Five endometrial cancer risk loci identified through genome-wide association analysis

doi:10.1038/ng.3562

Meta-Analysis

. 2016 Jun;48(6):667-674.

doi: 10.1038/ng.3562. Epub 2016 May 2.

Five endometrial cancer risk loci identified through genome-wide association analysis

Timothy Ht Cheng^#¹, Deborah J Thompson^#², Tracy A O'Mara³, Jodie N Painter³, Dylan M Glubb³, Susanne Flach¹, Annabelle Lewis¹, Juliet D French³, Luke Freeman-Mills¹, David Church¹, Maggie Gorman¹, Lynn Martin¹; National Study of Endometrial Cancer Genetics Group (NSECG); Shirley Hodgson⁴, Penelope M Webb³; Australian National Endometrial Cancer Study Group (ANECS); John Attia^{5

6}, Elizabeth G Holliday^{5

6}, Mark McEvoy⁶, Rodney J Scott^{5

7

8

9}, Anjali K Henders³, Nicholas G Martin³, Grant W Montgomery³, Dale R Nyholt^{3

10}, Shahana Ahmed¹¹, Catherine S Healey¹¹, Mitul Shah¹¹, Joe Dennis², Peter A Fasching^{12

13}, Matthias W Beckmann¹³, Alexander Hein¹³, Arif B Ekici¹⁴, Per Hall¹⁵, Kamila Czene¹⁵, Hatef Darabi¹⁵, Jingmei Li¹⁵, Thilo Dörk¹⁶, Matthias Dürst¹⁷, Peter Hillemanns¹⁸, Ingo Runnebaum¹⁷, Frederic Amant¹⁹, Stefanie Schrauwen¹⁹, Hui Zhao^{20

21}, Diether Lambrechts^{20

21}, Jeroen Depreeuw^{19

20

21}, Sean C Dowdy²², Ellen L Goode²³, Brooke L Fridley²⁴, Stacey J Winham²³, Tormund S Njølstad^{25

26}, Helga B Salvesen^{25

26}, Jone Trovik^{25

26}, Henrica Mj Werner^{25

26}, Katie Ashton^{5

8

9}, Geoffrey Otton²⁷, Tony Proietto²⁷, Tao Liu²⁸, Miriam Mints²⁹, Emma Tham^{28

30}; RENDOCAS; Chibcha Consortium^{1

31}, Mulin Jun Li³², Shun H Yip³², Junwen Wang³², Manjeet K Bolla², Kyriaki Michailidou², Qin Wang², Jonathan P Tyrer¹¹, Malcolm Dunlop^{33

34}, Richard Houlston³⁵, Claire Palles¹, John L Hopper³⁶; AOCS Group; Julian Peto³⁷, Anthony J Swerdlow^{35

38}, Barbara Burwinkel^{39

40}, Hermann Brenner^{41

42}, Alfons Meindl⁴³, Hiltrud Brauch^{42

44

45}, Annika Lindblom²⁸, Jenny Chang-Claude^{46

47}, Fergus J Couch^{23

48}, Graham G Giles^{36

49

50}, Vessela N Kristensen^{51

52}, Angela Cox⁵³, Julie M Cunningham⁴⁸, Paul D P Pharoah¹¹, Alison M Dunning¹¹, Stacey L Edwards³, Douglas F Easton^{2

11}, Ian Tomlinson¹, Amanda B Spurdle³

Affiliations

¹ Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK.
² Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
³ Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia.
⁴ Department of Clinical Genetics, St George's, University of London, London, UK.
⁵ Hunter Medical Research Institute, John Hunter Hospital, Newcastle, NSW, Australia.
⁶ Centre for Clinical Epidemiology and Biostatistics, School of Medicine and Public Health, University of Newcastle, NSW, Australia.
⁷ Hunter Area Pathology Service, John Hunter Hospital, Newcastle, NSW, Australia.
⁸ Centre for Information Based Medicine, University of Newcastle, NSW, Australia.
⁹ School of Biomedical Sciences and Pharmacy, University of Newcastle, Newcastle, NSW, Australia.
¹⁰ Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia.
¹¹ Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
¹² University of California at Los Angeles, Department of Medicine, Division of Hematology/Oncology, David Geffen School of Medicine, Los Angeles, CA, USA.
¹³ Department of Gynecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany.
¹⁴ Institute of Human Genetics, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany.
¹⁵ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
¹⁶ Hannover Medical School, Gynaecology Research Unit, Hannover, Germany.
¹⁷ Department of Gynaecology, Jena University Hospital - Friedrich Schiller University, Jena, Germany.
¹⁸ Hannover Medical School, Clinics of Gynaecology and Obstetrics, Hannover, Germany.
¹⁹ Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, University Hospitals, KU Leuven - University of Leuven, Belgium.
²⁰ Vesalius Research Center, VIB, Leuven, Belgium.
²¹ Laboratory for Translational Genetics, Department of Oncology, University Hospitals Leuven, Leuven, Belgium.
²² Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, Mayo Clinic, Rochester, MN, USA.
²³ Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.
²⁴ Department of Biostatistics, University of Kansas Medical Center, Kansas City, KS, USA.
²⁵ Centre for Cancerbiomarkers, Department of Clinical Science, The University of Bergen, Norway.
²⁶ Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway.
²⁷ School of Medicine and Public Health, University of Newcastle, Newcastle, NSW, Australia.
²⁸ Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
²⁹ Department of Women's and Children's Health, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.
³⁰ Clinical Genetics, Karolinska University Hospital Solna, Stockholm, Sweden.
³¹ A list of members and affiliations appears in the Supplementary Note.
³² Centre for Genomic Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China.
³³ Colon Cancer Genetics Group, Institute of Genetics and Molecular Medicine, University of Edinburgh, Edinburgh, UK.
³⁴ MRC Human Genetics Unit, Western General Hospital Edinburgh, Edinburgh, UK.
³⁵ Division of Genetics and Epidemiology, Institute of Cancer Research, London, UK.
³⁶ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Vic, Australia.
³⁷ London School of Hygiene and Tropical Medicine, London, UK.
³⁸ Division of Breast Cancer Research, Institute of Cancer Research, London, UK.
³⁹ Molecular Biology of Breast Cancer, Department of Gynecology and Obstetrics, University of Heidelberg, Heidelberg, Germany.
⁴⁰ Molecular Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴¹ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴² German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴³ Department of Obstetrics and Gynecology, Division of Tumor Genetics, Technical University of Munich, Munich, Germany.
⁴⁴ Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, Stuttgart, Germany.
⁴⁵ University of Tübingen, Tübingen, Germany.
⁴⁶ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴⁷ University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁴⁸ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁴⁹ Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Vic, Australia.
⁵⁰ Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Vic, Australia.
⁵¹ Department of Genetics, Institute for Cancer Research, The Norwegian Radium Hospital, Oslo, Norway.
⁵² Department of Clinical Molecular Oncology, Division of Medicine, Akershus University Hospital, Lørenskog, Norway.
⁵³ Sheffield Cancer Research, Department of Oncology, University of Sheffield, Sheffield, UK.

^# Contributed equally.

PMID: 27135401
PMCID: PMC4907351
DOI: 10.1038/ng.3562

Meta-Analysis

Five endometrial cancer risk loci identified through genome-wide association analysis

Timothy Ht Cheng et al. Nat Genet. 2016 Jun.

. 2016 Jun;48(6):667-674.

doi: 10.1038/ng.3562. Epub 2016 May 2.

Authors

Affiliations

¹ Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK.
² Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Cambridge, UK.
³ Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia.
⁴ Department of Clinical Genetics, St George's, University of London, London, UK.
⁵ Hunter Medical Research Institute, John Hunter Hospital, Newcastle, NSW, Australia.
⁶ Centre for Clinical Epidemiology and Biostatistics, School of Medicine and Public Health, University of Newcastle, NSW, Australia.
⁷ Hunter Area Pathology Service, John Hunter Hospital, Newcastle, NSW, Australia.
⁸ Centre for Information Based Medicine, University of Newcastle, NSW, Australia.
⁹ School of Biomedical Sciences and Pharmacy, University of Newcastle, Newcastle, NSW, Australia.
¹⁰ Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia.
¹¹ Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Cambridge, UK.
¹² University of California at Los Angeles, Department of Medicine, Division of Hematology/Oncology, David Geffen School of Medicine, Los Angeles, CA, USA.
¹³ Department of Gynecology and Obstetrics, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nuremberg, Erlangen, Germany.
¹⁴ Institute of Human Genetics, University Hospital Erlangen, Friedrich-Alexander-University Erlangen-Nuremberg, Erlangen, Germany.
¹⁵ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
¹⁶ Hannover Medical School, Gynaecology Research Unit, Hannover, Germany.
¹⁷ Department of Gynaecology, Jena University Hospital - Friedrich Schiller University, Jena, Germany.
¹⁸ Hannover Medical School, Clinics of Gynaecology and Obstetrics, Hannover, Germany.
¹⁹ Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, University Hospitals, KU Leuven - University of Leuven, Belgium.
²⁰ Vesalius Research Center, VIB, Leuven, Belgium.
²¹ Laboratory for Translational Genetics, Department of Oncology, University Hospitals Leuven, Leuven, Belgium.
²² Department of Obstetrics and Gynecology, Division of Gynecologic Oncology, Mayo Clinic, Rochester, MN, USA.
²³ Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.
²⁴ Department of Biostatistics, University of Kansas Medical Center, Kansas City, KS, USA.
²⁵ Centre for Cancerbiomarkers, Department of Clinical Science, The University of Bergen, Norway.
²⁶ Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway.
²⁷ School of Medicine and Public Health, University of Newcastle, Newcastle, NSW, Australia.
²⁸ Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden.
²⁹ Department of Women's and Children's Health, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.
³⁰ Clinical Genetics, Karolinska University Hospital Solna, Stockholm, Sweden.
³¹ A list of members and affiliations appears in the Supplementary Note.
³² Centre for Genomic Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China.
³³ Colon Cancer Genetics Group, Institute of Genetics and Molecular Medicine, University of Edinburgh, Edinburgh, UK.
³⁴ MRC Human Genetics Unit, Western General Hospital Edinburgh, Edinburgh, UK.
³⁵ Division of Genetics and Epidemiology, Institute of Cancer Research, London, UK.
³⁶ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Vic, Australia.
³⁷ London School of Hygiene and Tropical Medicine, London, UK.
³⁸ Division of Breast Cancer Research, Institute of Cancer Research, London, UK.
³⁹ Molecular Biology of Breast Cancer, Department of Gynecology and Obstetrics, University of Heidelberg, Heidelberg, Germany.
⁴⁰ Molecular Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴¹ Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴² German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴³ Department of Obstetrics and Gynecology, Division of Tumor Genetics, Technical University of Munich, Munich, Germany.
⁴⁴ Dr. Margarete Fischer-Bosch-Institute of Clinical Pharmacology, Stuttgart, Germany.
⁴⁵ University of Tübingen, Tübingen, Germany.
⁴⁶ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
⁴⁷ University Cancer Center Hamburg (UCCH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
⁴⁸ Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, USA.
⁴⁹ Cancer Epidemiology Centre, Cancer Council Victoria, Melbourne, Vic, Australia.
⁵⁰ Department of Epidemiology and Preventive Medicine, Monash University, Melbourne, Vic, Australia.
⁵¹ Department of Genetics, Institute for Cancer Research, The Norwegian Radium Hospital, Oslo, Norway.
⁵² Department of Clinical Molecular Oncology, Division of Medicine, Akershus University Hospital, Lørenskog, Norway.
⁵³ Sheffield Cancer Research, Department of Oncology, University of Sheffield, Sheffield, UK.

^# Contributed equally.

PMID: 27135401
PMCID: PMC4907351
DOI: 10.1038/ng.3562

Abstract

We conducted a meta-analysis of three endometrial cancer genome-wide association studies (GWAS) and two follow-up phases totaling 7,737 endometrial cancer cases and 37,144 controls of European ancestry. Genome-wide imputation and meta-analysis identified five new risk loci of genome-wide significance at likely regulatory regions on chromosomes 13q22.1 (rs11841589, near KLF5), 6q22.31 (rs13328298, in LOC643623 and near HEY2 and NCOA7), 8q24.21 (rs4733613, telomeric to MYC), 15q15.1 (rs937213, in EIF2AK4, near BMF) and 14q32.33 (rs2498796, in AKT1, near SIVA1). We also found a second independent 8q24.21 signal (rs17232730). Functional studies of the 13q22.1 locus showed that rs9600103 (pairwise r(2) = 0.98 with rs11841589) is located in a region of active chromatin that interacts with the KLF5 promoter region. The rs9600103[T] allele that is protective in endometrial cancer suppressed gene expression in vitro, suggesting that regulation of the expression of KLF5, a gene linked to uterine development, is implicated in tumorigenesis. These findings provide enhanced insight into the genetic and biological basis of endometrial cancer.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

**Figure 1. Endometrial cancer meta-analysis Manhattan plot**
Manhattan plot of −log₁₀-transformed P-values from meta-analysis of 22 autosomes. There are seven loci surpassing genome-wide significance including two known loci: 15q21 (*CYP19A1*) and 17q12 (*HNF1B*) and five novel loci: 6q22 (*NCOA7, HEY2*), 8q24 (*MYC*), 13q22 (*KLF5*), 14q32 (*AKT1, SIVA1*), 15q15 (*EIF2AK4, BMF*).

**Figure 2. Forest plots of novel endometrial cancer risk loci**
The odds ratio and 95% confidence intervals of each study of the meta-analysis are listed and shown in the adjacent plot. The I² heterogeneity scores (all <0.4) suggest that there is no marked difference in effects between studies. The SNPs represented are: a) rs11841589 (13q22), b) rs13328298 (6q22), c) rs4733613 (8q24), d) rs17232730 (8q24, pairwise r² 0.02 with rs4733613), e) rs937213 (15q15) and f) rs2498796 (14q32).

**Figure 3. Regional association plots for the five novel loci associated with endometrial cancer.**
The −log₁₀ P-values from the meta-analysis and regional imputation for three GWAS and eight iCOGS groups are shown for SNPs at: a) 13q22.1, b) 6q22, c) & d) 8q24, e) 15q15 and f) 14q32.33. The SNP with the lowest P-value at each locus is labeled and marked as a purple diamond, and the dot color represents the LD with the top SNP. The blue line shows recombination rates in cM/Mb. All plotted SNPs are either genotyped or have an IMPUTE info score of more than 0.9 in all datasets. Although genome-wide significant results for the 14q32.33 locus rely on imputed data, it should be noted that there is strong support from nearby genotyped markers. Supplementary Figure 6 displays similar regional association plots with a larger number of SNPs using a less stringent info score cut-off.

**Figure 4. The 13q22.1 endometrial cancer susceptibility locus**
a) Diagram showing the 16kb region around rs11841589, rs9600103 and correlated SNPs rs7981863, rs7988505 and rs7989799 (black marks), DNaseI hypersensitivity site (DHS) density signal in estrogen- and tamoxifen-treated ENCODE Ishikawa cells (Supplementary Note), and 100 vertebrates conservation. Vertical dotted line represents the position of rs9600103. FAIRE and ChIP assays for H3K4Me2 and H4Ac in endometrial cancer cell lines ARK-2 (rs9600103-TT), Ishikawa (rs9600103-AA) and AN3CA (rs9600103-AA) show evidence for enrichment of histone modifications. b) 3C experiment for KLF5-expressing Ishikawa cells. Relative interaction frequencies between an *Nco*I restriction fragment containing risk SNPs rs9600103 and rs11841589 (bait fragment) and *Nco*I fragments across the *KLF5* promoter region, plotted against fragment position on chromosome 13. *Nco*I restriction sites are displayed below the schematic of *KLF5* transcripts. H3K4Me3 binding, indicative of promoters, from multiple ENCODE cell lines are also shown.. The graph represents three biological replicates. Error bars represent standard deviation. A significant interaction was seen with the fragment containing a *KLF5* transcriptional start site (fragment shaded in grey). c) Luciferase reporter assays to analyze the activity of 3kb fragments containing either rs9600103 or rs11841589 using the pGL3-Promoter vector in Ishikawa cells. Green arrows represent the low-risk alleles, and red arrows the high-risk alleles. Error bars represent the standard error of the mean (n=3). Luciferase activity for the rs9600103-A risk allele was more than double that of the rs9600103-T protective allele (P=0.018). There was no significant difference in luciferase activity between the rs11841589 alleles (Supplementary Table 7).

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References

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64:9–29. - PubMed
1. Ferlay J, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013;49:1374–1403. - PubMed
1. Gruber SB, Thompson WD. A population-based study of endometrial cancer and familial risk in younger women. Cancer and Steroid Hormone Study Group. Cancer Epidemiol Biomarkers Prev. 1996;5:411–417. - PubMed
1. Win AK, Reece JC, Ryan S. Family history and risk of endometrial cancer: a systematic review and meta-analysis. Obstet Gynecol. 2015;125:89–98. - PubMed
1. Barrow E, Hill J, Evans DG. Cancer risk in Lynch Syndrome. Fam Cancer. 2013;12:229–240. - PubMed

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[1] Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64:9–29. - PubMed

[2] Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014;64:9–29. - PubMed

[3] Ferlay J, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013;49:1374–1403. - PubMed

[4] Ferlay J, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013;49:1374–1403. - PubMed

[5] Gruber SB, Thompson WD. A population-based study of endometrial cancer and familial risk in younger women. Cancer and Steroid Hormone Study Group. Cancer Epidemiol Biomarkers Prev. 1996;5:411–417. - PubMed

[6] Gruber SB, Thompson WD. A population-based study of endometrial cancer and familial risk in younger women. Cancer and Steroid Hormone Study Group. Cancer Epidemiol Biomarkers Prev. 1996;5:411–417. - PubMed

[7] Win AK, Reece JC, Ryan S. Family history and risk of endometrial cancer: a systematic review and meta-analysis. Obstet Gynecol. 2015;125:89–98. - PubMed

[8] Win AK, Reece JC, Ryan S. Family history and risk of endometrial cancer: a systematic review and meta-analysis. Obstet Gynecol. 2015;125:89–98. - PubMed

[9] Barrow E, Hill J, Evans DG. Cancer risk in Lynch Syndrome. Fam Cancer. 2013;12:229–240. - PubMed

[10] Barrow E, Hill J, Evans DG. Cancer risk in Lynch Syndrome. Fam Cancer. 2013;12:229–240. - PubMed

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Five endometrial cancer risk loci identified through genome-wide association analysis

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Five endometrial cancer risk loci identified through genome-wide association analysis

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