Induction of Lethal Shock and Tolerance by Porphyromonas Gingivalis Lipopolysaccharide in D-galactosamine-sensitized C3H/HeJ Mice

Overview

Journal Infect Immun

Publisher American Society for Microbiology

Specialty Allergy & Immunology

Date 1999 Jun 22

PMID 10377118

Citations 2

Authors

K Tanamoto

Affiliations

Soon will be listed here.

Abstract

Lipopolysaccharide (LPS) obtained from Porphyromonas gingivalis was found to exhibit marked lethal toxicity in galactosamine-sensitized C3H/HeJ mice. Although no lethality was observed in mice intraperitoneally challenged with 1 mg of P. gingivalis LPS without galactosamine, when they were sensitized with 30 mg of galactosamine, challenge with 1 and 10 micrograms of LPS resulted in 67 and 100% lethality, respectively. The lethal dose of LPS was almost the same in LPS-responsive C57BL/6 mice and non-LPS-responsive C3H/HeJ mice. Furthermore, when 1 microgram of P. gingivalis LPS was administered to each mouse 90 min before the challenge with the same LPS with galactosamine, tolerance to the lethal action of LPS was induced, and the mice were completely protected from death, even at a dose 100-fold greater than the lethal dose of LPS. Neither a lethal effect nor induction of tolerance to the lethality of P. gingivalis LPS was exhibited by Salmonella LPS in galactosamine-sensitized C3H/HeJ mice. A protein-LPS complex derived from Pseudomonas aeruginosa, which exhibited strong lethality and induced tolerance to a subsequent challenge with a lethal dose of LPS in galactosamine-sensitized LPS-responsive mice, did not exhibit lethal toxicity in galactosamine-sensitized C3H/HeJ mice and failed to induce tolerance in these mice to the lethality of P. gingivalis LPS. These results indicate that P. gingivalis LPS plays the central role in the activation of non-LPS-responsive C3H/HeJ mice.

Citing Articles

Lethal effect and apoptotic DNA fragmentation in response of D-GalN-treated mice to bacterial LPS can be suppressed by pre-exposure to minute amount of bacterial LPS: dual role of TNF receptor 1.

Zhou B, Gumenscheimer M, Freudenberg M, Galanos C World J Gastroenterol. 2005; 11(22):3398-404.

PMID: 15948245 PMC: 4315994. DOI: 10.3748/wjg.v11.i22.3398.

Biological properties of lipid A isolated from Flavobacterium meningosepticum.

Tanamoto K, Kato H, Haishima Y, Azumi S Clin Diagn Lab Immunol. 2001; 8(3):522-7.

PMID: 11329451 PMC: 96094. DOI: 10.1128/CDLI.8.3.522-527.2001.

References

Medzhitov R, Preston-Hurlburt P, Janeway Jr C . A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature. 1997; 388(6640):394-7. DOI: 10.1038/41131. View

Tanamoto K . Predominant role of the substituents on the hydroxyl groups of 3-hydroxy fatty acids of non-reducing glucosamine in lipid A for the endotoxic and antagonistic activity. FEBS Lett. 1994; 351(3):325-9. DOI: 10.1016/0014-5793(94)00857-4. View

Freudenberg M, Salomao R, Sing A, Mitov I, Galanos C . Reconciling the concepts of endotoxin sensitization and tolerance. Prog Clin Biol Res. 1998; 397:261-8. View

Yang R, Mark M, Gray A, Huang A, Xie M, Zhang M . Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature. 1998; 395(6699):284-8. DOI: 10.1038/26239. View

Kumada H, Haishima Y, Umemoto T, Tanamoto K . Structural study on the free lipid A isolated from lipopolysaccharide of Porphyromonas gingivalis. J Bacteriol. 1995; 177(8):2098-106. PMC: 176854. DOI: 10.1128/jb.177.8.2098-2106.1995. View

Tanamoto K, Azumi S, Haishima Y, Kumada H, Umemoto T . Endotoxic properties of free lipid A from Porphyromonas gingivalis. Microbiology (Reading). 1997; 143 ( Pt 1):63-71. DOI: 10.1099/00221287-143-1-63. View

Tanamoto K, Azumi S, Haishima Y, Kumada H, Umemoto T . The lipid A moiety of Porphyromonas gingivalis lipopolysaccharide specifically mediates the activation of C3H/HeJ mice. J Immunol. 1997; 158(9):4430-6. View

Poltorak A, He X, Smirnova I, Liu M, Van Huffel C, Du X . Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998; 282(5396):2085-8. DOI: 10.1126/science.282.5396.2085. View

CHEDID L, Parant M, Damais C, Parant F, Juy D, Galelli A . Failure of endotoxin to increase nonspecific resistance to infection of lipopolysaccharide low-responder mice. Infect Immun. 1976; 13(3):722-7. PMC: 420669. DOI: 10.1128/iai.13.3.722-727.1976. View

10.

SULTZER B, Goodman G . Endotoxin protein: a B-cell mitogen and polyclonal activator of C3H/HeJ lymphocytes. J Exp Med. 1976; 144(3):821-7. PMC: 2190414. DOI: 10.1084/jem.144.3.821. View

11.

Morrison D, Betz S, Jacobs D . Isolation of a lipid A bound polypeptide responsible for "LPS-initiated" mitogenesis of C3H/HeJ spleen cells. J Exp Med. 1976; 144(3):840-6. PMC: 2190404. DOI: 10.1084/jem.144.3.840. View

12.

Abe C, Tanamoto K, HOMMA J . Infection protective property of the common antigen (OEP) of Pseudomonas aeruginosa and its chemical composition. Jpn J Exp Med. 1977; 47(5):393-402. View

13.

Tanamoto K, Abe C, Homma Y, KURETANI K, Hoshi A, Kojima Y . A compound possessing antitumor and interferon-inducing activities derived from the common antigen (OEP) of Pseudomonas aeruginosa. J Biochem. 1978; 83(3):711-8. DOI: 10.1093/oxfordjournals.jbchem.a131964. View

14.

Tanamoto K, Abe C, HOMMA J, Kojima Y . Regions of the lipopolysaccharide of Pseudomonas aeruginosa essential for antitumor and interferon-inducing activities. Eur J Biochem. 1979; 97(2):623-9. DOI: 10.1111/j.1432-1033.1979.tb13152.x. View

15.

Galanos C, Freudenberg M, REUTTER W . Galactosamine-induced sensitization to the lethal effects of endotoxin. Proc Natl Acad Sci U S A. 1979; 76(11):5939-43. PMC: 411768. DOI: 10.1073/pnas.76.11.5939. View

16.

Galanos C, Lehmann V, LUDERITZ O, Rietschel E, Westphal O, Brade H . Endotoxic properties of chemically synthesized lipid A part structures. Comparison of synthetic lipid A precursor and synthetic analogues with biosynthetic lipid A precursor and free lipid A. Eur J Biochem. 1984; 140(2):221-7. DOI: 10.1111/j.1432-1033.1984.tb08090.x. View

17.

Hogan M, Vogel S . Lipid A-associated proteins provide an alternate "second signal" in the activation of recombinant interferon-gamma-primed, C3H/HeJ macrophages to a fully tumoricidal state. J Immunol. 1987; 139(11):3697-702. View

18.

Freudenberg M, Galanos C . Induction of tolerance to lipopolysaccharide (LPS)-D-galactosamine lethality by pretreatment with LPS is mediated by macrophages. Infect Immun. 1988; 56(5):1352-7. PMC: 259829. DOI: 10.1128/iai.56.5.1352-1357.1988. View

19.

Loppnow H, Brade H, Durrbaum I, Dinarello C, Kusumoto S, Rietschel E . IL-1 induction-capacity of defined lipopolysaccharide partial structures. J Immunol. 1989; 142(9):3229-38. View

20.

Schifferle R, Reddy M, Zambon J, Genco R, LeVine M . Characterization of a polysaccharide antigen from Bacteroides gingivalis. J Immunol. 1989; 143(9):3035-42. View