Enhancing the effectiveness of androgen deprivation in prostate cancer by inducing Filamin A nuclear localization

Endocrine-Related Cancer

Volumn 19, Issue 6, 2012, Pages 759-777

  Mooso, Benjamin A ^a,b   Vinall, Ruth L ^b,d   Tepper, Clifford G ^b   Savoy, Rosalinda M ^b   Cheung, Jean P ^b   Singh, Sheetal ^a,b   Siddiqui, Salma ^a   Wang, Yu ^b,e   Bedolla, Roble G ^c   Martinez, Anthony ^b   Mudryj, Maria ^a,b   Kung, Hsing Jien ^b   DeVere White, Ralph W ^b   Ghosh, Paramita M ^a,b  

^a VA NORTHERN CALIFORNIA HEALTH CARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d California Northstate College of Pharmacy   (United States)

^e LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DAIDZEIN; FILAMIN A; GENISTEIN; POLYSACCHARIDE;

ADVANCED CANCER; ANDROGEN DEPRIVATION THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER RECURRENCE; CASTRATION; CELL CYCLE ARREST; CONTROLLED STUDY; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PROSTATE CANCER; PROTEIN PHOSPHORYLATION; TUMOR XENOGRAFT;

ANDROGEN ANTAGONISTS; ANDROGENS; ANILIDES; ANIMALS; APOPTOSIS; CASTRATION; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL NUCLEUS; FILAMINS; GENISTEIN; MALE; MICE; MICE, NUDE; NITRILES; POLYSACCHARIDES; PROSTATIC NEOPLASMS; TOSYL COMPOUNDS; TUMOR BURDEN;

EID: 84869219105     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-12-0171     Document Type: Article

References (69)

1. Aggarwal BB & Shishodia S 2006 Molecular targets of dietary agents for prevention and therapy of cancer. Biochemical Pharmacology 71 1397-1421. (doi:10.1016/j.bcp.2006.02.009)
2. Agus DB, Cordon-Cardo C, Fox W, Drobnjak M, Koff A, Golde DW & Scher HI 1999 Prostate cancer cell cycle regulators: response to androgen withdrawal and development of androgen independence. Journal of the National Cancer Institute 91 1869-1876. (doi:10.1093/jnci/91.21.1869)
3. Agus DB, Akita RW, Fox WD, Lewis GD, Higgins B, Pisacane PI, Lofgren JA, Tindell C, Evans DP, Maiese K et al. 2002 Targeting ligand-activated ErbB2 signaling inhibits breast and prostate tumor growth. Cancer Cell 2 127-137. (doi:10.1016/S1535-6108(02)00097-1)
4. Anastasius N, Boston S, LaceyM, Storing N & Whitehead SA 2009 Evidence that low-dose, long-term genistein treatment inhibits oestradiol-stimulated growth in MCF-7 cells by down-regulation of the PI3-kinase/Akt signalling pathway. Journal of Steroid Biochemistry andMolecular Biology 116 50-55. (doi:10.1016/j.jsbmb.2009.04.009)
5. Bedolla RG, Wang Y, Asuncion A, Chamie K, Siddiqui S, Mudryj MM, Prihoda TJ, Siddiqui J, Chinnaiyan AM, MehraRet al. 2009 Nuclear versus cytoplasmic localization of filamin A in prostate cancer: immunohistochemical correlation with metastases. Clinical Cancer Research 15 788-796. (doi:10.1158/1078-0432. CCR-08-1402)
6. Bemis DL, Capodice JL, Desai M, Buttyan R & Katz AE 2004 A concentrated aglycone isoflavone preparation (GCP) that demonstrates potent anti-prostate cancer activity in vitro and in vivo. Clinical Cancer Research 10 5282-5292. (doi:10.1158/1078-0432.CCR-03-0828)
7. Burich RA, Holland WS, Vinall RL, Tepper C, White RW &Mack PC 2008 Genistein combined polysaccharide enhances activity of docetaxel, bicalutamide and Src kinase inhibition in androgen-dependent and independent prostate cancer cell lines. BJU International 102 1458-1466. (doi:10.1111/j.1464-410X.2008. 07826.x)
8. Cai C, Chen S, Ng P, Bubley GJ, Nelson PS, Mostaghel EA, Marck B, Matsumoto AM, Simon NI, Wang H et al. 2011 Intratumoral de novo steroid synthesis activates androgen receptor in castration-resistant prostate cancer and is upregulated by treatment with CYP17A1 inhibitors. Cancer Research 71 6503-6513. (doi:10.1158/0008-5472.CAN-11-0532)
9. Carriere A, Cargnello M, Julien LA, Gao H, Bonneil E, Thibault P & Roux PP 2008 Oncogenic MAPK signaling stimulates mTORC1 activity by promoting RSK-mediated raptor phosphorylation. Current Biology 18 1269-1277. (doi:10.1016/j.cub.2008.07.078)
10. Catalona WJ 1994 Management of cancer of the prostate. New England Journal of Medicine 331 996-1004. (doi:10.1056/NEJM199410133311507)
11. Chen H, Libertini SJ, George M, Dandekar S, Tepper CG, Al-Bataina B, Kung HJ, Ghosh PM & Mudryj M 2010a Genome-wide analysis of androgen receptor binding and gene regulation in two CWR22-derived prostate cancer cell lines. Endocrine-Related Cancer 17 857-873. (doi:10.1677/ERC-10-0081)
12. Chen H, Libertini SJ, Wang Y, Kung HJ, Ghosh P & MudryjM 2010b ERK regulates calpain 2-induced androgen receptor proteolysis in CWR22 relapsed prostate tumor cell lines. Journal of Biological Chemistry 285 2368-2374. (doi:10.1074/jbc.M109.049379)
13. Chen L, Siddiqui S, Bose S, Mooso B, Asuncion A, Bedolla RG, Vinall R, Tepper CG, Gandour-Edwards R, Shi X et al. 2010c Nrdp1-mediated regulation of ErbB3 expression by the androgen receptor in androgen-dependent but not castrate-resistant prostate cancer cells. Cancer Research 70 5994-6003. (doi:10.1158/0008-5472.CAN-09-4440)
14. Chen L, Mooso BA, Jathal MK, Madhav A, Johnson SD, van Spyk E, Mikhailova M, Zierenberg-Ripoll A, Xue L, Vinall RL et al. 2011 Dual EGFR/HER2 inhibition sensitizes prostate cancer cells to androgen withdrawal by suppressing ErbB3. Clinical Cancer Research 17 6218-6228. (doi:10.1158/1078-0432.CCR-11-1548)
15. D'Addario M, Arora PD, Ellen RP & McCulloch CA 2002 Interaction of p38 and Sp1 in a mechanical force-induced, β 1 integrin-mediated transcriptional circuit that regulates the actin-binding protein filamin-A. Journal of Biological Chemistry 277 47541-47550. (doi:10.1074/jbc.M207681200)
16. Das M, Ithychanda SS, Qin J & Plow EF 2011 Migfilin and filamin as regulators of integrin activation in endothelial cells and neutrophils. PLoS ONE 6 e26355. (doi:10.1371/journal.pone.0026355)
17. Deng W,Lopez-CamachoC,Tang JY,Mendoza-Villanueva D, Maya-Mendoza A, Jackson DA & Shore P 2012 Cytoskeletal protein filamin A is a nucleolar protein that suppresses ribosomal RNA gene transcription. PNAS 109 1524-1529. (doi:10.1073/pnas.1107879109)
18. Feldman BJ & Feldman D 2001 The development of androgen-independent prostate cancer. Nature Reviews. Cancer 1 34-45. (doi:10.1038/35094009)
19. Feng Y & Walsh CA 2004 The many faces of filamin: a versatile molecular scaffold for cell motility and signalling. Nature Cell Biology 6 1034-1038. (doi:10.1038/ncb1104-1034)
20. van der Flier A & Sonnenberg A 2001 Structural and functional aspects of filamins. Biochimica et Biophysica Acta 1538 99-117. (doi:10.1016/S0167- 4889(01)00072-6)
21. Gawecka JE, Griffiths GS, Ek-Rylander B, Ramos JW & Matter ML 2010 R-Ras regulates migration through an interaction with filamin A in melanoma cells. PLoS ONE 5 e11269. (doi:10.1371/journal.pone.0011269)
22. Ghafar MA, Golliday E, Bingham J, Mansukhani MM, Anastasiadis AG & Katz AE 2002 Regression of prostate cancer following administration of genistein combined polysaccharide (GCP), a nutritional supplement: a case report. Journal of Alternative and Complementary Medicine 8 493-497. (doi:10.1089/ 107555302760253694)
23. Ghosh PM, Malik SN, Bedolla RG, Wang Y, Mikhailova M, Prihoda TJ, Troyer DA & Kreisberg JI 2005 Signal transduction pathways in androgen-dependent and -independent prostate cancer cell proliferation. Endocrine-Related Cancer 12 119-134. (doi:10.1677/erc.1.00835)
24. Gorlin JB, Yamin R, Egan S, Stewart M, Stossel TP, Kwiatkowski DJ & Hartwig JH 1990 Human endothelial actin-binding protein (ABP-280, nonmuscle filamin): a molecular leaf spring. Journal of Cell Biology 111 1089-1105. (doi:10.1083/jcb.111.3.1089)
25. Gwin J, Drews N, Ali S, Stamschror J, Sorenson M & Rajah TT 2011 Effect of genistein on p90RSK phosphorylation and cell proliferation in T47D breast cancer cells. Anticancer Research 31 209-214.
26. Han H, Zhong C, Zhang X, Liu R, Pan M, Tan L, Li Y, Wu J, Zhu Y & Huang W 2010 Genistein induces growth inhibition and G2/M arrest in nasopharyngeal carcinoma cells. Nutrition and Cancer 62 641-647. (doi:10.1080/01635581003605490)
27. Hofman K, Swinnen JV, Verhoeven G & Heyns W 2001 E2F activity is biphasically regulated by androgens in LNCaP cells. Biochemical and Biophysical Research Communications 283 97-101. (doi:10.1006/bbrc.2001.4738)
28. Jay D, Garcia EJ, Lara JE, Medina MA & de la Luz Ibarra M 2000 Determination of a cAMP-dependent protein kinase phosphorylation site in the C-terminal region of human endothelial actin-binding protein. Archives of Biochemistry and Biophysics 377 80-84. (doi:10.1006/abbi.2000.1762)
29. Jay D, Garcia EJ & de la Luz Ibarra M 2004 In situ determination of a PKA phosphorylation site in the C-terminal region of filamin. Molecular and Cellular Biochemistry 260 49-53. (doi:10.1023/B:MCBI.0000026052.76418.55)
30. Kang NJ, LeeKW, Rogozin EA, Cho YY, Heo YS, Bode AM, Lee HJ & Dong Z 2007 Equol, a metabolite of the soybean isoflavone daidzein, inhibits neoplastic cell transformation by targeting the MEK/ERK/p90RSK/activator protein-1 pathway. Journal of Biological Chemistry 282 32856-32866. (doi:10.1074/jbc. M701459200)
31. Kuil CW, Berrevoets CA & Mulder E 1995 Ligand-induced conformational alterations of the androgen receptor analyzed by limited trypsinization. Studies on the mechanism of antiandrogen action. Journal of Biological Chemistry 270 27569-27576. (doi:10.1074/jbc.270.46.27569)
32. Lakshman M, Xu L, Ananthanarayanan V, Cooper J, Takimoto CH, Helenowski I, Pelling JC & Bergan RC 2008 Dietary genistein inhibits metastasis of human prostate cancer in mice. Cancer Research 68 2024-2032. (doi:10.1158/0008-5472.CAN-07-1246)
33. Laschak M, Bechtel M, Spindler KD & Hessenauer A 2011 Inability of NCoR/SMRT to repress androgen receptor transcriptional activity in prostate cancer cell lines. International Journal of Molecular Medicine 28 645-651. (doi:10.3892/ijmm.2011.735)
34. Lian F, Bhuiyan M, Li YW, Wall N, Kraut M & Sarkar FH 1998 Genistein-induced G2-M arrest, p21WAF1 upregulation, and apoptosis in a non-small-cell lung cancer cell line. Nutrition and Cancer 31 184-191. (doi:10.1080/01635589809514701)
35. Limpens J, Schroder FH, de Ridder CM, Bolder CA, Wildhagen MF, Obermuller-Jevic UC, Kramer K &van Weerden WM 2006 Combined lycopene and vitamin E treatment suppresses the growth of PC-346C human prostate cancer cells in nude mice. Journal of Nutrition 136 1287-1293.
36. Loy CJ, Sim KS & Yong EL 2003 Filamin-A fragment localizes to the nucleus to regulate androgen receptor and coactivator functions. PNAS 100 4562-4567. (doi:10.1073/pnas.0736237100)
37. Martinez-Montemayor MM, Otero-Franqui E, Martinez J, De La Mota-Peynado A, Cubano LA & Dharmawardhane S 2010 Individual and combined soy isoflavones exert differential effects on metastatic cancer progression. Clinical & Experimental Metastasis 27 465-480. (doi:10.1007/s10585-010-9336-x)
38. Masiello D, Cheng S, Bubley GJ, Lu ML & Balk SP 2002 Bicalutamide functions as an androgen receptor antagonist by assembly of a transcriptionally inactive receptor. Journal of Biological Chemistry 277 26321-26326. (doi:10.1074/jbc.M203310200)
39. Matsushima H, Goto T, Hosaka Y, Kitamura T & Kawabe K 1999 Correlation between proliferation, apoptosis, and angiogenesis in prostate carcinoma and their relation to androgen ablation. Cancer 85 1822-1827. (doi:10.1002/(SICI)1097-0142(19990415)85:8〈1822::AID-CNCR24〉3.0. CO;2-1)
40. Murphy WM, Soloway MS & Barrows GH 1991 Pathologic changes associated with androgen deprivation therapy for prostate cancer. Cancer 68 821-828. (doi:10.1002/1097-0142(19910815)68:4〈821::AID-CNCR2820680426〉3.0. CO;2-S)
41. Nagano T, Yoneda T, Hatanaka Y, Kubota C, Murakami F & Sato M 2002 Filamin A-interacting protein (FILIP) regulates cortical cell migration out of the ventricular zone. Nature Cell Biology 4 495-501. (doi:10.1038/ncb808)
42. Nakamura H, Wang Y, Kurita T, Adomat H & Cunha GR 2011 Genistein increases epidermal growth factor receptor signaling and promotes tumor progression in advanced human prostate cancer. PLoS ONE 6 e20034. (doi:10.1371/journal.pone.0020034)
43. Ohta Y & Hartwig JH 1995 Actin filament cross-linking by chicken gizzard filamin is regulated by phosphorylation in vitro. Biochemistry 34 6745-6754. (doi:10.1021/bi00020a020)
44. Ott I, Fischer EG, Miyagi Y, Mueller BM & Ruf W 1998 A role for tissue factor in cell adhesion and migration mediated by interaction with actin-binding protein 280. Journal of Cell Biology 140 1241-1253. (doi:10.1083/jcb.140.5.1241)
45. Ozanne DM, Brady ME, Cook S, Gaughan L, Neal DE & Robson CN 2000 Androgen receptor nuclear translocation is facilitated by the f-actin cross-linking protein filamin. Molecular Endocrinology 14 1618-1626. (doi:10.1210/me.14.10.1618)
46. Paprotka T, Delviks-Frankenberry KA, Cingoz O, Martinez A, Kung HJ, Tepper CG, Hu WS, Fivash MJ Jr, Coffin JM & Pathak VK 2011 Recombinant origin of the retrovirus XMRV. Science 333 97-101. (doi:10.1126/science.1205292)
47. Pavese JM, Farmer RL & Bergan RC 2010 Inhibition of cancer cell invasion and metastasis by genistein. Cancer Metastasis Reviews 29 465-482. (doi:10.1007/s10555-010-9238-z)
48. Robertson SP, Twigg SR, Sutherland-Smith AJ, Biancalana V, Gorlin RJ, Horn D, Kenwrick SJ, Kim CA, Morava E, Newbury-Ecob R et al. 2003 Localized mutations in the gene encoding the cytoskeletal protein filamin A cause diverse malformations in humans. Nature Genetics 33 487-491. (doi:10.1038/ng1119)
49. Roux PP, Shahbazian D, Vu H, Holz MK, Cohen MS, Taunton J, Sonenberg N & Blenis J 2007 RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. Journal of Biological Chemistry 282 14056-14064. (doi:10.1074/jbc.M700906200)
50. Schmidt F, Knobbe CB, Frank B, Wolburg H & Weller M 2008 The topoisomerase II inhibitor, genistein, induces G2/M arrest and apoptosis in human malignant glioma cell lines. Oncology Reports 19 1061-1066. (Pubitemid 351802681)
51. Sedelaar JP & Isaacs JT 2009 Tissue culture media supplemented with 10% fetal calf serum contains a castrate level of testosterone. Prostate 69 1724-1729. (doi:10.1002/pros.21028)
52. Sfanos KS, Aloia AL, Hicks JL, Esopi DM, Steranka JP, Shao W, Sanchez-Martinez S, Yegnasubramanian S, Burns KH, Rein A et al. 2011 Identification of replication competent murine gammaretroviruses in commonly used prostate cancer cell lines. PLoS ONE 6 e20874. (doi:10.1371/journal.pone. 0020874)
53. Singh-Gupta V, Zhang H, Yunker CK, Ahmad Z, Zwier D, Sarkar FH & Hillman GG 2010 Daidzein effect on hormone refractory prostate cancer in vitro and in vivo compared to genistein and soy extract: potentiation of radiotherapy. Pharmaceutical Research 27 1115-1127. (doi:10.1007/s11095-010-0107-9)
54. Tepper CG, Boucher DL, Ryan PE, Ma AH, Xia L, Lee LF, Pretlow TG & Kung HJ 2002 Characterization of a novel androgen receptor mutation in a relapsed CWR22 prostate cancer xenograft and cell line. Cancer Research 62 6606-6614. (Pubitemid 35364127)
55. Tepper CG, Vinall RL, Wee CB, Xue L, Shi XB, Burich R, Mack PC & deVere White RW 2007 GCP-mediated growth inhibition and apoptosis of prostate cancer cells via androgen receptor-dependent and -independent mechanisms. Prostate 67 521-535. (doi:10.1002/pros.20548)
56. Thalmann GN, Anezinis PE, Chang SM, Zhau HE, Kim EE, Hopwood VL, Pathak S, von Eschenbach AC & Chung LW 1994 Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Research 54 2577-2581. (Pubitemid 24173741)
57. Tigges U, Koch B, Wissing J, Jockusch BM & Ziegler WH 2003 The F-actin cross-linking and focal adhesion protein filamin A is a ligand and in vivo substrate for protein kinase C α. Journal of Biological Chemistry 278 23561-23569. (doi:10.1074/jbc.M302302200)
58. Travis MA, van der Flier A, Kammerer RA, Mould AP, Sonnenberg A & Humphries MJ 2004 Interaction of filamin A with the integrin β 7 cytoplasmic domain: role of alternative splicing and phosphorylation. FEBS Letters 569 185-190. (doi:10.1016/j.febslet.2004.04.099)
59. Vinall RL, Hwa K, Ghosh P, Pan CX, Lara PN Jr &deVere White RW 2007 Combination treatment of prostate cancer cell lines with bioactive soy isoflavones and perifosine causes increased growth arrest and/or apoptosis. Clinical Cancer Research 13 6204-6216. (doi:10.1158/1078-0432.CCR-07-0600)
60. Wang Y, Kreisberg JI, Bedolla RG, Mikhailova M, deVere White RW & Ghosh PM 2007 A 90 kDa fragment of filamin A promotes Casodex-induced growth inhibition in Casodex-resistant androgen receptor positive C4-2 prostate cancer cells. Oncogene 26 6061-6070. (doi:10.1038/sj.onc.1210435)
61. van Weerden WM, de Ridder CM, Verdaasdonk CL, Romijn JC, van der Kwast TH, Schroder FH &van Steenbrugge GJ 1996 Development of seven new human prostate tumor xenograft models and their histopathological characterization. American Journal of Pathology 149 1055-1062. (Pubitemid 26334187)
62. Westin P, Stattin P, Damber JE & Bergh A 1995 Castration therapy rapidly induces apoptosis in a minority and decreases cell proliferation in a majority of human prostatic tumors. American Journal of Pathology 146 1368-1375.
63. deVere White RW, Hackman RM, Soares SE, Beckett LA, Li Y & Sun B 2004 Effects of a genistein-rich extract on PSA levels in men with a history of prostate cancer. Urology 63 259-263. (doi:10.1016/j.urology.2003.09.061)
64. deVere White RW, Tsodikov A, Stapp EC, Soares SE, Fujii H & Hackman RM 2010 Effects of a high dose, aglycone-rich soy extract on prostate-specific antigen and serum isoflavone concentrations in men with localized prostate cancer. Nutrition and Cancer 62 1036-1043. (doi:10.1080/01635581.2010.492085)
65. Woo MS, Ohta Y, Rabinovitz I, Stossel TP & Blenis J 2004 Ribosomal S6 kinase (RSK) regulates phosphorylation of filamin A on an important regulatory site. Molecular and Cellular Biology 24 3025-3035. (doi:10.1128/MCB.24.7.3025- 3035.2004)
66. Xu Y, Bismar TA, Su J, Xu B, Kristiansen G, Varga Z, Teng L, Ingber DE, Mammoto A, Kumar R et al. 2010 Filamin A regulates focal adhesion disassembly and suppresses breast cancer cell migration and invasion. Journal of Experimental Medicine 207 2421-2437. (doi:10.1084/jem.20100433)
67. Zhang Y, Zhong S, Dong Z, Chen N, Bode AM & Ma W 2001 UVA induces Ser381 phosphorylation of p90RSK/MAPKAP-K1 via ERK and JNK pathways. Journal of Biological Chemistry 276 14572-14580. (doi:10.1074/jbc.M004615200)
68. Zhang Y, Zhu G, Gu S, Chen X, Hu H & Weng S 2010 Genistein inhibits osteolytic bone metastasis and enhances bone mineral in nude mice. Environmental Toxicology and Pharmacology 30 37-44. (doi:10.1016/j.etap.2010.03.016)
69. Zhao R, Xiang N, Domann FE & Zhong W 2009 Effects of selenite and genistein on G2/M cell cycle arrest and apoptosis in human prostate cancer cells. Nutrition and Cancer 61 397-407. (doi:10.1080/01635580802582751)