A Common Variant at the 14q32 Endometrial Cancer Risk Locus Activates AKT1 through YY1 Binding

American Journal of Human Genetics

Volumn 98, Issue 6, 2016, Pages 1159-1169

  Painter, Jodie N ^a   Kaufmann, Susanne ^a   O'Mara, Tracy A ^a   Hillman, Kristine M ^a   Sivakumaran, Haran ^a   Darabi, Hatef ^b   Cheng, Timothy H T ^c   Pearson, John ^a   Kazakoff, Stephen ^a   Waddell, Nicola ^a   Hoivik, Erling A ^d,e   Goode, Ellen L ^f   Scott, Rodney J ^g,h,i   Tomlinson, Ian ^c   Dunning, Alison M ^j   Easton, Douglas F ^j   French, Juliet D ^a   Salvesen, Helga B ^d,e   Pollock, Pamela M ^k   Thompson, Deborah J ^j   Spurdle, Amanda B ^a   Edwards, Stacey L ^a   more..

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF BERGEN   (Norway)

^e HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^f MAYO CLINIC   (United States)

^g JOHN HUNTER HOSPITAL   (Australia)

^h UNIVERSITY OF NEWCASTLE   (Australia)

ⁱ UNIVERSITY OF NEWCASTLE   (Australia)

^j UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^k TRANSLATIONAL RESEARCH INSTITUTE   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

SMALL INTERFERING RNA; TRANSCRIPTION FACTOR YY1; AKT1 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BINDING; PROTEIN KINASE B; YY1 PROTEIN, HUMAN;

AKT1 GENE; ALLELE; ARTICLE; BINDING SITE; CANCER RISK; CHROMOSOME 14Q; CHROMOSOME VARIANT; ENDOMETRIUM CANCER; FOLLOW UP; GENE; GENE EXPRESSION; GENE LOCUS; GENOTYPE; HUMAN; INTRACELLULAR SIGNALING; LUCIFERASE ASSAY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; SILENCER ELEMENT; SINGLE NUCLEOTIDE POLYMORPHISM; UTERINE TISSUE; ZBTB42 GENE; CHROMOSOME 14; ENDOMETRIUM TUMOR; FEMALE; GENETIC PREDISPOSITION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; PATHOLOGY; RISK FACTOR; SIGNAL TRANSDUCTION; UTERUS CANCER;

CHROMOSOMES, HUMAN, PAIR 14; ENDOMETRIAL NEOPLASMS; FEMALE; GENETIC LOCI; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASES; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; RISK FACTORS; SIGNAL TRANSDUCTION; UTERINE NEOPLASMS; YY1 TRANSCRIPTION FACTOR;

EID: 84971567624     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2016.04.012     Document Type: Article

References (65)

1. J.S.I. Ferlay, M. Ervik, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, D.M. Parkin, D. Forman, and F. Bray GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 2013 International Agency for Research on Cancer Lyon, France
2. J. Ferlay, I. Soerjomataram, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, D.M. Parkin, D. Forman, and F. Bray Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012 Int. J. Cancer 136 2015 E359 E386
3. A.B. Spurdle, D.J. Thompson, S. Ahmed, K. Ferguson, C.S. Healey, T. O'Mara, L.C. Walker, S.B. Montgomery, E.T. Dermitzakis, P. Fahey, et al. Australian National Endometrial Cancer Study Group National Study of Endometrial Cancer Genetics Group Genome-wide association study identifies a common variant associated with risk of endometrial cancer Nat. Genet. 43 2011 451 454
4. J.N. Painter, T.A. O'Mara, J. Batra, T. Cheng, F.A. Lose, J. Dennis, K. Michailidou, J.P. Tyrer, S. Ahmed, K. Ferguson, et al. National Study of Endometrial Cancer Genetics Group (NSECG) CHIBCHA Consortium Australian National Endometrial Cancer Study Group (ANECS) RENDOCAS Australian Ovarian Cancer Study (AOCS) GENICA Network Fine-mapping of the HNF1B multicancer locus identifies candidate variants that mediate endometrial cancer risk Hum. Mol. Genet. 24 2015 1478 1492
5. D.J. Thompson, T.A. O'Mara, D.M. Glubb, J.N. Painter, T. Cheng, E. Folkerd, D. Doody, J. Dennis, P.M. Webb, M. Gorman, and et al. CYP19A1 fine-mapping and Mendelian randomisation: estradiol is causal for endometrial cancer Endocr. Relat. Cancer 23 2015 77 91
6. T.H. Cheng, D.J. Thompson, T.A. O'Mara, J.N. Painter, D.M. Glubb, S. Flach, A. Lewis, J.D. French, L. Freeman-Mills, D. Church, et al. National Study of Endometrial Cancer Genetics Group (NSECG) Australian National Endometrial Cancer Study Group (ANECS) RENDOCAS CHIBCHA Consortium AOCS Group Five endometrial cancer risk loci identified through genome-wide association analysis Nat. Genet. 2016 10.1038/ng.3562
7. L.C. Cantley The phosphoinositide 3-kinase pathway Science 296 2002 1655 1657
8. H.B. Salvesen, S.L. Carter, M. Mannelqvist, A. Dutt, G. Getz, I.M. Stefansson, M.B. Raeder, M.L. Sos, I.B. Engelsen, J. Trovik, and et al. Integrated genomic profiling of endometrial carcinoma associates aggressive tumors with indicators of PI3 kinase activation Proc. Natl. Acad. Sci. USA 106 2009 4834 4839
9. B.M. Slomovitz, and R.L. Coleman The PI3K/AKT/mTOR pathway as a therapeutic target in endometrial cancer Clin. Cancer Res. 18 2012 5856 5864
10. K. Shoji, K. Oda, S. Nakagawa, S. Hosokawa, G. Nagae, Y. Uehara, K. Sone, Y. Miyamoto, H. Hiraike, O. Hiraike-Wada, and et al. The oncogenic mutation in the pleckstrin homology domain of AKT1 in endometrial carcinomas Br. J. Cancer 101 2009 145 148
11. Y. Cohen, B. Shalmon, J. Korach, I. Barshack, E. Fridman, and G. Rechavi AKT1 pleckstrin homology domain E17K activating mutation in endometrial carcinoma Gynecol. Oncol. 116 2010 88 91
12. J.H. Barrett, J.C. Taylor, C. Bright, M. Harland, A.M. Dunning, L.A. Akslen, P.A. Andresen, M.F. Avril, E. Azizi, G. Bianchi Scarrà, et al. GenoMEL Consortium Fine mapping of genetic susceptibility loci for melanoma reveals a mixture of single variant and multiple variant regions Int. J. Cancer 136 2015 1351 1360
13. L.G. Carvajal-Carmona, T.A. O'Mara, J.N. Painter, F.A. Lose, J. Dennis, K. Michailidou, J.P. Tyrer, S. Ahmed, K. Ferguson, C.S. Healey, et al. National Study of Endometrial Cancer Genetics Group (NSECG) Australian National Endometrial Cancer Study Group (ANECS) RENDOCAS Australian Ovarian Cancer Study (AOCS) GENICA Network Candidate locus analysis of the TERT-CLPTM1L cancer risk region on chromosome 5p15 identifies multiple independent variants associated with endometrial cancer risk Hum. Genet. 134 2015 231 245
14. T.A. O'Mara, D.M. Glubb, J.N. Painter, T. Cheng, J. Dennis, J. Attia, E.G. Holliday, M. McEvoy, R.J. Scott, K. Ashton, et al. Australian National Endometrial Cancer Study Group (ANECS) National Study of Endometrial Cancer Genetics Group (NSECG) RENDOCAS AOCS Group Comprehensive genetic assessment of the ESR1 locus identifies a risk region for endometrial cancer Endocr. Relat. Cancer 22 2015 851 861
15. B.N. Howie, P. Donnelly, and J. Marchini A flexible and accurate genotype imputation method for the next generation of genome-wide association studies PLoS Genet. 5 2009 e1000529
16. J. Marchini, B. Howie, S. Myers, G. McVean, and P. Donnelly A new multipoint method for genome-wide association studies by imputation of genotypes Nat. Genet. 39 2007 906 913
17. C.J. Willer, Y. Li, and G.R. Abecasis METAL: fast and efficient meta-analysis of genomewide association scans Bioinformatics 26 2010 2190 2191
18. R.J. Pruim, R.P. Welch, S. Sanna, T.M. Teslovich, P.S. Chines, T.P. Gliedt, M. Boehnke, G.R. Abecasis, and C.J. Willer LocusZoom: regional visualization of genome-wide association scan results Bioinformatics 26 2010 2336 2337
19. S.L. Edwards, J. Beesley, J.D. French, and A.M. Dunning Beyond GWASs: illuminating the dark road from association to function Am. J. Hum. Genet. 93 2013 779 797
20. M.S. Udler, J. Tyrer, and D.F. Easton Evaluating the power to discriminate between highly correlated SNPs in genetic association studies Genet. Epidemiol. 34 2010 463 468
21. M.J. Machiela, and S.J. Chanock LDlink: a web-based application for exploring population-specific haplotype structure and linking correlated alleles of possible functional variants Bioinformatics 31 2015 3555 3557
22. E. Birney, J.A. Stamatoyannopoulos, A. Dutta, R. Guigó, T.R. Gingeras, E.H. Margulies, Z. Weng, M. Snyder, E.T. Dermitzakis, R.E. Thurman, et al. ENCODE Project Consortium NISC Comparative Sequencing Program Baylor College of Medicine Human Genome Sequencing Center Washington University Genome Sequencing Center Broad Institute Children's Hospital Oakland Research Institute Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project Nature 447 2007 799 816
23. D. Hnisz, B.J. Abraham, T.I. Lee, A. Lau, V. Saint-André, A.A. Sigova, H.A. Hoke, and R.A. Young Super-enhancers in the control of cell identity and disease Cell 155 2013 934 947
24. O. Corradin, A. Saiakhova, B. Akhtar-Zaidi, L. Myeroff, J. Willis, R. Cowper-Sal lari, M. Lupien, S. Markowitz, and P.C. Scacheri Combinatorial effects of multiple enhancer variants in linkage disequilibrium dictate levels of gene expression to confer susceptibility to common traits Genome Res. 24 2014 1 13
25. G.T. Consortium GTEx Consortium The Genotype-Tissue Expression (GTEx) project Nat. Genet. 45 2013 580 585
26. C. Kandoth, N. Schultz, A.D. Cherniack, R. Akbani, Y. Liu, H. Shen, A.G. Robertson, I. Pashtan, R. Shen, C.C. Benz, et al. Cancer Genome Atlas Research Network Integrated genomic characterization of endometrial carcinoma Nature 497 2013 67 73
27. P. Flicek, M.R. Amode, D. Barrell, K. Beal, K. Billis, S. Brent, D. Carvalho-Silva, P. Clapham, G. Coates, S. Fitzgerald, and et al. Ensembl 2014 Nucleic Acids Res. 42 2014 D749 D755
28. A. Dobin, C.A. Davis, F. Schlesinger, J. Drenkow, C. Zaleski, S. Jha, P. Batut, M. Chaisson, and T.R. Gingeras STAR: ultrafast universal RNA-seq aligner Bioinformatics 29 2013 15 21
29. D.S. DeLuca, J.Z. Levin, A. Sivachenko, T. Fennell, M.D. Nazaire, C. Williams, M. Reich, W. Winckler, and G. Getz RNA-SeQC: RNA-seq metrics for quality control and process optimization Bioinformatics 28 2012 1530 1532
30. B. Li, and C.N. Dewey RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome BMC Bioinformatics 12 2011 323
31. Y. Li, C. Willer, S. Sanna, and G. Abecasis Genotype imputation Annu. Rev. Genomics Hum. Genet. 10 2009 387 406
32. Y. Li, C.J. Willer, J. Ding, P. Scheet, and G.R. Abecasis MaCH: using sequence and genotype data to estimate haplotypes and unobserved genotypes Genet. Epidemiol. 34 2010 816 834
33. C. Fuchsberger, G.R. Abecasis, and D.A. Hinds minimac2: faster genotype imputation Bioinformatics 2014
34. B. Howie, C. Fuchsberger, M. Stephens, J. Marchini, and G.R. Abecasis Fast and accurate genotype imputation in genome-wide association studies through pre-phasing Nat. Genet. 44 2012 955 959
35. M. Ghoussaini, S.L. Edwards, K. Michailidou, S. Nord, R. Cowper-Sal Lari, K. Desai, S. Kar, K.M. Hillman, S. Kaufmann, D.M. Glubb, et al. Australian Ovarian Cancer Management Group Australian Ovarian Cancer Management Group Evidence that breast cancer risk at the 2q35 locus is mediated through IGFBP5 regulation Nat. Commun. 4 2014 4999
36. J.D. French, M. Ghoussaini, S.L. Edwards, K.B. Meyer, K. Michailidou, S. Ahmed, S. Khan, M.J. Maranian, M. O'Reilly, K.M. Hillman, et al. GENICA Network kConFab Investigators Functional variants at the 11q13 risk locus for breast cancer regulate cyclin D1 expression through long-range enhancers Am. J. Hum. Genet. 92 2013 489 503
37. L.D. Ward, and M. Kellis HaploReg v4: systematic mining of putative causal variants, cell types, regulators and target genes for human complex traits and disease Nucleic Acids Res. 44 2015 D877 D881
38. N. Grabe AliBaba2: context specific identification of transcription factor binding sites In Silico Biol. (Gedrukt) 2 2002 S1 S15
39. M.P. Hayes, H. Wang, R. Espinal-Witter, W. Douglas, G.J. Solomon, S.J. Baker, and L.H. Ellenson PIK3CA and PTEN mutations in uterine endometrioid carcinoma and complex atypical hyperplasia Clin. Cancer Res. 12 2006 5932 5935
40. N. Ahmadiyeh, M.M. Pomerantz, C. Grisanzio, P. Herman, L. Jia, V. Almendro, H.H. He, M. Brown, X.S. Liu, M. Davis, and et al. 8q24 prostate, breast, and colon cancer risk loci show tissue-specific long-range interaction with MYC Proc. Natl. Acad. Sci. USA 107 2010 9742 9746
41. S. Voisin, M.S. Almén, G.Y. Zheleznyakova, L. Lundberg, S. Zarei, S. Castillo, F.E. Eriksson, E.K. Nilsson, M. Blüher, Y. Böttcher, and et al. Many obesity-associated SNPs strongly associate with DNA methylation changes at proximal promoters and enhancers Genome Med. 7 2015 103
42. C.G. Bell, S. Finer, C.M. Lindgren, G.A. Wilson, V.K. Rakyan, A.E. Teschendorff, P. Akan, E. Stupka, T.A. Down, I. Prokopenko, et al. International Type 2 Diabetes 1q Consortium Integrated genetic and epigenetic analysis identifies haplotype-specific methylation in the FTO type 2 diabetes and obesity susceptibility locus PLoS ONE 5 2010 e14040
43. I.K. Sur, O. Hallikas, A. Vähärautio, J. Yan, M. Turunen, M. Enge, M. Taipale, A. Karhu, L.A. Aaltonen, and J. Taipale Mice lacking a Myc enhancer that includes human SNP rs6983267 are resistant to intestinal tumors Science 338 2012 1360 1363
44. M. Uhlén, L. Fagerberg, B.M. Hallström, C. Lindskog, P. Oksvold, A. Mardinoglu, Å. Sivertsson, C. Kampf, E. Sjöstedt, A. Asplund, and et al. Proteomics. Tissue-based map of the human proteome Science 347 2015 1260419
45. I. Vivanco, and C.L. Sawyers The phosphatidylinositol 3-Kinase AKT pathway in human cancer Nat. Rev. Cancer 2 2002 489 501
46. H.B. Salvesen, I.S. Haldorsen, and J. Trovik Markers for individualised therapy in endometrial carcinoma Lancet Oncol. 13 2012 e353 e361
47. L.W. Cheung, B.T. Hennessy, J. Li, S. Yu, A.P. Myers, B. Djordjevic, Y. Lu, K. Stemke-Hale, M.D. Dyer, F. Zhang, and et al. High frequency of PIK3R1 and PIK3R2 mutations in endometrial cancer elucidates a novel mechanism for regulation of PTEN protein stability Cancer Discov. 1 2011 170 185
48. F. Fabi, and E. Asselin Expression, activation, and role of AKT isoforms in the uterus Reproduction 148 2014 R85 R95
49. G. Castellano, E. Torrisi, G. Ligresti, G. Malaponte, L. Militello, A.E. Russo, J.A. McCubrey, S. Canevari, and M. Libra The involvement of the transcription factor Yin Yang 1 in cancer development and progression Cell Cycle 8 2009 1367 1372
50. Y. Yang, L. Zhou, L. Lu, L. Wang, X. Li, P. Jiang, L.K. Chan, T. Zhang, J. Yu, J. Kwong, and et al. A novel miR-193a-5p-YY1-APC regulatory axis in human endometrioid endometrial adenocarcinoma Oncogene 32 2013 3432 3442
51. K.D. Courtney, R.B. Corcoran, and J.A. Engelman The PI3K pathway as drug target in human cancer J. Clin. Oncol. 28 2010 1075 1083
52. K. Gungorduk, I.E. Ertas, A. Sahbaz, S. Ozvural, Y. Sarica, A. Ozdemir, S. Sayhan, M. Gokcu, B. Yilmaz, M. Sanci, and et al. Immunolocalization of ERK1/2 and p-AKT in normal endometrium, endometrial hyperplasia, and early and advanced stage endometrioid endometrial adenocancer and their prognostic significance in malignant group Eur. J. Obstet. Gynecol. Reprod. Biol. 179 2014 147 152
53. Z. Zhu, W. Yu, X. Fu, M. Sun, Q. Wei, D. Li, H. Chen, J. Xiang, H. Li, Y. Zhang, and et al. Phosphorylated AKT1 is associated with poor prognosis in esophageal squamous cell carcinoma J. Exp. Clin. Cancer Res. 34 2015 95
54. Hyman, D.M.; Smyth, L.; Bedard, P.L.; Oza, A.; Dean, E.; Armstrobg, A.; Lima, J.; Bando, H.; Kabos, P.; Perez-Fidalgo, J.A.; et al. (2015). AZD5363, a catalytic pan-Akt inhibitor, in Akt1 E17K mutation positive advanced solid tumors. Molecular Targets and Cancer Therapeutics Meeting Boston Clinical trial number NCT01226316.
55. Eathiraj, S.; Schwartz, B.; Yu, Y.; Wick, M.J.; Hall, T.; Chai, F.; Sachdev, J.; and Abbadessa, G. (2015). Targeting PI3K pathway dependent endometrial tumors with allosteric AKT inhibitors, ARQ 092 and ARQ 751 Molecular Targets and Cancer Therapeutics Meeting Boston.
56. L. Cadzow, M.H. Lam, H. Wang, D. DeWitt, V. Pucci, J.-R. Mo, E. Lewies-Clark, H. Ferguson, M. Gindy, S. Low, and et al. Accurins improve the pharmacokinetics, pharmacodynamics, tolerability and anti-tumor activity of the AKT inhibitor MK-2206 2015 Molecular Targets and Cancer Therapeutics Meeting Boston
57. G. Rena, E.R. Pearson, and K. Sakamoto Molecular mechanism of action of metformin: old or new insights? Diabetologia 56 2013 1898 1906
58. C. Porta, C. Paglino, and A. Mosca Targeting PI3K/Akt/mTOR Signaling in Cancer Front. Oncol. 4 2014 64
59. X. Wang, M. Zha, X. Zhao, P. Jiang, W. Du, A.Y. Tam, Y. Mei, and M. Wu Siva1 inhibits p53 function by acting as an ARF E3 ubiquitin ligase Nat. Commun. 4 2013 1551
60. S.A. Devaney, S.E. Mate, J.M. Devaney, and E.P. Hoffman Characterization of the ZBTB42 gene in humans and mice Hum. Genet. 129 2011 433 441
61. N. Patel, L.L. Smith, E. Faqeih, J. Mohamed, V.A. Gupta, and F.S. Alkuraya ZBTB42 mutation defines a novel lethal congenital contracture syndrome (LCCS6) Hum. Mol. Genet. 23 2014 6584 6593
62. J.C. Miller, D.C. Blake Jr.; and C.R. Herzog Adenylosuccinate synthetase 1 gene is a novel target of deletion in lung adenocarcinoma Mol. Carcinog. 48 2009 1116 1122
63. M.A. Chesarone, A.G. DuPage, and B.L. Goode Unleashing formins to remodel the actin and microtubule cytoskeletons Nat. Rev. Mol. Cell Biol. 11 2010 62 74
64. M. Barua, E.J. Brown, V.T. Charoonratana, G. Genovese, H. Sun, and M.R. Pollak Mutations in the INF2 gene account for a significant proportion of familial but not sporadic focal and segmental glomerulosclerosis Kidney Int. 83 2013 316 322
65. O. Boyer, F. Nevo, E. Plaisier, B. Funalot, O. Gribouval, G. Benoit, E. Huynh Cong, C. Arrondel, M.J. Tete, R. Montjean, and et al. INF2 mutations in Charcot-Marie-Tooth disease with glomerulopathy N Engl J Med 365 2011 2377 2388