Cancer Genetics

You have full text access to this OnlineOpen article

Common alleles in candidate susceptibility genes associated with risk and development of epithelial ovarian cancer

  1. Maria Notaridou1,†,
  2. Lydia Quaye1,†,
  3. Dimitra Dafou2,†,
  4. Chris Jones1,
  5. Honglin Song3,
  6. Estrid Høgdall4,
  7. Susanne K. Kjaer4,
  8. Lise Christensen5,
  9. Claus Høgdall6,
  10. Jan Blaakaer7,
  11. Valerie McGuire8,
  12. Anna H. Wu9,
  13. David J. Van Den Berg9,
  14. Malcolm C. Pike9,
  15. Aleksandra Gentry-Maharaj1,
  16. Eva Wozniak1,
  17. Tanya Sher1,
  18. Ian J. Jacobs1,‡,
  19. Jonathan Tyrer3,
  20. Joellen M. Schildkraut10,
  21. Patricia G. Moorman10,
  22. Edwin S. Iversen11,
  23. Anna Jakubowska12,
  24. Krzysztof Mędrek12,
  25. Jan Lubiński12,
  26. Roberta B. Ness13,
  27. Kirsten B. Moysich14,
  28. Galina Lurie15,
  29. Lynne R. Wilkens15,
  30. Michael E. Carney15,
  31. Shan Wang-Gohrke16,
  32. Jennifer A. Doherty17,
  33. Mary Anne Rossing17,
  34. Matthias W. Beckmann18,
  35. Falk C. Thiel18,
  36. Arif B. Ekici19,
  37. Xiaoqing Chen20,
  38. Jonathan Beesley20,
  39. The Australian Ovarian Cancer Study Group/Australian Cancer Study (Ovarian Cancer)20,21,
  40. Jacek Gronwald12,
  41. Peter A. Fasching18,22,
  42. Jenny Chang-Claude23,
  43. Marc T. Goodman15,
  44. Georgia Chenevix-Trench20,
  45. Andrew Berchuck24,
  46. C. Leigh Pearce9,
  47. Alice S. Whittemore8,
  48. Usha Menon1,
  49. Paul D.P. Pharoah3,
  50. Simon A. Gayther1,*,
  51. Susan J. Ramus1,
  52. on behalf of the Ovarian Cancer Association Consortium24

Article first published online: 15 JUL 2010

DOI: 10.1002/ijc.25554

Issue

International Journal of Cancer

International Journal of Cancer

Volume 128, Issue 9, pages 2063–2074, 1 May 2011

Additional Information

How to Cite

Notaridou, M., Quaye, L., Dafou, D., Jones, C., Song, H., Høgdall, E., Kjaer, S. K., Christensen, L., Høgdall, C., Blaakaer, J., McGuire, V., Wu, A. H., Van Den Berg, D. J., Pike, M. C., Gentry-Maharaj, A., Wozniak, E., Sher, T., Jacobs, I. J., Tyrer, J., Schildkraut, J. M., Moorman, P. G., Iversen, E. S., Jakubowska, A., Mędrek, K., Lubiński, J., Ness, R. B., Moysich, K. B., Lurie, G., Wilkens, L. R., Carney, M. E., Wang-Gohrke, S., Doherty, J. A., Rossing, M. A., Beckmann, M. W., Thiel, F. C., Ekici, A. B., Chen, X., Beesley, J., The Australian Ovarian Cancer Study Group/Australian Cancer Study (Ovarian Cancer), Gronwald, J., Fasching, P. A., Chang-Claude, J., Goodman, M. T., Chenevix-Trench, G., Berchuck, A., Pearce, C. L., Whittemore, A. S., Menon, U., Pharoah, P. D.P., Gayther, S. A., Ramus, S. J. and on behalf of the Ovarian Cancer Association Consortium (2011), Common alleles in candidate susceptibility genes associated with risk and development of epithelial ovarian cancer. Int. J. Cancer, 128: 2063–2074. doi: 10.1002/ijc.25554

Author Information

  1. 1

    Gynaecological Oncology Unit, UCL EGA Institute for Women's Health, University College London, United Kingdom

  2. 2

    Department of Medical and Molecular Genetics, King's College London School of Medicine, Guy's Hospital, London, United Kingdom

  3. 3

    CR-UK Department of Oncology, University of Cambridge, Strangeways Research Laboratory, Cambridge, United Kingdom

  4. 4

    Department of Viruses, Hormones and Cancer, Institute of Cancer Epidemiology, Danish Cancer Society, Copenhagen, Denmark

  5. 5

    Department of Pathology, Bispebjerg Hospital, University of Copenhagen, Copenhagen, Denmark

  6. 6

    The Gynaecologic Clinic, The Juliane Marie Centre, Rigshospitalet, University of Copenhagen, Denmark

  7. 7

    Department of Gynaecology and Obstetrics, Aarhus University Hospital, Skejby, Aarhus, Denmark

  8. 8

    Department of Health Research and Policy, Stanford University School of Medicine, Stanford, CA

  9. 9

    University of Southern California, Keck School of Medicine, Department of Preventive Medicine, Los Angeles, CA

  10. 10

    Department of Community and Family Medicine, Duke University Medical Center, Durham, NC

  11. 11

    Department of Statistical Science, Duke University, Medical Center, Durham, NC

  12. 12

    Department of Genetics and Pathology, International Hereditary Cancer Center, Pomeranian Medical University, Szczecin, Poland

  13. 13

    University of Texas, School of Public Health, Houston, TX

  14. 14

    Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Buffalo, NY

  15. 15

    Cancer Research Center of Hawaii, University of Hawaii, Honolulu, HI

  16. 16

    Department of Obstetrics and Gynecology, University of Ulm, Ulm, Germany

  17. 17

    Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington

  18. 18

    Department of Gynecology and Obstetrics, University Hospital Erlangen, Erlangen, Germany

  19. 19

    Institute of Human Genetics, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany

  20. 20

    Genetics and Population Health, The Queensland Institute of Medical Research, Post Office Royal Brisbane Hospital, Australia

  21. 21

    Research Division, Peter MacCallum Cancer Centre, Melbourne, Australia

  22. 22

    Division of Hematology and Oncology, University of California at Los Angeles, David Geffen School of Medicine, Los Angeles, CA

  23. 23

    Division of Cancer Epidemiology, German Cancer Research Center, Heidelberg, Germany

  24. 24

    Department of Obstetrics and Gynecology/Division of Gynecologic Oncology, Duke University Medical Center, Durham, NC, 27710

  1. †

    M.N., L.Q., and D.D. contributed equally to this work.

  2. ‡

    Professor Ian J. Jacobs is a consultant to Beckton Dickinson in the field of ovarian cancer.

*Gynaecological Oncology Unit, UCL EGA Institute for Women's Health, University College London, Gower Street, London, WC1E 6BT, United Kingdom

Publication History

  1. Issue published online: 8 MAR 2011
  2. Article first published online: 15 JUL 2010
  3. Accepted manuscript online: 15 JUL 2010 12:00AM EST
  4. Manuscript Accepted: 24 JUN 2010
  5. Manuscript Revised: 26 MAY 2010
  6. Manuscript Received: 26 MAR 2010

Funded by

  • Cancer Research UK project grant. Grant Number: C8804/A7058
  • National Cancer Institute the Danish Cancer Society (MALOVA). Grant Number: RO1 CA61107
  • The Roswell Park Alliance and the National Cancer Institute (GEOCS study). Grant Number: CA71766 and Core Grant CA16056
  • NIH grant (the DOVE study). Grant Number: RO1 CA87538
  • NCI grants and Department of Defence grant (The HOPE project). Grant Number: K07-CA80668 and R01CA095023, and DAMD17-02-1-0669
  • California Cancer Research Program. Grant Numbers: 00-01389V-20170, 2110200
  • U.S. Public Health Service and California Department of Health Services sub-contract as part of its statewide cancer reporting program (University of Southern California). Grant Numbers: CA14089, CA17054, CA61132, CA63464, N01-PC-67010 and R03-CA113148 and sub-contract 050-E8709
  • U.S. Public Health Service grant and contracts from the Department of Health and Human Services, National Institutes of Health (HAW study). Grant Number: R01-CA-58598, and contracts N01-CN67001 and NO1-PC-035137

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (331K)

References

  • 1
    Stratton JF, Gayther SA, Russell P, Dearden J, Gore M, Blake P, Easton D, Ponder BA. Contribution of BRCA1 mutations to ovarian cancer. N Engl J Med 1997; 336: 1125–30.
  • 2
    Ramus SJ, Harrington PA, Pye C, DiCioccio RA, Cox MJ, Garlinghouse-Jones K, Oakley-Girvan I, Jacobs IJ, Hardy RM, Whittemore AS, Ponder BA, Piver MS, et al. Screening for the. BRCA1-ins6kb. Ex13 mutation: potential for misdiagnosis. Mutation in brief #964. Online. Hum Mutat 2007; 28: 525–6.
    Direct Link:
  • 3
    Gayther SA, Russell P, Harrington P, Antoniou AC, Easton DF, Ponder BA. The contribution of germline BRCA1 and BRCA2 mutations to familial ovarian cancer: no evidence for other ovarian cancer-susceptibility genes. Am J Hum Genet 1999; 65: 1021–9.
  • 4
    Antoniou AC, Easton DF. Risk prediction models for familial breast cancer. Future Oncol 2006; 2: 257–74.
  • 5
    Pharoah PD, Antoniou A, Bobrow M, Zimmern RL, Easton DF, Ponder BA. Polygenic susceptibility to breast cancer and implications for prevention. Nat Genet 2002; 31: 33–36.
  • 6
    Easton DF, Eeles RA. Genome-wide association studies in cancer. Hum Mol Genet 2008; 17: R109–15.
  • 7
    McCarthy MI, Hirschhorn JN. Genome-wide association studies: past, present and future. Hum Mol Genet 2008; 17: R100–1.
  • 8
    Pearce CL, Hirschhorn JN, Wu AH, Burtt NP, Stram DO, Young S, Kolonel LN, Henderson BE, Altshuler D, Pike MC. Clarifying the PROGINS allele association in ovarian and breast cancer risk: a haplotype-based analysis. J Natl Cancer Inst 2005; 97: 51–9.
  • 9
    Song H, Ramus SJ, Shadforth D, Quaye L, Kjaer SK, Dicioccio RA, Dunning AM, Hogdall E, Hogdall C, Whittemore AS, McGuire V, Lesueur F, et al. Common variants in RB1 gene and risk of invasive ovarian cancer. Cancer Res 2006; 66: 10220–6.
  • 10
    Song H, Ramus SJ, Kjaer SK, Hogdall E, Dicioccio RA, Whittemore AS, McGuire V, Hogdall C, Jacobs IJ, Easton DF, Ponder BA, Dunning AM, et al. Tagging single nucleotide polymorphisms in the BRIP1 gene and susceptibility to breast and ovarian cancer. PLoS ONE 2007; 2: e268.
  • 11
    Song H, Ramus SJ, Quaye L, DiCioccio RA, Tyrer J, Lomas E, Shadforth D, Hogdall E, Hogdall C, McGuire V, Whittemore AS, Easton DF, et al. Common variants in mismatch repair genes and risk of invasive ovarian cancer. Carcinogenesis 2006; 27: 2235–42.
  • 12
    Quaye L, Song H, Ramus SJ, Di Cioccio RA, McGuire V, Hogdall E, Hogdall C, Blaakr J, Easton DF, Ponder BA, Jacobs I, Kjaer SK, et al. Tagging single nucleotide polymorphisms in candidate oncogenes and susceptibility to ovarian cancer. Br J Cancer 2009; 100: 993–1001.
  • 13
    Fasching PA, Gayther SA, Pearce CL, Schildkraut JM, Goode E, Thiel F, Chenevix-Trench G, Chang-Claude J, Wang-Gohrke S, Ramus SJ, Pharoah PDP, Berchuck A, et al. Role of genetic polymorphisms and ovarian cancer susceptibility. Mol Oncol 2009; 3: 171–81.
  • 14
    Gayther SA, Song H, Ramus SJ, Kjaer SK, Whittemore AS, Quaye L, Tyrer J, Shadforth D, Hogdall E, Hogdall C, Blaeker J, DiCioccio R, et al. Tagging single nucleotide polymorphisms in cell cycle control genes and susceptibility to invasive epithelial ovarian cancer. Cancer Res 2007; 67: 3027–35.
  • 15
    Ramus SJ, Vierkant RA, Johnatty SE, Pike MC, Van Den Berg DJ, Wu AH, Pearce CL, Menon U, Gentry-Maharaj A, Gayther SA, Dicioccio RA, McGuire V, et al. Consortium analysis of seven candidate snps for ovarian cancer. Int J Cancer 2008; 123: 380–8.
    Direct Link:
  • 16
    Quaye L, Dafou D, Ramus SJ, Song H, Gentry-Maharaj A, Notaridou M, Hogdall E, Kjaer SK, Christensen L, Hogdall C, Easton DF, Jacobs I, et al. Functional complementation studies identify candidate genes and common genetic variants associated with ovarian cancer survival. Hum Mol Genet 2009; 18: 1869–78.
  • 17
    Dafou D, Ramus SJ, Choi K, Grun B, Trott DA, Newbold RF, Jacobs IJ, Jones C, Gayther SA. Neoplastic suppression in epithelial ovarian cancer cells lines by microcell-mediated transfer of chromosomes 5, 6 and 18. Int J Cancer 2009; 124: 1037–44.
    Direct Link:
  • 18
    Provencher DM, Lounis H, Champoux L, Tétrault M, Manderson EN, Wang JC, Eydoux P, Savoie R, Tonin PN, Mes-Masson AM. Characterization of four novel epithelial ovarian cancer cell lines. In Vitro Cell Dev Biol Anim 2000; 36: 357–61.
  • 19
    Benjamini Y, Yekutieli D. Quantitative trait loci analysis using the false discovery rate. Genetics 2005; 171: 783–90.
  • 20
    Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005; 21: 263–5.
  • 21
    de Bakker PI, Yelensky R, Pe'er I, Gabriel SB, Daly MJ, Altshuler D. Efficiency and power in genetic association studies. Nat Genet 2005; 37: 1217–23.
  • 22
    Song H, Ramus SJ, Tyrer J, Bolton K, Gentry-Maharaj A, Wozniak E, Anton-Culver H, Chang-Claude J, Cramer DW, DiCioccio R, Dörk T, Goode EL, et al. Genome-wide association study identifies a novel ovarian cancer susceptibility locus on 9p22.2. Nat Genet 2009; 41: 996–1000.
  • 23
    Khalique L, Ayhan A, Weale M, Jacobs IJ, Ramus SJ, Gayther SA. Genetic intra tumour heterogeneity in epithelial ovarian cancer: the implications for clinical diagnostics. J Pathol 2007; 211: 286–95.
    Direct Link:
  • 24
    Canzian F, Salovaara R, Hemminki A, Kristo P, Chadwick RB, Aaltonen LA, de la Chapelle A. Semiautomated assessment of loss of heterozygosity and replication error in tumors. Cancer Res 1996; 56: 3331–7.
  • 25
    Stram DO, Haiman CA, Hirschhorn JN, Altshuler D, Kolonel LN, Henderson BE, Pike MC. Choosing haplotype-tagging SNPS based on unphased genotype data using a preliminary sample of unrelated subjects with an example from the Multiethnic Cohort Study. Hum Hered 2003; 55: 27–36.
  • 26
    Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, Higgins J, DeFelice M, Lochner A, Faggart M, Liu-Cordero SN, Rotimi C, et al. The structure of haplotype blocks in the human genome. Science 2002; 296: 2225–9.
  • 27
    Zaykin DV, Westfall PH, Young SS, Karnoub MA, Wagner MJ, Ehm MG. Testing association of statistically inferred haplotypes with discrete and continuous traits in samples of unrelated individuals. Hum Hered 2002; 53: 79–91.
  • 28
    Knudson AG. All in the (cancer) family. Nat Genet 1993; 5: 103–104.
  • 29
    Thomas DC, Haile RW, Duggan D. Recent developments in genomewide association scans: a workshop summary and review. Am J Hum Genet 2005; 77: 337–45.
  • 30
    Lakhani SR, Manek S, Penault-Llorca F, Flanagan A, Arnout L, Merrett S, McGuffog L, Steele D, Devilee P, Klijn JG, Meijers-Heijboer H, Radice P, et al. Pathology of ovarian cancers in BRCA1 and BRCA2 carriers. Clin Cancer Res 2004; 10: 2473–81.
  • 31
    Pearce CL, Wu AH, Gayther SA, Bale AE; Australian Cancer Study (Ovarian Cancer) and Australian Cancer Study Group, Beck PA, Beesley J, Chanock S, Cramer DW, DiCioccio R, Edwards R, Fredericksen ZS, et al. Progesterone receptor variation and risk of ovarian cancer is limited to the invasive endometrioid subtype: results from the Ovarian Cancer Association Consortium pooled analysis. Br J Cancer 2008; 98: 282–8.
  • 32
    LaFramboise T, Weir BA, Zhao X, Beroukhim R, Li C, Harrington D, Sellers WR, Meyerson M. Allele-specific amplification in cancer revealed by SNP array analysis. PLoS Comput Biol 1: e65, 2005.
  • 33
    Mao X, Hamoudi RA, Talbot IC, Baudis M. Allele-specific loss of heterozygosity in multiple colorectal adenomas: toward an integrated molecular cytogenetic map II. Cancer Genet Cytogenet 2006; 167: 1–14.
  • 34
    Kittiniyom K, Mastronardi M, Roemer M, Wells WA, Greenberg ER, Titus-Ernstoff L, Newsham IF. Allele-specific loss of heterozygosity at the DAL-1/4.1B (EPB41L3) tumor-suppressor gene locus in the absence of mutation. Genes Chromosomes Cancer 2004; 40: 190–203.
    Direct Link:
  • 35
    Wang M, Vikis HG, Wang Y, Jia D, Wang D, Bierut LJ, Bailey-Wilson JE, Amos CI, Pinney SM, Petersen GM, de Andrade M, Yang P, et al. Identification of a novel tumor suppressor gene p34 on human chromosome 6q25.1. Cancer Res 2007; 67: 93–9.
  • 36
    Wegman PP, Marcus NJ, Malakkaran BP, Wingren S. Biological significance of allele specific loss of the p53 gene in breast carcinomas. Breast Cancer Res Treat 2009; 118: 15–20.
  • 37
    Pezzi N, Prieto I, Kremer L, Pérez Jurado LA, Valero C, Del Mazo J, Martínez-A C, Barbero JL. STAG3, a novel gene encoding a protein involved in meiotic chromosome pairing and location of STAG3-related genes flanking the Williams-Beuren syndrome deletion. FASEB J 2000; 14: 581–92.
  • 38
    Prieto I, Suja JA, Pezzi N, Kremer L, Martínez-A C, Rufas JS, Barbero JL. Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nat Cell Biol 2001; 3: 761–6.
  • 39
    Novak I, Lightfoot DA, Wang H, Eriksson A, Mahdy E, Höög C. Mouse embryonic stem cells form follicle-like ovarian structures but do not progress through meiosis. Stem Cells 2006; 24: 1931–6.
    Direct Link:
  • 40
    Kalejs M, Ivanov A, Plakhins G, Cragg MS, Emzinsh D, Illidge TM, Erenpreisa J. Upregulation of meiosis-specific genes in lymphoma cell lines following genotoxic insult and induction of mitotic catastrophe. BMC Cancer 2006; 6: 6.
  • 41
    Barber TD, McManus K, Yuen KW, Reis M, Parmigiani G, Shen D, Barrett I, Nouhi Y, Spencer F, Markowitz S, Velculescu VE, Kinzler KW, et al. Chromatid cohesion defects may underlie chromosome instability in human colorectal cancers. Proc Natl Acad Sci USA 2008; 105: 3443–8.
  • 42
    Skotheim RI, Lind GE, Monni O, Nesland JM, Abeler VM, Fosså SD, Duale N, Brunborg G, Kallioniemi O, Andrews PW, Lothe RA. Differentiation of human embryonal carcinomas in vitro and in vivo reveals expression profiles relevant to normal development. Cancer Res 2005; 65: 5588–98.
View Full Article with Supporting Information (HTML) Get PDF (331K)