Characterisation of the Bax-nucleophosmin interaction: The importance of the Bax C-terminus

Apoptosis

Volumn 13, Issue 3, 2008, Pages 394-403

  Thompson, Jane ^a,b   Finlayson, Keith ^a   Salvo Chirnside, Eliane ^a   MacDonald, David ^a   McCulloch, James ^a   Kerr, Lorraine ^a   Sharkey, John ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b CYCLACEL LTD   (United Kingdom)

Author keywords

Apoptosis; Bcl 2 family; Cell death; Proximity assay

Indexed keywords

2 (5 METHYL 2 PHENYL 13 THIAZOL 4 YL)ETHANOHYDRAZIDE; DETERGENT; HYDRAZIDE DERIVATIVE; NUCLEOPHOSMIN; PROTEIN ANTIBODY; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; TRITON X 114; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; HUMAN; HUMAN CELL; IC 50; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REPRODUCIBILITY; ULTRAVIOLET RADIATION;

EID: 40049093362     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-007-0177-2     Document Type: Article

References (40)

1. 1. A Gross J Jockel MC Wei SJ Korsmeyer 1998 Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis EMBO J 17 3878 3885 9670005 10.1093/emboj/17.14.3878 1:CAS:528:DyaK1cXltFygt74%3D Gross A, Jockel J, Wei MC, Korsmeyer SJ (1998) Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J 17:3878–3885
2. 2. YT Hsu KG Wolter RJ Youle 1997 Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis Proc Natl Acad Sci USA 94 3668 3672 9108035 10.1073/pnas.94.8.3668 1:CAS:528:DyaK2sXis1amu78%3D Hsu YT, Wolter KG, Youle RJ (1997) Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci USA 94:3668–3672
3. 3. ZN Oltvai CL Milliman SJ Korsmeyer 1993 Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death Cell 74 609 619 8358790 10.1016/0092-8674(93)90509-O 1:CAS:528:DyaK3sXms1eqtbs%3D Oltvai ZN, Milliman CL, Korsmeyer SJ (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609–619
4. 4. LH Boise M Gonzalez-Garcia CE Postema 1993 Bcl-x, a Bcl-2-related gene that functions as a dominant regulator of apoptotic cell death Cell 74 597 608 8358789 10.1016/0092-8674(93)90508-N 1:CAS:528:DyaK3sXmsVans7g%3D Boise LH, Gonzalez-Garcia M, Postema CE et al (1993) Bcl-x, a Bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74:597–608
5. 5. TW Sedlak ZN Oltvai E Yang 1995 Multiple Bcl-2 family members demonstrate selective dimerizations with Bax Proc Natl Acad Sci USA 92 7834 7838 7644501 10.1073/pnas.92.17.7834 1:CAS:528:DyaK2MXnsFOnt74%3D Sedlak TW, Oltvai ZN, Yang E et al (1995) Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc Natl Acad Sci USA 92:7834–7838
6. 6. S Desagher A Osen-Sand A Nichols 1999 Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis J Cell Biol 144 891 901 10085289 10.1083/jcb.144.5.891 1:CAS:528:DyaK1MXhs1yqtbY%3D Desagher S, Osen-Sand A, Nichols A et al (1999) Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 144:891–901
7. 7. R Eskes S Desagher B Antonsson JC Martinou 2000 Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane Mol Cell Biol 20 929 935 10629050 10.1128/MCB.20.3.929-935.2000 1:CAS:528:DC%2BD3cXmt1Sntg%3D%3D Eskes R, Desagher S, Antonsson B, Martinou JC (2000) Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20:929–935
8. 8. P Li D Nijhawan I Budihardjo 1997 Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade Cell 91 479 489 9390557 10.1016/S0092-8674(00)80434-1 1:CAS:528:DyaK2sXnsFGls70%3D Li P, Nijhawan D, Budihardjo I et al (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479–489
9. 9. LE Kerr JL Birse-Archbold DM Short 2007 Nucleophosmin is a novel Bax chaperone that regulates apoptotic cell death Oncogene 26 18 2554 2562 17072349 10.1038/sj.onc.1210044 1:CAS:528:DC%2BD2sXktlOitb0%3D Kerr LE, Birse-Archbold JL, Short DM et al (2007) Nucleophosmin is a novel Bax chaperone that regulates apoptotic cell death. Oncogene 26(18):2554–2562
10. 10. N Feuerstein S Spiegel JJ Mond 1988 The nuclear matrix protein, numatrin (B23), is associated with growth factor-induced mitogenesis in Swiss 3T3 fibroblasts and with T lymphocyte proliferation stimulated by lectins and anti-T cell antigen receptor antibody J Cell Biol 107 1629 1642 3141428 10.1083/jcb.107.5.1629 1:CAS:528:DyaL1cXlvVyls7o%3D Feuerstein N, Spiegel S, Mond JJ (1988) The nuclear matrix protein, numatrin (B23), is associated with growth factor-induced mitogenesis in Swiss 3T3 fibroblasts and with T lymphocyte proliferation stimulated by lectins and anti-T cell antigen receptor antibody. J Cell Biol 107:1629–1642
11. 11. M Okuwaki K Matsumoto M Tsujimoto K Nagata 2001 Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone FEBS Lett 506 272 276 11602260 10.1016/S0014-5793(01)02939-8 1:CAS:528:DC%2BD3MXnsF2nsr4%3D Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K (2001) Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett 506:272–276
12. 12. V Swaminathan AH Kishore KK Febitha TK Kundu 2005 Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription Mol Cell Biol 25 7534 7545 16107701 10.1128/MCB.25.17.7534-7545.2005 1:CAS:528:DC%2BD2MXpsFKhsL0%3D Swaminathan V, Kishore AH, Febitha KK, Kundu TK (2005) Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription. Mol Cell Biol 25:7534–7545
13. 13. EF Ullman H Kirakossian S Singh 1994 Luminescent oxygen channeling immunoassay: measurement of particle binding kinetics by chemiluminescence Proc Natl Acad Sci USA 91 5426 5430 8202502 10.1073/pnas.91.12.5426 1:CAS:528:DyaK2cXkslOltLc%3D Ullman EF, Kirakossian H, Singh S et al (1994) Luminescent oxygen channeling immunoassay: measurement of particle binding kinetics by chemiluminescence. Proc Natl Acad Sci USA 91:5426–5430
14. 14. M Suzuki RJ Youle N Tjandra 2000 Structure of Bax: coregulation of dimer formation and intracellular localization Cell 103 645 654 11106734 10.1016/S0092-8674(00)00167-7 1:CAS:528:DC%2BD3cXot1Gnu7c%3D Suzuki M, Youle RJ, Tjandra N (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103:645–654
15. 15. YT Hsu RJ Youle 1998 Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations J Biol Chem 273 10777 10783 9553144 10.1074/jbc.273.17.10777 1:CAS:528:DyaK1cXivFKms74%3D Hsu YT, Youle RJ (1998) Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J Biol Chem 273:10777–10783
16. 16. E Colombo JC Marine D Danovi B Falini PG Pelicci 2002 Nucleophosmin regulates the stability and transcriptional activity of p53 Nat Cell Biol 4 529 533 12080348 10.1038/ncb814 1:CAS:528:DC%2BD38XmtVWksbc%3D Colombo E, Marine JC, Danovi D, Falini B, Pelicci PG (2002) Nucleophosmin regulates the stability and transcriptional activity of p53. Nat Cell Biol 4:529–533
17. 17. Y Fan D Wu L Jin Z Yin 2005 Human glutamylcysteine synthetase protects HEK293 cells against UV-induced cell death through inhibition of c-Jun NH2-terminal kinase Cell Biol Int 29 695 702 15936221 10.1016/j.cellbi.2005.04.006 1:CAS:528:DC%2BD2MXosVahsr8%3D Fan Y, Wu D, Jin L, Yin Z (2005) Human glutamylcysteine synthetase protects HEK293 cells against UV-induced cell death through inhibition of c-Jun NH2-terminal kinase. Cell Biol Int 29:695–702
18. 18. AJ Garcia-Saez M Coraiola MD Serra I Mingarro P Muller J Salgado 2006 Peptides corresponding to helices 5 and 6 of Bax can independently form large lipid pores FEBS J 273 971 981 16478471 10.1111/j.1742-4658.2006.05123.x 1:CAS:528:DC%2BD28Xjs1OltrY%3D Garcia-Saez AJ, Coraiola M, Serra MD, Mingarro I, Muller P, Salgado J (2006) Peptides corresponding to helices 5 and 6 of Bax can independently form large lipid pores. FEBS J 273:971–981
19. 19. KG Wolter YT Hsu CL Smith A Nechushtan XG Xi RJ Youle 1997 Movement of Bax from the cytosol to mitochondria during apoptosis J Cell Biol 139 1281 1292 9382873 10.1083/jcb.139.5.1281 1:CAS:528:DyaK2sXnvFeqsLg%3D Wolter KG, Hsu YT, Smith CL, Nechushtan A, Xi XG, Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J Cell Biol 139:1281–1292
20. 20. A Schinzel T Kaufmann M Schuler J Martinalbo D Grubb C Borner 2004 Conformational control of Bax localization and apoptotic activity by Pro168 J Cell Biol 164 1021 1032 15037603 10.1083/jcb.200309013 1:CAS:528:DC%2BD2cXivVCht70%3D Schinzel A, Kaufmann T, Schuler M, Martinalbo J, Grubb D, Borner C (2004) Conformational control of Bax localization and apoptotic activity by Pro168. J Cell Biol 164:1021–1032
21. 21. IS Goping A Gross JN Lavoie 1998 Regulated targeting of BAX to mitochondria J Cell Biol 143 207 215 9763432 10.1083/jcb.143.1.207 1:CAS:528:DyaK1cXmsFalt7w%3D Goping IS, Gross A, Lavoie JN et al (1998) Regulated targeting of BAX to mitochondria. J Cell Biol 143:207–215
22. 22. A Nechushtan CL Smith YT Hsu RJ Youle 1999 Conformation of the Bax C-terminus regulates subcellular location and cell death EMBO J 18 2330 2341 10228148 10.1093/emboj/18.9.2330 1:CAS:528:DyaK1MXjtlKhsro%3D Nechushtan A, Smith CL, Hsu YT, Youle RJ (1999) Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J 18:2330–2341
23. 23. B Antonsson F Conti A Ciavatta 1997 Inhibition of Bax channel-forming activity by Bcl-2 Science 277 370 372 9219694 10.1126/science.277.5324.370 1:CAS:528:DyaK2sXkvVels7s%3D Antonsson B, Conti F, Ciavatta A et al (1997) Inhibition of Bax channel-forming activity by Bcl-2. Science 277:370–372
24. 24. I Otter S Conus U Ravn 1998 The binding properties and biological activities of Bcl-2 and Bax in cells exposed to apoptotic stimuli J Biol Chem 273 6110 6120 9497329 10.1074/jbc.273.11.6110 1:CAS:528:DyaK1cXitFalsrk%3D Otter I, Conus S, Ravn U et al (1998) The binding properties and biological activities of Bcl-2 and Bax in cells exposed to apoptotic stimuli. J Biol Chem 273:6110–6120
25. 25. H Zha C Aime-Sempe T Sato JC Reed 1996 Proapoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2 J Biol Chem 271 7440 7444 8631771 10.1074/jbc.271.23.13392 1:CAS:528:DyaK28XhvFyks74%3D Zha H, Aime-Sempe C, Sato T, Reed JC (1996) Proapoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2. J Biol Chem 271:7440–7444
26. 26. J Li X Zhang DP Sejas Q Pang 2005 Negative regulation of p53 by nucleophosmin antagonizes stress-induced apoptosis in human normal and malignant hematopoietic cells Leuk Res 29 1415 1423 15964625 10.1016/j.leukres.2005.05.005 1:CAS:528:DC%2BD2MXhtFOmsLbF Li J, Zhang X, Sejas DP, Pang Q (2005) Negative regulation of p53 by nucleophosmin antagonizes stress-induced apoptosis in human normal and malignant hematopoietic cells. Leuk Res 29:1415–1423
27. 27. B Lambert M Buckle 2006 Characterisation of the interface between nucleophosmin (NPM) and p53: Potential role in p53 stabilisation FEBS Lett 580 345 350 16376884 10.1016/j.febslet.2005.12.025 1:CAS:528:DC%2BD28XkvVSi Lambert B, Buckle M (2006) Characterisation of the interface between nucleophosmin (NPM) and p53: Potential role in p53 stabilisation. FEBS Lett 580:345–350
28. 28. R Ochs M Lischwe P O’Leary H Busch 1983 Localization of nucleolar phosphoproteins B23 and C23 during mitosis Exp Cell Res 146 139 149 6345184 10.1016/0014-4827(83)90332-4 1:CAS:528:DyaL3sXlsFGrsrw%3D Ochs R, Lischwe M, O’Leary P, Busch H (1983) Localization of nucleolar phosphoproteins B23 and C23 during mitosis. Exp Cell Res 146:139–149
29. 29. HJ Chan JJ Weng BY Yung 2005 Nucleophosmin/B23-binding peptide inhibits tumor growth and up-regulates transcriptional activity of p53 Biochem Biophys Res Commun 333 396 403 15950182 10.1016/j.bbrc.2005.04.176 1:CAS:528:DC%2BD2MXlsVChtbo%3D Chan HJ, Weng JJ, Yung BY (2005) Nucleophosmin/B23-binding peptide inhibits tumor growth and up-regulates transcriptional activity of p53. Biochem Biophys Res Commun 333:396–403
30. 30. K Hingorani A Szebeni MO Olson 2000 Mapping the functional domains of nucleolar protein B23 J Biol Chem 275 24451 24457 10829026 10.1074/jbc.M003278200 1:CAS:528:DC%2BD3cXlsl2jsrw%3D Hingorani K, Szebeni A, Olson MO (2000) Mapping the functional domains of nucleolar protein B23. J Biol Chem 275:24451–24457
31. 31. YY Lu CY Lam BY Yung 1996 Decreased accumulation and dephosphorylation of the mitosis-specific form of nucleophosmin/B23 in staurosporine-induced chromosome decondensation Biochem J 317 Pt 1 321 327 8694782 1:CAS:528:DyaK28Xktl2lsrs%3D Lu YY, Lam CY, Yung BY (1996) Decreased accumulation and dephosphorylation of the mitosis-specific form of nucleophosmin/B23 in staurosporine-induced chromosome decondensation. Biochem J 317(Pt 1):321–327
32. 32. B Guo DY Zhai E Cabezas 2003 Humanin peptide suppresses apoptosis by interfering with Bax activation Nature 423 456 461 12732850 10.1038/nature01627 1:CAS:528:DC%2BD3sXjvFaltL0%3D Guo B, Zhai DY, Cabezas E et al (2003) Humanin peptide suppresses apoptosis by interfering with Bax activation. Nature 423:456–461
33. 33. M Nomura S Shimizu T Sugiyama 2003 14-3-3 interacts directly with and negatively regulates pro-apoptotic bax J Biol Chem 278 2058 2065 12426317 10.1074/jbc.M207880200 1:CAS:528:DC%2BD3sXisFyqsw%3D%3D Nomura M, Shimizu S, Sugiyama T et al (2003) 14-3-3 interacts directly with and negatively regulates pro-apoptotic bax. J Biol Chem 278:2058–2065
34. 34. M Sawada WY Sun P Hayes K Leskov DA Boothman S Matsuyama 2003 Ku70 suppresses the apoptotic translocation of Bax to mitochondria Nat Cell Biol 5 320 329 12652308 10.1038/ncb950 1:CAS:528:DC%2BD3sXisFWrt7k%3D Sawada M, Sun WY, Hayes P, Leskov K, Boothman DA, Matsuyama S (2003) Ku70 suppresses the apoptotic translocation of Bax to mitochondria. Nat Cell Biol 5:320–329
35. 35. HL Zhang JK Kim CA Edwards ZH Xu R Taichman CY Wang 2005 Clusterin inhibits apoptosis by interacting with activated Bax Nat Cell Biol 7 909 915 16113678 10.1038/ncb1291 1:CAS:528:DC%2BD2MXpslaksb0%3D Zhang HL, Kim JK, Edwards CA, Xu ZH, Taichman R, Wang CY (2005) Clusterin inhibits apoptosis by interacting with activated Bax. Nat Cell Biol 7:909–915
36. 36. D Bertwistle M Sugimoto CJ Sherr 2004 Physical and functional interactions of the Arf tumor suppressor protein with nucleophosmin/B23 Mol Cell Biol 24 985 996 14729947 10.1128/MCB.24.3.985-996.2004 1:CAS:528:DC%2BD2cXmsFWhtQ%3D%3D Bertwistle D, Sugimoto M, Sherr CJ (2004) Physical and functional interactions of the Arf tumor suppressor protein with nucleophosmin/B23. Mol Cell Biol 24:985–996
37. 37. E Colombo P Bonetti EL Denchi 2005 Nucleophosmin is required for DNA integrity and p19(Arf) protein stability Mol Cell Biol 25 8874 8886 16199867 10.1128/MCB.25.20.8874-8886.2005 1:CAS:528:DC%2BD2MXhtFWisrfF Colombo E, Bonetti P, Denchi EL et al (2005) Nucleophosmin is required for DNA integrity and p19(Arf) protein stability. Mol Cell Biol 25:8874–8886
38. 38. C Korgaonkar J Hagen V Tompkins 2005 Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function Mol Cell Biol 25 1258 1271 15684379 10.1128/MCB.25.4.1258-1271.2005 1:CAS:528:DC%2BD2MXhs1Kgsb8%3D Korgaonkar C, Hagen J, Tompkins V et al (2005) Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function. Mol Cell Biol 25:1258–1271
39. 39. KH Vousden X Lu 2002 Live or let die: The cell’s response to p53 Nat Rev Cancer 2 594 604 12154352 10.1038/nrc864 1:CAS:528:DC%2BD38XlslGqsL8%3D Vousden KH, Lu X (2002) Live or let die: The cell’s response to p53. Nat Rev Cancer 2:594–604
40. 40. JH Zhang TDY Chung KR Oldenburg 1999 A simple statistical parameter for use in evaluation and validation of high throughput screening assays J Biomol Screen 4 67 73 10838414 10.1177/108705719900400206 Zhang JH, Chung TDY, Oldenburg KR (1999) A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screen 4:67–73