The chemopreventive retinoid 4HPR impairs prostate cancer cell migration and invasion by interfering with FAK/AKT/GSK3β pathway and β-catenin stability

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Benelli, Roberto ^a   Monteghirfo, Stefano ^a   Venè, Roberta ^a   Tosetti, Francesca ^a   Ferrari, Nicoletta ^a  

^a UNIVERSITY OF GENOA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN 2; CYCLIN D1; FENRETINIDE; FOCAL ADHESION KINASE; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE B; SOMATOMEDIN C; SURVIVIN; VASCULOTROPIN; ANTINEOPLASTIC AGENT; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA;

ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO CULTURE; PHENOTYPE; PROSTATE CANCER; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN SYNTHESIS INHIBITION; SIGNAL TRANSDUCTION; UPREGULATION; BIOSYNTHESIS; CANCER INVASION; ENZYMOLOGY; GENE SILENCING; GENETICS; MALE; METABOLISM; METASTASIS; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE; WESTERN BLOTTING;

ANTICARCINOGENIC AGENTS; BETA CATENIN; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN 2; CELL LINE, TUMOR; FENRETINIDE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE SILENCING; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MALE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 77953257323     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-142     Document Type: Article

References (51)

1. Hail N, Kim HJ, Lotan R. Mechanisms of fenretinide-induced apoptosis. Apoptosis 2006, 11:1677-1694. 10.1007/s10495-006-9289-3, 16850162.
2. Takahashi N, Watanabe Y, Maitani Y, Yamauchi T, Higashiyama K, Ohba T. p-Dodecylaminophenol derived from the synthetic retinoid, fenretinide: antitumor efficacy in vitro and in vivo against human prostate cancer and mechanism of action. Int J Cancer 2008, 122:689-698. 10.1002/ijc.23154, 17955489.
3. Shaker MR, Yang G, Timme TL, Park SH, Kadmon D, Ren C, Ji X, Lee HM, Sehgal I, Anzano M, et al. Dietary 4-HPR suppresses the development of bone metastasis in vivo in a mouse model of prostate cancer progression. Clin Exp Metastasis 2000, 18:429-438. 10.1023/A:1010905309570, 11467776.
4. Pienta KJ, Nguyen NM, Lehr JE. Treatment of prostate cancer in the rat with the synthetic retinoid fenretinide. Cancer Res 1993, 53:224-226.
5. Pollard M, Luckert PH, Sporn MB. Prevention of primary prostate cancer in Lobund-Wistar rats by N-(4-hydroxyphenyl)retinamide. Cancer Res 1991, 51:3610-3611.
6. Slawin K, Kadmon D, Park SH, Scardino PT, Anzano M, Sporn MB, Thompson TC. Dietary fenretinide, a synthetic retinoid, decreases the tumor incidence and the tumor mass of ras+myc-induced carcinomas in the mouse prostate reconstitution model system. Cancer Res 1993, 53:4461-4465.
7. Hsieh TC, Ng C, Wu JM. The synthetic retinoid N-(4-hydroxyphenyl) retinamide (4-HPR) exerts antiproliferative and apoptosis-inducing effects in the androgen-independent human prostatic JCA-1 cells. Biochem Mol Biol Int 1995, 37:499-506.
8. Igawa M, Tanabe T, Chodak GW, Rukstalis DB. N-(4-hydroxyphenyl) retinamide induces cell cycle specific growth inhibition in PC3 cells. Prostate 1994, 24:299-305. 10.1002/pros.2990240605, 8208624.
9. Sun SY, Yue P, Lotan R. Induction of apoptosis by N-(4-hydroxyphenyl)retinamide and its association with reactive oxygen species, nuclear retinoic acid receptors, and apoptosis-related genes in human prostate carcinoma cells. Mol Pharmacol 1999, 55:403-410.
10. Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, Wilkinson P, Hennekens CH, Pollak M. Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 1998, 279:563-566. 10.1126/science.279.5350.563, 9438850.
11. Stattin P, Bylund A, Rinaldi S, Biessy C, Dechaud H, Stenman UH, Egevad L, Riboli E, Hallmans G, Kaaks R. Plasma insulin-like growth factor-I, insulin-like growth factor-binding proteins, and prostate cancer risk: a prospective study. J Natl Cancer Inst 2000, 92:1910-1917. 10.1093/jnci/92.23.1910, 11106682.
12. Shishodia S, Gutierrez AM, Lotan R, Aggarwal BB. N-(4-hydroxyphenyl)retinamide inhibits invasion, suppresses osteoclastogenesis, and potentiates apoptosis through down-regulation of I(kappa)B(alpha) kinase and nuclear factor-kappaB-regulated gene products. Cancer Res 2005, 65:9555-9565. 10.1158/0008-5472.CAN-05-1585, 16230421.
13. Ferrari N, Morini M, Pfeffer U, Minghelli S, Noonan DM, Albini A. Inhibition of Kaposi's sarcoma in vivo by fenretinide. Clin Cancer Res 2003, 9:6020-6029.
14. Ferrari N, Pfeffer U, Dell'Eva R, Ambrosini C, Noonan DM, Albini A. The transforming growth factor-beta family members bone morphogenetic protein-2 and macrophage inhibitory cytokine-1 as mediators of the antiangiogenic activity of N-(4-hydroxyphenyl)retinamide. Clin Cancer Res 2005, 11:4610-4619. 10.1158/1078-0432.CCR-04-2210, 15958647.
15. Tosetti F, Vene R, Arena G, Morini M, Minghelli S, Noonan DM, Albini A. N-(4-hydroxyphenyl)retinamide inhibits retinoblastoma growth through reactive oxygen species-mediated cell death. Mol Pharmacol 2003, 63:565-573. 10.1124/mol.63.3.565, 12606763.
16. Ribatti D, Alessandri G, Baronio M, Raffaghello L, Cosimo E, Marimpietri D, Montaldo PG, De Falco G, Caruso A, Vacca A, Ponzoni M. Inhibition of neuroblastoma-induced angiogenesis by fenretinide. Int J Cancer 2001, 94:314-321. 10.1002/ijc.1441, 11745408.
17. Appierto V, Cavadini E, Pergolizzi R, Cleris L, Lotan R, Canevari S, Formelli F. b>Decrease in drug accumulation and in tumour aggressiveness marker expression in a fenretinide-induced resistant ovarian tumour cell line. Br J Cancer 2001, 84:1528-1534. 10.1054/bjoc.2001.1826, 2363672, 11384104.
18. Albini A, Iwamoto Y, Kleinman HK, Martin GR, Aaronson SA, Kozlowski JM, McEwan RN. A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 1987, 47:3239-3245.
19. Sonoda Y, Watanabe S, Matsumoto Y, Aizu-Yokota E, Kasahara T. FAK is the upstream signal protein of the phosphatidylinositol 3-kinase-Akt survival pathway in hydrogen peroxide-induced apoptosis of a human glioblastoma cell line. J Biol Chem 1999, 274:10566-10570. 10.1074/jbc.274.15.10566, 10187851.
20. van Nimwegen MJ, van de Water B. Focal adhesion kinase: a potential target in cancer therapy. Biochem Pharmacol 2007, 73:597-609. 10.1016/j.bcp.2006.08.011, 16997283.
21. Shukla S, Maclennan GT, Hartman DJ, Fu P, Resnick MI, Gupta S. Activation of PI3K-Akt signaling pathway promotes prostate cancer cell invasion. Int J Cancer 2007, 121:1424-1432. 10.1002/ijc.22862, 17551921.
22. Fang J, Ding M, Yang L, Liu LZ, Jiang BH. PI3K/PTEN/AKT signaling regulates prostate tumor angiogenesis. Cell Signal 2007, 19:2487-2497. 10.1016/j.cellsig.2007.07.025, 2094004, 17826033.
23. Sachdev D, Yee D. Disrupting insulin-like growth factor signaling as a potential cancer therapy. Mol Cancer Ther 2007, 6:1-12. 10.1158/1535-7163.MCT-06-0080, 17237261.
24. Chen G, Shukeir N, Potti A, Sircar K, Aprikian A, Goltzman D, Rabbani SA. Up-regulation of Wnt-1 and beta-catenin production in patients with advanced metastatic prostate carcinoma: potential pathogenetic and prognostic implications. Cancer 2004, 101:1345-1356. 10.1002/cncr.20518, 15316903.
25. Takahashi-Yanaga F, Sasaguri T. GSK-3beta regulates cyclin D1 expression: a new target for chemotherapy. Cell Signal 2008, 20:581-589. 10.1016/j.cellsig.2007.10.018, 18023328.
26. Ma H, Nguyen C, Lee KS, Kahn M. Differential roles for the coactivators CBP and p300 on TCF/beta-catenin-mediated survivin gene expression. Oncogene 2005, 24:3619-3631. 10.1038/sj.onc.1208433, 15782138.
27. Fang D, Hawke D, Zheng Y, Xia Y, Meisenhelder J, Nika H, Mills GB, Kobayashi R, Hunter T, Lu Z. Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem 2007, 282:11221-11229. 10.1074/jbc.M611871200, 1850976, 17287208.
28. Lu Z, Ghosh S, Wang Z, Hunter T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell 2003, 4:499-515. 10.1016/S1535-6108(03)00304-0, 14706341.
29. Grille SJ, Bellacosa A, Upson J, Klein-Szanto AJ, van Roy F, Lee-Kwon W, Donowitz M, Tsichlis PN, Larue L. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res 2003, 63:2172-2178.
30. He XC, Zhang J, Tong WG, Tawfik O, Ross J, Scoville DH, Tian Q, Zeng X, He X, Wiedemann LM, et al. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat Genet 2004, 36:1117-1121. 10.1038/ng1430, 15378062.
31. Haramis AP, Begthel H, van den Born M, van Es J, Jonkheer S, Offerhaus GJ, Clevers H. De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science 2004, 303:1684-1686. 10.1126/science.1093587, 15017003.
32. Buijs JT, Rentsch CA, van der Horst G, van Overveld PG, Wetterwald A, Schwaninger R, Henriquez NV, Ten Dijke P, Borovecki F, Markwalder R, et al. BMP7, a putative regulator of epithelial homeostasis in the human prostate, is a potent inhibitor of prostate cancer bone metastasis in vivo. Am J Pathol 2007, 171:1047-1057. 10.2353/ajpath.2007.070168, 1959502, 17724140.
33. Shukla S, MacLennan GT, Flask CA, Fu P, Mishra A, Resnick MI, Gupta S. Blockade of beta-catenin signaling by plant flavonoid apigenin suppresses prostate carcinogenesis in TRAMP mice. Cancer Res 2007, 67:6925-6935. 10.1158/0008-5472.CAN-07-0717, 17638904.
34. Thaller C, Shalev M, Frolov A, Eichele G, Thompson TC, Williams RH, Dillioglugil O, Kadmon D. Fenretinide therapy in prostate cancer: effects on tissue and serum retinoid concentration. J Clin Oncol 2000, 18:3804-3808.
35. Tremblay L, Hauck W, Aprikian AG, Begin LR, Chapdelaine A, Chevalier S. Focal adhesion kinase (pp125FAK) expression, activation and association with paxillin and p50CSK in human metastatic prostate carcinoma. Int J Cancer 1996, 68:164-171. 10.1002/(SICI)1097-0215(19961009)68:2<169::AID-IJC4>3.0.CO;2-W, 8900422.
36. Rovin JD, Frierson HF, Ledinh W, Parsons JT, Adams RB. Expression of focal adhesion kinase in normal and pathologic human prostate tissues. Prostate 2002, 53:124-132. 10.1002/pros.10114, 12242727.
37. Shimada K, Nakamura M, Ishida E, Kishi M, Yonehara S, Konishi N. Contributions of mitogen-activated protein kinase and nuclear factor kappa B to N-(4-hydroxyphenyl)retinamide-induced apoptosis in prostate cancer cells. Mol Carcinog 2002, 35:127-137. 10.1002/mc.10084, 12410564.
38. Mitra SK, Mikolon D, Molina JE, Hsia DA, Hanson DA, Chi A, Lim ST, Bernard-Trifilo JA, Ilic D, Stupack DG, et al. Intrinsic FAK activity and Y925 phosphorylation facilitate an angiogenic switch in tumors. Oncogene 2006, 25:5969-5984. 10.1038/sj.onc.1209588, 16682956.
39. Shah S, Hecht A, Pestell R, Byers SW. Trans-repression of beta-catenin activity by nuclear receptors. J Biol Chem 2003, 278:48137-48145. 10.1074/jbc.M307154200, 12972427.
40. Easwaran V, Pishvaian M, Salimuddin, Byers S. Cross-regulation of beta-catenin-LEF/TCF and retinoid signaling pathways. Curr Biol 1999, 9:1415-1418. 10.1016/S0960-9822(00)80088-3, 10607566.
41. Xiao JH, Ghosn C, Hinchman C, Forbes C, Wang J, Snider N, Cordrey A, Zhao Y, Chandraratna RA. Adenomatous polyposis coli (APC)-independent regulation of beta-catenin degradation via a retinoid X receptor-mediated pathway. J Biol Chem 2003, 278:29954-29962. 10.1074/jbc.M304761200, 12771132.
42. 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.
43. Mulholland DJ, Dedhar S, Coetzee GA, Nelson CC. Interaction of nuclear receptors with the Wnt/beta-catenin/Tcf signaling axis: Wnt you like to know?. Endocr Rev 2005, 26:898-915. 10.1210/er.2003-0034, 16126938.
44. Golubkov V, Garcia A, Markland FS. Action of fenretinide (4-HPR) on ovarian cancer and endothelial cells. Anticancer Res 2005, 25:249-253.
45. Pagnan G, Di Paolo D, Carosio R, Pastorino F, Marimpietri D, Brignole C, Pezzolo A, Loi M, Galietta LJ, Piccardi F, et al. The combined therapeutic effects of bortezomib and fenretinide on neuroblastoma cells involve endoplasmic reticulum stress response. Clin Cancer Res 2009, 15:1199-1209. 10.1158/1078-0432.CCR-08-2477, 19228726.
46. Lai TH, Fong YC, Fu WM, Yang RS, Tang CH. Osteoblasts-derived BMP-2 enhances the motility of prostate cancer cells via activation of integrins. Prostate 2008, 68:1341-1353. 10.1002/pros.20799, 18512729.
47. Dai J, Hall CL, Escara-Wilke J, Mizokami A, Keller JM, Keller ET. Prostate cancer induces bone metastasis through Wnt-induced bone morphogenetic protein-dependent and independent mechanisms. Cancer Res 2008, 68:5785-5794. 10.1158/0008-5472.CAN-07-6541, 18632632.
48. Feeley BT, Krenek L, Liu N, Hsu WK, Gamradt SC, Schwarz EM, Huard J, Lieberman JR. Overexpression of noggin inhibits BMP-mediated growth of osteolytic prostate cancer lesions. Bone 2006, 38:154-166. 10.1016/j.bone.2005.07.015, 16126463.
49. Qiu T, Grizzle WE, Oelschlager DK, Shen X, Cao X. Control of prostate cell growth: BMP antagonizes androgen mitogenic activity with incorporation of MAPK signals in Smad1. Embo J 2007, 26:346-357. 10.1038/sj.emboj.7601499, 1783451, 17183365.
50. Ide H, Yoshida T, Matsumoto N, Aoki K, Osada Y, Sugimura T, Terada M. Growth regulation of human prostate cancer cells by bone morphogenetic protein-2. Cancer Res 1997, 57:5022-5027.
51. Tomari K, Kumagai T, Shimizu T, Takeda K. Bone morphogenetic protein-2 induces hypophosphorylation of Rb protein and repression of E2F in androgen-treated LNCaP human prostate cancer cells. Int J Mol Med 2005, 15:253-258.