Wnt inhibitory factor 1 (Wif1) is regulated by androgens and enhances androgen-dependent prostate development

Endocrinology

Volumn 153, Issue 12, 2012, Pages 6091-6103

  Keil, Kimberly P ^a   Mehta, Vatsal ^a   Branam, Amanda M ^b   Abler, Lisa L ^a   Buresh Stiemke, Rita A ^b   Joshi, Pinak S ^a   Schmitz, Christopher T ^a   Marker, Paul C ^b   Vezina, Chad M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; AXIN; AXIN 2; BETA CATENIN; LYMPHOID ENHANCER FACTOR 1; MEMBRANE PROTEIN; MEMBRANE PROTEIN SFRP3; MESSENGER RNA; SECRETED FRIZZLED RELATED PROTEIN 2; STEROID 5ALPHA REDUCTASE 2; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ELONGATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM BASAL CELL; FEMALE; GENE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MESENCHYME; MORPHOGENESIS; MOUSE; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; PROSTATE; PROTEIN EXPRESSION; REGULATORY MECHANISM; RNA PROBE; SEX DIFFERENCE; UROGENITAL SINUS; WIF1 GENE;

3-OXO-5-ALPHA-STEROID 4-DEHYDROGENASE; ANDROGENS; ANIMALS; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE EXPRESSION REGULATION; IN SITU HYBRIDIZATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; PROSTATE; RNA, MESSENGER; SEX FACTORS; TESTOSTERONE; TIME FACTORS; URETHRA;

EID: 84870168885     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1564     Document Type: Article

References (54)

1. Sugimura Y, Cunha GR, Donjacour AA 1986 Morphogenesis of ductal networks in the mouse prostate. Biol Reprod 34:961-971
2. Hayward SW, Cunha GR 2000 The prostate: development and physiology. Radiol Clin North Am 38:1-14
3. Cunha GR, Chung LW, Shannon JM, Reese BA 1980 Stromal-epithelial interactions in sex differentiation. Biol Reprod 22:19-42
4. Cunha GR 1973 The role of androgens in the epithelio-mesenchymal interactions involved in prostatic morphogenesis in embryonic mice. Anat Rec 175:87-96
5. Lasnitzki I, Mizuno T 1980 Prostatic induction: interaction of epithelium and mesenchyme from normal wild-type mice and androgen-insensitive mice with testicular feminization. J Endocrinol 85:423-428
6. Memarzadeh S, Xin L, Mulholland DJ, Mansukhani A, Wu H, Teitell MA, Witte ON 2007 Enhanced paracrine fgf10 expression promotes formation of multifocal prostate adenocarcinoma and an increase in epithelial androgen receptor. Cancer Cell 12:572-585
7. Cantile M, Kisslinger A, Cindolo L, Schiavo G, D'Antò V, Franco R, Altieri V, Gallo A, Villacci A, Tramontano D, Cillo C 2005 cAMP induced modifications of HOX D gene expression in prostate cells allow the identification of a chromosomal area involved in vivo with neuroendocrine differentiation of human advanced prostate cancers. J Cell Physiol 205:202-210
8. Sheng T, Li C, Zhang X, Chi S, He N, Chen K, McCormick F, Gatalica Z, Xie J 2004 Activation of the hedgehog pathway in advanced prostate cancer. Mol Cancer 3:29
9. Feeley BT, Gamradt SC, Hsu WK, Liu N, Krenek L, Robbins P, Huard J, Lieberman JR 2005 Influence of BMPs on the formation of osteoblastic lesions in metastatic prostate cancer. J Bone Miner Res 20:2189-2199
10. Pienta KJ, Nguyen NM, Lehr JE 1993 Treatment of prostate cancer in the rat with the synthetic retinoid fenretinide. Cancer Res 53:224-226
11. Lai KP, Yamashita S, Vitkus S, Shyr CR, Yeh S, Chang C 2012 Suppressed prostate epithelial development with impaired branching morphogenesis in mice lacking stromal fibromuscular androgen receptor. Mol Endocrinol 26:52-66
12. Niu Y, Altuwaijri S, Lai KP, Wu CT, Ricke WA, Messing EM, Yao J, Yeh S, Chang C 2008 Androgen receptor is a tumor suppressor and proliferator in prostate cancer. Proc Natl Acad Sci USA 105:12182-12187
13. Yamamoto H, Oue N, Sato A, Hasegawa Y, Yamamoto H, Matsubara A, Yasui W, Kikuchi A 2010 Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase. Oncogene 29:2036-2046
14. Pritchard CC, Nelson PS 2008 Gene expression profiling in the developing prostate. Differentiation 76:624-640
15. Zhang TJ, Hoffman BG, Ruiz de Algara T, Helgason CD 2006 Sage reveals expression of wnt signaling pathway members during mouse prostate development. Gene Expr Patterns 6:310-324
16. Parker MG, Mainwaring WI 1977 Effects of androgens on the complexity of poly(a) RNA from rat prostate. Cell 12:401-407
17. Parker MG, White R, Williams JG 1980 Cloning and characterization of androgen-dependent mRNA from rat ventral prostate. J Biol Chem 255:6996-7001
18. Thomsen MK, Butler CM, Shen MM, Swain A 2008 Sox9 is required for prostate development. Dev Biol 316:302-311
19. Mehta V, Abler LL, Keil KP, Schmitz CT, Joshi PS, Vezina CM 2011 Atlas of wnt and r-spondin gene expression in the developing male mouse lower urogenital tract. Dev Dyn 240:2548-2560
20. Joesting MS, Perrin S, Elenbaas B, Fawell SE, Rubin JS, Franco OE, Hayward SW, Cunha GR, Marker PC 2005 Identification of sfrp1 as a candidate mediator of stromal-to-epithelial signaling in prostate cancer. Cancer Res 65:10423-10430
21. Wang BE, Wang XD, Ernst JA, Polakis P, Gao WQ 2008 Regulation of epithelial branching morphogenesis and cancer cell growth of the prostate by wnt signaling. PLoS One 3:e2186
22. Kansara M, Tsang M, Kodjabachian L, Sims NA, Trivett MK, Ehrich M, Dobrovic A, Slavin J, Choong PF, Simmons PJ, Dawid IB, Thomas DM 2009 Wnt inhibitory factor 1 is epigenetically silenced in human osteosarcoma, and targeted disruption accelerates osteosarcomagenesis in mice. J Clin Invest 119:837-851
23. Abler LL, Mehta V, Keil KP, Joshi PS, Flucus CL, Hardin HA, Schmitz CT, Vezina CM 2011 A high throughput in situ hybridization method to characterize mrna expression patterns in the fetal mouse lower urogenital tract. J Vis Exp 54:2912
24. Keil KP, Mehta V, Abler LL, Joshi PS, Schmitz CT, Vezina CM 2012 Visualization and quantification of mouse prostate development by in situ hybridization. Differentiation 84:232-239
25. Vezina CM, Allgeier SH, Fritz WA, Moore RW, Strerath M, Bushman W, Peterson RE 2008 Retinoic acid induces prostatic bud formation. Dev Dyn 237:1321-1333
26. Abler LL, Keil KP, Mehta V, Joshi PS, Schmitz CT, Vezina CM 2011 A high-resolution molecular atlas of the fetal mouse lower urogenital tract. Dev Dyn 240:2364-2377
27. Livak KJ, Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2[-ΔΔC(T)] method. Methods 25:402-408
28. Witte F, Dokas J, Neuendorf F, Mundlos S, Stricker S 2009 Comprehensive expression analysis of all Wnt genes and their major secreted antagonists during mouse limb development and cartilage differentiation. Gene Expr Patterns 9:215-223
29. Vezina CM, Allgeier SH, Moore RW, Lin TM, Bemis JC, Hardin HA, Gasiewicz TA, Peterson RE 2008 Dioxin causes ventral prostate agenesis by disrupting dorsoventral patterning in developing mouse prostate. Toxicol Sci 106:488-496
30. Lin TM, Rasmussen NT, Moore RW, Albrecht RM, Peterson RE 2003 Region-specific inhibition of prostatic epithelial bud formation in the urogenital sinus of c57bl/6 mice exposed in utero to 2,3,7,8-tetrachlorodibenzo- p-dioxin. Toxicol Sci 76:171-181
31. Matsui D, Sakari M, Sato T, Murayama A, Takada I, Kim M, Takeyama K, Kato S 2002 Transcriptional regulation of the mouse steroid 5α-reductase type II gene by progesterone in brain. Nucleic Acids Res 30:1387-1393
32. Bhatia-Gaur R, Donjacour AA, Sciavolino PJ, Kim M, Desai N, Young P, Norton CR, Gridley T, Cardiff RD, Cunha GR, Abate-Shen C, Shen MM 1999 Roles for nkx3.1 in prostate development and cancer. Genes Dev 13:966-977
33. Takeda H, Lasnitzki I, Mizuno T 1987 Change of mosaic pattern by androgens during prostatic bud formation in XTfm/X+ heterozygous female mice. J Endocrinol 114:131-137
34. Allgeier SH, Lin TM, Moore RW, Vezina CM, Abler LL, Peterson RE 2010 Androgenic regulation of ventral epithelial bud number and pattern in mouse urogenital sinus. Dev Dyn 239:373-385
35. Hsieh JC, Kodjabachian L, Rebbert ML, Rattner A, Smallwood PM, Samos CH, Nusse R, Dawid IB, Nathans J 1999 A new secreted protein that binds to wnt proteins and inhibits their activities. Nature 398:431-436
36. Buermans HP, van Wijk B, Hulsker MA, Smit NC, den Dunnen JT, van Ommen GB, Moorman AF, van den Hoff MJ, 't Hoen PA 2010 Comprehensive gene-expression survey identifies wif1 as a modulator of cardiomyocyte differentiation. PLoS One 5:e15504
37. Mathieu YD 2006 Identification of novel genes involved in the commitment of endodermal cells to the thymic epithelial cell fate. Dissertation, University of Basel (http://edoc.unibas.ch/diss/DissB-7888)
38. Surmann-Schmitt C, Widmann N, Dietz U, Saeger B, Eitzinger N, Nakamura Y, Rattel M, Latham R, Hartmann C, von der Mark H, Schett G, von der Mark K, Stock M 2009 Wif-1 is expressed at cartilage-mesenchyme interfaces and impedes wnt3a-mediated inhibition of chondrogenesis. J Cell Sci 122:3627-3637
39. Berman DM, Tian H, Russell DW 1995 Expression and regulation of steroid 5α-reductase in the urogenital tract of the fetal rat. Mol Endocrinol 9:1561-1570
40. Cunha GR 2008 Mesenchymal-epithelial interactions: past, present, and future. Differentiation 76:578-586
41. Cunha GR, Donjacour AA, Cooke PS, Mee S, Bigsby RM, Higgins SJ, Sugimura Y 1987 The endocrinology and developmental biology of the prostate. Endocr Rev 8:338-362
42. Reguart N, He B, Xu Z, You L, Lee AY, Mazieres J, Mikami I, Batra S, Rosell R, McCormick F, Jablons DM 2004 Cloning and characterization of the promoter of human wnt inhibitory factor-1. Biochem Biophys Res Commun 323:229-234
43. Zirn B, Samans B, Wittmann S, Pietsch T, Leuschner I, Graf N, Gessler M 2006 Target genes of the wnt/β-catenin pathway in Wilms tumors. Genes Chromosomes Cancer 45:565-574
44. Martinez G, Wijesinghe M, Turner K, Abud HE, Taketo MM, Noda T, Robinson ML, de Iongh RU 2009 Conditional mutations of β-catenin and APC reveal roles for canonical Wnt signaling in lens differentiation. Invest Ophthalmol Vis Sci 50:4794-4806
45. Simons BW, Hurley PJ, Huang Z, Ross AE, Miller R, Marchionni L, Berman DM, Schaeffer EM 2012 Wnt signaling through betacatenin is required for prostate lineage specification. Dev Biol 371: 246-255
46. Schmitz C, Mehta V, Joshi P, Abler L, Keil K, Vezina C Requirement for β-catenin in prostatic bud formation. Proc Society for Basic Urologic Research Fall Symposium, Las Vegas, NV, November 11, 2011, p 163 (Abstract 66)
47. Yee DS, Tang Y, Li X, Liu Z, Guo Y, Ghaffar S, McQueen P, Atreya D, Xie J, Simoneau AR, Hoang BH, Zi X 2010 The Wnt inhibitory factor 1 restoration in prostate cancer cells was associated with reduced tumor growth, decreased capacity of cell migration and invasion and a reversal of epithelial to mesenchymal transition. Mol Cancer 9:162
48. Costa VL, Henrique R, Ribeiro FR, Carvalho JR, Oliveira J, Lobo F, Teixeira MR, Jerónimo C 2010 Epigenetic regulation of wnt signaling pathway in urological cancer. Epigenetics 5:343-351
49. Ohigashi T, Mizuno R, Nakashima J, Marumo K, Murai M 2005 Inhibition of Wnt signaling downregulates AKT activity and induces chemosensitivity in PTEN-mutated prostate cancer cells. Prostate 62:61-68
50. Wissmann C, Wild PJ, Kaiser S, Roepcke S, Stoehr R, Woenckhaus M, Kristiansen G, Hsieh JC, Hofstaedter F, Hartmann A, Knuechel R, Rosenthal A, Pilarsky C 2003 Wif1, a component of the wnt pathway, is down-regulated in prostate, breast, lung, and bladder cancer. J Pathol 201:204-212
51. Li X, Wang Y, Sharif-Afshar AR, Uwamariya C, Yi A, Ishii K, Hayward SW, Matusik RJ, Bhowmick NA 2009 Urothelial transdifferentiation to prostate epithelia is mediated by paracrine TGF-β signaling. Differentiation 77:95-102
52. Glise B, Miller CA, Crozatier M, Halbisen MA, Wise S, Olson DJ, Vincent A, Blair SS 2005 Shifted, the drosophila ortholog of Wnt inhibitory factor-1, controls the distribution and movement of hedgehog. Dev Cell 8:255-266
53. Avanesov A, Honeyager SM, Malicki J, Blair SS 2012 The role of glypicans in Wnt inhibitory factor-1 activity and the structural basis of Wif1's effects on Wnt and hedgehog signaling. PLoS Genet 8:e1002503
54. Surmann-Schmitt C, Sasaki T, Hattori T, Eitzinger N, Schett G, von der Mark K, Stock M 2012 The Wnt antagonist Wif-1 interacts with CTGF and inhibits CTGF activity. J Cell Physiol 227:2207-2216