Cross-regulation of signaling pathways: An example of nuclear hormone receptors and the canonical Wnt pathway

Experimental Cell Research

Volumn 316, Issue 11, 2010, Pages 1763-1772

  Beildeck, Marcy E ^a   Gelmann, Edward P ^b   Byers, Stephen, W ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Androgen receptor; AR; Beta catenin; Catenin; Cross talk; Hormone; Nuclear hormone receptor; VDR; Vitamin D receptor

Indexed keywords

ANDROGEN RECEPTOR; AXIN; AXIN 2; BETA CATENIN; CADHERIN; CYCLIN D1; DEXAMETHASONE; DICKKOPF 1 PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; HORMONE RECEPTOR; LIOTHYRONINE; LIOTHYRONINE RECEPTOR; NUCLEAR HORMONE RECEPTOR; ORPHAN NUCLEAR RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROGESTERONE RECEPTOR; RETINOIC ACID; SECRETED FRIZZLED RELATED PROTEIN 1; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; VITAMIN D RECEPTOR; WNT PROTEIN; WNT7A PROTEIN;

ADIPOGENESIS; BONE DEVELOPMENT; CELL ADHESION; CELL DIFFERENTIATION; CELL FATE; COLORECTAL CANCER; EXTRACELLULAR SPACE; GENE REPRESSION; HUMAN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROSTATE CANCER; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

EID: 77953233022     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.02.001     Document Type: Review

References (95)

1. Munemitsu S., Albert I., Souza B., Rubinfeld B., Polakis P. Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:3046-3050.
2. Rubinfeld B., Albert I., Porfiri E., Fiol C., Munemitsu S., Polakis P. Binding of GSK3 beta to the APC-beta-catenin complex and regulation of complex assembly. Science 1996, 272:1023-1026.
3. Orford K., Crockett C., Jensen J.P., Weissman A.M., Byers S.W. Serine phosphorylation-regulated ubiquitination and degradation of beta-catenin. J. Biol. Chem. 1997, 272:24735-24738.
4. Barth A.I., Nathke I.S., Nelson W.J. Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr. Opin. Cell Biol. 1997, 9:683-690.
5. Behrens J., von Kries J.P., Kuhl M., Bruhn L., Wedlich D., Grosschedl R., Birchmeier W. Functional interaction of b-catenin with the transcription factor LEF-1. Nature 1996, 382:638-642.
6. Cong F., Schweizer L., Chamorro M., Varmus H. Requirement for a nuclear function of beta-catenin in Wnt signaling. Mol. Cell. Biol. 2003, 23:8462-8470.
7. Tolwinski N.S., Wieschaus E. A nuclear function for armadillo/beta-catenin. PLoS Biol. 2004, 2:E95.
8. Itasaki N., Jones C.M., Mercurio S., Rowe A., Domingos P.M., Smith J.C., Krumlauf R. Wise, a context-dependent activator and inhibitor of Wnt signalling. Development 2003, 130:4295-4305.
9. Kinzler K.W., Nilbert M.C., Vogelstein B., et al. Identification of a chromosome 5q21 gene that is mutated in colorectal cancers. Science 1991, 251:1366-1370.
10. Rubinfeld B., Robbins P., El-Gamil M., Albert I., Porfiri E., Polakis P. Stabilization of beta-catenin by genetic defects in melanoma cell lines. Science 1997, 275:1790-1792.
11. Palacios J., Gamallo C. Mutations in the beta-catenin gene (CTNNB1) in endometrioid ovarian carcinomas. Cancer Res. 1998, 58:1344-1347.
12. Zurawel R.H., Chiappa S.A., Allen C., Raffel C. Sporadic medulloblastomas contain oncogenic beta-catenin mutations. Cancer Res. 1998, 58:896-899.
13. Porfiri E., Rubinfeld B., Albert I., Hovanes K., Waterman M., Polakis P. Induction of a beta-catenin-LEF-1 complex by wnt-1 and transforming mutants of beta-catenin. Oncogene 1997, 15:2833-2839.
14. Kennell J.A., MacDougald O.A. Wnt signaling inhibits adipogenesis through beta-catenin-dependent and -independent mechanisms. J. Biol. Chem. 2005, 280:24004-24010.
15. Bennett C.N., Longo K.A., Wright W.S., Suva L.J., Lane T.F., Hankenson K.D., MacDougald O.A. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:3324-3329.
16. Kang S., Bennett C.N., Gerin I., Rapp L.A., Hankenson K.D., MacDougald O.A. Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein alpha and peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 2007, 282:14515-14524.
17. Moldes M., Zuo Y., Morrison R.F., Silva D., Park B.H., Liu J.J., Farmer S.R. Peroxisome-proliferator-activated receptor gamma suppresses Wnt/beta-catenin signalling during adipogenesis. Biochem. J. 2003, 376:607-613.
18. Okamura M., Kudo H., Wakabayashi K., Tanaka T., Nonaka A., Uchida A., Tsutsumi S., Sakakibara I., Naito M., Osborne T.F., Hamakubo T., Ito S., Aburatani H., Yanagisawa M., Kodama T., Sakai J. COUP-TFII acts downstream of Wnt/beta-catenin signal to silence PPAR gamma gene expression and repress adipogenesis. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:5819-5824.
19. Wang C.G., Pattabiraman N., Zhou J.N., Fu M.F., Sakamaki T., Albanese C., Li Z.P., Wu K.M., Hulit J., Neumeister P., Novikoff P.M., Brownlee M., Scherer P.E., Jones J.G., Whitney K.D., Donehower L.A., Harris E.L., Rohan T., Johns D.C., Pestell R.G. Cyclin D1 repression of peroxisome proliferator-activated receptor gamma expression and transactivation. Mol. Cell. Biol. 2003, 23:6159-6173.
20. Winn R.A., Van Scoyk M., Hammond M., Rodriguez K., Crossno J.T., Heasley L.E., Nemenoff R.A. Antitumorigenic effect of Wnt 7a and Fzd 9 in non-small cell lung cancer cells is mediated through ERK-5-dependent activation of peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 2006, 281:26943-26950.
21. Gerhold D.L., Liu F., Jiang G., Li Z., Xu J., Lu M., Sachs J.R., Bagchi A., Fridman A., Holder D.J., Doebber T.W., Berger J., Elbrecht A., Moller D.E., Zhang B.B. Gene expression profile of adipocyte differentiation and its regulation by peroxisome proliferator-activated receptor-gamma agonists. Endocrinology 2002, 143:2106-2118.
22. Liu J.J., Farmer S.R. Regulating the balance between peroxisome proliferator-activated receptor gamma and beta-catenin signaling during adipogenesis-A glycogen synthase kinase 3 beta phosphorylation-defective mutant of beta-catenin inhibits expression of a subset of adipogenic genes. J. Biol. Chem. 2004, 279:45020-45027.
23. Ross S.E., Hemati N., Longo K.A., Bennett C.N., Lucas P.C., Erickson R.L., MacDougald O.A. Inhibition of adipogenesis by Wnt signaling. Science 2000, 289:950-953.
24. Sharma C., Pradeep A., Wong L., Rana A., Rana B. Peroxisome proliferator-activated receptor gamma activation can regulate beta-catenin levels via a proteasome-mediated and adenomatous polyposis coli-independent pathway. J. Biol. Chem. 2004, 279:35583-35594.
25. Christodoulides C., Laudes M., Cawthorn W.P., Schinner S., Soos M., O'Rahilly S., Sethi J.K., Vidal-Puig A. The Wnt antagonist Dickkopf-1 and its receptors are coordinately regulated during early human adipogenesis. J. Cell Sci. 2006, 119:2613-2620.
26. Bennett C.N., Ross S.E., Longo K.A., Bajnok L., Hemati N., Johnson K.W., Harrison S.D., MacDougald O.A. Regulation of Wnt signaling during adipogenesis. J. Biol. Chem. 2002, 277:30998-31004.
27. Ohnaka K., Taniguchi H., Kawate H., Nawata H., Takayanagi R. Glucocorticoid enhances the expression of dickkopf-1 in human osteoblasts: novel mechanism of glucocorticoid-induced osteoporosis. Biochem. Biophys. Res. Commun. 2004, 318:259-264.
28. Wang F.S., Lin C.L., Chen Y.J., Wang C.J., Yang K.D., Huang Y.T., Sun Y.C., Huang H.C. Secreted frizzled-related protein 1 modulates glucocorticoid attenuation of osteogenic activities and bone mass. Endocrinology 2005, 146:2415-2423.
29. Hayashi K., Yamaguchi T., Yano S., Kanazawa I., Yamauchi M., Yamamoto M., Sugimoto T. BMP/Wnt antagonists are upregulated by dexamethasone in osteoblasts and reversed by alendronate and PTH: potential therapeutic targets for glucocorticoid-induced osteoporosis. Biochem. Biophys. Res. Commun. 2009, 379:261-266.
30. Zhao X., Duester G. Effect of retinoic acid signaling on Wnt/beta-catenin and FGF signaling during body axis extension. Gene Expr. Patterns 2009, 9:430-435.
31. Guan Y., Rubenstein N.M., Failor K.L., Woo P.L., Firestone G.L. Glucocorticoids control beta-catenin protein expression and localization through distinct pathways that can be uncoupled by disruption of signaling events required for tight junction formation in rat mammary epithelial tumor cells. Mol. Endocrinol. 2004, 18:214-227.
32. Cianferotti L., Demay M.B. VDR-mediated inhibition of DKK1 and SFRP2 suppresses adipogenic differentiation of murine bone marrow stromal cells. J. Cell. Biochem. 2007, 101:80-88.
33. Fretz J.A., Zella L.A., Kim S., Shevde N.K., Pike J.W. 1,25-Dihydroxyvitamin D-3 regulates the expression of low-density lipoprotein receptor-related protein 5 via deoxyribonucleic acid sequence elements located downstream of the start site of transcription. Mol. Endocrinol. 2006, 20:2215-2230.
34. Aguilera O., Pena C., Garcia J.M., Larriba M.J., Ordonez-Moran P., Navarro D., Barbachano A., de Silanes I.L., Ballestar E., Fraga M.F., Esteller M., Gamallo C., Bonilla F., Gonzalez-Sancho J.M., Munoz A. The Wnt antagonist DICKKOPF-1 gene is induced by 1 alpha,25-dihydroxyvitamin D-3 associated to the differentiation of human colon cancer cells. Carcinogenesis 2007, 28:1877-1884.
35. Pendas-Franco N., Aguilera O., Pereira F., Gonzalez-Sancho J.M., Munoz A. Vitamin D and Wnt/beta-catenin pathway in colon cancer: role and regulation of DICKKOPF genes. Anticancer Res. 2008, 28:2613-2623.
36. Verani R., Cappuccio I., Spinsanti P., Gradini R., Caruso A., Magnotti M.C., Motolese M., Nicoletti F., Melchiorri D. Expression of the Wnt inhibitor Dickkopf-1 is required for the induction of neural markers in mouse embryonic stem cells differentiating in response to retinoic acid. J. Neurochem. 2007, 100:242-250.
37. Shum A.S.W., Poon L.L.M., Tang W.W.T., Koide T., Chan B.W.H., Leung Y.C.G., Shiroishi T., Copp A.J. Retinoic acid induces down-regulation of Wnt-3a, apoptosis and diversion of tail bud cells to a neural fate in the mouse embryo. Mech. Dev. 1999, 84:17-30.
38. Li S.W., Lou X., Wang J.H., Liu B., Ma L.P., Su Z.P., Ding X.Y. Retinoid signaling can repress blastula Wnt signaling and impair dorsal development in Xenopus embryo. Differentiation 2008, 76:897-907.
39. Katoh M. Regulation of WNT signaling molecules by retinoic acid during neuronal differentiation in NT2 cells: threshold model of WNT action (review). Int. J. Mol. Med. 2002, 10:683-687.
40. Onai T., Lin H.C., Schubert M., Koop D., Osborne P.W., Alvarez S., Alvarez R., Holland N.D., Holland L.Z. Retinoic acid and Wnt/beta-catenin have complementary roles in anterior/posterior patterning embryos of the basal chordate amphioxus. Dev. Biol. 2009, 332:223-233.
41. Tice D.A., Szeto W., Soloviev I., Rubinfeld B., Fong S.E., Dugger D.L., Winer J., Williams P.M., Wieand D., Smith V., Schwall R.H., Pennica D., Polakis P. Synergistic induction of tumor antigens by Wnt-1 signaling and retinoic acid revealed by gene expression profiling. J. Biol. Chem. 2002, 277:14329-14335.
42. Tulac S., Overgaard M.T., Hamilton A.E., Jumbe N.L., Suchanek E., Giudice L.C. Dickkopf-1, an inhibitor of Wnt signaling, is regulated by progesterone in human endometrial stromal cells. J. Clin. Endocrinol. Metab. 2006, 91:1453-1461.
43. Brisken C., Heineman A., Chavarria T., Elenbaas B., Tan J., Dey S.K., McMahon J.A., McMahon A.P., Weinberg R.A. Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev. 2000, 14:650-654.
44. Bocchinfuso W.P., Hively W.P., Couse J.F., Varmus H.E., Korach K.S. A mouse mammary tumor virus Wnt-1 transgene induces mammary gland hyperplasia and tumorigenesis in mice lacking estrogen receptor-alpha. Cancer Res. 1999, 59:1869-1876.
45. Kress E., Rezza A., Nadjar J., Samarut J., Plateroti M. The frizzled-related sFRP2 gene is a target of thyroid hormone receptor alpha 1 and activates beta-catenin signaling in mouse intestine. J. Biol. Chem. 2009, 284:1234-1241.
46. Vermeulen S.J., Bruyneel E.A., Van Roy F.M., Mareel M.M., Bracke M.E. Activation of the E-cadherin/catenin complex in human MCF-7 breast cancer cells by all-trans-retinoic acid. Br. J. Cancer 1995, 72:1447-1453.
47. Byers S., Pishvaian M., Crockett C., Peer C., Tozeren A., Sporn M., Anzano M., Lechleider R. Retinoids increase cell-cell adhesion strength, beta-catenin protein stability, and localization to the cell membrane in a breast cancer cell line: a role for serine kinase activity. Endocrinology 1996, 137:3265-3273.
48. Easwaran V., Pishvaian M., Salimuddin S., Byers S. Cross-regulation of beta-catenin-LEF/TCF and retinoid signaling pathways. Curr. Biol. 1999, 9:1415-1418.
49. Palmer H.G., Gonzalez-Sancho J.M., Espada J., Berciano M.T., Puig I., Baulida J., Quintanilla M., Cano A., de Herreros A.G., Lafarga M., Munoz A. Vitamin D(3) promotes the differentiation of colon carcinoma cells by the induction of E-cadherin and the inhibition of beta-catenin signaling. J. Cell Biol. 2001, 154:369-387.
50. Ohta T., Elnemr A., Yamamoto M., Ninomiya I., Fushida S., Nishimura G.I., Fujimura T., Kitagawa H., Kayahara M., Shimizu K., Yi S.Q., Miwa K. Thiazolidinedione, a peroxisome proliferator-activated receptor-gamma ligand, modulates the E-cadherin/beta-catenin system in a human pancreatic cancer cell line, BxPC-3. Int. J. Oncol. 2002, 21:37-42.
51. Plateroti M., Kress E., Mori J.I., Samarut J. Thyroid hormone receptor alpha 1 directly controls transcription of the beta-catenin gene in intestinal epithelial cells. Mol. Cell. Biol. 2006, 26:3204-3214.
52. Natsume H., Sasaki S., Kitagawa M., Kashiwabara Y., Matsushita A., Nakano K., Nishiyama K., Nagayama K., Misawa H., Masuda H., Nakamura H. Beta-catenin/Tcf-1-mediated transactivation of cyclin D1 promoter is negatively regulated by thyroid hormone. Biochem. Biophys. Res. Commun. 2003, 309:408-413.
53. Miller L.D., Park K.S., Guo Q.B.M., Alkharouf N.W., Malek R.L., Lee N.H., Liu E.T., Cheng S.Y. Silencing of Wnt signaling and activation of multiple metabolic pathways in response to thyroid hormone-stimulated cell proliferation. Mol. Cell. Biol. 2001, 21:6626-6639.
54. Xiao J.H., Ghosn C., Hinchman C., Forbes C., Wang J., Snider N., Cordrey A., Zhao Y., Chandraratna R.A.S. Adenomatous polyposis coli (APC)-independent regulation of beta-catenin degradation via a retinoid X receptor-mediated pathway. J. Biol. Chem. 2003, 278:29954-29962.
55. Dillard A.C., Lane M. Retinol reduces beta-catenin protein in retinoic acid-resistant colon cancer cells by increasing beta-catenin-RXR-alpha interaction in the nucleus and translocation into the cytosol. FASEB J. 2007, 21:A59.
56. Dillard A.C., Lane M.A. Retinol decreases beta-catenin protein levels in retinoic acid-resistant colon cancer cell lines. Mol. Carcinog. 2007, 46:315-329.
57. Y. Li, R. Wu, X. Wang, and W. Chen (2004). Effects of retinoic acid on the beta-catenin/TCF pathway in cultured porcine tracheobronchial epithelial cells. J. Huazhong.Univ. Sci. Technolog. Med. Sci. 24, 421-3, 432.
58. Zwijsen R.M.L., Wientjens E., Klompmaker R., vanderSman J., Bernards R., Michalides R.J.A.M. CDK-independent activation of estrogen receptor by cyclin D1. Cell 1997, 88:405-415.
59. Neuman E., Ladha M.H., Lin N., Upton T.M., Miller S.J., DiRenzo J., Pestell R.G., Hinds P.W., Dowdy S.F., Brown M., Ewen M.E. Cyclin D1 stimulation of estrogen receptor transcriptional activity independent of cdk4. Mol. Cell. Biol. 1997, 17:5338-5347.
60. Zwijsen R.M.L., Buckle R.S., Hijmans E.M., Loomans C.J.M., Bernards R. Ligand-independent recruitment of steroid receptor coactivators to estrogen receptor by cyclin D1. Genes Dev. 1998, 12:3488-3498.
61. Cardona-Gomez G.P., Mendez P., DonCarlos L.L., Azcoitia I., Garcia-Segura L.M. Interactions of estrogen and insulin-like growth factor-I in the brain: molecular mechanisms and functional implications. J. Steroid Biochem. Mol. Biol. 2002, 83:211-217.
62. Mulholland D.J., Dedhar S., Coetzee G.A., Nelson C.C. Interaction of nuclear receptors with the Wnt/beta-catenin/Tcf signaling axis: Wnt you like to know?. Endocr. Rev. 2005, 26:898-915.
63. Li Y.C., Pirro A.E., Amling M., Delling G., Baron R., Bronson R., Demay M.B. Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:9831-9835.
64. Cianferotti L., Cox M., Skorija K., Demay M.B. Vitamin D receptor is essential for normal keratinocyte stem cell function. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:9428-9433.
65. Palmer H.G., Anjos-Afonso F., Carmeliet G., Takeda H., Watt F.M. The vitamin D receptor is a Wnt effector that controls hair follicle differentiation and specifies tumor type in adult epidermis. PLoS ONE 2008, 3:e1483.
66. Pawlowski J.E., Ertel J.R., Allen M.P., Xu M., Butler C., Wilson E.M., Wierman M.E. Liganded androgen receptor interaction with beta-catenin-Nuclear co-localization and modulation of transcriptional activity in neuronal cells. J. Biol. Chem. 2002, 277:20702-20710.
67. Truica C.I., Byers S., Gelmann E.P. Beta-catenin affects androgen receptor transcriptional activity and ligand specificity. Cancer Res. 2000, 60:4709-4713.
68. Chesire D.R., Isaacs W.B. Ligand-dependent inhibition of beta-catenin/TCF signaling by androgen receptor. Oncogene 2002, 21:8453-8469.
69. Mulholland D.J., Cheng H., Reid K., Rennie P.S., Nelson C.C. The androgen receptor can promote beta-catenin nuclear translocation independently of adenomatous polyposis coli. J. Biol. Chem. 2002, 277:17933-17943.
70. Shah S., Islam M.N., Dakshanamurthy S., Rizvi I., Rao M., Herrell R., Zinser G., Valrance M., Aranda A., Moras D., Norman A., Welsh J., Byers S.W. The molecular basis of vitamin D receptor and beta-catenin crossregulation. Mol. Cell. 2006, 21:799-809.
71. Jansson E.A., Are A., Greicius G., Kuo I.C., Kelly D., Arulampalam V., Pettersson S. The Wnt/beta-catenin signaling pathway targets PPAR gamma activity in colon cancer cells. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:1460-1465.
72. Kouzmenko A.P., Takeyama K., Ito S., Furutani T., Sawatsubashi S., Maki A., Suzuki E., Kawasaki Y., Akiyama T., Tabata T., Kato S. Wnt/beta-catenin and estrogen signaling converge in vivo. J. Biol. Chem. 2004, 279:40255-40258.
73. Uno S., Endo K., Jeong Y., Kawana K., Miyachi H., Hashimoto Y., Makishima M. Suppression of beta-catenin signaling by liver X receptor ligands. Biochem. Pharmacol. 2009, 77:186-195.
74. Amir A.L., Barua M., McKnight N.C., Cheng S.T., Yuan X., Balk S.P. A direct beta-catenin-independent interaction between androgen receptor and T cell factor 4. J. Biol. Chem. 2003, 278:30828-30834.
75. Song L.N., Herrell R., Byers S., Shah S., Wilson E.M., Gelmann E.P. 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. 2003, 23:1674-1687.
76. El Tanani M., Fernig D.G., Barraclough R., Green C., Rudland P. Differential modulation of transcriptional activity of estrogen receptors by direct protein-protein interactions with the T cell factor family of transcription factors. J. Biol. Chem. 2001, 276:41675-41682.
77. Watanabe M., Kakiuchi H., Kato H., Shiraishi T., Yatani R., Sugimura T., Nagao M. APC gene mutations in human prostate cancer. Jpn. J. Clin. Oncol. 1996, 26:77-81.
78. Phillips S.M., Morton D.G., Lee S.J., Wallace D.M., Neoptolemos J.P. Loss of heterozygosity of the retinoblastoma and adenomatous polyposis susceptibility gene loci and in chromosomes 10p, 10q and 16q in human prostate cancer. Br. J. Urol. 1994, 73:390-395.
79. Lehrer S., McCurdy L.D., Stock R.G., Kornreich R., Stone N.N., Eng C. Body mass, age, and the APC I1307K allele in Ashkenazi Jewish prostate cancer patients. Cancer Genet. Cytogenet. 2000, 122:131-133.
80. Henrique R., Ribeiro F.R., Fonseca D., Hoque M.O., Carvalho A.L., Costa V.L., Pinto M., Oliveira J., Teixeira M.R., Sidransky D., Jeronimo C. High promoter methylation levels of APC predict poor prognosis in sextant biopsies from prostate cancer patients. Clin. Cancer Res. 2007, 13:6122-6129.
81. Richiardi L., Fiano V., Vizzini L., De M.L., Delsedime L., Akre O., Gillio T.A., Merletti F. Promoter methylation in APC, RUNX3, and GSTP1 and mortality in prostate cancer patients. J. Clin. Oncol. 2009, 27:3161-3168.
82. Gerstein A.V., Almeida T.A., Zhao G., Chess E., Shih I., Buhler K., Pienta K., Rubin M.A., Vessella R., Papadopoulos N. APC/CTNNB1 (beta-catenin) pathway alterations in human prostate cancers. Genes Chromosomes Cancer 2002, 34:9-16.
83. Voeller H.J., Truica C.I., Gelmann E.P. Beta-catenin mutations in human prostate cancer. Cancer Res. 1998, 58:2520-2523.
84. Chesire D.R., Ewing C.M., Sauvageot J., Bova G.S., Isaacs W.B. Detection and analysis of beta-catenin mutations in prostate cancer. Prostate 2000, 45:323-334.
85. Yang F., Li X., Sharma M., Sasaki C.Y., Longo D.L., Lim B., Sun Z. Linking beta-catenin to androgen-signaling pathway. J. Biol. Chem. 2002, 277:11336-11344.
86. Masiello D., Chen S.Y., Xu Y., Verhoeven M.C., Choi E., Hollenberg A.N., Balk S.P. Recruitment of beta-catenin by wild-type or mutant androgen receptors correlates with ligand-stimulated growth of prostate cancer cells. Mol. Endocrinol. 2004, 18:2388-2401.
87. Li H., Kim J.H., Koh S.S., Stallcup M.R. Synergistic effects of coactivators GRIP1 and beta-catenin on gene activation: cross-talk between androgen receptor and Wnt signaling pathways. J. Biol. Chem. 2004, 279:4212-4220.
88. Sharma M., Chuang W.W., Sun Z. Phosphatidylinositol 3-kinase/Akt stimulates androgen pathway through GSK3beta inhibition and nuclear beta-catenin accumulation. J. Biol. Chem. 2002, 277:30935-30941.
89. Verras M., Sun Z. Beta-catenin is involved in insulin-like growth factor 1-mediated transactivation of the androgen receptor. Mol. Endocrinol. 2005, 19:391-398.
90. Mulholland D.J., Read J.T., Rennie P.S., Cox M.E., Nelson C.C. 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 2003, 22:5602-5613.
91. Chen S.Y., Wulf G., Zhou X.Z., Rubin M.A., Lu K.P., Balk S.P. Activation of {beta}-catenin signaling in prostate cancer by peptidyl-prolyl isomerase Pin1-mediated abrogation of the androgen receptor-{beta}-catenin interaction. Mol. Cell. Biol. 2006, 26:929-939.
92. Berger R., Febbo P.G., Majumder P.K., Zhao J.J., Mukherjee S., Signoretti S., Campbell K.T., Sellers W.R., Roberts T.M., Loda M., Golub T.R., Hahn W.C. Androgen-induced differentiation and tumorigenicity of human prostate epithelial cells. Cancer Res. 2004, 64:8867-8875.
93. Rios-Doria J., Kuefer R., Ethier S.P., Day M.L. Cleavage of beta-catenin by calpain in prostate and mammary tumor cells. Cancer Res. 2004, 64:7237-7240.
94. Linja M.J., Porkka K.P., Kang Z., Savinainen K.J., Janne O.A., Tammela T.L., Vessella R.L., Palvimo J.J., Visakorpi T. Expression of androgen receptor coregulators in prostate cancer. Clin. Cancer Res. 2004, 10:1032-1040.
95. Horvath L.G., Henshall S.M., Lee C.S., Kench J.G., Golovsky D., Brenner P.C., O'neill G.F., Kooner R., Stricker P.D., Grygiel J.J., Sutherland R.L. Lower levels of nuclear beta-catenin predict for a poorer prognosis in localized prostate cancer. Int. J. Cancer 2005, 113:415-422.