Identification of glucocorticoid-induced leucine zipper as a key regulator of tumor cell proliferation in epithelial ovarian cancer

Molecular Cancer

Volumn 8, Issue , 2009, Pages 83-

  Redjimi, Nassima ^a   Gaudin, Françoise ^a   Touboul, Cyril ^a   Emilie, Dominique ^a,b   Pallardy, Marc ^a   Biola Vidamment, Armelle ^a   Fernandez, Hervé ^b   Prévot, Sophie ^b   Balabanian, Karl ^a   Machelon, Véronique ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE INHIBITOR 1A; GLUCOCORTICOID INDUCED LEUCINE ZIPPER; KI 67 ANTIGEN; LEUCINE ZIPPER PROTEIN; PROTEIN KINASE B; RETINOBLASTOMA PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CANCER CELL; CANCER GROWTH; CANCER INVASION; CARCINOGENESIS; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EPITHELIAL OVARIAN CANCER; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; OVARY CANCER; PATHOPHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ADULT; AGED; AGED, 80 AND OVER; CELL PROLIFERATION; CYCLIN D1; CYCLIN-DEPENDENT KINASE INHIBITOR P21; ENZYME ACTIVATION; EPITHELIAL CELLS; FEMALE; GENE SILENCING; HUMANS; MIDDLE AGED; OVARIAN NEOPLASMS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; TRANSCRIPTION FACTORS;

EID: 70449580480     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-8-83     Document Type: Article

References (53)

1. Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC. Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev 2001, 22:255-288. 10.1210/er.22.2.255, 11294827.
2. Yancik R. Ovarian cancer. Age contrasts in incidence, histology, disease stage at diagnosis, and mortality. Cancer 1993, 71:517-523.
3. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ. Cancer statistics, 2008. CA Cancer J Clin 2008, 58:71-96. 10.3322/CA.2007.0010, 18287387.
4. Raspollini MR, Taddei GL. Tumor markers in ovarian carcinoma. Int J Gynaecol Obstet 2007, 97:175-181. 10.1016/j.ijgo.2007.02.011, 17379219.
5. D'Adamio F, Zollo O, Moraca R, Ayroldi E, Bruscoli S, Bartoli A, Cannarile L, Migliorati G, Riccardi C. A new dexamethasone-induced gene of the leucine zipper family protects T lymphocytes from TCR/CD3-activated cell death. Immunity 1997, 7:803-812. 10.1016/S1074-7613(00)80398-2, 9430225.
6. Riccardi C, Cifone MG, Migliorati G. Glucocorticoid hormone-induced modulation of gene expression and regulation of T-cell death: role of GITR and GILZ, two dexamethasone-induced genes. Cell Death Differ 1999, 6:1182-1189. 10.1038/sj.cdd.4400609, 10637434.
7. Riccardi C, Zollo O, Nocentini G, Bruscoli S, Bartoli A, D'Adamio F, Cannarile L, Delfino D, Ayroldi E, Migliorati G. Glucocorticoid hormones in the regulation of cell death. Therapie 2000, 55:165-169.
8. Ayroldi E, Migliorati G, Bruscoli S, Marchetti C, Zollo O, Cannarile L, D'Adamio F, Riccardi C. Modulation of T-cell activation by the glucocorticoid-induced leucine zipper factor via inhibition of nuclear factor kappaB. Blood 2001, 98:743-753. 10.1182/blood.V98.3.743, 11468175.
9. Berrebi D, Bruscoli S, Cohen N, Foussat A, Migliorati G, Bouchet-Delbos L, Maillot MC, Portier A, Couderc J, Galanaud P. Synthesis of glucocorticoid-induced leucine zipper (GILZ) by macrophages: an anti-inflammatory and immunosuppressive mechanism shared by glucocorticoids and IL-10. Blood 2003, 101:729-738. 10.1182/blood-2002-02-0538, 12393603.
10. Cohen N, Mouly E, Hamdi H, Maillot MC, Pallardy M, Godot V, Capel F, Balian A, Naveau S, Galanaud P. GILZ expression in human dendritic cells redirects their maturation and prevents antigen-specific T lymphocyte response. Blood 2006, 107:2037-2044. 10.1182/blood-2005-07-2760, 16293609.
11. Godot V, Garcia G, Capel F, Arock M, Durand-Gasselin I, Asselin-Labat ML, Emilie D, Humbert M. Dexamethasone and IL-10 stimulate glucocorticoid-induced leucine zipper synthesis by human mast cells. Allergy 2006, 61:886-890. 10.1111/j.1398-9995.2006.01065.x, 16792589.
12. Ellestad LE, Malkiewicz SA, Guthrie HD, Welch GR, Porter TE. Expression and regulation of glucocorticoid-induced leucine zipper in the developing anterior pituitary gland. J Mol Endocrinol 2009, 42:171-183. 10.1677/JME-08-0066, 19060181.
13. Robert-Nicoud M, Flahaut M, Elalouf JM, Nicod M, Salinas M, Bens M, Doucet A, Wincker P, Artiguenave F, Horisberger JD. Transcriptome of a mouse kidney cortical collecting duct cell line: effects of aldosterone and vasopressin. Proc Natl Acad Sci USA 2001, 98:2712-2716. 10.1073/pnas.051603198, 30204, 11226305.
14. Tynan SH, Lundeen SG, Allan GF. Cell type-specific bidirectional regulation of the glucocorticoid-induced leucine zipper (GILZ) gene by estrogen. J Steroid Biochem Mol Biol 2004, 91:225-239. 10.1016/j.jsbmb.2004.05.002, 15336700.
15. Ayroldi E, Zollo O, Macchiarulo A, Di Marco B, Marchetti C, Riccardi C. Glucocorticoid-induced leucine zipper inhibits the Raf-extracellular signal-regulated kinase pathway by binding to Raf-1. Mol Cell Biol 2002, 22:7929-7941. 10.1128/MCB.22.22.7929-7941.2002, 134721, 12391160.
16. Mittelstadt PR, Ashwell JD. Inhibition of AP-1 by the glucocorticoid-inducible protein GILZ. J Biol Chem 2001, 276:29603-29610. 10.1074/jbc.M101522200, 11397794.
17. Asselin-Labat ML, David M, Biola-Vidamment A, Lecoeuche D, Zennaro MC, Bertoglio J, Pallardy M. GILZ, a new target for the transcription factor FoxO3, protects T lymphocytes from interleukin-2 withdrawal-induced apoptosis. Blood 2004, 104:215-223. 10.1182/blood-2003-12-4295, 15031210.
18. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 2003, 3:11-22. 10.1038/nrc969, 12509763.
19. Grugan KD, Ma C, Singhal S, Krett NL, Rosen ST. Dual regulation of glucocorticoid-induced leucine zipper (GILZ) by the glucocorticoid receptor and the PI3-kinase/AKT pathways in multiple myeloma. J Steroid Biochem Mol Biol 2008, 110:244-254. 10.1016/j.jsbmb.2007.11.003, 18499442.
20. Bachmann PS, Gorman R, Papa RA, Bardell JE, Ford J, Kees UR, Marshall GM, Lock RB. Divergent mechanisms of glucocorticoid resistance in experimental models of pediatric acute lymphoblastic leukemia. Cancer Res 2007, 67:4482-4490. 10.1158/0008-5472.CAN-06-4244, 17483364.
21. Blind RD, Garabedian MJ. Differential recruitment of glucocorticoid receptor phospho-isoforms to glucocorticoid-induced genes. J Steroid Biochem Mol Biol 2008, 109:150-157. 10.1016/j.jsbmb.2008.01.002, 2699583, 18304804.
22. Chen W, Rogatsky I, Garabedian MJ. MED14 and MED1 differentially regulate target-specific gene activation by the glucocorticoid receptor. Mol Endocrinol 2006, 20:560-572. 10.1210/me.2005-0318, 16239257.
23. Khouja MH, Baekelandt M, Nesland JM, Holm R. The clinical importance of Ki-67, p16, p14, and p57 expression in patients with advanced ovarian carcinoma. Int J Gynecol Pathol 2007, 26:418-425. 10.1097/pgp.0b013e31804216a0, 17885492.
24. Guo RX, Qiao YH, Zhou Y, Li LX, Shi HR, Chen KS. Increased staining for phosphorylated AKT and nuclear factor-kappaB p65 and their relationship with prognosis in epithelial ovarian cancer. Pathol Int 2008, 58:749-756. 10.1111/j.1440-1827.2008.02306.x, 19067848.
25. Altomare DA, Wang HQ, Skele KL, De Rienzo A, Klein-Szanto AJ, Godwin AK, Testa JR. AKT and mTOR phosphorylation is frequently detected in ovarian cancer and can be targeted to disrupt ovarian tumor cell growth. Oncogene 2004, 23:5853-5857. 10.1038/sj.onc.1207721, 15208673.
26. Gao N, Flynn DC, Zhang Z, Zhong XS, Walker V, Liu KJ, Shi X, Jiang BH. G1 cell cycle progression and the expression of G1 cyclins are regulated by PI3K/AKT/mTOR/p70S6K1 signaling in human ovarian cancer cells. Am J Physiol Cell Physiol 2004, 287:C281-291. 10.1152/ajpcell.00422.2003, 15028555.
27. Franke TF. PI3K/Akt: getting it right matters. Oncogene 2008, 27:6473-6488. 10.1038/onc.2008.313, 18955974.
28. Mitsuuchi Y, Johnson SW, Selvakumaran M, Williams SJ, Hamilton TC, Testa JR. The phosphatidylinositol 3-kinase/AKT signal transduction pathway plays a critical role in the expression of p21WAF1/CIP1/SDI1 induced by cisplatin and paclitaxel. Cancer Res 2000, 60:5390-5394.
29. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 1999, 13:1501-1512. 10.1101/gad.13.12.1501, 10385618.
30. Weinberg RA. The retinoblastoma protein and cell cycle control. Cell 1995, 81:323-330. 10.1016/0092-8674(95)90385-2, 7736585.
31. Naora H, Montell DJ. Ovarian cancer metastasis: integrating insights from disparate model organisms. Nat Rev Cancer 2005, 5:355-366. 10.1038/nrc1611, 15864277.
32. Shih Ie M, Kurman RJ. Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol 2004, 164:1511-1518. 1615664, 15111296.
33. Schwartz DR, Kardia SL, Shedden KA, Kuick R, Michailidis G, Taylor JM, Misek DE, Wu R, Zhai Y, Darrah DM. Gene expression in ovarian cancer reflects both morphology and biological behavior, distinguishing clear cell from other poor-prognosis ovarian carcinomas. Cancer Res 2002, 62:4722-4729.
34. Zorn KK, Bonome T, Gangi L, Chandramouli GV, Awtrey CS, Gardner GJ, Barrett JC, Boyd J, Birrer MJ. Gene expression profiles of serous, endometrioid, and clear cell subtypes of ovarian and endometrial cancer. Clin Cancer Res 2005, 11:6422-6430. 10.1158/1078-0432.CCR-05-0508, 16166416.
35. Kobel M, Kalloger SE, Boyd N, McKinney S, Mehl E, Palmer C, Leung S, Bowen NJ, Ionescu DN, Rajput A. Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLoS Med 2008, 5:e232. 10.1371/journal.pmed.0050232, 2592352,2592352, 19053170.
36. Shayesteh L, Lu Y, Kuo WL, Baldocchi R, Godfrey T, Collins C, Pinkel D, Powell B, Mills GB, Gray JW. PIK3CA is implicated as an oncogene in ovarian cancer. Nat Genet 1999, 21:99-102. 10.1038/5042, 9916799.
37. Altomare DA, Testa JR. Perturbations of the AKT signaling pathway in human cancer. Oncogene 2005, 24:7455-7464. 10.1038/sj.onc.1209085, 16288292.
38. Ayroldi E, Zollo O, Bastianelli A, Marchetti C, Agostini M, Di Virgilio R, Riccardi C. GILZ mediates the antiproliferative activity of glucocorticoids by negative regulation of Ras signaling. J Clin Invest 2007, 117:1605-1615. 10.1172/JCI30724, 1865030, 17492054.
39. Abbas T, Dutta A. p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 2009, 9:400-414. 10.1038/nrc2657, 19440234.
40. Muise-Helmericks RC, Grimes HL, Bellacosa A, Malstrom SE, Tsichlis PN, Rosen N. Cyclin D expression is controlled post-transcriptionally via a phosphatidylinositol 3-kinase/Akt-dependent pathway. J Biol Chem 1998, 273:29864-29872. 10.1074/jbc.273.45.29864, 9792703.
41. Liang J, Slingerland JM. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2003, 2:339-345.
42. Zhang W, Yang N, Shi XM. Regulation of mesenchymal stem cell osteogenic differentiation by glucocorticoid-induced leucine zipper (GILZ). J Biol Chem 2008, 283:4723-4729. 10.1074/jbc.M704147200, 18084007.
43. Nam EJ, Kim YT. Alteration of cell-cycle regulation in epithelial ovarian cancer. Int J Gynecol Cancer 2008, 18:1169-1182. 10.1111/j.1525-1438.2008.01191.x, 18298566.
44. Vivanco I, Sawyers CL. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2002, 2:489-501. 10.1038/nrc839, 12094235.
45. Alao JP. The regulation of cyclin D1 degradation: roles in cancer development and the potential for therapeutic invention. Mol Cancer 2007, 6:24. 10.1186/1476-4598-6-24, 1851974, 17407548.
46. Bali A, O'Brien PM, Edwards LS, Sutherland RL, Hacker NF, Henshall SM. Cyclin D1, p53, and p21Waf1/Cip1 expression is predictive of poor clinical outcome in serous epithelial ovarian cancer. Clin Cancer Res 2004, 10:5168-5177. 10.1158/1078-0432.CCR-03-0751, 15297421.
47. Shimizu Y, Kamoi S, Amada S, Akiyama F, Silverberg SG. Toward the development of a universal grading system for ovarian epithelial carcinoma: testing of a proposed system in a series of 461 patients with uniform treatment and follow-up. Cancer 1998, 82:893-901. 10.1002/(SICI)1097-0142(19980301)82:5<893::AID-CNCR14>3.0.CO;2-W, 9486579.
48. Chan TO, Rittenhouse SE, Tsichlis PN. AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide-dependent phosphorylation. Annu Rev Biochem 1999, 68:965-1014. 10.1146/annurev.biochem.68.1.965, 10872470.
49. Noske A, Kaszubiak A, Weichert W, Sers C, Niesporek S, Koch I, Schaefer B, Sehouli J, Dietel M, Lage H, Denkert C. Specific inhibition of AKT2 by RNA interference results in reduction of ovarian cancer cell proliferation: increased expression of AKT in advanced ovarian cancer. Cancer Lett 2007, 246:190-200. 10.1016/j.canlet.2006.02.018, 16584837.
50. Sun M, Wang G, Paciga JE, Feldman RI, Yuan ZQ, Ma XL, Shelley SA, Jove R, Tsichlis PN, Nicosia SV, Cheng JQ. AKT1/PKBalpha kinase is frequently elevated in human cancers and its constitutive activation is required for oncogenic transformation in NIH3T3 cells. Am J Pathol 2001, 159:431-437. 1850562, 11485901.
51. Runz S, Keller S, Rupp C, Stoeck A, Issa Y, Koensgen D, Mustea A, Sehouli J, Kristiansen G, Altevogt P. Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol Oncol 2007, 107:563-571. 10.1016/j.ygyno.2007.08.064, 17900673.
52. Belot MP, Abdennebi-Najar L, Gaudin F, Emilie D, Machelon V. Progesterone increases csk homologous kinase in HMC-1560 human mast cells and reduces cell proliferation. J Cell Biochem 2007, 102:1271-1280. 10.1002/jcb.21357, 17492661.
53. Sansregret L, Goulet B, Harada R, Wilson B, Leduy L, Bertoglio J, Nepveu A. The p110 isoform of the CDP/Cux transcription factor accelerates entry into S phase. Mol Cell Biol 2006, 26:2441-2455. 10.1128/MCB.26.6.2441-2455.2006, 1430290, 16508018.