Human antibody titers to Epstein-Barr Virus (EBV) gp350 correlate with neutralization of infectivity better than antibody titers to EBV gp42 using a rapid flow cytometry-based EBV neutralization assay

Virology

Volumn 391, Issue 2, 2009, Pages 249-256

  Sashihara, Junji ^a   Burbelo, Peter D ^b   Savoldo, Barbara ^c   Pierson, Theodore C ^a   Cohen, Jeffrey I ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c HOUSTON METHODIST HOSPITAL   (United States)

Author keywords

Antibody mediated neutralization; Epstein Barr virus; Glycoprotein 350; Glycoprotein 42; Herpesvirus; Transformation

Indexed keywords

GLYCOPROTEIN GP 350; GLYCOPROTEIN GP 42; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; EPSTEIN BARR VIRUS; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS CELL TRANSFORMATION; VIRUS IMMUNITY; VIRUS NEUTRALIZATION; VIRUS VIRULENCE;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; B-LYMPHOCYTES; CELL LINE; FLOW CYTOMETRY; GLYCOPROTEINS; HERPESVIRUS 4, HUMAN; HUMANS; MEMBRANE GLYCOPROTEINS; NEUTRALIZATION TESTS; VIRAL MATRIX PROTEINS; VIRAL PROTEINS;

HERPESVIRIDAE; HUMAN HERPESVIRUS 4;

EID: 68549139880     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.06.013     Document Type: Article

References (49)

1. Andrewes C.H., and Elford W.J. Observations on anti-phage sera. I: The percentage law. Br. J. Exp. Pathol. 14 (1933) 367-376
2. Beisel C., Tanner J., Matsuo T., Thorley-Lawson D., Kezdy F., and Kieff E. Two major outer envelope glycoproteins of Epstein-Barr virus are encoded by the same gene. J. Virol. 54 (1985) 665-674
3. Biacchesi S., Skiadopoulos M.H., Yang L., Murphy B.R., Collins P.L., and Buchholz U.J. Rapid human metapneumovirus microneutralization assay based on green fluorescent protein expression. J. Virol. Methods 128 (2005) 192-197
4. Bilello J.P., Morgan J.S., Damania B., Lang S.M., and Desrosiers R.C. A genetic system for rhesus monkey rhadinovirus: use of recombinant virus to quantitate antibody-mediated neutralization. J. Virol. 80 (2006) 1549-1562
5. Borza C.M., and Hutt-Fletcher L.M. Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat. Med. 8 (2002) 594-599
6. Brioen P., and Boeye A. Poliovirus neutralization and the percentage law. Brief report. Arch. Virol. 83 (1985) 105-111
7. Burbelo P.D., Goldman R., and Mattson T.L. A simplified immunoprecipitation method for quantitatively measuring antibody responses in clinical sera samples by using mammalian-produced Renilla luciferase-antigen fusion proteins. BMC Biotechnol. 5 (2005) 22
8. Burbelo P.D., Hoshino Y., Leahy H., Krogmann T., Hornung R.L., Iadarola M.J., and Cohen J.I. Serological diagnosis of human HSV-1 and HSV-2 infection by luciferase immunoprecipitation systems (LIPS) assay. Clin. Vaccine Immunol. 16 (2009) 366-371
9. Cohen J.I. Epstein-Barr virus infection. N. Engl. J. Med. 343 (2000) 481-492
10. Delecluse H.J., Hilsendegen T., Pich D., Zeidler R., and Hammerschmidt W. Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 8245-8250
11. Earl P.L., Americo J.L., and Moss B. Development and use of a vaccinia virus neutralization assay based on flow cytometric detection of green fluorescent protein. J. Virol. 77 (2003) 10684-10688
12. Epstein M.A., Morgan A.J., Finerty S., Randle B.J., and Kirkwood J.K. Protection of cottontop tamarins against Epstein-Barr virus-induced malignant lymphoma by a prototype subunit vaccine. Nature 318 (1985) 287-289
13. Finerty S., Tarlton J., Mackett M., Conway M., Arrand J.R., Watkins P.E., and Morgan A.J. Protective immunization against Epstein-Barr virus-induced disease in cottontop tamarins using the virus envelope glycoprotein gp340 produced from a bovine papillomavirus expression vector. J. Gen. Virol. 73 (1992) 449-453
14. Finerty S., Mackett M., Arrand J.R., Watkins P.E., Tarlton J., and Morgan A.J. Immunization of cottontop tamarins and rabbits with a candidate vaccine against the Epstein-Barr virus based on the major viral envelope glycoprotein gp340 and alum. Vaccine 12 (1994) 1180-1184
15. Fingeroth J.D., Weis J.J., Tedder T.F., Strominger J.L., Biro P.A., and Fearon D.T. Epstein-Barr virus receptor of human B lymphocytes is the C3d receptor CR2. Proc. Natl. Acad. Sci. U. S. A. 81 (1984) 4510-4514
16. Frade R., Barel M., Ehlin-Henriksson B., and Klein G. gp140, the C3d receptor of human B lymphocytes, is also the Epstein-Barr virus receptor. Proc. Natl. Acad. Sci. U. S. A. 82 (1985) 1490-1493
17. Gu S.Y., Huang T.M., Ruan L., Miao Y.H., Lu H., Chu C.M., Motz M., and Wolf H. First EBV vaccine trial in humans using recombinant vaccinia virus expressing the major membrane antigen. Dev. Biol. Stand. 84 (1995) 171-177
18. Henderson E., Miller G., Robinson J., and Heston L. Efficiency of transformation of lymphocytes by Epstein-Barr virus. Virology 76 (1977) 152-163
19. Hoffman G.J., Lazarowitz S.G., and Hayward S.D. Monoclonal antibody against a 250,000-dalton glycoprotein of Epstein-Barr virus identifies a membrane antigen and a neutralizing antigen. Proc. Natl. Acad. Sci. U. S. A. 77 (1980) 2979-2983
20. Hoshino Y., Qin J., Follmann D., Cohen J.I., and Straus S.E. The number of herpes simplex virus-infected neurons and the number of viral genome copies per neuron correlate with the latent viral load in ganglia. Virology 372 (2008) 56-63
21. Jackman W.T., Mann K.A., Hoffmann H.J., and Spaete R.R. Expression of Epstein-Barr virus gp350 as a single chain glycoprotein for an EBV subunit vaccine. Vaccine 17 (1999) 660-668
22. Jiang R., Scott R.S., and Hutt-Fletcher L.M. Epstein-Barr virus shed in saliva is high in B-cell-tropic glycoprotein gp42. J. Virol. 80 (2006) 7281-7283
23. Johannsen E., Luftig M., Chase M.R., Weicksel S., Cahir-McFarland E., Illanes D., Sarracino D., and Kieff E. Proteins of purified Epstein-Barr virus. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 16286-16291
24. Khawplod P., Inoue K., Shoji Y., Wilde H., Ubol S., Nishizono A., Kurane I., and Morimoto K. A novel rapid fluorescent focus inhibition test for rabies virus using a recombinant rabies virus visualizing a green fluorescent protein. J. Virol. Methods 125 (2005) 35-40
25. Kirschner A.N., Lowrey A.S., Longnecker R., and Jardetzky T.S. Binding-site interactions between Epstein-Barr virus fusion proteins gp42 and gH/gL reveal a peptide that inhibits both epithelial and B-cell membrane fusion. J. Virol. 81 (2007) 9216-9229
26. Li Q., Turk S.M., and Hutt-Fletcher L.M. The Epstein-Barr virus (EBV) BZLF2 gene product associates with the gH and gL homologs of EBV and carries an epitope critical to infection of B cells but not of epithelial cells. J. Virol. 69 (1995) 3987-3994
27. Li Q., Spriggs M.K., Kovats S., Turk S.M., Comeau M.R., Nepom B., and Hutt-Fletcher L.M. Epstein-Barr virus uses HLA class II as a cofactor for infection of B lymphocytes. J. Virol. 71 (1997) 4657-4662
28. Miller N., and Hutt-Fletcher L.M. A monoclonal antibody to glycoprotein gp85 inhibits fusion but not attachment of Epstein-Barr virus. J. Virol. 62 (1988) 2366-2372
29. Miller G., Niederman J.C., and Stitt D.A. Infectious mononucleosis: appearance of neutralizing antibody to Epstein-Barr virus measured by inhibition of formation of lymphoblastoid cell lines. J. Infect. Dis. 125 (1972) 403-406
30. Miller G., Heston L., and Hoffman G. Neutralization of lymphocyte immortalization by different strains of Epstein-Barr virus with a murine monoclonal antibody. Infect. Immun. 37 (1982) 1028-1031
31. Morgan A.J., Finerty S., Lovgren K., Scullion F.T., and Morein B. Prevention of Epstein-Barr (EB) virus-induced lymphoma in cottontop tamarins by vaccination with the EB virus envelope glycoprotein gp340 incorporated into immune-stimulating complexes. J. Gen. Virol. 69 (1988) 2093-2096
32. Morgan A.J., Mackett M., Finerty S., Arrand J.R., Scullion F.T., and Epstein M.A. Recombinant vaccinia virus expressing Epstein-Barr virus glycoprotein gp340 protects cottontop tamarins against EB virus-induced malignant lymphomas. J. Med. Virol. 25 (1988) 189-195
33. Moss D.J., and Pope J.H. Assay of the infectivity of Epstein-Barr virus by transformation of human leucocytes in vitro. J. Gen. Virol. 17 (1972) 233-236
34. Moutschen M., Leonard P., Sokal E.M., Smets F., Haumont M., Mazzu P., Bollen A., Denamur F., Peeters P., Dubin G., and Denis M. Phase I/II studies to evaluate safety and immunogenicity of a recombinant gp350 Epstein-Barr virus vaccine in healthy adults. Vaccine 25 (2007) 4697-4705
35. Nemerow G.R., Wolfert R., McNaughton M.E., and Cooper N.R. Identification and characterization of the Epstein-Barr virus receptor on human B lymphocytes and its relationship to the C3d complement receptor (CR2). J. Virol. 55 (1985) 347-351
36. Neuhierl B., Feederle R., Hammerschmidt W., and Delecluse H.J. Glycoprotein gp110 of Epstein-Barr virus determines viral tropism and efficiency of infection. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 15036-15041
37. Pearson G., Dewey F., Klein G., Henle G., and Henle W. Relation between neutralization of Epstein-Barr virus and antibodies to cell-membrane antigens-induced by the virus. J. Natl. Cancer Inst. 45 (1970) 989-995
38. Pierson T.C., Sanchez M.D., Puffer B.A., Ahmed A.A., Geiss B.J., Valentine L.E., Altamura L.A., Diamond M.S., and Doms R.W. A rapid and quantitative assay for measuring antibody-mediated neutralization of West Nile virus infection. Virology 346 (2006) 53-65
39. Ragot T., Finerty S., Watkins P.E., Perricaudet M., and Morgan A.J. Replication-defective recombinant adenovirus expressing the Epstein-Barr virus (EBV) envelope glycoprotein gp340/220 induces protective immunity against EBV-induced lymphomas in the cottontop tamarin. J. Gen. Virol. 74 (1993) 501-507
40. Randle B.J., and Epstein M.A. A highly sensitive enzyme linked immunosorbent assay to quantitate antibodies to Epstein-Barr membrane antigen gp340. J. Virol. Methods 9 (1984) 201-208
41. Reed L., and Muench H. A simple method of estimating 50 percent end points. Am. J. Hyg. 27 (1938) 493-497
42. Ressing M.E., van Leeuwen D., Verreck F.A., Keating S., Gomez R., Franken K.L., Ottenhoff T.H., Spriggs M., Schumacher T.N., Hutt-Fletcher L.M., Rowe M., and Wiertz E.J. Epstein-Barr virus gp42 is posttranslationally modified to produce soluble gp42 that mediates HLA class II immune evasion. J. Virol. 79 (2005) 841-852
43. Rocchi G., and Hewetson J.F. A practical and quantitative microtest for determination of neutralizing antibodies against Epstein-Barr virus. J. Gen. Virol. 18 (1973) 385-391
44. Sokal E.M., Hoppenbrouwers K., Vandermeulen C., Moutschen M., Leonard P., Moreels A., Haumont M., Bollen A., Smets F., and Denis M. Recombinant gp350 vaccine for infectious mononucleosis: a phase 2, randomized, double-blind, placebo-controlled trial to evaluate the safety, immunogenicity, and efficacy of an Epstein-Barr virus vaccine in healthy young adults. J. Infect. Dis. 196 (2007) 1749-1753
45. Sugden B., and Mark W. Clonal transformation of adult human leukocytes by Epstein-Barr virus. J. Virol. 23 (1977) 503-508
46. Tanner J., Weis J., Fearon D., Whang Y., and Kieff E. Epstein-Barr virus gp350/220 binding to the B lymphocyte C3d receptor mediates adsorption, capping, and endocytosis. Cell 50 (1987) 203-213
47. Wang X., and Hutt-Fletcher L.M. Epstein-Barr virus lacking glycoprotein gp42 can bind to B cells but is not able to infect. J. Virol. 72 (1998) 158-163
48. Wilson A.D., and Morgan A.J. Indirect measurement of Epstein-Barr virus neutralising antibodies by ELISA. J. Virol. Methods 73 (1998) 11-19
49. Zhang P.F., and Marcus-Sekura C.J. Conformation-dependent recognition of baculovirus-expressed Epstein-Barr virus gp350 by a panel of monoclonal antibodies. J. Gen. Virol. 74 (1993) 2171-2179