6-Shogaol induces apoptosis in human leukemia cells through a process involving caspase-mediated cleavage of eIF2α

Molecular Cancer

Volumn 12, Issue 1, 2013, Pages

  Liu, Qun ^a   Peng, Yong Bo ^a   Zhou, Ping ^a   Qi, Lian Wen ^a   Zhang, Mu ^a   Gao, Ning ^b   Liu, E Hu ^a   Li, Ping ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

6 shogaol; Apoptosis; eIF2 ; Leukemia; Shotgun proteome

Indexed keywords

6 SHOGAOL; ANTINEOPLASTIC AGENT; CASPASE 3; CASPASE 7; CATHEPSIN D; CTSD PROTEIN; DDX1 PROTEIN; EIF2S1 PROTEIN; GANAB PROTEIN; INITIATION FACTOR 2ALPHA; INTEGRIN; INTERLEUKIN ENHANCER BINDING FACTOR 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NONO PROTEIN; PROTEIN; PROTEOME; SALUBRINAL; SHOGAOL; SSRP1 PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; VIMENTIN;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; LEUKEMIA CELL LINE; MOLECULAR DOCKING; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEOMICS; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT;

EUKARYOTA; ZINGIBER OFFICINALE;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CASPASE 3; CASPASE 7; CATECHOLS; ENZYME ACTIVATION; EUKARYOTIC INITIATION FACTOR-2; HL-60 CELLS; HUMANS; JURKAT CELLS; LEUKEMIA; LEUKOCYTES, MONONUCLEAR; MICE; MICE, INBRED NOD; MICE, NUDE; MICE, SCID; MOLECULAR DOCKING SIMULATION; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; U937 CELLS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84887303412     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-12-135     Document Type: Article

References (44)

1. Shim S, Kim S, Choi DS, Kwon YB, Kwon J. Anti-inflammatory effects of [6]-shogaol: potential roles of HDAC inhibition and HSP70 induction. Food Chem Toxicol 2011, 49:2734-2740. 10.1016/j.fct.2011.08.012, 21864631.
2. Haniadka R, Rajeev AG, Palatty PL, Arora R, Baliga MS. Zingiber officinale (ginger) as an anti-emetic in cancer chemotherapy: a review. J Altern Complement Med 2012, 18:440-444. 10.1089/acm.2010.0737, 22540971.
3. Gan FF, Nagle AA, Ang X, Ho OH, Tan SH, Yang H, Chui WK, Chew EH. Shogaols at proapoptotic concentrations induce G(2)/M arrest and aberrant mitotic cell death associated with tubulin aggregation. Apoptosis 2011, 16:856-867. 10.1007/s10495-011-0611-3, 21598039.
4. Li F, Nitteranon V, Tang X, Liang J, Zhang G, Parkin KL, Hu Q. In vitro antioxidant and anti-inflammatory activities of 1-dehydro-[6]-gingerdione, 6-shogaol, 6-dehydroshogaol and hexahydrocurcumin. Food Chem 2012, 135:332-337. 10.1016/j.foodchem.2012.04.145, 22868095.
5. Hung JY, Hsu YL, Li CT, Ko YC, Ni WC, Huang MS, Kuo PL. 6-Shogaol, an active constituent of dietary ginger, induces autophagy by inhibiting the AKT/mTOR pathway in human non-small cell lung cancer A549 cells. J Agric Food Chem 2009, 57:9809-9816. 10.1021/jf902315e, 19799425.
6. Pan MH, Hsieh MC, Kuo JM, Lai CS, Wu H, Sang S, Ho CT. 6-Shogaol induces apoptosis in human colorectal carcinoma cells via ROS production, caspase activation, and GADD 153 expression. Mol Nutr Food Res 2008, 52:527-537. 10.1002/mnfr.200700157, 18384088.
7. Hu R, Zhou P, Peng YB, Xu X, Ma J, Liu Q, Zhang L, Wen XD, Qi LW, Gao N, Li P. 6-Shogaol induces apoptosis in human hepatocellular carcinoma cells and exhibits anti-tumor activity in vivo through endoplasmic reticulum stress. PLoS One 2012, 7:e39664. 10.1371/journal.pone.0039664, 3387266, 22768104.
8. Weng CJ, Chou CP, Ho CT, Yen GC. Molecular mechanism inhibiting human hepatocarcinoma cell invasion by 6-shogaol and 6-gingerol. Mol Nutr Food Res 2012, 56:1304-1314. 10.1002/mnfr.201200173, 22714996.
9. Ling H, Yang H, Tan SH, Chui WK, Chew EH. 6-Shogaol, an active constituent of ginger, inhibits breast cancer cell invasion by reducing matrix metalloproteinase-9 expression via blockade of nuclear factor-kappaB activation. Br J Pharmacol 2010, 161:1763-1777. 10.1111/j.1476-5381.2010.00991.x, 3010581, 20718733.
10. Chen CY, Yang YH, Kuo SY. Effect of [6]-shogaol on cytosolic Ca2+ levels and proliferation in human oral cancer cells (OC2). J Nat Prod 2010, 73:1370-1374. 10.1021/np100213a, 20669930.
11. Ishiguro K, Ando T, Watanabe O, Goto H. Specific reaction of alpha, beta-unsaturated carbonyl compounds such as 6-shogaol with sulfhydryl groups in tubulin leading to microtubule damage. FEBS Lett 2008, 582:3531-3536. 10.1016/j.febslet.2008.09.027, 18805415.
12. Hong BH, Wu CH, Yeh CT, Yen GC. Invadopodia-associated proteins blockade as a novel mechanism for 6-shogaol and pterostilbene to reduce breast cancer cell motility and invasion. Mol Nutr Food Res 2013, 57:886-895. 10.1002/mnfr.201200715, 23417847.
13. Liu Q, Peng YB, Qi LW, Cheng XL, Xu XJ, Liu LL, Liu EH, Li P. The cytotoxicity mechanism of 6-Shogaol-treated HeLa human cervical cancer cells revealed by label-free shotgun proteomics and bioinformatics analysis. Evid Based Complement Alternat Med 2013, 2012:278652.
14. Reed JC. Apoptosis-regulating proteins as targets for drug discovery. Trends Mol Med 2001, 7:314-319. 10.1016/S1471-4914(01)02026-3, 11425640.
15. Herr I, Debatin KM. Cellular stress response and apoptosis in cancer therapy. Blood 2001, 98:2603-2614. 10.1182/blood.V98.9.2603, 11675328.
16. Rao RV, Ellerby HM, Bredesen DE. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 2004, 11:372-380. 10.1038/sj.cdd.4401378, 14765132.
17. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403:98-103. 10.1038/47513, 10638761.
18. Kim I, Shu CW, Xu W, Shiau CW, Grant D, Vasile S, Cosford ND, Reed JC. Chemical biology investigation of cell death pathways activated by endoplasmic reticulum stress reveals cytoprotective modulators of ASK1. J Biol Chem 2009, 284:1593-1603. 2615512, 19004820.
19. Yamaguchi H, Wang HG. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J Biol Chem 2004, 279:45495-45502. 10.1074/jbc.M406933200, 15322075.
20. Wang G, Wu WW, Zeng W, Chou CL, Shen RF. Label-free protein quantification using LC-coupled ion trap or FT mass spectrometry: reproducibility, linearity, and application with complex proteomes. J Proteome Res 2006, 5:1214-1223. 10.1021/pr050406g, 16674111.
21. Chen LJ, Seo JH, Eller MJ, Verkhoturov SV, Shah SS, Revzin A, Schweikert EA. Quantitative label-free characterization of avidin-biotin assemblies on silanized glass. Anal Chem 2011, 83:7173-7178. 10.1021/ac2016085, 3186069, 21842883.
22. Ito T, Marintchev A, Wagner G. Solution structure of human initiation factor eIF2alpha reveals homology to the elongation factor eEF1B. Structure 2004, 12:1693-1704. 10.1016/j.str.2004.07.010, 15341733.
23. Li X, Xu X, Wang J, Yu H, Wang X, Yang H, Xu H, Tang S, Li Y, Yang L, et al. A system-level investigation into the mechanisms of Chinese Traditional Medicine: compound Danshen Formula for cardiovascular disease treatment. PLoS One 2012, 7:e43918. 10.1371/journal.pone.0043918, 3433480, 22962593.
24. Srivastava SP, Kumar KU, Kaufman RJ. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J Biol Chem 1998, 273:2416-2423. 10.1074/jbc.273.4.2416, 9442091.
25. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 2000, 101:249-258. 10.1016/S0092-8674(00)80835-1, 10847680.
26. Earnshaw WC, Martins LM, Kaufmann SH. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 1999, 68:383-424. 10.1146/annurev.biochem.68.1.383, 10872455.
27. Bokoch GM. Caspase-mediated activation of PAK2 during apoptosis: proteolytic kinase activation as a general mechanism of apoptotic signal transduction?. Cell Death Differ 1998, 5:637-645. 10.1038/sj.cdd.4400405, 10200518.
28. Jiang HY, Wek RC. Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J Biol Chem 2005, 280:14189-14202. 10.1074/jbc.M413660200, 15684420.
29. Kim R, Emi M, Tanabe K, Murakami S. Role of the unfolded protein response in cell death. Apoptosis 2006, 11:5-13. 10.1007/s10495-005-3088-0, 16374548.
30. Drexler HC. Synergistic apoptosis induction in leukemic cells by the phosphatase inhibitor salubrinal and proteasome inhibitors. PLoS One 2009, 4:e4161. 10.1371/journal.pone.0004161, 2613525, 19129918.
31. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 2005, 307:935-939. 10.1126/science.1101902, 15705855.
32. Hamanaka RB, Bennett BS, Cullinan SB, Diehl JA. PERK and GCN2 contribute to eIF2alpha phosphorylation and cell cycle arrest after activation of the unfolded protein response pathway. Mol Biol Cell 2005, 16:5493-5501. 10.1091/mbc.E05-03-0268, 1289396, 16176978.
33. Liu Y, Laszlo C, Liu W, Chen X, Evans SC, Wu S. Regulation of G(1) arrest and apoptosis in hypoxia by PERK and GCN2-mediated eIF2alpha phosphorylation. Neoplasia 2010, 12:61-68. 2805884, 20072654.
34. Marissen WE, Guo Y, Thomas AA, Matts RL, Lloyd RE. Identification of caspase 3-mediated cleavage and functional alteration of eukaryotic initiation factor 2alpha in apoptosis. J Biol Chem 2000, 275:9314-9323. 10.1074/jbc.275.13.9314, 10734073.
35. Schewe DM, Aguirre-Ghiso JA. ATF6alpha-Rheb-mTOR signaling promotes survival of dormant tumor cells in vivo. Proc Natl Acad Sci USA 2008, 105:10519-10524. 10.1073/pnas.0800939105, 2492459, 18650380.
36. Schewe DM, Aguirre-Ghiso JA. Inhibition of eIF2alpha dephosphorylation maximizes bortezomib efficiency and eliminates quiescent multiple myeloma cells surviving proteasome inhibitor therapy. Cancer Res 2009, 69:1545-1552. 10.1158/0008-5472.CAN-08-3858, 2726651, 19190324.
37. Wang W, Li CY, Wen XD, Li P, Qi LW. Simultaneous determination of 6-gingerol, 8-gingerol, 10-gingerol and 6-shogaol in rat plasma by liquid chromatography-mass spectrometry: application to pharmacokinetics. J Chromatogr B Analyt Technol Biomed Life Sci 2009, 877:671-679. 10.1016/j.jchromb.2009.01.021, 19201263.
38. Gao N, Rahmani M, Shi X, Dent P, Grant S. Synergistic antileukemic interactions between 2-medroxyestradiol (2-ME) and histone deacetylase inhibitors involve Akt down-regulation and oxidative stress. Blood 2006, 107:241-249. 10.1182/blood-2005-06-2409, 1895355, 16141349.
39. Peng Y-B, Zhou P, Chu C, Liu E-H, Wen X-D, Liu Q, Chen J, Gao N, Qi L-W, Li P. Proteomic analysis for malonylastragaloside I in U937 leukemia cells by modified label-free quantitative strategy with LC Chip Q-TOF MS/MS. Chinese Journal of Natural Medicines 2011, 9:305-316.
40. Thomas PD, Kejariwal A, Guo N, Mi H, Campbell MJ, Muruganujan A, Lazareva-Ulitsky B. Applications for protein sequence-function evolution data: mRNA/protein expression analysis and coding SNP scoring tools. Nucleic Acids Res 2006, 34:W645-W650. 10.1093/nar/gkl229, 1538848, 16912992.
41. Hou X, Du J, Zhang J, Du L, Fang H, Li M. How to improve docking accuracy of AutoDock4.2: a case study using different electrostatic potentials. J Chem Inf Model 2012, 53:188-200.
42. Rosenfeld RJ, Goodsell DS, Musah RA, Morris GM, Goodin DB, Olson AJ. Automated docking of ligands to an artificial active site: augmenting crystallographic analysis with computer modeling. J Comput Aided Mol Des 2003, 17:525-536.
43. Cheng S, Gao N, Zhang Z, Chen G, Budhraja A, Ke Z, Son YO, Wang X, Luo J, Shi X. Quercetin induces tumor-selective apoptosis through downregulation of Mcl-1 and activation of Bax. Clin Cancer Res 2010, 16:5679-5691. 10.1158/1078-0432.CCR-10-1565, 3069720, 21138867.
44. Yu C, Rahmani M, Conrad D, Subler M, Dent P, Grant S. The proteasome inhibitor bortezomib interacts synergistically with histone deacetylase inhibitors to induce apoptosis in Bcr/Abl + cells sensitive and resistant to STI571. Blood 2003, 102:3765-3774. 10.1182/blood-2003-03-0737, 12893773.