Abstract
The route of transfer of anti-Borrelia duttonii antibody subclasses from mother to young and their role in protection against borrelial challenge infection in ddY mice were investigated. Offspring from infected and noninfected mice were segregated and nursed by noninfected or infected mothers. Enzyme-linked immunosorbent assay analysis of antibodies of the cross-suckled offspring revealed that anti-B. duttonii immunoglobulin G1 (IgG1) is transferred exclusively in milk and that IgG2a is transferred mainly in milk but also slightly through the yolk sac route. On the other hand, IgG3 is transferred mainly through the yolk sac route but also slightly in milk, whereas IgG2b is transferred through both routes but to a lesser extent. Anti-borrelial IgM was not detected in any offspring. The protective role of transferred IgG subclasses was examined by challenge infection with B. duttonii. Offspring from noninfected mice fed by infected mothers had IgG1, IgG2a, and IgG3 at challenge and were completely protected against the challenge infection. On the other hand, offspring from infected mice fed by noninfected mothers had only IgG3, and 8 of 10 were completely protected from challenge infection whereas the other 2 contracted slight and transient spirochetemia. These findings suggested that anti-borrelial IgG3 alone has considerable protective activity and that IgG1, IgG2a, or both, either by themselves or together with IgG3, have a complete protective activity against borrelial infection.
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- Albright J. W., Albright J. F. Immunological and nonimmunological control of severity of Trypanosoma musculi infections in C3H and C57BL/6 inbred mice. Infect Immun. 1989 Jun;57(6):1647–1655. doi: 10.1128/iai.57.6.1647-1655.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Albright J. W., Matusewicz N. M., Albright J. F. Aging of the murine immune system is reflected by declining ability to generate antibodies that promote elimination of Trypanosoma musculi. J Immunol. 1988 Aug 15;141(4):1318–1325. [PubMed] [Google Scholar]
- Arimitsu Y., Akama K. Characterization of protective antibodies produced in mice infected with Borrelia duttonii. Jpn J Med Sci Biol. 1973 Dec;26(5):229–237. doi: 10.7883/yoken1952.26.229. [DOI] [PubMed] [Google Scholar]
- Barbour A. G. Antigenic variation of a relapsing fever Borrelia species. Annu Rev Microbiol. 1990;44:155–171. doi: 10.1146/annurev.mi.44.100190.001103. [DOI] [PubMed] [Google Scholar]
- Barrett D. J., Ayoub E. M. IgG2 subclass restriction of antibody to pneumococcal polysaccharides. Clin Exp Immunol. 1986 Jan;63(1):127–134. [PMC free article] [PubMed] [Google Scholar]
- Brambell F. W. The transmission of immunity from mother to young and the catabolism of immunoglobulins. Lancet. 1966 Nov 19;2(7473):1087–1093. doi: 10.1016/s0140-6736(66)92190-8. [DOI] [PubMed] [Google Scholar]
- Der Balian G. P., Slack J., Clevinger B. L., Bazin H., Davie J. M. Subclass restriction of murine antibodies. III. Antigens that stimulate IgG3 in mice stimulate IgG2c in rats. J Exp Med. 1980 Jul 1;152(1):209–218. doi: 10.1084/jem.152.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fikrig E., Barthold S. W., Kantor F. S., Flavell R. A. Protection of mice against the Lyme disease agent by immunizing with recombinant OspA. Science. 1990 Oct 26;250(4980):553–556. doi: 10.1126/science.2237407. [DOI] [PubMed] [Google Scholar]
- Goubau P. F., Munyangeyo C. Fièvre récurrente congénitale à Borrelia duttoni. A propos d'un cas au Rwanda. Ann Soc Belg Med Trop. 1983 Dec;63(4):367–369. [PubMed] [Google Scholar]
- Grey H. M., Hirst J. W., Cohn M. A new mouse immunoglobulin: IgG3. J Exp Med. 1971 Feb 1;133(2):289–304. doi: 10.1084/jem.133.2.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hammarström L., Granström M., Oxelius V., Persson M. A., Smith C. I. IgG subclass distribution of antibodies against S. aureus teichoic acid and alpha-toxin in normal and immunodeficient donors. Clin Exp Immunol. 1984 Mar;55(3):593–601. [PMC free article] [PubMed] [Google Scholar]
- Heiman H. S., Weisman L. E. Transplacental or enteral transfer of maternal immunization-induced antibody protects suckling rats from type III group B streptococcal infection. Pediatr Res. 1989 Dec;26(6):629–632. doi: 10.1203/00006450-198912000-00023. [DOI] [PubMed] [Google Scholar]
- Katz J., Leary R. M., Ward D. C., Harmon C. C., Michalek S. M. Humoral response to Porphyromonas (Bacteroides) gingivalis in rats: time course and T-cell dependence. Infect Immun. 1992 Sep;60(9):3579–3585. doi: 10.1128/iai.60.9.3579-3585.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Konishi H., Morshed M. G., Akitomi H., Nakazawa T. In vitro cultivation of Borrelia duttonii on cultures of SflEp cells. Microbiol Immunol. 1993;37(3):229–232. doi: 10.1111/j.1348-0421.1993.tb03204.x. [DOI] [PubMed] [Google Scholar]
- Masuzawa T., Beppu Y., Kawabata H., Yanagihara Y., Iwamoto Y., Shimizu T., Johnson R. C. Experimental Borrelia burgdorferi infection of outbred mice. J Clin Microbiol. 1992 Nov;30(11):3016–3018. doi: 10.1128/jcm.30.11.3016-3018.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mbawuike I. N., Six H. R., Cate T. R., Couch R. B. Vaccination with inactivated influenza A virus during pregnancy protects neonatal mice against lethal challenge by influenza A viruses representing three subtypes. J Virol. 1990 Mar;64(3):1370–1374. doi: 10.1128/jvi.64.3.1370-1374.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moreno C., Esdaile J. Immunoglobulin isotype in the murine response to polysaccharide antigens. Eur J Immunol. 1983 Mar;13(3):262–264. doi: 10.1002/eji.1830130317. [DOI] [PubMed] [Google Scholar]
- Natsuume-Sakai S., Motonishi K., Migita S. Quantitative estimations of five classes of immunoglobulin in inbred mouse strains. Immunology. 1977 Jun;32(6):861–866. [PMC free article] [PubMed] [Google Scholar]
- Perlmutter R. M., Hansburg D., Briles D. E., Nicolotti R. A., Davie J. M. Subclass restriction of murine anti-carbohydrate antibodies. J Immunol. 1978 Aug;121(2):566–572. [PubMed] [Google Scholar]
- Reuman P. D., Paganini C. M., Ayoub E. M., Small P. A., Jr Maternal-infant transfer of influenza-specific immunity in the mouse. J Immunol. 1983 Feb;130(2):932–936. [PubMed] [Google Scholar]
- Roberts D. M., Guenthert M., Rodewald R. Isolation and characterization of the Fc receptor from the fetal yolk sac of the rat. J Cell Biol. 1990 Nov;111(5 Pt 1):1867–1876. doi: 10.1083/jcb.111.5.1867. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaible U. E., Kramer M. D., Eichmann K., Modolell M., Museteanu C., Simon M. M. Monoclonal antibodies specific for the outer surface protein A (OspA) of Borrelia burgdorferi prevent Lyme borreliosis in severe combined immunodeficiency (scid) mice. Proc Natl Acad Sci U S A. 1990 May;87(10):3768–3772. doi: 10.1073/pnas.87.10.3768. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmitz J. L., Schell R. F., Callister S. M., Lovrich S. D., Day S. P., Coe J. E. Immunoglobulin G2 confers protection against Borrelia burgdorferi infection in LSH hamsters. Infect Immun. 1992 Jul;60(7):2677–2682. doi: 10.1128/iai.60.7.2677-2682.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simister N. E., Mostov K. E. An Fc receptor structurally related to MHC class I antigens. Nature. 1989 Jan 12;337(6203):184–187. doi: 10.1038/337184a0. [DOI] [PubMed] [Google Scholar]
- Slack J. H. Strain-dependent IgG subclass response patterns. J Immunol. 1987 Dec 1;139(11):3734–3738. [PubMed] [Google Scholar]
- Tsay D. D., Ogden D., Schlamowitz M. Binding of homologous and heterologous IgG to Fc receptors on the fetal rabbit yolk sac membrane. J Immunol. 1980 Apr;124(4):1562–1565. [PubMed] [Google Scholar]
- Wechsler D. S., Kongshavn P. A. Heat-labile IgG2a antibodies affect cure of Trypanosoma musculi infection in C57BL/6 mice. J Immunol. 1986 Nov 1;137(9):2968–2972. [PubMed] [Google Scholar]
- Wilske B. Serodiagnostik der Lyme-Borreliose. Z Hautkr. 1988 Jun 15;63(6):511–514. [PubMed] [Google Scholar]
- Zackrisson G., Lagergård T., Trollfors B. Subclass compositions of immunoglobulin G to pertussis toxin in patients with whooping cough, in healthy individuals, and in recipients of a pertussis toxoid vaccine. J Clin Microbiol. 1989 Jul;27(7):1567–1571. doi: 10.1128/jcm.27.7.1567-1571.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van der Meulen J. A., McNabb T. C., Haeffner-Cavaillon N., Klein M., Dorrington K. J. The Fc gamma receptor on human placental plasma membrane. I. Studies on the binding of homologous and heterologous immunoglobulin G1. J Immunol. 1980 Feb;124(2):500–507. [PubMed] [Google Scholar]