Structure and function of A41, a vaccinia virus chemokine binding protein

PLoS Pathogens

Volumn 4, Issue 1, 2008, Pages 0055-0068

  Bahar, Mohammad W ^a   Kenyon, Julia C ^b   Putz, Mike M ^b   Abrescia, Nicola G A ^a   Pease, James E ^b   Wise, Emma L ^b   Stuart, David I ^a   Smith, Geoffrey L ^b   Grimes, Jonathan M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CHEMOKINE; BINDING PROTEIN; CHEMOKINE CCL25; CHEMOKINE CCL28; CHEMOKINE INHIBITOR; CHEMOKINE INHIBITOR VCCI; EOTAXIN 3; GLYCOSAMINOGLYCAN; HEPARIN; PROTEIN VCKBP; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG; VIRUS PROTEIN A41; VIRUS PROTEIN;

A41L GENE; ANIMAL CELL; ARTICLE; BINDING SITE; CD8+ T LYMPHOCYTE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DOSE RESPONSE; DRUG MECHANISM; HUMAN; IMMUNE RESPONSE; LIGAND BINDING; NONHUMAN; OPTICAL RESOLUTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION; SURFACE PLASMON RESONANCE; VACCINIA VIRUS; VIRUS GENE; VIRUS REPLICATION; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CHEMOTAXIS; CRYSTALLIZATION; CYTOLOGY; IMMUNOLOGY; LEUKOCYTE; METABOLISM; MOLECULAR GENETICS; MOUSE; PHYSIOLOGY; PROTEIN BINDING; PROTEIN CONFORMATION;

MURINAE; POXVIRIDAE; VACCINIA VIRUS;

AMINO ACID SEQUENCE; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CHEMOKINES, CC; CHEMOTAXIS; CRYSTALLIZATION; GLYCOSAMINOGLYCANS; HEPARIN; HUMANS; LEUKOCYTES; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; VACCINIA VIRUS; VIRAL PROTEINS;

EID: 38949213433     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0040005     Document Type: Article

References (67)

1. Charo IF, Ransohoff RM (2006) The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354: 610-621.
2. Rot A, von Andrian UH (2004) Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu Rev Immunol 22: 891-928.
3. Zlotnik A, Yoshie O (2000) Chemokines: a new classification system and their role in immunity. Immunity 12: 121-127.
4. Lau EK, Allen S, Hsu AR, Handel TM (2004) Chemokine-receptor interactions: GPCRs, glycosaminoglycans and viral chemokine binding proteins. Adv Protein Chem 68: 351-391.
5. Fernandez EJ, Lolis E (2002) Structure, function, and inhibition of chemokines. Annu Rev Pharmacol Toxicol 42: 469-499.
6. Moss B (2007) Poxviridae: the viruses and their replicaton. In: Knipe DM, editor. Fields Virology. Philadelphia: Lippincott Williams & Wilkins. pp. 2905-2946.
7. Fenner F, Anderson DA, Arita I, Jezek Z, Ladnyi ID (1988) Smallpox and its eradication. Geneva.
8. Goebel SJ, Johnson GP, Perkus ME, Davis SW, Winslow JP, et al. (1990) The complete DNA sequence of vaccinia virus. Virology 179: 247-266, 517-263.
9. Poxvirus Bioinformatics Resource Center. (2007) Ver. 6.3.1. Available: http://www.poxvirus.org/. Accessed June 2007.
10. Alcami A (2003) Viral mimicry of cytokines, chemokines and their receptors. Nat Rev Immunol 3: 36-50.
11. Lalani AS, Barrett JW, McFadden G (2000) Modulating chemokines: more lessons from viruses. Immunol Today 21: 100-106.
12. Graham KA, Lalani AS, Macen JL, Ness TL, Barry M, et al. (1997) The T1/35kDa family of poxvirus-secreted proteins bind chemokines and modulate leukocyte influx into virus-infected tissues. Virology 229: 12-24.
13. Alcami A, Symons JA, Collins PD, Williams TJ, Smith GL (1998) Blockade of chemokine activity by a soluble chemokine binding protein from vaccinia virus. J Immunol 160: 624-633.
14. Smith CA, Smith TD, Smolak PJ, Friend D, Hagen H, et al. (1997) Poxvirus genomes encode a secreted, soluble protein that preferentially inhibits beta chemokine activity yet lacks sequence homology to known chemokine receptors. Virology 236: 316-327.
15. Lalani AS, Graham K, Mossman K, Rajarathnam K, Clark-Lewis I, et al. (1997) The purified myxoma virus gamma interferon receptor homolog MT7 interacts with the heparin-binding domains of chemokines. J Virol 71: 4356-4363.
16. Carfi A, Smith CA, Smolak PJ, McGrew J, Wiley DC (1999) Structure of a soluble secreted chemokine inhibitor vCCI (p35) from cowpox virus. Proc Natl Acad Sci U S A 96: 12379-12383.
17. Zhang L, Derider M, McCornack MA, Jao SC, Isern N, et al. (2006) Solution structure of the complex between poxvirus-encoded CC chemokine inhibitor vCCI and human MIP-1beta. Proc Natl Acad Sci U S A 103: 13985-13990.
18. Arnold PL, Fremont DH (2006) Structural determinants of chemokine binding by an Ectromelia virus-encoded decoy receptor. J Virol 80: 7439-7449.
19. Ng A, Tscharke DC, Reading PC, Smith GL (2001) The vaccinia virus A41L protein is a soluble 30 kDa glycoprotein that affects virus virulence. J Gen Virol 82: 2095-2105.
20. Clark RH, Kenyon JC, Bartlett NW, Tscharke DC, Smith GL (2006) Deletion of gene A41L enhances vaccinia virus immunogenicity and vaccine efficacy. J Gen Virol 87: 29-38.
21. Deane D, McInnes CJ, Percival A, Wood A, Thomson J, et al. (2000) Orf virus encodes a novel secreted protein inhibitor of granulocyte-macrophage colony-stimulating factor and interleukin-2. J Virol 74: 1313-1320.
22. Ward GA, Stover CK, Moss B, Fuerst TR (1995) Stringent chemical and thermal regulation of recombinant gene expression by vaccinia virus vectors in mammalian cells. Proc Natl Acad Sci U S A 92: 6773-6777.
23. Lalani AS, Ness TL, Singh R, Harrison JK, Seet BT, et al. (1998) Functional comparisons among members of the poxvirus T1/35kDa family of soluble CC-chemokine inhibitor glycoproteins. Virology 250: 173-184.
24. Seet BT, Singh R, Paavola C, Lau EK, Handel TM, et al. (2001) Molecular determinants for CC-chemokine recognition by a poxvirus CC-chemokine inhibitor. Proc Natl Acad Sci U S A 98: 9008-9013.
25. Pease JE, Wang J, Ponath PD, Murphy PM (1998) The N-terminal extracellular segments of the chemokine receptors CCR1 and CCR3 are determinants for MIP-1alpha and eotaxin binding, respectively, but a second domain is essential for efficient receptor activation. J Biol Chem 273: 19972-19976.
26. Wang L, Fuster M, Sriramarao P, Esko JD (2005) Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat Immunol 6: 902-910.
27. Alexander JM, Nelson CA, van Berkel V, Lau EK, Studts JM, et al. (2002) Structural basis of chemokine sequestration by a herpesvirus decoy receptor. Cell 111: 343-356.
28. Stuart DI, Levine M, Muirhead H, Stammers DK (1979) Crystal structure of cat muscle pyruvate kinase at a resolution of 2.6 A. J Mol Biol 134: 109-142.
29. Burns JM, Dairaghi DJ, Deitz M, Tsang M, Schall TJ (2002) Comprehensive mapping of poxvirus vCCI chemokine-binding protein. Expanded range of ligand interactions and unusual dissociation kinetics. J Biol Chem 277: 2785-2789.
30. Proudfoot AE, Handel TM, Johnson Z, Lau EK, LiWang P, et al. (2003) Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc Natl Acad Sci U S A 100: 1885-1890.
31. Flanagan K, Moroziewicz D, Kwak H, Horig H, Kaufman HL (2004) The lymphoid chemokine CCL21 costimulates naive T cell expansion and Th1 polarization of non-regulatory CD4+ T cells. Cell Immunol 231: 75-84.
32. Ashour AE, Turnquist HR, Singh RK, Talmadge JE, Solheim JC (2007) CCL21-induced immune cell infiltration. Int Immunopharmacol 7: 272-276.
33. Okada T, Cyster JG (2007) CC chemokine receptor 7 contributes to Gi-dependent T cell motility in the lymph node. J Immunol 178: 2973-2978.
34. Worbs T, Mempel TR, Bolter J, von Andrian UH, Forster R (2007) CCR7 ligands stimulate the intranodal motility of T lymphocytes in vivo. J Exp Med 204: 489-495.
35. Chen Q, Fisher DT, Clancy KA, Gauguet JM, Wang WC, et al. (2006) Fever-range thermal stress promotes lymphocyte trafficking across high endothelial venules via an interleukin 6 trans-signaling mechanism. Nat Immunol 7: 1299-1308.
36. Choi YK, Fallert BA, Murphey-Corb MA, Reinhart TA (2003) Simian immunodeficiency virus dramatically alters expression of homeostatic chemokines and dendritic cell markers during infection in vivo. Blood 101: 1684-1691.
37. Nattermann J, Zimmermann H, Iwan A, von Lilienfeld-Toal M, Leifeld L, et al. (2006) Hepatitis C virus E2 and CD81 interaction may be associated with altered trafficking of dendritic cells in chronic hepatitis C. Hepatology 44: 945-954.
38. Jensen KK, Chen SC, Hipkin RW, Wiekowski MT, Schwarz MA, et al. (2003) Disruption of CCL21-induced chemotaxis in vitro and in vivo by M3, a chemokine-binding protein encoded by murine gammaherpesvirus 68. J Virol 77: 624-630.
39. Soldevila G, Licona I, Salgado A, Ramirez M, Chavez R, et al. (2004) Impaired chemokine-induced migration during T-cell development in the absence of Jak 3. Immunology 112: 191-200.
40. Wurbel MA, Malissen M, Guy-Grand D, Meffre E, Nussenzweig MC, et al. (2001) Mice lacking the CCR9 CC-chemokine receptor show a mild impairment of early T- and B-cell development and a reduction in T-cell receptor gammadelta(+) gut intraepithelial lymphocytes. Blood 98: 2626-2632.
41. Wang W, Soto H, Oldham ER, Buchanan ME, Homey B, et al. (2000) Identification of a novel chemokine (CCL28), which binds CCR10 (GPR2). J Biol Chem 275: 22313-22323.
42. Hieshima K, Ohtani H, Shibano M, Izawa D, Nakayama T, et al. (2003) CCL28 has dual roles in mucosal immunity as a chemokine with broad-spectrum antimicrobial activity. J Immunol 170: 1452-1461.
43. Reading PC, Symons JA, Smith GL (2003) A soluble chemokine-binding protein from vaccinia virus reduces virus virulence and the inflammatory response to infection. J Immunol 170: 1435-1442.
44. Stachowiak AN, Wang Y, Huang YC, Irvine DJ (2006) Homeostatic lymphoid chemokines synergize with adhesion ligands to trigger T and B lymphocyte chemokinesis. J Immunol 177: 2340-2348.
45. Hanson CV, Riggs JL, Lennette EH (1978) Photochemical inactivation of DNA and RNA viruses by psoralen derivatives. J Gen Virol 40: 345-358.
46. Duchesnes CE, Murphy PM, Williams TJ, Pease JE (2006) Alanine scanning mutagenesis of the chemokine receptor CCR3 reveals distinct extracellular residues involved in recognition of the eotaxin family of chemokines. Mol Immunol 43: 1221-1231.
47. de Mendonca FL, da Fonseca PC, Phillips RM, Saldanha JW, Williams TJ, et al. (2005) Site-directed mutagenesis of CC chemokine receptor 1 reveals the mechanism of action of UCB 35625, a small molecule chemokine receptor antagonist. J Biol Chem 280: 4808-4816.
48. Martinelli R, Sabroe I, LaRosa G, Williams TJ, Pease JE (2001) The CC chemokine eotaxin (CCL11) is a partial agonist of CC chemokine receptor 2b. J Biol Chem 276: 42957-42964.
49. Phillips RM, Stubbs VE, Henson MR, Williams TJ, Pease JE, et al. (2003) Variations in eosinophil chemokine responses: an investigation of CCR1 and CCR3 function, expression in atopy, and identification of a functional CCR1 promoter. J Immunol 170: 6190-6201.
50. Walter TS, Diprose J, Brown J, Pickford M, Owens RJ, et al. (2003) A procedure for setting up high-throughput nanolitre crystallization experiments. I. Protocol design and validation. Journal of Applied Crystallography 36: 308-314.
51. Brown J, Walter TS, Carter L, Abrescia NGA, Aricescu AR, et al. (2003) A procedure for setting up high-throughput nanolitre crystallization experiments. II. Crystallization results. Journal of Applied Crystallography 36: 315-318.
52. Walter TS, Diprose JM, Mayo CJ, Siebold C, Pickford MG, et al. (2005) A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization. Acta Crystallogr D Biol Crystallogr 61: 651-657.
53. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Macromolecular Crystallography, Pt A 276: 307-326.
54. Schneider TR, Sheldrick GM (2002) Substructure solution with SHELXD. Acta Crystallogr D Biol Crystallogr 58: 1772-1779.
55. Sheldrick GM (2002) Macromolecular phasing with SHELXE. Z Kristallogr 217: 644-650.
56. Pape T, Schneider TR (2004) HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. Journal of Applied Crystallography 37: 843-844.
57. Terwilliger T (2000) Maximum-likelihood density modification. Acta Crystallographica Section D 56: 965-972.
58. Perrakis A, Morris R, Lamzin VS (1999) Automated protein model building combined with iterative structure refinement. Nat Struct Biol 6: 458-463.
59. Jones TA, , Zou JY, Cowan SW, Kjeldgaard (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47 ( Pt 2): 110-119.
60. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54 ( Pt 5): 905-921.
61. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of Macromolecular Structures by the Maximum-Likelihood Method. Acta Crystallographica Section D 53: 240-255.
62. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
63. Davis IW, Murray LW, Richardson JS, Richardson DC (2004) MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res 32: W615-619.
64. Gouet P, Courcelle E, Stuart DI, Metoz F (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.
65. DeLano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA.
66. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041.
67. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.