Structure of M11L: A myxoma virus structural homolog of the apoptosis inhibitor, Bcl-2

Protein Science

Volumn 16, Issue 4, 2007, Pages 695-703

  Douglas, Andrew E ^a,b   Corbett, Kevin D ^a,d   Berger, James M ^a   Mcfadden, Grant ^c   Handel, Tracy M ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis inhibitor; Bcl 2 homology; Fluorescence polarization; Immunomodulation; M11L; Poxvirus; X ray crystallography

Indexed keywords

APOPTOSIS INHIBITOR; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN M11L; UNCLASSIFIED DRUG; VIRUS PROTEIN;

APOPTOSIS; ARTICLE; BINDING AFFINITY; CRYSTAL STRUCTURE; MITOCHONDRION; MYXOMA VIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; APOPTOSIS; CRYSTALLOGRAPHY, X-RAY; FLUORESCENCE POLARIZATION; MOLECULAR SEQUENCE DATA; MYXOMA VIRUS; PROTEIN CONFORMATION; PROTO-ONCOGENE PROTEINS C-BCL-2; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

MYXOMA VIRUS; POXVIRIDAE;

EID: 33947727119     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.062720107     Document Type: Article

References (53)

1. Aoyagi, M., Zhai, D., Jin, C., Aleshin, A.E., Stec, B., Reed, J.C., and Liddington, R.C. 2007. Vaccinia virus N1L protein resembles a B cell lymphoma-2 (Bcl-2) family protein. Protein Sci. 16: 118-124.
2. Baker, N.A., Sept, D., Joseph, S., Holst, M.J., and McCammon, J.A. 2001. Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc. Natl. Acad. Sci. 98: 10037-10041.
3. Barry, M., Wasilenko, S.T., Stewart, T.L., and Taylor, J.M. 2004. Apoptosis regulator genes encoded by poxviruses. Prog. Mol. Subcell. Biol. 36: 19-37.
4. Benedict, C.A., Norris, P.S., and Ware, C.F. 2002. To kill or be killed: Viral evasion of apoptosis. Nat. Immunol. 3: 1013-1018.
5. Borner, C. 2003. The Bcl-2 protein family: Sensors and checkpoints for life-or-death decisions. Mol. Immunol. 39: 615-647.
6. Boya, P., Pauleau, A.L., Poncet, D., Gonzalez-Polo, R.A., Zamzami, N., and Kroemer, G. 2004. Viral proteins targeting mitochondria: Controlling cell death. Biochim. Biophys. Acta 1659: 178-189.
7. Clarke, A. 1996. Analysis of ligand binding by enzymes. In Enzymology labfax (ed. P.C. Engel), pp. 199-221. BIOS Scientific, Oxford UK.
8. Clem, R.J., Cheng, E.H., Karp, C.L., Kirsch, D.G., Ueno, K., Takahashi, A., Kastan, M.B., Griffin, D.E., Earnshaw, W.C., Veliuona, M.A., et al. 1998. Modulation of cell death by Bcl-XL through caspase interaction. Proc. Natl. Acad. Sci. 95: 554-559.
9. Collaborative Computational Project, N. 1994. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50: 760-763.
10. Cuconati, A. and White, E. 2002. Viral homologs of BCL-2: Role of apoptosis in the regulation of virus infection. Genes & Dev. 16: 2465-2478.
11. De Lano, W. 2002. The PyMOL molecular graphics system. Delando Scientific, San Carlos, CA.
12. Everett, H. and McFadden, G. 2001. Viruses and apoptosis: Meddling with mitochondria. Virology 288: 1-7.
13. Everett, H., Barry, M., Lee, S.F., Sun, X., Graham, K., Stone, J., Bleackley, R.C., and McFadden, G. 2000. M11L: A novel mitochondria-localized protein of myxoma virus that blocks apoptosis of infected leukocytes. J. Exp. Med. 191: 1487-1498.
14. Everett, H., Barry, M., Sun, X., Lee, S.F., Frantz, C., Berthiaume, L.G., McFadden, G., and Bleackley, R.C. 2002. The myxoma poxvirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore. J. Exp. Med. 196: 1127-1139.
15. Fischer, S.F., Ludwig, H., Holzapfel, J., Kvansakul, M., Chen, L., Huang, D.C., Sutter, G., Knese, M., and Hacker, G. 2006. 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: 109-118.
16. Gubser, C., Hue, S., Kellam, P., and Smith, G.L. 2004. Poxvirus genomes: A phylogenetic analysis. J. Gen. Virol. 85: 105-117.
17. Holton, J. and Alber, T. 2004. Automated protein crystal structure determination using ELVES. Proc. Natl. Acad. Sci. 101: 1537-1542.
18. Huang, Q., Petros, A.M., Virgin, H.W., Fesik, S.W., and Olejniczak, E.T. 2002. Solution structure of a Bcl-2 homolog from Kaposi sarcoma virus. Proc. Natl. Acad. Sci. 99: 3428-3433.
19. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
20. Kantardjieff, K.A. and Rupp, B. 2003. Matthews coefficient probabilities: Improved estimates for unit cell contents of proteins, DNA, and protein-nucleic acid complex crystals. Protein Sci. 12: 1865-1871.
21. Kapust, R.B. and Waugh, D.S. 1999. Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused. Protein Sci. 8: 1668-1674.
22. Kelekar, A., Chang, B.S., Harlan, J.E., Fesik, S.W., and Thompson, C.B. 1997. Bad is a BH3 domain-containing protein that forms an inactivating dimer with Bcl-XL. Mol. Cell. Biol. 17: 7040-7046.
23. Kerr, P. and McFadden, G. 2002. Immune responses to myxoma virus. Viral Immunol. 15: 229-246.
24. Kleywegt, G.J. 1996. Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr. D Biol. Crystallogr. 52: 842-857.
25. MacDowell, A.A., Celestre, R.S., Howells, M., McKinney, W., Krupnick, J., Cambie, D., Domning, E.E., Duarte, R.M., Kelez, N., Plate, D.W., et al. 2004. Suite of three protein crystallography beamlines with single superconducting bend magnet as the source. J. Synchrotron Radiat. 11: 447-455.
26. Marsden, V.S. and Strasser, A. 2003. Control of apoptosis in the immune system: Bcl-2, BH3-only proteins and more. Annu. Rev. Immunol. 21: 71-105.
27. Matthews, B.W. 1968. Solvent content of protein crystals. J. Mol. Biol. 33: 491-497.
28. Muchmore, S.W., Sattler, M., Liang, H., Meadows, R.P., Harlan, J.E., Yoon, H.S., Nettesheim, D., Chang, B.S., Thompson, C.B., Wong, S.L., et al. 1996. X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381: 335-341.
29. Ojala, P.M., Yamamoto, K., Castanos-Velez, E., Biberfeld, P., Korsmeyer, S.J., and Makela, T.P. 2000. The apoptotic v-cyclin-CDK6 complex phosphorylates and inactivates Bcl-2. Nat. Cell Biol. 2: 819-825.
30. Opgenorth, A., Graham, K., Nation, N., Strayer, D., and McFadden, G. 1992. Deletion analysis of two tandemly arranged virulence genes in myxoma virus, M11L and myxoma growth factor. J. Virol. 66: 4720-4731.
31. Ottilie, S., Diaz, J.-L., Horne, W., Chang, J., Wang, Y., Wilson, G., Chang, S., Weeks, S., Fritz, L.C., and Oltersdorf, T. 1997. Dimerization properties of human BAD. Identification of a BH-3 domain and analysis of its binding to mutant BCL-2 and BCL-XL proteins. J. Biol. Chem. 272: 30866-30872.
32. Otwinowski, Z., Minor, W., and Carter, Jr., C.W. 1997. Processing of X-ray diffraction data collected in oscillation mode. In Methods in enzymology, pp. 307-326. Academic Press, San Diego, CA.
33. Petros, A.M., Nettesheim, D.G., Wang, Y., Olejniczak, E.T., Meadows, R.P., Mack, J., Swift, K., Matayoshi, E.D., Zhang, H., Thompson, C.B., et al. 2000. Rationale for Bcl-xL/Bad peptide complex formation from structure, mutagenesis, and biophysical studies. Protein Sci. 9: 2528-2534.
34. Petros, A.M., Medek, A., Nettesheim, D.G., Kim, D.H., Yoon, H.S., Swift, K., Matayoshi, E.D., Oltersdorf, T., and Fesik, S.W. 2001. Solution structure of the antiapoptotic protein bcl-2. Proc. Natl. Acad. Sci. 98: 3012-3017.
35. Petros, A.M., Olejniczak, E.T., and Fesik, S.W. 2004. Structural biology of the Bcl-2 family of proteins. Biochim. Biophys. Acta 1644: 83-94.
36. Polster, B.M., Pevsner, J., and Hardwick, J.M. 2004. Viral Bcl-2 homologs and their role in virus replication and associated diseases. Biochim. Biophys. Acta 1644: 211-227.
37. Postigo, A., Cross, J.R., Downward, J., and Way, M. 2006. Interaction of F1L with the BH3 domain of Bak is responsible for inhibiting vaccinia-induced apoptosis. Cell Death Differ. 13: 1651-1662.
38. Prinz, W.A., Aslund, F., Holmgren, A., and Beckwith, J. 1997. The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J. Biol. Chem. 272: 15661-15667.
39. Reed, J.C., Jurgensmeier, J.M., and Matsuyama, S. 1998. Bcl-2 family proteins and mitochondria. Biochim. Biophys. Acta 1366: 127-137.
40. Sattler, M., Liang, H., Nettesheim, D., Meadows, R.P., Harlan, J.E., Eberstadt, M., Yoon, H.S., Shuker, S.B., Chang, B.S., Minn, A.J., et al. 1997. Structure of Bcl-xL-Bak peptide complex: Recognition between regulators of apoptosis. Science 275: 983-986.
41. Sharpe, J.C., Arnoult, D., and Youle, R.J. 2004. Control of mitochondrial permeability by Bcl-2 family members. Biochim. Biophys. Acta 1644: 107-113.
42. Stewart, T.L., Wasilenko, S.T., and Barry, M. 2005. Vaccinia virus F1L protein is a tail-anchored protein that functions at the mitochondria to inhibit apoptosis. J. Virol. 79: 1084-1098.
43. Su, J., Wang, G., Barrett, J.W., Irvine, T.S., Gao, X., and McFadden, G. 2006. Myxoma virus M11L blocks apoptosis through inhibition of conformational activation of Bax at the mitochondria. J. Virol. 80: 1140-1151.
44. Suzuki, M., Youle, R.J., and Tjandra, N. 2000. Structure of Bax: Coregulation of dimer formation and intracellular localization. Cell 103: 645-654.
45. Taylor, J.M. and Barry, M. 2006. Near death experiences: Poxvirus regulation of apoptotic death. Virology 344: 139-150.
46. Taylor, J.M., Quilty, D., Banadyga, L., and Barry, M. 2006. The vaccinia virus protein F1L interacts with Bim and inhibits activation of the pro-apoptotic protein Bax. J. Biol. Chem. 281: 39728-39739.
47. Terwilliger, T. 2004. SOLVE and RESOLVE: Automated structure solution, density modification and model building. J. Synchrotron Radiat. 11: 49-52.
48. Van Duyne, G.D., Standaert, R.F., Karplus, P.A., Schreiber, S.L., and Clardy, J. 1993. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229: 105-124.
49. Wang, G., Barrett, J.W., Nazarian, S.H., Everett, H., Gao, X., Bleackley, C., Colwill, K., Moran, M.F., and McFadden, G. 2004. Myxoma virus M11L prevents apoptosis through constitutive interaction with Bak. J. Virol. 78: 7097-7111.
50. Wasilenko, S.T., Stewart, T.L., Meyers, A.F., and Barry, M. 2003. Vaccinia virus encodes a previously uncharacterized mitochondrial-associated inhibitor of apoptosis. Proc. Natl. Acad. Sci. 100: 14345-14350.
51. Wasilenko, S.T., Banadyga, L., Bond, D., and Barry, M. 2005. The vaccinia virus F1L protein interacts with the proapoptotic protein Bak and inhibits Bak activation. J. Virol. 79: 14031-14043.
52. Winn, M.D., Isupov, M.N., and Murshudov, G.N. 2001. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 57: 122-133.
53. Zhang, H., Nimmer, P., Rosenberg, S.H., Ng, S.C., and Joseph, M. 2002. Development of a high-throughput fluorescence polarization assay for Bcl-x(L). Anal. Biochem. 307: 70-75.