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Pooled genome linkage scan of aggressive prostate cancer: results from the International Consortium for Prostate Cancer Genetics

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An Erratum to this article was published on 16 December 2006

Abstract

While it is widely appreciated that prostate cancers vary substantially in their propensity to progress to a life-threatening stage, the molecular events responsible for this progression have not been identified. Understanding these molecular mechanisms could provide important prognostic information relevant to more effective clinical management of this heterogeneous cancer. Hence, through genetic linkage analyses, we examined the hypothesis that the tendency to develop aggressive prostate cancer may have an important genetic component. Starting with 1,233 familial prostate cancer families with genome scan data available from the International Consortium for Prostate Cancer Genetics, we selected those that had at least three members with the phenotype of clinically aggressive prostate cancer, as defined by either high tumor grade and/or stage, resulting in 166 pedigrees (13%). Genome-wide linkage data were then pooled to perform a combined linkage analysis for these families. Linkage signals reaching a suggestive level of significance were found on chromosomes 6p22.3 (LOD = 3.0), 11q14.1–14.3 (LOD = 2.4), and 20p11.21–q11.21 (LOD = 2.5). For chromosome 11, stronger evidence of linkage (LOD = 3.3) was observed among pedigrees with an average at diagnosis of 65 years or younger. Other chromosomes that showed evidence for heterogeneity in linkage across strata were chromosome 7, with the strongest linkage signal among pedigrees without male-to-male disease transmission (7q21.11, LOD = 4.1), and chromosome 21, with the strongest linkage signal among pedigrees that had African American ancestry (21q22.13–22.3; LOD = 3.2). Our findings suggest several regions that may contain genes which, when mutated, predispose men to develop a more aggressive prostate cancer phenotype. This provides a basis for attempts to identify these genes, with potential clinical utility for men with aggressive prostate cancer and their relatives.

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Acknowledgments

We would like to express our gratitude to the many families who participated in this study and to the many urologists who kindly assisted us by providing information and access to their patients. All members of the ICPCG are supported by the U.S. Public Health Service (USPHS), National Institutes of Health (CA89600). Additional support to participating groups, or members within groups, follows. ACTANE Group: Genotyping and statistical analysis for this study and recruitment of U.K. families was supported by Cancer Research U.K. Additional support was provided by the Prostate Cancer Charitable Trust (now Prostate Cancer Research Foundation), The Times Christmas Appeal, and the Institute of Cancer Research. Genotyping was conducted in the Jean Rook Gene Cloning Laboratory, which is supported by BREAKTHROUGH Breast Cancer-Charity 328323. The funds for the ABI 377 used in this study were generously provided by the legacy of the late Marion Silcock. We thank Mrs Sheila Seal and Mrs Anita Hall for kindly storing and logging the samples that were provided. D.F.E. is a principal research fellow of Cancer Research U.K. Recruitment of Australian PC-affected families was funded by National Health and Medical Research Council grant 940934 and was further supported by Tattersall’s and the Whitten Foundation; infrastructure was provided by the Cancer Council Victoria. We acknowledge the work of study coordinator Margaret Staples; the research team of Bernadette McCudden, John Connal, Richard Thorowgood, Chris Costa, Melodie Kevan, and Sue Palmer; and Jolanta Karpowicz, for DNA extractions. The Texas study of familial PC was initiated by the Department of Epidemiology, M.D. Anderson Cancer Center. M.B. was supported by NCI post-doctoral fellowship in Cancer Prevention R25. Additional support to W.D.F. was supplied by grant DAMD-17-00-10033. BC/CA/HI Group: USPHS CA67044. JHU Group: USPHS CA58236 (W.B.I.), CA95052-01 (J.X.), CA106523-01A1 (J.X.). Genotyping for the JHU, Michigan, Tampere, and Umeå groups were performed by Elizabeth Gillanders, MaryPat Jones, Derk Gildea, Erica Riedesel, Julie Albertus, Diana Freas-Lutz, Carol Markey, John Carpten, and Jeff Trent at the National Human Genome Research Institute, NIH. Mayo Clinic Group: USPHS CA72818. Michigan Group: USPHS CA079596. Fred Hutchinson/ISB Group: USPHS CA78835 (E.A.O.), CA080122 (J.L.S.), and from the Prostate Cancer Foundation and the Fred Hutchinson Cancer Research Center. Tampere Group: Medical Research Fund of Tampere University Hospital, Reino Lahtikari Foundation, Finnish Cancer Organizations, Sigrid Juselius Foundation and Academy of Finland (grant number 201480). Ulm Group: Deutsche Krebshilfe, grant number 70-3111-V03. Umeå Group: Grants from the Swedish Cancer Society (Cancerfonden) and Stiftelsen för Strategisk Forskning. Utah Group: NIH National Cancer Institute grant number R01 CA90752 (to L.A.C.). National Institutes of Health grant number K07 CA98364 (to N.J.C.). Data collected for this publication was assisted by the Utah Cancer Registry supported by National Institutes of Health Contract NO1-PC-35141, Surveillance, Epidemiology and End Results (SEER) Program, with additional support from the Utah Department of Health and the University of Utah. Partial support for all datasets within the Utah Population Database (UPDB) was provided by the University of Utah Huntsman Cancer Institute. Public Health Services research grant number M01-RR00064 from the National Center for Research Resources. Genotyping services were provided by the Center for Inherited Disease Research (CIDR). CIDR is fully funded through a federal contract from the National Institutes of Health to The Johns Hopkins University, contract number N01-HG-65403. Washington University Group: Urological Research Foundation.

Mayo Clinic

Authors: Daniel J. Schaid, Shannon K. McDonnell, Katherine E. Zarfas, Julie M. Cunningham, Scott Hebbring, Stephen N. Thibodeau

Affiliations: Mayo Clinic, Rochester, MN, USA (D.J.S., S.K.M, K.E.Z, J.M.C., S.H., and S.N.T.)

ACTANE

Authors: Rosalind A. Eeles, Douglas F. Easton, William D. Foulkes, Jacques Simard, Graham G. Giles, John L. Hopper, Lovise Mahle, Pal Moller, Michael Badzioch, D. Timothy Bishop, Chris Evans, Steve Edwards, Julia Meitz, Sarah Bullock, Questa Hope, Michelle Guy, The ACTANE Consortium

Affiliations: Institute of Cancer Research and Royal Marsden National Health Service Trust Foundation Hospital, Sutton, UK (R.A.E., S.E., J.M., S.B., Q.H., and M.G.); Cancer Research U.K. Genetic Epidemiology Unit, Strangeways Research Labs, Cambridge, UK (D.F.E. and C.E.); Program in Cancer Genetics, Departments of Oncology and Human Genetics, McGill University, Montreal, Canada (W.D.F.); Cancer Genomics Laboratory, Centre hospitalier de l’Universite Laval Research Centre, Sainte-Foy, QC, Canada (J. Simard); Cancer Epidemiology Centre, Cancer Council Victoria (G.G.G.), and Centre for Genetic Epidemiology, University of Melbourne, Carlton, Australia (J.L.H.); Unit of Medical Genetics, Norwegian Radium Hospital, Oslo, Norway (L.M. and P.M.); Cancer Research U.K. Genetic Epidemiology Laboratory, St. James’ University Hospital, Leeds, UK (T.B.); MD Anderson Cancer Center, Houston, TX, USA (M.B)

BC/CA/HI

Authors: Chih-lin Hsieh, Jerry Halpern, Raymond R. Balise, Ingrid Oakley-Girvan, Alice S. Whittemore

Affiliations: University of Southern California, Los Angeles, USA (C.-l.H.); Stanford University School of Medicine, Stanford, USA (J.H., R.N.B., and A.S.W.); Northern California Cancer Center, Union City and Stanford, USA (I.O.-G.)

Data Coordinating Center

Authors: Jianfeng Xu, Latchezar Dimitrov, Bao-Li Chang, Tamara S. Adams, Aubrey R. Turner, Deborah A. Meyers

Affiliations: Center for Human Genomics, Wake Forest University School of Medicine, Winston-Salem, NC, USA (J.X., L.D., B.-L.C., T.S.A., A.R.T., and D.A.M.)

Fred Hutchinson Cancer Research Center/Institute for Systems Biology

Authors: Danielle M. Friedrichsen, Kerry Deutsch, Suzanne Kolb, Marta Janer, Leroy Hood, Elaine A. Ostrander, Janet L. Stanford

Affiliations: Divisions of Human Biology (D.M.F.) and Public Health Sciences (S.K. and J.L.S.), Fred Hutchinson Cancer Center, and Institute for Systems Biology (K.D., M.J., and L.H.), Seattle, USA

Johns Hopkins University

Authors: Charles M. Ewing, Marta Gielzak, Sarah D. Isaacs, Patrick C. Walsh, Kathleen E. Wiley, William B. Isaacs

Affiliations: Department of Urology, Johns Hopkins Medical Institutions (C.M.E., M.G., S.D.I. P.C.W., K.E.W., and W.B.I), and Inherited Disease Research Branch, National Human Genome Research Institute, NIH (J.B.-W.), Baltimore, USA

University of Michigan

Authors: Ethan M. Lange, Lindsey A. Ho, Jennifer L. Beebe-Dimmer, David P. Wood, Kathleen A. Cooney

Affiliations: Departments of Genetics and Biostatistics, University of North Carolina, Chapel Hill, USA (E.M.L. and L.A.H); Departments of Internal Medicine and Urology, University of Michigan, Ann Arbor, USA (J.L.B.-D., D.P.W, and K.A.C.)

National Institutes of Health

Authors: Daniela Seminara

Affiliations: Cancer Genetics Branch, National Human Genome Research Institute, (E.A.O.), National Cancer Institute (NCI) (D.S.), and Inherited Disease Research Branch, National Human Genome Research Institute, (J.B-W.), National Institutes of Health, Bethesda, USA

University of Tampere and Tampere University Hospital

Authors: Tarja Ikonen, Agnes Baffoe-Bonnie, Henna Fredriksson, Mika P. Matikainen, Teuvo LJ Tammela, Joan Bailey-Wilson, Johanna Schleutker

Affiliations: University of Tampere and Tampere University Hospital, Tampere, Finland (T.I., H.F., M.P.M. T.L.T., and J. Schleutker); Fox Chase Cancer Center, Division of Population Science, Philadelphia, USA (A.B.-B.)

University of Ulm

Authors: Christiane Maier, Kathleen Herkommer, Josef J. Hoegel, Walther Vogel, Thomas Paiss

Affiliations: Abteilung Humangenetik, Universität Ulm, Ulm, Germany (C.M., J.J.H., and W.V.), and Urologische Universitätsklinik und Poliklinik, Abteilung für Urologie und Kinderurologie (K.H. and T.P.), Ulm, Germany

University of Umeå

Authors: Fredrik Wiklund, Monica Emanuelsson, Elisabeth Stenman, Björn-Anders Jonsson, Henrik Grönberg

Affiliations: Department of Radiation Sciences, Oncology, University of Umeå, Umeå, Sweden (F.W., M.E., E.S., B.-A.J., and H.G.)

University of Utah

Authors: Nicola J. Camp, James Farnham, Lisa A. Cannon-Albright

Affiliations: Division of Genetic Epidemiology, Department of Biomedical Informatics, University of Utah, Salt Lake City, USA (N.J.C., J.F., and L.C.A)

Washington University

Authors: William J. Catalona, Brian K. Suarez, and Kimberly A. Roehl

Affiliations: Department of Urology and the Robert H. Lurie Comprehensive Cancer Center, Northwestern University Feinberg School of Medicine, Chicago, IL, USA (W.J.C.); Department of Psychiatry, Washington University School of Medicine, St. Louis, MO, USA (B.K.S and K.A.R.)

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    Daniel J. Schaid

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Investigators of the International Consortium for Prostate Cancer Genetics

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Correspondence to Daniel J. Schaid.

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The names of all authors and their affiliations are listed in the Acknowledgements. The fact that Dr Schaid’s name is given here for purposes of correspondence should not be taken to imply that he played the sole leading part in writing this article.

An erratum to this article can be found at http://dx.doi.org/10.1007/s00439-006-0287-x

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Schaid, D.J., Investigators of the International Consortium for Prostate Cancer Genetics. Pooled genome linkage scan of aggressive prostate cancer: results from the International Consortium for Prostate Cancer Genetics. Hum Genet 120, 471–485 (2006). https://doi.org/10.1007/s00439-006-0219-9

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