A Structural Viral Mimic of Prosurvival Bcl-2: A Pivotal Role for Sequestering Proapoptotic Bax and Bak

Molecular Cell

Volumn 25, Issue 6, 2007, Pages 933-942

  Kvansakul, Marc ^a   van Delft, Mark F ^a,b   Lee, Erinna F ^a,b   Gulbis, Jacqueline M ^a   Fairlie, W Douglas ^a   Huang, David C S ^a   Colman, Peter M ^a  

^a Institute of Medical Research   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

CELLCYCLE; MICROBIO

Indexed keywords

BH3 PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR MIMICRY; MYXOMA VIRUS; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; VIRUS EXPRESSION;

AMINO ACID SEQUENCE; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CELL DEATH; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYXOMA VIRUS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTO-ONCOGENE PROTEINS C-BCL-2; VIRAL PROTEINS;

DNA VIRUSES; MYXOMA VIRUS;

EID: 33947304650     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.02.004     Document Type: Article

References (47)

1. Adams J.M. Ways of dying: multiple pathways to apoptosis. Genes Dev. 17 (2003) 2481-2495
2. Aoyagi M., Zhai D., Jin C., Aleshin A.E., Stec B., Reed J.C., and Liddington R.C. Vaccinia virus N1L protein resembles a B cell lymphoma-2 (Bcl-2) family protein. Protein Sci. 16 (2007) 118-124
3. Bouillet P., Metcalf D., Huang D.C.S., Tarlinton D.M., Kay T.W.H., Köntgen F., Adams J.M., and Strasser A. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286 (1999) 1735-1738
4. Bricogne G., Vonrhein C., Flensburg C., Schiltz M., and Paciorek W. Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr. D Biol. Crystallogr. 59 (2003) 2023-2030
5. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
6. Cartron P.F., Gallenne T., Bougras G., Gautier F., Manero F., Vusio P., Meflah K., Vallette F.M., and Juin P. The first alpha helix of Bax plays a necessary role in its ligand-induced activation by the BH3-only proteins Bid and Puma. Mol. Cell 16 (2004) 807-818
7. Certo M., Moore Vdel G., Nishino M., Wei G., Korsmeyer S., Armstrong S.A., and Letai A. Mitochondria primed by death signals determine cellular addiction to anti-apoptotic Bcl-2 family members. Cancer Cell 9 (2006) 351-365
8. Chen L., Willis S.N., Wei A., Smith B.J., Fletcher J.I., Hinds M.G., Colman P.M., Day C.L., Adams J.M., and Huang D.C.S. Differential targeting of pro-survival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol. Cell 17 (2005) 393-403
9. Cuconati A., and White E. Viral homologs of Bcl-2: role of apoptosis in the regulation of virus infection. Genes Dev. 16 (2002) 2465-2478
10. Cuconati A., Degenhardt K., Sundararajan R., Anschel A., and White E. Bak and Bax function to limit adenovirus replication through apoptosis induction. J. Virol. 76 (2002) 4547-4558
11. Danial N.N., and Korsmeyer S.J. Cell death: critical control points. Cell 116 (2004) 205-219
12. Day C.L., Chen L., Richardson S.J., Harrison P.J., Huang D.C.S., and Hinds M.G. Solution structure of prosurvival Mcl-1 and characterization of its binding by proapoptotic BH3-only ligands. J. Biol. Chem. 280 (2005) 4738-4744
13. DeLano W.L. The PyMOL Molecular Graphics System (2002). http://www.pymol.org
14. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
15. Everett H., Barry M., Sun X., Lee S.F., Frantz C., Berthiaume L.G., McFadden G., and Bleackley R.C. The myxoma poxvirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore. J. Exp. Med. 196 (2002) 1127-1139
16. Fenner F., and Ratcliffe F.N. Myxomatosis (1965), Cambridge University Press, Cambridge, UK
17. Fischer S.F., Ludwig H., Holzapfel J., Kvansakul M., Chen L., Huang D.C.S., Sutter G., Knese M., and Häcker G. Modified vaccinia virus ankara protein F1L is a novel BH3-domain binding protein and acts together with the early viral protein E3L to block virus-associated apoptosis. Cell Death Differ. 13 (2006) 109-118
18. Graham K.A., Opgenorth A., Upton C., and McFadden G. Myxoma virus M11L ORF encodes a protein for which cell surface localization is critical in manifestation of viral virulence. Virology 191 (1992) 112-124
19. Holm L., and Sander C. Touring protein fold space with Dali/FSSP. Nucleic Acids Res. 26 (1998) 316-319
20. Huang D.C.S., and Strasser A. BH3-only proteins - essential initiators of apoptotic cell death. Cell 103 (2000) 839-842
21. Huang Q., Petros A.M., Virgin H.W., Fesik S.W., and Olejniczak E.T. Solution structure of a Bcl-2 homolog from Kaposi sarcoma virus. Proc. Natl. Acad. Sci. USA 99 (2002) 3428-3433
22. Huang Q., Petros A.M., Virgin H.W., Fesik S.W., and Olejniczak E.T. Solution structure of the BHRF1 protein from Epstein-Barr virus, a homolog of human Bcl-2. J. Mol. Biol. 332 (2003) 1123-1130
23. Johnston J.B., and McFadden G. Poxvirus immunomodulatory strategies: current perspectives. J. Virol. 77 (2003) 6093-6100
24. Kim H., Rafiuddin-Shah M., Tu H.C., Jeffers J.R., Zambetti G.P., Hsieh J.J., and Cheng E.H. Hierarchical regulation of mitochondrion-dependent apoptosis by Bcl-2 subfamilies. Nat. Cell Biol. 8 (2006) 1348-1358
25. Kuwana T., Bouchier-Hayes L., Chipuk J.E., Bonzon C., Sullivan B.A., Green D.R., and Newmeyer D.D. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol. Cell 17 (2005) 525-535
26. Letai A., Bassik M., Walensky L., Sorcinelli M., Weiler S., and Korsmeyer S. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2 (2002) 183-192
27. Lindsten T., Ross A.J., King A., Zong W., Rathmell J.C., Shiels H.A., Ulrich E., Waymire K.G., Mahar P., Frauwirth K., et al. The combined functions of proapoptotic Bcl-2 family members Bak and Bax are essential for normal development of multiple tissues. Mol. Cell 6 (2000) 1389-1399
28. L/Bim fragment complex: Implications for Bim function. Immunity 19 (2003) 341-352
29. Loh J., Huang Q., Petros A.M., Nettesheim D., van Dyk L.F., Labrada L., Speck S.H., Levine B., Olejniczak E.T., and Virgin H.W. A surface groove essential for viral Bcl-2 function during chronic infection in vivo. PLoS Pathog. 1 (2005) e10 10.1371/journal.ppat.0010010
30. L, an inhibitor of programmed cell death. Nature 381 (1996) 335-341
31. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53 (1997) 240-255
32. Neidhardt F.C., Bloch P.L., and Smith D.F. Culture medium for enterobacteria. J. Bacteriol. 119 (1974) 736-747
33. Oltersdorf T., Elmore S.W., Shoemaker A.R., Armstrong R.C., Augeri D.J., Belli B.A., Bruncko M., Deckwerth T.L., Dinges J., Hajduk P.J., et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435 (2005) 677-681
34. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
35. L/Bad peptide complex formation from structure, mutagenesis, and biophysical studies. Protein Sci. 9 (2000) 2528-2534
36. Petros A.M., Olejniczak E.T., and Fesik S.W. Structural biology of the Bcl-2 family of proteins. Biochim. Biophys. Acta 1644 (2004) 83-94
37. Postigo A., Cross J.R., Downward J., and Way M. Interaction of F1L with the BH3 domain of Bak is responsible for inhibiting vaccinia-induced apoptosis. Cell Death Differ. 13 (2006) 1651-1662
38. L-Bak peptide complex: recognition between regulators of apoptosis. Science 275 (1997) 983-986
39. Storoni L.C., McCoy A.J., and Read R.J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 432-438
40. Su J., Wang G., Barrett J.W., Irvine T.S., Gao X., and McFadden G. Myxoma virus M11L blocks apoptosis through inhibition of conformational activation of Bax at the mitochondria. J. Virol. 80 (2006) 1140-1151
41. van Delft M.F., Wei A.H., Mason K.D., Vandenberg C.J., Chen L., Czabotar P.E., Willis S.N., Scott C.L., Day C.L., Cory S., et al. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 10 (2006) 389-399
42. Wang G., Barrett J.W., Nazarian S.H., Everett H., Gao X., Bleackley C., Colwill K., Moran M.F., and McFadden G. Myxoma virus M11L prevents apoptosis through constitutive interaction with Bak. J. Virol. 78 (2004) 7097-7111
43. White E., Sabbatini P., Debbas M., Wold W.S.M., Kusher D.I., and Gooding L.R. The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor α. Mol. Cell. Biol. 12 (1992) 2570-2580
44. Willis S.N., and Adams J.M. Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell Biol. 17 (2005) 617-625
45. L, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 19 (2005) 1294-1305
46. Willis S.N., Fletcher J.I., Kaufmann T., van Delft M.F., Chen L., Czabotar P.E., Ierino H., Lee E.F., Fairlie W.D., Bouillet P., et al. Apoptosis is induced when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315 (2007) 856-859
47. Yan N., Chai J., Lee E.S., Gu L., Liu Q., He J., Wu J.W., Kokel D., Li H., Hao Q., et al. Structure of the CED-4-CED-9 complex provides insights into programmed cell death in Caenorhabditis elegans. Nature 437 (2005) 831-837