CTCF genetic alterations in endometrial carcinoma are pro-tumorigenic

Oncogene

Volumn 36, Issue 29, 2017, Pages 4100-4110

  Marshal, A D ^a,b   Bailey, C G ^a,b   Champ, K ^a,b   Vellozzi, M ^a,b   O'Young, P ^a,b   Metierre, C ^a,b   Feng, Y ^a,b   Thoeng, A ^a,b   Richards, A M ^c   Schmitz, U ^a,b   Biro, M ^d   Jayasinghe, R ^e,f   Ding, L ^e,f   Anderson, L ^b,c   Mardis, E R ^e,f   Rasko, J E J ^a,b,c  

^a CENTENARY INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; TRANSCRIPTION FACTOR CTCF; CCCTC-BINDING FACTOR; REPRESSOR PROTEIN;

ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CLEAR CELL CARCINOMA; DNA BINDING; DNA EXTRACTION; ENDOMETRIUM CARCINOMA; FEMALE; GAIN OF FUNCTION MUTATION; GENE CONTROL; GENE DELETION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC TRANSFECTION; HAPLOINSUFFICIENCY; HEK293T CELL LINE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LOSS OF FUNCTION MUTATION; MISSENSE MUTATION; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; OVERALL SURVIVAL; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; SHORT TANDEM REPEAT; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; CARCINOGENESIS; ENDOMETRIUM TUMOR; GENE EXPRESSION; GENETICS; PATHOLOGY; TUMOR CELL LINE; TUMOR RECURRENCE;

CARCINOGENESIS; CELL LINE, TUMOR; ENDOMETRIAL NEOPLASMS; FEMALE; GENE EXPRESSION; HUMANS; MUTATION, MISSENSE; NEOPLASM RECURRENCE, LOCAL; REPRESSOR PROTEINS;

EID: 85015622363     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2017.25     Document Type: Article

References (54)

1. Haidopoulos D, Simou M, Akrivos N, Rodolakis A, Vlachos G, Fotiou S et al. Risk factors in women 40 years of age and younger with endometrial carcinoma. Acta Obstet Gynecol Scand 2010; 89: 1326-1330.
2. Ukraintseva SV, Arbeev KG, Yashin AI. Epidemiology of hormone-associated cancers as a reflection of age. Adv Exp Med Biol 2008; 630: 57-71.
3. Kurman RJ, Caracangiu ML, Herrington CS, Young RHE. World Health Organization Classification of Tumours of Female Reproductive Organs., 4th edn, IARC: Lyon, France, 2014, p 128.
4. Llaurado M, Ruiz A, Majem B, Ertekin T, Colas E, Pedrola N et al. Molecular bases of endometrial cancer: New roles for new actors in the diagnosis and the therapy of the disease. Mol Cell Endocrinol 2012; 358: 244-255.
5. Kandoth C, Schultz N, Cherniack AD, Akbani R, Liu Y, Shen H et al. Integrated genomic characterization of endometrial carcinoma. Nature 2013; 497: 67-73.
6. Walker CJ, Miranda MA, O'Hern MJ, McElroy JP, Coombes KR, Bundschuh R et al. Patterns of CTCF and ZFHX3 mutation and associated outcomes in endometrial cancer. J Natl Cancer Inst 2015; 107: 249.
7. Zighelboim I, Mutch DG, Knapp A, Ding L, Xie M, Cohn DE et al. High frequency strand slippage mutations in CTCF in MSI-positive endometrial cancers. Hum Mutat 2014; 35: 63-65.
8. Kandoth C, McLellan MD, Vandin F, Ye K, Niu B, Lu C et al. Mutational landscape and significance across 12 major cancer types. Nature 2013; 502: 333-339.
9. Aulmann S, Blaker H, Penzel R, Rieker RJ, Otto HF, Sinn HP. CTCF gene mutations in invasive ductal breast cancer. Breast Cancer Res Treat 2003; 80: 347-352.
10. Filippova GN, Qi CF, Ulmer JE, Moore JM, Ward MD, Hu YJ et al. Tumor-associated zinc finger mutations in the CTCF transcription factor selectively alters its DNAbinding specificity. Cancer Res 2002; 62: 48-52.
11. Mullighan CG, Zhang J, Kasper LH, Lerach S, Payne-Turner D, Phillips LA et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature 2011; 471: 235-239.
12. Yoshida K, Toki T, Okuno Y, Kanezaki R, Shiraishi Y, Sato-Otsubo A et al. The landscape of somatic mutations in Down syndrome-related myeloid disorders. Nat Genet 2013; 45: 1293-1299.
13. Phillips JE, Corces VG. CTCF: Master weaver of the genome. Cell 2009; 137: 1194-1211.
14. Marshall AD, Bailey CG, Rasko JE. CTCF and BORIS in genome regulation and cancer. Curr Opin Genet Dev 2014; 24: 8-15.
15. Rasko JE, Klenova EM, Leon J, Filippova GN, Loukinov Di, Vatolin S et al. Cell growth inhibition by the multifunctional multivalent zinc-finger factor CTCF. Cancer Res 2001; 61: 6002-6007.
16. Li T, Lu L. Functional role of CCCTC binding factor (CTCF) in stress-induced apoptosis. Exp Cell Res 2007; 313: 3057-3065.
17. Tiffen JC, Bailey CG, Marshall AD, Metierre C, Feng Y, Wang Q et al. The cancertestis antigen BORIS phenocopies the tumor suppressor CTCF in normal and neoplastic cells. Int J Cancer 2013; 133: 1603-1613.
18. Lobanenkov VV, Nicolas RH, Adler VV, Paterson H, Klenova EM, Polotskaja AV et al. A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5'-flanking sequence of the chicken c-myc gene. Oncogene 1990; 5: 1743-1753.
19. Watanabe N, Haruta M, Soejima H, Fukushi D, Yokomori K, Nakadate H et al. Duplication of the paternal IGF2 allele in trisomy 11 and elevated expression levels of IGF2 mRNA in congenital mesoblastic nephroma of the cellular or mixed type. Genes Chromosomes Cancer 2007; 46: 929-935.
20. Soto-Reyes E, Recillas-Targa F. Epigenetic regulation of the human p53 gene promoter by the CTCF transcription factor in transformed cell lines. Oncogene 2010; 29: 2217-2227.
21. Renaud S, Loukinov D, Bosman FT, Lobanenkov V, Benhattar J. CTCF binds the proximal exonic region of hTERT and inhibits its transcription. Nucleic Acids Res 2005; 33: 6850-6860.
22. Hirosue A, Ishihara K, Tokunaga K, Watanabe T, Saitoh N, Nakamoto M et al. Quantitative assessment of higher-order chromatin structure of the INK4/ARF locus in human senescent cells. Aging Cell 2012; 11: 553-556.
23. Lai AY, Fatemi M, Dhasarathy A, Malone C, Sobol SE, Geigerman C et al. DNA methylation prevents CTCF-mediated silencing of the oncogene BCL6 in B cell lymphomas. J Exp Med 2010; 207: 1939-1950.
24. Witcher M, Emerson BM. Epigenetic silencing of the p16(INK4a) tumor suppressor is associated with loss of CTCF binding and a chromatin boundary. Mol Cell 2009; 34: 271-284.
25. Kemp CJ, Moore JM, Moser R, Bernard B, Teater M, Smith LE et al. CTCF haploinsufficiency destabilizes DNA methylation and predisposes to cancer. Cell Rep 2014; 7: 1020-1029.
26. Le Gallo M, O'Hara AJ, Rudd ML, Urick ME, Hansen NF, O'Neil NJ et al. Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes. Nat Genet 2012; 44: 1310-1315.
27. Kuramoto H, Tamura S, Notake Y. Establishment of a cell line of human endometrial adenocarcinoma in vitro. Am J Obstet Gynecol 1972; 114: 1012-1019.
28. Richardson GS, Dickersin GR, Atkins L, MacLaughlin DT, Raam S, Merk LP et al. KLE: A cell line with defective estrogen receptor derived from undifferentiated endometrial cancer. Gynecol Oncol 1984; 17: 213-230.
29. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012; 483: 603-607.
30. Jung H, Lee D, Lee J, Park D, Kim YJ, Park WY et al. Intron retention is a widespread mechanism of tumor-suppressor inactivation. Nat Genet 2015; 47: 1242-1248.
31. Nagy E, Maquat LE. A rule for termination-codon position within intron-containing genes: When nonsense affects RNA abundance. Trends Biochem Sci 1998; 23: 198-199.
32. Marshall AD, van Geldermalsen M, Otte NJ, Anderson LA, Lum T, Vellozzi MA et al. LAT1 is a putative therapeutic target in endometrioid endometrial carcinoma. Int J Cancer 2016; 139: 2529-2539.
33. Eritja N, Llobet D, Domingo M, Santacana M, Yeramian A, Matias-Guiu X et al. A novel three-dimensional culture system of polarized epithelial cells to study endometrial carcinogenesis. Am J Pathol 2010; 176: 2722-2731.
34. Royer C, Lu X. Epithelial cell polarity: A major gatekeeper against cancer? Cell Death Differ 2011; 18: 1470-1477.
35. Wong JJ, Ritchie W, Ebner OA, Selbach M, Wong JW, Huang Y et al. Orchestrated intron retention regulates normal granulocyte differentiation. Cell 2013; 154: 583-595.
36. Nakahashi H, Kwon KR, Resch W, Vian L, Dose M, Stavreva D et al. A Genomewide Map of CTCF Multivalency Redefines the CTCF Code. Cell Rep 2013; 3: 1678-1689.
37. Filippova GN, Lindblom A, Meincke LJ, Klenova EM, Neiman PE, Collins SJ et al. A widely expressed transcription factor with multiple DNA sequence specificity, CTCF, is localized at chromosome segment 16q22.1 within one of the smallest regions of overlap for common deletions in breast and prostate cancers. Genes Chromosomes Cancer 1998; 22: 26-36.
38. Rakha EA, Armour JA, Pinder SE, Paish CE, Ellis IO. High-resolution analysis of 16q22.1 in breast carcinoma using DNA amplifiable probes (multiplex amplifiable probe hybridization technique) and immunohistochemistry. Int J Cancer 2005; 114: 720-729.
39. Reardon SN, King ML, MacLean JA 2nd, Mann JL, DeMayo FJ, Lydon JP et al. CDH1 is essential for endometrial differentiation, gland development, and adult function in the mouse uterus. Biol Reprod 2012; 86: 141.
40. Carico E, Atlante M, Giarnieri E, Raffa S, Bucci B, Giovagnoli MR et al. E-cadherin and alpha-catenin expression in normal, hyperplastic and neoplastic endometrium. Anticancer Res 2010; 30: 4993-4997.
41. Gonzalez-Rodilla I, Aller L, Llorca J, Munoz AB, Verna V, Estevez J et al. The E-Cadherin expression vs. tumor cell proliferation paradox in endometrial cancer. Anticancer Res 2013; 33: 5091-5095.
42. Moore JM, Rabaia NA, Smith LE, Fagerlie S, Gurley K, Loukinov D et al. Loss of maternal CTCF is associated with peri-implantation lethality of Ctcf null embryos. PLoS One 2012; 7: E34915.
43. Kumar MS, Pester RE, Chen CY, Lane K, Chin C, Lu J et al. Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev 2009; 23: 2700-2704.
44. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144: 646-674.
45. Jiménez-Ayala M, J-AP B. Cytology of the normal endometrium-cycling and postmenopausal. Endometrial Adenocarcinoma: Prevention and Early Diagnosis. Karger: Basel, Switzerland, 2008; pp 32-39.
46. Allison KH, Reed SD, Voigt LF, Jordan CD, Newton KM, Garcia RL. Diagnosing endometrial hyperplasia: Why is it so difficult to agree? Am J Surg Pathol 2008; 32: 691-698.
47. Lacey Jr JV, Chia VM. Endometrial hyperplasia and the risk of progression to carcinoma. Maturitas 2009; 63: 39-44.
48. Moreno-Bueno G, Portillo F, Cano A. Transcriptional regulation of cell polarity in EMT and cancer. Oncogene 2008; 27: 6958-6969.
49. Brar AK, Kessler CA, Meyer AJ, Cedars MI, Jikihara H. Retinoic acid suppresses invitro decidualization of human endometrial stromal cells. Mol Hum Reprod 1996; 2: 185-193.
50. Cheng YH, Utsunomiya H, Pavone ME, Yin P, Bulun SE. Retinoic acid inhibits endometrial cancer cell growth via multiple genomic mechanisms. J Mol Endocrinol 2011; 46: 139-153.
51. Li R, Saito T, Tanaka R, Satohisa S, Adachi K, Horie M et al. Hypermethylation in promoter region of retinoic acid receptor-beta gene and immunohistochemical findings on retinoic acid receptors in carcinogenesis of endometrium. Cancer Lett 2005; 219: 33-40.
52. Seewaldt VL, Caldwell LE, Johnson BS, Swisshelm K, Collins SJ, Tsai S. Inhibition of retinoic acid receptor function in normal human mammary epithelial cells results in increased cellular proliferation and inhibits the formation of a polarized epithelium in vitro. Exp Cell Res 1997; 236: 16-28.
53. Herold MJ, van den Brandt J, Seibler J, Reichardt HM. Inducible and reversible gene silencing by stable integration of an shRNA-encoding lentivirus in transgenic rats. Proc Natl Acad Sci USA 2008; 105: 18507-18512.
54. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: A tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 2009; 10: 48.