B-cell translocation gene 2 mediates crosstalk between PI3K/Akt1 and NFκB pathways which enhances transcription of MnSOD by accelerating IκBα degradation in normal and cancer cells

Cell Communication and Signaling

Volumn 11, Issue 1, 2013, Pages

  Sundaramoorthy, Santhoshkumar ^a   Ryu, Min Sook ^a   Lim, In Kyoung ^a  

^a Ajou University School of Medicine   (South Korea)

Author keywords

Akt1; BTG2 TIS21 Pc3 gene; G2 M arrest; I B ; MnSOD; NF B

Indexed keywords

AKT1 PROTEIN; BTG2 PROTEIN; CYCLIN B1; CYCLIN DEPENDENT KINASE INHIBITOR 1; DOXORUBICIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MANGANESE SUPEROXIDE DISMUTASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOPROTEIN; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; BTG2 PROTEIN, HUMAN; HYDROGEN PEROXIDE; I KAPPA B; IMMEDIATE EARLY PROTEIN; NF-KAPPAB INHIBITOR ALPHA; SUPEROXIDE DISMUTASE; TUMOR SUPPRESSOR PROTEIN; NF KAPPAB INHIBITOR ALPHA;

ANTIOXIDANT ACTIVITY; ARTICLE; B CELL TRANSLOCATION GENE 2; BINDING KINETICS; CANCER CELL; DOWN REGULATION; ENHANCER REGION; G2 PHASE CELL CYCLE CHECKPOINT; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSDUCTION; GENETIC TRANSFECTION; HELA CELL; INTRON; M PHASE CELL CYCLE CHECKPOINT; MNSOD GENE; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEIN TARGETING; RNA INTERFERENCE; UPREGULATION; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; NEOPLASM;

RATTUS;

HELA CELLS; HUMANS; HYDROGEN PEROXIDE; I-KAPPA B PROTEINS; IMMEDIATE-EARLY PROTEINS; NEOPLASMS; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SUPEROXIDE DISMUTASE; TUMOR SUPPRESSOR PROTEINS;

EID: 84884176695     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/1478-811X-11-69     Document Type: Article

References (52)

1. In search of a function for the TIS21/PC3/BTG1/TOB family. Matsuda S, Rouault J, Magaud J, Berthet C, FEBS Lett 2001 497 67 72 10.1016/S0014-5793(01) 02436-X 11377414 (Pubitemid 32476878)
2. PC3 potentiates NGF-induced differentiation and protects neurons from apoptosis. Corrente G, Guardavaccaro D, Tirone F, Neuroreport 2002 25 417 422 (Pubitemid 34293181)
3. B cell translocation gene 2 enhances susceptibility of HeLa cells to Doxorubicin induced oxidative damage. Lim YB, Park TJ, Lim IK, J Biol Chem 2008 283 33110 33118 10.1074/jbc.M804255200 18840609
4. Structure and expression of TIS21, a primary response gene induced by growth factors and tumor promoters. Fletcher BS, Lim RW, Varnum BC, Kujubu DA, Koski RA, Herschman HR, J Biol Chem 1991 2661 4511 14518
5. Molecular cloning of PC3, a putatively secreted protein whose mRNA is induced by nerve growth factor and depolarization. Bradbury A, Possenti R, Shooter EM, Tirone F, Proc Natl Acad Sci USA 1991 88 3353 3357 10.1073/pnas.88.8.3353 1849653 (Pubitemid 21916619)
6. Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Rouault JP, Falette N, Guéhenneux F, Guillot C, Rimokh R, Wang Q, Berthet C, Moyret-Lalle C, Savatier P, Pain B, Shaw P, Berger R, Samarut J, Magaud JP, Ozturk M, Samarut C, Puisieux A, Nat Genet 1996 14 482 486 10.1038/ng1296-482 8944033 (Pubitemid 26414597)
7. Expression of B-cell translocation gene 2 protein in normal human tissues. Melamed J, Kernizan S, Walden PD, Tissue Cell 2002 34 28 32 10.1054/tice.2001.0220 11989967 (Pubitemid 34436184)
8. Differential expression of TIS21 and TIS1 genes in the various organs of Balb/c mice, thymic carcinoma tissues and human cancer cell lines. Lim IK, Lee MS, Lee SH, Kim NK, Jou I, Seo JS, Park SC, J Cancer Res Clin Oncol 1995 121 279 284 10.1007/BF01209594 7768965
9. Antiproliferative B cell translocation gene 2 protein is down-regulated post-transcriptionally as an early event in prostate carcinogenesis. Ficazzola MA, Fraiman M, Gitlin J, Woo K, Melamed J, Rubin MA, Walden PD, Carcinogenesis 2001 22 1271 1279 10.1093/carcin/22.8.1271 11470758 (Pubitemid 32737344)
10. Impaired expression of the cell cycle regulator BTG2 is common in clear cell renal cell carcinoma. Struckmann K, Schraml P, Simon R, Elmenhorst K, Mirlacher M, Kononen J, Moch H, Cancer Res 2004 64 1632 1638 10.1158/0008-5472.CAN-03-1687 14996721 (Pubitemid 38428683)
11. Expression of the NF-kappaB-responsive gene BTG2 is aberrantly regulated in breast cancer. Kawakubo H, Carey JL, Brachtel E, Gupta V, Green JE, Walden PD, Maheswaran S, Oncogene 2004 23 8310 8319 10.1038/sj.onc.1208008 15378000 (Pubitemid 39531842)
12. TIS21 negatively regulates hepatocarcinogenesis by disruption of cyclin B1-Forkhead box M1 regulation loop. Park TJ, Kim JY, Oh SP, Kang SY, Kim BW, Wang HJ, Song KY, Kim HC, Lim IK, Hepatology 2008 47 1533 1543 10.1002/hep.22212 18393292 (Pubitemid 351702737)
13. TIS21 knock-out enhances the frequency of medulloblastoma in Patched1 heterozygous mice by inhibiting the Cxcl3-dependent migration of cerebellar neurons. Farioli-Vecchioli S, Cinà I, Ceccarelli M, Micheli L, Leonardi L, Ciotti MT, De Bardi M, Di Rocco C, Pallini R, Cavallaro S, Tirone F, J Neurosci 2012 32 15547 15564 10.1523/JNEUROSCI.0412-12.2012 23115191
14. Breast tumor progression induced by loss of BTG2 expression is inhibited by targeted therapy with the ErbB/HER inhibitor lapatinib. Takahashi F, Chiba N, Tajima K, Hayashida T, Shimada T, Takahashi M, Moriyama H, Brachtel E, Edelman EJ, Ramaswamy S, Maheswaran S, Oncogene 2011 30 3084 3095 10.1038/onc.2011.24 21339742
15. BTG2 suppresses cancer cell migration through inhibition of Src-FAK signaling by downregulation of reactive oxygen species generation in mitochondria. Lim SK, Choi YW, Lim IK, Park TJ, Clin Exp Metastasis 2012 29 901 913 10.1007/s10585-012-9479-z 22562501
16. DNA microarrays identification of primary and secondary target genes regulated by p53. Kannan K, Amariglio N, Rechavi G, Jakob-Hirsch J, Kela I, Kaminski N, Getz G, Domany E, Givol D, Oncogene 2001 20 2225 2234 10.1038/sj.onc.1204319 11402317 (Pubitemid 32531280)
17. A systematic search for downstream mediators of tumor suppressor function of p53 reveals a major role of BTG2 in suppression of Ras-induced transformation. Boiko AD, Porteous S, Razorenova OV, Krivokrysenko VI, Williams BR, Gudkov AV, Genes Dev 2006 20 236 252 10.1101/gad.1372606 16418486 (Pubitemid 43112941)
18. p53 regulates the Ras circuit to inhibit the expression of a cancer-related gene signature by various molecular pathways. Buganim Y, Solomon H, Rais Y, Kistner D, Nachmany I, Brait M, Madar S, Goldstein I, Kalo E, Adam N, Gordin M, Rivlin N, Kogan I, Brosh R, Sefadia-Elad G, Goldfinger N, Sidransky D, Kloog Y, Rotter V, Cancer Res 2010 70 2274 2284 10.1158/0008-5472.CAN-09-2661 20197462
19. Various p53 mutant proteins differently regulate the Ras circuit to induce a cancer-related gene signature. Solomon H, Buganim Y, Kogan-Sakin I, Pomeraniec L, Assia Y, Madar S, Goldstein I, Brosh R, Kalo E, Beatus T, Goldfinger N, Rotter V, J Cell Sci 2012 125 3144 3152 10.1242/jcs.099663 22427690
20. Induction of growth inhibition of 293 cells by downregulation of the cyclin E and cyclin-dependent kinase 4 proteins due to overexpression of TIS21. Lim IK, Lee MS, Ryu MS, Park TJ, Fujiki H, Eguchi H, Paik WK, Mol Carcinog 1998 23 25 35 10.1002/(SICI)1098-2744(199809)23:1<25::AID-MC4>3.0.CO;2-G 9766435 (Pubitemid 28441057)
21. Arrest of G(1)-S progression by the p53-inducible gene PC3 is Rb dependent and relies on the inhibition of cyclin D1 transcription. Guardavaccaro D, Corrente G, Covone F, Micheli L, D'Agnano I, Starace G, Caruso M, Tirone F, Mol Cell Biol 2000 20 1797 1815 10.1128/MCB.20.5.1797-1815.2000 10669755 (Pubitemid 30100197)
22. TIS21/BTG2/PC3 is expressed through PKC-delta pathway and inhibits binding of cyclin B1-Cdc2 and its activity, independent of p53 expression. Ryu MS, Lee MS, Hong JW, Hahn TR, Moon E, Lim IK, Exp Cell Res 2004 299 159 170 10.1016/j.yexcr.2004.05.014 15302583 (Pubitemid 39078391)
23. Phosphorylation of serine 147 of tis21/BTG2/pc3 by p-Erk1/2 induces Pin-1 binding in cytoplasm and cell death. Hong JW, Ryu MS, Lim IK, J Biol Chem 2005 280 21256 21263 10.1074/jbc.M500318200 15788397 (Pubitemid 40805688)
24. The BTG2 protein is a general activator of mRNA deadenylation. Mauxion F, Faux C, Séraphin B, EMBO J 2008 27 1039 1048 10.1038/emboj.2008.43 18337750 (Pubitemid 351508153)
25. BTG/TOB factors impact deadenylases. Mauxion F, Chen CY, Séraphin B, Shyu AB, Trends Biochem Sci 2009 34 640 647 10.1016/j.tibs.2009.07.008 19828319
26. The mammalian anti-proliferative BTG/Tob protein family. Winkler GS, J Cell Physiol 2010 222 66 72 10.1002/jcp.21919 19746446
27. SOD2: a new type of tumor-suppressor gene? Bravard A, Sabatier L, Hoffschir F, Ricoul M, Luccioni C, Dutrillaux B, Int J Cancer 1992 51 476 480 10.1002/ijc.2910510323 1592538
28. Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Church SL, Grant JW, Ridnour LA, Oberley LW, Swanson PE, Meltzer PS, Trent JM, Proc Natl Acad Sci USA 1993 90 3113 3117 10.1073/pnas.90.7.3113 8464931 (Pubitemid 23113568)
29. Transcriptional regulation of the human manganese superoxide dismutase gene: the role of specificity protein 1 (Sp1) and activating protein-2 (AP-2). Xu Y, Porntadavity S, Clair DK St, Biochem J 2002 362 401 412 10.1042/0264-6021:3620401 11853549 (Pubitemid 34214483)
30. An intronic NF-kappaB element is essential for induction of the human manganese superoxide dismutase gene by tumor necrosis factor-alpha and interleukin-1beta. Xu Y, Kiningham KK, Devalaraja MN, Yeh CC, Majima H, Kasarskis EJ, Clair DK St, DNA Cell Bio 1999 18 709 722 10.1089/104454999314999 (Pubitemid 29439223)
31. Acetylation of MnSOD directs enzymatic activity responding to cellular nutrient status or oxidative stress. Ozden O, Park SH, Kim HS, Jiang H, Coleman MC, Spitz DR, Gius D, Aging 2011 3 102 107 21386137
32. Cellularly generated active oxygen species and HeLa cell proliferation. Burdon RH, Gill V, Free Radic Res Commun 1993 19 203 213 10.3109/ 10715769309111603 8244089 (Pubitemid 2001293)
33. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Kops GJ, Dansen TB, Polderman PE, Saarloos I, Wirtz KW, Coffer PJ, Huang TT, Bos JL, Medema RH, Burgering BM, Nature 2002 419 316 321 10.1038/nature01036 12239572
34. Stimulation-dependent I kappa B alpha phosphorylation marks the NF-kappa B inhibitor for degradation via the ubiquitin-proteasome pathway. Alkalay I, Yaron A, Hatzubai A, Orian A, Ciechanover A, Ben-Neriah Y, Proc Natl Acad Sci USA 1995 92 10599 10603 10.1073/pnas.92.23.10599 7479848 (Pubitemid 3009135)
35. Mapping of the inducible IkappaB phosphorylation sites that signal its ubiquitination and degradation. DiDonato J, Mercurio F, Rosette C, Wu-Li J, Suyang H, Ghosh S, Karin M, Mol Cell Biol 1996 16 4 1295 1304 8657102
36. Nuclear factor kappaB-dependent mechanisms coordinate the synergistic effect of PMA and cytokines on the induction of superoxide dismutase 2. Kiningham KK, Xu Y, Daosukho C, Popova B, St Clair DK, Biochem J 2001 353 147 156 11115408 (Pubitemid 32094609)
37. TIS21/(BTG2) negatively regulates estradiol-stimulated expansion of hematopoietic stem cells by derepressing Akt phosphorylation and inhibiting mTOR signal transduction. Kim BC, Ryu MS, Oh SP, Lim IK, Stem Cells 2008 26 2339 23348 10.1634/stemcells.2008-0327 18556508
38. Enhanced G2-M arrest by nuclear factor-{kappa}B-dependent p21waf1/cip1 induction. Wuerzberger-Davis SM, Chang PY, Berchtold C, Miyamoto S, Mol Cancer Res 2005 3 345 353 10.1158/1541-7786.MCR-05-0028 15972853 (Pubitemid 40905626)
39. B-cell translocation gene 2 (BTG2) stimulates cellular antioxidant defenses through the antioxidant transcription factor NFE2L2 in human mammary epithelial cells. Karve TM, Rosen EM, J Biol Chem 2012 287 31503 31514 10.1074/jbc.M112.367433 22493435
40. Cross-talk between NFkB and the PI3-kinase/AKT pathway can be targeted in primary effusion lymphoma (PEL) cell lines for efficient apoptosis. Hussain AR, Ahmed SO, Ahmed M, Khan OS, Al Abdulmohsen S, Platanias LC, Al-Kuraya KS, Uddin S, PLoS One 2012 7 39945 10.1371/journal.pone.0039945 22768179
41. α-Catulin drives metastasis by activating ILK and driving an αvβ3 integrin signaling axis. Liang CH, Chiu SY, Hsu IL, Wu YY, Tsai YT, Ke JY, Pan SH, Hsu YC, Li KC, Yang PC, Chen YL, Hong TM, Cancer Res 2013 73 428 438 10.1158/0008-5472.CAN-12-2095 23047866
42. Metformin, an antidiabetic agent reduces growth of cutaneous squamous cell carcinoma by targeting mTOR signaling pathway. Chaudhary SC, Kurundkar D, Elmets CA, Kopelovich L, Athar M, Photochem Photobiol 2012 88 1149 56 10.1111/j.1751-1097.2012.01165.x 22540890
43. Dehydroepiandrosterone-induced proliferation of prostatic epithelial cell is mediated by NFKB via PI3K/AKT signaling pathway. Sun HZ, Yang TW, Zang WJ, Wu SF, J Endocrinol 2010 204 311 318 10.1677/JOE-09-0270 20007738
44. Akt fine-tunes NF-κB-dependent gene expression during T cell activation. Cheng J, Phong B, Wilson DC, Hirsch R, Kane LP, J Biol Chem 2011 286 36076 36085 10.1074/jbc.M111.259549 21862580
45. Manganese superoxide dismutase regulation and cancer. Dhar SK, Clair DK St, Free Radic Biol Med 2012 52 2209 2222 10.1016/j.freeradbiomed.2012.03.009 22561706
46. Induction of p21 by p65 in p53 null cells treated with Doxorubicin. Ma S, Tang J, Feng J, Xu Y, Yu X, Deng Q, Lu Y, Biochim Biophys Acta 2008 1783 935 940 10.1016/j.bbamcr.2008.01.008 18269916
47. Roles of nuclear factor-kappaB, p53, and p21/WAF1 in daunomycin-induced cell cycle arrest and apoptosis. Hellin AC, Bentires-Alj M, Verlaet M, Benoit V, Gielen J, Bours V, Merville MP, J Pharmacol Exp Ther 2000 295 870 878 11082419
48. Mitochondria and cancer. Wallace DC, Nat Rev Cancer 2012 12 685 698 23001348
49. On the origin of cancer cells. WARBURG O, Science 1956 123 309 314 10.1126/science.123.3191.309 13298683
50. Manganese superoxide dismutase: guardian of the powerhouse. Holley AK, Bakthavatchalu V, Velez-Roman JM, Clair DK St, Int J Mol Sci 2011 12 7114 7162 10.3390/ijms12107114 22072939
51. In situ reduction of oxidative damage, increased cell turnover, and delay of mitochondrial injury by overexpression of manganese superoxide dismutase in a multistage skin carcinogenesis model. Oberley TD, Xue Y, Zhao Y, Kiningham K, Szweda LI, Clair DK St, Antioxid Redox Signal 2004 6 537 548 10.1089/152308604773934297 15130280 (Pubitemid 38625374)
52. 2 Choi YW, Park TJ, Kim HS, Lim IK, Biochem Biophys Res Commun 2013 434 559 65 10.1016/j.bbrc.2013.03.114 23583382