2-Methoxyestradiol-induced cell death in osteosarcoma cells is preceded by cell cycle arrest

Journal of Cellular Biochemistry

Volumn 104, Issue 5, 2008, Pages 1937-1945

  Maran, Avudaiappan ^a   Shogren, Kristen L ^a   Benedikt, Michaela ^a   Sarkar, Gobinda ^a   Turner, Russell T ^b   Yaszemski, Michael J ^a  

^a MAYO CLINIC   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Cell cycle arrest; Estrogen metabolite; MG63 cells; PKR

Indexed keywords

2 METHOXYESTRADIOL; CELL MARKER; COMPLEMENTARY DNA; PROTEIN KINASE; PROTEIN P21; PROTEIN P27; PROTEIN P53; STEROID;

ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL DEATH; CONTROLLED STUDY; HUMAN; HUMAN CELL; OSTEOSARCOMA CELL; PRIORITY JOURNAL; TRANSIENT TRANSFECTION;

CELL CYCLE; CELL CYCLE PROTEINS; CELL DEATH; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; EIF-2 KINASE; ESTRADIOL; FLOW CYTOMETRY; GENES, DOMINANT; HUMANS; LIGANDS; MUTANT PROTEINS; OSTEOSARCOMA;

MAMMALIA;

EID: 50249178462     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21758     Document Type: Article

References (59)

1. Aylon Y, Oren M. 2007. Living with p53, dying of p53 [comment]. Cell 130:597-600.
2. Barber GN. 2005. The dsRNA-dependent protein kinase, PER and cell death. Cell Death Differ 12:563-570.
3. Barber GN, Jagus R, Meurs EF, Hovanessian AG, Katze MG. 1995. Molecular mechanisms responsible for malignant transformation by regulatory and catalytic domain variants of the interferon-induced enzyme RNA-dependent protein kinase. J Biol Chem 270: 17423-17428.
4. Barchiesi F, Jackson EK, Fingerle J, Gillespie DG, Odermatt B, Dubey RK. 2006. 2-Methoxyestradiol, an estradiol metabolite, inhibits neointima formation and smooth muscle cell growth via double blockade of the cell cycle. [see comment. Circ Res 99:266-274.
5. Carothers AM, Hughes SA, Ortega D, Bertagnolli MM. 2002. 2-Methoxyestradiol induces p53-associated apoptosis of colorectal cancer cells. Cancer Lett 187:77-86.
6. Catzavelos C, Bhattacharya N, Ung YC, Wilson JA, Roncari L, Sandhu C, Shaw P, Yeger H, Morava-Protzner I, Kapusta L, Franssen E, Pritchard KI, Slingerland JM. 1997. Decreased levels of the cell-cycle inhibitor p27Kip1 protein: Prognostic implications in primary breast cancer [see comment]. Nat Med 3:227-230.
7. Chen X, Ko LJ, Jayaraman L, Prives C. p53 levels, functional domains, and DNA damage determine the extent of the apoptotic response of tumor cells. Genes Dev 10: 1996. 2438-2451.
8. Clemens MJ. 2003. Interferons and apoptosis. J Interferon Cytokine Res 23:277-292.
9. Cuddihy AR, Li S, Tam NW, Wong AH, Taya Y, Abraham N, Bell JC, Koromilas AE. 1999. Double-stranded-RNA-activated protein kinase PKR enhances transcriptional activation by tumor suppressor p5. Mol Cell Biol 19: 2475-2484.
10. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, Wang XF. 1995. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci USA 92: 5545-5549.
11. el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
12. Englert C, Maheswaran S, Garvin AJ, Kreidberg J, Haber DA. 1997. Induction of p21 by the Wilms' tumor suppressor gene WT. Cancer Res 57:1429-1434.
13. Esposito V, Baldi A, De Luca A, Groger AM, Loda M, Giordano GG, Caputi M, Baldi F, Pagano M, Giordano A. 1997. Prognostic role of the cyclin-dependent kinase inhibitor p27 in non-small cell lung cancer. Cancer Res 57:3381-3385.
14. Fong YC, Yang WH, Hsu SF, Hsu HC, Tseng KF, Hsu CJ, Lee CY, Scully SP. 2007. 2-Methoxyestradiol induces apoptosis and cell cycle arrest in human chondrosarcoma cells. J Orthop Res 25:1106-1114.
15. Fotsis T, Zhang Y, Pepper MS, Adlercreutz H, Montesano R, Nawroth PP, Schweigerer L. 1994. The endogenous oestrogen metabolite 2-methoxyoestradiol inhibits angiogenesis and suppresses tumour growth. Nature 368:237-239.
16. Gartel AL, Tyner AL. 1999. Transcriptional regulation of the p21((WAF1/CIP1)) gene. Exp Cell Res 246:280-289.
17. Gartel AL, Tyner AL. 2002. The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol Cancer Therap 1:639-649.
18. Gelbke HP, Knuppen R. 1976. The excretion of five different 2-hydroxyoestrogen monomethyl ethers in human pregnancy urine. J Steroid Biochem 7:457-463.
19. Ghosh R, Ott AM, Seetharam D, Slaga TJ, Kumar AP. 2003. Cell cycle block and apoptosis induction in a human melanoma cell line following treatment with 2-methoxyoestradiol: Therapeutic implications? Melanoma Res 13: 119-127.
20. Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ. 1993. The p21 Cdk-interacting protein Cipl is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805-816.
21. Hershko DD, Shapira M. 2006. Prognostic role of p27Kip1 deregulation in colorectal cancer. Cancer 107:668-675.
22. Huober JB, Nakamura S, Meyn R, Roth JA, Mukhopadhyay T. 2000. Oral administration of an estrogen metabolite-induced potentiation of radiation antitumor effects in presence of wild-type p53 in non-small-cell lung cancer. Int J Radiat Oncol Biol Phys 48:1127-1137.
23. Jiang H, Lin J, Su ZZ, Collart FR, Huberman E, Fisher PB. 1994. Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p5. Oncogene 9:3397-3406.
24. Katayama T, Nakanishi K, Nishihara H, Kamiyama N, Nakagawa T, Kamiyama T, Iseki K, Tanaka S, Todo S. 2007. Type I interferon prolongs cell cycle progression via p21WAF1/CIP1 induction in human colon cancer cells. Int J Oncol 31:613-620.
25. Kennedy AM, Shogren KL, Zhang M, Turner RT, Spelsberg TC, Maran A. 2005. 17beta-estradiol-dependent activation of signal transducer and activator of transcription-1 in human fetal osteoblasts is dependent on Src kinase activity. Endocrinology 146:201-207.
26. Koromilas AE, Roy S, Barber GN, Katze MG, Sonenberg N. 1992. Malignant transformation by a mutant of the IFN-inducible dsRNA-dependent protein kinase. Science 257: 1685-1689.
27. Kumar AP, Garcia GE, Slaga TJ. 2001. 2-methoxyestradiol blocks cell-cycle progression at G(2)/M phase and inhibits growth of human prostate cancer cells. Mol Carcinog 31:111-124.
28. Lin HL, Liu TY, Chau GY, Lui WY, Chi CW. 2000. Comparison of 2-methoxyestradiol-induced, docetaxel-induced, and paclitaxel-induced apoptosis in hepatoma cells and its correlation with reactive oxygen species. Cancer 89:983-994.
29. Liu S, Bishop WR, Liu M. 2003. Differential effects of cell cycle regulatory protein p21(WAF1/Cip1) on apoptosis and sensitivity to cancer chemotherapy. Drug Resist Updates 6:183-195.
30. Loda M, Cukor B, Tam SW, Lavin P, Fiorentino M, Draetta GF, Jessup JM, Pagano M. 1997. Increased proteasome-dependent degradation of the cyclin-dependent kinase inhibitor p27 in aggressive colorectal carcinomas [see comment]. Nat Med 3:231-234.
31. Lotinun S, Westerlind KC, Turner RT. 2001. Tissue-selective effects of continuous release of 2-hydroxyestrone and 16alpha-hydroxyestrone on bone, uterus and mammary gland in ovariectomized growing rats. J Endocrinol 170:165-174.
32. Lottering ML, Haag M, Seegers JC. 1992. Effects of 17 beta-estradiol metabolites on cell cycle events in MCF-7 cells. Cancer Res 52:5926-5932.
33. Maran A, Zhang M, Kennedy AM, Sibonga JD, Rickard DJ, Spelsberg TC, Turner RT. 2002. 2-Methoxyestradiol induces interferon gene expression and apoptosis in osteosarcoma cells. BONE 30:393-398.
34. Meurs EF, Galabru J, Barber GN, Katze MG, Hovanessian AG. 1993. Tumor suppressor function of the interferon-induced double-stranded RNA-activated protein kinase. Proc Natl Acad Sci USA 90:232-236.
35. Mori M, Mimori K, Shiraishi T, Tanaka S, Ueo H, Sugimachi K, Akiyoshi T. 1997. p27 expression and gastric carcinoma. Nat Med 3:593.
36. Mukhopadhyay T, Roth JA. 1997. Induction of apoptosis in human lung cancer cells after wild-type p53 activation by methoxyestradiol. Oncogene 14:379-384.
37. Mukhopadhyay T, Roth JA. 1998. Superinduction of wild-type p53 protein after 2-methoxyestradiol treatment of Ad5p53-transduced cells induces tumor cell apoptosis. Oncogene 17:241-246.
38. Niculescu AB III, Chen X, Smeets M, Hengst L, Prives C, Reed SI. 1998. Effects of p21(Cip1/Waf1) at both the G1/S and the G2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication [erratum appears in Mol Cell Biol 1998 Mar;18(3):1763]. Mol Cell Biol 18:629-643.
39. Noda A, Ning Y, Venable SF, Pereira-Smith OM, Smith JR. 1994. Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp Cell Res 211: 90-98.
40. Ogryzko W, Wong P, Howard BH. 1997. WAF1 retards S-phase progression primarily by inhibition of cyclin-dependent kinases. Mol Cell Biol 17:4877-4882.
41. Pribluda VS, Gubish ER, Jr., Lavallee TM, Treston A, Swartz GM, Green SJ. 2000. 2-Methoxyestradiol: An endogenous antiangiogenic and antiproliferative drug candidate. Cancer Metastasis Rev 19:173-179.
42. Qadan LR, Perez-Stable CM, Anderson C, D'Ippolito G, Herron A, Howard GA, Roos BA. 2001. 2-Methoxyestradiol induces G2/M arrest and apoptosis in prostate cancer. Biochem Biophys Res Commun 285:1259-1266.
43. Reiser F, Way D, Bernas M, Witte M, Witte C. 1998. Inhibition of normal and experimental angiotumor endothelial cell proliferation and cell cycle progression by 2-methoxyestradiol. Proc Soc Exp Biol Med 219:211-216.
44. Robinson JA, Harris SA, Riggs BL, Spelsberg TC, Turner RT, Kidder LS, Zhang M, Westerlind KC. 1997. Estrogen regulation of human osteoblastic cell proliferation and differentiation. Endocrinology 138:2919-2927.
45. Schumacher G, Kataoka M, Roth JA, Mukhopadhyay T. 1999. Potent antitumor activity of 2-methoxyestradiol in human pancreatic cancer cell lines. Clin Cancer Res 5: 493-499.
46. Schumacher G, Scheunert S, Rueggeberg A, Bachem MG, Nussler AK, Spinelli A, Mukhopadhyay T, Pratschke J, Neuhaus P. 2006. A very low toxic agent induces apoptosis and reduces growth of human hepatocellular carcinoma cells. J Gastroenterol Hepatol 21:1207-1212.
47. Seegers JC, Lottering ML, Grobler CJ, van Papendorp DH, Habbersett RC, Shou Y, Lehnert BE. 1997. The mammalian metabolite, 2-methoxyestradiol, affects P53 levels and apoptosis induction in transformed cells but not in normal cells. J Steroid Biochem Mol Biol 62:253-267.
48. Shogren K. Double-stranded RNA dependent protein kinase is involved in 2-methoxyestradiol-mediated cell death in osteosarcoma cells. J Bone Miner Res 2007. 22.
49. Sibonga JD, Sommer U, Turner RT. 2002. Evidence that 2-methoxyestradiol suppresses proliferation and accelerates apoptosis in normal rat growth plate chondrocytes. J Cancer Res Clin Oncol 128:477-483.
50. Somasundaram K, Zhang H, Zeng YX, Houvras Y, Peng Y, Wu GS, Licht JD, Weber BL, El-Deiry WS. 1997. Arrest of the cell cycle by the tumour-suppressor BRCA1 requires the CDK-inhibitor p21WAF1/CiP. Nature 389: 187-190.
51. Tsihlias J, Kapusta LR, DeBoer G, Morava-Protzner I, Zbieranowski I, Bhattacharya N, Catzavelos GC, Klotz LH, Slingerland JM. 1998. Loss of cyclin-dependent kinase inhibitor p27Kip1 is a novel prognostic factor in localized human prostate adenocarcinoma. Cancer Res 58:542-548.
52. Tsihlias J, Kapusta L, Slingerland J. 1999. The prognostic significance of altered cyclin-dependent kinase inhibitors in human cancer. Annu Rev Med 50:401-423.
53. Vousden KH. 2006. Outcomes of p53 activation-spoilt for choice. J Cell Sci 119:5015-5020.
54. Williams BR. 1999. PKR; a sentinel kinase for cellular stress. Oncogene 18:6112-6120.
55. Xiong Y, Hannon GJ, Zhang H, Casso D, Kobayashi R, Beach D. 1993. p21 is a universal inhibitor of cyclin kinases [see comment]. Nature 366:701-704.
56. Yue TL, Wang X, Louden CS, Gupta S, Pillarisetti K, Gu JL, Hart TK, Lysko PG, Feuerstein GZ. 1997. 2-Methoxyestradiol, an endogenous estrogen metabolite, induces apoptosis in endothelial cells and inhibits angiogenesis: Possible role for stress-activated protein kinase signaling pathway and Fas expression. Mol Pharmacol 51:951-962.
57. Zhou NN, Zhu XF, Zhou JM, Li MZ, Zhang XS, Huang P, Jiang WQ. 2004. 2-Methoxyestradiol induces cell cycle arrest and apoptosis of nasopharyngeal carcinoma cells. Acta Pharmacologica Sinica 25:1515-1520.
58. Zhu BT, Conney AH. 1998. Functional role of estrogen metabolism in target cells: Review and perspectives. Carcinogenesis 19:1-27.
59. Zhu BT, Conney AH. 1998. Is 2-methoxyestradiol an endogenous estrogen metabolite that inhibits mammary carcinogenesis? Cancer Res 58:2269-2277.