Oncogenic Wnt/β-catenin signalling pathways in the cancer-resistant epididymis have implications for cancer research

Molecular Human Reproduction

Volumn 19, Issue 2, 2013, Pages 57-71

  Wang, K ^a   Li, N ^a   Yeung, C H ^a   Li, J Y ^a   Wang, H Y ^a   Cooper, T G ^a  

^a YANTAI YUHUANGDING HOSPITAL   (China)

Author keywords

Cancer; Human epididymis; MiRNA; Tumour suppressors; Wnt catenin signalling

Indexed keywords

ANDROGEN RECEPTOR; BETA CATENIN; CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; KRUPPEL LIKE FACTOR 4; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; MICRORNA; T CELL FACTOR PROTEIN; UVOMORULIN; WNT PROTEIN;

ANGIOGENESIS; CANCER INCIDENCE; CANCER STEM CELL; CARCINOGENESIS; CELL COMPARTMENTALIZATION; CELL NUCLEUS; COLORECTAL CARCINOMA; EPIDIDYMIS; EPIDIDYMIS CANCER; EPIDIDYMIS DISEASE; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE MUTATION; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; TELOMERE; TESTIS CANCER; UNINDEXED SEQUENCE; WNT SIGNALING PATHWAY;

EPIDIDYMIS; HUMANS; MALE; NEOPLASMS; WNT SIGNALING PATHWAY;

ANIMALIA;

EID: 84872701985     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gas051     Document Type: Review

References (137)

1. Anton R, Chatterjee SS, Simundza J, Cowin P, Dasgupta R. A systematic screen for micro-RNAs regulating the canonical Wnt pathway. PLoS One 2011;6:e26257.
2. Aprelikova O, Palla J, Hibler B, Yu X, Greer YE, Yi M, Stephens R, Maxwell GL, Jazaeri A, Risinger JI et al. Silencing of miR-148a in cancer-associated fibroblasts results in WNT10B-mediated stimulation of tumor cell motility. Oncogene 2012. Epub ahead of print. doi: 10.1038/onc.2012.351.
3. Belleannee C, Calvo E, Thimon V, Cyr DG, Legare C, Garneau L, Sullivan R. Role of MicroRNAs in controlling gene expression in different segments of the human epididymis. PLoS One 2012;7:e34996.
4. Berx G, Cleton-Jansen AM, Nollet F, de Leeuw WJ, van de Vijver M, Cornelisse C, van Roy F. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J 1995; 14:6105-6107.
5. Bisson I, Prowse DM. WNT signaling regulates self-renewal and differentiation of prostate cancer cells with stem cell characteristics. Cell Res 2009;19:683-697.
6. Brattain MG, Fine WD, Khaled FM, Thompson J, Brattain DE. Heterogeneity of malignant cells from a human colonic carcinoma. Cancer Res 1981;41:1751-1756.
7. Cai C, Zhu X. The Wnt/beta-catenin pathway regulates self-renewal of cancer stem-like cells in human gastric cancer. Mol Med Report 2012; 5:1191-1196.
8. Cantilena S, Pastorino F, Pezzolo A, Chayka O, Pistoia V, Ponzoni M, Sala A. Frizzled receptor 6 marks rare, highly tumourigenic stem-like cells in mouse and human neuroblastomas. Oncotarget 2011;2:976-983.
9. Cao L, Zhou Y, Zhai B, Liao J, Xu W, Zhang R, Li J, Zhang Y, Chen L, Qian H et al. Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines. BMC Gastroenterol 2011; 11:71.
10. Cao M, Seike M, Soeno C, Mizutani H, Kitamura K, Minegishi Y, Noro R, Yoshimura A, Cai L, Gemma A. MiR-23a regulates TGF-beta-induced epithelial-mesenchymal transition by targeting E-cadherin in lung cancer cells. Int J Oncol 2012;41:869-875.
11. Carroll TJ, Park JS, Hayashi S, Majumdar A, McMahon AP. Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev Cell 2005;9:283-292.
12. Cespedes MV, Larriba MJ, Pavon MA, Alamo P, Casanova I, Parreno M, Feliu A, Sancho FJ, Munoz A, Mangues R. Site-dependent E-cadherin cleavage and nuclear translocation in a metastatic colorectal cancer model. Am J Pathol 2010;177:2067-2079.
13. Ceteci F, Ceteci S, Karreman C, Kramer BW, Asan E, Gotz R, Rapp UR. Disruption of tumor cell adhesion promotes angiogenic switch and progression to micrometastasis in RAF-driven murine lung cancer. Cancer Cell 2007;12:145-159.
14. Chesire DR, Ewing CM, Gage WR, Isaacs WB. In vitro evidence for complex modes of nuclear beta-catenin signaling during prostate growth and tumorigenesis. Oncogene 2002;21:2679-2694.
15. Chetty R, Serra S. Nuclear E-cadherin immunoexpression: from biology to potential applications in diagnostic pathology. Adv Anat Pathol 2008; 15:234-240.
16. Chim CS, ChanWW, Pang A, Kwong YL. Preferential methylation of Wnt inhibitory factor-1 in acute promyelocytic leukemia: an independent poor prognostic factor. Leukemia 2006;20:907-909.
17. Clevers H. The cancer stem cell: premises, promises and challenges. Nat Med 2011;17:313-319.
18. Cornwall GA. New insights into epididymal biology and function. Hum Reprod Update 2009;15:213-227.
19. Cortes-Sempere M, Ibanez de Caceres I. \MicroRNAs as novel epigenetic biomarkers for human cancer. Clin Transl Oncol 2011;13:357-362.
20. Coulon A, Flahaut M, Muhlethaler-Mottet A, Meier R, Liberman J, Balmas-Bourloud K, Nardou K, Yan P, Tercier S, Joseph JM et al. Functional sphere profiling reveals the complexity of neuroblastoma tumor-initiating cell model. Neoplasia 2011;13:991-1004.
21. Cyr DG, Hermo L, Blaschuk OW, Robaire B. Distribution and regulation of epithelial cadherin messenger ribonucleic acid and immunocytochemical localization of epithelial cadherin in the rat epididymis. Endocrinology 1992;130:353-363.
22. DeBellefeuille S, Hermo L, Gregory M, Dufresne J, Cyr DG. Catenins in the rat epididymis: their expression and regulation in adulthood and during postnatal development. Endocrinology 2003;144:5040-5049.
23. Dellinger TH, Planutis K, Jandial DD, Eskander RN, Martinez ME, Zi X, Monk BJ, Holcombe RF. Expression of the Wnt antagonist Dickkopf-3 is associated with prognostic clinicopathologic characteristics and impairs proliferation and invasion in endometrial cancer. Gynecol Oncol 2012;126:259-267.
24. Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B, van Beijnum JR, Griffioen AW, Vink J, Krimpenfort P et al. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 2006;10:437-449.
25. Deshpande SN, Vijayakumar G, Rao AJ. Oestrogenic regulation and differential expression of WNT4 in the bonnet monkey and rodent epididymis. Reprod Biomed Online 2009;18:555-561.
26. Dube E, Chan PT, Hermo L, Cyr DG. Gene expression profiling and its relevance to the blood-epididymal barrier in the human epididymis. Biol Reprod 2007;76:1034-1044.
27. Dube E, Dufresne J, Chan PT, Hermo L, Cyr DG. Assessing the role of claudins in maintaining the integrity of epididymal tight junctions using novel human epididymal cell lines. Biol Reprod 2010a; 82:1119-1128.
28. Dube E, Hermo L, Chan PT, Cyr DG. Alterations in the human blood-epididymis barrier in obstructive azoospermia and the development of novel epididymal cell lines from infertile men. Biol Reprod 2010b;83:584-596.
29. Eisenberg DT. An evolutionary review of human telomere biology: the thrifty telomere hypothesis and notes on potential adaptive paternal effects. Am J Hum Biol 2011;23:149-167.
30. Elston MS, Gill AJ, Conaglen JV, Clarkson A, Cook RJ, Little NS, Robinson BG, Clifton-Bligh RJ, McDonald KL. Nuclear accumulation of e-cadherin correlates with loss of cytoplasmic membrane staining and invasion in pituitary adenomas. J Clin Endocrinol Metab 2009; 94:1432-1436.
31. Ergun S, Kilik N, Ziegeler G, Hansen A, Nollau P, Gotze J, Wurmbach JH, Horst A, Weil J, Fernando M et al. CEA-related cell adhesion molecule 1: a potent angiogenic factor and a major effector of vascular endothelial growth factor. Mol Cell 2000;5:311-320.
32. Evans PM, Chen X, Zhang W, Liu C. KLF4 interacts with beta-catenin/ TCF4 and blocks p300/CBP recruitment by beta-catenin. Mol Cell Biol 2010;30:372-381.
33. Filipovich A, Gehrke I, Poll-Wolbeck SJ, Kreuzer KA. Physiological inhibitors of Wnt signaling. Eur J Haematol 2011;86:453-465.
34. Fujii M, Katase N, Lefeuvre M, Gunduz M, Buery RR, Tamamura R, Tsujigiwa H, Nagatsuka H. Dickkopf (Dkk)-3 and beta-catenin expressions increased in the transition from normal oral mucosal to oral squamous cell carcinoma. J Mol Histol 2011;42:499-504.
35. Ganem JP, Jhaveri FM, Marroum MC. Primary adenocarcinoma of the epididymis: case report and review of the literature. Urology 1998; 52:904-908.
36. Godmann M, Kosan C, Behr R. Kruppel-like factor 4 is widely expressed in the mouse male and female reproductive tract and responds as an immediate early gene to activation of the protein kinase A in TM4 Sertoli cells. Reproduction 2010;139:771-782.
37. Goss KH, Kahn M. Targeting the Wnt Pathway in Cancer. New York: Springer, 2011, 1-248.
38. Hao HX, Xie Y, Zhang Y, Charlat O, Oster E, Avello M, Lei H, Mickanin C, Liu D, Ruffner H et al. ZNRF3 promotes Wnt receptor turnover in an R-spondin-sensitive manner. Nature 2012;485:195-200.
39. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, Oshima M, Taketo MM. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 1999;18:5931-5942.
40. Hashimi ST, Fulcher JA, Chang MH, Gov L, Wang S, Lee B. MicroRNA profiling identifies miR-34a and miR-21 and their target genes JAG1 and WNT1 in the coordinate regulation of dendritic cell differentiation. Blood 2009;114:404-414.
41. Hassan MQ, Maeda Y, Taipaleenmaki H, Zhang W, Jafferji M, Gordon JA, Li Z, Croce CM, Van Wijnen AJ, Stein JL et al. miR-218 Directs a Wnt signaling circuit to promote differentiation of osteoblasts and osteomimicry of metastatic cancer cells. J Biol Chem 2012. Epub ahead of print. doi: 10.1074/jbc.M112.377515.
42. Hirata H, Hinoda Y, Ueno K, Majid S, Saini S, Dahiya R. Role of secreted frizzled-related protein 3 in human renal cell carcinoma. Cancer Res 2010;70:1896-1905.
43. Hirata H, Hinoda Y, Ueno K, Nakajima K, Ishii N, Dahiya R. MicroRNA-1826 directly targets beta-catenin (CTNNB1) and MEK1 (MAP2K1) in VHL inactivated renal cancer. Carcinogenesis 2011a;33:501-508.
44. Hirata H, Hinoda Y, Ueno K, Shahryari V, Tabatabai ZL, Dahiya R. MicroRNA-1826 targets VEGFC, beta-catenin (CTNNB1) and MEK1 (MAP2K1) in human bladder cancer. Carcinogenesis 2011b;33:41-48.
45. Hoffmeyer K, Raggioli A, Rudloff S, Anton R, Hierholzer A, Del Valle I, Hein K, Vogt R, Kemler R. Wnt/beta-catenin signaling regulates telomerase in stem cells and cancer cells. Science 2012;336:1549-1554.
46. Howard S, Deroo T, Fujita Y, Itasaki N. A positive role of cadherin in Wnt/beta-catenin signalling during epithelial-mesenchymal transition. PLoS One 2011;6:e23899.
47. Huber O, Bierkamp C, Kemler R. Cadherins and catenins in development. Curr Opin Cell Biol 1996;8:685-691.
48. Itasaki N, Jones CM, Mercurio S, Rowe A, Domingos PM, Smith JC, Krumlauf R. Wise, a context-dependent activator and inhibitor of Wnt signalling. Development 2003;130:4295-4305.
49. Jelinsky SA, Turner TT, Bang HJ, Finger JN, Solarz MK, Wilson E, Brown EL, Kopf GS, Johnston DS. The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides. Biol Reprod 2007;76:561-570.
50. Jin L, Li Y, Chen CJ, Sherman MA, Le K, Shively JE. Direct interaction of tumor suppressor CEACAM1 with beta catenin: identification of key residues in the long cytoplasmic domain. Exp Biol Med (Maywood) 2008;233:849-859.
51. Johnson JM, Castle J, Garrett-Engele P, Kan Z, Loerch PM, Armour CD, Santos R, Schadt EE, Stoughton R, Shoemaker DD. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 2003;302:2141-2144.
52. Johnston DS, Jelinsky SA, Bang HJ, DiCandeloro P, Wilson E, Kopf GS, Turner TT. The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol Reprod 2005;73:404-413.
53. Kammerer R, Riesenberg R, Weiler C, Lohrmann J, Schleypen J, Zimmermann W. The tumour suppressor gene CEACAM1 is completely but reversibly downregulated in renal cell carcinoma. J Pathol 2004;204:258-267.
54. Kanwar SS, Yu Y, Nautiyal J, Patel BB, Majumdar AP. The Wnt/ beta-catenin pathway regulates growth and maintenance of colonospheres. Mol Cancer 2010;9:212.
55. Katase N, Gunduz M, Beder L, Gunduz E, Lefeuvre M, Hatipoglu OF, Borkosky SS, Tamamura R, Tominaga S, Yamanaka N et al. Deletion at Dickkopf (dkk)-3 locus (11p15.2) is related with lower lymph node metastasis and better prognosis in head and neck squamous cell carcinomas. Oncol Res 2008;17:273-282.
56. Kawano Y, Kypta R. Secreted antagonists of the Wnt signalling pathway. J Cell Sci 2003;116:2627-2634.
57. Kennell JA, Gerin I, MacDougald OA, Cadigan KM. The microRNA miR-8 is a conserved negative regulator of Wnt signaling. Proc Natl Acad Sci USA 2008;105:15417-15422.
58. Khaidakov M, Mitra S, Mehta JL. Adherence junction proteins in angiogenesis: modulation by aspirin and salicylic acid. J Cardiovasc Med (Hagerstown) 2012;13:187-193.
59. Kilic N, Tilki D, Ergun B, Seitz M, Stief CG, Reich O, Ergun S. Epithelial versus endothelial CEACAM1 expression and angiogenesis in epididymal adenomatoid tumor. Anticancer Res 2010;30:2651-2657.
60. Kim KI, Cho HJ, Hahn JY, Kim TY, Park KW, Koo BK, Shin CS, Kim CH, Oh BH, Lee MM et al. Beta-catenin overexpression augments angiogenesis and skeletal muscle regeneration through dual mechanism of vascular endothelial growth factor-mediated endothelial cell proliferation and progenitor cell mobilization. Arterioscler Thromb Vasc Biol 2006;26:91-98.
61. Kim NH, Kim HS, Kim NG, Lee I, Choi HS, Li XY, Kang SE, Cha SY, Ryu JK, Na JM et al. p53 and MicroRNA-34 are suppressors of canonical Wnt signaling. Sci Signal 2011a;4:ra71.
62. Kim NH, Kim HS, Li XY, Lee I, Choi HS, Kang SE, Cha SY, Ryu JK, Yoon D, Fearon ER et al. A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition. J Cell Biol 2011b; 195:417-433.
63. Kokontis JM, Liao S. Molecular action of androgen in the normal and neoplastic prostate. Vitam Horm 1999;55:219-307.
64. Koo BK, Spit M, Jordens I, Low TY, Stange DE, van de Wetering M, van Es JH, Mohammed S, Heck AJ, Maurice MM et al. Tumour suppressor RNF43 is a stem-cell E3 ligase that induces endocytosis of Wnt receptors. Nature 2012;488:665-669.
65. Kristensen DM, Nielsen JE, Kalisz M, Dalgaard MD, Audouze K, Larsen ME, Jacobsen GK, Horn T, Brunak S, Skakkebaek NE et al. OCT4 and downstream factors are expressed in human somatic urogenital epithelia and in culture of epididymal spheres. Mol Hum Reprod 2010;16:835-845.
66. Krutzfeldt J, Rosch N, Hausser J, Manoharan M, Zavolan M, Stoffel M. MicroRNA-194 is a target of transcription factor 1 (Tcf1, Hnf1alpha) in adult liver and controls expression of frizzled-6. Hepatology 2012; 55:98-107.
67. Lee I, Ajay SS, Yook JI, Kim HS, Hong SH, Kim NH, Dhanasekaran SM, Chinnaiyan AM, Athey BD. New class of microRNA targets containing simultaneous 5'-UTR and 3'-UTR interaction sites. Genome Res 2009;19:1175-1183.
68. Li J, Zhou BP. Activation of beta-catenin and Akt pathways by Twist are critical for the maintenance of EMT associated cancer stem cell-like characters. BMC Cancer 2011. Epub ahead of print. doi: 10.1186/ 1471-2407-11-49.
69. Li J, Liu F, Liu X, Liu J, Zhu P, Wan F, Jin S, Wang W, Li N, Wang H. Mapping of the human testicular proteome and its relationship with that of the epididymis and spermatozoa. Mol Cell Proteomics 2011. Epub ahead of print. doi: 10.1074/mcp.M110.004630.
70. Li Y, Wang HY, Wan FC, Liu FJ, Liu J, Zhang N, Jin SH, Li JY. Deep sequencing analysis of small non-coding RNAs reveals the diversity of microRNAs and piRNAs in the human epididymis. Gene 2012; 497:330-335.
71. Liu H, Fergusson MM, Castilho RM, Liu J, Cao L, Chen J, Malide D, Rovira II, Schimel D, Kuo CJ et al. Augmented Wnt signaling in a mammalian model of accelerated aging. Science 2007;317:803-806.
72. Liu Y, Yan W, Zhang W, Chen L, You G, Bao Z, Wang Y, Wang H, Kang C, Jiang T. MiR-218 reverses high invasiveness of glioblastoma cells by targeting the oncogenic transcription factor LEF1. Oncol Rep 2012;28:1013-1021.
73. Ma L, Young J, Prabhala H, Pan E, Mestdagh P, Muth D, Teruya-Feldstein J, Reinhardt F, Onder TT, Valastyan S et al. miR-9, a MYC/ MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 2010;12:247-256.
74. Ma W, Xie S, Ni M, Huang X, Hu S, Liu Q, Liu A, Zhang J, Zhang Y. MicroRNA-29a inhibited epididymal epithelial cell proliferation by targeting nuclear autoantigenic sperm protein (NASP). J Biol Chem 2012;287:10189-10199.
75. Maiese K, Li F, Chong ZZ, Shang YC. The Wnt signaling pathway: aging gracefully as a protectionist? Pharmacol Ther 2008;118:58-81.
76. Marín-Briggiler CI, Veiga MF, Matos ML, Echeverria MF, Furlong LI, Vazquez-Levin MH. Expression of epithelial cadherin in the human male reproductive tract and gametes and evidence of its participation in fertilization. Mol Hum Reprod 2008;14:561-571.
77. Miyake A, Takahashi Y, Miwa H, Shimada A, Konishi M, Itoh N. Neucrin is a novel neural-specific secreted antagonist to canonical Wnt signaling. Biochem Biophys Res Commun 2009;390:1051-1055.
78. Mulholland DJ, Cheng H, Reid K, Rennie PS, Nelson CC. The androgen receptor can promote beta-catenin nuclear translocation independently of adenomatous polyposis coli. J Biol Chem 2002;277:17933-17943.
79. Murashima A, Miyagawa S, Ogino Y, Nishida-Fukuda H, Araki K, Matsumoto T, Kaneko T, Yoshinaga K, Yamamura K, Kurita T et al. Essential roles of androgen signaling in Wolffian duct stabilization and epididymal cell differentiation. Endocrinology 2011;152:1640-1651.
80. Nagel R, Le Sage C, Diosdado B, van derWaal M, Oude Vrielink JA, Bolijn A, Meijer GA, Agami R. Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res 2008;68:5795-5802.
81. Nittka S, Bohm C, Zentgraf H, Neumaier M. The CEACAM1-mediated apoptosis pathway is activated by CEA and triggers dual cleavage of CEACAM1. Oncogene 2008;27:3721-3728.
82. Nose A, Tsuji K, Takeichi M. Localization of specificity determining sites in cadherin cell adhesion molecules. Cell 1990;61:147-155.
83. Nusse R, Varmus HE. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 1982;31:99-109.
84. Nusse R, Brown A, Papkoff J, Scambler P, Shackleford G, McMahon A, Moon R, Varmus H. A new nomenclature for int-1 and related genes: the Wnt gene family. Cell 1991;64:231.
85. Oberwalder M, Zitt M, Wontner C, Fiegl H, Goebel G, Kohle O, Muhlmann G, Ofner D, Margreiter R, Muller HM. SFRP2 methylation in fecal DNA-a marker for colorectal polyps. Int J Colorectal Dis 2008; 23:15-19.
86. Oda H, Takeichi M. Evolution: structural and functional diversity of cadherin at the adherens junction. J Cell Biol 2011;193:1137-1146.
87. Ohishi Y, Kurihara S, Takeuchi T, Aman M, Kaku T, Kobayashi H, Wake N, Oda Y. E-cadherin nuclear staining is useful for the diagnosis of ovarian adult granulosa cell tumor. Hum Pathol 2012;43:808-817.
88. Ozguven BY, Karacetin D, Kabukcuoglu F, Taskin T, Yener S. Immunohistochemical study of E-cadherin and beta-catenin expression in colorectal carcinomas. Pol J Pathol 2011;62:19-24.
89. Paris F, Weinbauer GF, Blum V, Nieschlag E. The effect of androgens and antiandrogens on the immunohistochemical localization of the androgen receptor in accessory reproductive organs of male rats. J Steroid Biochem Mol Biol 1994;48:129-137.
90. Pastrana E, Silva-Vargas V, Doetsch F. Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell StemCell 2011;8:486-498.
91. Pinheiro H, Carvalho J, Oliveira P, Ferreira D, Pinto MT, Osorio H, Licastro D, Bordeira-Carrico R, Jordan P, Lazarevic D et al. Transcription initiation arising from E-cadherin/CDH1 intron2: a novel protein isoform that increases gastric cancer cell invasion and angiogenesis. Hum Mol Genet 2012;21:4253-4269.
92. Rizk CC, Scholes J, Chen SK, Ward J, Romas NA. Epididymal metastasis from prostatic adenocarcinoma mimicking adenomatoid tumor. Urology 1990;36:526-530.
93. Robaire B, Hamzeh M. Androgen action in the epididymis. J Androl 2011; 32:592-599.
94. Ruizeveld de Winter JA, Trapman J, Vermey M, Mulder E, Zegers ND, van der Kwast TH. Androgen receptor expression in human tissues: an immunohistochemical study. J Histochem Cytochem 1991;39:927-936.
95. Salahshor S, Naidoo R, Serra S, ShihW, Tsao MS, Chetty R, Woodgett JR. Frequent accumulation of nuclear E-cadherin and alterations in the Wnt signaling pathway in esophageal squamous cell carcinomas. Mod Pathol 2008;21:271-281.
96. Sathi GA, Inoue M, Harada H, Rodriguez AP, Tamamura R, Tsujigiwa H, Borkosky SS, Gunduz M, Nagatsuka H. Secreted frizzled related protein (sFRP)-2 inhibits bone formation and promotes cell proliferation in ameloblastoma. Oral Oncol 2009;45:856-860.
97. Saydam O, Shen Y, Wurdinger T, Senol O, Boke E, James MF, Tannous BA, Stemmer-Rachamimov AO, Yi M, Stephens RM et al. Downregulated microRNA-200a in meningiomas promotes tumor growth by reducing E-cadherin and activating the Wnt/beta-catenin signaling pathway. Mol Cell Biol 2009;29:5923-5940.
98. Schweizer L, Rizzo CA, Spires TE, Platero JS, Wu Q, Lin TA, Gottardis MM, Attar RM. The androgen receptor can signal through Wnt/beta-Catenin in prostate cancer cells as an adaptation mechanism to castration levels of androgens. BMC Cell Biol 2008;9:4.
99. Sekine S, Shibata T, Sakamoto M, Hirohashi S. Target disruption of the mutant beta-catenin gene in colon cancer cell line HCT116 preservation of its malignant phenotype. Oncogene 2002;21:5906-5911.
100. Sellak H, Wu S, Lincoln TM. KLF4 and SOX9 transcription factors antagonize beta-catenin and inhibit TCF-activity in cancer cells. Biochim Biophys Acta 2012;1823:1666-1675.
101. Semenov M, Tamai K, He X. SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J Biol Chem 2005;280:26770-26775.
102. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. Generation of a functional mammary gland from a single stem cell. Nature 2006;439:84-88.
103. Shen Q, Fan J, Yang XR, Tan Y, Zhao W, Xu Y, Wang N, Niu Y, Wu Z, Zhou J et al. Serum DKK1 as a protein biomarker for the diagnosis of hepatocellular carcinoma: a large-scale, multicentre study. Lancet Oncol 2012;13:817-826.
104. Shimomura Y, Agalliu D, Vonica A, Luria V, Wajid M, Baumer A, Belli S, Petukhova L, Schinzel A, Brivanlou AH et al. APCDD1 is a novel Wnt inhibitor mutated in hereditary hypotrichosis simplex. Nature 2010; 464:1043-1047.
105. Siemens H, Jackstadt R, Hunten S, Kaller M, Menssen A, Gotz U, Hermeking H. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 2011; 10:4256-4271.
106. Silver SJ, Hagen JW, Okamura K, Perrimon N, Lai EC. Functional screening identifies miR-315 as a potent activator of Wingless signaling. Proc Natl Acad Sci USA 2007;104:18151-18156.
107. Staal FJ, Luis TC, Tiemessen MM. WNT signalling in the immune system: WNT is spreading its wings. Nat Rev Immunol 2008;8:581-593.
108. Strillacci A, Valerii MC, Sansone P, Caggiano C, Sgromo A, Vittori L, Fiorentino M, Poggioli G, Rizzello F, Campieri M et al. Loss of miR-101 expression promotes Wnt/beta-Catenin signalling pathway activation and malignancy in colon cancer cells. J Pathol 2012;Epub ahead of print. doi: 10.1074/jbc.M112.377515.
109. Su J, Zhang A, Shi Z, Ma F, Pu P, Wang T, Zhang J, Kang C, Zhang Q. MicroRNA-200a suppresses the Wnt/beta-catenin signaling pathway by interacting with beta-catenin. Int J Oncol 2011;40:1162-1170.
110. Sun JY, Huang Y, Li JP, Zhang X, Wang L, Meng YL, Yan B, Bian YQ, Zhao J, Wang WZ et al. MicroRNA-320a suppresses human colon cancer cell proliferation by directly targeting beta-catenin. Biochem Biophys Res Commun 2012;420:787-792.
111. Terry S, Yang X, Chen MW, Vacherot F, Buttyan R. Multifaceted interaction between the androgen and Wnt signaling pathways and the implication for prostate cancer. J Cell Biochem 2006;99:402-410.
112. Thatcher EJ, Paydar I, Anderson KK, Patton JG. Regulation of zebrafish fin regeneration by microRNAs. Proc Natl Acad Sci USA 2008; 105:18384-18389.
113. Thudi NK, Martin CK, Murahari S, Shu ST, Lanigan LG, Werbeck JL, Keller ET, McCauley LK, Pinzone JJ, Rosol TJ. Dickkopf-1 (DKK-1) stimulated prostate cancer growth and metastasis and inhibited bone formation in osteoblastic bone metastases. Prostate 2011;71:615-625.
114. Tilki D, Kilic N, Herbst H, Reich O, Seitz M, Lauke H, Stief CG, Ergun S. High level of endostatin in epididymal epithelium: protection against primary malignancies in this organ? Histochem Cell Biol 2008; 130:527-535.
115. Turner TT. De Graaf's thread: the human epididymis. J Androl 2008; 29:237-250.
116. Ueno K, Hirata H, Majid S, Tabatabai ZL, Hinoda Y, Dahiya R. IGFBP-4 activates the Wnt/beta-catenin signaling pathway and induces M-CAM expression in human renal cell carcinoma. Int J Cancer 2011a; 129:2360-2369.
117. Ueno K, Hirata H, Majid S, Yamamura S, Shahryari V, Tabatabai ZL, Hinoda Y, Dahiya R. Tumor suppressor microRNA-493 decreases cell motility and migration ability in human bladder cancer cells by down-regulating RhoC and FZD4. Mol Cancer Ther 2011b;11:244-253.
118. Ungefroren H, Ivell R, Ergun S. Region-specific expression of the androgen receptor in the human epididymis. Mol Hum Reprod 1997;3:933-940.
119. VanWynsberghe PM, Chan SP, Slack FJ, Pasquinelli AE. Analysis of microRNA expression and function. Methods Cell Biol 2011;106:219-252.
120. von Marschall Z, Fisher LW. Secreted frizzled-related protein-2 (sFRP2) augments canonical Wnt3a-induced signaling. Biochem Biophys Res Commun 2010;400:299-304.
121. Wang J, Ruan K. miR-200c affects the mRNA expression of E-cadherin by regulating the mRNA level of TCF8 during post-natal epididymal development in juvenile rats. Acta Biochim Biophys Sin (Shanghai) 2010a;42:628-634.
122. Wang J, Ruan K. miR-335 is involved in the rat epididymal development by targeting the mRNA of RASA1. Biochem Biophys Res Commun 2010b; 402:222-227.
123. Wang K, Diao LH, Gong Y, Liu X, Li Y. NEMO differentially regulates TCR and TNF-alpha induced NF-kappaB pathways and has an inhibitory role in TCR-induced NF-kappaB activation. Cell Signal 2012;24:1556-1564.
124. Whitaker HC, Girling J, Warren AY, Leung H, Mills IG, Neal DE. Alterations in beta-catenin expression and localization in prostate cancer. Prostate 2008;68:1196-1205.
125. Wu X, Zhao B, Li W, Chen Y, Liang R, Li L, Jin Y, Ruan K. MiR-200a is involved in rat epididymal development by targeting beta-catenin mRNA. Acta Biochim Biophys Sin (Shanghai) 2012;44:233-240.
126. Xia H, Ooi LL, Hui KM. MiR-214 targets beta-catenin pathway to suppress invasion, stem-like traits and recurrence of human hepatocellular carcinoma. PLoS One 2012;7:e44206.
127. Xu J, Zhu X, Wu L, Yang R, Yang Z, Wang Q, Wu F. MicroRNA-122 suppresses cell proliferation and induces cell apoptosis in hepatocellular carcinoma by directly targeting Wnt/beta-catenin pathway. Liver Int 2012a;32:752-760.
128. Xu WH, Liu ZB, Yang C, Qin W, Shao ZM. Expression of dickkopf-1 and Beta-catenin related to the prognosis of breast cancer patients with triple negative phenotype. PLoS One 2012b;7:e37624.
129. Yao H, Ashihara E, Maekawa T. Targeting the Wnt/beta-catenin signaling pathway in human cancers. Expert Opin Ther Targets 2011; 15:873-887.
130. Yeung CH, Wang K, Cooper TG. Why are epididymal tumours so rare? Asian J Androl 2012;14:465-475.
131. Yoshino M, Suzuki M, Tian L, Moriya Y, Hoshino H, Okamoto T, Yoshida S, Shibuya K, Yoshino I. Promoter hypermethylation of the p16 and Wif-1 genes as an independent prognostic marker in stage IA non-small cell lung cancers. Int J Oncol 2009;35:1201-1209.
132. Yu T, Chen X, Zhang W, Colon D, Shi J, Napier D, Rychahou P, Lu W, Lee EY, Weiss HL et al. Regulation of the potential marker for intestinal cells, bmi1, by beta-Catenin and the zinc finger protein KLF4: implications for colon cancer. J Biol Chem 2012; 287:3760-3768.
133. Zenzmaier C, Heitz M, Klocker H, Buck M, Gardiner RA, Berger P. Elevated levels of Dickkopf-related protein 3 in seminal plasma of prostate cancer patients. J Transl Med 2011;9:193.
134. Zhang JS, Liu Q, Li YM, Hall SH, French FS, Zhang YL. Genome-wide profiling of segmental-regulated transcriptomes in human epididymis using oligo microarray. Mol Cell Endocrinol 2006;250:169-177.
135. Zhang N, Wei P, Gong A, Chiu WT, Lee HT, Colman H, Huang H, Xue J, Liu M, Wang Y et al. FoxM1 promotes beta-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell 2011;20:427-442.
136. Zhou AD, Diao LT, Xu H, Xiao ZD, Li JH, Zhou H, Qu LH. Beta-catenin/ LEF1 transactivates the microRNA-371-373 cluster that modulates the Wnt/beta-catenin-signaling pathway. Oncogene 2012;31: 2968-2978.
137. Zhu W, Shiojima I, Ito Y, Li Z, Ikeda H, Yoshida M, Naito AT, Nishi J, Ueno H, Umezawa A et al. IGFBP-4 is an inhibitor of canonical Wnt signalling required for cardiogenesis. Nature 2008;454:345-349.