Immunogenic and antigenic dominance of a nonneutralizing epitope over a highly conserved neutralizing epitope in the gp41 envelope glycoprotein of human immunodeficiency virus type 1: Its deletion leads to a strong neutralizing response

Virology

Volumn 266, Issue 1, 2000, Pages 66-78

  Cleveland, S Matthew ^a   Buratti, Emanuele ^b   Jones, Tim D ^c   North, Philip ^c   Baralle, Francisco ^b   McLain, Lesley ^a   McInerney, Tracey ^a   Durrani, Zarmina ^a   Dimmock, Nigel J ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^c Axis Genetics plc   (United Kingdom)

Author keywords

HIV 1; Immunodominance; Immunogenicity; Neutralizing antibody; Plant virus chimera; Vaccine

Indexed keywords

EPITOPE; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; T LYMPHOCYTE ANTIGEN; VIRUS ANTIBODY; VIRUS GLYCOPROTEIN; VIRUS VACCINE;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANTIGENICITY; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNIZATION; IMMUNOGENICITY; MOUSE; NONHUMAN; PLANT VIRUS; PRIORITY JOURNAL; RABBIT; T LYMPHOCYTE; VIRUS NEUTRALIZATION;

ANIMALIA; COWPEA MOSAIC VIRUS; HIV 1; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MURINAE; ORYCTOLAGUS CUNICULUS; RNA VIRUSES;

EID: 0034606661     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1999.0041     Document Type: Article

References (56)

1. Abacioglu Y. H., Fouts T. R., Laman J. D., Classen E., Pincus S. H., Moore J. P., Roby C. A., Kamin-Lewis R., Lewis G. K. Epitope mapping and topology of baculovirus-expressed HIV-1 gp160 determined with a panel of murine monoclonal antibodies. AIDS Res. Hum. Retroviruses. 10:1994;371-381.
2. Amit A., Mariuzza R. A., Phillips S. E. V., Poljak R. J. Three-dimensional structure of an antigen-antibody complex at 2.8Å resolution. Science. 233:1986;747-753.
3. Bachmann M. F., Zinkernagel R. M. The influenza of virus structure on antibody responses and virus serotype formation. Immunol. Today. 17:1996;553-558.
4. Bachmann M. F., Zinkernagel R. M. Neutralizing antiviral B cell responses. Annu. Rev. Immunol. 15:1997;235-270.
5. Benjamin D. C., Berzofsky J. A., East I. J., Gurd F. R. N., Hannum C., Leach S. J., Margoliash E., Michael J. G., Miller A., Prager E. M., Reichlim M., Sercarz E. E., Smith-Gill S. J., Todd P. E., Wilson A. C. The antigenic structure of proteins: A reappraisal. Annu. Rev. Immunol. 2:1984;67-101.
6. Berzofsky J. A., Richman L. K., Killion D. J. Distinct H-2-linked Ir genes control both antibody and T cell responses to different determinants on the same antigen, myoglobin. Proc. Natl. Acad. Sci. USA. 76:1979;4046-4050.
7. Bretscher P., Cohn M. A theory of self-nonself discrimination. Science. 169:1970;1042-1049.
8. Broliden P.-A., von Gegerfelt A., Clapham P., Rosen J., Fenyö E.-M., Wahren B., Broliden K. Identification of human neutralization-inducing regions of the human immunodeficiency virus type 1 envelope glycoproteins. Proc. Natl. Acad. Sci. USA. 89:1992;461-465.
9. Brusic V., Rudy G., Harrison L. MHCPEP: A database of MHC-binding peptides. Nucleic Acids Res. 22:1994;3663-3665.
10. Buratti E., Tisminetzky S. G., Scodeller E. S., Baralle F. E. Conformational display of two neutralizing epitopes of HIV-1 gp41 in the Flock House virus capsid protein. J. Immunol. Methods. 197:1996;7-18.
11. Buratti E., McLain L., Tisminetzky S. G., Cleveland S. M., Dimmock N. J., Baralle F. E. The neutralizing antibody response against a conserved region of HIV-1 gp41 (amino acid residues 731-752) is uniquely directed against a conformational epitope. J. Gen. Virol. 79:1998;2709-2716.
12. Burton D. R. A vaccine for HIV type 1: The antibody perspective. Proc. Natl. Acad. Sci. USA. 94:1997;10018-10023.
13. Chanh T. C., Dreesman G., Kanda P., Linette G. P., Sparrow J. T., Ho D. D., Kennedy R. C. Induction of anti-HIV neutralizing antibodies by synthetic peptides. EMBO J. 5:1986;3065-3071.
14. Chanh T. C., Kennedy R. C., Kanda P. Synthetic peptides homologous to HIV transmembrane glycoprotein suppress normal human lymphocyte blastogenic response. Cell. Immunol. 111:1988;77-88.
15. Dalgleish A. G., Chanh T. C., Kennedy R. C., Kanda P., Clapham P. R., Weiss R. A. Neutralization of diverse strains of HIV-1 by monoclonal antibodies raised against a gp41 synthetic peptide. Virology. 165:1988;209-215.
16. Dalsgaard K., Uttethal Å., Jones T. D., Xu F., Merryweather A., Hamilton W. D. O., Langeveld J. P. M., Boshuizen R. S., Kamstrup S., Lomonossoff G. P., Porta C., Vela C., Casal J. I., Meloen R. H., Rodgers P. B. Plant-derived vaccine protects target animals against a viral disease. Nature Biotechnol. 15:1997;248-252.
17. Davis D., Chaudri B., Stephens D. M., Carne C. A., Willers C., Lachmann P. J. The immunodominance of epitopes within the transmembrane protein (gp41) of human immunodeficiency virus type 1 may be related by the host's previous exposure to similar epitopes on unrelated antigens. J. Gen. Virol. 71:1990;1975-1983.
18. Durrani Z., McInerney T. L., McLain L., Jones T., Bellaby T., Brennan F. R., Dimmock N. J. Intranasal immunization with a plant virus expressing a peptide from HIV-1 gp41 stimulates better mucosal and systemic HIV-1-specific IgA and IgG than oral immunization. J. Immunol. Methods. 220:1998;93-103.
19. Evans D. J., McKeating J. A., Meredith J. M., Burke K. L., Katrak K., Ferguson M., Minor P. D., Weiss R. A., Almond J. W. An engineered poliovirus chimaera elicits broadly reactive HIV-1 neutralizing antibodies. Nature (London). 339:1989;385-388.
20. Fitzgerald D. J., Bronson E. C., Anderson J. N. Compositional similarities between the human immunodeficiency virus and surface antigens of pathogens. AIDS Res. Hum. Retroviruses. 12:1996;99-106.
21. Gajewski T. F., Joyce J., Fitch F. W. Antiproliferative effect of interferon-gamma in immune regulation. J. Immunol. 143:1989;15-22.
22. Gallagher W. R., Henderson L. A., Fermin C., Montelaro R. C., Martin A., Qureshi N., Ball J. M., Sattentau Q., Luo-Zhang H., Garry R. F. Membrane interactions of human immunodeficiency virus: Attachment, fusion, and cytopathology. Membrane Interactions of HIV. 1992;Wiley-Liss, New York. p. 113-142.
23. Garrity R. R., Rimmelzwaan G., Minassian A., Tsai W.-P., Lin G., Conley S., Dunlop N., DeJong J., Keulen W., Moore J., Goudsmit J., Nara P. Site-directed mutations introduced into the V3 domain of HIV-1 gp120 results in an augmented humoral response to other epitopes. Vaccine 93. 1994;Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
24. Garrity R. R., Rimmelzwaan G., Minassian A., Tsai W.-P., Lin G., de Jong J.-J., Goudsmit J., Nara P. L. Refocussing neutralizing antibody response by targeted dampening of an immunodominant epitope. J. Immunol. 159:1997;279-289.
25. Gnann J. W., Nelson J. A., Oldstone M. B. A. Fine mapping of an immunodominant domain in the transmembrame glycoprotein of human immunodeficency virus. J. Virol. 61:1987;2639-2641.
26. Goudsmit J., Meloen R. H., Brasseur R. Map of sequential B cell epitopes of the HIV-1 transmembrane protein using human antibodies as probe. Intervirology. 31:1990;327-338.
27. Jackson D. C., Poumbourios P., White D. O. Simultaneous binding of two monoclonal antibodies to epitopes separated in sequence by only three amino acid residues. Mol. Immunol. 25:1988;465-471.
28. Ju S.-T., Nonogaki T., Bernatowicz M. S., Matsueda G. R. The B cell immune response to an idiotype-inducing peptide epitope can be inhibited by immunodominance of a neighboring epitope. J. Immunol. 150:1993;2641-2647.
29. Kalyan N. K., Lee S.-G., Wilhelm J., Pisano M. R., Hum W.-T., Hsiao C.-L., Davis A. R., Eichberg J. W., Robert-Guroff M., Hung P. P. Immunogenicity of recombinant influenza virus haemagglutinin carrying peptides from the envelope protein of human immunodeficiency virus type 1. Vaccine. 12:1994;753-760.
30. Karpatkin S., Nardi M., Lennette E. T., Byrne B., Poiesz B. Anti-human immunodeficiency virus type 1 antibody complexes on platelets of seropositive thrombocytopenic homosexuals and narcotic addicts. Proc. Natl. Acad. Sci. USA. 85:1988;9673-9767.
31. Kennedy R. C., Henkel R. D., Pauletti D., Allan J. S., Lee T. H., Essex M., Dreesman G. R. Antiserum to a synthetic peptide recognizes the HTLV-III envelope glycoprotein. Science. 231:1986;1556-1559.
32. Krause R. M., Dimmock N. J., Morens D. M. Summary of antibody workshop: the role of humoral immunity in the treatment and prevention of emerging and extant infectious diseases. J. Infect. Dis. 176:1997;549-559.
33. Kumar A., Kumar V., Shukla G., Rao K. V. S. Immunological characteristics of a recombinant hepatitis B virus-derived multiple epitope polypeptide: A study on polyvalent vaccine design. Vaccine. 12:1994;259-266.
34. Kunkl A., Fenoglio F., Manca F., Pira G. L., Cambiaggi C., Strom R., Celada F. Kinetic immunodominance: Functionally competing antibodies against exposed and cryptic epitopes of Escherichia coli β-galactosidase are produced in time sequence. Int. Immunol. 4:1992;627-636.
35. Manca F., Fenoglio F., Kunkl A., Cambiaggi C., Pira G. L., Celada F. B cells on the podium: regulatory roles of surface and secreted immunoglobulins. Immunol. Today. 9:1988;300-303.
36. Mathiesen T., Chiodi F., Broliden P.-A., Albert J., Houghten R. A., Utter G., Wahren B., Norrby E. Analysis of a subclass-restricted HIV-1 gp41 epitope by omission peptides. Immunol. 67:1989;1-7.
37. McInerney T. L., Brennan F. R., Jones T. D., Dimmock N. J. Analysis of the ability of five adjuvants to enhance immune responses to a chimeric plant virus displaying a HIV-1 peptide. Vaccine. 17:1999;1359-1368.
38. McLain L., Dimmock N. J. Single- and multi-hit kinetics of immunoglobulin G neutralization of human immunodeficiency virus type 1 by monoclonal antibodies. J. Gen. Virol. 75:1994;1457-1460.
39. McLain L., Porta C., Lomonossoff G. P., Durrani Z., Dimmock N. J. Human immunodeficiency virus type 1 neutralizing antibodies raised to a gp41 peptide expressed on the surface of a plant virus. AIDS Res. Hum. Retroviruses. 11:1995;327-334.
40. McLain L., Durrani Z., Wisniewski L. A., Porta C., Lomonossoff G. P., Dimmock N. J. A plant virus-HIV-1 chimera stimulates antibody that neutralizes HIV-1. Brown F., Burton D. R., Collier J., Mekalonos J., Norrby E. Vaccine 96. 1996a;311-316 Cold Spring Harbor Laboratory Press, Cold Spring Harbor Laboratory.
41. McLain L., Durrani Z., Wisniewski L. A., Porta C., Lomonossoff G. P., Dimmock N. J. Stimulation of neutralizing antibodies to human immunodeficiency virus type 1 in three strains of mice immunized with a 22-mer amino acid peptide expressed on the surface of a plant virus. Vaccine. 14:1996b;799-810.
42. Modrow S., Hahn B. H., Shaw G. M., Gallo R. C., Wong-Staal F., Wolf H. Computer assisted analysis of envelope protein sequences of seven human immunodeficiency virus isolates: Prediction of antigenic epitopes in conserved and variable regions. J. Virol. 61:1987;570-578.
43. Muster T., Steindl F., Purtscher M., Trkola A., Klima A., Himmler G., Rüker F., Katinger H. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J. Virol. 67:1993;6642-6647.
44. Myers G., Korber B., Wain-Hobson S., Smith R. F., Pavlakis G. N. Human Retroviruses and AIDS, 1995: A Compilation and Analysis of Nucleic Acid and Amino Acid Sequences. 1993;Los Alamos National Laboratory, Los Alamos.
45. Nayak B. P., Tuteja R., Manival V., Roy R. P., Vishwakarma R. A., Rao K. V. S. B cell responses to a peptide epitope. V. Kinetic regulation of repertoire discrimination and antibody optimum for epitope. J. Immunol. 161:1998;3510-3519.
46. Newton S. M. C., Joys T. M., Anderson S. A., Kennedy R. C., Hovi M. E., Stocker B. A. D. Expression and immunogenicity of an 18-residue epitope of HIV-1 gp41 inserted in the flagellar protein of a Salmonella live vaccine. Res. Microbiol. 146:1995;203-216.
47. Niedrig M., Bröker M., Walter G., Stüber W., Harthus H.-P., Mehdi S., Gelderblom H. R., Pauli G. Murine monoclonal antibodies directed against the transmembrane protein gp41 of human immunodeficiency virus type 1 enhance its infectivity. J. Gen. Virol. 73:1992;951-954.
48. Pincus S. H., Messer K. G., Schwartz D. H., Lewis G. K., Graham B. S., Blattner W. A., Fisher G. Differences in the antibody response to human immunodeficiency virus type 1 envelope protein (gp160) in infected laboratory workers and vaccines. J. Clin. Invest. 91:1993;1987-1996.
49. Pincus S. H., Messer K. G., Hsu S.-L. Effect of non-protective vaccination on antibody response to subsequent human immunodeficiency virus infection. J. Clin. Invest. 93:1994;140-146.
50. Porta C., Spall V. E., Loveland J., Johnson J. E., Barker P. J., Lomonossoff G. P. Development of cowpea mosaic virus as a high yielding system for the presentation of foreign peptides. Virology. 202:1994;949-955.
51. Sattentau Q. J. HIV gp120: Double lock strategy foils host defences. Structure. 6:1998;945-949.
52. Sattentau Q. J., Zolla-Pazner S., Poignard P. Epitopes exposed on functional, oligomeric gp41 molecules. Virology. 206:1995;713-717.
53. Vella C., Minor P. D., Weller I. V. D., Jenkins O., Evans D., Almond J. Recognition of poliovirus/HIV chimeras by antisera from individuals with HIV infection. AIDS. 5:1991;425-430.
54. Vella C., Ferguson M., Dunn G., Meloen R., Langedijk H., Evans D., Minor P. D. Characterization and primary structure of a human immunodeficiency virus type 1 (HIV-1) neutralization domain as presented by a poliovirus type 1/HIV-1 chimera. J. Gen. Virol. 74:1993;2603-2607.
55. Vijaykrishnan L., Sarkar S., Roy R. P., Rao K. V. S. B cell responses to a peptide epitope. IV. Subtle sequence changes in flanking residues modulate immunization. J. Immunol. 159:1997;1809-1819.
56. Wilson I. A., Stanfield R. L. Antibody-antigen interactions. Curr. Opin. Struct. Biol. 3:1993;113-118.