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. 1992 Apr;60(4):1415–1421. doi: 10.1128/iai.60.4.1415-1421.1992

Hemolysin-producing Listeria monocytogenes affects the immune response to T-cell-dependent and T-cell-independent antigens.

C M Hage-Chahine 1, G Del Giudice 1, P H Lambert 1, J C Pechere 1
PMCID: PMC257013  PMID: 1548067

Abstract

A murine experimental infection with a hemolysin-producing (Hly+) strain of Listeria monocytogenes and a non-hemolysin-producing (Hly-) mutant was used as an in vivo model to evaluate the role of hemolysin production in the immune response. No antilisterial antibodies were detectable following sublethal infection with Hly+ bacteria, but consistent antilisterial immunoglobulin G (IgG) and IgM antibody production was observed following sublethal infection with the Hly- mutant. Hly+ but not Hly- L. monocytogenes induced transient inhibition of antibody response to Hly- bacteria and to unrelated T-cell-dependent (tetanus toxoid) and T-cell-independent (pneumococcal polysaccharide 3) antigens. Transient inhibition of the activation of an antigen-specific T-cell clone was also observed following Hly+ infection of antigen-presenting cells but not following Hly- infection. These results suggest that hemolysin production by L. monocytogenes is an important factor in modulating the immune response to T-cell-dependent and T-cell-independent antigens in infected individuals.

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Selected References

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  1. Aalund O., Osebold J. W., Murphy F. A., Di Capua R. A. Antibody heterogeneity in experimental listeriosis. J Immunol. 1966 Jul;97(1):150–157. [PubMed] [Google Scholar]
  2. Baker P. J., Amsbaugh D. F., Stashak P. W., Caldes G., Prescott B. Regulation of the antibody response to pneumococcal polysaccharide by thymus-derived cells. Rev Infect Dis. 1981 Mar-Apr;3(2):332–341. doi: 10.1093/clinids/3.2.332. [DOI] [PubMed] [Google Scholar]
  3. Berche P. A. Resistance to listeriosis in two lines of mice genetically selected for high and low antibody production. Immunology. 1985 Dec;56(4):707–716. [PMC free article] [PubMed] [Google Scholar]
  4. Berche P., Gaillard J. L., Richard S. Invasiveness and intracellular growth of Listeria monocytogenes. Infection. 1988;16 (Suppl 2):S145–S148. doi: 10.1007/BF01639738. [DOI] [PubMed] [Google Scholar]
  5. Berche P., Gaillard J. L., Sansonetti P. J. Intracellular growth of Listeria monocytogenes as a prerequisite for in vivo induction of T cell-mediated immunity. J Immunol. 1987 Apr 1;138(7):2266–2271. [PubMed] [Google Scholar]
  6. Buchmeier N. A., Schreiber R. D. Requirement of endogenous interferon-gamma production for resolution of Listeria monocytogenes infection. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7404–7408. doi: 10.1073/pnas.82.21.7404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cluff C. W., Garcia M., Ziegler H. K. Intracellular hemolysin-producing Listeria monocytogenes strains inhibit macrophage-mediated antigen processing. Infect Immun. 1990 Nov;58(11):3601–3612. doi: 10.1128/iai.58.11.3601-3612.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cluff C. W., Ziegler H. K. Inhibition of macrophage-mediated antigen presentation by hemolysin-producing Listeria monocytogenes. J Immunol. 1987 Dec 1;139(11):3808–3812. [PubMed] [Google Scholar]
  9. Cossart P., Vicente M. F., Mengaud J., Baquero F., Perez-Diaz J. C., Berche P. Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect Immun. 1989 Nov;57(11):3629–3636. doi: 10.1128/iai.57.11.3629-3636.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. De Libero G., Kaufmann S. H. Antigen-specific Lyt-2+ cytolytic T lymphocytes from mice infected with the intracellular bacterium Listeria monocytogenes. J Immunol. 1986 Oct 15;137(8):2688–2694. [PubMed] [Google Scholar]
  11. Geoffroy C., Gaillard J. L., Alouf J. E., Berche P. Purification, characterization, and toxicity of the sulfhydryl-activated hemolysin listeriolysin O from Listeria monocytogenes. Infect Immun. 1987 Jul;55(7):1641–1646. doi: 10.1128/iai.55.7.1641-1646.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gessner A., Moskophidis D., Lehmann-Grube F. Enumeration of single IFN-gamma-producing cells in mice during viral and bacterial infection. J Immunol. 1989 Feb 15;142(4):1293–1298. [PubMed] [Google Scholar]
  13. Gray M. L., Killinger A. H. Listeria monocytogenes and listeric infections. Bacteriol Rev. 1966 Jun;30(2):309–382. doi: 10.1128/br.30.2.309-382.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. HOOD M. Listeriosis as an infection of pregnancy manifested in the newborn. Pediatrics. 1961 Mar;27:390–396. [PubMed] [Google Scholar]
  15. Hahn H., Kaufmann S. H. The role of cell-mediated immunity in bacterial infections. Rev Infect Dis. 1981 Nov-Dec;3(6):1221–1250. doi: 10.1093/clinids/3.6.1221. [DOI] [PubMed] [Google Scholar]
  16. Handa T., Mitsuyama M., Serushago B. A., Muramori K., Nomoto K. Co-operative effect of MCF and MAF(IFN-gamma) in the protection of mice against Listeria monocytogenes. Immunology. 1988 Nov;65(3):427–432. [PMC free article] [PubMed] [Google Scholar]
  17. Havell E. A., Spitalny G. L., Patel P. J. Enhanced production of murine interferon gamma by T cells generated in response to bacterial infection. J Exp Med. 1982 Jul 1;156(1):112–127. doi: 10.1084/jem.156.1.112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Havell E. A. Synthesis and secretion of interferon by murine fibroblasts in response to intracellular Listeria monocytogenes. Infect Immun. 1986 Dec;54(3):787–792. doi: 10.1128/iai.54.3.787-792.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kaufmann S. H., Hug E., De Libero G. Listeria monocytogenes-reactive T lymphocyte clones with cytolytic activity against infected target cells. J Exp Med. 1986 Jul 1;164(1):363–368. doi: 10.1084/jem.164.1.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kiderlen A. F., Kaufmann S. H., Lohmann-Matthes M. L. Protection of mice against the intracellular bacterium Listeria monocytogenes by recombinant immune interferon. Eur J Immunol. 1984 Oct;14(10):964–967. doi: 10.1002/eji.1830141019. [DOI] [PubMed] [Google Scholar]
  21. LaGrange P. H., Hurtrel B. Listeria monocytogenes infection in Biozzi mouse lines with high or low antibody responses, or with high (Hi/PHA) or low (Lo/PHA) responses to phytohemagglutinin. Cell Immunol. 1985 Nov;96(1):210–222. doi: 10.1016/0008-8749(85)90352-1. [DOI] [PubMed] [Google Scholar]
  22. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  23. Lenzini L., Rottoli P., Rottoli L. The spectrum of human tuberculosis. Clin Exp Immunol. 1977 Feb;27(2):230–237. [PMC free article] [PubMed] [Google Scholar]
  24. MACKANESS G. B. Cellular resistance to infection. J Exp Med. 1962 Sep 1;116:381–406. doi: 10.1084/jem.116.3.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Magee D. M., Wing E. J. Cloned L3T4+ T lymphocytes protect mice against Listeria monocytogenes by secreting IFN-gamma. J Immunol. 1988 Nov 1;141(9):3203–3207. [PubMed] [Google Scholar]
  26. Nakane A., Minagawa T., Kato K. Endogenous tumor necrosis factor (cachectin) is essential to host resistance against Listeria monocytogenes infection. Infect Immun. 1988 Oct;56(10):2563–2569. doi: 10.1128/iai.56.10.2563-2569.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nieman R. E., Lorber B. Listeriosis in adults: a changing pattern. Report of eight cases and review of the literature, 1968-1978. Rev Infect Dis. 1980 Mar-Apr;2(2):207–227. doi: 10.1093/clinids/2.2.207. [DOI] [PubMed] [Google Scholar]
  28. Osebold J. W., DiCapua R. A. Cellular immunity of mice infected with Listeria monocytogenes in diffusion chambers. J Bacteriol. 1968 Jun;95(6):2158–2164. doi: 10.1128/jb.95.6.2158-2164.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Portnoy D. A., Jacks P. S., Hinrichs D. J. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med. 1988 Apr 1;167(4):1459–1471. doi: 10.1084/jem.167.4.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Reynolds D. S., Boom W. H., Abbas A. K. Inhibition of B lymphocyte activation by interferon-gamma. J Immunol. 1987 Aug 1;139(3):767–773. [PubMed] [Google Scholar]
  31. Rodriguez G. E., McClatchy J. K., Campbell P. A. Induction of Resistance by Listeria monocytogenes Cell Wall Fraction. Infect Immun. 1974 Nov;10(5):1163–1169. doi: 10.1128/iai.10.5.1163-1169.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. SUTER E. Interaction between phagocytes and pathogenic microorganisms. Bacteriol Rev. 1956 Jun;20(2):94–132. doi: 10.1128/br.20.2.94-132.1956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Safley S. A., Cluff C. W., Marshall N. E., Ziegler H. K. Role of listeriolysin-O (LLO) in the T lymphocyte response to infection with Listeria monocytogenes. Identification of T cell epitopes of LLO. J Immunol. 1991 May 15;146(10):3604–3616. [PubMed] [Google Scholar]
  34. Sansonetti P., Lagrange P. H. The immunology of leprosy: speculations on the leprosy spectrum. Rev Infect Dis. 1981 May-Jun;3(3):422–469. doi: 10.1093/clinids/3.3.422. [DOI] [PubMed] [Google Scholar]
  35. Seeliger H. P. Etat actuel de nos connaissances sur les Listeria et les listérioses. Bull Acad Natl Med. 1987 Oct;171(7):799–806. [PubMed] [Google Scholar]
  36. Togna A. R., Del Giudice G., Verdini A. S., Bonelli F., Pessi A., Engers H. D., Corradin G. Synthetic Plasmodium falciparum circumsporozoite peptides elicit heterogenous L3T4+ T cell proliferative responses in H-2b mice. J Immunol. 1986 Nov 1;137(9):2956–2960. [PubMed] [Google Scholar]
  37. Visintine A. M., Oleske J. M., Nahmias A. J. Infection in infants and children. Am J Dis Child. 1977 Apr;131(4):393–397. doi: 10.1001/archpedi.1977.02120170019002. [DOI] [PubMed] [Google Scholar]
  38. WELSHIMER H. J. Staphylococcal antibody production in response to injections with Listeria monocytogenes. J Bacteriol. 1960 Mar;79:456–457. doi: 10.1128/jb.79.3.456-457.1960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Winters W. D., Cox R. A. Serodiagnosis of tuberculosis by radioimmunoassay. Am Rev Respir Dis. 1981 Nov;124(5):582–585. doi: 10.1164/arrd.1981.124.5.582. [DOI] [PubMed] [Google Scholar]
  40. Yamada A., Himeno K., Nakamura S., Kawamura I., Nomoto K. Transfer of resistance to primary infection of Listeria monocytogenes and early induction of delayed hypersensitivity by sera from L. monocytogenes-infected mice. Infect Immun. 1987 Dec;55(12):3078–3084. doi: 10.1128/iai.55.12.3078-3084.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

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