Human antibodies to herpes simplex virus type 1 glycoprotein C are neutralizing and target the heparan sulfate-binding domain

Virology

Volumn 400, Issue 2, 2010, Pages 197-206

  Adamiak, Beata ^a,b   Trybala, Edward ^a   Mardberg, Kristina ^a   Johansson, Maria ^a   Liljeqvist, Jan Ake ^a   Olofsson, Sigvard ^a   Grabowska, Agnieszka ^b   Bienkowska Szewczyk, Krystyna ^b   Szewczyk, Boguslaw ^b   Bergstrom, Tomas ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF GDA SK   (Poland)

Author keywords

Anti gC antibody; Glycoprotein gC; Glycosaminoglycans; Herpes simplex virus type 1; Virus neutralizing activity

Indexed keywords

CHONDROITIN SULFATE; HEPARAN SULFATE; HEPARIN LYASE; NEUTRALIZING ANTIBODY; PROTEIN C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN BINDING; ARTICLE; CELL SURFACE; CONTROLLED STUDY; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; KERATINOCYTE; L CELL; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SURVIVAL TIME; VIRUS ATTACHMENT; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; DISEASE MODELS, ANIMAL; EPITOPES; HEPARITIN SULFATE; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; HUMANS; KERATINOCYTES; MICE; NEUTRALIZATION TESTS; SURVIVAL ANALYSIS; VIRAL ENVELOPE PROTEINS; VIRUS ATTACHMENT;

HUMAN HERPESVIRUS 1; MURINAE; MUS; SIMIAE;

EID: 77949568869     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.01.032     Document Type: Article

References (43)

1. Arvin A.M., Koropchak C.M., Yeager A.S., Pereira L. Detection of type-specific antibody to herpes simplex virus type 1 by radioimmunoassay with herpes simplex virus type 1 glycoprotein C purified with monoclonal antibody. Infect. Immun. 1983, 40:184-189.
2. Babic N., Rodger G., Arthur J., Minson A.C. A study of primary neuronal infection by mutants of herpes simplex virus type 1 lacking dispensable and non-dispensable glycoproteins. J. Gen. Virol. 1999, 80:2403-2409.
3. Banfield B.W., Leduc Y., Esford L., Schubert K., Tufaro F. Sequential isolation of proteoglycan synthesis mutants by using herpes simplex virus as a selective agent: evidence for a proteoglycan-independent virus entry pathway. J. Virol. 1995, 69:3290-3298.
4. Bergefall K., Trybala E., Johansson M., Uyama T., Naito S., Yamada S., Kitagawa H., Sugahara K., Bergstrom T. Chondroitin sulfate characterized by the E disaccharide unit is a potent inhibitor of herpes simplex virus infectivity and provides the virus binding sites on gro2c cells. J. Biol. Chem. 2005, 280:32193-32199.
5. Bergstrom T., Alestig K., Svennerholm B., Horal P., Vahlne A. Neurovirulence of herpes simplex virus types 1 and 2 isolates in diseases of the central nervous system. Eur. J. Clin. Microbiol. Infect. Dis. 1990, 9:751-757.
6. Bergstrom T., Sjogren-Jansson E., Jeansson S., Lycke E. Mapping neuroinvasiveness of the herpes simplex virus type 1 encephalitis-inducing strain 2762 by the use of monoclonal antibodies. Mol. Cell. Probes 1992, 6:41-49.
7. Boukamp P., Petrussevska R.T., Breitkreutz D., Hornung J., Markham A., Fusenig N.E. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 1988, 106:761-771.
8. Brown C.T., Nugent M.A., Lau F.W., Trinkaus-Randal V. Characterization of proteoglycans synthesized by cultured corneal fibroblasts in response to transforming growth factor beta and fetal calf serum. J. Biol. Chem. 1999, 274:7111-7119.
9. Corey L., Langenberg A.G., Ashley R., Sekulovich R.E., Izu A.E., Douglas J.M., Handsfield H.H., Warren T., Marr L., Tyring S., DiCarlo R., Adimora A.A., Leone P., Dekker C.L., Burke R.L., Leong W.P., Straus S.E. Recombinant glycoprotein vaccine for the prevention of genital HSV-2 infection: two randomized controlled trials. JAMA 1999, 282:331-340. Chiron HSV Vaccine Study Group.
10. Duff R., Rapp F. Oncogenic transformation of hamster cells after exposure to herpes simplex virus type 2. Nat. New Biol. 1971, 233:48-50.
11. Frank R. Spot-synthesis: an easy technique for the positionally addressable, parallel chemical synthesis on a membrane support. Tetrahedron 1992, 48:9217-9232.
12. Glorioso J., Kees U., Kumel G., Kirchner H., Krammer P.H. Identification of herpes simplex virus type 1 (HSV-1) glycoprotein gC as the immunodominant antigen for HSV-1-specific memory cytotoxic T lymphocytes. J. Immunol. 1985, 135:575-582.
13. Griffiths A., Renfrey S., Minson T. Glycoprotein C-deficient mutants of two strains of herpes simplex virus type 1 exhibit unaltered adsorption characteristics on polarized or non-polarized cells. J. Gen. Virol. 1998, 79:807-812.
14. Gruenheid S., Gatzke L., Meadows H., Tufaro F. Herpes simplex virus infection and propagation in a mouse L cell mutant lacking heparan sulfate proteoglycans. J. Virol. 1993, 67:93-100.
15. Gupta P.K., Saini M., Gupta L.K., Rao V.D., Bandyopadhyay S.K., Butchaiah G., Garg G.K., Garg S.K. Induction of immune responses in cattle with a DNA vaccine encoding glycoprotein C of bovine herpesvirus-1. Vet. Microbiol. 2001, 78:293-305.
16. Herold B.C., WuDunn D., Soltys N., Spear P.G. Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectivity. J. Virol. 1991, 65:1090-1098.
17. Herold B.C., WuDunn D., Visalli R.J., Sumarski N., Brandt C., Spear P.G. Glycoprotein C-independent binding of herpes simplex virus to cells requires cell surface heparan sulfate and glycoprotein B. J. Gen. Virol. 1994, 75:1211-1222.
18. Holland T.C., Marlin S.D., Levine M., Glorioso J. Antigenic variants of herpes simplex virus selected with glycoprotein-specific monoclonal antibodies. J. Virol. 1983, 45:672-682.
19. Holland T.C., Homa F.L., Marlin S.D., Levine M., Glorioso J. Herpes simplex virus type 1 glycoprotein C-negative mutants exhibit multiple phenotypes, including secretion of truncated glycoproteins. J. Virol. 1984, 52:566-574.
20. Karger A., Mettenleiter T.C. Glycoproteins gIII and gp50 play dominant roles in the biphasic attachment of pseudorabies virus. Virology 1993, 194:654-664.
21. Karger A., Saalmuller A., Tufaro F., Banfield B.W., Mettenleiter T.C. Cell surface proteoglycans are not essential for infection by pseudorabies virus. J. Virol. 1995, 69:3482-3489.
22. Korir A.K., Larive C.K. Advances in the separation, sensitive detection, and characterization of heparin and heparan sulfate. Anal. Bioanal. Chem. 2009, 393:155-169.
23. Kramer A., Schuster A., Reineke U., Malin R., Volkmer-Engert R., Landgraf C., Schneider-Mergener J. Combinatorial cellulose-bound peptide libraries: screening tools for the identification of peptides that bind ligands with predefined specificity. Methods (A Comp. Meth Enzymol.) 1994, 6:388-395.
24. Liljeqvist J.-A., Trybala E., Svennerholm B., Jeansson S., Sjogren-Jansson E., Bergstrom T. Localization of type-specific epitopes of herpes simplex virus type 2 glycoprotein G by human and mouse antibodies. J. Gen. Virol. 1998, 79:1215-1224.
25. Liljeqvist J.-A., Svennerholm B., Bergstrom T. Typing of clinical herpes simplex virus type 1 and type 2 isolates with monoclonal antibodies. J. Clin. Microbiol. 1999, 37:2717-2718.
26. Mardberg K., Trybala E., Glorioso J.C., Bergstrom T. Mutational analysis of the major heparan sulfate-binding domain of herpes simplex virus type 1 glycoprotein C. J. Gen. Virol. 2001, 82:1941-1950.
27. Mardberg K., Trybala E., Tufaro F., Bergstrom T. Herpes simplex virus type 1 glycoprotein C is necessary for efficient infection of chondroitin sulfate-expressing gro2C cells. J. Gen. Virol. 2002, 83:291-300.
28. McCormick C., Leduc L., Martindale D., Mattison K., Esford L.E., Dyer A.P., Tufaro F. The putative tumour suppressor EXT1 alters the expression of cell-surface heparan sulfate. Nat. Genet. 1998, 19:158-161.
29. Moffat J.F., Zerboni L., Kinchington P.R., Grose C., Kaneshima H., Arvin A.M. Attenuation of the vaccine Oka strain of varicella-zoster virus and role of glycoprotein C in alphaherpesvirus virulence demonstrated in the SCID-hu mouse. J. Virol. 1998, 72:965-974.
30. Morano S., Guidobaldi L., Cipriani R., Gabriele A., Pantellini F., Medici F., D'Erme M., Di Mario U. High glucose modifies heparan sulphate synthesis by mouse glomerular epithelial cells. Diabetes Metab. Res. Rev. 1999, 15:13-20.
31. Ober B.T., Teufel B., Wiesmuller K.H., Jung G., Pfaff E., Saalmuller A., Rziha H.J. The porcine humoral immune response against pseudorabies virus specifically targets attachment sites on glycoprotein gC. J. Virol. 2000, 74:1752-1760.
32. Olofsson S., Bolmstedt A., Biller M., Mardberg K., Leckner J., Malmstrom B.G., Trybala E., Bergstrom T. The role of a single N-linked glycosylation site for a functional epitope of herpes simplex virus type 1 envelope glycoprotein C. Glycobiology 1999, 9:73-81.
33. Ross C., Glorioso J., Sacks S., Lavery C., Rawls W.E. Competitive inhibition by human sera of mouse monoclonal antibody binding to glycoproteins C and D of herpes simplex virus types 1 and 2. J. Virol. 1985, 54:851-855.
34. Sjoblom I., Sjogren-Jansson E., Glorioso J.C., Olofsson S. Antigenic structure of the herpes simplex virus type 1 glycoprotein C: demonstration of a linear epitope, situated in an environment of highly conformation-dependent epitopes. Apmis 1992, 100:229-236.
35. Spear P.G. Herpes simplex virus: receptors and ligands for cell entry. Cell. Microbiol. 2004, 6:401-410.
36. Svennerholm B., Jeansson S., Vahlne A., Lycke E. Involvement of glycoprotein C (gC) in adsorption of herpes simplex virus type 1 (HSV-1) to the cell. Arch. Virol. 1991, 120:273-279.
37. Tal-Singer R., Peng C., Ponce De Leon M., Abrams W.R., Banfield B.W., Tufaro F., Cohen G.H., Eisenberg R.J. Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. J. Virol. 1995, 69:4471-4483.
38. Trybala E., Bergstrom T., Svennerholm B., Jeansson S., Glorioso J.C., Olofsson S. Localization of a functional site of herpes simplex virus type 1 glycoprotein C involved in binding to cell surface heparan sulphate. J. Gen. Virol. 1994, 75:743-752.
39. Trybala E., Liljeqvist J.-Å., Svennerholm B., Bergstrom T. Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. J. Virol. 2000, 74:9106-9114.
40. Trybala E., Roth A., Johansson M., Liljeqvist J.-Å., Rekabdar E., Larm O., Bergstrom T. Glycosaminoglycan-binding ability is a feature of wild-type strains of herpes simplex virus type 1. Virology 2002, 302:413-419.
41. Wu C.-T.B., Levine M., Homa F., Highlander S.L., Glorioso J.C. Characterization of the antigenic structure of herpes simplex virus type 1 glycoprotein C through DNA sequence analysis of monoclonal antibody resistant mutants. J. Virol. 1990, 64:856-863.
42. WuDunn D., Spear P.G. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J. Virol. 1989, 63:52-58.
43. Yamasaki R.B., Vega A., Feeney R.E. Modification of available arginine residues in proteins by p-hydroxyphenylglyoxal. Anal. Biochem. 1980, 109:32-40.