",

volume = "43",

pages = "785--791",

journal = "Nature Genetics",

issn = "1061-4036",

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Kote-Jarai, Z, Olama, AAA, Giles, GG, Severi, G, Schleutker, J, Weischer, M, Campa, D, Riboli, E, Key, T, Gronberg, H, Hunter, DJ, Kraft, P, Thun, MJ, Ingles, S, Chanock, S, Albanes, D, Hayes, RB, Neal, DE, Hamdy, FC, Donovan, JL, Pharoah, P, Schumacher, F, Henderson, BE, Stanford, JL, Ostrander, EA, Sorensen, KD, Dörk, T, Andriole, G, Dickinson, JL, Cybulski, C, Lubinski, J, Spurdle, A, Clements, JA, Chambers, S, Aitken, J, Gardiner, RAF, Thibodeau, SN, Schaid, D, John, EM, Maier, C, Vogel, W, Cooney, KA, Park, JY, Cannon-Albright, L, Brenner, H, Habuchi, T, Zhang, HW, Lu, YJ, Kaneva, R, Muir, K, Benlloch, S, Leongamornlert, DA, Saunders, EJ, Tymrakiewicz, M, Mahmud, N, Guy, M, O'Brien, LT, Wilkinson, RA, Hall, AL, Sawyer, EJ, Dadaev, T, Morrison, J, Dearnaley, DP, Horwich, A, Huddart, RA, Khoo, VS, Parker, CC, Van As, N, Woodhouse, CJ, Thompson, A, Christmas, T, Ogden, C, Cooper, CS, Lophatonanon, A, Southey, MC, Hopper, JL, English, DR, Wahlfors, T, Tammela, TLJ, Klarskov, P, Nordestgaard, BG, Røder, MA, Tybjarg-Hansen, A, Bojesen, SE, Travis, R, Canzian, F, Kaaks, R, Wiklund, F, Aly, M, Lindstrom, S, Diver, WR, Gapstur, S, Stern, MC, Corral, R, Virtamo, J, Cox, A, Haiman, CA, Le Marchand, L, Fitzgerald, L, Kolb, S, Kwon, EM, Karyadi, DM, Ørntoft, TF, Borre, M, Meyer, A, Serth, J, Yeager, M, Berndt, SI, Marthick, JR, Patterson, B, Wokolorczyk, D, Batra, J, Lose, F, McDonnell, SK, Joshi, AD, Shahabi, A, Rinckleb, AE, Ray, A, Sellers, TA, Lin, HY, Stephenson, RA, Farnham, J, Muller, H, Rothenbacher, D, Tsuchiya, N, Narita, S, Cao, GW, Slavov, C, Mitev, V, Easton, DF & Eeles, RA 2011, 'Seven prostate cancer susceptibility loci identified by a multi-stage genome-wide association study', Nature Genetics, vol. 43, no. 8, pp. 785-791. https://doi.org/10.1038/ng.882

TY - JOUR

T1 - Seven prostate cancer susceptibility loci identified by a multi-stage genome-wide association study

AU - Kote-Jarai, Zsofia

AU - Olama, Ali Amin Al

AU - Giles, Graham G.

AU - Severi, Gianluca

AU - Schleutker, Johanna

AU - Weischer, Maren

AU - Campa, Daniele

AU - Riboli, Elio

AU - Key, Tim

AU - Gronberg, Henrik

AU - Hunter, David J.

AU - Kraft, Peter

AU - Thun, Michael J.

AU - Ingles, Sue

AU - Chanock, Stephen

AU - Albanes, Demetrius

AU - Hayes, Richard B.

AU - Neal, David E.

AU - Hamdy, Freddie C.

AU - Donovan, Jenny L.

AU - Pharoah, Paul

AU - Schumacher, Fredrick

AU - Henderson, Brian E.

AU - Stanford, Janet L.

AU - Ostrander, Elaine A.

AU - Sorensen, Karina Dalsgaard

AU - Dörk, Thilo

AU - Andriole, Gerald

AU - Dickinson, Joanne L.

AU - Cybulski, Cezary

AU - Lubinski, Jan

AU - Spurdle, Amanda

AU - Clements, Judith A.

AU - Chambers, Suzanne

AU - Aitken, Joanne

AU - Gardiner, R. A.Frank

AU - Thibodeau, Stephen N.

AU - Schaid, Dan

AU - John, Esther M.

AU - Maier, Christiane

AU - Vogel, Walther

AU - Cooney, Kathleen A.

AU - Park, Jong Y.

AU - Cannon-Albright, Lisa

AU - Brenner, Hermann

AU - Habuchi, Tomonori

AU - Zhang, Hong Wei

AU - Lu, Yong Jie

AU - Kaneva, Radka

AU - Muir, Ken

AU - Benlloch, Sara

AU - Leongamornlert, Daniel A.

AU - Saunders, Edward J.

AU - Tymrakiewicz, Malgorzata

AU - Mahmud, Nadiya

AU - Guy, Michelle

AU - O'Brien, Lynne T.

AU - Wilkinson, Rosemary A.

AU - Hall, Amanda L.

AU - Sawyer, Emma J.

AU - Dadaev, Tokhir

AU - Morrison, Jonathan

AU - Dearnaley, David P.

AU - Horwich, Alan

AU - Huddart, Robert A.

AU - Khoo, Vincent S.

AU - Parker, Christopher C.

AU - Van As, Nicholas

AU - Woodhouse, Christopher J.

AU - Thompson, Alan

AU - Christmas, Tim

AU - Ogden, Chris

AU - Cooper, Colin S.

AU - Lophatonanon, Aritaya

AU - Southey, Melissa C.

AU - Hopper, John L.

AU - English, Dallas R.

AU - Wahlfors, Tiina

AU - Tammela, Teuvo L.J.

AU - Klarskov, Peter

AU - Nordestgaard, Børge G.

AU - Røder, M. Andreas

AU - Tybjarg-Hansen, Anne

AU - Bojesen, Stig E.

AU - Travis, Ruth

AU - Canzian, Federico

AU - Kaaks, Rudolf

AU - Wiklund, Fredrik

AU - Aly, Markus

AU - Lindstrom, Sara

AU - Diver, W. Ryan

AU - Gapstur, Susan

AU - Stern, Mariana C.

AU - Corral, Roman

AU - Virtamo, Jarmo

AU - Cox, Angela

AU - Haiman, Christopher A.

AU - Le Marchand, Loic

AU - Fitzgerald, Liesel

AU - Kolb, Suzanne

AU - Kwon, Erika M.

AU - Karyadi, Danielle M.

AU - Ørntoft, Torben Falck

AU - Borre, Michael

AU - Meyer, Andreas

AU - Serth, Jürgen

AU - Yeager, Meredith

AU - Berndt, Sonja I.

AU - Marthick, James R.

AU - Patterson, Briony

AU - Wokolorczyk, Dominika

AU - Batra, Jyotsna

AU - Lose, Felicity

AU - McDonnell, Shannon K.

AU - Joshi, Amit D.

AU - Shahabi, Ahva

AU - Rinckleb, Antje E.

AU - Ray, Ana

AU - Sellers, Thomas A.

AU - Lin, Hui Yi

AU - Stephenson, Robert A.

AU - Farnham, James

AU - Muller, Heiko

AU - Rothenbacher, Dietrich

AU - Tsuchiya, Norihiko

AU - Narita, Shintaro

AU - Cao, Guang Wen

AU - Slavov, Chavdar

AU - Mitev, Vanio

AU - Easton, Douglas F.

AU - Eeles, Rosalind A.

PY - 2011/8/1

Y1 - 2011/8/1

N2 - Prostate cancer (PrCa) is the most frequently diagnosed male cancer in developed countries. We conducted a multi-stage genome-wide association study for PrCa and previously reported the results of the first two stages, which identified 16 PrCa susceptibility loci. We report here the results of stage 3, in which we evaluated 1,536 SNPs in 4,574 individuals with prostate cancer (cases) and 4,164 controls. We followed up ten new association signals through genotyping in 51,311 samples in 30 studies from the Prostate Cancer Association Group to Investigate Cancer Associated Alterations in the Genome (PRACTICAL) consortium. In addition to replicating previously reported loci, we identified seven new prostate cancer susceptibility loci on chromosomes 2p11, 3q23, 3q26, 5p12, 6p21, 12q13 and Xq12 (P = 4.0 × 10-8 to P = 2.7 × 10-24). We also identified a SNP in TERT more strongly associated with PrCa than that previously reported. More than 40 PrCa susceptibility loci, explaining 425% of the familial risk in this disease, have now been identified.

AB - Prostate cancer (PrCa) is the most frequently diagnosed male cancer in developed countries. We conducted a multi-stage genome-wide association study for PrCa and previously reported the results of the first two stages, which identified 16 PrCa susceptibility loci. We report here the results of stage 3, in which we evaluated 1,536 SNPs in 4,574 individuals with prostate cancer (cases) and 4,164 controls. We followed up ten new association signals through genotyping in 51,311 samples in 30 studies from the Prostate Cancer Association Group to Investigate Cancer Associated Alterations in the Genome (PRACTICAL) consortium. In addition to replicating previously reported loci, we identified seven new prostate cancer susceptibility loci on chromosomes 2p11, 3q23, 3q26, 5p12, 6p21, 12q13 and Xq12 (P = 4.0 × 10-8 to P = 2.7 × 10-24). We also identified a SNP in TERT more strongly associated with PrCa than that previously reported. More than 40 PrCa susceptibility loci, explaining 425% of the familial risk in this disease, have now been identified.

UR - http://www.scopus.com/inward/record.url?scp=79960924160&partnerID=8YFLogxK

U2 - 10.1038/ng.882

DO - 10.1038/ng.882

M3 - Article

C2 - 21743467

AN - SCOPUS:79960924160

SN - 1061-4036

VL - 43

SP - 785

EP - 791

JO - Nature Genetics

JF - Nature Genetics

IS - 8

ER -

Seven prostate cancer susceptibility loci identified by a multi-stage genome-wide association study

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