Doxorubicin-mediated apoptosis in glioma cells requires NFAT3

Cellular and Molecular Life Sciences

Volumn 66, Issue 24, 2009, Pages 3967-3978

  Gopinath, Sreelatha ^a   Vanamala, Sravan K ^a   Gujrati, Meena ^a   Klopfenstein, Jeffrey D ^a   Dinh, Dzung H ^a   Rao, Jasti S ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Doxorubicin and apoptosis; Glioma; NFAT3; SNB19; U87

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE DIPHOSPHATE RIBOSE; CASPASE 10; CASPASE 3; DOXORUBICIN; MATRIGEL; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR NFAT3; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL INVASION; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; DNA FRAGMENTATION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; FLUORESCENCE ACTIVATED CELL SORTING; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; NICK END LABELING; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; WOUND HEALING;

ACTIVE TRANSPORT, CELL NUCLEUS; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; BLOTTING, WESTERN; CASPASE 10; CASPASE 3; CELL LINE, TUMOR; CELL MOVEMENT; CELL NUCLEUS; CELL SURVIVAL; DOXORUBICIN; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; G0 PHASE; G1 PHASE; GLIOMA; HUMANS; NFATC TRANSCRIPTION FACTORS; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN TRANSPORT; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 70849087248     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-009-0157-5     Document Type: Article

References (64)

1. H Ohgaki P Kleihues 2005 Epidemiology and etiology of gliomas Acta Neuropathol 109 93 108 10.1007/s00401-005-0991-y 15685439 (Pubitemid 40287792)
2. JW Campbell IF Pollack AJ Martinez B Shultz 1996 High-grade astrocytomas in children: radiologically complete resection is associated with an excellent long-term prognosis Neurosurgery 38 258 264 10.1097/00006123-199602000-00006 1:STN:280:DyaK2s%2Fit1KqsA%3D%3D 8869052 (Pubitemid 26030704)
3. BC Devaux JR O'Fallon PJ Kelly 1993 Resection, biopsy, and survival in malignant glial neoplasms. A retrospective study of clinical parameters, therapy, and outcome J Neurosurg 78 767 775 10.3171/jns.1993.78.5.0767 1:STN:280:DyaK3s3isV2ktw%3D%3D 8468607
4. A Ashkenazi VM Dixit 1998 Death receptors: signaling and modulation Science 281 1305 1308 10.1126/science.281.5381.1305 1:CAS:528:DyaK1cXlvVegsL0%3D 9721089
5. G Minotti P Menna E Salvatorelli G Cairo L Gianni 2004 Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity Pharmacol Rev 56 185 229 10.1124/pr.56.2.6 1:CAS:528: DC%2BD2cXltlKgtb0%3D 15169927 (Pubitemid 38720829)
6. PG Hogan L Chen J Nardone A Rao 2003 Transcriptional regulation by calcium, calcineurin, and NFAT Genes Dev 17 2205 2232 10.1101/gad.1102703 1:CAS:528:DC%2BD3sXnsFaitbo%3D 12975316 (Pubitemid 37128637)
7. V Horsley GK Pavlath 2002 NFAT: ubiquitous regulator of cell differentiation and adaptation J Cell Biol 156 771 774 10.1083/jcb.200111073 1:CAS:528:DC%2BD38XitVGmsbw%3D 11877454 (Pubitemid 34839859)
8. T Hoey YL Sun K Williamson X Xu 1995 Isolation of two new members of the NFAT gene family and functional characterization of the NFAT proteins Immunity 2 461 472 10.1016/1074-7613(95)90027-6 1:CAS:528:DyaK2MXlvVWrsLo%3D 7749981
9. L Lyakh P Ghosh NR Rice 1997 Expression of NFAT-family proteins in normal human T cells Mol Cell Biol 17 2475 2484 1:STN:280:DyaK2s3msFekuw%3D%3D 9111316 (Pubitemid 27175128)
10. AB Benedito M Lehtinen R Massol UG Lopes T Kirchhausen A Rao A Bonni 2005 The transcription factor NFAT3 mediates neuronal survival J Biol Chem 280 2818 2825 10.1074/jbc.M408741200 1:CAS:528:DC%2BD2MXmt1ylsg%3D%3D 15537643 (Pubitemid 40189389)
11. PB Bushdid H Osinska RR Waclaw JD Molkentin KE Yutzey 2003 NFATc3 and NFATc4 are required for cardiac development and mitochondrial function Circ Res 92 1305 1313 10.1161/01.RES.0000077045.84609.9F 1:CAS:528:DC%2BD3sXks1Kmsrk%3D 12750314 (Pubitemid 36773472)
12. RD Groth PG Mermelstein 2003 Brain-derived neurotrophic factor activation of NFAT (nuclear factor of activated T cells)-dependent transcription: a role for the transcription factor NFATc4 in neurotrophin-mediated gene expression J Neurosci 23 8125 8134 1:CAS:528:DC%2BD3sXnt1Wqtb8%3D 12954875
13. HB Kim M Kong TM Kim YH Suh WH Kim JH Lim JH Song MH Jung 2006 NFATc4 and ATF3 negatively regulate adiponectin gene expression in 3T3-L1 adipocytes Diabetes 55 1342 1352 10.2337/db05-1507 1:CAS:528:DC%2BD28XksFahtL0%3D 16644691 (Pubitemid 44195373)
14. S Mathew E Mascareno MA Siddiqui 2004 A ternary complex of transcription factors, Nished and NFATc4, and co-activator p300 bound to an intronic sequence, intronic regulatory element, is pivotal for the up-regulation of myosin light chain-2v gene in cardiac hypertrophy J Biol Chem 279 41018 41027 10.1074/jbc.M403578200 1:CAS:528:DC%2BD2cXnslWnu7s%3D 15272022 (Pubitemid 39287703)
15. H Zhang X Xie X Zhu J Zhu C Hao Q Lu L Ding Y Liu L Zhou Y Liu C Huang C Wen Q Ye 2005 Stimulatory cross-talk between NFAT3 and estrogen receptor in breast cancer cells J Biol Chem 280 43188 43197 10.1074/jbc.M506598200 1:CAS:528:DC%2BD2MXhtlCmsb3O 16219765 (Pubitemid 43049285)
16. A Rao C Luo PG Hogan 1997 Transcription factors of the NFAT family: regulation and function Annu Rev Immunol 15 707 747 10.1146/annurev.immunol.15. 1.707 1:CAS:528:DyaK2sXisVCmtLc%3D 9143705 (Pubitemid 27169297)
17. S Baksh HR Widlund AA Frazer-Abel J Du S Fosmire DE Fisher JA DeCaprio JF Modiano SJ Burakoff 2002 NFATc2-mediated repression of cyclin-dependent kinase 4 expression Mol Cell 10 1071 1081 10.1016/S1097-2765(02)00701-3 1:CAS:528:DC%2BD38Xptl2ksb4%3D 12453415 (Pubitemid 35453825)
18. PN Cockerill MF Shannon AG Bert GR Ryan MA Vadas 1993 The granulocyte-macrophage colony-stimulating factor/interleukin 3 locus is regulated by an inducible cyclosporin A-sensitive enhancer Proc Natl Acad Sci USA 90 2466 2470 10.1073/pnas.90.6.2466 1:CAS:528:DyaK3sXitVKrt70%3D 8460159
19. MA Iniguez S Martinez-Martinez C Punzon JM Redondo M Fresno 2000 An essential role of the nuclear factor of activated T cells in the regulation of the expression of the cyclooxygenase-2 gene in human T lymphocytes J Biol Chem 275 23627 23635 10.1074/jbc.M001381200 1:CAS:528:DC%2BD3cXls12mtb8%3D 10816557 (Pubitemid 30624647)
20. PG McCaffrey AE Goldfeld A Rao 1994 The role of NFATp in cyclosporin A-sensitive tumor necrosis factor-alpha gene transcription J Biol Chem 269 30445 30450 1:CAS:528:DyaK2cXmsleksrk%3D 7982959
21. MF Shannon LS Coles MA Vadas PN Cockerill 1997 Signals for activation of the GM-CSF promoter and enhancer in T cells Crit Rev Immunol 17 301 323 1:CAS:528:DyaK2sXktlyhsr4%3D 9202885
22. GR Crabtree EN Olson 2002 NFAT signaling: choreographing the social lives of cells Cell 109 Suppl S67 S79 10.1016/S0092-8674(02)00699-2 1:CAS:528:DC%2BD38Xjt1eqtbc%3D 11983154 (Pubitemid 34457853)
23. PK Singal N Iliskovic 1998 Doxorubicin-induced cardiomyopathy N Engl J Med 339 900 905 10.1056/NEJM199809243391307 1:STN:280:DyaK1cvhsVektw%3D%3D 9744975 (Pubitemid 28446849)
24. C Tan E Etcubanas N Wollner G Rosen A Gilladoga J Showel ML Murphy IH Krakoff 1973 Adriamycin-an antitumor antibiotic in the treatment of neoplastic diseases Cancer 32 9 17 10.1002/1097-0142(197307)32:1<9::AID- CNCR2820320102>3.0.CO;2-6 1:STN:280:DyaE3s3htlWktg%3D%3D 4352019
25. DA Gewirtz 1999 A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin Biochem Pharmacol 57 727 741 10.1016/S0006-2952(98)00307-4 1:CAS:528:DyaK1MXhsFeksL8%3D 10075079 (Pubitemid 29094544)
26. LH Hurley 2002 DNA and its associated processes as targets for cancer therapy Nat Rev Cancer 2 188 200 10.1038/nrc749 1:CAS:528:DC%2BD38Xis1KktL0%3D 11990855
27. K Jung R Reszka 2001 Mitochondria as subcellular targets for clinically useful anthracyclines Adv Drug Deliv Rev 49 87 105 10.1016/S0169-409X(01)00128-4 1:CAS:528:DC%2BD3MXjslSmtb4%3D 11377805 (Pubitemid 32493802)
28. JE Wolff T Trilling G Molenkamp RM Egeler H Jurgens 1999 Chemosensitivity of glioma cells in vitro: a meta-analysis J Cancer Res Clin Oncol 125 481 486 10.1007/s004320050305 1:CAS:528:DyaK1MXlsF2nsbw%3D 10480340 (Pubitemid 29410412)
29. M Niiya K Niiya T Kiguchi M Shibakura N Asaumi K Shinagawa F Ishimaru K Kiura K Ikeda H Ueoka M Tanimoto 2003 Induction of TNF-alpha, uPA, IL-8 and MCP-1 by doxorubicin in human lung carcinoma cells Cancer Chemother Pharmacol 52 391 398 10.1007/s00280-003-0665-1 12908082 (Pubitemid 37363612)
30. W Cao WH Chi J Wang JJ Tang YJ Lu 2005 TNF-alpha promotes doxorubicin-induced cell apoptosis and anti-cancer effect through downregulation of p21 in p53-deficient tumor cells Biochem Biophys Res Commun 330 1034 1040 10.1016/j.bbrc.2005.02.188 1:CAS:528:DC%2BD2MXjtVylurc%3D 15823547
31. SV Kalivendi EA Konorev S Cunningham SK Vanamala EH Kaji J Joseph B Kalyanaraman 2005 Doxorubicin activates nuclear factor of activated T-lymphocytes and Fas ligand transcription: role of mitochondrial reactive oxygen species and calcium Biochem J 389 527 539 10.1042/BJ20050285 1:CAS:528:DC%2BD2MXmtVSms7Y%3D 15799720 (Pubitemid 41021156)
32. X Huang MD Adams H Zhou AR Kerlavage 1997 A tool for analyzing and annotating genomic sequences Genomics 46 37 45 10.1006/geno.1997.4984 1:CAS:528:DyaK2sXnvVCkurw%3D 9403056 (Pubitemid 27527689)
33. SS Lakka M Rajan CS Gondi N Yanamandra N Chandrasekar SL Jasti Y Adachi K Siddique M Gujrati W Olivero DH Dinh G Kouraklis AP Kyritsis JS Rao 2002 Adenovirus-mediated expression of antisense MMP-9 in glioma cells inhibits tumor growth and invasion Oncogene 21 8011 8019 10.1038/sj.onc.1205894 1:CAS:528:DC%2BD38XoslGlsL0%3D 12439751 (Pubitemid 35434187)
34. Y Yan J Li W Ouyang Q Ma Y Hu D Zhang J Ding Q Qu K Subbaramaiah C Huang 2006 NFAT3 is specifically required for TNF-alpha-induced cyclooxygenase-2 (COX-2) expression and transformation of Cl41 cells J Cell Sci 119 2985 2994 10.1242/jcs.03014 1:CAS:528:DC%2BD28XotleitLs%3D 16803872 (Pubitemid 44177877)
35. J Li L Song D Zhang L Wei C Huang 2006 Knockdown of NFAT3 blocked TPA-induced COX-2 and iNOS expression, and enhanced cell transformation in Cl41 cells J Cell Biochem 99 1010 1020 10.1002/jcb.20834 1:CAS:528:DC%2BD28XhtFygtLrM 16475165 (Pubitemid 44673960)
36. T Kuwano S Nakao H Yamamoto M Tsuneyoshi T Yamamoto M Kuwano M Ono 2004 Cyclooxygenase 2 is a key enzyme for inflammatory cytokine-induced angiogenesis FASEB J 18 300 310 10.1096/fj.03-0473com 1:CAS:528:DC%2BD2cXht1Ggtr8%3D 14769824 (Pubitemid 38186249)
37. M Mann H Sheng J Shao CS Williams PI Pisacane MX Sliwkowski RN DuBois 2001 Targeting cyclooxygenase 2 and HER-2/neu pathways inhibits colorectal carcinoma growth Gastroenterology 120 1713 1719 10.1053/gast.2001.24844 1:CAS:528:DC%2BD3MXkslGku70%3D 11375952
38. H Sheng J Shao RN DuBois 2001 K-Ras-mediated increase in cyclooxygenase 2 mRNA stability involves activation of the protein kinase B1 Cancer Res 61 2670 2675 1:CAS:528:DC%2BD3MXisVSksLo%3D 11289146
39. AM Ranger LC Gerstenfeld J Wang T Kon H Bae EM Gravallese MJ Glimcher LH Glimcher 2000 The nuclear factor of activated T cells (NFAT) transcription factor NFATp (NFATc2) is a repressor of chondrogenesis J Exp Med 191 9 22 10.1084/jem.191.1.9 1:CAS:528:DC%2BD3cXktFyksA%3D%3D 10620601 (Pubitemid 30043644)
40. TT Yang Q Xiong H Enslen RJ Davis CW Chow 2002 Phosphorylation of NFATc4 by p38 mitogen-activated protein kinases Mol Cell Biol 22 3892 3904 10.1128/MCB.22.11.3892-3904.2002 1:CAS:528:DC%2BD38XjslWlt7k%3D 11997522 (Pubitemid 34525229)
41. JP Viola LD Carvalho BP Fonseca LK Teixeira 2005 NFAT transcription factors: from cell cycle to tumor development Braz J Med Biol Res 38 335 344 10.1590/S0100-879X2005000300003 1:CAS:528:DC%2BD2MXjsFejsrw%3D 15761612
42. H Zhang X Wang J Li J Zhu X Xie B Yuan Z Yang M Zeng Z Jiang J Li C Huang Q Ye 2007 Tissue type-specific modulation of ER transcriptional activity by NFAT3 Biochem Biophys Res Commun 353 576 581 10.1016/j.bbrc.2006.12.046 1:CAS:528:DC%2BD2sXmtVajtQ%3D%3D 17194453 (Pubitemid 46048708)
43. H Zhu W Gao H Jiang J Wu YF Shi XJ Zhang 2007 Calcineurin mediates acetylcholinesterase expression during calcium ionophore A23187-induced HeLa cell apoptosis Biochim Biophys Acta 1773 593 602 10.1016/j.bbamcr.2007.01.008 1:CAS:528:DC%2BD2sXjsVensL4%3D 17320203 (Pubitemid 46454338)
44. PW Szlosarek FR Balkwill 2003 Tumour necrosis factor alpha: a potential target for the therapy of solid tumours Lancet Oncol 4 565 573 10.1016/S1470-2045(03)01196-3 1:CAS:528:DC%2BD3sXntVGhsrs%3D 12965278 (Pubitemid 38351714)
45. S Chuvpilo E Jankevics D Tyrsin A Akimzhanov D Moroz MK Jha J Schulze-Luehrmann B Santner-Nanan E Feoktistova T Konig A Avots E Schmitt F Berberich-Siebelt A Schimpl E Serfling 2002 Autoregulation of NFATc1/A expression facilitates effector T cells to escape from rapid apoptosis Immunity 16 881 895 10.1016/S1074-7613(02)00329-1 1:CAS:528:DC%2BD38XltF2guro%3D 12121669 (Pubitemid 34786486)
46. MS Soengas RM Alarcon H Yoshida AJ Giaccia R Hakem TW Mak SW Lowe 1999 Apaf-1 and caspase-9 in p53-dependent apoptosis and tumor inhibition Science 284 156 159 10.1126/science.284.5411.156 1:CAS:528:DyaK1MXitlClu7w%3D 10102818 (Pubitemid 29282071)
47. A Rivera SA Maxwell 2005 The p53-induced gene-6 (proline oxidase) mediates apoptosis through a calcineurin-dependent pathway J Biol Chem 280 29346 29354 10.1074/jbc.M504852200 1:CAS:528:DC%2BD2MXntVegtrc%3D 15914462 (Pubitemid 41161390)
48. W Liao S Wang C Han Y Zhang 2005 14-3-3 proteins regulate glycogen synthase 3beta phosphorylation and inhibit cardiomyocyte hypertrophy FEBS J 272 1845 1854 10.1111/j.1742-4658.2005.04614.x 1:CAS:528:DC%2BD2MXjslGktLg%3D 15819880 (Pubitemid 40547243)
49. R Passier H Zeng N Frey FJ Naya RL Nicol TA McKinsey P Overbeek JA Richardson SR Grant EN Olson 2000 CaM kinase signaling induces cardiac hypertrophy and activates the MEF2 transcription factor in vivo J Clin Invest 105 1395 1406 10.1172/JCI8551 1:CAS:528:DC%2BD3cXjtlOnsLs%3D 10811847
50. JP Shaw PJ Utz DB Durand JJ Toole EA Emmel GR Crabtree 1988 Identification of a putative regulator of early T cell activation genes Science 241 202 205 10.1126/science.3260404 1:CAS:528:DyaL1cXls1Cls7k%3D 3260404
51. A Yaghi SM Sims 2005 Constrictor-induced translocation of NFAT3 in human and rat pulmonary artery smooth muscle Am J Physiol Lung Cell Mol Physiol 289 L1061 L1074 10.1152/ajplung.00096.2005 1:CAS:528:DC%2BD28XlslOnsw%3D%3D 16055480 (Pubitemid 41681341)
52. MS Caetano A Vieira-de-Abreu LK Teixeira MB Werneck MA Barcinski JP Viola 2002 NFATC2 transcription factor regulates cell cycle progression during lymphocyte activation: evidence of its involvement in the control of cyclin gene expression FASEB J 16 1940 1942 1:CAS:528:DC%2BD38Xps1Kqurs%3D 12368232
53. IA Graef F Wang F Charron L Chen J Neilson M Tessier-Lavigne GR Crabtree 2003 Neurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons Cell 113 657 670 10.1016/S0092-8674(03)00390-8 1:CAS:528:DC%2BD3sXksFehurw%3D 12787506 (Pubitemid 36694190)
54. GL Hernandez OV Volpert MA Iniguez E Lorenzo S Martinez-Martinez R Grau M Fresno JM Redondo 2001 Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin A: roles of the nuclear factor of activated T cells and cyclooxygenase 2 J Exp Med 193 607 620 10.1084/jem.193.5.607 1:CAS:528:DC%2BD3MXhslGls70%3D 11238591 (Pubitemid 32539557)
55. TA Zaichuk EH Shroff R Emmanuel S Filleur T Nelius OV Volpert 2004 Nuclear factor of activated T cells balances angiogenesis activation and inhibition J Exp Med 199 1513 1522 10.1084/jem.20040474 1:CAS:528: DC%2BD2cXkvV2jsb8%3D 15184502 (Pubitemid 38780406)
56. S Baksh JA DeCaprio SJ Burakoff 2000 Calcineurin regulation of the mammalian G0/G1 checkpoint element, cyclin dependent kinase 4 Oncogene 19 2820 2827 10.1038/sj.onc.1203585 1:CAS:528:DC%2BD3cXkt12rtLo%3D 10851085
57. Y Anraku Y Ohya H Iida 1991 Cell cycle control by calcium and calmodulin in Saccharomyces cerevisiae Biochim Biophys Acta 1093 169 177 10.1016/0167-4889(91)90119-I 1:CAS:528:DyaK3MXkvVyrtLw%3D 1863597
58. 2+ signaling and control of growth and proliferation Biol Cell 96 55 68 10.1016/j.biolcel.2003.11.001 1:CAS:528:DC%2BD2cXhs12ntr4%3D 15093128 (Pubitemid 38240399)
59. N Terada JJ Lucas EW Gelfand 1991 Differential regulation of the tumor suppressor molecules, retinoblastoma susceptibility gene product (Rb) and p53, during cell cycle progression of normal human T cells J Immunol 147 698 704 1:CAS:528:DyaK3MXmtVGrtrs%3D 1906503
60. M Tomono K Toyoshima M Ito H Amano 1996 Calcineurin is essential for DNA synthesis in Swiss 3T3 fibroblasts Biochem J 317 Pt 3 675 680 1:CAS:528:DyaK28XltlSgtLo%3D 8760349
61. M Tomono K Toyoshima M Ito H Amano Z Kiss 1998 Inhibitors of calcineurin block expression of cyclins A and E induced by fibroblast growth factor in Swiss 3T3 fibroblasts Arch Biochem Biophys 353 374 378 10.1006/abbi.1998.0667 1:CAS:528:DyaK1cXjt1Krtr0%3D 9606972 (Pubitemid 28373022)
62. JW Neal NA Clipstone 2003 A constitutively active NFATc1 mutant induces a transformed phenotype in 3T3-L1 fibroblasts J Biol Chem 278 17246 17254 10.1074/jbc.M300528200 1:CAS:528:DC%2BD3sXjsVKms7o%3D 12598522 (Pubitemid 36799606)
63. A Giese R Bjerkvig ME Berens M Westphal 2003 Cost of migration: invasion of malignant gliomas and implications for treatment J Clin Oncol 21 1624 1636 10.1200/JCO.2003.05.063 1:STN:280:DC%2BD3s7nvFWitw%3D%3D 12697889 (Pubitemid 46594118)
64. S Jauliac C Lopez-Rodriguez LM Shaw LF Brown A Rao A Toker 2002 The role of NFAT transcription factors in integrin-mediated carcinoma invasion Nat Cell Biol 4 540 544 10.1038/ncb816 1:CAS:528:DC%2BD38XmtVWktr8%3D 12080349 (Pubitemid 34752442)