Structures of B-Lymphotropic Polyomavirus VP1 in Complex with Oligosaccharide Ligands

PLoS Pathogens

Volumn 9, Issue 10, 2013, Pages

  Neu, Ursula ^a,e   Khan, Zaigham Mahmood ^a   Schuch, Benjamin ^a,f   Palma, Angelina S ^b,g   Liu, Yan ^b   Pawlita, Michael ^c   Feizi, Ten ^b   Stehle, Thilo ^a,d  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^f MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^g UNIVERSIDADE NOVA DE LISBOA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; OLIGOSACCHARIDE; PROTEIN VP1; SIALIC ACID;

ARTICLE; B LYMPHOTROPIC POLYOMAVIRUS; CELL STRUCTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME SPECIFICITY; GENE AMPLIFICATION; GLYCAN ARRAY SCREENING; HUMAN; HUMAN CELL; LIGAND BINDING; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE MAPPING; POLYMERASE CHAIN REACTION; POLYOMA VIRUS; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RECEPTOR BINDING; STRUCTURE ANALYSIS;

AMINO ACID MOTIFS; BINDING SITES; CAPSID PROTEINS; CARBOHYDRATE CONFORMATION; CROSS REACTIONS; HUMANS; N-ACETYLNEURAMINIC ACID; OLIGOSACCHARIDES; POLYOMAVIRUS; SIMIAN VIRUS 40;

EID: 84887269915     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003714     Document Type: Article

References (47)

1. zur Hausen H, Gissmann L, (1979) Lymphotropic papovaviruses isolated from African green monkey and human cells. Med Microbiol Immunol 167: 137-153.
2. Brade L, Vogl W, Gissman L, zur Hausen H, (1981) Propagation of B-lymphotropic papovavirus (LPV) in human B-lymphoma cells and characterization of its DNA. Virology 114: 228-235.
3. Shein HM, Enders JF, (1962) Transformation induced by simian virus 40 in human renal cell cultures. I. Morphology and growth characteristics. Proc Natl Acad Sci U S A 48: 1164-1172.
4. Eddy BE, Borman GS, Grubbs GE, Young RD, (1962) Identification of the oncogenic substance in rhesus monkey kidney cell culture as simian virus 40. Virology 17: 65-75.
5. Feng H, Shuda M, Chang Y, Moore PS, (2008) Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319: 1096-1100.
6. Jiang M, Abend JR, Johnson SF, Imperiale MJ, (2009) The role of polyomaviruses in human disease. Virology 384: 266-273.
7. Scuda N, Hofmann J, Calvignac-Spencer S, Ruprecht K, Liman P, et al. (2011) A novel human polyomavirus closely related to the African green monkey-derived lymphotropic polyomavirus (LPV). J Virol 85: 4586-4590.
8. Sauvage V, Foulongne V, Cheval J, Ar Gouilh M, Pariente K, et al. (2011) Human polyomavirus related to african green monkey lymphotropic polyomavirus. Emerg Infect Dis 17: 1364-1370.
9. Trusch F, Klein M, Finsterbusch T, Kuhn J, Hofmann J, et al. (2012) Seroprevalence of the human polyomavirus 9 (HPyV9) and cross-reactivity to the African green monkey-derived lymphotropic polyomavirus (LPV). J Gen Virol 93: 698-705.
10. Haun G, Keppler OT, Bock CT, Herrmann M, Zentgraf H, et al. (1993) The cell surface receptor is a major determinant restricting the host range of the B-lymphotropic papovavirus. J Virol 67: 7482-7492.
11. Keppler OT, Stehling P, Herrmann M, Kayser H, Grunow D, et al. (1995) Biosynthetic modulation of sialic acid-dependent virus-receptor interactions of two primate polyoma viruses. J Biol Chem 270: 1308-1314.
12. Oetke C, Brossmer R, Mantey LR, Hinderlich S, Isecke R, et al. (2002) Versatile biosynthetic engineering of sialic acid in living cells using synthetic sialic acid analogues. J Biol Chem 277: 6688-6695.
13. Varki A, (2001) Loss of N-glycolylneuraminic acid in humans: Mechanisms, consequences, and implications for hominid evolution. Am J Phys Anthropol Suppl 33: 54-69.
14. Neu U, Bauer J, Stehle T, (2011) Viruses and sialic acids: rules of engagement. Curr Opin Struct Biol 21: 610-618.
15. Tsai B, Gilbert JM, Stehle T, Lencer W, Benjamin TL, et al. (2003) Gangliosides are receptors for murine polyoma virus and SV40. EMBO J 22: 4346-4355.
16. Low JA, Magnuson B, Tsai B, Imperiale MJ, (2006) Identification of gangliosides GD1b and GT1b as receptors for BK virus. J Virol 80: 1361-1366.
17. Neu U, Maginnis MS, Palma AS, Stroh LJ, Nelson CD, et al. (2010) Structure-function analysis of the human JC polyomavirus establishes the LSTc pentasaccharide as a functional receptor motif. Cell Host Microbe 8: 309-319.
18. Stehle T, Yan Y, Benjamin TL, Harrison SC, (1994) Structure of murine polyomavirus complexed with an oligosaccharide receptor fragment. Nature 369: 160-163.
19. Liddington RC, Yan Y, Moulai J, Sahli R, Benjamin TL, et al. (1991) Structure of simian virus 40 at 3.8-A resolution. Nature 354: 278-284.
20. Neu U, Woellner K, Gauglitz G, Stehle T, (2008) Structural basis of GM1 ganglioside recognition by simian virus 40. Proc Natl Acad Sci U S A 105: 5219-5224.
21. Neu U, Hengel H, Blaum BS, Macejak D, Schowalter RM, et al. (2012) Structures of Merkel Cell Polyomavirus VP1 Complexes Define a Sialic Acid Binding Site Required for Infection. PLoS Pathog 8: e1002738.
22. Stehle T, Harrison SC, (1997) High-resolution structure of a polyomavirus VP1-oligosaccharide complex: implications for assembly and receptor binding. EMBO J 16: 5139-5148.
23. Stehle T, Gamblin SJ, Yan Y, Harrison SC, (1996) The structure of simian virus 40 refined at 3.1 A resolution. Structure 4: 165-182.
24. Chai W, Stoll MS, Galustian C, Lawson AM, Feizi T, (2003) Neoglycolipid technology: deciphering information content of glycome. Methods Enzymol 362: 160-195.
25. Liu Y, Feizi T, Campanero-Rhodes MA, Childs RA, Zhang Y, et al. (2007) Neoglycolipid probes prepared via oxime ligation for microarray analysis of oligosaccharide-protein interactions. Chem Biol 14: 847-859.
26. Breg J, Kroon-Batenburg LM, Strecker G, Montreuil J, Vliegenthart JF, (1989) Conformational analysis of the sialyl alpha(2-3/6)N-acetyllactosamine structural element occurring in glycoproteins, by two-dimensional NOE 1H-NMR spectroscopy in combination with energy calculations by hard-sphere exo-anomeric and molecular mechanics force-field with hydrogen-bonding potential. Eur J Biochem 178: 727-739.
27. Poppe L, Dabrowski J, von der Lieth CW, Numata M, Ogawa T, (1989) Solution conformation of sialosylcerebroside (GM4) and its NeuAc(alpha 2----3)Gal beta sugar component. Eur J Biochem 180: 337-342.
28. Pawlita M, Clad A, zur Hausen H, (1985) Complete DNA sequence of lymphotropic papovavirus: prototype of a new species of the polyomavirus genus. Virology 143: 196-211.
29. Furuno A, Kanda T, Yoshiike K, (1986) Monkey B-lymphotropic papovavirus genome: the entire DNA sequence and variable regions. Jpn J Med Sci Biol 39: 151-161.
30. Kanda T, Furuno A, Yoshiike K, (1986) Mutation in the VP-1 gene is responsible for the extended host range of a monkey B-lymphotropic papovavirus mutant capable of growing in T-lymphoblastoid cells. J Virol 59: 531-534.
31. Gamblin SJ, Skehel JJ, (2010) Influenza hemagglutinin and neuraminidase membrane glycoproteins. J Biol Chem 285: 28403-28409.
32. Kean JM, Rao S, Wang M, Garcea RL, (2009) Seroepidemiology of human polyomaviruses. PLoS Pathog 5: e1000363.
33. Keppler OT, Herrmann M, Oppenlander M, Meschede W, Pawlita M, (1994) Regulation of susceptibility and cell surface receptor for the B-lymphotropic papovavirus by N glycosylation. J Virol 68: 6933-6939.
34. Demarco ML, Woods RJ, Prestegard JH, Tian F, (2010) Presentation of membrane-anchored glycosphingolipids determined from molecular dynamics simulations and NMR paramagnetic relaxation rate enhancement. J Am Chem Soc 132: 1334-1338.
35. Stromberg N, Karlsson KA, (1990) Characterization of the binding of propionibacterium granulosum to glycosphingolipids adsorbed on surfaces. An apparent recognition of lactose which is dependent on the ceramide structure. J Biol Chem 265: 11244-11250.
36. Feizi T, (1992) Angling for recognition. Curr Biol 2: 185-187.
37. Liu Y, Childs RA, Palma AS, Campanero-Rhodes MA, Stoll MS, et al. (2012) Neoglycolipid-based oligosaccharide microarray system: preparation of NGLs and their noncovalent immobilization on nitrocellulose-coated glass slides for microarray analyses. Meth Mol Biol 808: 117-136.
38. Palma AS, Feizi T, Zhang Y, Stoll MS, Lawson AM, et al. (2006) Ligands for the beta-glucan receptor, Dectin-1, assigned using "designer" microarrays of oligosaccharide probes (neoglycolipids) generated from glucan polysaccharides. J Biol Chem 281: 5771-5779.
39. Marchant J, Cowper B, Liu Y, Lai L, Pinzan C, et al. (2012) Galactose recognition by the apicomplexan parasite Toxoplasma gondii. J Biol Chem 287: 16720-16733.
40. Stoll MS, Feizi T (2009) Software tools for storing, processing and displaying carbohydrate microarray data. In: Kettner C, editor. Potsdam, Germany: Beilstein Institute for the Advancement of Chemical Sciences.
41. Kabsch W, (2010) Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr D Biol Crystallogr 66: 133-144.
42. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
43. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
44. Afonine PV, Grosse-Kunstleve RW, Adams PD, (2005) The Phenix refinement framework. CCP4 Newsletter 42: contribution 8.
45. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
46. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
47. Brunger AT, (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355: 472-475.