β-Catenin Is Required for Prostate Development and Cooperates with Pten Loss to Drive Invasive Carcinoma

PLoS Genetics

Volumn 9, Issue 1, 2013, Pages

  Francis, Jeffrey C ^a   Thomsen, Martin K ^a,c   Taketo, Makoto M ^b   Swain, Amanda ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b KYOTO UNIVERSITY   (Japan)

^c Centro Nacional de Investigaciones Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INVASION; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; FEMALE; GENE DELETION; GENE EXPRESSION; GENE FREQUENCY; MALE; MOUSE; NKX3.1 GENE; NONHUMAN; ONCOGENE; ONCOGENE C MYC; PATHOGENESIS; PHENOTYPE; PROSTATE CANCER; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; PTEN GENE;

ANIMALS; BETA CATENIN; CARCINOMA; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; NEOPLASM INVASIVENESS; ORCHIECTOMY; ORGAN CULTURE TECHNIQUES; PROSTATE; PROSTATIC NEOPLASMS; PTEN PHOSPHOHYDROLASE;

EID: 84873486287     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003180     Document Type: Article

References (67)

1. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, et al. (2010) Integrative genomic profiling of human prostate cancer. Cancer Cell 18: 11-22.
2. Schaeffer EM, Marchionni L, Huang Z, Simons B, Blackman A, et al. (2008) Androgen-induced programs for prostate epithelial growth and invasion arise in embryogenesis and are reactivated in cancer. Oncogene 27: 7180-7191.
3. Ewing CM, Ray AM, Lange EM, Zuhlke KA, Robbins CM, et al. (2012) Germline mutations in HOXB13 and prostate-cancer risk. N Engl J Med 366: 141-149.
4. Thomsen MK, Ambroisine L, Wynn S, Cheah KS, Foster CS, et al. (2010) SOX9 elevation in the prostate promotes proliferation and cooperates with PTEN loss to drive tumor formation. Cancer Res 70: 979-987.
5. Bhatia-Gaur R, Donjacour AA, Sciavolino PJ, Kim M, Desai N, et al. (1999) Roles for Nkx3.1 in prostate development and cancer. Genes Dev 13: 966-977.
6. Marker PC, Donjacour AA, Dahiya R, Cunha GR, (2003) Hormonal, cellular, and molecular control of prostatic development. Dev Biol 253: 165-174.
7. Hudson DL, (2004) Epithelial stem cells in human prostate growth and disease. Prostate Cancer Prostatic Dis 7: 188-194.
8. Yap TA, Zivi A, Omlin A, de Bono JS, (2011) The changing therapeutic landscape of castration-resistant prostate cancer. Nat Rev Clin Oncol 8: 597-610.
9. Clevers H, (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
10. Kypta RM, Waxman J, (2012) Wnt/beta-catenin signalling in prostate cancer. Nat Rev Urol.
11. Voeller HJ, Truica CI, Gelmann EP, (1998) Beta-catenin mutations in human prostate cancer. Cancer Res 58: 2520-2523.
12. Szasz AM, Nyirady P, Majoros A, Szendroi A, Szucs M, et al. (2010) beta-catenin expression and claudin expression pattern as prognostic factors of prostatic cancer progression. BJU Int 105: 716-722.
13. Whitaker HC, Girling J, Warren AY, Leung H, Mills IG, et al. (2008) Alterations in beta-catenin expression and localization in prostate cancer. Prostate 68: 1196-1205.
14. Chen G, Shukeir N, Potti A, Sircar K, Aprikian A, et al. (2004) Up-regulation of Wnt-1 and beta-catenin production in patients with advanced metastatic prostate carcinoma: potential pathogenetic and prognostic implications. Cancer 101: 1345-1356.
15. Morita N, Uemura H, Tsumatani K, Cho M, Hirao Y, et al. (1999) E-cadherin and alpha-, beta- and gamma-catenin expression in prostate cancers: correlation with tumour invasion. Br J Cancer 79: 1879-1883.
16. de la Taille A, Rubin MA, Chen MW, Vacherot F, de Medina SG, et al. (2003) Beta-catenin-related anomalies in apoptosis-resistant and hormone-refractory prostate cancer cells. Clin Cancer Res 9: 1801-1807.
17. Masiello D, Chen SY, Xu Y, Verhoeven MC, Choi E, et al. (2004) Recruitment of beta-catenin by wild-type or mutant androgen receptors correlates with ligand-stimulated growth of prostate cancer cells. Mol Endocrinol 18: 2388-2401.
18. Mulholland DJ, Read JT, Rennie PS, Cox ME, Nelson CC, (2003) Functional localization and competition between the androgen receptor and T-cell factor for nuclear beta-catenin: a means for inhibition of the Tcf signaling axis. Oncogene 22: 5602-5613.
19. Song LN, Coghlan M, Gelmann EP, (2004) Antiandrogen effects of mifepristone on coactivator and corepressor interactions with the androgen receptor. Mol Endocrinol 18: 70-85.
20. Truica CI, Byers S, Gelmann EP, (2000) Beta-catenin affects androgen receptor transcriptional activity and ligand specificity. Cancer Res 60: 4709-4713.
21. Verras M, Brown J, Li X, Nusse R, Sun Z, (2004) Wnt3a growth factor induces androgen receptor-mediated transcription and enhances cell growth in human prostate cancer cells. Cancer Res 64: 8860-8866.
22. Song LN, Herrell R, Byers S, Shah S, Wilson EM, et al. (2003) Beta-catenin binds to the activation function 2 region of the androgen receptor and modulates the effects of the N-terminal domain and TIF2 on ligand-dependent transcription. Mol Cell Biol 23: 1674-1687.
23. Pawlowski JE, Ertel JR, Allen MP, Xu M, Butler C, et al. (2002) Liganded androgen receptor interaction with beta-catenin: nuclear co-localization and modulation of transcriptional activity in neuronal cells. J Biol Chem 277: 20702-20710.
24. Wang G, Wang J, Sadar MD, (2008) Crosstalk between the androgen receptor and beta-catenin in castrate-resistant prostate cancer. Cancer Res 68: 9918-9927.
25. Bierie B, Nozawa M, Renou JP, Shillingford JM, Morgan F, et al. (2003) Activation of beta-catenin in prostate epithelium induces hyperplasias and squamous transdifferentiation. Oncogene 22: 3875-3887.
26. Gounari F, Signoretti S, Bronson R, Klein L, Sellers WR, et al. (2002) Stabilization of beta-catenin induces lesions reminiscent of prostatic intraepithelial neoplasia, but terminal squamous transdifferentiation of other secretory epithelia. Oncogene 21: 4099-4107.
27. Yu X, Wang Y, Jiang M, Bierie B, Roy-Burman P, et al. (2009) Activation of beta-Catenin in mouse prostate causes HGPIN and continuous prostate growth after castration. Prostate 69: 249-262.
28. Yu X, Wang Y, DeGraff DJ, Wills ML, Matusik RJ, (2011) Wnt/beta-catenin activation promotes prostate tumor progression in a mouse model. Oncogene 30: 1868-1879.
29. Pearson HB, Phesse TJ, Clarke AR, (2009) K-ras and Wnt signaling synergize to accelerate prostate tumorigenesis in the mouse. Cancer Res 69: 94-101.
30. Dahia PL, (2000) PTEN, a unique tumor suppressor gene. Endocr Relat Cancer 7: 115-129.
31. Suzuki H, Freije D, Nusskern DR, Okami K, Cairns P, et al. (1998) Interfocal heterogeneity of PTEN/MMAC1 gene alterations in multiple metastatic prostate cancer tissues. Cancer Res 58: 204-209.
32. Song MS, Salmena L, Pandolfi PP, (2012) The functions and regulation of the PTEN tumour suppressor. Nat Rev Mol Cell Biol 13: 283-296.
33. Persad S, Troussard AA, McPhee TR, Mulholland DJ, Dedhar S, (2001) Tumor suppressor PTEN inhibits nuclear accumulation of beta-catenin and T cell/lymphoid enhancer factor 1-mediated transcriptional activation. J Cell Biol 153: 1161-1174.
34. Sharma M, Chuang WW, Sun Z, (2002) Phosphatidylinositol 3-kinase/Akt stimulates androgen pathway through GSK3beta inhibition and nuclear beta-catenin accumulation. J Biol Chem 277: 30935-30941.
35. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, et al. (2001) Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128: 1253-1264.
36. Eastman Q, Grosschedl R, (1999) Regulation of LEF-1/TCF transcription factors by Wnt and other signals. Curr Opin Cell Biol 11: 233-240.
37. Herbrand H, Pabst O, Hill R, Arnold HH, (2002) Transcription factors Nkx3.1 and Nkx3.2 (Bapx1) play an overlapping role in sclerotomal development of the mouse. Mech Dev 117: 217-224.
38. Soriano P, (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
39. Thomsen MK, Butler CM, Shen MM, Swain A, (2008) Sox9 is required for prostate development. Dev Biol 316: 302-311.
40. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, et al. (1999) Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 18: 5931-5942.
41. Wang S, Gao J, Lei Q, Rozengurt N, Pritchard C, et al. (2003) Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 4: 209-221.
42. Ding Z, Wu CJ, Chu GC, Xiao Y, Ho D, et al. (2011) SMAD4-dependent barrier constrains prostate cancer growth and metastatic progression. Nature 470: 269-273.
43. Sugimura Y, Cunha GR, Donjacour AA, Bigsby RM, Brody JR, (1986) Whole-mount autoradiography study of DNA synthetic activity during postnatal development and androgen-induced regeneration in the mouse prostate. Biol Reprod 34: 985-995.
44. Bouchard C, Staller P, Eilers M, (1998) Control of cell proliferation by Myc. Trends Cell Biol 8: 202-206.
45. Trumpp A, Refaeli Y, Oskarsson T, Gasser S, Murphy M, et al. (2001) c-Myc regulates mammalian body size by controlling cell number but not cell size. Nature 414: 768-773.
46. Simons BW, Hurley PJ, Huang Z, Ross AE, Miller R, et al. (2012) Wnt signaling though beta-catenin is required for prostate lineage specification. Dev Biol 371: 246-255.
47. Lin Y, Liu G, Zhang Y, Hu YP, Yu K, et al. (2007) Fibroblast growth factor receptor 2 tyrosine kinase is required for prostatic morphogenesis and the acquisition of strict androgen dependency for adult tissue homeostasis. Development 134: 723-734.
48. Mehta V, Abler LL, Keil KP, Schmitz CT, Joshi PS, et al. (2011) Atlas of Wnt and R-spondin gene expression in the developing male mouse lower urogenital tract. Dev Dyn 240: 2548-2560.
49. 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 doi:10.1371/journal.pone.0002186.
50. Lukacs RU, Memarzadeh S, Wu H, Witte ON, (2010) Bmi-1 is a crucial regulator of prostate stem cell self-renewal and malignant transformation. Cell Stem Cell 7: 682-693.
51. Bisson I, Prowse DM, (2009) WNT signaling regulates self-renewal and differentiation of prostate cancer cells with stem cell characteristics. Cell Res 19: 683-697.
52. Xin L, Lukacs RU, Lawson DA, Cheng D, Witte ON, (2007) Self-renewal and multilineage differentiation in vitro from murine prostate stem cells. Stem Cells 25: 2760-2769.
53. Risbridger G, Wang H, Young P, Kurita T, Wang YZ, et al. (2001) Evidence that epithelial and mesenchymal estrogen receptor-alpha mediates effects of estrogen on prostatic epithelium. Dev Biol 229: 432-442.
54. Risbridger GP, Wang H, Frydenberg M, Cunha G, (2001) The metaplastic effects of estrogen on mouse prostate epithelium: proliferation of cells with basal cell phenotype. Endocrinology 142: 2443-2450.
55. Chen M, Yeh CR, Chang HC, Vitkus S, Wen XQ, et al. (2012) Loss of epithelial oestrogen receptor alpha inhibits oestrogen-stimulated prostate proliferation and squamous metaplasia via in vivo tissue selective knockout models. J Pathol 226: 17-27.
56. Romano RA, Ortt K, Birkaya B, Smalley K, Sinha S, (2009) An active role of the DeltaN isoform of p63 in regulating basal keratin genes K5 and K14 and directing epidermal cell fate. PLoS ONE 4: e5623 doi:10.1371/journal.pone.0005623.
57. Hu H, Xia SH, Li AD, Xu X, Cai Y, et al. (2002) Elevated expression of p63 protein in human esophageal squamous cell carcinomas. Int J Cancer 102: 580-583.
58. Ruptier C, De Gasperis A, Ansieau S, Granjon A, Taniere P, et al. (2011) TP63 P2 promoter functional analysis identifies beta-catenin as a key regulator of DeltaNp63 expression. Oncogene 30: 4656-4665.
59. Grasso CS, Wu YM, Robinson DR, Cao X, Dhanasekaran SM, et al. (2012) The mutational landscape of lethal castration-resistant prostate cancer. Nature 487: 239-243.
60. Kumar A, White TA, MacKenzie AP, Clegg N, Lee C, et al. (2011) Exome sequencing identifies a spectrum of mutation frequencies in advanced and lethal prostate cancers. Proc Natl Acad Sci U S A 108: 17087-17092.
61. Huang SM, Mishina YM, Liu S, Cheung A, Stegmeier F, et al. (2009) Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 461: 614-620.
62. Wu X, Wu J, Huang J, Powell WC, Zhang J, et al. (2001) Generation of a prostate epithelial cell-specific Cre transgenic mouse model for tissue-specific gene ablation. Mech Dev 101: 61-69.
63. Lesche R, Groszer M, Gao J, Wang Y, Messing A, et al. (2002) Cre/loxP-mediated inactivation of the murine Pten tumor suppressor gene. Genesis 32: 148-149.
64. Val P, Jeays-Ward K, Swain A, (2006) Identification of a novel population of adrenal-like cells in the mammalian testis. Dev Biol 299: 250-256.
65. Swain A, Narvaez V, Burgoyne P, Camerino G, Lovell-Badge R, (1998) Dax1 antagonizes Sry action in mammalian sex determination. Nature 391: 761-767.
66. Park JH, Walls JE, Galvez JJ, Kim M, Abate-Shen C, et al. (2002) Prostatic intraepithelial neoplasia in genetically engineered mice. Am J Pathol 161: 727-735.
67. Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, et al. (2004) Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee. Cancer Res 64: 2270-2305.