Hic-5 influences genomic and non-genomic actions of the androgen receptor in prostate myofibroblasts

Molecular and Cellular Endocrinology

Volumn 384, Issue 1-2, 2014, Pages 185-199

  Leach, Damien A ^a   Need, Eleanor F ^a   Trotta, Andrew P ^a   Grubisha, Melanie J ^b   DeFranco, Donald B ^b   Buchanan, Grant ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Androgen receptor; Fibroblasts; Focal adhesions; Microenvironment; Prostate cancer; Stroma

Indexed keywords

ADAPTOR PROTEIN; ANDROGEN; ANDROGEN RECEPTOR; FOCAL ADHESION KINASE; HYDROGEN PEROXIDE INDUCIBLE GENE 5 PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL GROWTH; CELL INVASION; CELL MOTILITY; CELL NUCLEUS; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; FOCAL ADHESION; GENE AMPLIFICATION; GENE CONTROL; GENE TARGETING; GENOME; GROWTH REGULATION; HORMONE ACTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR TRANSPORT; MOLECULAR BIOLOGY; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROSTATE STROMAL MYOFIBROBLAST; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; STROMA CELL;

ANDROGEN RECEPTOR; FIBROBLASTS; FOCAL ADHESIONS; MICROENVIRONMENT; PROSTATE CANCER; STROMA;

ANDROGENS; CELL ADHESION; CELL LINE, TRANSFORMED; CELL MOVEMENT; CELL NUCLEUS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIM DOMAIN PROTEINS; MALE; MOLECULAR SEQUENCE ANNOTATION; MYOFIBROBLASTS; PHOSPHORYLATION; PROSTATE; PROTEIN TRANSPORT; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION; STROMAL CELLS; TESTOSTERONE; TUMOR MICROENVIRONMENT;

EID: 84896854384     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.01.004     Document Type: Article

References (104)

1. Avraamides C., Bromberg M.E., Gaughan J.P., Thomas S.M., Tsygankov A.Y., Panetti T.S. Hic-5 promotes endothelial cell migration to lysophosphatidic acid. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H193-H203.
2. Baron S., Manin M., Beaudoin C., Leotoing L., Communal Y., Veyssiere G., Morel L. Androgen receptor mediates non-genomic activation of phosphatidylinositol 3-OH kinase in androgen-sensitive epithelial cells. J. Biol. Chem. 2004, 279:14579-14586.
3. Bebermeier J.H., Brooks J.D., Deprimo S.E., Werner R., Deppe U., Demeter J., Hiort O., Holterhus P.M. Cell-line and tissue-specific signatures of androgen receptor-coregulator transcription. J. Mol. Med. (Berl.) 2006, 84:919-931.
4. Bhowmick N.A., Neilson E.G., Moses H.L. Stromal fibroblasts in cancer initiation and progression. Nature 2004, 432:332-337.
5. Bohen S.P., Kralli A., Yamamoto K.R. Hold 'em and fold 'em: chaperones and signal transduction. Science 1995, 268:1303-1304.
6. Bonaccorsi L., Marchiani S., Ferruzzi P., Muratori M., Crescioli C., Forti G., Maggi M., Baldi E. Non-genomic effects of the androgen receptor and vitamin D agonist are involved in suppressing invasive phenotype of prostate cancer cells. Steroids 2006, 71:304-309.
7. Bonaccorsi L., Nosi D., Quercioli F., Formigli L., Zecchi S., Maggi M., Forti G., Baldi E. Prostate cancer: a model of integration of genomic and non-genomic effects of the androgen receptor in cell lines model. Steroids 2008, 73:1030-1037.
8. Boonyaratanakornkit V., Edwards D.P. Receptor mechanisms mediating non-genomic actions of sex steroids. Semin. Reprod. Med. 2007, 25:139-153.
9. Buchanan G., Craft P.S., Yang M., Cheong A., Prescott J., Jia L., Coetzee G.A., Tilley W.D. PC-3 cells with enhanced androgen receptor signaling: a model for clonal selection in prostate cancer. Prostate 2004, 60:352-366.
10. Buchanan G., Ricciardelli C., Harris J.M., Prescott J., Yu Z.C., Jia L., Butler L.M., Marshall V.R., Scher H.I., Gerald W.L., Coetzee G.A., Tilley W.D. Control of androgen receptor signaling in prostate cancer by the cochaperone small glutamine rich tetratricopeptide repeat containing protein alpha. Cancer Res. 2007, 67:10087-10096.
11. Cai G., Huang H., Shapiro E., Zhou H., Yeh S., Melamed J., Greco M.A., Lee P. Expression of androgen receptor associated protein 55 (ARA55) in the developing human fetal prostate. J. Urol. 2005, 173:2190-2193.
12. Cano P., Godoy A., Escamilla R., Dhir R., Onate S.A. Stromal-epithelial cell interactions and androgen receptor-coregulator recruitment is altered in the tissue microenvironment of prostate cancer. Cancer Res. 2007, 67:511-519.
13. Chang H.C., Chen S.C., Chen J., Hsieh J.T. In vitro gene expression changes of androgen receptor coactivators after hormone deprivation in an androgen-dependent prostate cancer cell line. J. Formos. Med. Assoc. 2005, 104:652-658.
14. Chmelar R., Buchanan G., Need E.F., Tilley W., Greenberg N.M. Androgen receptor coregulators and their involvement in the development and progression of prostate cancer. Int. J. Cancer 2007, 120:719-733.
15. Chung L.W., Cunha G.R. Stromal-epithelial interactions: II. Regulation of prostatic growth by embryonic urogenital sinus mesenchyme. Prostate 1983, 4:503-511.
16. Cunha G.R., Chung L.W., Shannon J.M., Taguchi O., Fujii H. Hormone-induced morphogenesis and growth: role of mesenchymal-epithelial interactions. Recent Prog. Horm. Res. 1983, 39:559-598.
17. Cunha G.R., Fujii H., Neubauer B.L., Shannon J.M., Sawyer L., Reese B.A. Epithelial-mesenchymal interactions in prostatic development. I. Morphological observations of prostatic induction by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder. J. Cell Biol. 1983, 96:1662-1670.
18. Deakin N.O., Turner C.E. Distinct roles for paxillin and Hic-5 in regulating breast cancer cell morphology, invasion, and metastasis. Mol. Biol. Cell 2011, 22:327-341.
19. Dhanasekaran S.M., Barrette T.R., Ghosh D., Shah R., Varambally S., Kurachi K., Pienta K.J., Rubin M.A., Chinnaiyan A.M. Delineation of prognostic biomarkers in prostate cancer. Nature 2001, 412:822-826.
20. Drori S., Girnun G.D., Tou L., Szwaya J.D., Mueller E., Xia K., Shivdasani R.A., Spiegelman B.M. Hic-5 regulates an epithelial program mediated by PPARgamma. Genes Dev. 2005, 19:362-375.
21. Franco O.E., Jiang M., Strand D.W., Peacock J., Fernandez S., Jackson R.S., Revelo M.P., Bhowmick N.A., Hayward S.W. Altered TGF-beta signaling in a subpopulation of human stromal cells promotes prostatic carcinogenesis. Cancer Res. 2011, 71:1272-1281.
22. Fujimoto N., Miyamoto H., Mizokami A., Harada S., Nomura M., Ueta Y., Sasaguri T., Matsumoto T. Prostate cancer cells increase androgen sensitivity by increase in nuclear androgen receptor and androgen receptor coactivators; a possible mechanism of hormone-resistance of prostate cancer cells. Cancer Invest. 2007, 25:32-37.
23. Fujimoto N., Yeh S., Kang H.Y., Inui S., Chang H.C., Mizokami A., Chang C. Cloning and characterization of androgen receptor coactivator, ARA55, in human prostate. J. Biol. Chem. 1999, 274:8316-8321.
24. Fujita H., Kamiguchi K., Cho D., Shibanuma M., Morimoto C., Tachibana K. Interaction of Hic-5, a senescence-related protein, with focal adhesion kinase. J. Biol. Chem. 1998, 273:26516-26521.
25. Gaggioli C., Hooper S., Hidalgo-Carcedo C., Grosse R., Marshall J.F., Harrington K., Sahai E. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 2007, 9:1392-1400.
26. Gmyrek G.A., Walburg M., Webb C.P., Yu H.M., You X., Vaughan E.D., Vande Woude G.F., Knudsen B.S. Normal and malignant prostate epithelial cells differ in their response to hepatocyte growth factor/scatter factor. Am. J. Pathol. 2001, 159:579-590.
27. Gregory C.W., Johnson R.T., Mohler J.L., French F.S., Wilson E.M. Androgen receptor stabilization in recurrent prostate cancer is associated with hypersensitivity to low androgen. Cancer Res. 2001, 61:2892-2898.
28. Guerrero-Santoro J., Yang L., Stallcup M.R., Defranco D.B. Distinct LIM domains of Hic-5/ARA55 are required for nuclear matrix targeting and glucocorticoid receptor binding and coactivation. J. Cell Biochem. 2004, 92:810-819.
29. Hayward S.W., Rosen M.A., Cunha G.R. Stromal-epithelial interactions in the normal and neoplastic prostate. Br. J. Urol. 1997, 79(Suppl. 2):18-26.
30. Hayward S.W., Wang Y., Cao M., Hom Y.K., Zhang B., Grossfeld G.D., Sudilovsky D., Cunha G.R. Malignant transformation in a nontumorigenic human prostatic epithelial cell line. Cancer Res. 2001, 61:8135-8142.
31. He B., Kemppainen J.A., Voegel J.J., Gronemeyer H., Wilson E.M. Activation function 2 in the human androgen receptor ligand binding domain mediates interdomain communication with the NH(2)-terminal domain. J. Biol. Chem. 1999, 274:37219-37225.
32. Heitzer M.D., Defranco D.B. Hic-5/ARA55, a LIM domain-containing nuclear receptor coactivator expressed in prostate stromal cells. Cancer Res. 2006, 66:7326-7333.
33. Heitzer M.D., Defranco D.B. Mechanism of action of Hic-5/androgen receptor activator 55, a LIM domain-containing nuclear receptor coactivator. Mol. Endocrinol. 2006, 20:56-64.
34. Heitzer M.D., Defranco D.B. Hic-5/ARA55: a prostate stroma-specific AR coactivator. Steroids 2007, 72:218-220.
35. Henshall S.M., Quinn D.I., Lee C.S., Head D.R., Golovsky D., Brenner P.C., Delprado W., Stricker P.D., Grygiel J.J., Sutherland R.L. Altered expression of androgen receptor in the malignant epithelium and adjacent stroma is associated with early relapse in prostate cancer. Cancer Res. 2001, 61:423-427.
36. Hetey S.E., Lalonde D.P., Turner C.E. Tyrosine-phosphorylated Hic-5 inhibits epidermal growth factor-induced lamellipodia formation. Exp. Cell Res. 2005, 311:147-156.
37. Hidalgo A.A., Montecinos V.P., Paredes R., Godoy A.S., McNerney E.M., Tovar H., Pantoja D., Johnson C., Trump D., Onate S.A. Biochemical characterization of nuclear receptors for vitamin D3 and glucocorticoids in prostate stroma cell microenvironment. Biochem. Biophys. Res. Commun. 2011, 412:13-19.
38. Hidalgo A.A., Paredes R., Garcia V.M., Flynn G., Johnson C.S., Trump D.L., Onate S.A. Altered VDR-mediated transcriptional activity in prostate cancer stroma. J. Steroid Biochem. Mol. Biol. 2007, 103:731-736.
39. Huang Da W., Sherman B.T., Lempicki R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucl. Acids Res. 2009, 37:1-13.
40. Huang Da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
41. Inui S., Itami S., Pan H.J., Chang C. Lack of androgen receptor transcriptional activity in human keratinocytes. J. Dermatol. Sci. 2000, 23:87-92.
42. Jia L., Berman B.P., Jariwala U., Yan X., Cogan J.P., Walters A., Chen T., Buchanan G., Frenkel B., Coetzee G.A. Genomic androgen receptor-occupied regions with different functions, defined by histone acetylation, coregulators and transcriptional capacity. PLoS One 2008, 3:e3645.
43. Kaku N., Matsuda K., Tsujimura A., Kawata M. Characterization of nuclear import of the domain-specific androgen receptor in association with the importin alpha/beta and Ran-guanosine 5'-triphosphate systems. Endocrinology 2008, 149:3960-3969.
44. Kojima S., Mulholland D.J., Ettinger S., Fazli L., Nelson C.C., Gleave M.E. Differential regulation of IGFBP-3 by the androgen receptor in the lineage-related androgen-dependent LNCaP and androgen-independent C4-2 prostate cancer models. Prostate 2006, 66:971-986.
45. Kuperwasser C., Chavarria T., Wu M., Magrane G., Gray J.W., Carey L., Richardson A., Weinberg R.A. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc. Natl. Acad. Sci. USA 2004, 101:4966-4971.
46. Kwabi-Addo B., Ozen M., Ittmann M. The role of fibroblast growth factors and their receptors in prostate cancer. Endocr. Relat. Cancer 2004, 11:709-724.
47. Lapointe J., Li C., Higgins J.P., van de Rijn M., Bair E., Montgomery K., Ferrari M., Egevad L., Rayford W., Bergerheim U., Ekman P., Demarzo A.M., Tibshirani R., Botstein D., Brown P.O., Brooks J.D., Pollack J.R. Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc. Natl. Acad. Sci. USA 2004, 101:811-816.
48. Latulippe E., Satagopan J., Smith A., Scher H., Scardino P., Reuter V., Gerald W.L. Comprehensive gene expression analysis of prostate cancer reveals distinct transcriptional programs associated with metastatic disease. Cancer Res. 2002, 62:4499-4506.
49. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., Fong S.F., Csiszar K., Giaccia A., Weninger W., Yamauchi M., Gasser D.L., Weaver V.M. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
50. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
51. Li P., Yu X., Ge K., Melamed J., Roeder R.G., Wang Z. Heterogeneous expression and functions of androgen receptor co-factors in primary prostate cancer. Am. J. Pathol. 2002, 161:1467-1474.
52. Li X., Martinez-Ferrer M., Botta V., Uwamariya C., Banerjee J., Bhowmick N.A. Epithelial Hic-5/ARA55 expression contributes to prostate tumorigenesis and castrate responsiveness. Oncogene 2011, 30:167-177.
53. Li Y., Li C.X., Ye H., Chen F., Melamed J., Peng Y., Liu J., Wang Z., Tsou H.C., Wei J., Walden P., Garabedian M.J., Lee P. Decrease in stromal androgen receptor associates with androgen-independent disease and promotes prostate cancer cell proliferation and invasion. J. Cell. Mol. Med. 2008, 12:2790-2798.
54. Luo J.H., Yu Y.P., Cieply K., Lin F., Deflavia P., Dhir R., Finkelstein S., Michalopoulos G., Becich M. Gene expression analysis of prostate cancers. Mol. Carcinogen. 2002, 33:25-35.
55. Magee J.A., Araki T., Patil S., Ehrig T., True L., Humphrey P.A., Catalona W.J., Watson M.A., Milbrandt J. Expression profiling reveals hepsin overexpression in prostate cancer. Cancer Res. 2001, 61:5692-5696.
56. Marques R.B., Erkens-Schulze S., de Ridder C.M., Hermans K.G., Waltering K., Visakorpi T., Trapman J., Romijn J.C., van Weerden W.M., Jenster G. Androgen receptor modifications in prostate cancer cells upon long-termandrogen ablation and antiandrogen treatment. Int. J. Cancer 2005, 117:221-229.
57. McEwan I.J., Gustafsson J. Interaction of the human androgen receptor transactivation function with the general transcription factor TFIIF. Proc. Natl. Acad. Sci. USA 1997, 94:8485-8490.
58. Mellor J. Dynamic nucleosomes and gene transcription. Trends Genet. 2006, 22:320-329.
59. Mestayer C., Blanchere M., Jaubert F., Dufour B., Mowszowicz I. Expression of androgen receptor coactivators in normal and cancer prostate tissues and cultured cell lines. Prostate 2003, 56:192-200.
60. Miyoshi Y., Ishiguro H., Uemura H., Fujinami K., Miyamoto H., Kitamura H., Kubota Y. Expression of AR associated protein 55 (ARA55) and androgen receptor in prostate cancer. Prostate 2003, 56:280-286.
61. Mohler J.L., Chen Y., Hamil K., Hall S.H., Cidlowski J.A., Wilson E.M., French F.S., Sar M. Androgen and glucocorticoid receptors in the stroma and epithelium of prostatic hyperplasia and carcinoma. Clin. Cancer Res. 1996, 2:889-895.
62. Need E.F., Scher H.I., Peters A.A., Moore N.L., Cheong A., Ryan C.J., Wittert G.A., Marshall V.R., Tilley W.D., Buchanan G. A novel androgen receptor amino terminal region reveals two classes of amino/carboxyl interaction-deficient variants with divergent capacity to activate responsive sites in chromatin. Endocrinology 2009, 150:2674-2682.
63. Nessler-Menardi C., Jotova I., Culig Z., Eder I.E., Putz T., Bartsch G., Klocker H. Expression of androgen receptor coregulatory proteins in prostate cancer and stromal-cell culture models. Prostate 2000, 45:124-131.
64. Nishiya N., Tachibana K., Shibanuma M., Mashimo J.I., Nose K. Hic-5-reduced cell spreading on fibronectin: competitive effects between paxillin and Hic-5 through interaction with focal adhesion kinase. Mol. Cell Biol. 2001, 21:5332-5345.
65. Niu Y., Xu Y., Zhang J., Bai J., Yang H., Ma T. Proliferation and differentiation of prostatic stromal cells. BJU Int. 2001, 87:386-393.
66. Noguchi F., Inui S., Nakajima T., Itami S. Hic-5 affects proliferation, migration and invasion of B16 murine melanoma cells. Pigment Cell Melanoma Res. 2012, 25:773-782.
67. Olapade-Olaopa E.O., Mackay E.H., Taub N.A., Sandhu D.P., Terry T.R., Habib F.K. Malignant transformation of human prostatic epithelium is associated with the loss of androgen receptor immunoreactivity in the surrounding stroma. Clin. Cancer Res. 1999, 5:569-576.
68. Olapade-Olaopa E.O., Moscatello D.K., Mackay E.H., Sandhu D.P., Terry T.R., Wong A.J., Habib F.K. Alterations in the expression of androgen receptor, wild type-epidermal growth factor receptor and a mutant epidermal growth factor receptor in human prostate cancer. Afr. J. Med. Sci. 2004, 33:245-253.
69. Olapade-Olaopa E.O., Muronda C.A., Mackay E.H., Danso A.P., Sandhu D.P., Terry T.R., Habib F.K. Androgen receptor protein expression in prostatic tissues in Black and Caucasian men. Prostate 2004, 59:460-468.
70. Olumi A.F., Grossfeld G.D., Hayward S.W., Carroll P.R., Tlsty T.D., Cunha G.R. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res. 1999, 59:5002-5011.
71. Ozanne D.M., Brady M.E., Cook S., Gaughan L., Neal D.E., Robson C.N. Androgen receptor nuclear translocation is facilitated by the f-actin cross-linking protein filamin. Mol. Endocrinol. 2000, 14:1618-1626.
72. Palumbo A., Ferreira L.B., Reis De Souza P.A., Oliveira F.L., Pontes B., Viana N.B., Machado D.E., Palmero C.Y., Alves L.M., Gimba E.R., Nasciutti L.E. Extracellular matrix secreted by reactive stroma is a main inducer of pro-tumorigenic features on LNCaP prostate cancer cells. Cancer Lett. 2012, 321:55-64.
73. Pignatelli J., Tumbarello D.A., Schmidt R.P., Turner C.E. Hic-5 promotes invadopodia formation and invasion during TGF-beta-induced epithelial-mesenchymal transition. J. Cell Biol. 2012, 197:421-437.
74. Rahman M.M., Miyamoto H., Lardy H., Chang C. Inactivation of androgen receptor coregulator ARA55 inhibits androgen receptor activity and agonist effect of antiandrogens in prostate cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100:5124-5129.
75. Ricciardelli C., Choong C.S., Buchanan G., Vivekanandan S., Neufing P., Stahl J., Marshall V.R., Horsfall D.J., Tilley W.D. Androgen receptor levels in prostate cancer epithelial and peritumoral stromal cells identify non-organ confined disease. Prostate 2005, 63:19-28.
76. Ricke E.A., Williams K., Lee Y.F., Couto S., Wang Y., Hayward S.W., Cunha G.R., Ricke W.A. Androgen hormone action in prostatic carcinogenesis: stromal androgen receptors mediate prostate cancer progression, malignant transformation and metastasis. Carcinogenesis 2012.
77. Risbridger G.P., Taylor R.A. Minireview: regulation of prostatic stem cells by stromal niche in health and disease. Endocrinology 2008, 149:4303-4306.
78. Saelzler M.P., Spackman C.C., Liu Y., Martinez L.C., Harris J.P., Abe M.K. ERK8 down-regulates transactivation of the glucocorticoid receptor through Hic-5. J. Biol. Chem. 2006, 281:16821-16832.
79. Shaw A., Papadopoulos J., Johnson C., Bushman W. Isolation and characterization of an immortalized mouse urogenital sinus mesenchyme cell line. Prostate 2006, 66:1347-1358.
80. Shibanuma M., Kim-Kaneyama J.R., Ishino K., Sakamoto N., Hishiki T., Yamaguchi K., Mori K., Mashimo J., Nose K. Hic-5 communicates between focal adhesions and the nucleus through oxidant-sensitive nuclear export signal. Mol. Biol. Cell 2003, 14:1158-1171.
81. Shibanuma M., Kim-Kaneyama J.R., Sato S., Nose K. A LIM protein, Hic-5, functions as a potential coactivator for Sp1. J. Cell Biochem. 2004, 91:633-645.
82. Shibanuma M., Mashimo J., Kuroki T., Nose K. Characterization of the TGF beta 1-inducible hic-5 gene that encodes a putative novel zinc finger protein and its possible involvement in cellular senescence. J. Biol. Chem. 1994, 269:26767-26774.
83. Singh D., Febbo P.G., Ross K., Jackson D.G., Manola J., Ladd C., Tamayo P., Renshaw A.A., D'Amico A.V., Richie J.P., Lander E.S., Loda M., Kantoff P.W., Golub T.R., Sellers W.R. Gene expression correlates of clinical prostate cancer behavior. Cancer Cell 2002, 1:203-209.
84. Smith D.F., Toft D.O. Steroid receptors and their associated proteins. Mol. Endocrinol. 1993, 7:4-11.
85. Suzuki K., Bose P., Leong-Quong R.Y., Fujita D.J., Riabowol K. REAP: a two minute cell fractionation method. BMC Res. Notes 2010, 3:294.
86. Trotta A.P., Need E.F., Butler L.M., Selth L.A., O'Loughlin M.A., Coetzee G.A., Tilley W.D., Buchanan G. Subdomain structure of the co-chaperone SGTA and activity of its androgen receptor client. J. Mol. Endocrinol. 2012, 49:57-68.
87. Tumbarello D.A., Brown M.C., Hetey S.E., Turner C.E. Regulation of paxillin family members during epithelial-mesenchymal transformation: a putative role for paxillin delta. J. Cell Sci. 2005, 118:4849-4863.
88. Tumbarello D.A., Turner C.E. Hic-5 contributes to epithelial-mesenchymal transformation through a RhoA/ROCK-dependent pathway. J. Cell Physiol. 2007, 211:736-747.
89. Tuxhorn J.A., Ayala G.E., Rowley D.R. Reactive stroma in prostate cancer progression. J. Urol. 2001, 166:2472-2483.
90. Tuxhorn J.A., Ayala G.E., Smith M.J., Smith V.C., Dang T.D., Rowley D.R. Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodeling. Clin. Cancer Res. 2002, 8:2912-2923.
91. Uhlen M., Bjorling E., Agaton C., Szigyarto C.A., Amini B., Andersen E., Andersson A.C., Angelidou P., Asplund A., Asplund C., Berglund L., Bergstrom K., Brumer H., Cerjan D., Ekstrom M., Elobeid A., Eriksson C., Fagerberg L., Falk R., Fall J., Forsberg M., Bjorklund M.G., Gumbel K., Halimi A., Hallin I., Hamsten C., Hansson M., Hedhammar M., Hercules G., Kampf C., Larsson K., Lindskog M., Lodewyckx W., Lund J., Lundeberg J., Magnusson K., Malm E., Nilsson P., Odling J., Oksvold P., Olsson I., Oster E., Ottosson J., Paavilainen L., Persson A., Rimini R., Rockberg J., Runeson M., Sivertsson A., Skollermo A., Steen J., Stenvall M., Sterky F., Stromberg S., Sundberg M., Tegel H., Tourle S., Wahlund E., Walden A., Wan J., Wernerus H., Westberg J., Wester K., Wrethagen U., Xu L.L., Hober S., Ponten F. A Human Protein Atlas for normal and cancer tissues based on antibody proteomics. Mol. Cell Proteomics 2005, 4:1920-1932.
92. Uhlen M., Oksvold P., Fagerberg L., Lundberg E., Jonasson K., Forsberg M., Zwahlen M., Kampf C., Wester K., Hober S., Wernerus H., Bjorling L., Ponten F. Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol. 2010, 28:1248-1250.
93. Wang Y., Mikhailova M., Bose S., Pan C.X., Devere White R.W., Ghosh P.M. Regulation of androgen receptor transcriptional activity by rapamycin in prostate cancer cell proliferation and survival. Oncogene 2008, 27:7106-7117.
94. Wang Y., Sudilovsky D., Zhang B., Haughney P.C., Rosen M.A., Wu D.S., Cunha T.J., Dahiya R., Cunha G.R., Hayward S.W. A human prostatic epithelial model of hormonal carcinogenesis. Cancer Res. 2001, 61:6064-6072.
95. Webber M.M., Trakul N., Thraves P.S., Bello-Deocampo D., Chu W.W., Storto P.D., Huard T.K., Rhim J.S., Williams D.E. A human prostatic stromal myofibroblast cell line WPMY-1: a model for stromal-epithelial interactions in prostatic neoplasia. Carcinogenesis 1999, 20:1185-1192.
96. Welsh J.B., Sapinoso L.M., Su A.I., Kern S.G., Wang-Rodriguez J., Moskaluk C.A., Frierson H.F., Hampton G.M. Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Res. 2001, 61:5974-5978.
97. Wikstrom P., Marusic J., Stattin P., Bergh A. Low stroma androgen receptor level in normal and tumor prostate tissue is related to poor outcome in prostate cancer patients. Prostate 2009, 69:799-809.
98. Wu H.C., Hsieh J.T., Gleave M.E., Brown N.M., Pathak S., Chung L.W. Derivation of androgen-independent human LNCaP prostatic cancer cell sublines: role of bone stromal cells. Int. J. Cancer 1994, 57:406-412.
99. Wu R.F., Xu Y.C., Ma Z., Nwariaku F.E., Sarosi G.A., Terada L.S. Subcellular targeting of oxidants during endothelial cell migration. J. Cell Biol. 2005, 171:893-904.
100. Yang L., Guerrero J., Hong H., Defranco D.B., Stallcup M.R. Interaction of the tau2 transcriptional activation domain of glucocorticoid receptor with a novel steroid receptor coactivator, Hic-5, which localizes to both focal adhesions and the nuclear matrix. Mol. Biol. Cell 2000, 11:2007-2018.
101. Yang N.Q., Li R.S., Li D., Sha J.J., Li P., Wang Y.X. Expression of ARA55 mRNA in prostate carcinoma tissues and its significance. Zhonghua Nan Ke Xue 2007, 13:696-699.
102. Yeh S., Chang H.C., Miyamoto H., Takatera H., Rahman M., Kang H.Y., Thin T.H., Lin H.K., Chang C. Differential induction of the androgen receptor transcriptional activity by selective androgen receptor coactivators. Keio J. Med. 1999, 48:87-92.
103. Yeh S., Kang H.Y., Miyamoto H., Nishimura K., Chang H.C., Ting H.J., Rahman M., Lin H.K., Fujimoto N., Hu Y.C., Mizokami A., Huang K.E., Chang C. Differential induction of androgen receptor transactivation by different androgen receptor coactivators in human prostate cancer DU145 cells. Endocrine 1999, 11:195-202.
104. Yu Y.P., Landsittel D., Jing L., Nelson J., Ren B., Liu L., McDonald C., Thomas R., Dhir R., Finkelstein S., Michalopoulos G., Becich M., Luo J.H. Gene expression alterations in prostate cancer predicting tumor aggression and preceding development of malignancy. J. Clin. Oncol. 2004, 22:2790-2799.