Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1968 Jun 1;127(6):1087–1107. doi: 10.1084/jem.127.6.1087

THE PRIMARY IMMUNE RESPONSE IN MICE

I. THE ENHANCEMENT AND SUPPRESSION OF HEMOLYSIN PRODUCTION BY A BACTERIAL ENDOTOXIN

Robert E Franzl 1, Philip D McMaster 1
PMCID: PMC2138497  PMID: 5653220

Abstract

The manner in which a single injection of S. typhosa endotoxin effects the primary hemolysin response to sheep erythrocytes in the mouse has been shown to depend on the dosage, route, and time of administration of the endotoxin, as well as on the route employed for the injection of antigen. The normal production of antibody, following an intravenous or an intraperitoneal injection of red blood cells, is suppressed if the bacterial lipopolysaccharide is given before and by the same route as the antigen. The response to an intraperitoneal injection of sheep red cells is also inhibited if preceded by an intravenous injection of endotoxin. By contrast, hemolysin formation to intravenous antigen is enhanced considerably by a previous intraperitoneal injection of endotoxin, and the response both to intravenous and to intraperitoneal injections of the antigen increases if the endotoxin is given by the same route either simultaneously or shortly after the foreign red cells. These findings are discussed in regard to the physiological action of bacterial endotoxins and the early events in antibody formation.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. AMIEL J. L., MATHE G., MATSUKURA M., MERY A. M., DAGUET G., TENENBAUM R., GARATTINI S., BREZIN C., PALMA V. TESTS FOR THE DETERMINATION OF THE EFFECT OF ANTIMITOTIC PRODUCTS ON IMMUNE REACTIONS. Immunology. 1964 Sep;7:511–526. [PMC free article] [PubMed] [Google Scholar]
  2. BENACERRAF B., SEBESTYEN M. M. Effect of bacterial endotoxins on the reticuloendothelial system. Fed Proc. 1957 Sep;16(3):860–867. [PubMed] [Google Scholar]
  3. BIOZZI G., BENACERRAF B., HALPERN B. N. The effect of Salm. typhi and its endotoxin on the phagocytic activity of the reticuloendothelial system in mice. Br J Exp Pathol. 1955 Jun;36(3):226–235. [PMC free article] [PubMed] [Google Scholar]
  4. BRADLEY S. G., WATSON D. W. SUPPRESSION BY ENDOTOXIN OF THE IMMUNE RESPONSE TO ACTINOPHAGE IN THE MOUSE. Proc Soc Exp Biol Med. 1964 Nov;117:570–572. doi: 10.3181/00379727-117-29640. [DOI] [PubMed] [Google Scholar]
  5. CONDIE R. M., GOOD R. A. Inhibition of immunological enhancement by endotoxin in refractory rabbits; immunochemical study. Proc Soc Exp Biol Med. 1956 Mar;91(3):414–418. doi: 10.3181/00379727-91-22280. [DOI] [PubMed] [Google Scholar]
  6. CUTLER J. L. The enhancement of hemolysin production in the rat by Zymosan. J Immunol. 1960 Apr;84:416–419. [PubMed] [Google Scholar]
  7. DILUZIO N. R., WOOLES W. R. DEPRESSION OF PHAGOCYTIC ACTIVITY AND IMMUNE RESPONSE BY METHYL PALMITATE. Am J Physiol. 1964 May;206:939–943. doi: 10.1152/ajplegacy.1964.206.5.939. [DOI] [PubMed] [Google Scholar]
  8. DIXON F. J., TALMAGE D. W., MAURER P. H., DEICHMILLER M. The half-life on homologous gamma globulin (antibody) in several species. J Exp Med. 1952 May;95(5):313–318. doi: 10.1084/jem.96.4.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. DUBOS R. J., SCHAEDLER R. W. The effect of the intestinal flora on the growth rate of mice, and on their susceptibility to experimental infections. J Exp Med. 1960 Mar 1;111:407–417. doi: 10.1084/jem.111.3.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. FREEDMAN H. H., SULTZER B. M. OPPOSITE CHANGES IN PHAGOCYTIC ACTIVITY INDUCED BY TWO ENDOTOXINS. J Reticuloendothel Soc. 1964 Jul;1:216–223. [PubMed] [Google Scholar]
  11. FRUHMAN G. J. Mobilization of neutrophils into peritoneal fluid following intraperitoneal injection of bacterial endotoxins. Proc Soc Exp Biol Med. 1959 Nov;102:423–425. doi: 10.3181/00379727-102-25272. [DOI] [PubMed] [Google Scholar]
  12. HALPERN B. N., BIOZZI G., BENACERRAF B., STIFFEL C. Phagocytosis of foreign red blood cells by the reticulo-endothelial system. Am J Physiol. 1957 Jun;189(3):520–526. doi: 10.1152/ajplegacy.1957.189.3.520. [DOI] [PubMed] [Google Scholar]
  13. HALPERN B. N. The role and function of the reticulo-endothelial system in immunological processes. J Pharm Pharmacol. 1959 Jun;11(6):321–338. doi: 10.1111/j.2042-7158.1959.tb12560.x. [DOI] [PubMed] [Google Scholar]
  14. HERION J. C., WALKER R. I., HERRING W. B., PALMER J. G. EFFECTS OF ENDOTOXIN AND NITROGEN MUSTARD ON LEUKOCYTE KINETICS. Blood. 1965 Apr;25:522–540. [PubMed] [Google Scholar]
  15. HOOK E. W., WAGNER R. R. The resistance-promoting activity of endotoxins and other microbial products. I. Their effect on Salmonella typhosa infections of mice. J Immunol. 1959 Sep;83:302–309. [PubMed] [Google Scholar]
  16. HOWARD J. G. Activation of the reticulo-endothelial cells of the mouse liver by bacterial lipopolysaccharide. J Pathol Bacteriol. 1959 Oct;78:465–470. doi: 10.1002/path.1700780212. [DOI] [PubMed] [Google Scholar]
  17. HOWARD J. G., ROWLEY D., WARDLAW A. C. Investigations on the mechanism of stimulation of non-specific immunity by bacterial lipopolysaccharides. Immunology. 1958 Jul;1(3):181–203. [PMC free article] [PubMed] [Google Scholar]
  18. Heilman D. H. In vitro studies on changes in the reticuloendothelial system of rabbits after an injection of endotoxin. J Reticuloendothel Soc. 1965 Jul;2(2):89–104. [PubMed] [Google Scholar]
  19. JOHNSON A. G., GAINES S., LANDY M. Studies on the O antigen of Salmonella typhosa. V. Enhancement of antibody response to protein antigens by the purified lipopolysaccharide. J Exp Med. 1956 Feb 1;103(2):225–246. doi: 10.1084/jem.103.2.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. JOHNSON A. G., NOWOTNY A. RELATIONSHIP OF STRUCTURE TO FUNCTION IN BACTERIAL O ANTIGENS. III. BIOLOGICAL PROPERTIES OF ENDOTOXOIDS. J Bacteriol. 1964 Apr;87:809–814. doi: 10.1128/jb.87.4.809-814.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. KIND P., JOHNSON A. G. Studies on the adjuvant action of bacterial endotoxins on antibody formation. I. Time limitation of enhancing effect and restoration of antibody formation in x-irradiated rabbits. J Immunol. 1959 May;82(5):415–427. [PubMed] [Google Scholar]
  22. LUECKE D. H., SIBAL L. R. Enhancement by endotoxin of the primary antibody response to bovine serum albumin in chickens. J Immunol. 1962 Oct;89:539–544. [PubMed] [Google Scholar]
  23. MERRITT K., JOHNSON A. G. STUDIES ON THE ADJUVANT ACTION OF BACTERIAL ENDOTOXINS ON ANTIBODY FORMATION. V. THE INFLUENCE OF ENDOTOXIN AND 5-FLUORO-2-DEOXYURIDINE ON THE PRIMARY ANTIBODY RESPONSE OF THE BALB MOUSE TO A PURIFIED PROTEIN ANTIGEN. J Immunol. 1963 Aug;91:266–272. [PubMed] [Google Scholar]
  24. MERRITT K., JOHNSON A. G. STUDIES ON THE ADJUVANT ACTION OF BACTERIAL ENDOTOXINS ON ANTIBODY FORMATION. VI. ENHANCEMENT OF ANTIBODY FORMATION BY NUCLEIC ACIDS. J Immunol. 1965 Mar;94:416–422. [PubMed] [Google Scholar]
  25. Makinodan T., Albright J. F., Perkins E. H., Nettesheim P. Suppression of immunologic responses. Med Clin North Am. 1965 Nov;49(6):1569–1596. doi: 10.1016/s0025-7125(16)33247-3. [DOI] [PubMed] [Google Scholar]
  26. McMaster P. D., Franzl R. E. The primary immune response in mice. II. Cellular responses of lymphoid tissue accompanying the enhancement or complete suppression of antibody formation by a bacterial endotoxin. J Exp Med. 1968 Jun 1;127(6):1109–1125. doi: 10.1084/jem.127.6.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Michael J. G. The release of specific bactericidal antibodies by endotoxin. J Exp Med. 1966 Feb 1;123(2):205–212. doi: 10.1084/jem.123.2.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. NATHAN H. C., BIEBER S., ELION G. B., HITCHINGS G. H. Detection of agents which interfere with the immune response. Proc Soc Exp Biol Med. 1961 Aug-Sep;107:796–799. doi: 10.3181/00379727-107-26758. [DOI] [PubMed] [Google Scholar]
  29. NOYES H. E., McINTURF C. R., BLAHUTA G. J. Studies on distribution of Escherichia coli endotoxin in mice. Proc Soc Exp Biol Med. 1959 Jan;100(1):65–68. doi: 10.3181/00379727-100-24525. [DOI] [PubMed] [Google Scholar]
  30. RIBI E., MILNER K. C., PERRINE T. D. Endotoxic and antigenic fractions from the cell wall of Salmonella enteritidis; methods for separation and some biologic activities. J Immunol. 1959 Jan;82(1):75–84. [PubMed] [Google Scholar]
  31. ROBERTS K. B. Antibody formation in the omentum. Br J Exp Pathol. 1955 Aug;36(4):357–362. [PMC free article] [PubMed] [Google Scholar]
  32. ROWLANDS D. T., Jr, CLAMAN H. N., KIND P. D. THE EFFECT OF ENDOTOXIN ON THE THYMUS OF YOUNG MICE. Am J Pathol. 1965 Feb;46:165–176. [PMC free article] [PubMed] [Google Scholar]
  33. ROWLEY D. A. The effect of splenectomy on the formation of circulating antibody in the adult male albino rat. J Immunol. 1950 Apr;64(4):289–295. [PubMed] [Google Scholar]
  34. STUART A. E., DAVIDSON A. E. EFFECT OF SIMPLE LIPIDS ON ANTIBODY FORMATION AFTER INJECTION OF FOREIGN RED CELLS. J Pathol Bacteriol. 1964 Apr;87:305–316. doi: 10.1002/path.1700870210. [DOI] [PubMed] [Google Scholar]
  35. SULTZER B. M., FREEDMAN H. H. The stimulation of non-specific host resistance to infection by chemically modified endotoxin. J Exp Med. 1962 Dec 1;116:943–956. doi: 10.1084/jem.116.6.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schwartz R. S. Specificity of immunosuppression by antimetabolites. Fed Proc. 1966 Jan-Feb;25(1):165–168. [PubMed] [Google Scholar]
  37. TALIAFERRO W. H., TALIAFERRO L. G. The dynamics of hemolysin formation in intact and splenectomized rabbits. J Infect Dis. 1950 Jul-Aug;87(1):37–62. doi: 10.1093/infdis/87.1.37. [DOI] [PubMed] [Google Scholar]
  38. THORBECKE G. J., BENACERRAF B. The reticulo-endothelial system and immunological phenomena. Prog Allergy. 1962;6:559–598. [PubMed] [Google Scholar]
  39. UCHITEL I. Y., KHASMAN E. L. ON THE MECHANISM OF ADJUVANT ACTION OF NONSPECIFIC STIMULATORS OF ANTIBODY FORMATION. J Immunol. 1965 Apr;94:492–497. [PubMed] [Google Scholar]
  40. WARD P. A., JOHNSON A. G., ABELL M. R. Studies on the adjuvant action of bacterial endotoxins on antibody formation. III. Histologic response of the rabbit spleen to a single injection of a purified protein antigen. J Exp Med. 1959 May 1;109(5):463–474. doi: 10.1084/jem.109.5.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. WEBSTER M. E., SAGIN J. F., LANDY M., JOHNSON A. G. Studies on the O antigen of Salmonella typhosa. I. Purification of the antigen. J Immunol. 1955 Jun;74(6):455–465. [PubMed] [Google Scholar]
  42. WIZNITZER T., BETTER N., RACHLIN W., ATKINS N., FRANK E. D., FINE J. In vivo detoxification of endotoxin by the reticuloendothelial system. J Exp Med. 1960 Dec 1;112:1157–1166. doi: 10.1084/jem.112.6.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. WOODS M. W., LANDY M., WHITBY J. L., BURK D. Symposium on bacterial endotoxins. III. Metabolic effects of endotoxins on mammalian cells. Bacteriol Rev. 1961 Dec;25:447–456. doi: 10.1128/br.25.4.447-456.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. WOOLES W. R., DILUZIO N. R. RETICULOENDOTHELIAL FUNCTION AND THE IMMUNE RESPONSE. Science. 1963 Nov 22;142(3595):1078–1080. doi: 10.1126/science.142.3595.1078. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES