Structural basis for apoptosis inhibition by Epstein-Barr virus bhrf1

PLoS Pathogens

Volumn 6, Issue 12, 2010, Pages

  Kvansakul, Marc ^a,c   Wei, Andrew H ^a,d   Fletcher, Jamie I ^a,e   Willis, Simon N ^a,f   Chen, Lin ^a,b   Roberts, Andrew W ^a,b   Huang, David C S ^a,b   Colman, Peter M ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c LA TROBE UNIVERSITY   (Australia)

^d MONASH UNIVERSITY   (Australia)

^e CHILDREN S CANCER INSTITUTE AUSTRALIA FOR MEDICAL RESEARCH   (Australia)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; PROTEIN BAK; PROTEIN BCL 2; PROTEIN BHRF1; PROTEIN BID; PUMA PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; APOPTOSIS REGULATORY PROTEIN; BHRF1 PROTEIN, HUMAN HERPESVIRUS 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BURKITT LYMPHOMA; CONTROLLED STUDY; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; LYMPHOID CELL; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN STRUCTURE; VIRUS CARCINOGENESIS; VIRUS INFECTIVITY; ANIMAL; DRUG RESISTANCE; HOST PATHOGEN INTERACTION; METABOLISM; PATHOGENICITY; PHYSIOLOGY; PROTEIN BINDING; VIROLOGY;

HUMAN HERPESVIRUS 4; MAMMALIA;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BURKITT LYMPHOMA; DRUG RESISTANCE; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; MICE; PROTEIN BINDING; VIRAL PROTEINS;

EID: 78651262604     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001236     Document Type: Article

References (56)

1. Galluzzi L, Brenner C, Morselli E, Touat Z, Kroemer G (2008) Viral control of mitochondrial apoptosis. PLoS Pathog 4: e1000018.
2. Cuconati A, White E (2002) Viral homologs of BCL-2: role of apoptosis in the regulation of virus infection. Genes and Development 16: 2465-2478.
3. Cuconati A, Degenhardt K, Sundararajan R, Anschel A, White E (2002) Bak and Bax function to limit adenovirus replication through apoptosis induction. J Virol 76: 4547-4558.
4. Marchini A, Tomkinson B, Cohen JI, Kieff E (1991) BHRF1, the Epstein-Barr virus gene with homology to Bc12, is dispensable for B-lymphocyte transformation and virus replication. J Virol 65: 5991-6000.
5. Henderson S, Huen D, Rowe M, Dawson C, Johnson G, et al. (1993) Epstein-Barr virus-coded BHRF1 protein, a viral homologue of Bcl-2, protects human B cells from programmed cell death. Proc Natl Acad Sci U S A 90: 8479-8483.
6. Thorley-Lawson DA, Gross A (2004) Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med 350: 1328-1337.
7. Tsujimoto Y, Cossman J, Jaffe E, Croce CM (1985) Involvement of the bcl-2 gene in human follicular lymphoma. Science 228: 1440-1443.
8. Altmann M, Hammerschmidt W (2005) Epstein-Barr virus provides a new paradigm: a requirement for the immediate inhibition of apoptosis. PLoS Biol 3: e404.
9. Kelly GL, Long HM, Stylianou J, Thomas WA, Leese A, et al. (2009) An Epstein-Barr virus anti-apoptotic protein constitutively expressed in transformed cells and implicated in burkitt lymphomagenesis: the Wp/BHRF1 link. PLoS Pathog 5: e1000341.
10. Taub R, Kirsch I, Morton C, Lenoir G, Swan D, et al. (1982) Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proc Natl Acad Sci U S A 79: 7837-7841.
11. Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, et al. (1985) The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318: 533-538.
12. Magrath I (1990) The pathogenesis of Burkitt's lymphoma. Adv Cancer Res 55: 133-270.
13. Strasser A, Harris AW, Bath ML, Cory S (1990) Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 348: 331-333.
14. Beverly LJ, Varmus HE (2009) MYC-induced myeloid leukemogenesis is accelerated by all six members of the antiapoptotic BCL family. Oncogene 28: 1274-1279.
15. Kelly G, Bell A, Rickinson A (2002) Epstein-Barr virus-associated Burkitt lymphomagenesis selects for downregulation of the nuclear antigen EBNA2. Nat Med 8: 1098-1104.
16. Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305: 626-629.
17. Cross JR, Postigo A, Blight K, Downward J (2008) Viral pro-survival proteins block separate stages in Bax activation but changes in mitochondrial ultrastructure still occur. Cell Death Differ 15: 997-1008.
18. Flanagan AM, Letai A (2008) BH3 domains define selective inhibitory interactions with BHRF-1 and KSHV BCL-2. Cell Death Differ 15: 580-588.
19. Uren RT, Dewson G, Chen L, Coyne SC, Huang DC, et al. (2007) Mitochondrial permeabilization relies on BH3 ligands engaging multiple prosurvival Bcl-2 relatives, not Bak. J Cell Biol 177: 277-287.
20. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, et al. (2005) Differential targeting of pro-survival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Molecular Cell 17: 393-403.
21. Willis SN, Fletcher JI, Kaufmann T, van Delft MF, Chen L, et al. (2007) Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315: 856-859.
22. Cartron PF, Gallenne T, Bougras G, Gautier F, Manero F, et al. (2004) The first alpha helix of Bax plays a necessary role in its ligand-induced activation by the BH3-only proteins Bid and PUMA. Molecular Cell 16: 807-818.
23. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, et al. (2005) BH3 Domains of BH3-Only Proteins Differentially Regulate Bax-Mediated Mitochondrial Membrane Permeabilization Both Directly and Indirectly. Molecular Cell 17: 525-535.
24. Letai A, Bassik M, Walensky L, Sorcinelli M, Weiler S, et al. (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2: 183-192.
25. 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.
26. White E, Sabbatini P, Debbas M, Wold WSM, Kusher DI, et al. (1992) The 19- kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor a. Molecular and Cellular Biology 12: 2570-2580.
27. Kvansakul M, van Delft MF, Lee EF, Gulbis JM, Fairlie WD, et al. (2007) A structural viral mimic of prosurvival bcl-2: a pivotal role for sequestering proapoptotic bax and bak. Molecular Cell 25: 933-942.
28. Jabbour AM, Puryer MA, Yu JY, Lithgow T, Riffkin CD, et al. (2006) Human Bcl-2 cannot directly inhibit the Caenorhabditis elegans Apaf-1 homologue CED-4, but can interact with EGL-1. J Cell Sci 119: 2572-2582.
29. Hsu YT, Youle RJ (1997) Nonionic detergents induce dimerization among members of the Bcl-2 family. J Biol Chem 272: 13829-13834.
30. Tao W, Kurschner C, Morgan JI (1997) Modulation of cell death in yeast by the Bcl-2 family of proteins. J Biol Chem 272: 15547-15552.
31. Desbien AL, Kappler JW, Marrack P (2009) The Epstein-Barr virus Bcl-2 homolog, BHRF1, blocks apoptosis by binding to a limited amount of Bim. Proc Natl Acad Sci U S A 106: 5663-5668.
32. Theodorakis P, D'Sa-Eipper C, Subramanian T, Chinnadurai G (1996) Unmasking of a proliferation-restraining activity of the anti-apoptosis protein EBV BHRF1. Oncogene 12: 1707-1713.
33. Bouillet P, Metcalf D, Huang DCS, Tarlinton DM, Kay TWH, et al. (1999) Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286: 1735-1738.
34. Egle A, Harris AW, Bouillet P, Cory S (2004) Bim is a suppressor of Mycinduced mouse B cell leukemia. Proc Natl Acad Sci U S A 101: 6164-6169.
35. Huang Q, Petros AM, Virgin HW, Fesik SW, Olejniczak ET (2003) Solution structure of the BHRF1 protein from Epstein-Barr virus, a homolog of human Bcl-2. Journal of Molecular Biology 332: 1123-1130.
36. L/Bim fragment complex: Implications for Bim function. Immunity 19: 341-352.
37. L, an inhibitor of programmed cell death. Nature 381: 335-341.
38. Czabotar PE, Lee EF, van Delft MF, Day CL, Smith BJ, et al. (2007) Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc Natl Acad Sci U S A 104: 6217-6222.
39. Lee EF, Sadowsky JD, Smith BJ, Czabotar PE, Peterson-Kaufman KJ, et al. (2009) High-resolution structural characterization of a helical alpha/beta-peptide foldamer bound to the anti-apoptotic protein Bcl-xL. Angew Chem Int Ed Engl 48: 4318-4322.
40. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, et al. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435: 677-681.
41. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, et al. (2006) 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: 389-399.
42. Schmitt CA, Rosenthal CT, Lowe SW (2000) Genetic analysis of chemoresistance in primary murine lymphomas. Nat Med 6: 1029-1035.
43. Liu MY, Shih YY, Li LY, Chou SP, Sheen TS, et al. (2000) Expression of the Epstein-Barr virus BHRF1 gene, a homologue of Bcl-2, in nasopharyngeal carcinoma tissue. J Med Virol 61: 241-250.
44. Oudejans JJ, van den Brule AJ, Jiwa NM, de Bruin PC, Ossenkoppele GJ, et al. (1995) BHRF1, the Epstein-Barr virus (EBV) homologue of the BCL-2 protooncogene, is transcribed in EBV-associated B-cell lymphomas and in reactive lymphocytes. Blood 86: 1893-1902.
45. Kvansakul M, Yang H, Fairlie WD, Czabotar PE, Fischer SF, et al. (2008) Vaccinia virus anti-apoptotic F1L is a novel Bcl-2-like domain-swapped dimmer that binds a highly selective subset of BH3-containing death ligands. Cell Death Differ 15: 1564-1571.
46. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
47. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
48. Storoni LC, McCoy AJ, Read RJ (2004) Likelihood-enhanced fast rotation functions. Acta Crystallogr D Biol Crystallogr 60: 432-438.
49. O'Connor L, Strasser A, O'Reilly LA, Hausmann G, Adams JM, et al. (1998) Bim: a novel member of the Bcl-2 family that promotes apoptosis. Embo J 17: 384-395.
50. Moriishi K, Huang DC, Cory S, Adams JM (1999) Bcl-2 family members do not inhibit apoptosis by binding the caspase activator Apaf-1. Proc Natl Acad Sci U S A 96: 9683-9688.
51. Fletcher JI, Meusburger S, Hawkins CJ, Riglar DT, Lee EF, et al. (2008) Apoptosis is triggered when prosurvival Bcl-2 proteins cannot restrain Bax. Proc Natl Acad Sci U S A 105: 18081-18087.
52. Huang DC, O'Reilly LA, Strasser A, Cory S (1997) The anti-apoptosis function of Bcl-2 can be genetically separated from its inhibitory effect on cell cycle entry. Embo J 16: 4628-4638.
53. Dewson G, Snowden RT, Almond JB, Dyer MJ, Cohen GM (2003) Conformational change and mitochondrial translocation of Bax accompany proteasome inhibitor-induced apoptosis of chronic lymphocytic leukemic cells. Oncogene 22: 2643-2654.
54. Wilson-Annan J, O'Reilly LA, Crawford SA, Hausmann G, Beaumont JG, et al. (2003) Proapoptotic BH3-only proteins trigger membrane integration of prosurvival Bcl-w and neutralize its activity. J Cell Biol 162: 877-887.
55. Hawkins CJ, Wang SL, Hay BA (1999) A cloning method to identify caspases and their regulators in yeast: identification of Drosophila IAP1 as an inhibitor of the Drosophila caspase DCP-1. Proc Natl Acad Sci U S A 96: 2885-2890.
56. Zha J, Harada H, Osipov K, Jockel J, Waksman G, et al. (1997) BH3 domain of BAD is required for heterodimerization with BCL-XL and pro-apoptotic activity. J Biol Chem 272: 24101-24104.