Mucin-like region of herpes simplex virus type 1 attachment protein glycoprotein C (gC) modulates the virus-glycosaminoglycan interaction

Journal of Biological Chemistry

Volumn 290, Issue 35, 2015, Pages 21473-21485

  Altgärde, Noomi ^a   Eriksson, Charlotta ^b   Peerboom, Nadia ^a   Phan Xuan, Tuan ^a   Moeller, Stephanie ^c   Schnabelrauch, Matthias ^c   Svedhem, Sofia ^a   Trybala, Edward ^b   Bergström, Tomas ^b   Bally, Marta ^a,d  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c BIOMATERIALS DEPARTMENT   (Germany)

^d INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL MEMBRANES; CELLS; CYTOLOGY; GLYCOPROTEINS; HYALURONIC ACID; PROTEINS; PURIFICATION; SURFACE PLASMON RESONANCE;

BINDING ACTIVITIES; BINDING SPECIFICITIES; CHONDROITIN SULFATES; EQUILIBRIUM BINDING; GLYCOSAMINOGLYCANS; HERPES SIMPLEX VIRUS TYPE 1; SULFATED HYALURONAN; VIRUS ATTACHMENTS;

VIRUSES;

CHONDROITIN SULFATE; GLYCOSAMINOGLYCAN; HYALURONIC ACID; MUTANT PROTEIN; PROTEIN C; GLYCOPROTEIN GC, HERPES SIMPLEX VIRUS TYPE 1; MUCIN; PROTEIN BINDING; SIALIDASE; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DISSOCIATION; GLYCOSYLATION; HERPES SIMPLEX VIRUS 1; MUCIN LIKE REGION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; VIRUS ATTACHMENT; VIRUS MUTANT; VIRUS PARTICLE; VIRUS RELEASE; ANIMAL; CELL LINE; CHEMISTRY; FLUORESCENCE MICROSCOPY; HUMAN; KINETICS; METABOLISM; MUTATION; OSMOLARITY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE; VIRION;

ANIMALS; CELL LINE; GLYCOSAMINOGLYCANS; HERPESVIRUS 1, HUMAN; HUMANS; KINETICS; MICROSCOPY, FLUORESCENCE; MUCINS; MUTANT PROTEINS; MUTATION; NEURAMINIDASE; OSMOLAR CONCENTRATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SURFACE PLASMON RESONANCE; VIRAL ENVELOPE PROTEINS; VIRION;

EID: 84940706334     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.637363     Document Type: Article

References (56)

1. Palese, P., Tobita, K., Ueda, M., and Compans, R. W. (1974) Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology 61, 397-410
2. von Itzstein, M., Wu, W. Y., Kok, G. B., Pegg, M. S., Dyason, J. C., Jin, B., Van Phan, T., Smythe, M. L., White, H. F., Oliver, S. W., Colman, P. M., Varghese, J. N., Ryan, D. M., Woods, J. M., Bethell, R. C., Hotham, V. J., Cameronf, J. M., and Penn, C. R. (1993) Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 363, 418-423
3. Vaheri, A. (1964) Heparin and related polyionic substances as virus inhibitors. Acta Pathol. Microbiol. Scand. Suppl. 171, 171-198
4. WuDunn, D., and Spear, P. G. (1989) Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J. Virol. 63, 52-58
5. Krusat, T., and Streckert, H. J. (1997) Heparin-dependent attachment of respiratory syncytial virus (RSV) to host cells. Arch. Virol. 142, 1247-1254
6. Salvador, B., Sexton, N. R., Carrion, R., Jr., Nunneley, J., Patterson, J. L., Steffen, I., Lu, K., Muench, M. O., Lembo, D., and Simmons, G. (2013) Filoviruses utilize glycosaminoglycans for their attachment to target cells. J. Virol. 87, 3295-3304
7. Saphire, A. C. S., Bobardt, M. D., Zhang, Z., David, G., and Gallay, P. A. (2001) Syndecans serve as attachment receptors for human immunodeficiency virus type 1 on macrophages. J. Virol. 75, 9187-9200
8. Olofsson, S., and Bergström, T. (2005) Glycoconjugate glycans as viral receptors. Ann. Med. 37, 154-172
9. Vigerust, D. J., and Shepherd, V. L. (2007) Virus glycosylation: role in virulence and immune interactions. Trends Microbiol. 15, 211-218
10. Olofsson, S., and Hansen, J. E. S. (1998) Host cell glycosylation of viral glycoproteins: a battlefield for host defence and viral resistance. Scand. J. Infect. Dis. 30, 435-440
11. Friedman, H. M., Cohen, G. H., Eisenberg, R. J., Seidel, C. A., and Cines, D. B. (1984) Glycoprotein C of herpes simplex virus 1 acts as a receptor for the C3b complement component on infected cells. Nature 309, 633-635
12. Ekblad, M., Adamiak, B., Bergefall, K., Nenonen, H., Roth, A., Bergstrom, T., Ferro, V., and Trybala, E. (2007) Molecular basis for resistance of herpes simplex virus type 1 mutants to the sulfated oligosaccharide inhibitor PI-88. Virology 367, 244-252
13. Adamiak, B., Ekblad, M., Bergström, T., Ferro, V., and Trybala, E. (2007) Herpes simplex virus type 2 glycoprotein G is targeted by the sulfated oligo- and polysaccharide inhibitors of virus attachment to cells. J. Virol. 81, 13424-13434
14. Herold, B. C., WuDunn, D., Soltys, N., and Spear, P. G. (1991) Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectivity. J. Virol. 65, 1090-1098
15. Spear, P. G. (2004) Herpes simplex virus: receptors and ligands for cell entry. Cell Microbiol. 6, 401-410
16. Altgärde, N., Nilebäck, E., de Battice, L., Pashkuleva, I., Reis, R. L., Becher, J., Möller, S., Schnabelrauch, M., and Svedhem, S. (2013) Probing the biofunctionality of biotinylated hyaluronan and chondroitin sulfate by hyaluronidase degradation and aggrecan interaction. Acta Biomater. 9, 8158-8166
17. Baranova, N. S., Nilebäck, E., Haller, F. M., Briggs, D. C., Svedhem, S., Day, A. J., and Richter, R. P. (2011) The inflammation-associated protein TSG-6 cross-links hyaluronan via hyaluronan-induced TSG-6 oligomers. J. Biol. Chem. 286, 25675-25686
18. Richter, R. P., Hock, K. K., Burkhartsmeyer, J., Boehm, H., Bingen, P., Wang, G., Steinmetz, N. F., Evans, D. J., and Spatz, J. P. (2007) Membrane-grafted hyaluronan films: a well-defined model system of glycoconjugate cell coats. J. Am. Chem. Soc. 129, 5306-5307
19. Osmond, R. I. W., Kett, W. C., Skett, S. E., and Coombe, D. R. (2002) Protein-heparin interactions measured by BIAcore 2000 are affected by the method of heparin immobilization. Anal. Biochem. 310, 199-207
20. Yu, G., Gunay, N. S., Linhardt, R. J., Toida, T., Fareed, J., Hoppensteadt, D. A., Shadid, H., Ferro, V., Li, C., Fewings, K., Palermo, M. C., and Podger, D. (2002) Preparation and anticoagulant activity of the phosphosulfomannan PI-88. Eur. J. Med. Chem. 37, 783-791
21. Adamiak, B., Trybala, E., Mardberg, K., Johansson, M., Liljeqvist, J. A., Olofsson, S., Grabowska, A., Bienkowska-Szewczyk, K., Szewczyk, B., and Bergstrom, T. (2010) Human antibodies to herpes simplex virus type 1 glycoprotein C are neutralizing and target the heparan sulfate-binding domain. Virology 400, 197-206
22. Guenalp, A. (1965) Growth and cytophatic effect of rubella virus in a line of green monkey kidney cells. Proc. Soc. Exp. Biol. Med. 118, 85-90
23. Holland, T. C., Marlin, S. D., Levine, M., and Glorioso, J. (1983) Antigenic variants of herpes simplex virus selected with glycoprotein-specific monoclonal antibodies. J. Virol. 45, 672-682
24. Trybala, E., Bergström, T., Svennerholm, B., Jeansson, S., Glorioso, J. C., and Olofsson, S. (1994) Localization of a functional site on herpes simplex virus type 1 glycoprotein C involved in binding to cell surface heparan sulphate. J. Gen. Virol. 75, 743-752
25. Trybala, E., Liljeqvist, J. A., Svennerholm, B., and Bergström, T. (2000) Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. J. Virol. 74, 9106-9114
26. Ekblad, M., Adamiak, B., Bergstrom, T., Johnstone, K. D., Karoli, T., Liu, L., Ferro, V., and Trybala, E. (2010) A highly lipophilic sulfated tetrasaccharide glycoside related to muparfostat (PI-88) exhibits virucidal activity against herpes simplex virus. Antiviral Res. 86, 196-203
27. Widéhn, S., and Kindblom, L. G. (1990) Agarose embedding: a new method for the ultrastructural examination of the in-situ morphology of cell cultures. Ultrastructural Pathology 14, 81-85
28. Namvar, L., Olofsson, S., Bergström, T., and Lindh, M. (2005) Detection and typing of herpes simplex virus (HSV) in mucocutaneous samples by TaqMan PCR targeting a gB segment homologous for HSV types 1 and 2. J. Clin. Microbiol. 43, 2058-2064
29. Nilebäck, E., Feuz, L., Uddenberg, H., Valiokas, R., and Svedhem, S. (2011) Characterization and application of a surface modification designed for QCM-D studies of biotinylated biomolecules. Biosens. Bioelectron. 28, 407-413
30. Larsson, C., Rodahl, M., and Höök, F. (2003) Characterization of DNA immobilization and subsequent hybridization on a 2D arrangement of streptavidin on a biotin-modified lipid bilayer supported on SiO2. Anal. Chem. 75, 5080-5087
31. Hokputsa, S., Jumel, K., Alexander, C., and Harding, S. E. (2003) Hydrodynamic characterisation of chemically degraded hyaluronic acid. Carbohydr. Polym. 52, 111-117
32. Horkay, F., Basser, P. J., Hecht, A. M., and Geissler, E. (2012) Chondroitin sulfate in solution: effects of mono- and divalent salts. Macromolecules 45, 2882-2890
33. DeAngelis, P. L., Gunay, N. S., Toida, T., Mao, W. J., and Linhardt, R. J. (2002) Identification of the capsular polysaccharides of Type D and F Pasteurella multocida as unmodified heparin and chondroitin, respectively. Carbohydr. Res. 337, 1547-1552
34. Satoh, A., Toida, T., Yoshida, K., Kojima, K., and Matsumoto, I. (2000) New role of glycosaminoglycans on the plasma membrane proposed by their interaction with phosphatidylcholine. FEBS Lett. 477, 249-252
35. Arakawa, T., and Wen, J. (2001) Determination of carbohydrate contents from excess light scattering. Anal. Biochem. 299, 158-161
36. Hill, A. V. (1913) The Combinations of haemoglobin with oxygen and with carbon monoxide. I. Biochem. J. 7, 471-480
37. Weiss, J. N. (1997) The Hill equation revisited: uses and misuses. FASEB J. 11, 835-841
38. Bally, M., Gunnarsson, A., Svensson, L., Larson, G., Zhdanov, V. P., and Höök, F. (2011) Interaction of single viruslike particles with vesicles containing glycosphingolipids. Phys. Rev. Lett. 107, 188103
39. Mårdberg, K., Trybala, E., Glorioso, J. C., and Bergström, T. (2001) Mutational analysis of the major heparan sulfate-binding domain of herpes simplex virus type 1 glycoprotein C. J. Gen. Virol. 82, 1941-1950
40. Mårdberg, K., Trybala, E., Tufaro, F., and Bergström, T. (2002) Herpes simplex virus type 1 glycoprotein C is necessary for efficient infection of chondroitin sulfate-expressing gro2C cells. J. Gen. Virol. 83, 291-300
41. Hadigal, S. R., Agelidis, A. M., Karasneh, G. A., Antoine, T. E., Yakoub, A. M., Ramani, V. C., Djalilian, A. R., Sanderson, R. D., and Shukla, D. (2015) Heparanase is a host enzyme required for herpes simplex virus-1 release from cells. Nat. Commun. 6, 6985
42. Hoffman, J., Larm, O., and Scholander, E. (1983) A new method for covalent coupling of heparin and other glycosaminoglycans to substances containing primary amino groups. Carbohydr. Res. 117, 328-331
43. Tkachenko, E., Rhodes, J. M., and Simons, M. (2005) Syndecans: new kids on the signaling block. Circ. Res. 96, 488-500
44. Stannard, L. M., Fuller, A. O., and Spear, P. G. (1987) Herpes simplex virus glycoproteins associated with different morphological entities projecting from the virion envelope. J. Gen. Virol. 68, 715-725
45. Tal-Singer, R., Peng, C., Ponce De Leon, M., Abrams, W. R., Banfield, B. W., Tufaro, F., Cohen, G. H., and Eisenberg, R. J. (1995) Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. J. Virol. 69, 4471-4483
46. Rux, A. H., Lou, H., Lambris, J. D., Friedman, H. M., Eisenberg, R. J., and Cohen, G. H. (2002) Kinetic analysis of glycoprotein C of herpes simplex virus types 1 and 2 binding to heparin, heparan sulfate, and complement component C3b. Virology 294, 324-332
47. Mårdberg, K., Nyström, K., Tarp, M. A., Trybala, E., Clausen, H., Bergström, T., and Olofsson, S. (2004) Basic amino acids as modulators of an O-linked glycosylation signal of the herpes simplex virus type 1 glycoprotein gC: functional roles in viral infectivity. Glycobiology 14, 571-581
48. Carlström, D. (1957) The crystal structure of α-chitin (poly-N- acetyl-D-glucosamin). J. Biophys. Biochem. Cytol. 3, 669-683
49. Feyzi, E., Trybala, E., Bergström, T., Lindahl, U., and Spillmann, D. (1997) Structural requirement of heparan sulfate for interaction with herpes simplex virus type 1 virions and isolated glycoprotein C. J. Biol. Chem. 272, 24850-24857
50. Jentoft, N. (1990) Why are proteins O-glycosylated? Trends Biochem. Sci. 15, 291-294
51. Pearson, J. T., Hill, J. J., Swank, J., Isoherranen, N., Kunze, K. L., and Atkins, W. M. (2006) Surface plasmon resonance analysis of antifungal azoles binding to CYP3A4 with kinetic resolution of multiple binding orientations. Biochemistry 45, 6341-6353
52. Lebedev, K., Mafé, S., and Stroeve, P. (2006) Convection, diffusion and reaction in a surface-based biosensor: modeling of cooperativity and binding site competition on the surface and in the hydrogel. J. Colloid Interface Sci. 296, 527-537
53. Tao, Y., Carta, G., Ferreira, G., and Robbins, D. (2011) Adsorption of deamidated antibody variants on macroporous and dextran-grafted cation exchangers: II. adsorption kinetics. J. Chromatogr. A 1218, 1530-1537
54. Rabe, M., Verdes, D., and Seeger, S. (2011) Understanding protein adsorption phenomena at solid surfaces. Adv. Colloid Interface Sci. 162, 87-106
55. Gama, C. I., and Hsieh-Wilson, L. C. (2005) Chemical approaches to deciphering the glycosaminoglycan code. Curr. Opin. Chem. Biol. 9, 609-619
56. Raman, R., Sasisekharan, V., and Sasisekharan, R. (2005) Structural insights into biological roles of protein-glycosaminoglycan interactions. Chem. Biol. 12, 267-277