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. 1996 Dec;70(12):9074–9078. doi: 10.1128/jvi.70.12.9074-9078.1996

Role of different lymphoid tissues in the initiation and maintenance of DNA-raised antibody responses to the influenza virus H1 glycoprotein.

C M Boyle 1, M Morin 1, R G Webster 1, H L Robinson 1
PMCID: PMC191015  PMID: 8971047

Abstract

Antibody responses in mice immunized by a single gene gun inoculation of plasmid expressing the influenza virus H1 hemagglutinin and in mice immunized by a sublethal H1 influenza virus infection have been compared. Both immunizations raised long-lived serum responses that were associated with the localization of antibody-secreting cells (ASC) to the bone marrow. However, the kinetics of these responses were 4 to 8 weeks slower in the DNA-immunized than in the infection-primed mice. Following a gene gun booster, the presence of ASC in the inguinal lymph nodes, but not in other lymph nodes, revealed gene gun responses being initiated in the nodes that drain the skin target site. Both pre- and postchallenge, the DNA-immunized mice had 5- to 10-times-lower levels of antibody and ASC than the infection-primed mice.

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Selected References

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  1. Ada G. L., Jones P. D. The immune response to influenza infection. Curr Top Microbiol Immunol. 1986;128:1–54. doi: 10.1007/978-3-642-71272-2_1. [DOI] [PubMed] [Google Scholar]
  2. Bachmann M. F., Kündig T. M., Odermatt B., Hengartner H., Zinkernagel R. M. Free recirculation of memory B cells versus antigen-dependent differentiation to antibody-forming cells. J Immunol. 1994 Oct 15;153(8):3386–3397. [PubMed] [Google Scholar]
  3. Baine Y., Ponzio N. M., Thorbecke G. J. Transfer of memory cells into antigen-pretreated hosts. II. Influence of localized antigen on the migration of specific memory B cells. Eur J Immunol. 1981 Dec;11(12):990–996. doi: 10.1002/eji.1830111208. [DOI] [PubMed] [Google Scholar]
  4. Baine Y., Ponzio N. M., Thorbecke G. J. Unilateral localization of hapten-specific B memory cells in lymph node draining a footpad injection of antigen. Adv Exp Med Biol. 1982;149:167–178. doi: 10.1007/978-1-4684-9066-4_23. [DOI] [PubMed] [Google Scholar]
  5. Benner R., Hijmans W., Haaijman J. J. The bone marrow: the major source of serum immunoglobulins, but still a neglected site of antibody formation. Clin Exp Immunol. 1981 Oct;46(1):1–8. [PMC free article] [PubMed] [Google Scholar]
  6. Benner R., Meima F., van der Meulen G. M. Antibody formation in mouse bone marrow. II. Evidence for a memory-dependent phenomenon. Cell Immunol. 1974 Jul;13(1):95–106. doi: 10.1016/0008-8749(74)90230-5. [DOI] [PubMed] [Google Scholar]
  7. Benner R., Meima F., van der Meulen G. M., van Muiswinkel W. B. Antibody formation in mouse bone marrow. I. Evidence for the development of plaque-forming cells in situ. Immunology. 1974 Feb;26(2):247–255. [PMC free article] [PubMed] [Google Scholar]
  8. Doherty P. C. Anatomical environment as a determinant in viral immunity. J Immunol. 1995 Aug 1;155(3):1023–1027. [PubMed] [Google Scholar]
  9. Donnelly J. J., Ulmer J. B., Liu M. A. Immunization with DNA. J Immunol Methods. 1994 Dec 2;176(2):145–152. doi: 10.1016/0022-1759(94)90308-5. [DOI] [PubMed] [Google Scholar]
  10. Fynan E. F., Webster R. G., Fuller D. H., Haynes J. R., Santoro J. C., Robinson H. L. DNA vaccines: protective immunizations by parenteral, mucosal, and gene-gun inoculations. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11478–11482. doi: 10.1073/pnas.90.24.11478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gray D. Immunological memory. Annu Rev Immunol. 1993;11:49–77. doi: 10.1146/annurev.iy.11.040193.000405. [DOI] [PubMed] [Google Scholar]
  12. Hill S. W. Distribution of plaque-forming cells in the mouse for a protein antigen. Evidence for highly active parathymic lymph nodes following intraperitoneal injection of hen lysozyme. Immunology. 1976 Jun;30(6):895–906. [PMC free article] [PubMed] [Google Scholar]
  13. Hyland L., Sangster M., Sealy R., Coleclough C. Respiratory virus infection of mice provokes a permanent humoral immune response. J Virol. 1994 Sep;68(9):6083–6086. doi: 10.1128/jvi.68.9.6083-6086.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Justewicz D. M., Doherty P. C., Webster R. G. The B-cell response in lymphoid tissue of mice immunized with various antigenic forms of the influenza virus hemagglutinin. J Virol. 1995 Sep;69(9):5414–5421. doi: 10.1128/jvi.69.9.5414-5421.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Justewicz D. M., Morin M. J., Robinson H. L., Webster R. G. Antibody-forming cell response to virus challenge in mice immunized with DNA encoding the influenza virus hemagglutinin. J Virol. 1995 Dec;69(12):7712–7717. doi: 10.1128/jvi.69.12.7712-7717.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Koch G., Weerheijm-De Wit C., Benner R. Quantitation of antibody production in mouse bone marrow during the secondary response to sheep erythrocytes. Int Arch Allergy Appl Immunol. 1982;67(3):239–244. doi: 10.1159/000233025. [DOI] [PubMed] [Google Scholar]
  17. Liew F. Y., Russell S. M., Appleyard G., Brand C. M., Beale J. Cross-protection in mice infected with influenza A virus by the respiratory route is correlated with local IgA antibody rather than serum antibody or cytotoxic T cell reactivity. Eur J Immunol. 1984 Apr;14(4):350–356. doi: 10.1002/eji.1830140414. [DOI] [PubMed] [Google Scholar]
  18. MacLennan I. C., Liu Y. J., Johnson G. D. Maturation and dispersal of B-cell clones during T cell-dependent antibody responses. Immunol Rev. 1992 Apr;126:143–161. doi: 10.1111/j.1600-065x.1992.tb00635.x. [DOI] [PubMed] [Google Scholar]
  19. Mor G., Klinman D. M., Shapiro S., Hagiwara E., Sedegah M., Norman J. A., Hoffman S. L., Steinberg A. D. Complexity of the cytokine and antibody response elicited by immunizing mice with Plasmodium yoelii circumsporozoite protein plasmid DNA. J Immunol. 1995 Aug 15;155(4):2039–2046. [PubMed] [Google Scholar]
  20. Pardoll D. M., Beckerleg A. M. Exposing the immunology of naked DNA vaccines. Immunity. 1995 Aug;3(2):165–169. doi: 10.1016/1074-7613(95)90085-3. [DOI] [PubMed] [Google Scholar]
  21. Ponzio N. M., Chapman-Alexander J. M., Thorbecke G. J. Transfer of memory cells into antigen-pretreated hosts. I. Functional detection of migration sites for antigen-specific B cells. Cell Immunol. 1977 Nov;34(1):79–92. doi: 10.1016/0008-8749(77)90231-3. [DOI] [PubMed] [Google Scholar]
  22. Raz E., Carson D. A., Parker S. E., Parr T. B., Abai A. M., Aichinger G., Gromkowski S. H., Singh M., Lew D., Yankauckas M. A. Intradermal gene immunization: the possible role of DNA uptake in the induction of cellular immunity to viruses. Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9519–9523. doi: 10.1073/pnas.91.20.9519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sangster M., Hyland L., Sealy R., Coleclough C. Distinctive kinetics of the antibody-forming cell response to Sendai virus infection of mice in different anatomical compartments. Virology. 1995 Feb 20;207(1):287–291. doi: 10.1006/viro.1995.1079. [DOI] [PubMed] [Google Scholar]
  24. Slifka M. K., Matloubian M., Ahmed R. Bone marrow is a major site of long-term antibody production after acute viral infection. J Virol. 1995 Mar;69(3):1895–1902. doi: 10.1128/jvi.69.3.1895-1902.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tang D. C., DeVit M., Johnston S. A. Genetic immunization is a simple method for eliciting an immune response. Nature. 1992 Mar 12;356(6365):152–154. doi: 10.1038/356152a0. [DOI] [PubMed] [Google Scholar]
  26. Yankauckas M. A., Morrow J. E., Parker S. E., Abai A., Rhodes G. H., Dwarki V. J., Gromkowski S. H. Long-term anti-nucleoprotein cellular and humoral immunity is induced by intramuscular injection of plasmid DNA containing NP gene. DNA Cell Biol. 1993 Nov;12(9):771–776. doi: 10.1089/dna.1993.12.771. [DOI] [PubMed] [Google Scholar]

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