Phosphatidylinositol 3-kinase signaling in proliferating cells maintains an anti-apoptotic transcriptional program mediated by inhibition of FOXO and non-canonical activation of NFκB transcription factors

BMC Cell Biology

Volumn 9, Issue , 2008, Pages

  Terragni, Jolyon ^a   Graham, Julie R ^a   Adams, Kenneth W ^a,b   Schaffer, Michael E ^a,c   Tullai, John W ^a   Cooper, Geoffrey M ^a  

^a Boston University   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPROTEIN; APOPROTEIN L; ATROGIN 1; BRAIN DERIVED NEUROTROPHIC FACTOR; CONNECTIVE TISSUE GROWTH FACTOR; CYCLIN G2; CYCLINE; DEOXYCYTIDINE KINASE; ENDOTHELIN 1; F BOX PROTEIN; FIBROBLAST GROWTH FACTOR 2; FOLLISTATIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 7; KRUPPEL LIKE FACTOR 6; METALLOTHIONEIN I; METALLOTHIONEIN IE; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 6; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE 31; THROMBOPLASTIN; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR RELB; UNCLASSIFIED DRUG; 2 MORPHOLINO 8 PHENYLCHROMONE; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; CHROMONE DERIVATIVE; FORKHEAD TRANSCRIPTION FACTOR; MORPHOLINE DERIVATIVE; TRANSCRIPTION FACTOR;

APOPTOSIS; ARTICLE; BINDING SITE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; ENZYME REGULATION; GENE EXPRESSION REGULATION; GENE FUNCTION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; PROMOTER REGION; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; CELL CULTURE; CELL STRAIN U937; DNA MICROARRAY; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS; BINDING SITES; CELL PROLIFERATION; CHROMONES; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MORPHOLINES; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR CELLS, CULTURED; U937 CELLS;

EID: 41049085574     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-9-6     Document Type: Article

References (96)

1. Cantley LC The phosphoinositide 3-kinase pathway Science 2002, 296(5573):1655-1657. 10.1126/science.296.5573.1655 12040186
2. Datta SR Brunet A Greenberg ME Cellular survival: A play in three Akts Genes Dev 1999, 13(22):2905-2927. 10.1101/gad.13.22.2905 10579998
3. Datta SR Dudek H Tao X Masters S Fu H Gotoh Y Greenberg ME Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery Cell 1997, 91(2):231-241. 10.1016/S0092-8674(00)80405-5 9346240
4. del Peso L Gonzalez-Garcia M Page C Herrera R Nunez G Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt Science 1997, 278(5338):687-689. 10.1126/science.278.5338.687 9381178
5. Cross DA Alessi DR Cohen P Andjelkovich M Hemmings BA Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B Nature 1995, 378(6559):785-789. 10.1038/378785a0 8524413
6. Pap M Cooper GM Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway J Biol Chem 1998, 273(32):19929-19932. 10.1074/jbc.273.32.19929 9685326
7. Maurer U Charvet C Wagman AS Dejardin E Green DR Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1 Mol Cell 2006, 21(6):749-760. 10.1016/j.molcel.2006.02.009 16543145
8. Diehl JA Cheng M Roussel MF Sherr CJ Glycogen synthase kinase-3β regulates cyclin D1 proteolysis and subcellular localization Genes Dev 1998, 12(22):3499-3511. 317244 9832503 10.1101/gad.12.22.3499
9. Pap M Cooper GM Role of translation initiation factor 2B in control of cell survival by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3β signaling pathway Mol Cell Biol 2002, 22(2):578-586. 10.1128/MCB.22.2.578-586.2002 11756553 139729
10. Doble BW Woodgett JR GSK-3: Tricks of the trade for a multi-tasking kinase J Cell Sci 2003, 116(Pt 7):1175-1186. 10.1242/jcs.00384 12615961
11. Jope RS Johnson GV The glamour and gloom of glycogen synthase kinase-3 Trends Biochem Sci 2004, 29(2):95-102. 10.1016/j.tibs.2003.12.004 15102436
12. Brazil DP Hemmings BA Ten years of protein kinase B signalling: A hard Akt to follow Trends Biochem Sci 2001, 26(11):657-664. 10.1016/ S0968-0004(01)01958-2 11701324
13. Brazil DP Yang ZZ Hemmings BA Advances in protein kinase B signalling: AKTion on multiple fronts Trends Biochem Sci 2004, 29(5):233-242. 10.1016/j.tibs.2004.03.006 15130559
14. Brunet A Bonni A Zigmond MJ Lin MZ Juo P Hu LS Anderson MJ Arden KC Blenis J Greenberg ME Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor Cell 1999, 96(6):857-868. 10.1016/S0092-8674(00)80595-4 10102273
15. Kops GJ de Ruiter ND De Vries-Smits AM Powell DR Bos JL Burgering BM Direct control of the Forkhead transcription factor AFX by protein kinase B Nature 1999, 398(6728):630-634. 10.1038/19328 10217147
16. van der Horst A Burgering BM Stressing the role of FoxO proteins in lifespan and disease Nat Rev Mol Cell Biol 2007, 8(6):440-450. 10.1038/ nrm2190 17522590
17. Mayo LD Donner DB A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus Proc Natl Acad Sci U S A 2001 98 20 11598 11603 10.1073/pnas.181181198 11504915 58775
18. Basu S Totty NF Irwin MS Sudol M Downward J Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis Mol Cell 2003, 11(1):11-23. 10.1016/S1097-2765(02)00776-1 12535517
19. Romashkova JA Makarov SS NF-κB is a target of AKT in anti-apoptotic PDGF signalling Nature 1999, 401(6748):86-90. 10.1038/ 43474 10485711
20. Ozes ON Mayo LD Gustin JA Pfeffer SR Pfeffer LM Donner DB NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase Nature 1999, 401(6748):82-85. 10.1038/43466 10485710
21. Du K Montminy M CREB is a regulatory target for the protein kinase Akt/ PKB J Biol Chem 1998, 273(49):32377-32379. 10.1074/jbc.273.49.32377 9829964
22. Grimes CA Jope RS CREB DNA binding activity is inhibited by glycogen synthase kinase-3 β and facilitated by lithium J Neurochem 2001, 78(6):1219-1232. 10.1046/j.1471-4159.2001.00495.x 11579131 1947002
23. Pulverer BJ Fisher C Vousden K Littlewood T Evan G Woodgett JR Site-specific modulation of c-Myc cotransformation by residues phosphorylated in vivo Oncogene 1994, 9(1):59-70. 8302604
24. Lutterbach B Hann SR Hierarchical phosphorylation at N-terminal transformation-sensitive sites in c-Myc protein is regulated by mitogens and in mitosis Mol Cell Biol 1994, 14(8):5510-5522. 359071 8035827
25. Boyle WJ Smeal T Defize LH Angel P Woodgett JR Karin M Hunter T Activation of protein kinase C decreases phosphorylation of c-Jun at sites that negatively regulate its DNA-binding activity Cell 1991, 64(3):573-584. 10.1016/0092-8674(91)90241-P 1846781
26. Tullai JW Schaffer ME Mullenbrock S Kasif S Cooper GM Identification of transcription factor binding sites upstream of human genes regulated by the phosphatidylinositol 3-kinase and MEK/ERK signaling pathways J Biol Chem 2004, 279(19):20167-20177. 10.1074/jbc.M309260200 14769801
27. Bromann PA Korkaya H Webb CP Miller J Calvin TL Courtneidge SA Platelet-derived growth factor stimulates Src-dependent mRNA stabilization of specific early genes in fibroblasts J Biol Chem 2005, 280(11):10253-10263. 10.1074/jbc.M413806200 15637050
28. Demoulin JB Ericsson J Kallin A Rorsman C Ronnstrand L Heldin CH Platelet-derived growth factor stimulates membrane lipid synthesis through activation of phosphatidylinositol 3-kinase and sterol regulatory element-binding proteins J Biol Chem 2004, 279(34):35392-35402. 10.1074/jbc.M405924200 15213220
29. Gu J Iyer VR PI3K signaling and miRNA expression during the response of quiescent human fibroblasts to distinct proliferative stimuli Genome Biol 2006, 7(5):R42. 10.1186/gb-2006-7-5-r42 16737555 1779520
30. Tullai JW Chen J Schaffer ME Kamenetsky E Kasif S Cooper GM Glycogen synthase kinase-3 represses cyclic AMP response element-binding protein (CREB)-targeted immediate early genes in quiescent cells J Biol Chem 2007, 282(13):9482-9491. 10.1074/jbc.M700067200 17277356 1839957
31. Yao R Cooper GM Growth factor-dependent survival of rodent fibroblasts requires phosphatidylinositol 3-kinase but is independent of pp70S6K activity Oncogene 1996, 13(2):343-351. 8710373
32. Takahashi Y Rayman JB Dynlacht BD Analysis of promoter binding by the E2F and pRB families in vivo: Distinct E2F proteins mediate activation and repression Genes Dev 2000, 14(7):804-816. 316494 10766737
33. Stein GH T98G: An anchorage-independent human tumor cell line that exhibits stationary phase G1 arrest in vitro J Cell Physiol 1979, 99(1):43-54. 10.1002/jcp.1040990107 222778
34. Vlahos CJ Matter WF Hui KY Brown RF A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002) J Biol Chem 1994, 269(7):5241-5248. 8106507
35. Knight ZA Gonzalez B Feldman ME Zunder ER Goldenberg DD Williams O Loewith R Stokoe D Balla A Toth B Balla T Weiss WA Williams RL Shokat KM A pharmacological map of the PI3-K family defines a role for p110α in insulin signaling Cell 2006, 125(4):733-747. 10.1016/ j.cell.2006.03.035 16647110
36. Oyadomari S Mori M Roles of CHOP/GADD153 in endoplasmic reticulum stress Cell Death Differ 2004, 11(4):381-389. 10.1038/sj.cdd.4401373 14685163
37. Selvakumaran M Lin HK Sjin RT Reed JC Liebermann DA Hoffman B The novel primary response gene MyD118 and the proto-oncogenes myb, myc, and bcl-2 modulate transforming growth factor β 1-induced apoptosis of myeloid leukemia cells Mol Cell Biol 1994, 14(4):2352-2360. 358602 8139540
38. Hossain GS van Thienen JV Werstuck GH Zhou J Sood SK Dickhout JG de Koning AB Tang D Wu D Falk E Poddar R Jacobsen DW Zhang K Kaufman RJ Austin RC TDAG51 is induced by homocysteine, promotes detachment-mediated programmed cell death, and contributes to the development of atherosclerosis in hyperhomocysteinemia J Biol Chem 2003, 278(32):30317-30327. 10.1074/jbc.M212897200 12738777
39. Wang CY Mayo MW Korneluk RG Goeddel DV Baldwin AS Jr. NF-κB antiapoptosis: Induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation Science 1998, 281(5383):1680-1683. 10.1126/ science.281.5383.1680 9733516
40. Emery JG McDonnell P Burke MB Deen KC Lyn S Silverman C Dul E Appelbaum ER Eichman C DiPrinzio R Dodds RA James IE Rosenberg M Lee JC Young PR Osteoprotegerin is a receptor for the cytotoxic ligand TRAIL J Biol Chem 1998, 273(23):14363-14367. 10.1074/jbc.273.23.14363 9603945
41. Bennin DA Don AS Brake T McKenzie JL Rosenbaum H Ortiz L DePaoli-Roach AA Horne MC Cyclin G2 associates with protein phosphatase 2A catalytic and regulatory B' subunits in active complexes and induces nuclear aberrations and a G1/S phase cell cycle arrest J Biol Chem 2002, 277(30):27449-27467. 10.1074/jbc.M111693200 11956189
42. Rouault JP Rimokh R Tessa C Paranhos G Ffrench M Duret L Garoccio M Germain D Samarut J Magaud JP BTG1, a member of a new family of antiproliferative genes Embo J 1992, 11(4):1663-1670. 556617 1373383
43. Zhan Q Lord KA Alamo I Jr. Hollander MC Carrier F Ron D Kohn KW Hoffman B Liebermann DA Fornace AJ Jr. The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth Mol Cell Biol 1994, 14(4):2361-2371. 358603 8139541
44. Tullai JW Schaffer ME Mullenbrock S Sholder G Kasif S Cooper GM Immediate-early and delayed primary response genes are distinct in function and genomic architecture J Biol Chem 2007, 282(33):23981-23995. 10.1074/jbc.M702044200 17575275 2039722
45. Wasserman WW Sandelin A Applied bioinformatics for the identification of regulatory elements Nat Rev Genet 2004, 5(4):276-287. 10.1038/nrg1315 15131651
46. Ramaswamy S Nakamura N Sansal I Bergeron L Sellers WR A novel mechanism of gene regulation and tumor suppression by the transcription factor FKHR Cancer Cell 2002, 2(1):81-91. 10.1016/S1535-6108(02)00086-7 12150827
47. Martinez-Gac L Marques M Garcia Z Campanero MR Carrera AC Control of cyclin G2 mRNA expression by forkhead transcription factors: Novel mechanism for cell cycle control by phosphoinositide 3-kinase and forkhead Mol Cell Biol 2004, 24(5):2181-2189. 10.1128/ MCB.24.5.2181-2189.2004 14966295 350549
48. Bakker WJ Blazquez-Domingo M Kolbus A Besooyen J Steinlein P Beug H Coffer PJ Lowenberg B von Lindern M van Dijk TB FoxO3a regulates erythroid differentiation and induces BTG1, an activator of protein arginine methyl transferase 1 J Cell Biol 2004, 164(2):175-184. 10.1083/ jcb.200307056 14734530 2172323
49. Fernandez de Mattos S Essafi A Soeiro I Pietersen AM Birkenkamp KU Edwards CS Martino A Nelson BH Francis JM Jones MC Brosens JJ Coffer PJ Lam EW FoxO3a and BCR-ABL regulate cyclin D2 transcription through a STAT5/BCL6-dependent mechanism Mol Cell Biol 2004, 24(22):10058-10071. 10.1128/MCB.24.22.10058-10071.2004 15509806 525464
50. Tang TT Dowbenko D Jackson A Toney L Lewin DA Dent AL Lasky LA The forkhead transcription factor AFX activates apoptosis by induction of the BCL-6 transcriptional repressor J Biol Chem 2002, 277(16):14255-14265. 10.1074/jbc.M110901200 11777915
51. Sandri M Sandri C Gilbert A Skurk C Calabria E Picard A Walsh K Schiaffino S Lecker SH Goldberg AL Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy Cell 2004, 117(3):399-412. 10.1016/S0092-8674(04)00400-3 15109499
52. Perkins ND Integrating cell-signalling pathways with NF-κB and IKK function Nat Rev Mol Cell Biol 2007, 8(1):49-62. 10.1038/nrm2083 17183360
53. Schreiber J Jenner RG Murray HL Gerber GK Gifford DK Young RA Coordinated binding of NF-κB family members in the response of human cells to lipopolysaccharide Proc Natl Acad Sci U S A 2006, 103(15):5899-5904. 10.1073/pnas.0510996103 16595631 1426243
54. Hong SY Yoon WH Park JH Kang SG Ahn JH Lee TH Involvement of two NF-κ B binding elements in tumor necrosis factor α -, CD40-, and epstein-barr virus latent membrane protein 1-mediated induction of the cellular inhibitor of apoptosis protein 2 gene J Biol Chem 2000, 275(24):18022-18028. 10.1074/jbc.M001202200 10751398
55. Ueda A Okuda K Ohno S Shirai A Igarashi T Matsunaga K Fukushima J Kawamoto S Ishigatsubo Y Okubo T NF-κ B and Sp1 regulate transcription of the human monocyte chemoattractant protein-1 gene J Immunol 1994, 153(5):2052-2063. 8051410
56. Guttridge DC Albanese C Reuther JY Pestell RG Baldwin AS Jr. NF-κB controls cell growth and differentiation through transcriptional regulation of cyclin D1 Mol Cell Biol 1999, 19(8):5785-5799. 84428 10409765
57. Quehenberger P Bierhaus A Fasching P Muellner C Klevesath M Hong M Stier G Sattler M Schleicher E Speiser W Nawroth PP Endothelin 1 transcription is controlled by nuclear factor-κB in AGE-stimulated cultured endothelial cells Diabetes 2000, 49(9):1561-1570. 10.2337/ diabetes.49.9.1561 10969841
58. Mackman N Brand K Edgington TS Lipopolysaccharide-mediated transcriptional activation of the human tissue factor gene in THP-1 monocytic cells requires both activator protein 1 and nuclear factor κ B binding sites J Exp Med 1991, 174(6):1517-1526. 10.1084/ jem.174.6.1517 1744583
59. Tian B Nowak DE Jamaluddin M Wang S Brasier AR Identification of direct genomic targets downstream of the nuclear factor-κB transcription factor mediating tumor necrosis factor signaling J Biol Chem 2005, 280(17):17435-17448. 10.1074/jbc.M500437200 15722553
60. Yang H Sadda MR Yu V Zeng Y Lee TD Ou X Chen L Lu SC Induction of human methionine adenosyltransferase 2A expression by tumor necrosis factor α. Role of NF-κ B and AP-1 J Biol Chem 2003, 278(51):50887-50896. 10.1074/jbc.M307600200 14530285
61. Novak U Cocks BG Hamilton JA A labile repressor acts through the NFkB-like binding sites of the human urokinase gene Nucleic Acids Res 1991, 19(12):3389-3393. 10.1093/nar/19.12.3389 1905804 32833
62. Basile A Sica A d'Aniello E Breviario F Garrido G Castellano M Mantovani A Introna M Characterization of the promoter for the human long pentraxin PTX3. Role of NF-κB in tumor necrosis factor-α and interleukin-1β regulation J Biol Chem 1997, 272(13):8172-8178. 10.1074/jbc.272.13.8172 9079634
63. Lipsky RH Xu K Zhu D Kelly C Terhakopian A Novelli A Marini AM Nuclear factor κB is a critical determinant in N-methyl-D-aspartate receptor-mediated neuroprotection J Neurochem 2001, 78(2):254-264. 10.1046/j.1471-4159.2001.00386.x 11461961
64. Gustin JA Korgaonkar CK Pincheira R Li Q Donner DB Akt regulates basal and induced processing of NF-κB2 (p100) to p52 J Biol Chem 2006, 281(24):16473-16481. 10.1074/jbc.M507373200 16613850
65. Coller HA Sang L Roberts JM A new description of cellular quiescence PLoS Biol 2006, 4(3):e83. 10.1371/journal.pbio.0040083 16509772 1393757
66. el-Deiry WS Kern SE Pietenpol JA Kinzler KW Vogelstein B Definition of a consensus binding site for p53 Nat Genet 1992, 1(1):45-49. 10.1038/ ng0492-45 1301998
67. Davidoff AM Kerns BJ Iglehart JD Marks JR Maintenance of p53 alterations throughout breast cancer progression Cancer Res 1991, 51(10):2605-2610. 1850660
68. Madrid LV Mayo MW Reuther JY Baldwin AS Jr. Akt stimulates the transactivation potential of the RelA/p65 Subunit of NF-κ B through utilization of the Iκ B kinase and activation of the mitogen-activated protein kinase p38 J Biol Chem 2001, 276(22):18934-18940. 10.1074/jbc.M101103200 11259436
69. Madrid LV Wang CY Guttridge DC Schottelius AJ Baldwin AS Jr. Mayo MW Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-κB Mol Cell Biol 2000, 20(5):1626-1638. 10.1128/MCB.20.5.1626-1638.2000 10669740 85346
70. Sizemore N Leung S Stark GR Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-κB p65/RelA subunit Mol Cell Biol 1999, 19(7):4798-4805. 84278 10373529
71. Adams KW Cooper GM Rapid turnover of mcl-1 couples translation to cell survival and apoptosis J Biol Chem 2007, 282(9):6192-6200. 10.1074/ jbc.M610643200 17200126 1831535
72. Meares GP Jope RS Resolution of the nuclear localization mechanism of glycogen synthase kinase-3: Functional effects in apoptosis J Biol Chem 2007, 282(23):16989-17001. 10.1074/jbc.M700610200 17438332 1948884
73. Smyth GK Limma: Linear models for microarray data. In Bioinformatics and Computational Biology Solutions using R and Bioconductor. Gentleman, R., Carey, V., Dudoit, S., Irizarry, R., and Huber, W. (eds) New York, Springer 2005, pp 397-420.
74. Gentleman RC Carey VJ Bates DM Bolstad B Dettling M Dudoit S Ellis B Gautier L Ge Y Gentry J Hornik K Hothorn T Huber W Iacus S Irizarry R Leisch F Li C Maechler M Rossini AJ Sawitzki G Smith C Smyth G Tierney L Yang JY Zhang J Bioconductor: Open software development for computational biology and bioinformatics Genome Biol 2004, 5(10):R80. 10.1186/gb-2004-5-10-r80 15461798 545600
75. Benjamini Y and Hochberg Controlling the false discovery rate: A practical and powerful approach to multiple testing J R Statist Soc 1995, 57:289-300.
76. Beissbarth T Speed TP GOstat: Find statistically overrepresented Gene Ontologies within a group of genes Bioinformatics 2004, 20(9):1464-1465. 10.1093/bioinformatics/bth088 14962934
77. Kel AE Gossling E Reuter I Cheremushkin E Kel-Margoulis OV Wingender E MATCH: A tool for searching transcription factor binding sites in DNA sequences Nucleic Acids Res 2003, 31(13):3576-3579. 10.1093/nar/gkg585 12824369 169193
78. Matys V Kel-Margoulis OV Fricke E Liebich I Land S Barre-Dirrie A Reuter I Chekmenev D Krull M Hornischer K Voss N Stegmaier P Lewicki-Potapov B Saxel H Kel AE Wingender E TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes Nucleic Acids Res 2006 34 Database issue D108-10. 10.1093/nar/gkj143 16381825 1347505
79. Kuhn RM Karolchik D Zweig AS Trumbower H Thomas DJ Thakkapallayil A Sugnet CW Stanke M Smith KE Siepel A Rosenbloom KR Rhead B Raney BJ Pohl A Pedersen JS Hsu F Hinrichs AS Harte RA Diekhans M Clawson H Bejerano G Barber GP Baertsch R Haussler D Kent WJ The UCSC genome browser database: Update 2007 Nucleic Acids Res 2007 35 Database issue D668-73. 10.1093/nar/gkl928 17142222 1669757
80. Albagli-Curiel O Ambivalent role of BCL6 in cell survival and transformation Oncogene 2003, 22(4):507-516. 10.1038/sj.onc.1206152 12555064
81. Matsuda S Rouault J Magaud J Berthet C In search of a function for the TIS21/PC3/BTG1/TOB family FEBS Lett 2001, 497(2-3):67-72. 10.1016/ S0014-5793(01)02436-X 11377414
82. Barone MV Crozat A Tabaee A Philipson L Ron D CHOP (GADD153) and its oncogenic variant, TLS-CHOP, have opposing effects on the induction of G1/S arrest Genes Dev 1994, 8(4):453-464. 10.1101/gad.8.4.453 8125258
83. Bieker JJ Kruppel-like factors: Three fingers in many pies J Biol Chem 2001, 276(37):34355-34358. 10.1074/jbc.R100043200 11443140
84. Wang Z Rong YP Malone MH Davis MC Zhong F Distelhorst CW Thioredoxin-interacting protein (txnip) is a glucocorticoid-regulated primary response gene involved in mediating glucocorticoid-induced apoptosis Oncogene 2006, 25(13):1903-1913. 10.1038/sj.onc.1209218 16301999
85. Ono T Sekino-Suzuki N Kikkawa Y Yonekawa H Kawashima S Alivin 1, a novel neuronal activity-dependent gene, inhibits apoptosis and promotes survival of cerebellar granule neurons J Neurosci 2003, 23(13):5887-5896. 12843293
86. Kalb R The protean actions of neurotrophins and their receptors on the life and death of neurons Trends Neurosci 2005, 28(1):5-11. 10.1016/ j.tins.2004.11.003 15626491
87. Liston P Roy N Tamai K Lefebvre C Baird S Cherton-Horvat G Farahani R McLean M Ikeda JE MacKenzie A Korneluk RG Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes Nature 1996, 379(6563):349-353. 10.1038/379349a0 8552191
88. Eugenin EA D'Aversa TG Lopez L Calderon TM Berman JW MCP-1 (CCL2) protects human neurons and astrocytes from NMDA or HIV-tat-induced apoptosis J Neurochem 2003, 85(5):1299-1311. 10.1046/ j.1471-4159.2003.01775.x 12753088
89. Alberts GF Peifley KA Johns A Kleha JF Winkles JA Constitutive endothelin-1 overexpression promotes smooth muscle cell proliferation via an external autocrine loop J Biol Chem 1994, 269(13):10112-10118. 8144511
90. Nelson JB Udan MS Guruli G Pflug BR Endothelin-1 inhibits apoptosis in prostate cancer Neoplasia 2005, 7(7):631-637. 10.1593/neo.04787 16026642 1501426
91. Cunningham MA Zhu Q Unterman TG Hammond JM Follicle-stimulating hormone promotes nuclear exclusion of the forkhead transcription factor FoxO1a via phosphatidylinositol 3-kinase in porcine granulosa cells Endocrinology 2003, 144(12):5585-5594. 10.1210/en.2003-0678 12960025
92. Russell L Forsdyke DR A human putative lymphocyte G0/G1 switch gene containing a CpG-rich island encodes a small basic protein with the potential to be phosphorylated DNA Cell Biol 1991, 10(8):581-591. 1930693
93. Tanno B Cesi V Vitali R Sesti F Giuffrida ML Mancini C Calabretta B Raschella G Silencing of endogenous IGFBP-5 by micro RNA interference affects proliferation, apoptosis and differentiation of neuroblastoma cells Cell Death Differ 2005, 12(3):213-223. 10.1038/sj.cdd.4401546 15618969
94. Yin P Xu Q Duan C Paradoxical actions of endogenous and exogenous insulin-like growth factor-binding protein-5 revealed by RNA interference analysis J Biol Chem 2004, 279(31):32660-32666. 10.1074/ jbc.M401378200 15155755
95. Mazzucchelli R Durum SK Interleukin-7 receptor expression: Intelligent design Nat Rev Immunol 2007, 7(2):144-154. 10.1038/nri2023 17259970
96. Pulukuri SM Gondi CS Lakka SS Jutla A Estes N Gujrati M Rao JS RNA interference-directed knockdown of urokinase plasminogen activator and urokinase plasminogen activator receptor inhibits prostate cancer cell invasion, survival, and tumorigenicity in vivo J Biol Chem 2005, 280(43):36529-36540. 10.1074/jbc.M503111200 16127174 1351057