Vitamin E δ-Tocotrienol Induces p27Kip1-Dependent Cell-Cycle Arrest in Pancreatic Cancer Cells via an E2F-1-Dependent Mechanism

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Hodul, Pamela J ^a   Dong, Yanbin ^a   Husain, Kazim ^a   Pimiento, Jose M ^a   Chen, Jiandong ^a   Zhang, Anying ^b   Francois, Rony ^c   Pledger, Warren J ^a   Coppola, Domenico ^a   Sebti, Said M ^a   Chen, Dung Tsa ^a   Malafa, Mokenge P ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF ELECTRONIC SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DELTA TOCOTRIENOL; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; RAF PROTEIN; TRANSCRIPTION FACTOR E2F1; UNCLASSIFIED DRUG;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOACCUMULATION; CANCER CELL CULTURE; CANCER PROGNOSIS; CDKN1B GENE; CELL CYCLE ARREST; CONTROLLED STUDY; DRUG EFFECT; DRUG STRUCTURE; ENZYME ACTIVATION; FEMALE; G1 PHASE CELL CYCLE CHECKPOINT; GENE FUNCTION; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; ONCOGENE; PANCREAS CANCER; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

BLOTTING, WESTERN; CELL CYCLE CHECKPOINTS; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P27; E2F1 TRANSCRIPTION FACTOR; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; PANCREATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VITAMIN E;

EID: 84873516380     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052526     Document Type: Article

References (50)

1. Jemal A, Siegel R, Xu J, Ward E, (2010) Cancer statistics, 2010. CA Cancer J Clin 60: 277-300.
2. Chan JM, Wang F, Holly EA, (2005) Vegetable and fruit intake and pancreatic cancer in a population-based case-control study in the San Francisco bay area. Cancer Epidemiol Biomarkers Prev 14: 2093-2097.
3. Mills PK, Beeson WL, Abbey DE, Fraser GE, Phillips RL, (1988) Dietary habits and past medical history as related to fatal pancreas cancer risk among Adventists. Cancer 61: 2578-2585.
4. Silverman DT, Swanson CA, Gridley G, Wacholder S, Greenberg RS, et al. (1998) Dietary and nutritional factors and pancreatic cancer: a case-control study based on direct interviews. J Natl Cancer Inst 90: 1710-1719.
5. Sen CK, Khanna S, Roy S, (2007) Tocotrienols in health and disease: the other half of the natural vitamin E family. Mol Aspects Med 28: 692-728.
6. Sylvester PW, Shah SJ, (2005) Mechanisms mediating the antiproliferative and apoptotic effects of vitamin E in mammary cancer cells. Front Biosci 10: 699-709.
7. Wada S, Satomi Y, Murakoshi M, Noguchi N, Yoshikawa T, et al. (2005) Tumor suppressive effects of tocotrienol in vivo and in vitro. Cancer Lett 229: 181-191.
8. Xu WL, Liu JR, Liu HK, Qi GY, Sun XR, et al. (2009) Inhibition of proliferation and induction of apoptosis by gamma-tocotrienol in human colon carcinoma HT-29 cells. Nutrition 25: 555-566.
9. Gould MN, Haag JD, Kennan WS, Tanner MA, Elson CE, (1991) A comparison of tocopherol and tocotrienol for the chemoprevention of chemically induced rat mammary tumors. Am J Clin Nutr 53: 1068S-1070S.
10. Ngah WZ, Jarien Z, San MM, Marzuki A, Top GM, et al. (1991) Effect of tocotrienols on hepatocarcinogenesis induced by 2-acetylaminofluorene in rats. Am J Clin Nutr 53: 1076S-1081S.
11. Husain K, Francois RA, Yamauchi T, Perez M, Sebti SM, et al. (2011) Vitamin E {delta}-Tocotrienol Augments the Anti-tumor Activity of Gemcitabine and Suppresses Constitutive NF-{kappa}B Activation in Pancreatic Cancer. Mol Cancer Ther 10: 2363-2372.
12. Husain K, Francois RA, Hutchinson SZ, Neuger AM, Lush R, et al. (2009) Vitamin E delta-tocotrienol levels in tumor and pancreatic tissue of mice after oral administration. Pharmacology 83: 157-163.
13. Springett GM, Neuger AM, Centeno BA, Hutchinson T, Jump H, et al. (2011) A phase I doese-escalation study of the safety, PK, and PD of vitamin E delta-tocotrienol administered to subjects with resectable pancreatic exocrine neoplasia (Abstract). Cancer Res 71: 1299.
14. Hu YX, Watanabe H, Li P, Wang Y, Ohtsubo K, et al. (2000) An immunohistochemical analysis of p27 expression in human pancreatic carcinomas. Pancreas 21: 226-230.
15. Lu CD, Morita S, Ishibashi T, Hara H, Isozaki H, et al. (1999) Loss of p27Kip1 expression independently predicts poor prognosis for patients with resectable pancreatic adenocarcinoma. Cancer 85: 1250-1260.
16. Viglietto G, Motti ML, Fusco A, (2002) Understanding p27(kip1) deregulation in cancer: down-regulation or mislocalization. Cell Cycle 1: 394-400.
17. Juuti A, Nordling S, Louhimo J, Lundin J, von Boguslawski K, et al. (2003) Loss of p27 expression is associated with poor prognosis in stage I-II pancreatic cancer. Oncology 65: 371-377.
18. Furukawa T, Duguid WP, Rosenberg L, Viallet J, Galloway DA, et al. (1996) Long-term culture and immortalization of epithelial cells from normal adult human pancreatic ducts transfected by the E6E7 gene of human papilloma virus 16. Am J Pathol 148: 1763-1770.
19. Bagui TK, Jackson RJ, Agrawal D, Pledger WJ, (2000) Analysis of cyclin D3-cdk4 complexes in fibroblasts expressing and lacking p27(kip1) and p21(cip1). Mol Cell Biol 20: 8748-8757.
20. Bagui TK, Mohapatra S, Haura E, Pledger WJ, (2003) P27Kip1 and p21Cip1 are not required for the formation of active D cyclin-cdk4 complexes. Mol Cell Biol 23: 7285-7290.
21. Wang C, Hou X, Mohapatra S, Ma Y, Cress WD, et al. (2005) Activation of p27Kip1 Expression by E2F1. A negative feedback mechanism. J Biol Chem 280: 12339-12343.
22. Arora S, Bhardwaj A, Srivastava SK, Singh S, McClellan S, et al. (2011) Honokiol arrests cell cycle, induces apoptosis, and potentiates the cytotoxic effect of gemcitabine in human pancreatic cancer cells. PLoS One 6: e21573.
23. Kawa S, Yoshizawa K, Nikaido T, Kiyosawa K, (2005) Inhibitory effect of 22-oxa-1,25-dihydroxyvitamin D3, maxacalcitol, on the proliferation of pancreatic cancer cell lines. J Steroid Biochem Mol Biol 97: 173-177.
24. Shankar S, Suthakar G, Srivastava RK, (2007) Epigallocatechin-3-gallate inhibits cell cycle and induces apoptosis in pancreatic cancer. Front Biosci 12: 5039-5051.
25. Wiseman DA, Werner SR, Crowell PL, (2007) Cell cycle arrest by the isoprenoids perillyl alcohol, geraniol, and farnesol is mediated by p21(Cip1) and p27(Kip1) in human pancreatic adenocarcinoma cells. J Pharmacol Exp Ther 320: 1163-1170.
26. Zhou X, Zheng M, Chen F, Zhu Y, Yong W, et al. (2009) Gefitinib inhibits the proliferation of pancreatic cancer cells via cell cycle arrest. Anat Rec (Hoboken) 292: 1122-1127.
27. Orend G, Hunter T, Ruoslahti E, (1998) Cytoplasmic displacement of cyclin E-cdk2 inhibitors p21Cip1 and p27Kip1 in anchorage-independent cells. Oncogene 16: 2575-2583.
28. Reynisdottir I, Massague J, (1997) The subcellular locations of p15(Ink4b) and p27(Kip1) coordinate their inhibitory interactions with cdk4 and cdk2. Genes Dev 11: 492-503.
29. Elson CE, (1995) Suppression of mevalonate pathway activities by dietary isoprenoids: protective roles in cancer and cardiovascular disease. J Nutr 125: 1666S-1672S.
30. Parker RA, Pearce BC, Clark RW, Gordon DA, Wright JJ, (1993) Tocotrienols regulate cholesterol production in mammalian cells by post-transcriptional suppression of 3-hydroxy-3-methylglutaryl-coenzyme A reductase. J Biol Chem 268: 11230-11238.
31. Elson CE, Yu SG, (1994) The chemoprevention of cancer by mevalonate-derived constituents of fruits and vegetables. J Nutr 124: 607-614.
32. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
33. Chu IM, Hengst L, Slingerland JM, (2008) The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy. Nat Rev Cancer 8: 253-267.
34. Wang X, Gorospe M, Huang Y, Holbrook NJ, (1997) p27Kip1 overexpression causes apoptotic death of mammalian cells. Oncogene 15: 2991-2997.
35. Besson A, Gurian-West M, Chen X, Kelly-Spratt KS, Kemp CJ, et al. (2006) A pathway in quiescent cells that controls p27Kip1 stability, subcellular localization, and tumor suppression. Genes Dev 20: 47-64.
36. Connor MK, Kotchetkov R, Cariou S, Resch A, Lupetti R, et al. (2003) CRM1/Ran-mediated nuclear export of p27(Kip1) involves a nuclear export signal and links p27 export and proteolysis. Mol Biol Cell 14: 201-213.
37. Rodier G, Montagnoli A, Di Marcotullio L, Coulombe P, Draetta GF, et al. (2001) p27 cytoplasmic localization is regulated by phosphorylation on Ser10 and is not a prerequisite for its proteolysis. EMBO J 20: 6672-6682.
38. Fujita N, Sato S, Tsuruo T, (2003) Phosphorylation of p27Kip1 at threonine 198 by p90 ribosomal protein S6 kinases promotes its binding to 14-3-3 and cytoplasmic localization. J Biol Chem 278: 49254-49260.
39. Hong F, Larrea MD, Doughty C, Kwiatkowski DJ, Squillace R, et al. (2008) mTOR-raptor binds and activates SGK1 to regulate p27 phosphorylation. Mol Cell 30: 701-711.
40. Liang J, Zubovitz J, Petrocelli T, Kotchetkov R, Connor MK, et al. (2002) PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat Med 8: 1153-1160.
41. Sekimoto T, Fukumoto M, Yoneda Y, (2004) 14-3-3 suppresses the nuclear localization of threonine 157-phosphorylated p27(Kip1). EMBO J 23: 1934-1942.
42. Shin I, Rotty J, Wu FY, Arteaga CL, (2005) Phosphorylation of p27Kip1 at Thr-157 interferes with its association with importin alpha during G1 and prevents nuclear re-entry. J Biol Chem 280: 6055-6063.
43. Grunewald K, Lyons J, Frohlich A, Feichtinger H, Weger RA, et al. (1989) High frequency of Ki-ras codon 12 mutations in pancreatic adenocarcinomas. Int J Cancer 43: 1037-1041.
44. Ishimura N, Yamasawa K, Karim Rumi MA, Kadowaki Y, Ishihara S, et al. (2003) BRAF and K-ras gene mutations in human pancreatic cancers. Cancer Lett 199: 169-173.
45. Motojima K, Urano T, Nagata Y, Shiku H, Tsurifune T, et al. (1993) Detection of point mutations in the Kirsten-ras oncogene provides evidence for the multicentricity of pancreatic carcinoma. Ann Surg 217: 138-143.
46. Pruitt K, Der CJ, (2001) Ras and Rho regulation of the cell cycle and oncogenesis. Cancer Lett 171: 1-10.
47. Roovers K, Assoian RK, (2000) Integrating the MAP kinase signal into the G1 phase cell cycle machinery. Bioessays 22: 818-826.
48. Mirza AM, Gysin S, Malek N, Nakayama K, Roberts JM, et al. (2004) Cooperative regulation of the cell division cycle by the protein kinases RAF and AKT. Mol Cell Biol 24: 10868-10881.
49. Gysin S, Lee SH, Dean NM, McMahon M, (2005) Pharmacologic inhibition of RAF->MEK->ERK signaling elicits pancreatic cancer cell cycle arrest through induced expression of p27Kip1. Cancer Res 65: 4870-4880.
50. Hussein D, Mo H, (2009) d-delta-Tocotrienol-mediated suppression of the proliferation of human PANC-1, MIA PaCa-2, and BxPC-3 pancreatic carcinoma cells. Pancreas 38: e124-136.