Studies on molecular mechanisms of growth inhibitory effects of thymoquinone against prostate cancer cells: Role of reactive oxygen species

Experimental Biology and Medicine

Volumn 235, Issue 6, 2010, Pages 751-760

  Koka, Padma Sandeep ^a   Mondal, Debasis ^a   Schultz, Michelle ^a   Abdel Mageed, Asim B ^a   Agrawal, Krishna C ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Androgen receptor; Prostate cancer cells; Reactive oxygen species; Thymoquinone

Indexed keywords

ACETYLCYSTEINE; ANDROGEN RECEPTOR; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; APOPTOSIS INDUCING FACTOR; BAG 1 PROTEIN; BCL2 RELATED PROTEIN A1; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; CASPASE 6; CASPASE 8; CASPASE 9; GLUTATHIONE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN BID; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; THYMOQUINONE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; GROWTH DISORDER; HUMAN; HUMAN CELL; IC 50; PROSTATE CANCER; UPREGULATION;

ANTINEOPLASTIC AGENTS; BENZOQUINONES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION PROFILING; HUMANS; INHIBITORY CONCENTRATION 50; MALE; NIGELLA SATIVA; PROSTATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

NIGELLA SATIVA;

EID: 77953178795     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1258/ebm.2010.009369     Document Type: Article

References (51)

1. Sharifi N, Gulley JL, Dahut WL. Androgen deprivation therapy for prostate cancer. JAMA 2005;294:238-244
2. Crawford ED, Eisenberger MA, McLeod DG, Spaulding JT, Benson R, Dorr FA, Blumenstein BA, Davis MA, Goodman PJ. A controlled trial of leuprolide with and without flutamide in prostatic carcinoma. N Engl J Med 1989;321:419-424 (Pubitemid 19211484)
3. Eisenberger MA, Blumenstein BA, Crawford ED, Miller G, McLeod DG, Loehrer PJ, Wilding G, Sears K, Culkin DJ, Thompson IM Jr, Bueschen AJ, Lowe BA. Bilateral orchiectomy with or without flutamide for metastatic prostate cancer. N Engl J Med 1998;339:1036-1042
4. Gali-Muhtasib H, Roessner A, Schneider-Stock R. Thymoquinone: a promising anti-cancer drug from natural sources. Int J Biochem Cell Biol 2006;38:1249-1253
5. Shoieb AM, Elgayyar M, Dudrick PS, Bell JL, Tithof PK. In vitro inhibition of growth and induction of apoptosis in cancer cell lines by thymoquinone. Int J Oncol 2003;22:107-113
6. Worthen DR, Ghosheh OA, Crooks PA. The in vitro anti-tumor activity of some crude and purified components of blackseed, Nigella sativa L. Anticancer Res 1998;18:1527-1532
7. Gali-Muhtasib H, Diab-Assaf M, Boltze C, Al-Hmaira J, Hartig R, Roessner A, Schneider-Stock R. Thymoquinone extracted from black seed triggers apoptotic cell death in human colorectal cancer cells via a p53-dependent mechanism. Int J Oncol 2004;25:857-866
8. Rooney S, Ryan MF. Effects of alpha-hederin and thymoquinone, constituents of Nigella sativa, on human cancer cell lines. Anticancer Res 2005;25:2199-2204 (Pubitemid 40904623)
9. El-Mahdy MA, Zhu Q, Wang QE, Wani G, Wani AA. Thymoquinone induces apoptosis through activation of caspase-8 and mitochondrial events in p53-null myeloblastic leukemia HL-60 cells. Int J Cancer 2005;117:409-417
10. Sethi G, Ahn KS, Aggarwal BB. Targeting nuclear factor-kappa B activation pathway by thymoquinone: role in suppression of antiapoptotic gene products and enhancement of apoptosis. Mol Cancer Res 2008;6:1059-1070
11. Yi T, Cho SG, Yi Z, Pang X, Rodriguez M, Wang Y, Sethi G, Aggarwal BB, Liu M. Thymoquinone inhibits tumor angiogenesis and tumor growth through suppressing AKT and extracellular signal-regulated kinase signaling pathways. Mol Cancer Ther 2008;7:1789-1796
12. Kaseb AO, Chinnakannu K, Chen D, Sivanandam A, Tejwani S, Menon M, Dou QP, Reddy GP. Androgen receptor and E2F-1 targeted thymoquinone therapy for hormone-refractory prostate cancer. Cancer Res 2007;67:7782-7788
13. Bolton JL, Trush MA, Penning TM, Dryhurst G, Monks TJ. Role of quinones in toxicology. Chem Res Toxicol 2000;13:135-160
14. Simamura E, Hirai K, Shimada H, Koyama J, Niwa Y, Shimizu S. Furanonaphthoquinones cause apoptosis of cancer cells by inducing the production of reactive oxygen species by the mitochondrial voltage-dependent anion channel. Cancer Biol Ther 2006;5:1523-1529
15. Kamal A, Ramu R, Tekumalla V, Khanna GB, Barkume MS, Juvekar AS, Zingde SM. Synthesis, DNA binding, and cytotoxicity studies of pyrrolo[2,1-c][1,4] benzodiazepine-anthraquinone conjugates. Bioorg Med Chem 2007;15:6868-6875
16. Bezerra DP, Alves AP, de Alencar NM, Mesquita Rde O, Lima MW, Pessoa C, de Moraes MO, Lopes JN, Lopes NP, Costa-Lotufo LV. Antitumor activity of two derivatives from 2-acylamine-1, 4-naphthoquinone in mice bearing S180 tumor. J Exp Ther Oncol 2008;7:113-121
17. Kumar MR, Aithal K, Rao BN, Udupa N, Rao BS. Cytotoxic, genotoxic and oxidative stress induced by 1, 4-naphthoquinone in B16F1 melanoma tumor cells. Toxicol In Vitro 2009;23:242-250
18. Higuchi Y. Glutathione depletion-induced chromosomal DNA fragmentation associated with apoptosis and necrosis. J Cell Mol Med 2004;8:455-464 (Pubitemid 44145478)
19. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000;408:239-247
20. Curtin JF, Donovan M, Cotter TG. Regulation and measurement of oxidative stress in apoptosis. J Immunol Methods 2002;265:49-72
21. Giovannini C, Chieco P, Bertaccini A, Gramantieri L, Lacchini M, Martorana G. Checkpoint effectors CDKN1A and Gadd45 correlate with oxidative DNA damage in human prostate carcinoma. Anticancer Res 2004;24:3955-3960 (Pubitemid 40468692)
22. Bower JJ, Leonard SS, Chen F, Shi X. As(III) transcriptionally activates the gadd45a gene via the formation of H2O2. Free Radic Biol Med 2006;41:285-294
23. Adams JM, Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007;26:1324-1337
24. Chen YR, Shrivastava A, Tan TH. Down-regulation of the c-Jun N-terminal kinase (JNK) phosphatase M3/6 and activation of JNK by hydrogen peroxide and pyrrolidine dithiocarbamate. Oncogene 2001;20:367-374
25. Marnett LJ. Lipid peroxidation-DNA damage by malondialdehyde. Mutat Res 1999;424:83-95
26. Shigenaga MK, Ames BN. Assays for 8-hydroxy-2(-deoxyguanosine: a biomarker of in vivo oxidative DNA damage. Free Radic Biol Med 1991;10:211-6
27. van den Dobbelsteen DJ, Nobel CS, Schlegel J, Cotgreave IA, Orrenius S, Slater AF. Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/APO-1 antibody. J Biol Chem 1996;271:15420-15427
28. Hamasu T, Inanami O, Asanuma T, Kuwabara M. Enhanced induction of apoptosis by combined treatment of human carcinoma cells with X rays and death receptor agonists. J Radiat Res (Tokyo) 2005;46:103-110
29. Wang X, Thomas B, Sachdeva R, Arterburn L, Frye L, Hatcher PG, Cornwell DG, Ma J. Mechanism of arylating quinone toxicity involving Michael adduct formation and induction of endoplasmic reticulum stress. Proc Natl Acad Sci USA 2006;103:3604-3609
30. Cornwell DG, Jones KH, Jiang Z, Lantry LE, Southwell-Keely P, Kohar I, Thornton DE. Cytotoxicity of tocopherols and their quinones in drugsensitive and multidrug-resistant leukemia cells. Lipids 1998;33:295-301
31. Barron J, Benghuzzi H, Tucci M. Effects of thymoquinone and selenium on the proliferation of mg 63 cells in tissue culture. Biomed Sci Instrum 2008;44:434-440 (Pubitemid 351619727)
32. Ragheb A, Attia A, Eldin WS, Elbarbry F, Gazarin S, Shoker A. The protective effect of thymoquinone, an anti-oxidant and anti-inflammatory agent, against renal injury: a review. Saudi J Kidney Dis Transpl 2009;20:741-752
33. El-Najjar N, Chatila M, Moukadem H, Vuorela H, Ocker M, Gandesiri M, Schneider-Stock R, Gali-Muhtasib H. Reactive oxygen species mediate thymoquinone-induced apoptosis and activate ERK and JNK signaling. Apoptosis 2010;15:183-195
34. Roepke M, Diestel A, Bajbouj K, Walluscheck D, Schonfeld P, Roessner A, Schneider-Stock R, Gali-Muhtasib H. Lack of p53 augments thymoquinone-induced apoptosis and caspase activation in human osteosarcoma cells. Cancer Biol Ther 2007;6:160-169
35. Wada T, Penninger JM. Mitogen-activated protein kinases in apoptosis regulation. Oncogene 2004;23:2838-2849
36. Sheikh MS, Hollander MC, Fornance AJ Jr. Role of Gadd45 in apoptosis. Biochem Pharmacol 2000;59:43-45
37. Zhan Q, Antinore MJ, Wang XW, Carrier F, Smith ML, Harris CC, Fornace AJ Jr. Association with Cdc2 and inhibition of Cdc2/Cyclin B1 kinase activity by the p53-regulated protein Gadd45. Oncogene 1999;18:2892-2900
38. Cutress RI, Townsend PA, Brimmell M, Bateman AC, Hague A, Packham G. BAG-1 expression and function in human cancer. Br J Cancer 2002;87:834-839
39. Song J, Takeda M, Morimoto RI. Bag1-Hsp70 mediates a physiological stress signaling pathway that regulates Raf-1/ERK and cell growth. Nat Cell Biol 2001;3:276-282
40. Catz SD, Johnson JL. BCL-2 in prostate cancer: a minireview. Apoptosis 2003;8:29-37
41. Reed JC. Bcl-2 and the regulation of programmed cell death. J Cell Biol 1994;124:1-6 (Pubitemid 24054605)
42. Krajewska M, Krajewski S, Epstein JI, Shabaik A, Sauvageot J, Song K, Kitada S, Reed JC. Immunohistochemical analysis of bcl-2, bax, bcl-X, and mcl-1 expression in prostate cancers. Am J Pathol 1996;148:1567-1576 (Pubitemid 26135897)
43. Mayer B, Oberbauer R. Mitochondrial regulation of apoptosis. News Physiol Sci 2003;18:89-94
44. Yin XM. Bid, a BH3-only multi-functional molecule, is at the cross road of life and death. Gene 2006;369:7-19
45. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A, Daugas E, Geuskens M, Kroemer G. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 1996;184:1331-1341
46. Tsujimoto Y. Cell death regulation by the Bcl-2 protein family in the mitochondria. J Cell Physiol 2003;195:158-167
47. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999;397:441-446
48. Kim JT, Kim KD, Song EY, Lee HG, Kim JW, Kim JW, Chae SK, Kim E, Lee MS, Yang Y, Lim JS. Apoptosis-inducing factor (AIF) inhibits protein synthesis by interacting with the eukaryotic translation initiation factor 3 subunit p44 (eIF3g). FEBS Lett 2006;580:6375-6383
49. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002;297:259-263
50. Scher HI, Sawyers CL. Biology of progressive, castration-resistant prostate cancer: directed therapies targeting the androgen-receptor signaling axis. J Clin Oncol 2005;23:8253-8261
51. Husbeck B, Bhattacharyya RS, Feldman D, Knox SJ. Inhibition of androgen receptor signaling by selenite and methylseleninic acid in prostate cancer cells: two distinct mechanisms of action. Mol Cancer Ther 2006;5:2078-2085