Growth of poorly differentiated endometrial carcinoma is inhibited by combined action of medroxyprogesterone acetate and the Ras inhibitor Salirasib

Oncotarget

Volumn 4, Issue 2, 2013, Pages 316-328

  Faigenbaum, Raya ^a   Haklai, Roni ^a   Ben Baruch, Gilad ^a   Kloog, Yoel ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Endometrial cancer; ER ; ER ; FTS; Medroxyprogesterone acetate; Ras

Indexed keywords

ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MEDROXYPROGESTERONE ACETATE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B; PROTEIN C FOS; PROTEIN KINASE B; PROTEIN PS2; RAS PROTEIN; SALIRASIB;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CARCINOMA CELL; CELL DIFFERENTIATION; CELL SURVIVAL; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG EFFECT; DRUG SENSITIZATION; ENDOMETRIUM CARCINOMA; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IC 50; INTRACELLULAR SIGNALING; ONCOGENE C FOS; PROGESTERONE RECEPTOR A GENE; PROGESTERONE RECEPTOR B GENE; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PS2 GENE; UPREGULATION;

EID: 84875778651     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.867     Document Type: Article

References (51)

1. Kim JJ, Kurita T,Bulun SE. Progesterone Action in Endometrial Cancer, Endometriosis, Uterine Fibroids, and Breast Cancer. Endocr Rev. 2013;34:130-62
2. Amant F, Moerman P, Neven P, Timmerman D, Van Limbergen E,Vergote I. Endometrial cancer. Lancet. 2005; 366:491-505.
3. Umene K, Banno K, Kisu I, Yanokura M, Nogami Y, Tsuji K, Masuda K, Ueki A, Kobayashi Y, Yamagami W, Tominaga E, Susumu N,Aoki D. New candidate therapeutic agents for endometrial cancer: Potential for clinical practice (Review). Oncol Rep. 2013;29:855-60
4. Moxley KM,McMeekin DS. Endometrial carcinoma: a review of chemotherapy, drug resistance, and the search for new agents. Oncologist. 2010;15:1026-1033.
5. Samarnthai N, Hall K,Yeh IT. Molecular profiling of endometrial malignancies. Obstet Gynecol Int. 2010;2010:162363.
6. Bergstrom A, Pisani P, Tenet V, Wolk A,Adami HO. Overweight as an avoidable cause of cancer in Europe. Int J Cancer. 2001; 91:421-430.
7. Fisher B, Costantino JP, Wickerham DL, Redmond CK, Kavanah M, Cronin WM, Vogel V, Robidoux A, Dimitrov N, Atkins J, Daly M, Wieand S, Tan-Chiu E, Ford L,Wolmark N. Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Natl Cancer Inst. 1998; 90:1371-1388.
8. Thigpen JT, Brady MF, Alvarez RD, Adelson MD, Homesley HD, Manetta A, Soper JT,Given FT. Oral medroxyprogesterone acetate in the treatment of advanced or recurrent endometrial carcinoma: a dose-response study by the Gynecologic Oncology Group. J Clin Oncol. 1999; 17:1736-1744.
9. Zagouri F, Bozas G, Kafantari E, Tsiatas M, Nikitas N, Dimopoulos MA,Papadimitriou CA. Endometrial cancer: what is new in adjuvant and molecularly targeted therapy? Obstet Gynecol Int. 2010;2010:749579.
10. Fujiwara H, Jobo T, Takei Y, Saga Y, Imai M, Arai T, Taneichi A, Machida S, Takahashi Y,Suzuki M. Fertilitysparing treatment using medroxyprogesterone acetate for endometrial carcinoma. Oncol Lett. 2012;3:1002-1006.
11. del Carmen MG, Birrer M,Schorge JO. Uterine papillary serous cancer: a review of the literature. Gynecol Oncol. 2012;127:651-661.
12. Thomas C,Gustafsson JA. The different roles of ER subtypes in cancer biology and therapy. Nat Rev Cancer. 2011;11:597-608.
13. Bjornstrom L,Sjoberg M. Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol. 2005; 19:833-842.
14. Enmark E, Pelto-Huikko M, Grandien K, Lagercrantz S, Lagercrantz J, Fried G, Nordenskjold M,Gustafsson JA. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab. 1997; 82:4258-4265.
15. Hall JM,McDonnell DP. The estrogen receptor betaisoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology. 1999; 140:5566-5578.
16. Matthews J, Wihlen B, Tujague M, Wan J, Strom A,Gustafsson JA. Estrogen receptor (ER) beta modulates ERalpha-mediated transcriptional activation by altering the recruitment of c-Fos and c-Jun to estrogen-responsive promoters. Mol Endocrinol. 2006; 20:534-543.
17. Krakstad C, Birkeland E, Seidel D, Kusonmano K, Petersen K, Mjos S, Hoivik EA, Wik E, Halle MK, Oyan AM, Kalland KH, Werner HM, Trovik J,Salvesen H. High- Throughput Mutation Profiling of Primary and Metastatic Endometrial Cancers Identifies KRAS, FGFR2 and PIK3CA to Be Frequently Mutated. PLoS ONE. 2012;7:e52795.
18. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Montalto G, Cervello M, Nicoletti F, Fagone P, Malaponte G, Mazzarino MC, Candido S, Libra M, Basecke J, Mijatovic S, Maksimovic-Ivanic D, Milella M, Tafuri A, Cocco L, Evangelisti C, Chiarini F,Martelli AM. Mutations and deregulation of Ras/Raf/MEK/ERK and PI3K/ PTEN/Akt/mTOR cascades which alter therapy response. Oncotarget. 2012;3:954-987.
19. Marciano D, Ben Baruch G, Marom M, Egozi Y, Haklai R,Kloog Y. Farnesyl derivatives of rigid carboxylic acidsinhibitors of ras-dependent cell growth. J Med Chem. 1995; 38:1267-1272.
20. Haklai R, Elad-Sfadia G, Egozi Y,Kloog Y. Orally administered FTS (salirasib) inhibits human pancreatic tumor growth in nude mice. Cancer Chemother Pharmacol. 2008; 61:89-96.
21. Haklai R, Gana-Weisz G, Elad G, Paz A, Marciano D, Egozi Y, Ben Baruch G,Kloog Y. Dislodgment and accelerated degradation of Ras. Biochemistry. 1998; 37:1306-1314.
22. Gana-Weisz M, Haklai R, Marciano D, Egozi Y, Ben-Baruch G,Kloog Y. The Ras antagonist S-farnesylthiosalicylic acid induces inhibition of MAPK activation. Biochem Biophys Res Commun. 1997; 239:900- 904.
23. Aizman E, Mor A, Levy A, George J,Kloog Y. Ras inhibition by FTS attenuates brain tumor growth in mice by direct antitumor activity and enhanced reactivity of cytotoxic lymphocytes. Oncotarget. 2012;3:144-157.
24. Schmukler E, Grinboim E, Schokoroy S, Amir A, Wolfson E, Kloog Y,Pinkas-Kramarski R. Ras inhibition enhances autophagy, which partially protects cells from death. Oncotarget. 2013. In press.
25. Laheru D, Shah P, Rajeshkumar NV, McAllister F, Taylor G, Goldsweig H, Le DT, Donehower R, Jimeno A, Linden S, Zhao M, Song D, Rudek MA,Hidalgo M. Integrated preclinical and clinical development of S-trans, trans- Farnesylthiosalicylic Acid (FTS, Salirasib) in pancreatic cancer. Invest new drugs. 2012;30:2391-2399.
26. Goldberg L, Israeli R,Kloog Y. FTS and 2-DG induce pancreatic cancer cell death and tumor shrinkage in mice. Cell Death Dis. 2012;3:e284.
27. Yaari-Stark S, Nevo-Caspi Y, Jacob-Hircsh J, Rechavi G, Nagler A,Kloog Y. Combining the Ras inhibitor Salirasib and proteasome inhibitor:A potential treatment for multiple myeloma. cancer science and therapy. 2011; 3:187-194.
28. Levy R, Grafi-Cohen M, Kraiem Z,Kloog Y. Galectin-3 promotes chronic activation of K-Ras and differentiation block in malignant thyroid carcinomas. Mol Cancer Ther. 2011; 9:2208-2219.
29. Barkan B, Kloog Y,Ehrlich M. Phenotypic reversion of invasive neurofibromin-deficient schwannoma by FTS: Ras inhibition reduces BMP4/Erk/Smad signaling. Mol Cancer Ther. 2011;10:1317-1326.
30. Zhao S, Choi M, Overton JD, Bellone S, Roque DM, Cocco E, Guzzo F, English DP, Varughese J, Gasparrini S, Bortolomai I, Buza N, Hui P, Abu-Khalaf M, Ravaggi A, Bignotti E, Bandiera E, Romani C, Todeschini P, Tassi R, Zanotti L, Carrara L, Pecorelli S, Silasi DA, Ratner E, Azodi M, Schwartz PE, Rutherford TJ, Stiegler AL, Mane S, Boggon TJ, Schlessinger J, Lifton RP,Santin AD. Landscape of somatic single-nucleotide and copy-number mutations in uterine serous carcinoma. Proc Natl Acad Sci U S A. 2013. In press.
31. Elad-Sfadia G, Haklai R, Ballan E, Gabius HJ,Kloog Y. Galectin-1 augments Ras activation and diverts Ras signals to Raf-1 at the expense of phosphoinositide 3-kinase. J Biol Chem. 2002; 277:37169-37175.
32. Biran A, Brownstein M, Haklai R,Kloog Y. Downregulation of survivin and aurora a by histone deacetylase and RAS inhibitors: A new drug combination for cancer therapy. Int J Cancer. 2010;128:691-701.
33. Mo B, Vendrov AE, Palomino WA, DuPont BR, Apparao KB,Lessey BA. ECC-1 cells: a well-differentiated steroid responsive endometrial cell line with characteristics of luminal epithelium. Biol Reprod. 2006; 75:387-394.
34. Lannigan DA. Estrogen receptor phosphorylation. Steroids. 2003; 68:1-9.
35. Pearce ST,Jordan VC. The biological role of estrogen receptors alpha and beta in cancer. Crit Rev Oncol Hematol. 2004; 50:3-22.
36. Lee YJ,Gorski J. Estrogen-induced transcription of the progesterone receptor gene does not parallel estrogen receptor occupancy. Proc Natl Acad Sci U S A. 1996; 93:15180-15184.
37. Brown AM, Jeltsch JM, Roberts M,Chambon P. Activation of pS2 gene transcription is a primary response to estrogen in the human breast cancer cell line MCF-7. Proc Natl Acad Sci U S A. 1984; 81:6344-6348.
38. Dardes RC, Schafer JM, Pearce ST, Osipo C, Chen B,Jordan VC. Regulation of estrogen target genes and growth by selective estrogen-receptor modulators in endometrial cancer cells. Gynecol Oncol. 2002; 85:498-506.
39. Baron S, Escande A, Alberola G, Bystricky K, Balaguer P,Richard-Foy H. Estrogen receptor alpha and the activating protein-1 complex cooperate during insulin-like growth factor-I-induced transcriptional activation of the pS2/TFF1 gene. J Biol Chem. 2007; 282:11732-11741.
40. Albanito L, Madeo A, Lappano R, Vivacqua A, Rago V, Carpino A, Oprea TI, Prossnitz ER, Musti AM, Ando S,Maggiolini M. G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17beta-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res. 2007; 67:1859-1866.
41. Rio MC, Bellocq JP, Gairard B, Rasmussen UB, Krust A, Koehl C, Calderoli H, Schiff V, Renaud R,Chambon P. Specific expression of the pS2 gene in subclasses of breast cancers in comparison with expression of the estrogen and progesterone receptors and the oncogene ERBB2. Proc Natl Acad Sci U S A. 1987; 84:9243-9247.
42. Duan R, Porter W,Safe S. Estrogen-induced c-fos protooncogene expression in MCF-7 human breast cancer cells: role of estrogen receptor Sp1 complex formation. Endocrinology. 1998; 139:1981-1990.
43. Yang S, Thiel KW,Leslie KK. Progesterone: the ultimate endometrial tumor suppressor. Trends Endocrinol Metab. 2011;22:145-152.
44. Hu Q, Yu L, Chen R, Wang YL, Ji L, Zhang Y, Xie Y,Liao QP. 5-aza-2'-deoxycytidine improves the sensitivity of endometrial cancer cells to progesterone therapy. Int J Gynecol Cancer. 2012;22:951-959.
45. Xie Y, Wang YL, Yu L, Hu Q, Ji L, Zhang Y,Liao QP. Metformin promotes progesterone receptor expression via inhibition of mammalian target of rapamycin (mTOR) in endometrial cancer cells. J Steroid Biochem Mol Biol. 2011;126:113-120.
46. Minig L, Franchi D, Boveri S, Casadio C, Bocciolone L,Sideri M. Progestin intrauterine device and GnRH analogue for uterus-sparing treatment of endometrial precancers and well-differentiated early endometrial carcinoma in young women. Ann Oncol. 2011;22:643-649.
47. Pashov AI, Tskhay VB,Ionouchene SV. The combined GnRH-agonist and intrauterine levonorgestrel-releasing system treatment of complicated atypical hyperplasia and endometrial cancer: a pilot study. Gynecol Endocrinol. 2012;28:559-561.
48. Gonzalez-Rodilla I, Verna V, Munoz AB, Estevez J, Boix M,Schneider J. Expression of the apoptosis-related genes Bcl-2 and p53 in clinical samples from endometrial carcinoma patients. Anticancer Res. 2011;31:4191-4193.
49. Bailey ST, Shin H, Westerling T, Liu XS,Brown M. Estrogen receptor prevents p53-dependent apoptosis in breast cancer. Proc Natl Acad Sci U S A. 2012;109:18060- 18065.
50. Le May C, Chu K, Hu M, Ortega CS, Simpson ER, Korach KS, Tsai MJ,Mauvais-Jarvis F. Estrogens protect pancreatic beta-cells from apoptosis and prevent insulin-deficient diabetes mellitus in mice. Proc Natl Acad Sci U S A. 2006; 103:9232-9237.
51. Juttermann R, Li E,Jaenisch R. Toxicity of 5-aza-2'- deoxycytidine to mammalian cells is mediated primarily by covalent trapping of DNA methyltransferase rather than DNA demethylation. Proc Natl Acad Sci U S A. 1994; 91:11797-11801.