Dissociation of Influenza Virus Hemagglutinin and Neuraminidase Eliminates Their Intravirionic Antigenic Competition

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 1993 Oct 1

PMID 8371337

Citations 50

Authors

B E Johansson

E D KILBOURNE

Affiliations

Soon will be listed here.

Abstract

When presented together on the intact influenza virus particle, the external hemagglutinin (HA) and neuraminidase (NA) antigens are competitive, with HA dominant over NA in both T- and B-cell priming (B. E. Johansson, T. M. Moran, and E. D. Kilbourne, Proc. Natl. Acad. Sci. USA 84:6869-6873, 1987). Dissociation and purification of HA and NA from virus and their injection separately or in combination into BALB/c mice eliminates their antigenic competition as measured by antibody response, confirming that it is their structural association that leads to what we have termed intravirionic antigenic competition. We discuss this phenomenon with respect to previously described intermolecular antigenic competition and with regard to its probable mechanism. Our findings are relevant to contemporary interest in viral vaccine vectors and multicomponent vaccines.

Citing Articles

Headless hemagglutinin-containing influenza viral particles direct immune responses toward more conserved epitopes.

Hamele C, Luo Z, Leonard R, Spurrier M, Burke K, Webb S J Virol. 2024; 98(10):e0116624.

PMID: 39324791 PMC: 11495035. DOI: 10.1128/jvi.01166-24.

COBRA N2 NA vaccines induce protective immune responses against influenza viral infection.

Zhang X, Skarlupka A, Shi H, Ross T Hum Vaccin Immunother. 2024; 20(1):2403175.

PMID: 39291424 PMC: 11657087. DOI: 10.1080/21645515.2024.2403175.

Anti-neuraminidase immunity in the combat against influenza.

Zhang X, Ross T Expert Rev Vaccines. 2024; 23(1):474-484.

PMID: 38632930 PMC: 11157429. DOI: 10.1080/14760584.2024.2343689.

Sequential Immunizations with Influenza Neuraminidase Protein Followed by Peptide Nanoclusters Induce Heterologous Protection.

Song W, Wan M, She J, Zhao S, Liu D, Chang H Viruses. 2024; 16(1).

PMID: 38257777 PMC: 10819419. DOI: 10.3390/v16010077.

Pre-existing CD4 T cell help boosts antibody responses but has limited impact on germinal center, antigen-specific B cell frequencies after influenza infection.

Besavilla D, Reusch L, Enriquez J, Schon K, Angeletti D Front Immunol. 2023; 14:1243164.

PMID: 37711622 PMC: 10499173. DOI: 10.3389/fimmu.2023.1243164.

References

Erickson A, KILBOURNE E . Comparative amino acid analysis of influenza A viral proteins. Virology. 1980; 100(1):34-42. DOI: 10.1016/0042-6822(80)90549-8. View

Barr M, LLEWELLYN-JONES M . Some factors influencing the response to immunisation with single and combined prophylactics. Br J Exp Pathol. 1955; 36(2):147-54. PMC: 2083361. View

Russell S, Liew F . T cells primed by influenza virion internal components can cooperate in the antibody response to haemagglutinin. Nature. 1979; 280(5718):147-8. DOI: 10.1038/280147a0. View

Lamb J, Woody J, Hartzman R, Eckels D . In vitro influenza virus-specific antibody production in man: antigen-specific and HLA-restricted induction of helper activity mediated by cloned human T lymphocytes. J Immunol. 1982; 129(4):1465-70. View

Scherle P, GERHARD W . Functional analysis of influenza-specific helper T cell clones in vivo. T cells specific for internal viral proteins provide cognate help for B cell responses to hemagglutinin. J Exp Med. 1986; 164(4):1114-28. PMC: 2188433. DOI: 10.1084/jem.164.4.1114. View

KILBOURNE E, CERINI C, Khan M, Mitchell Jr J, Ogra P . Immunologic response to the influenza virus neuraminidase is influenced by prior experience with the associated viral hemagglutinin. I. Studies in human vaccinees. J Immunol. 1987; 138(9):3010-3. View

Johansson B, Moran T, Bona C, Popple S, KILBOURNE E . Immunologic response to influenza virus neuraminidase is influenced by prior experience with the associated viral hemagglutinin. II. Sequential infection of mice simulates human experience. J Immunol. 1987; 139(6):2010-4. View

Johansson B, Moran T, Bona C, KILBOURNE E . Immunologic response to influenza virus neuraminidase is influenced by prior experience with the associated viral hemagglutinin. III. Reduced generation of neuraminidase-specific helper T cells in hemagglutinin-primed mice. J Immunol. 1987; 139(6):2015-9. View

Johansson B, Moran T, KILBOURNE E . Antigen-presenting B cells and helper T cells cooperatively mediate intravirionic antigenic competition between influenza A virus surface glycoproteins. Proc Natl Acad Sci U S A. 1987; 84(19):6869-73. PMC: 299186. DOI: 10.1073/pnas.84.19.6869. View

10.

Hammerl P, Weger R, Thalhamer J . Antigenic competition in the immune response against protein mixtures: strain-specific non-immunogenicity of Escherichia coli antigens. Mol Immunol. 1988; 25(3):313-20. DOI: 10.1016/0161-5890(88)90023-5. View

11.

Johansson B, Bucher D, KILBOURNE E . Purified influenza virus hemagglutinin and neuraminidase are equivalent in stimulation of antibody response but induce contrasting types of immunity to infection. J Virol. 1989; 63(3):1239-46. PMC: 247820. DOI: 10.1128/JVI.63.3.1239-1246.1989. View

12.

Jones A, Johns A, MAGRATH D, Sheffield F . Durability of immunity to diphtheria, tetanus and poliomyelitis after a three dose immunization schedule completed in the first eight months of life. Vaccine. 1989; 7(4):300-2. DOI: 10.1016/0264-410x(89)90189-8. View

13.

Compans R, Klenk H, CALIGUIRI L, Choppin P . Influenza virus proteins. I. Analysis of polypeptides of the virion and identification of spike glycoproteins. Virology. 1970; 42(4):880-9. DOI: 10.1016/0042-6822(70)90337-5. View

14.

Taussig M . The effect of Freund's complete adjuvant on the specificity of an immune response, and its relationship to antigenic competition. Cell Immunol. 1974; 11(1-3):484-7. DOI: 10.1016/0008-8749(74)90046-x. View

15.

Jackson D, Crabb B, Poumbourios P, Tulip W, Laver W . Three antibody molecules can bind simultaneously to each monomer of the tetramer of influenza virus neuraminidase and the trimer of influenza virus hemagglutinin. Arch Virol. 1991; 116(1-4):45-56. DOI: 10.1007/BF01319230. View

16.

Johansson B, KILBOURNE E . Programmed antigenic stimulation: kinetics of the immune response to challenge infections of mice primed with influenza inactivated whole virus or neuraminidase vaccine. Vaccine. 1991; 9(5):330-3. DOI: 10.1016/0264-410x(91)90059-f. View

17.

Jalil F, Zaman S, Carlsson B, Glass R, Kapikian A, Mellander L . Immunogenicity and reactogenicity of rhesus rotavirus vaccine given in combination with oral or inactivated poliovirus vaccines and diphtheria-tetanus-pertussis vaccine. Trans R Soc Trop Med Hyg. 1991; 85(2):292-6. DOI: 10.1016/0035-9203(91)90061-3. View

18.

Amano H, Uemoto H, Kuroda K, Hosaka Y . Immunoelectron microscopy of influenza A virus neuraminidase glycoprotein topography. J Gen Virol. 1992; 73 ( Pt 8):1969-75. DOI: 10.1099/0022-1317-73-8-1969. View

19.

Barr M, LLEWELLYN-JONES M . Some factors influencing the response of animals to immunisation with combined prophylactics. Br J Exp Pathol. 1953; 34(1):12-22. PMC: 2073477. View

20.

Barr M, LLEWELLYN-JONES M . Interference with antitoxic responses in immunisation with combined prophylactics. Br J Exp Pathol. 1953; 34(3):233-40. PMC: 2073513. View