EGR-1/Bax pathway plays a role in vitamin E δ-tocotrienol-induced apoptosis in pancreatic cancer cells

Journal of Nutritional Biochemistry

Volumn 26, Issue 8, 2015, Pages 797-807

  Wang, Chen ^a,b   Husain, Kazim ^a   Zhang, Anying ^a,c   Centeno, Barbara A ^a   Chen, Dung Tsa ^a   Tong, Zhongsheng ^b   Sebti, Säid M ^a   Malafa, Mokenge P ^a  

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

^b TIANJIN MEDICAL UNIVERSITY   (China)

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

Author keywords

Apoptosis; Early gene; Early growth response protein 1; Pancreatic cancer; Vitamin E; Tocotrienol

Indexed keywords

ALPHA TOCOPHEROL DERIVATIVE; DELTA TOCOTRIENOL; EARLY GROWTH RESPONSE FACTOR 1; PROTEIN BAX; PROTEIN BCL 2; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR EGR 1; UNCLASSIFIED DRUG; ALPHA TOCOPHEROL; BAX PROTEIN, HUMAN; EGR1 PROTEIN, HUMAN; TOCOTRIENOL, DELTA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER SURVIVAL; CELL DEATH; CELL PROLIFERATION; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; DNA MICROARRAY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LUCIFERASE ASSAY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PANCREAS CANCER; PANCREAS CELL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL RATE; TUNEL ASSAY; UPREGULATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; CELL SURVIVAL; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PANCREAS TUMOR; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; EARLY GROWTH RESPONSE PROTEIN 1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IN SITU NICK-END LABELING; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PANCREATIC NEOPLASMS; PROMOTER REGIONS, GENETIC; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VITAMIN E;

EID: 84931561729     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.02.008     Document Type: Article

References (81)

1. Aggarwal B., Nesaretnam K. Vitamin E tocotrienols: life beyond tocopherols. Genes Nutr 2012, 7:1.
2. Aggarwal B.B., Sundaram C., Prasad S., Kannappan R. Tocotrienols, the vitamin E of the 21st century: its potential against cancer and other chronic diseases. Biochem Pharmacol 2010, 80:1613-1631.
3. Husain K., Francois R.A., Yamauchi T., Perez M., Sebti S.M., Malafa M.P. Vitamin E delta-tocotrienol augments the antitumor activity of gemcitabine and suppresses constitutive NF-kappaB activation in pancreatic cancer. Mol Cancer Ther 2011, 10:2363-2372.
4. Husain K., Centeno B.A., Chen D.T., Fulp W.J., Perez M., Zhang Lee G., et al. Prolonged survival and delayed progression of pancreatic intraepithelial neoplasia in LSL-KrasG12D/+;Pdx-1-Cre mice by vitamin E delta-tocotrienol. Carcinogenesis 2013, 34:858-863.
5. Husain K., Centeno B.A., Chen D.T., Hingorani S.R., Sebti S.M., Malafa M.P. Vitamin E delta-tocotrienol prolongs survival in the LSL-KrasG12D/+;LSL-Trp53R172H/+;Pdx-1-Cre (KPC) transgenic mouse model of pancreatic cancer. Cancer Prev Res (Phila) 2013, 6:1074-1083.
6. Hodul P.J., Dong Y., Husain K., Pimiento J.M., Chen J., Zhang A., et al. Vitamin E delta-tocotrienol induces p27(Kip1)-dependent cell-cycle arrest in pancreatic cancer cells via an E2F-1-dependent mechanism. PLoS One 2013, 8:e52526.
7. Bai J., Sui J., Demirjian A., Vollmer C.M., Marasco W., Callery M.P. Predominant Bcl-XL knockdown disables antiapoptotic mechanisms: tumor necrosis factor-related apoptosis-inducing ligand-based triple chemotherapy overcomes chemoresistance in pancreatic cancer cells in vitro. Cancer Res 2005, 65:2344-2352.
8. Jones R.L., Pepling M.E. Role of the antiapoptotic proteins BCL2 and MCL1 in the neonatal mouse ovary. Biol Reprod 2013, 88:46.
9. Kontos C.K., Christodoulou M.I., Scorilas A. Apoptosis-related BCL2-family members: key players in chemotherapy. Anticancer Agents Med Chem 2014, 14:353-374.
10. Sharawat S.K., Bakhshi R., Vishnubhatla S., Gupta R., Bakhshi S. BAX/BCL2 RMFI ratio predicts better induction response in pediatric patients with acute myeloid leukemia. Pediatr Blood Cancer 2013, 60:E63-E66.
11. Fulda S., Debatin K.M. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 2006, 25:4798-4811.
12. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
13. Bouallegue A., Simo Cheyou E.R., Anand-Srivastava M.B., Srivastava A.K. ET-1-induced growth promoting responses involving ERK1/2 and PKB signaling and Egr-1 expression are mediated by Ca2+/CaM-dependent protein kinase-II in vascular smooth muscle cells. Cell Calcium 2013, 54:428-435.
14. Cabodi S., Morello V., Masi A., Cicchi R., Broggio C., Distefano P., et al. Convergence of integrins and EGF receptor signaling via PI3K/Akt/FoxO pathway in early gene Egr-1 expression. J Cell Physiol 2009, 218:294-303.
15. Chu L., Wang T., Hu Y., Gu Y., Su Z., Jiang H. Activation of Egr-1 in human lung epithelial cells exposed to silica through MAPKs signaling pathways. PLoS One 2013, 8:e68943.
16. Eliseev R.A., Dong Y.F., Sampson E., Zuscik M.J., Schwarz E.M., O'Keefe R.J., et al. Runx2-mediated activation of the Bax gene increases osteosarcoma cell sensitivity to apoptosis. Oncogene 2008, 27:3605-3614.
17. Hudson C.D., Morris P.J., Latchman D.S., Budhram-Mahadeo V.S. Brn-3a transcription factor blocks p53-mediated activation of proapoptotic target genes Noxa and Bax in vitro and in vivo to determine cell fate. J Biol Chem 2005, 280:11851-11858.
18. Shin S.Y., Kim C.G., Lim Y., Lee Y.H. The ETS family transcription factor ELK-1 regulates induction of the cell cycle-regulatory gene p21(Waf1/Cip1) and the BAX gene in sodium arsenite-exposed human keratinocyte HaCaT cells. J Biol Chem 2011, 286:26860-26872.
19. Trabosh V.A., Daher A., Divito K.A., Amin K., Simbulan-Rosenthal C.M., Rosenthal D.S. UVB upregulates the bax promoter in immortalized human keratinocytes via ROS induction of Id3. Exp Dermatol 2009, 18:387-395.
20. Zagurovskaya M., Shareef M.M., Das A., Reeves A., Gupta S., Sudol M., et al. EGR-1 forms a complex with YAP-1 and upregulates Bax expression in irradiated prostate carcinoma cells. Oncogene 2009, 28:1121-1131.
21. Hussein D., Mo H. d-delta-Tocotrienol-mediated suppression of the proliferation of human PANC-1, MIA PaCa-2, and BxPC-3 pancreatic carcinoma cells. Pancreas 2009, 38:e124-e136.
22. Shin-Kang S., Ramsauer V.P., Lightner J., Chakraborty K., Stone W., Campbell S., et al. Tocotrienols inhibit AKT and ERK activation and suppress pancreatic cancer cell proliferation by suppressing the ErbB2 pathway. Free Radic Biol Med 2011, 51:1164-1174.
23. Ahsan H., Ahad A., Iqbal J., Siddiqui W.A. Pharmacological potential of tocotrienols: a review. Nutr Metab (Lond) 2014, 11:52.
24. Ji X., Wang Z., Sarkar F.H., Gupta S.V. Delta-tocotrienol augments cisplatin-induced suppression of non-small cell lung cancer cells via inhibition of the Notch-1 pathway. Anticancer Res 2012, 32:2647-2655.
25. Pierpaoli E., Viola V., Barucca A., Orlando F., Galli F., Provinciali M. Effect of annatto-tocotrienols supplementation on the development of mammary tumors in HER-2/neu transgenic mice. Carcinogenesis 2013, 34:1352-1360.
26. Kannappan R., Gupta S.C., Kim J.H., Aggarwal B.B. Tocotrienols fight cancer by targeting multiple cell signaling pathways. Genes Nutr 2012, 7:43-52.
27. Viola V., Ciffolilli S., Legnaioli S., Piroddi M., Betti M., Mazzini F., et al. Mitochondrial-dependent anticancer activity of delta-tocotrienol and its synthetic derivatives in HER-2/neu overexpressing breast adenocarcinoma cells. Biofactors 2013, 39:485-493.
28. Christy B., Nathans D. DNA binding site of the growth factor-inducible protein Zif268. Proc Natl Acad Sci U S A 1989, 86:8737-8741.
29. Al-Sarraj A., Day R.M., Thiel G. Specificity of transcriptional regulation by the zinc finger transcription factors Sp1, Sp3, and Egr-1. J Cell Biochem 2005, 94:153-167.
30. Russo M.W., Sevetson B.R., Milbrandt J. Identification of NAB1, a repressor of NGFI-A- and Krox20-mediated transcription. Proc Natl Acad Sci U S A 1995, 92:6873-6877.
31. Svaren J., Sevetson B.R., Apel E.D., Zimonjic D.B., Popescu N.C., Milbrandt J. NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli. Mol Cell Biol 1996, 16:3545-3553.
32. Thiel G., Kaufmann K., Magin A., Lietz M., Bach K., Cramer M. The human transcriptional repressor protein NAB1: expression and biological activity. Biochim Biophys Acta 2000, 1493:289-301.
33. Xie B., Wang C., Zheng Z., Song B., Ma C., Thiel G., et al. Egr-1 transactivates Bim gene expression to promote neuronal apoptosis. J Neurosci 2011, 31:5032-5044.
34. Wei F., Xu Z.C., Qu Z., Milbrandt J., Zhuo M. Role of EGR1 in hippocampal synaptic enhancement induced by tetanic stimulation and amputation. J Cell Biol 2000, 149:1325-1334.
35. Liao Y., Shikapwashya O.N., Shteyer E., Dieckgraefe B.K., Hruz P.W., Rudnick D.A. Delayed hepatocellular mitotic progression and impaired liver regeneration in early growth response-1-deficient mice. J Biol Chem 2004, 279:43107-43116.
36. Lee S.L., Sadovsky Y., Swirnoff A.H., Polish J.A., Goda P., Gavrilina G., et al. Luteinizing hormone deficiency and female infertility in mice lacking the transcription factor NGFI-A (Egr-1). Science 1996, 273:1219-1221.
37. Safford M., Collins S., Lutz M.A., Allen A., Huang C.T., Kowalski J., et al. Egr-2 and Egr-3 are negative regulators of T cell activation. Nat Immunol 2005, 6:472-480.
38. Gibbs J.D., Liebermann D.A., Hoffman B. Egr-1 abrogates the E2F-1 block in terminal myeloid differentiation and suppresses leukemia. Oncogene 2008, 27:98-106.
39. Topilko P., Schneider-Maunoury S., Levi G., Baron-Van Evercooren A., Chennoufi A.B., Seitanidou T., et al. Krox-20 controls myelination in the peripheral nervous system. Nature 1994, 371:796-799.
40. Yan S.F., Fujita T., Lu J., Okada K., Shan Zou Y., Mackman N., et al. Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress. Nat Med 2000, 6:1355-1361.
41. Levi G., Topilko P., Schneider-Maunoury S., Lasagna M., Mantero S., Cancedda R., et al. Defective bone formation in Krox-20 mutant mice. Development 1996, 122:113-120.
42. Ji B., Chen X.Q., Misek D.E., Kuick R., Hanash S., Ernst S., et al. Pancreatic gene expression during the initiation of acute pancreatitis: identification of EGR-1 as a key regulator. Physiol Genomics 2003, 14:59-72.
43. Tourtellotte W.G., Milbrandt J. Sensory ataxia and muscle spindle agenesis in mice lacking the transcription factor Egr3. Nat Genet 1998, 20:87-91.
44. Jones M.W., Errington M.L., French P.J., Fine A., Bliss T.V., Garel S., et al. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 2001, 4:289-296.
45. Eid M.A., Kumar M.V., Iczkowski K.A., Bostwick D.G., Tindall D.J. Expression of early growth response genes in human prostate cancer. Cancer Res 1998, 58:2461-2468.
46. Kobayashi D., Yamada M., Kamagata C., Kaneko R., Tsuji N., Nakamura M., et al. Overexpression of early growth response-1 as a metastasis-regulatory factor in gastric cancer. Anticancer Res 2002, 22:3963-3970.
47. Abdulkadir S.A., Qu Z., Garabedian E., Song S.K., Peters T.J., Svaren J., et al. Impaired prostate tumorigenesis in Egr1-deficient mice. Nat Med 2001, 7:101-107.
48. Haas T.L., Stitelman D., Davis S.J., Apte S.S., Madri J.A. Egr-1 mediates extracellular matrix-driven transcription of membrane type 1 matrix metalloproteinase in endothelium. J Biol Chem 1999, 274:22679-22685.
49. Vidal F., Aragones J., Alfranca A., de Landazuri M.O. Up-regulation of vascular endothelial growth factor receptor Flt-1 after endothelial denudation: role of transcription factor Egr-1. Blood 2000, 95:3387-3395.
50. Fernandez-Busquets X., Burger M.M. The main protein of the aggregation factor responsible for species-specific cell adhesion in the marine sponge Microciona prolifera is highly polymorphic. J Biol Chem 1997, 272:27839-27847.
51. Liu C., Rangnekar V.M., Adamson E., Mercola D. Suppression of growth and transformation and induction of apoptosis by EGR-1. Cancer Gene Ther 1998, 5:3-28.
52. Nair P., Muthukkumar S., Sells S.F., Han S.S., Sukhatme V.P., Rangnekar V.M. Early growth response-1-dependent apoptosis is mediated by p53. J Biol Chem 1997, 272:20131-20138.
53. Rao T.K. Human immunodeficiency virus infection in end-stage renal disease patients. Semin Dial 2003, 16:233-244.
54. Thiel G., Cibelli G. Regulation of life and death by the zinc finger transcription factor Egr-1. J Cell Physiol 2002, 193:287-292.
55. Thiel G., Muller I., Rossler O.G. Expression, signaling and function of Egr transcription factors in pancreatic beta-cells and insulin-responsive tissues. Mol Cell Endocrinol 2014, 388:10-19.
56. Eto K., Kaur V., Thomas M.K. Regulation of insulin gene transcription by the immediate-early growth response gene Egr-1. Endocrinology 2006, 147:2923-2935.
57. Eto K., Kaur V., Thomas M.K. Regulation of pancreas duodenum homeobox-1 expression by early growth response-1. J Biol Chem 2007, 282:5973-5983.
58. Garnett K.E., Chapman P., Chambers J.A., Waddell I.D., Boam D.S. Differential gene expression between Zucker Fatty rats and Zucker Diabetic Fatty rats: a potential role for the immediate-early gene Egr-1 in regulation of beta cell proliferation. J Mol Endocrinol 2005, 35:13-25.
59. Kang J.H., Kim M.J., Ko S.H., Jeong I.K., Koh K.H., Rhie D.J., et al. Upregulation of rat Ccnd1 gene by exendin-4 in pancreatic beta cell line INS-1: interaction of early growth response-1 with cis-regulatory element. Diabetologia 2006, 49:969-979.
60. Hayes H.L., Moss L.G., Schisler J.C., Haldeman J.M., Zhang Z., Rosenberg P.B., et al. Pdx-1 activates islet alpha- and beta-cell proliferation via a mechanism regulated by transient receptor potential cation channels 3 and 6 and extracellular signal-regulated kinases 1 and 2. Mol Cell Biol 2013, 33:4017-4029.
61. Muller I., Rossler O.G., Wittig C., Menger M.D., Thiel G. Critical role of Egr transcription factors in regulating insulin biosynthesis, blood glucose homeostasis, and islet size. Endocrinology 2012, 153:3040-3053.
62. Perez-Castillo A., Pipaon C., Garcia I., Alemany S. NGFI-A gene expression is necessary for T lymphocyte proliferation. J Biol Chem 1993, 268:19445-19450.
63. Biesiada E., Razandi M., Levin E.R. Egr-1 activates basic fibroblast growth factor transcription. Mechanistic implications for astrocyte proliferation. J Biol Chem 1996, 271:18576-18581.
64. Kaufmann K., Thiel G. Epidermal growth factor and platelet-derived growth factor induce expression of Egr-1, a zinc finger transcription factor, in human malignant glioma cells. J Neurol Sci 2001, 189:83-91.
65. Hofer G., Grimmer C., Sukhatme V.P., Sterzel R.B., Rupprecht H.D. Transcription factor Egr-1 regulates glomerular mesangial cell proliferation. J Biol Chem 1996, 271:28306-28310.
66. Kaufmann K., Thiel G. Epidermal growth factor and thrombin induced proliferation of immortalized human keratinocytes is coupled to the synthesis of Egr-1, a zinc finger transcriptional regulator. J Cell Biochem 2002, 85:381-391.
67. Bai J., Sata N., Nagai H., Wada T., Yoshida K., Mano H., et al. Genistein-induced changes in gene expression in Panc 1 cells at physiological concentrations of genistein. Pancreas 2004, 29:93-98.
68. Seki T., Kokuryo T., Yokoyama Y., Suzuki H., Itatsu K., Nakagawa A., et al. Antitumor effects of alpha-bisabolol against pancreatic cancer. Cancer Sci 2011, 102:2199-2205.
69. Jutooru I., Chadalapaka G., Chintharlapalli S., Papineni S., Safe S. Induction of apoptosis and nonsteroidal anti-inflammatory drug-activated gene 1 in pancreatic cancer cells by a glycyrrhetinic acid derivative. Mol Carcinog 2009, 48:692-702.
70. Cho K.N., Sukhthankar M., Lee S.H., Yoon J.H., Baek S.J. Green tea catechin (-)-epicatechin gallate induces tumour suppressor protein ATF3 via EGR-1 activation. Eur J Cancer 2007, 43:2404-2412.
71. Whitlock N.C., Bahn J.H., Lee S.H., Eling T.E., Baek S.J. Resveratrol-induced apoptosis is mediated by early growth response-1, Kruppel-like factor 4, and activating transcription factor 3. Cancer Prev Res (Phila) 2011, 4:116-127.
72. Sakamoto K.M., Bardeleben C., Yates K.E., Raines M.A., Golde D.W., Gasson J.C. 5' upstream sequence and genomic structure of the human primary response gene, EGR-1/TIS8. Oncogene 1991, 6:867-871.
73. Whitmarsh A.J., Shore P., Sharrocks A.D., Davis R.J. Integration of MAP kinase signal transduction pathways at the serum response element. Science 1995, 269:403-407.
74. Hoffmann E., Ashouri J., Wolter S., Doerrie A., Dittrich-Breiholz O., Schneider H., et al. Transcriptional regulation of EGR-1 by the interleukin-1-JNK-MKK7-c-Jun pathway. J Biol Chem 2008, 283:12120-12128.
75. Woo S.M., Min K.J., Kim S., Park J.W., Kim D.E., Chun K.S., et al. Silibinin induces apoptosis of HT29 colon carcinoma cells through early growth response-1 (EGR-1)-mediated non-steroidal anti-inflammatory drug-activated gene-1 (NAG-1) up-regulation. Chem Biol Interact 2014, 211:36-43.
76. Li Y.B., Guo C.X., Wang Z.C., Dong L.H., Guan F., Liu Y., et al. Radiosensitization of breast cancer cells by TRAIL-endostatin-targeting gene therapy. Neoplasma 2013, 60:613-619.
77. Liu J.L., Liu X.L., Qian Q., Du Q., Guo S.Y., Li C.J., et al. Expression of the radio-inducible TK suicide gene controlled by Egr-1 promoter in pancreatic cancer cells: an in vitro experiment. Zhonghua Yi Xue Za Zhi 2008, 88:1952-1955.
78. Wenke L., Peng L., Xing W., Yujun S., Qi Z., Haibo R., et al. Treatment of brain glioblastoma multiforme with pcDNA3.1-Egr. 1p-p16 combined with gamma knife radiation: an experimental study on nude mice. Neurol India 2013, 61:491-496.
79. Zwang Y., Oren M., Yarden Y. Consistency test of the cell cycle: roles for p53 and EGR1. Cancer Res 2012, 72:1051-1054.
80. Nesaretnam K., Ambra R., Selvaduray K.R., Radhakrishnan A., Reimann K., Razak G., et al. Tocotrienol-rich fraction from palm oil affects gene expression in tumors resulting from MCF-7 cell inoculation in athymic mice. Lipids 2004, 39:459-467.
81. Nesaretnam K., Meganathan P., Veerasenan S.D., Selvaduray K.R. Tocotrienols and breast cancer: the evidence to date. Genes Nutr 2012, 7:3-9.