Abstract
Purified reovirus serotype 1, encapsulated in biodegradable aqueous microcapsules, was found to bypass maternal antibody passively transferred by suckling to neonates. Genetically identical, immunocompetent F1 scid/+ mice were generated by the reciprocal crosses of C.B17 scid/scid and normal congenic +/+ adult mice. The immunocompetent +/+ dams were either orally infected with reovirus prior to mating or not. Thus, these immunocompetent F1 pups developed either in the absence or in presence of passively transferred maternal immunity. The F1 mice were orally immunized on day 10 with either live virus, microencapsulated reovirus, or empty microcapsules plus live virus. The immune responses were assessed in the neonatal gut-associated lymphoid tissues (GALT). Examination of reovirus specific immunoglobulin A in the serum and GALT, taken on days 7, 14, and 21 postimmunization, clearly demonstrated that microencapsulated reovirus could bypass the normal effect of maternal antibodies, passively acquired by suckling, to inhibit active priming of neonates by oral route. These observations seem relevant to the development of efficacious oral vaccines that also allow passive, protective immunity via suckled maternal antibodies while permitting active oral immunization of neonates.
Full Text
The Full Text of this article is available as a PDF (164.0 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bass D. M., Trier J. S., Dambrauskas R., Wolf J. L. Reovirus type I infection of small intestinal epithelium in suckling mice and its effect on M cells. Lab Invest. 1988 Feb;58(2):226–235. [PubMed] [Google Scholar]
- Bosma M. J., Carroll A. M. The SCID mouse mutant: definition, characterization, and potential uses. Annu Rev Immunol. 1991;9:323–350. doi: 10.1146/annurev.iy.09.040191.001543. [DOI] [PubMed] [Google Scholar]
- Ceyhan M., Kanra G., Seçmeer G., Midthun K., Davidson B. L., Zito E. T., Vesikari T. Take of rhesus-human reassortant tetravalent rotavirus vaccine in breast-fed infants. Acta Paediatr. 1993 Mar;82(3):223–227. doi: 10.1111/j.1651-2227.1993.tb12646.x. [DOI] [PubMed] [Google Scholar]
- Chui L. W., Marusyk R. G., Pabst H. F. Measles virus specific antibody in infants in a highly vaccinated society. J Med Virol. 1991 Mar;33(3):199–204. doi: 10.1002/jmv.1890330311. [DOI] [PubMed] [Google Scholar]
- Cuff C. F., Lavi E., Cebra C. K., Cebra J. J., Rubin D. H. Passive immunity to fatal reovirus serotype 3-induced meningoencephalitis mediated by both secretory and transplacental factors in neonatal mice. J Virol. 1990 Mar;64(3):1256–1263. doi: 10.1128/jvi.64.3.1256-1263.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cunningham A. S. Morbidity in breast-fed and artificially fed infants. J Pediatr. 1977 May;90(5):726–729. doi: 10.1016/s0022-3476(77)81236-5. [DOI] [PubMed] [Google Scholar]
- Cushing A. H., Anderson L. Diarrhea in breast-fed and non-breast-fed infants. Pediatrics. 1982 Dec;70(6):921–925. [PubMed] [Google Scholar]
- Edelman R., Russell R. G., Losonsky G., Tall B. D., Tacket C. O., Levine M. M., Lewis D. H. Immunization of rabbits with enterotoxigenic E. coli colonization factor antigen (CFA/I) encapsulated in biodegradable microspheres of poly (lactide-co-glycolide). Vaccine. 1993;11(2):155–158. doi: 10.1016/0264-410x(93)90012-m. [DOI] [PubMed] [Google Scholar]
- Eldridge J. H., Gilley R. M., Staas J. K., Moldoveanu Z., Meulbroek J. A., Tice T. R. Biodegradable microspheres: vaccine delivery system for oral immunization. Curr Top Microbiol Immunol. 1989;146:59–66. doi: 10.1007/978-3-642-74529-4_6. [DOI] [PubMed] [Google Scholar]
- Eldridge J. H., Staas J. K., Meulbroek J. A., McGhee J. R., Tice T. R., Gilley R. M. Biodegradable microspheres as a vaccine delivery system. Mol Immunol. 1991 Mar;28(3):287–294. doi: 10.1016/0161-5890(91)90076-v. [DOI] [PubMed] [Google Scholar]
- George A., Kost S. I., Witzleben C. L., Cebra J. J., Rubin D. H. Reovirus-induced liver disease in severe combined immunodeficient (SCID) mice. A model for the study of viral infection, pathogenesis, and clearance. J Exp Med. 1990 Mar 1;171(3):929–934. doi: 10.1084/jem.171.3.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glass R. I., Ing D. J., Stoll B. J., Ing R. T. Immune response to rotavirus vaccines among breast-fed and nonbreast-fed children. Adv Exp Med Biol. 1991;310:249–254. doi: 10.1007/978-1-4615-3838-7_33. [DOI] [PubMed] [Google Scholar]
- Glass R. I., Stoll B. J. The protective effect of human milk against diarrhea. A review of studies from Bangladesh. Acta Paediatr Scand Suppl. 1989;351:131–136. doi: 10.1111/j.1651-2227.1989.tb11225.x. [DOI] [PubMed] [Google Scholar]
- Jänne J., Pösö H., Raina A. Polyamines in rapid growth and cancer. Biochim Biophys Acta. 1978 Apr 6;473(3-4):241–293. doi: 10.1016/0304-419x(78)90015-x. [DOI] [PubMed] [Google Scholar]
- Keljo D. J., Butler D. G., Hamilton J. R. Altered jejunal permeability to macromolecules during viral enteritis in the piglet. Gastroenterology. 1985 Apr;88(4):998–1004. doi: 10.1016/S0016-5085(85)80020-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kramer D. R., Cebra J. J. Early appearance of "natural" mucosal IgA responses and germinal centers in suckling mice developing in the absence of maternal antibodies. J Immunol. 1995 Mar 1;154(5):2051–2062. [PubMed] [Google Scholar]
- Kramer D. R., Cebra J. J. Role of maternal antibody in the induction of virus specific and bystander IgA responses in Peyer's patches of suckling mice. Int Immunol. 1995 Jun;7(6):911–918. doi: 10.1093/intimm/7.6.911. [DOI] [PubMed] [Google Scholar]
- Logan A. C., Chow K. P., George A., Weinstein P. D., Cebra J. J. Use of Peyer's patch and lymph node fragment cultures to compare local immune responses to Morganella morganii. Infect Immun. 1991 Mar;59(3):1024–1031. doi: 10.1128/iai.59.3.1024-1031.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- London S. D., Rubin D. H., Cebra J. J. Gut mucosal immunization with reovirus serotype 1/L stimulates virus-specific cytotoxic T cell precursors as well as IgA memory cells in Peyer's patches. J Exp Med. 1987 Mar 1;165(3):830–847. doi: 10.1084/jem.165.3.830. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moldoveanu Z., Novak M., Huang W. Q., Gilley R. M., Staas J. K., Schafer D., Compans R. W., Mestecky J. Oral immunization with influenza virus in biodegradable microspheres. J Infect Dis. 1993 Jan;167(1):84–90. doi: 10.1093/infdis/167.1.84. [DOI] [PubMed] [Google Scholar]
- Narayanan I., Gupta J. Human milk and neonatal infections. Acta Paediatr Scand Suppl. 1989;351:126–130. doi: 10.1111/j.1651-2227.1989.tb11224.x. [DOI] [PubMed] [Google Scholar]
- Neutra M. R., Phillips T. L., Mayer E. L., Fishkind D. J. Transport of membrane-bound macromolecules by M cells in follicle-associated epithelium of rabbit Peyer's patch. Cell Tissue Res. 1987 Mar;247(3):537–546. doi: 10.1007/BF00215747. [DOI] [PubMed] [Google Scholar]
- O'Hagan D. T., McGee J. P., Holmgren J., Mowat A. M., Donachie A. M., Mills K. H., Gaisford W., Rahman D., Challacombe S. J. Biodegradable microparticles for oral immunization. Vaccine. 1993;11(2):149–154. doi: 10.1016/0264-410x(93)90011-l. [DOI] [PubMed] [Google Scholar]
- O'Hagan D. T., Rahman D., McGee J. P., Jeffery H., Davies M. C., Williams P., Davis S. S., Challacombe S. J. Biodegradable microparticles as controlled release antigen delivery systems. Immunology. 1991 Jun;73(2):239–242. [PMC free article] [PubMed] [Google Scholar]
- Offit P. A., Clark H. F. Maternal antibody-mediated protection against gastroenteritis due to rotavirus in newborn mice is dependent on both serotype and titer of antibody. J Infect Dis. 1985 Dec;152(6):1152–1158. doi: 10.1093/infdis/152.6.1152. [DOI] [PubMed] [Google Scholar]
- Offit P. A., Clark H. F., Plotkin S. A. Response of mice to rotaviruses of bovine or primate origin assessed by radioimmunoassay, radioimmunoprecipitation, and plaque reduction neutralization. Infect Immun. 1983 Oct;42(1):293–300. doi: 10.1128/iai.42.1.293-300.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Offit P. A., Khoury C. A., Moser C. A., Clark H. F., Kim J. E., Speaker T. J. Enhancement of rotavirus immunogenicity by microencapsulation. Virology. 1994 Aug 15;203(1):134–143. doi: 10.1006/viro.1994.1463. [DOI] [PubMed] [Google Scholar]
- Ogra P. L. Mucosal immune response to poliovirus vaccines in childhood. Rev Infect Dis. 1984 May-Jun;6 (Suppl 2):S361–S368. doi: 10.1093/clinids/6.supplement_2.s361. [DOI] [PubMed] [Google Scholar]
- Okamoto Y., Tsutsumi H., Kumar N. S., Ogra P. L. Effect of breast feeding on the development of anti-idiotype antibody response to F glycoprotein of respiratory syncytial virus in infant mice after post-partum maternal immunization. J Immunol. 1989 Apr 1;142(7):2507–2512. [PubMed] [Google Scholar]
- Pabst H. F., Godel J., Grace M., Cho H., Spady D. W. Effect of breast-feeding on immune response to BCG vaccination. Lancet. 1989 Feb 11;1(8633):295–297. doi: 10.1016/s0140-6736(89)91307-x. [DOI] [PubMed] [Google Scholar]
- Plotkin S. A., Katz M., Brown R. E., Pagano J. S. Oral poliovirus vaccination in newborn African infants. The inhibitory effect of breast feeding. Am J Dis Child. 1966 Jan;111(1):27–30. doi: 10.1001/archpedi.1966.02090040063004. [DOI] [PubMed] [Google Scholar]
- Ray R., Novak M., Duncan J. D., Matsuoka Y., Compans R. W. Microencapsulated human parainfluenza virus induces a protective immune response. J Infect Dis. 1993 Mar;167(3):752–755. doi: 10.1093/infdis/167.3.752. [DOI] [PubMed] [Google Scholar]
- Wolf J. L., Kauffman R. S., Finberg R., Dambrauskas R., Fields B. N., Trier J. S. Determinants of reovirus interaction with the intestinal M cells and absorptive cells of murine intestine. Gastroenterology. 1983 Aug;85(2):291–300. [PubMed] [Google Scholar]