Caffeic acid phenethyl ester causes p21 cip1 induction, Akt signaling reduction, and growth inhibition in PC-3 human prostate cancer cells

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Lin, Hui Ping ^a   Jiang, Shih Sheng ^a   Chuu, Chih Pin ^a,b  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; BETA TUBULIN; CAFFEIC ACID PHENETHYL ESTER; CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN E; ESTRAMUSTINE; ETOPOSIDE; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; KRUPPEL LIKE FACTOR 6; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOXANTRONE; MYC PROTEIN; PACLITAXEL; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN AKT1; PROTEIN AKT3; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN KINASE B BETA; RETINOBLASTOMA PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 2; UNCLASSIFIED DRUG; VINBLASTINE; ANTINEOPLASTIC AGENT; CAFFEIC ACID DERIVATIVE; DRUG DERIVATIVE; P21 ACTIVATED KINASE; PHENETHYL ALCOHOL;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER ADJUVANT THERAPY; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL DEATH; CELL MOTION; CELL PROLIFERATION; CELL STRAIN PC3; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG POTENTIATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; MITOSIS INHIBITION; PROSTATE CANCER; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; BIOSYNTHESIS; CELL CYCLE; DRUG ANTAGONISM; DRUG EFFECT; MALE; PHOSPHORYLATION; PROSTATE TUMOR; TUMOR CELL LINE;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CAFFEIC ACIDS; CELL CYCLE; CELL DEATH; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DRUG SYNERGISM; HUMANS; MALE; MICROARRAY ANALYSIS; P21-ACTIVATED KINASES; PHENYLETHYL ALCOHOL; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84863071290     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031286     Document Type: Article

References (70)

1. Bubendorf L, Schopfer A, Wagner U, Sauter G, Moch H, et al. (2000) Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol 31: 578-583.
2. Ibrahim T, Flamini E, Mercatali L, Sacanna E, Serra P, et al. (2010) Pathogenesis of osteoblastic bone metastases from prostate cancer. Cancer 116: 1406-1418.
3. Keller ET, Zhang J, Cooper CR, Smith PC, McCauley LK, et al. (2001) Prostate carcinoma skeletal metastases: cross-talk between tumor and bone. Cancer Metastasis Rev 20: 333-349.
4. Huggins C, Stevens R, Hodges C, (1941) Studies on prostatic cancer: II. The effects of castration on advanced carcinoma of the prostate gland. Arch Surg 43: 15.
5. Hellerstedt BA, Pienta KJ, (2002) The current state of hormonal therapy for prostate cancer. CA Cancer J Clin 52: 154-179.
6. Chuu CP, Kokontis JM, Hiipakka RA, Fukuchi J, Lin HP, et al. (2011) Androgens as therapy for androgen receptor-positive castration-resistant prostate cancer. Journal of biomedical science 18: 63.
7. Gilligan T, Kantoff PW, (2002) Chemotherapy for prostate cancer. Urology 60: 94-100; discussion 100.
8. Pinto AC, Moreira JN, Simoes S, (2011) Liposomal imatinib-mitoxantrone combination: formulation development and therapeutic evaluation in an animal model of prostate cancer. Prostate 71: 81-90.
9. Bhimani RS, Troll W, Grunberger D, Frenkel K, (1993) Inhibition of oxidative stress in HeLa cells by chemopreventive agents. Cancer Res 53: 4528-4533.
10. Natarajan K, Singh S, Burke TR Jr, Grunberger D, Aggarwal BB, (1996) Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad Sci U S A 93: 9090-9095.
11. Watabe M, Hishikawa K, Takayanagi A, Shimizu N, Nakaki T, (2004) Caffeic acid phenethyl ester induces apoptosis by inhibition of NFkappaB and activation of Fas in human breast cancer MCF-7 cells. J Biol Chem 279: 6017-6026.
12. McEleny K, Coffey R, Morrissey C, Fitzpatrick JM, Watson RW, (2004) Caffeic acid phenethyl ester-induced PC-3 cell apoptosis is caspase-dependent and mediated through the loss of inhibitors of apoptosis proteins. BJU Int 94: 402-406.
13. Chen YJ, Shiao MS, Hsu ML, Tsai TH, Wang SY, (2001) Effect of caffeic acid phenethyl ester, an antioxidant from propolis, on inducing apoptosis in human leukemic HL-60 cells. J Agric Food Chem 49: 5615-5619.
14. Kuo HC, Kuo WH, Lee YJ, Lin WL, Chou FP, et al. (2006) Inhibitory effect of caffeic acid phenethyl ester on the growth of C6 glioma cells in vitro and in vivo. Cancer Lett 234: 199-208.
15. He YJ, Liu BH, Xiang DB, Qiao ZY, Fu T, et al. (2006) Inhibitory effect of caffeic acid phenethyl ester on the growth of SW480 colorectal tumor cells involves beta-catenin associated signaling pathway down-regulation. World J Gastroenterol 12: 4981-4985.
16. Chuu CP, Kokontis JM, Hiipakka RA, Liao S, (2007) Modulation of liver X receptor signaling as novel therapy for prostate cancer. J Biomed Sci 14: 543-553.
17. Lebedeva I, Rando R, Ojwang J, Cossum P, Stein CA, (2000) Bcl-xL in prostate cancer cells: effects of overexpression and down-regulation on chemosensitivity. Cancer Res 60: 6052-6060.
18. Liu QY, Stein CA, (1997) Taxol and estramustine-induced modulation of human prostate cancer cell apoptosis via alteration in bcl-xL and bak expression. Clin Cancer Res 3: 2039-2046.
19. Williams JF, Muenchen HJ, Kamradt JM, Korenchuk S, Pienta KJ, (2000) Treatment of androgen-independent prostate cancer using antimicrotubule agents docetaxel and estramustine in combination: an experimental study. Prostate 44: 275-278.
20. Pienta KJ, Lehr JE, (1993) Inhibition of prostate cancer growth by estramustine and etoposide: evidence for interaction at the nuclear matrix. J Urol 149: 1622-1625.
21. Shankar S, Chen X, Srivastava RK, (2005) Effects of sequential treatments with chemotherapeutic drugs followed by TRAIL on prostate cancer in vitro and in vivo. Prostate 62: 165-186.
22. Polin L, Valeriote F, White K, Panchapor C, Pugh S, et al. (1997) Treatment of human prostate tumors PC-3 and TSU-PR1 with standard and investigational agents in SCID mice. Invest New Drugs 15: 99-108.
23. Celli N, Dragani LK, Murzilli S, Pagliani T, Poggi A, (2007) In vitro and in vivo stability of caffeic acid phenethyl ester, a bioactive compound of propolis. J Agric Food Chem 55: 3398-3407.
24. Majumder PK, Sellers WR, (2005) Akt-regulated pathways in prostate cancer. Oncogene 24: 7465-7474.
25. Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ, (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805-816.
26. Gartel AL, Radhakrishnan SK, (2005) Lost in transcription: p21 repression, mechanisms, and consequences. Cancer Res 65: 3980-3985.
27. Frescas D, Pagano M, (2008) Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat Rev Cancer 8: 438-449.
28. Chellappan SP, Hiebert S, Mudryj M, Horowitz JM, Nevins JR, (1991) The E2F transcription factor is a cellular target for the RB protein. Cell 65: 1053-1061.
29. Marshall CJ, (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80: 179-185.
30. Elledge SJ, Harper JW, (1994) Cdk inhibitors: on the threshold of checkpoints and development. Curr Opin Cell Biol 6: 847-852.
31. Kreisberg JI, Malik SN, Prihoda TJ, Bedolla RG, Troyer DA, et al. (2004) Phosphorylation of Akt (Ser473) is an excellent predictor of poor clinical outcome in prostate cancer. Cancer Res 64: 5232-5236.
32. Coffer PJ, Jin J, Woodgett JR, (1998) Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem J 355 (Pt 1): 1-13.
33. Gonzalez E, McGraw TE, (2009) The Akt kinases: isoform specificity in metabolism and cancer. Cell Cycle 8: 2502-2508.
34. Nakatani K, Thompson DA, Barthel A, Sakaue H, Liu W, et al. (1999) Up-regulation of Akt3 in estrogen receptor-deficient breast cancers and androgen-independent prostate cancer lines. J Biol Chem 274: 21528-21532.
35. Sasaki T, Nakashiro K, Tanaka H, Azuma K, Goda H, et al. (2010) Knockdown of Akt isoforms by RNA silencing suppresses the growth of human prostate cancer cells in vitro and in vivo. Biochem Biophys Res Commun 399: 79-83.
36. Wang LC, Chu KH, Liang YC, Lin YL, Chiang BL, (2010) Caffeic acid phenethyl ester inhibits nuclear factor-kappaB and protein kinase B signalling pathways and induces caspase-3 expression in primary human CD4+ T cells. Clin Exp Immunol 160: 223-232.
37. Ho HC, Hsu SL, Ting CT, Kuo CY, Yang VC, (2009) Caffeic acid phenethyl ester inhibits arterial smooth muscle cell proliferation and migration in vitro and in vivo using a local delivery system. Cell Mol Biol (Noisy-le-grand) 55 (Suppl): OL1161-1167.
38. Shigeoka Y, Igishi T, Matsumoto S, Nakanishi H, Kodani M, et al. (2004) Sulindac sulfide and caffeic acid phenethyl ester suppress the motility of lung adenocarcinoma cells promoted by transforming growth factor-beta through Akt inhibition. J Cancer Res Clin Oncol 130: 146-152.
39. Cantley LC, Neel BG, (1999) New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc Natl Acad Sci U S A 96: 4240-4245.
40. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, et al. (1997) Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol 7: 261-269.
41. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM, (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307: 1098-1101.
42. Jacinto E, Facchinetti V, Liu D, Soto N, Wei S, et al. (2006) SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127: 125-137.
43. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA, (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378: 785-789.
44. Liang J, Slingerland JM, (2003) Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2: 339-345.
45. Alao JP, (2007) The regulation of cyclin D1 degradation: roles in cancer development and the potential for therapeutic invention. Molecular cancer 6: 24.
46. Liu R, Wang L, Chen G, Katoh H, Chen C, et al. (2009) FOXP3 up-regulates p21 expression by site-specific inhibition of histone deacetylase 2/histone deacetylase 4 association to the locus. Cancer Res 69: 2252-2259.
47. Chen X, Johns DC, Geiman DE, Marban E, Dang DT, et al. (2001) Kruppel-like factor 4 (gut-enriched Kruppel-like factor) inhibits cell proliferation by blocking G1/S progression of the cell cycle. J Biol Chem 276: 30423-30428.
48. Zhang W, Geiman DE, Shields JM, Dang DT, Mahatan CS, et al. (2000) The gut-enriched Kruppel-like factor (Kruppel-like factor 4) mediates the transactivating effect of p53 on the p21WAF1/Cip1 promoter. J Biol Chem 275: 18391-18398.
49. Katsuki Y, Sakamoto K, Minamizato T, Makino H, Umezawa A, et al. (2008) Inhibitory effect of CT domain of CCN3/NOV on proliferation and differentiation of osteogenic mesenchymal stem cells, Kusa-A1. Biochem Biophys Res Commun 368: 808-814.
50. Zimmers TA, Jin X, Gutierrez JC, Acosta C, McKillop IH, et al. (2008) Effect of in vivo loss of GDF-15 on hepatocellular carcinogenesis. J Cancer Res Clin Oncol 134: 753-759.
51. Schutyser E, Struyf S, Menten P, Lenaerts JP, Conings R, et al. (2000) Regulated production and molecular diversity of human liver and activation-regulated chemokine/macrophage inflammatory protein-3 alpha from normal and transformed cells. J Immunol 165: 4470-4477.
52. Wolpe SD, Sherry B, Juers D, Davatelis G, Yurt RW, et al. (1989) Identification and characterization of macrophage inflammatory protein 2. Proc Natl Acad Sci U S A 86: 612-616.
53. Duchene J, Lecomte F, Ahmed S, Cayla C, Pesquero J, et al. (2007) A novel inflammatory pathway involved in leukocyte recruitment: role for the kinin B1 receptor and the chemokine CXCL5. J Immunol 179: 4849-4856.
54. Bektic J, Pfeil K, Berger AP, Ramoner R, Pelzer A, et al. (2005) Small G-protein RhoE is underexpressed in prostate cancer and induces cell cycle arrest and apoptosis. Prostate 64: 332-340.
55. Narla G, Heath KE, Reeves HL, Li D, Giono LE, et al. (2001) KLF6, a candidate tumor suppressor gene mutated in prostate cancer. Science 294: 2563-2566.
56. Malhotra S, Lapointe J, Salari K, Higgins JP, Ferrari M, et al. (2011) A tri-marker proliferation index predicts biochemical recurrence after surgery for prostate cancer. PLoS One 6: e20293.
57. Zhao H, Jin S, Antinore MJ, Lung FD, Fan F, et al. (2000) The central region of Gadd45 is required for its interaction with p21/WAF1. Exp Cell Res 258: 92-100.
58. Jin S, Antinore MJ, Lung FD, Dong X, Zhao H, et al. (2000) The GADD45 inhibition of Cdc2 kinase correlates with GADD45-mediated growth suppression. J Biol Chem 275: 16602-16608.
59. Gao H, Jin S, Song Y, Fu M, Wang M, et al. (2005) B23 regulates GADD45a nuclear translocation and contributes to GADD45a-induced cell cycle G2-M arrest. J Biol Chem 280: 10988-10996.
60. Yagi A, Hasegawa Y, Xiao H, Haneda M, Kojima E, et al. (2003) GADD34 induces p53 phosphorylation and p21/WAF1 transcription. J Cell Biochem 90: 1242-1249.
61. Ding H, Duan W, Zhu WG, Ju R, Srinivasan K, et al. (2003) P21 response to DNA damage induced by genistein and etoposide in human lung cancer cells. Biochem Biophys Res Commun 305: 950-956.
62. Horiguchi-Yamada J, Fukumi S, Saito S, Nakayama R, Iwase S, et al. (2002) DNA topoisomerase II inhibitor, etoposide, induces p21WAF1/CIP1 through down-regulation of c-Myc in K562 cells. Anticancer Res 22: 3827-3832.
63. Zhao H, Halicka HD, Traganos F, Jorgensen E, Darzynkiewicz Z, (2010) New biomarkers probing depth of cell senescence assessed by laser scanning cytometry. Cytometry A 77: 999-1007.
64. Kolomeichuk SN, Bene A, Upreti M, Dennis RA, Lyle CS, et al. (2008) Induction of apoptosis by vinblastine via c-Jun autoamplification and p53-independent down-regulation of p21WAF1/CIP1. Mol Pharmacol 73: 128-136.
65. Heliez C, Baricault L, Barboule N, Valette A, (2003) Paclitaxel increases p21 synthesis and accumulation of its AKT-phosphorylated form in the cytoplasm of cancer cells. Oncogene 22: 3260-3268.
66. Chuu CP, Chen RY, Hiipakka RA, Kokontis JM, Warner KV, et al. (2007) The liver X receptor agonist T0901317 acts as androgen receptor antagonist in human prostate cancer cells. Biochem Biophys Res Commun 357: 341-346.
67. Chuu CP, Chen RY, Kokontis JM, Hiipakka RA, Liao S, (2009) Suppression of androgen receptor signaling and prostate specific antigen expression by (-)-epigallocatechin-3-gallate in different progression stages of LNCaP prostate cancer cells. Cancer Lett 275: 86-92.
68. Chuu CP, Lin HP, (2010) Antiproliferative effect of LXR agonists T0901317 and 22(R)-hydroxycholesterol on multiple human cancer cell lines. Anticancer Res 30: 3643-3648.
69. Chuu CP, Kokontis JM, Hiipakka RA, Fukuchi J, Lin HP, et al. (2011) Androgen suppresses proliferation of castration-resistant LNCaP 104-R2 prostate cancer cells through androgen receptor, Skp2, and c-Myc. Cancer science 102: 2022-2028.
70. Jiang SS, Fang WT, Hou YH, Huang SF, Yen BL, et al. (2010) Upregulation of SOX9 in lung adenocarcinoma and its involvement in the regulation of cell growth and tumorigenicity. Clin Cancer Res 16: 4363-4373.