Selective glucocorticoid receptor translational isoforms reveal glucocorticoid-induced apoptotic transcriptomes

Cell Death and Disease

Volumn 4, Issue 1, 2013, Pages

  Wu, I ^a,d   Shin, S C ^a   Cao, Y ^a   Bender, I K ^a   Jafari, N ^b   Feng, G ^a   Lin, S ^a,e   Cidlowski, J A ^c   Schleimer, R P ^a   Lu, N Z ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b Genomics Core Facility   (United States)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d New York Presbyterian Columbia University Medical Center   (United States)

^e MARSHFIELD CLINIC   (United States)

Author keywords

alternative translation; apoptosis; glucocorticoid; glucocorticoid receptor; T cell

Indexed keywords

COMPLEMENTARY DNA; DEXAMETHASONE; GLUCOCORTICOID RECEPTOR; GLUCOCORTICOID RECEPTOR A; GLUCOCORTICOID RECEPTOR B; GLUCOCORTICOID RECEPTOR C; GLUCOCORTICOID RECEPTOR D; TRANSCRIPTOME; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; CYTOKINE; GLUCOCORTICOID; ISOPROTEIN; MEMBRANE PROTEIN; MICRORNA; MYC PROTEIN; ONCOPROTEIN;

APOPTOSIS; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA MICROARRAY; DNA MODIFICATION; LEUKEMIA CELL LINE; PRIORITY JOURNAL; CHROMATIN; CYTOLOGY; DRUG EFFECT; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; T LYMPHOCYTE;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CHROMATIN; CYTOKINES; DEXAMETHASONE; GLUCOCORTICOIDS; HUMANS; JURKAT CELLS; MEMBRANE PROTEINS; MICRORNAS; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTORS, GLUCOCORTICOID; T-LYMPHOCYTES; TRANSCRIPTOME;

MLCS; MLOWN;

EID: 84872190061     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2012.193     Document Type: Article

References (52)

1. Rhen T, Cidlowski JA. Antiinflammatory action of glucocorticoids - new mechanisms for old drugs. N Engl J Med 2005; 353: 1711-1723.
2. Mok CL, Gil-Gomez G, Williams O, Coles M, Taga S, Tolaini M et al. Bad can act as a key regulator of T cell apoptosis and T cell development. J Exp Med 1999; 189: 575-586. (Pubitemid 29187379)
3. Wang Z, Malone MH, He H, McColl KS, Distelhorst CW. Microarray analysis uncovers the induction of the proapoptotic BH3-only protein Bim in multiple models of glucocorticoidinduced apoptosis. J Biol Chem 2003; 278: 23 861-23 867.
4. Hoijman E, Rocha Viegas L, Keller Sarmiento MI, Rosenstein RE, Pecci A. Involvement of Bax protein in the prevention of glucocorticoid-induced thymocytes apoptosis by melatonin. Endocrinology 2004; 145: 418-425. (Pubitemid 38094538)
5. Broome HE, Yu AL, Diccianni M, Camitta BM, Monia BP, Dean NM. Inhibition of Bcl-xL expression sensitizes T-cell acute lymphoblastic leukemia cells to chemotherapeutic drugs. Leuk Res 2002; 26: 311-316. (Pubitemid 34037028)
6. Rogatsky I, Hittelman AB, Pearce D, Garabedian MJ. Distinct glucocorticoid receptor transcriptional regulatory surfaces mediate the cytotoxic and cytostatic effects of glucocorticoids. Mol Cell Biol 1999; 19: 5036-5049. (Pubitemid 29289542)
7. Herr I, Gassler N, Friess H, Buchler MW. Regulation of differential pro- And anti-Apoptotic signaling by glucocorticoids. Apoptosis 2007; 12: 271-291. (Pubitemid 46169909)
8. Ploner C, Schmidt S, Presul E, Renner K, Schrocksnadel K, Rainer J et al. Glucocorticoidinduced apoptosis and glucocorticoid resistance in acute lymphoblastic leukemia. J Steroid Biochem Mol Biol 2005; 93: 153-160. (Pubitemid 40602487)
9. Miller AL, Komak S, Webb MS, Leiter EH, Thompson EB. Gene expression profiling of leukemic cells and primary thymocytes predicts a signature for apoptotic sensitivity to glucocorticoids. Cancer Cell Int 2007; 7: 18.
10. Oakley RH, Webster JC, Sar M, Parker Jr. CR, Cidlowski JA. Expression and subcellular distribution of the beta-isoform of the human glucocorticoid receptor. Endocrinology 1997; 138: 5028-5038. (Pubitemid 27460944)
11. Lu NZ, Cidlowski JA. Translational regulatory mechanisms generate N-terminal glucocorticoid receptor isoforms with unique transcriptional target genes. Mol Cell 2005; 18: 331-342. (Pubitemid 41350538)
12. Lu NZ, Collins JB, Grissom SF, Cidlowski JA. Selective regulation of bone cell apoptosis by translational isoforms of the glucocorticoid receptor. Mol Cell Biol 2007; 27: 7143-7160. (Pubitemid 47549751)
13. Riml S, Schmidt S, Ausserlechner MJ, Geley S, Kofler R. Glucocorticoid receptor heterozygosity combined with lack of receptor auto-induction causes glucocorticoid resistance in Jurkat acute lymphoblastic leukemia cells. Cell Death Differ 2004 11(Suppl 1): S65-S72. (Pubitemid 39139546)
14. Buckley AF, Kuo CT, Leiden JM. Transcription factor LKLF is sufficient to program T cell quiescence via a c-Myc - dependent pathway. Nat Immunol 2001; 2: 698-704. (Pubitemid 32747158)
15. Thulasi R, Harbour DV, Thompson EB. Suppression of c-myc is a critical step in glucocorticoid-induced human leukemic cell lysis. J Biol Chem 1993; 268: 18 306-18 312.
16. Zhou F, Medh RD, Thompson EB. Glucocorticoid mediated transcriptional repression of c-myc in apoptotic human leukemic CEM cells. J Steroid Biochem Mol Biol 2000; 73: 195-202.
17. Surjit M, Ganti KP, Mukherji A, Ye T, Hua G, Metzger D et al. Widespread negative response elements mediate direct repression by agonist- liganded glucocorticoid receptor. Cell 2011; 145: 224-241.
18. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, Hsieh JJ et al. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 2006; 8: 1348-1358. (Pubitemid 44835109)
19. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, Czabotar PE et al. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 2007; 315: 856-859.
20. Bouillet P, Metcalf D, Huang DC, Tarlinton DM, Kay TW, Kontgen F et al. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 1999; 286: 1735-1738. (Pubitemid 129515880)
21. Abrams MT, Robertson NM, Yoon K, Wickstrom E. 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 2004; 279: 55 809-55 817.
22. Lu J, Quearry B, Harada H. p38-MAP kinase activation followed by BIM induction is essential for glucocorticoid-induced apoptosis in lymphoblastic leukemia cells. FEBS Lett 2006; 580: 3539-3544. (Pubitemid 44208999)
23. Ploner C, Rainer J, Niederegger H, Eduardoff M, Villunger A, Geley S et al. The BCL2 rheostat in glucocorticoid-induced apoptosis of acute lymphoblastic leukemia. Leukemia 2008; 22: 370-377. (Pubitemid 351250542)
24. Linsley PS, Schelter J, Burchard J, Kibukawa M, Martin MM, Bartz SR et al. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol Cell Biol 2007; 27: 2240-2252. (Pubitemid 46418479)
25. Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 2005; 102: 13944-13949. (Pubitemid 41377683)
26. Rainer J, Ploner C, Jesacher S, Ploner A, Eduardoff M, Mansha M et al. Glucocorticoidregulated microRNAs and mirtrons in acute lymphoblastic leukemia. Leukemia 2009; 23: 746-752.
27. Smith LK, Shah RR, Cidlowski JA. Glucocorticoids modulate microRNA expression and processing during lymphocyte apoptosis. J Biol Chem 2010; 285: 36 698-36 708.
28. Yamaguchi H, Chen J, Bhalla K, Wang HG. Regulation of Bax activation and apoptotic response to microtubule-damaging agents by p53 transcription-dependent and -independent pathways. J Biol Chem 2004; 279: 39 431-39 437.
29. Tudor G, Aguilera A, Halverson DO, Laing ND, Sausville EA. Susceptibility to drug-induced apoptosis correlates with differential modulation of Bad, Bcl-2 and Bcl-xL protein levels. Cell Death Differ 2000; 7: 574-586. (Pubitemid 30303613)
30. Makin GW, Corfe BM, Griffiths GJ, Thistlethwaite A, Hickman JA, Dive C. Damage-induced Bax N-terminal change, translocation to mitochondria and formation of Bax dimers/complexes occur regardless of cell fate. EMBO J 2001; 20: 6306-6315. (Pubitemid 33078704)
31. Marine JC, Topham DJ, McKay C, Wang D, Parganas E, Stravopodis D et al. SOCS1 deficiency causes a lymphocyte-dependent perinatal lethality. Cell 1999; 98: 609-616. (Pubitemid 29418952)
32. Metcalf D, Greenhalgh CJ, Viney E, Willson TA, Starr R, Nicola NA et al. Gigantism in mice lacking suppressor of cytokine signalling-2. Nature 2000; 405: 1069-1073. (Pubitemid 30447793)
33. Ayroldi E, Migliorati G, Bruscoli S, Marchetti C, Zollo O, Cannarile L et al. Modulation of T-cell activation by the glucocorticoid-induced leucine zipper factor via inhibition of nuclear factor kappaB. Blood 2001; 98: 743-753.
34. Jamieson CA, Yamamoto KR. Crosstalk pathway for inhibition of glucocorticoid-induced apoptosis by T cell receptor signaling. Proc Natl Acad Sci USA 2000; 97: 7319-7324. (Pubitemid 30431461)
35. Obexer P, Certa U, Kofler R, Helmberg A. Expression profiling of glucocorticoid-treated T-ALL cell lines: rapid repression of multiple genes involved in RNA-, protein- And nucleotide synthesis. Oncogene 2001; 20: 4324-4336. (Pubitemid 32726874)
36. Schmidt S, Rainer J, Riml S, Ploner C, Jesacher S, Achmuller C et al. Identification of glucocorticoid-response genes in children with acute lymphoblastic leukemia. Blood 2006; 107: 2061-2069. (Pubitemid 43292367)
37. Tissing WJ, den Boer ML, Meijerink JP, Menezes RX, Swagemakers S, van der Spek PJ et al. Genomewide identification of prednisolone-responsive genes in acute lymphoblastic leukemia cells. Blood 2007; 109: 3929-3935. (Pubitemid 46646638)
38. Li R, Moudgil T, Ross HJ, Hu HM. Apoptosis of non-small-cell lung cancer cell lines after paclitaxel treatment involves the BH3-only proapoptotic protein Bim. Cell Death Differ 2005; 12: 292-303. (Pubitemid 40360952)
39. Puthalakath H, Huang DC, O'Reilly LA, King SM, Strasser A. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol Cell 1999; 3: 287-296. (Pubitemid 29290669)
40. Wang D, Muller N, McPherson KG, Reichardt HM. Glucocorticoids engage different signal transduction pathways to induce apoptosis in thymocytes and mature T cells. J Immunol 2006; 176: 1695-1702. (Pubitemid 43134314)
41. Amsterdam A, Sasson R. The anti-inflammatory action of glucocorticoids is mediated by cell type specific regulation of apoptosis. Mol Cell Endocrinol 2002; 189: 1-9. (Pubitemid 34229159)
42. Viegas LR, Hoijman E, Beato M, Pecci A. Mechanisms involved in tissue-specific apopotosis regulated by glucocorticoids. J Steroid Biochem Mol Biol 2008; 109: 273-278.
43. Gross KL, Oakley RH, Scoltock AB, Jewell CM, Cidlowski JA. Glucocorticoid receptor alpha isoform-selective regulation of antiapoptotic genes in osteosarcoma cells: a new mechanism for glucocorticoid resistance. Mol Endocrinol 2011; 25: 1087-1099.
44. Ishmael FT, Fang X, Houser KR, Pearce K, Abdelmohsen K, Zhan M et al. The human glucocorticoid receptor as an RNA-binding protein: global analysis of glucocorticoid receptor-Associated transcripts and identification of a target RNA motif. J Immunol 2011; 186: 1189-1198.
45. Funder JW, Pearce PT, Smith R, Smith AI. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science 1988; 242: 583-585. (Pubitemid 18263202)
46. Albiston AL, Obeyesekere VR, Smith RE, Krozowski ZS. Cloning and tissue distribution of the human 11 beta-hydroxysteroid dehydrogenase type 2 enzyme. Mol Cell Endocrinol 1994; 105: R11-R17.
47. Jenkins BD, Pullen CB, Darimont BD. Novel glucocorticoid receptor coactivator effector mechanisms. Trends Endocrinol Metab 2001; 12: 122-126. (Pubitemid 33714200)
48. Xu J, Li Q. Review of the in vivo functions of the p160 steroid receptor coactivator family. Mol Endocrinol 2003; 17: 1681-1692. (Pubitemid 37072287)
49. Ricci MS, Jin Z, Dews M, Yu D, Thomas-Tikhonenko A, Dicker DT et al. Direct repression of FLIP expression by c-myc is a major determinant of TRAIL sensitivity. Mol Cell Biol 2004; 24: 8541-8555. (Pubitemid 39245075)
50. Popov N, Wanzel M, Madiredjo M, Zhang D, Beijersbergen R, Bernards R et al. The ubiquitin-specific protease USP28 is required for MYC stability. Nat Cell Biol 2007; 9: 765-774. (Pubitemid 47019463)
51. Du P, Kibbe WA, Lin SM. Lumi: a pipeline for processing Illumina microarray. Bioinformatics 2008; 24: 1547-1548. (Pubitemid 351911712)
52. Lin SM, Du P, Huber W, Kibbe WA. Model-based variance-stabilizing transformation for Illumina microarray data. Nucleic Acids Res 2008; 36: e11.