Crystal Structure of Vaccinia Viral A27 Protein Reveals a Novel Structure Critical for Its Function and Complex Formation with A26 Protein

PLoS Pathogens

Volumn 9, Issue 8, 2013, Pages

  Chang, Tao Hsin ^a,f,g   Chang, Shu Jung ^b,c   Hsieh, Fu Lien ^a,d,f   Ko, Tzu Ping ^a   Lin, Cheng Tse ^a   Ho, Meng Ru ^a   Wang, Iren ^a   Hsu, Shang Te Danny ^a,d   Guo, Rey Ting ^a,h   Chang, Wen ^b,c   Wang, Andrew H J ^a,d,e  

^a INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e ACADEMIA SINICA   (Taiwan)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g UNIVERSITY OF OXFORD   (United Kingdom)

^h Chinese Academy of Sciences   (China)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VACCINIA VIRUS PROTEIN A27; VIRUS ENVELOPE PROTEIN; VIRUS FUSION PROTEIN; A27 PROTEIN, VACCINIA VIRUS; CARRIER PROTEIN; MULTIPROTEIN COMPLEX;

AFFINITY CHROMATOGRAPHY; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUSION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; FLUORESCENCE MICROSCOPY; GEL PERMEATION CHROMATOGRAPHY; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SEQUENCE ALIGNMENT; ULTRACENTRIFUGATION; VACCINIA VIRUS; CHEMISTRY; GENETICS; HELA CELL LINE; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; HELA CELLS; HUMANS; MULTIPROTEIN COMPLEXES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; VACCINIA VIRUS; VIRAL FUSION PROTEINS;

EID: 84883438662     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003563     Document Type: Article

References (61)

1. Goebel SJ, Johnson GP, Perkus ME, Davis SW, Winslow JP, et al. (1990) The complete DNA sequence of vaccinia virus. Virology 179: 247-266, 517263.
2. Condit RC, Moussatche N, Traktman P, (2006) In a nutshell: structure and assembly of the vaccinia virion. Adv Virus Res 66: 31-124.
3. Chung CS, Chen CH, Ho MY, Huang CY, Liao CL, et al. (2006) Vaccinia virus proteome: identification of proteins in vaccinia virus intracellular mature virion particles. J Virol 80: 2127-2140.
4. Resch W, Hixson KK, Moore RJ, Lipton MS, Moss B, (2007) Protein composition of the vaccinia virus mature virion. Virology 358: 233-247.
5. Chung CS, Hsiao JC, Chang YS, Chang W, (1998) A27L protein mediates vaccinia virus interaction with cell surface heparan sulfate. J Virol 72: 1577-1585.
6. Hsiao JC, Chung CS, Chang W, (1999) Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J Virol 73: 8750-8761.
7. Lin CL, Chung CS, Heine HG, Chang W, (2000) Vaccinia virus envelope H3L protein binds to cell surface heparan sulfate and is important for intracellular mature virion morphogenesis and virus infection in vitro and in vivo. J Virol 74: 3353-3365.
8. Chiu WL, Lin CL, Yang MH, Tzou DL, Chang W, (2007) Vaccinia virus 4c (A26L) protein on intracellular mature virus binds to the extracellular cellular matrix laminin. J Virol 81: 2149-2157.
9. Rodriguez JF, Janeczko R, Esteban M, (1985) Isolation and characterization of neutralizing monoclonal antibodies to vaccinia virus. J Virol 56: 482-488.
10. Rodriguez JF, Esteban M, (1987) Mapping and nucleotide sequence of the vaccinia virus gene that encodes a 14-kilodalton fusion protein. J Virol 61: 3550-3554.
11. Rodriguez JF, Paez E, Esteban M, (1987) A 14,000-Mr envelope protein of vaccinia virus is involved in cell fusion and forms covalently linked trimers. J Virol 61: 395-404.
12. Gong SC, Lai CF, Esteban M, (1990) Vaccinia virus induces cell fusion at acid pH and this activity is mediated by the N-terminus of the 14-kDa virus envelope protein. Virology 178: 81-91.
13. Vazquez MI, Rivas G, Cregut D, Serrano L, Esteban M, (1998) The vaccinia virus 14-kilodalton (A27L) fusion protein forms a triple coiled-coil structure and interacts with the 21-kilodalton (A17L) virus membrane protein through a C-terminal alpha-helix. J Virol 72: 10126-10137.
14. Kochan G, Escors D, Gonzalez JM, Casasnovas JM, Esteban M, (2008) -Membrane cell fusion activity of the vaccinia virus A17A27 protein complex. Cell Microbiol 10: 149-164.
15. Moss B, (2012)? Poxvirus cell entry: how many proteins does it take Viruses 4: 688-707.
16. Whitbeck JC, Foo CH, Ponce de Leon M, Eisenberg RJ, Cohen GH, (2009) Vaccinia virus exhibits cell-type-dependent entry characteristics. Virology 385: 383-391.
17. Chang SJ, Chang YX, Izmailyan R, Tang YL, Chang W, (2010) Vaccinia virus A25 and A26 proteins are fusion suppressors for mature virions and determine strain-specific virus entry pathways into HeLa, CHO-K1, and L cells. Journal of virology 84: 8422-8432.
18. Bengali Z, Satheshkumar PS, Moss B, (2012) Orthopoxvirus species and strain differences in cell entry. Virology 433: 506-512.
19. Izmailyan R, Hsao JC, Chung CS, Chen CH, Hsu PW, et al. (2012) Integrin beta1 mediates vaccinia virus entry through activation of PI3K/Akt signaling. J Virol 86: 6677-6687.
20. Schroeder N, Chung CS, Chen CH, Liao CL, Chang W, (2012) The lipid raft-associated protein CD98 is required for vaccinia virus endocytosis. J Virol 86: 4868-4882.
21. Chang SJ, Shih AC, Tang YL, Chang W, (2012) Vaccinia mature virus fusion regulator A26 protein binds to A16 and G9 proteins of the viral entry fusion complex and dissociates from mature virions at low pH. J Virol 86: 3809-18.
22. Howard AR, Senkevich TG, Moss B, (2008) Vaccinia virus A26 and A27 proteins form a stable complex tethered to mature virions by association with the A17 transmembrane protein. J Virol 82: 12384-12391.
23. Ching YC, Chung CS, Huang CY, Hsia Y, Tang YL, et al. (2009) Disulfide bond formation at the C termini of vaccinia virus A26 and A27 proteins does not require viral redox enzymes and suppresses glycosaminoglycan-mediated cell fusion. J Virol 83: 6464-6476.
24. Rodriguez D, Rodriguez JR, Esteban M, (1993) The vaccinia virus 14-kilodalton fusion protein forms a stable complex with the processed protein encoded by the vaccinia virus A17L gene. J Virol 67: 3435-3440.
25. Sanderson CM, Hollinshead M, Smith GL, (2000) The vaccinia virus A27L protein is needed for the microtubule-dependent transport of intracellular mature virus particles. J Gen Virol 81: 47-58.
26. Ward BM, (2005) Visualization and characterization of the intracellular movement of vaccinia virus intracellular mature virions. J Virol 79: 4755-4763.
27. Rodriguez JF, Smith GL, (1990) Inducible gene expression from vaccinia virus vectors. Virology 177: 239-250.
28. Rodriguez JF, Smith GL, (1990) IPTG-dependent vaccinia virus: identification of a virus protein enabling virion envelopment by Golgi membrane and egress. Nucleic Acids Res 18: 5347-5351.
29. Lin TH, Chia CM, Hsiao JC, Chang W, Ku CC, et al. (2002) Structural analysis of the extracellular domain of vaccinia virus envelope protein, A27L, by NMR and CD spectroscopy. J Biol Chem 277: 20949-20959.
30. Shih PC, Yang MS, Lin SC, Ho Y, Hsiao JC, et al. (2009) A turn-like structure "KKPE" segment mediates the specific binding of viral protein A27 to heparin and heparan sulfate on cell surfaces. J Biol Chem 284: 36535-36546.
31. Ho Y, Hsiao JC, Yang MH, Chung CS, Peng YC, et al. (2005) The oligomeric structure of vaccinia viral envelope protein A27L is essential for binding to heparin and heparan sulfates on cell surfaces: a structural and functional approach using site-specific mutagenesis. J Mol Biol 349: 1060-1071.
32. Hsiao JC, Chung CS, Chang W, (1998) Cell surface proteoglycans are necessary for A27L protein-mediated cell fusion: identification of the N-terminal region of A27L protein as the glycosaminoglycan-binding domain. J Virol 72: 8374-8379.
33. Krissinel E, (2010) 'Crystal contacts as natures docking solutions. J Comput Chem 31: 133-143.
34. Fry EE, Lea SM, Jackson T, Newman JW, Ellard FM, et al. (1999) The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. Embo J 18: 543-554.
35. Xie Q, Bu W, Bhatia S, Hare J, Somasundaram T, et al. (2002) The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proc Natl Acad Sci U S A 99: 10405-10410.
36. Opie SR, Warrington KH Jr, Agbandje-McKenna M, Zolotukhin S, Muzyczka N, (2003) Identification of amino acid residues in the capsid proteins of adeno-associated virus type 2 that contribute to heparan sulfate proteoglycan binding. J Virol 77: 6995-7006.
37. Kern A, Schmidt K, Leder C, Muller OJ, Wobus CE, et al. (2003) Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J Virol 77: 11072-11081.
38. Vazquez MI, Esteban M, (1999) Identification of functional domains in the 14-kilodalton envelope protein (A27L) of vaccinia virus. J Virol 73: 9098-9109.
39. van Holde KE, Johnson WC, Ho PS (2005) Principles of Physical Biochemistry Upper Saddle River: Prentice-Hall, Inc.
40. Davison AJ, Moss B, (1990) New vaccinia virus recombination plasmids incorporating a synthetic late promoter for high level expression of foreign proteins. Nucleic Acids Res 18: 4285-4286.
41. Chang SJ, Shih AC, Tang YL, Chang W, (2012) Vaccinia mature virus fusion regulator A26 protein binds to A16 and G9 proteins of the viral entry fusion complex and dissociates from mature virions at low pH. J Virol 86: 3809-3818.
42. Fauvet B, Mbefo MK, Fares MB, Desobry C, Michael S, et al. (2012) alpha-Synuclein in central nervous system and from erythrocytes, mammalian cells, and Escherichia coli exists predominantly as disordered monomer. J Biol Chem 287: 15345-15364.
43. Vazquez M-I, Rivas G, Cregut D, Serrano L, Esteban M, (1998) αThe vaccinia virus 14-Kilodalton (A27L) fusion protein forms a triple coiled-coil structure and interacts with the 21-Kilodalton (A17L) virus membrane protein through a C-terminal-helix. J Virol 72: 10126-10137.
44. Senkevich TG, Ojeda S, Townsley A, Nelson GE, Moss B, (2005) Poxvirus multiprotein entry-fusion complex. Proc Natl Acad Sci U S A 102: 18572-18577.
45. Engelstad M, Smith GL, (1993) The vaccinia virus 42-kDa envelope protein is required for the envelopment and egress of extracellular virus and for virus virulence. Virology 194: 627-637.
46. Payne L, (1978) Polypeptide composition of extracellular enveloped vaccinia virus. J Virol 27: 28-37.
47. -Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Macromolecular Crystallography, Pt A. San Diego: Academic Press Inc. pp. 307326.
48. Brunger AT, (1993) Assessment of phase accuracy by cross validation: the free R value. Methods and applications. Acta Crystallogr D Biol Crystallogr 49: 24-36.
49. Sheldrick GM, (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr D Biol Crystallogr 66: 479-485.
50. Vonrhein C, Blanc E, Roversi P, Bricogne G, (2007) Automated structure solution with autoSHARP. Methods Mol Biol 364: 215-230.
51. Cowtan K, (1999) Error estimation and bias correction in phase-improvement calculations. Acta Crystallogr D Biol Crystallogr 55: 1555-1567.
52. Cowtan K, (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62: 1002-1011.
53. McCoy AJ, (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr 63: 32-41.
54. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
55. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
56. Chen VB, Arendall WB, (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21.
57. Hayes D, Laue T, Philo J (1995) Program Sednterp: sedimentation interpretation program. Durham, NH: University of New Hampshire.
58. Schuck P, (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78: 1606-1619.
59. Izmailyan RA, Huang CY, Mohammad S, Isaacs SN, Chang W, (2006) The envelope G3L protein is essential for entry of vaccinia virus into host cells. J Virol 80: 8402-8410.
60. Bullough PA, Hughson FM, Skehel JJ, Wiley DC, (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371: 37-43.
61. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.