Glucocorticoid-mediated repression of the oncogenic microRNA cluster miR-17-92 contributes to the induction of bim and initiation of apoptosis

Molecular Endocrinology

Volumn 25, Issue 3, 2011, Pages 409-420

  Molitoris, Jason K ^a   McColl, Karen S ^a   Distelhorst, Clark W ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; GLUCOCORTICOID; MICRORNA; MICRORNA 17-92; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; GENE CLUSTER; GENE SILENCING; LYMPHOCYTE; LYMPHOMA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; T CELL LYMPHOMA; UPREGULATION;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL LINE, TUMOR; FEMALE; GLUCOCORTICOIDS; HUMANS; IMMUNOBLOTTING; MALE; MEMBRANE PROTEINS; MICRORNAS; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 79952165235     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2010-0402     Document Type: Article

References (53)

1. Rhen T, Cidlowski JA 2005 Antiinflammatory action of glucocorticoids - new mechanisms for old drugs. N Engl J Med 353:1711-1723
2. Gaynon PS, Carrel AL 1999 Glucocorticosteroid therapy in childhood acute lymphoblastic leukemia. Adv Exp Med Biol 457:593-605 (Pubitemid 129735357)
3. Smets LA, Salomons G, van den Berg J 1999 Glucocorticoid induced apoptosis in leukemia. Adv Exp Med Biol 457:607-614 (Pubitemid 129735358)
4. Cidlowski JA, King KL, Evans-Storms RB, Montague JW, Bortner CD, Hughes Jr FM 1996 The biochemistry and molecular biology of glucocorticoid-induced apoptosis in the immune system. Recent Prog Horm Res 51:457-490; discussion 490-451
5. Schmidt S, Rainer J, Ploner C, Presul E, Riml S, Kofler R 2004 Glucocorticoid-induced apoptosis and glucocorticoid resistance: molecular mechanisms and clinical relevance. Cell Death Differ 11(Suppl 1):S45-S55 (Pubitemid 39136798)
6. Distelhorst CW 2002 Recent insights into the mechanism of glucocorticosteroid-induced apoptosis. Cell Death Differ 9:6-19 (Pubitemid 34071989)
7. Thompson EB, Johnson BH 2003 Regulation of a distinctive set of genes in glucocorticoid-evoked apoptosis in CEM human lymphoid cells. Recent Prog Horm Res 58:175-197 (Pubitemid 37339309)
8. Medh RD, Webb MS, Miller AL, Johnson BH, Fofanov Y, Li T, Wood TG, Luxon BA, Thompson EB 2003 Gene expression profile of human lymphoid CEM cells sensitive and resistant to glucocorticoid-evoked apoptosis. Genomics 81:543-555 (Pubitemid 36627498)
9. Wang Z, Malone MH, He H, McColl KS, Distelhorst CW 2003 Microarray analysis uncovers the induction of the proapoptotic BH3-only protein Bim in multiple models of glucocorticoid-induced apoptosis. J Biol Chem 278:23861-23867 (Pubitemid 36830212)
10. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR 2010 The BCL-2 family reunion. Mol Cell 37:299-310
11. Youle RJ, Strasser A 2008 The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9:47-59
12. O'Connor L, Strasser A, O'Reilly LA, Hausmann G, Adams JM, Cory S, Huang DC 1998 Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J 17:384-395 (Pubitemid 28045479)
13. Strasser A 2005 The role of BH3-only proteins in the immune system. Nat Rev Immunol 5:189-200 (Pubitemid 40364821)
14. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ 2002 Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2:183-192 (Pubitemid 41043974)
15. Cory S, Huang DC, Adams JM 2003 The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22:8590-8607 (Pubitemid 38028528)
16. Abrams MT, Robertson NM, Yoon K, Wickstrom E 2004 Inhibition of glucocorticoid-induced apoptosis by targeting the major splice variants of BIM mRNA with small interfering RNA and short hairpin RNA. J Biol Chem 279:55809-55817
17. Bouillet P, Metcalf D, Huang DC, Tarlinton DM, Kay TW, Köntgen F, Adams JM, Strasser A 1999 Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286:1735-1738 (Pubitemid 129515880)
18. Erlacher M, Michalak EM, Kelly PN, Labi V, Niederegger H, Coultas L, Adams JM, Strasser A, Villunger A 2005 BH3-only proteins Puma and Bim are rate-limiting for γ-radiation- and glucocorticoid-induced apoptosis of lymphoid cells in vivo. Blood 106:4131-4138 (Pubitemid 41775918)
19. Bachmann PS, Gorman R, Mackenzie KL, Lutze-Mann L, Lock RB 2005 Dexamethasone resistance in B-cell precursor childhood acute lymphoblastic leukemia occurs downstream of ligand-induced nuclear translocation of the glucocorticoid receptor. Blood 105:2519-2526 (Pubitemid 40387054)
20. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ 2000 Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol 10:1201-1204
21. Essafi A, Fernández de Mattos S, Hassen YA, Soeiro I, Mufti GJ, Thomas NS, Medema RH, Lam EW 2005 Direct transcriptional regulation of Bim by FoxO3a mediates STI571-induced apoptosis in Bcr-Abl-expressing cells. Oncogene 24:2317-2329 (Pubitemid 40546691)
22. Whitfield J, Neame SJ, Paquet L, Bernard O, Ham J 2001 Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29:629-643 (Pubitemid 32323937)
23. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, Huntington ND, Hughes PD, Michalak EM, McKimm-Breschkin J, Motoyama N, Gotoh T, Akira S, Bouillet P, Strasser A 2007 ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129:1337-1349 (Pubitemid 46962086)
24. Matsui H, Asou H, Inaba T 2007 Cytokines direct the regulation of Bim mRNA stability by heat-shock cognate protein 70. Mol Cell 25:99-112 (Pubitemid 46049065)
25. Ewings KE, Hadfield-Moorhouse K, Wiggins CM, Wickenden JA, Balmanno K, Gilley R, Degenhardt K, White E, Cook SJ 2007 ERK1/2-dependent phosphorylation of BimEL promotes its rapid dissociation from Mcl-1 and Bcl-xL. EMBO J 26:2856-2867 (Pubitemid 46975775)
26. Ley R, Balmanno K, Hadfield K, Weston C, Cook SJ 2003 Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, Bim. J Biol Chem 278:18811-18816 (Pubitemid 36799262)
27. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T 2008 Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132:875-886 (Pubitemid 351312807)
28. Xiao C, Srinivasan L, Calado DP, Patterson HC, Zhang B, Wang J, Henderson JM, Kutok JL, Rajewsky K 2008 Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 9:405-414 (Pubitemid 351405110)
29. Carthew RW, Sontheimer EJ 2009 Origins and Mechanisms of miRNAs and siRNAs. Cell 136:642-655
30. Filipowicz W, Bhattacharyya SN, Sonenberg N 2008 Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9:102-114
31. Ota A, Tagawa H, Karnan S, Tsuzuki S, Karpas A, Kira S, Yoshida Y, Seto M 2004 Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res 64:3087-3095 (Pubitemid 38581408)
32. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, Hammond SM 2005 A microRNA polycistron as a potential human oncogene. Nature 435:828-833 (Pubitemid 40839734)
33. Sibley CH, Tomkins GM 1974 Isolation of lymphoma cell variants resistant to killing by glucocorticoids. Cell 2:213-220
34. Dowd DR, MacDonald PN, Komm BS, Haussler MR, Miesfeld R 1991 Evidence for early induction of calmodulin gene expression in lymphocytes undergoing glucocorticoid-mediated apoptosis. J Biol Chem 266:18423-18426 (Pubitemid 21908098)
35. Fontana L, Fiori ME, Albini S, Cifaldi L, Giovinazzi S, Forloni M, Boldrini R, Donfrancesco A, Federici V, Giacomini P, Peschle C, Fruci D 2008 Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS One 3:e2236
36. Mavrakis KJ, Wolfe AL, Oricchio E, Palomero T, de Keersmaecker K, McJunkin K, Zuber J, James T, Khan AA, Leslie CS, Parker JS, Paddison PJ, Tam W, Ferrando A, Wendel HG 2010 Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia. Nat Cell Biol 12:372-379
37. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, Thomas-Tikhonenko A 2006 Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 38:1060-1065 (Pubitemid 44325933)
38. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N 2005 Combinatorial microRNA target predictions. Nat Genet 37:495-500 (Pubitemid 40617277)
39. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB 2003 Prediction of mammalian microRNA targets. Cell 115:787-798 (Pubitemid 38058492)
40. Hwang HW, Wentzel EA, Mendell JT 2007 A hexanucleotide element directs microRNA nuclear import. Science 315:97-100 (Pubitemid 46196987)
41. Zhang L, Insel PA 2004 The pro-apoptotic protein Bim is a convergence point for cAMP/protein kinase A- and glucocorticoid-promoted apoptosis of lymphoid cells. J Biol Chem 279:20858-20865 (Pubitemid 38656482)
42. Shinjyo T, Kuribara R, Inukai T, Hosoi H, Kinoshita T, Miyajima A, Houghton PJ, Look AT, Ozawa K, Inaba T 2001 Downregulation of Bim, a proapoptotic relative of Bcl-2, is a pivotal step in cytokine-initiated survival signaling in murine hematopoietic progenitors. Mol Cell Biol 21:854-864 (Pubitemid 32104733)
43. Sunters A, Fernández de Mattos S, Stahl M, Brosens JJ, Zoumpoulidou G, Saunders CA, Coffer PJ, Medema RH, Coombes RC, Lam EW 2003 FoxO3a transcriptional regulation of Bim controls apoptosis in paclitaxel-treated breast cancer cell lines. J Biol Chem 278:49795-49805
44. Qi XJ, Wildey GM, Howe PH 2006 Evidence that Ser87 of BimEL is phosphorylated by Akt and regulates BimEL apoptotic function. J Biol Chem 281:813-823
45. Dehan E, Bassermann F, Guardavaccaro D, Vasiliver-Shamis G, Cohen M, Lowes KN, Dustin M, Huang DC, Taunton J, Pagano M 2009 βTrCP- and Rsk1/2-mediated degradation of BimEL inhibits apoptosis. Mol Cell 33:109-116
46. Mendell JT 2008 miRiad roles for the miR-17-92 cluster in development and disease. Cell 133:217-222 (Pubitemid 351508308)
47. Rainer J, Ploner C, Jesacher S, Ploner A, Eduardoff M, Mansha M, Wasim M, Panzer-Grümayer R, Trajanoski Z, Niederegger H, Kofler R 2009 Glucocorticoid-regulated microRNAs and mirtrons in acute lymphoblastic leukemia. Leukemia 23:746-752
48. Smith LK, Shah RR, Cidlowski JA 2010 Glucocorticoids modulate microRNA expression and processing during lymphocyte apoptosis. J Biol Chem 285:36698-36708
49. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT 2005 c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435:839-843 (Pubitemid 40839736)
50. Sylvestre Y, De Guire V, Querido E, Mukhopadhyay UK, Bourdeau V, Major F, Ferbeyre G, Chartrand P 2007 An E2F/miR-20a autoregulatory feedback loop. J Biol Chem 282:2135-2143 (Pubitemid 47076740)
51. Zhou F, Medh RD, Thompson EB 2000 Glucocorticoid mediated transcriptional repression of c-myc in apoptotic human leukemic CEM cells. J Steroid Biochem Mol Biol 73:195-202
52. Kota J, Chivukula RR, O'Donnell KA, Wentzel EA, Montgomery CL, Hwang HW, Chang TC, Vivekanandan P, Torbenson M, Clark KR, Mendell JR, Mendell JT 2009 Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137:1005-1017
53. Lennox KA, Behlke MA 2010 A Direct Comparison of Anti-microRNA Oligonucleotide Potency. Pharm Res 27:1788-1799