Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1985 Jun;48(3):763–768. doi: 10.1128/iai.48.3.763-768.1985

Ontogeny of macrophage-mediated protection against Listeria monocytogenes.

R Ohara, M Mitsuyama, M Miyata, K Nomoto
PMCID: PMC261256  PMID: 3997246

Abstract

We investigated the ontogenic development of macrophage functions which are important in the expression of host defense against infection by Listeria monocytogenes. Macrophage functions, including accumulation in response to local stimuli, chemotaxis in vitro, and intracellular killing, as well as number of macrophages, were examined by using mice 1, 2, 3, 4, and 8 weeks old. The number of peritoneal macrophages was extremely low in younger mice even when their body weights were taken into consideration. Macrophage accumulation in response to infectious stimulus with viable listeria was poor in younger mice and showed an age-dependent development. In younger groups, chemotaxis in vitro was as immature as chemotaxis in vivo. In 1- and 2-week-old mice, macrophages did not show any intracellular killing activity against L. monocytogenes, but killing was observed in mice over 3 weeks of age. These functions developed in an age-dependent manner and reached the 8-week-old adult level after the mice were 4 weeks of age. In adult mice, these macrophage functions were shown to be enhanced after immunization with viable listeria; however, such an immunization-induced enhancement was very poor in the younger groups of mice. Protection judged by mortality and in vivo bacterial growth was weaker in the younger groups against both primary and secondary challenges. In vivo protection against L. monocytogenes seemed to develop in the same age-dependent manner as the development of macrophage functions. These results indicate that age-dependent immaturity of macrophage functions mainly comprises the age-dependent immaturity of protection against L. monocytogenes.

Full text

PDF
765

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Argyris B. F. Role of macrophages in immunological maturation. J Exp Med. 1968 Sep 1;128(3):459–467. doi: 10.1084/jem.128.3.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bortolussi R., Ferrier P. Protection against Escherichia coli K1 infection in newborn rats by antibody to K1 capsular polysaccharide antigen. Infect Immun. 1980 Apr;28(1):111–117. doi: 10.1128/iai.28.1.111-117.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bortolussi R., Ferrieri P., Wannamaker L. W. Dynamics of Escherichia coli infection and meningitis in infant rats. Infect Immun. 1978 Nov;22(2):480–485. doi: 10.1128/iai.22.2.480-485.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boumsell L., Meltzer M. S. Mouse mononuclear cell chemotaxis. I. Differential response of monocytes and macrophages. J Immunol. 1975 Dec;115(6):1746–1748. [PubMed] [Google Scholar]
  5. Burakoff S. J., Finberg R., Glimcher L., Lemonnier F., Benacerraf B., Cantor H. The biologic significance of alloreactivity. The ontogeny of T-cell sets specific for alloantigens or modified self antigens. J Exp Med. 1978 Nov 1;148(5):1414–1422. doi: 10.1084/jem.148.5.1414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chiscon M. Q., Golub E. S. Functional development of the interacting cells in the immune response. I. Development of T cell and B cell function. J Immunol. 1972 May;108(5):1379–1386. [PubMed] [Google Scholar]
  7. Costello R. T., Izumi T., Sakurami T. Behavior of attenuated mycobacteria in organs of neonatal and adult mice. J Exp Med. 1971 Aug 1;134(2):366–380. doi: 10.1084/jem.134.2.366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fowles R. E., Fajardo I. M., Leibowitch J. L., David J. R. The enhancement of macrophage bacteriostasis by products of activated lymphocytes. J Exp Med. 1973 Oct 1;138(4):952–964. doi: 10.1084/jem.138.4.952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hardy B., Globerson A., Danon D. Ontogenic development of the reactivity of macrophages to antigenic stimulation. Cell Immunol. 1973 Nov;9(2):282–288. doi: 10.1016/0008-8749(73)90079-8. [DOI] [PubMed] [Google Scholar]
  10. Hirsch M. S., Zisman B., Allison A. C. Macrophages and age-dependent resistance to Herpes simplex virus in mice. J Immunol. 1970 May;104(5):1160–1165. [PubMed] [Google Scholar]
  11. Lu C. Y., Calamai E. G., Unanue E. R. A defect in the antigen-presenting function of macrophages from neonatal mice. Nature. 1979 Nov 15;282(5736):327–329. doi: 10.1038/282327a0. [DOI] [PubMed] [Google Scholar]
  12. Lu C. Y., Unanue E. R. Ontogeny of murine macrophages: functions related to antigen presentation. Infect Immun. 1982 Apr;36(1):169–175. doi: 10.1128/iai.36.1.169-175.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. MACKANESS G. B. THE IMMUNOLOGICAL BASIS OF ACQUIRED CELLULAR RESISTANCE. J Exp Med. 1964 Jul 1;120:105–120. doi: 10.1084/jem.120.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. MIKI K., MACKANESS G. B. THE PASSIVE TRANSFER OF ACQUIRED RESISTANCE TO LISTERIA MONOCYTOGENES. J Exp Med. 1964 Jul 1;120:93–103. doi: 10.1084/jem.120.1.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mackaness G. B. The influence of immunologically committed lymphoid cells on macrophage activity in vivo. J Exp Med. 1969 May 1;129(5):973–992. doi: 10.1084/jem.129.5.973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mitsuyama M., Takeya K., Nomoto K., Shimotori S. Three phases of phagocyte contribution to resistance against Listeria monocytogenes. J Gen Microbiol. 1978 May;106(1):165–171. doi: 10.1099/00221287-106-1-165. [DOI] [PubMed] [Google Scholar]
  17. Miyata M., Mitsuyama M., Ogata N., Nomoto K. Protective mechanisms against infection by Listeria monocytogenes: accumulation and activation of macrophages. J Clin Lab Immunol. 1984 Mar;13(3):111–115. [PubMed] [Google Scholar]
  18. Miyata M., Mitsuyama M., Ogata N., Nomoto K., Takeya K. Two steps in the generation of acquired cellular resistance against Listeria monocytogenes: accumulation and activation of macrophages. Immunology. 1982 Oct;47(2):247–253. [PMC free article] [PubMed] [Google Scholar]
  19. NICOL T., BILBEY D. L., CHARLES L. M., CORDINGLEY J. L., VERNON-ROBERTS B. OESTROGEN: THE NATURAL STIMULANT OF BODY DEFENCE. J Endocrinol. 1964 Oct;30:277–291. doi: 10.1677/joe.0.0300277. [DOI] [PubMed] [Google Scholar]
  20. Rao G. R., Rawls W. E., Perey D. Y., Tompkins W. A. Macrophage activation in congenitally athymic mice raised under conventional or germ-free conditions. J Reticuloendothel Soc. 1977 Jan;21(1):13–20. [PubMed] [Google Scholar]
  21. Stevenson M. M., Kongshavn P. A., Skamene E. Genetic linkage of resistance to Listeria monocytogenes with macrophage inflammatory responses. J Immunol. 1981 Aug;127(2):402–407. [PubMed] [Google Scholar]
  22. Taniguchi T. [Immunobiological characteristics of germfree mice (author's transl)]. Fukuoka Igaku Zasshi. 1978 Feb;69(2):23–36. [PubMed] [Google Scholar]
  23. Tardieu M., Héry C., Dupuy J. M. Neonatal susceptibility to MHV3 infection in mice. II. Role of natural effector marrow cells in transfer of resistance. J Immunol. 1980 Jan;124(1):418–423. [PubMed] [Google Scholar]
  24. Tatsukawa K., Mitsuyama M., Takeya K., Nomoto K. Differing contribution of polymorphonuclear cells and macrophages to protection of mice against Listeria monocytogenes and Pseudomonas aeruginosa. J Gen Microbiol. 1979 Nov;115(1):161–166. doi: 10.1099/00221287-115-1-161. [DOI] [PubMed] [Google Scholar]
  25. Trejo R. A., Loose L. D., Di Luzio N. R. Influence of diethylstilbestrol (DES) on reticuloendothelial function, tissue distribution, and detoxication of S. enteritidis endotoxin. J Reticuloendothel Soc. 1972 Jan;11(1):88–97. [PubMed] [Google Scholar]
  26. Ward P. A. Chemotoxis of mononuclear cells. J Exp Med. 1968 Nov 1;128(5):1201–1221. doi: 10.1084/jem.128.5.1201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yang H. Y., Skinsnes O. K. Peritoneal macrophage response in neonatal mice. J Reticuloendothel Soc. 1973 Aug;14(2):181–191. [PubMed] [Google Scholar]
  28. Zeligs B. J., Nerurkar L. S., Bellanti J. A. Maturation of the rabbit alveolar macrophage during animal development. III. Phagocytic and bactericidal functions. Pediatr Res. 1977 Dec;11(12):1208–1211. doi: 10.1203/00006450-197712000-00008. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES