Expression of the Wnt antagonist Dickkopf-3 is associated with prognostic clinicopathologic characteristics and impairs proliferation and invasion in endometrial cancer

Gynecologic Oncology

Volumn 126, Issue 2, 2012, Pages 259-267

  Dellinger, Thanh H ^a   Planutis, Kestutis ^b   Jandial, Danielle D ^a   Eskander, Ramez N ^a   Martinez, Micaela E ^a   Zi, Xiaolin ^c   Monk, Bradley J ^d   Holcombe, Randall F ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Canonical Wnt pathway; Dickkopf 3; Endometrial cancer; REIC Dkk 3; Tumor suppressor; Wnt antagonist

Indexed keywords

BETA CATENIN; DICKKOPF 3 PROTEIN; MESSENGER RNA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ADULT; AGED; ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER INVASION; CANCER STAGING; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; ENDOMETRIUM CANCER; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PELVIS LYMPH NODE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR NECROSIS; TUMOR XENOGRAFT;

ANIMALS; CELL CYCLE; CELL GROWTH PROCESSES; DOWN-REGULATION; ENDOMETRIAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; PROGNOSIS; SIGNAL TRANSDUCTION; TRANSFECTION; TRANSPLANTATION, HETEROLOGOUS; WNT PROTEINS;

EID: 84862866541     PISSN: 00908258     EISSN: 10956859     Source Type: Journal    
DOI: 10.1016/j.ygyno.2012.04.026     Document Type: Article

References (63)

1. Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 2011;61(4):212-36.
2. Bokhman JV. Two pathogenetic types of endometrial carcinoma. Gynecol Oncol 1983;15(1):10-7. (Pubitemid 13194678)
3. Obel JC, Friberg G, Fleming GF. Chemotherapy in endometrial cancer. Clin Adv Hematol Oncol 2006;4(6):459-68. (Pubitemid 44018491)
4. Dellinger TH, Monk BJ. Systemic therapy for recurrent endometrial cancer: a review of North American trials. Expert Rev Anticancer Ther 2009;9(7):905-16.
5. Aghajanian C, Sill MW, Darcy KM, et al. Phase II trial of bevacizumab in recurrent or persistent endometrial cancer: a Gynecologic Oncology Group study. J Clin Oncol 2011;29(16):2259-65.
6. Oza AM, Elit L, Tsao MS, et al. Phase II study of temsirolimus in women with recurrent or metastatic endometrial cancer: a trial of the NCIC Clinical Trials Group. J Clin Oncol 2011;29(24):3278-85.
7. Creasman WT, Boronow RC, Morrow CP, DiSaia PJ, Blessing J. Adenocarcinoma of the endometrium: its metastatic lymph node potential. A preliminary report. Gynecol Oncol 1976;4(3):239-43.
8. Vogelstein B, Fearon ER, Hamilton SR, et al. Genetic alterations during colorectal-tumor development. N Engl J Med 1988;319(9):525-32.
9. Giles RH, van Es JH, Clevers H. Caught up in a Wnt storm: Wnt signaling in cancer. Biochim Biophys Acta 2003;1653(1):1-24. (Pubitemid 36627817)
10. Gatcliffe TA, Monk BJ, Planutis K, Holcombe RF. Wnt signaling in ovarian tumorigenesis. Int J Gynecol Cancer 2008;18(5):954-62.
11. Hsieh SY, Hsieh PS, Chiu CT, Chen WY. Dickkopf-3/REIC functions as a suppressor gene of tumor growth. Oncogene 2004;23(57):9183-9.
12. Tsuji T, Miyazaki M, Sakaguchi M, Inoue Y, Namba M. A REIC gene shows downregulation in human immortalized cells and human tumor-derived cell lines. Biochem Biophys Res Commun 2000;268(1):20-4. (Pubitemid 30116603)
13. Sakaguchi M, Kataoka K, Abarzua F, et al. Overexpression of REIC/Dkk-3 in normal fibroblasts suppresses tumor growth via induction of interleukin-7. J Biol Chem 2009;284(21):14236-44.
14. Veeck J, Niederacher D, An H, et al. Aberrant methylation of the Wnt antagonist SFRP1 in breast cancer is associated with unfavourable prognosis. Oncogene 2006;25(24):3479-88. (Pubitemid 43877051)
15. Yao X, Jiang H, Zhang C, et al. Dickkopf-1 autoantibody is a novel serological biomarker for non-small cell lung cancer. Biomarkers 2010;15(2):128-34.
16. Saegusa M, Hashimura M, Yoshida T, Okayasu I. beta-Catenin mutations and aberrant nuclear expression during endometrial tumorigenesis. Br J Cancer 2001;84(2):209-17. (Pubitemid 32113448)
17. Saegusa M, Okayasu I. Frequent nuclear beta-catenin accumulation and associated mutations in endometrioid-type endometrial and ovarian carcinomas with squamous differentiation. J Pathol 2001;194(1):59-67.
18. Mirabelli-Primdahl L, Gryfe R, Kim H, et al. Beta-catenin mutations are specific for colorectal carcinomas with microsatellite instability but occur in endometrial carcinomas irrespective of mutator pathway. Cancer Res 1999;59(14):3346-51. (Pubitemid 29334489)
19. Fukuchi T, Sakamoto M, Tsuda H, Maruyama K, Nozawa S, Hirohashi S. Beta-catenin mutation in carcinoma of the uterine endometrium. Cancer Res 1998;58(16):3526-8. (Pubitemid 28376543)
20. Machin P, Catasus L, Pons C, Munoz J, Matias-Guiu X, Prat J. CTNNB1 mutations and beta-catenin expression in endometrial carcinomas. Hum Pathol 2002;33(2):206-12. (Pubitemid 34298736)
21. Nei H, Saito T, Yamasaki H, Mizumoto H, Ito E, Kudo R. Nuclear localization of beta-catenin in normal and carcinogenic endometrium. Mol Carcinog 1999;25(3):207-18. (Pubitemid 29319286)
22. Ikeda T, Yoshinaga K, Semba S, Kondo E, Ohmori H, Horii A. Mutational analysis of the CTNNB1 (beta-catenin) gene in human endometrial cancer: frequent mutations at codon 34 that cause nuclear accumulation. Oncol Rep 2000;7(2):323-6.
23. Schlosshauer PW, Pirog EC, Levine RL, Ellenson LH. Mutational analysis of the CTNNB1 and APC genes in uterine endometrioid carcinoma. Mod Pathol 2000;13(10):1066-71.
24. Scholten AN, Creutzberg CL, van den Broek LJ, Noordijk EM, Smit VT. Nuclear beta-catenin is a molecular feature of type I endometrial carcinoma. J Pathol 2003;201(3):460-5. (Pubitemid 37408267)
25. Moreno-Bueno G, Hardisson D, Sanchez C, et al. Abnormalities of the APC/beta-catenin pathway in endometrial cancer. Oncogene 2002;21(52):7981-90. (Pubitemid 35430609)
26. Ashihara K, Saito T, Mizumoto H, Nishimura M, Tanaka R, Kudo R. Mutation of beta-catenin gene in endometrial cancer but not in associated hyperplasia. Med Electron Microsc 2002;35(1):9-15. (Pubitemid 34601463)
27. Aguilera O, Fraga MF, Ballestar E, et al. Epigenetic inactivation of the Wnt antagonist DICKKOPF-1 (DKK-1) gene in human colorectal cancer. Oncogene 2006;25(29):4116-21. (Pubitemid 44024874)
28. Tanimoto R, Abarzua F, Sakaguchi M, et al. REIC/Dkk-3 as a potential gene therapeutic agent against human testicular cancer. Int J Mol Med 2007;19(3):363-8.
29. Voorzanger-Rousselot N, Goehrig D, Journe F, et al. Increased Dickkopf-1 expression in breast cancer bone metastases. Br J Cancer 2007;97(7):964-70. (Pubitemid 47519305)
30. Veeck J, Bektas N, Hartmann A, et al. Wnt signalling in human breast cancer: expression of the putative Wnt inhibitor Dickkopf-3 (DKK3) is frequently suppressed by promoter hypermethylation in mammary tumours. Breast Cancer Res 2008;10(5):R82.
31. Yue W, Sun Q, Dacic S, et al. Downregulation of Dkk3 activates beta-catenin/TCF-4 signaling in lung cancer. Carcinogenesis 2008;29(1):84-92. (Pubitemid 351201745)
32. Jiang T, Wang S, Huang L, Zhang S. Clinical significance of serum DKK-1 in patients with gynecological cancer. Int J Gynecol Cancer 2009;19(7):1177-81.
33. Fong D, Hermann M, Untergasser G, et al. Dkk-3 expression in the tumor endothelium: a novel prognostic marker of pancreatic adenocarcinomas. Cancer Sci 2009;100(8):1414-20.
34. Lee EJ, Jo M, Rho SB, et al. Dkk3, downregulated in cervical cancer, functions as a negative regulator of beta-catenin. Int J Cancer 2009;124(2):287-97.
35. Yi N, Liao QP, Li T, Xiong Y. Novel expression profiles and invasiveness-related biology function of DKK1 in endometrial carcinoma. Oncol Rep 2009;21(6):1421-7.
36. Kawasaki K, Watanabe M, Sakaguchi M, et al. REIC/Dkk-3 overexpression downregulates P-glycoprotein in multidrug-resistant MCF7/ADR cells and induces apoptosis in breast cancer. Cancer Gene Ther 2009;16(1):65-72.
37. Hoang BH, Kubo T, Healey JH, et al. Dickkopf 3 inhibits invasion and motility of Saos-2 osteosarcoma cells by modulating the Wnt-beta-catenin pathway. Cancer Res 2004;64(8):2734-9. (Pubitemid 38500609)
38. Barrantes Idel B, Montero-Pedrazuela A, Guadano-Ferraz A, et al. Generation and characterization of dickkopf3 mutant mice. Mol Cell Biol 2006;26(6):2317-26. (Pubitemid 43346931)
39. Veeck J, Dahl E. Targeting the Wnt pathway in cancer: The emerging role of Dickkopf-3. Biochim Biophys Acta 2012;1825(1):18-28.
40. Nozaki I, Tsuji T, Iijima O, et al. Reduced expression of REIC/Dkk-3 gene in nonsmall cell lung cancer. Int J Oncol 2001;19(1):117-21.
41. Abarzua F, Sakaguchi M, Takaishi M, et al. Adenovirus-mediated overexpression of REIC/Dkk-3 selectively induces apoptosis in human prostate cancer cells through activation of c-Jun-NH2-kinase. Cancer Res 2005;65(21):9617-22. (Pubitemid 41541434)
42. Yu J, Tao Q, Cheng YY, et al. Promoter methylation of the Wnt/beta-catenin signaling antagonist Dkk-3 is associated with poor survival in gastric cancer. Cancer 2009;115(1):49-60.
43. Ding Z, Qian YB, Zhu LX, Xiong QR. Promoter methylation and mRNA expression of DKK-3 and WIF-1 in hepatocellular carcinoma. World J Gastroenterol 2009;15(21):2595-601.
44. Yang B, Du Z, Gao YT, et al. Methylation of Dickkopf-3 as a prognostic factor in cirrhosis-related hepatocellular carcinoma.World J Gastroenterol 2010;16(6):755-63.
45. Lodygin D, Epanchintsev A, Menssen A, Diebold J, Hermeking H. Functional epigenomics identifies genes frequently silenced in prostate cancer. Cancer Res 2005;65(10):4218-27. (Pubitemid 40775660)
46. Fujikane T, Nishikawa N, Toyota M, et al. Genomic screening for genes upregulated by demethylation revealed novel targets of epigenetic silencing in breast cancer. Breast Cancer Res Treat 2010;122(3):699-710.
47. Kobayashi K,OuchidaM, Tsuji T, et al. Reduced expression of the REIC/Dkk-3 gene by promoter-hypermethylation in human tumor cells. Gene 2002;282(1-2):151-8.
48. Jiang T, Huang L, Wang S, Zhang S. Clinical significance of serum Dkk-3 in patients with gynecological cancer. J Obstet Gynaecol Res 2010;36(4):769-73.
49. Dellinger TH, Planutis K, Tewari KS, Holcombe RF. Role of canonical Wnt signaling in endometrial carcinogenesis. Expert Rev Anticancer Ther 2012;12(1):51-62.
50. Krikun G, Mor G, Alvero A, et al. A novel immortalized human endometrial stromal cell line with normal progestational response. Endocrinology 2004;145(5):2291-6. (Pubitemid 38535058)
51. Mo B, Vendrov AE, Palomino WA, DuPont BR, Apparao KB, Lessey BA. ECC-1 cells: a well-differentiated steroid-responsive endometrial cell line with characteristics of luminal epithelium. Biol Reprod 2006;75(3):387-94. (Pubitemid 44268073)
52. Fujita K, Janz S. Attenuation of WNT signaling by DKK-1 and -2 regulates BMP2- induced osteoblast differentiation and expression of OPG, RANKL and M-CSF. Mol Cancer 2007;6:71.
53. Kawakami K, Hirata H, Yamamura S, et al. Functional significance of Wnt inhibitory factor-1 gene in kidney cancer. Cancer Res 2009;69(22):8603-10.
54. Kurose K, Sakaguchi M, Nasu Y, et al. Decreased expression of REIC/Dkk-3 in human renal clear cell carcinoma. J Urol 2004;171(3):1314-8. (Pubitemid 38327602)
55. Creasman WT, Morrow CP, Bundy BN, Homesley HD, Graham JE, Heller PB. Surgical pathologic spread patterns of endometrial cancer. A Gynecologic Oncology Group study. Cancer 1987;60(8 Suppl.):2035-41. (Pubitemid 17145924)
56. Keys HM, Roberts JA, Brunetto VL, et al. A phase III trial of surgerywith orwithout adjunctive external pelvic radiation therapy in intermediate risk endometrial adenocarcinoma: a Gynecologic Oncology Group study. Gynecol Oncol 2004;92(3):744-51. (Pubitemid 38251372)
57. Nishida M. The Ishikawa cells from birth to the present. Hum Cell 2002;15(3):104-17.
58. Carmon KS, Loose DS. Secreted frizzled-related protein 4 regulates two Wnt7a signaling pathways and inhibits proliferation in endometrial cancer cells. Mol Cancer Res 2008;6(6):1017-28.
59. Zi X, Guo Y, Simoneau AR, et al. Expression of Frzb/secreted Frizzled-related protein 3, a secreted Wnt antagonist, in human androgen-independent prostate cancer PC-3 cells suppresses tumor growth and cellular invasiveness. Cancer Res 2005;65(21):9762-70. (Pubitemid 41541453)
60. Guo Y, Zi X, Koontz Z, et al. Blocking Wnt/LRP5 signaling by a soluble receptor modulates the epithelial to mesenchymal transition and suppresses met and metalloproteinases in osteosarcoma Saos-2 cells. J Orthop Res 2007;25(7):964-71. (Pubitemid 47046444)
61. Tsuji T, Nozaki I, Miyazaki M, et al. Antiproliferative activity of REIC/Dkk-3 and its significant down-regulation in non-small-cell lung carcinomas. Biochem Biophys Res Commun 2001;289(1):257-63. (Pubitemid 33108824)
62. Edamura K, Nasu Y, Takaishi M, et al. Adenovirus-mediated REIC/Dkk-3 gene transfer inhibits tumor growth and metastasis in an orthotopic prostate cancer model. Cancer Gene Ther 2007;14(9):765-72. (Pubitemid 47262756)
63. Chen J, Watanabe M, Huang P, et al. REIC/Dkk-3 stable transfection reduces the malignant phenotype of mouse prostate cancer RM9 cells. Int J Mol Med 2009;24(6):789-94.