Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1997 Sep;65(9):3713–3718. doi: 10.1128/iai.65.9.3713-3718.1997

Release of tumor necrosis factor alpha in response to Vibrio vulnificus capsular polysaccharide in in vivo and in vitro models.

J L Powell 1, A C Wright 1, S S Wasserman 1, D M Hone 1, J G Morris Jr 1
PMCID: PMC175529  PMID: 9284142

Abstract

Vibrio vulnificus produces a severe septic shock syndrome in susceptible individuals. Virulence of the bacterium has been closely linked to the presence of a surface-exposed acidic capsular polysaccharide (CPS). To investigate whether CPS plays an additional role in pathogenesis by modulating inflammatory-associated cytokine production, studies were initiated in a mouse model and followed by investigations of cytokine release from human peripheral blood mononuclear cells (PBMCs). Mouse tumor necrosis factor alpha (TNF-alpha) could be detected in serum up to 12 h postinoculation in animals challenged with the encapsulated parent strain MO6-24/O. The unencapsulated strain CVD752 was quickly eliminated by the animals, thus preventing a direct association between serum TNF-alpha levels and the presence or absence of the CPS. Purified CPS from MO6-24/O when injected into D-galactosamine-sensitized mice was a more immediate inducer of TNF-alpha than an equivalent quantity of MO6-24/O lipopolysaccharide (LPS). Both V. vulnificus CPS and V. vulnificus LPS induced inflammation-associated cytokine responses from primary human PBMCs in vitro. CPS elicited TNF-alpha from PBMCs in a dose-dependent manner, with maximal induction at 6 to 10 h, and was not inhibited by polymyxin B. Expression of interleukin-6 (IL-6) mRNAs was also induced in the presence of CPS. Interestingly, while adherent PBMCs secreted high levels of TNF-alpha after stimulation with LPS, they secreted little TNF-alpha in response to CPS. These studies provide evidence that V. vulnificus CPS directly stimulates the expression and secretion of proinflammatory cytokines by murine and human cells and suggest that CPS activation of PBMCs operates through a cellular mechanism distinct from that of LPS.

Full Text

The Full Text of this article is available as a PDF (413.4 KB).

Selected References

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

  1. Bahrani K. F., Oliver J. D. Electrophoretic analysis of lipopolysaccharide isolated from opaque and translucent colony variants of Vibrio vulnificus using various extraction methods. Microbios. 1991;66(267):83–93. [PubMed] [Google Scholar]
  2. Bahrani K., Oliver J. D. Studies on the lipopolysaccharide of a virulent and an avirulent strain of Vibrio vulnificus. Biochem Cell Biol. 1990 Feb;68(2):547–551. doi: 10.1139/o90-078. [DOI] [PubMed] [Google Scholar]
  3. Benabdelmoumene S., Dumont S., Petit C., Poindron P., Wachsmann D., Klein J. P. Activation of human monocytes by Streptococcus mutans serotype f polysaccharide: immunoglobulin G Fc receptor expression and tumor necrosis factor and interleukin-1 production. Infect Immun. 1991 Sep;59(9):3261–3266. doi: 10.1128/iai.59.9.3261-3266.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blake P. A., Merson M. H., Weaver R. E., Hollis D. G., Heublein P. C. Disease caused by a marine Vibrio. Clinical characteristics and epidemiology. N Engl J Med. 1979 Jan 4;300(1):1–5. doi: 10.1056/NEJM197901043000101. [DOI] [PubMed] [Google Scholar]
  5. Devi S. J., Hayat U., Frasch C. E., Kreger A. S., Morris J. G., Jr Capsular polysaccharide-protein conjugate vaccines of carbotype 1 Vibrio vulnificus: construction, immunogenicity, and protective efficacy in a murine model. Infect Immun. 1995 Aug;63(8):2906–2911. doi: 10.1128/iai.63.8.2906-2911.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Devi S. J., Hayat U., Powell J. L., Morris J. G., Jr Preclinical immunoprophylactic and immunotherapeutic efficacy of antisera to capsular polysaccharide-tetanus toxoid conjugate vaccines of Vibrio vulnificus. Infect Immun. 1996 Jun;64(6):2220–2224. doi: 10.1128/iai.64.6.2220-2224.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Espat N. J., Auffenberg T., Abouhamze A., Baumhofer J., Moldawer L. L., Howard R. J. A role for tumor necrosis factor-alpha in the increased mortality associated with Vibrio vulnificus infection in the presence of hepatic dysfunction. Ann Surg. 1996 Apr;223(4):428–433. doi: 10.1097/00000658-199604000-00012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Espevik T., Otterlei M., Skjåk-Braek G., Ryan L., Wright S. D., Sundan A. The involvement of CD14 in stimulation of cytokine production by uronic acid polymers. Eur J Immunol. 1993 Jan;23(1):255–261. doi: 10.1002/eji.1830230140. [DOI] [PubMed] [Google Scholar]
  9. Gray L. D., Kreger A. S. Purification and characterization of an extracellular cytolysin produced by Vibrio vulnificus. Infect Immun. 1985 Apr;48(1):62–72. doi: 10.1128/iai.48.1.62-72.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Henderson B., Poole S., Wilson M. Bacterial modulins: a novel class of virulence factors which cause host tissue pathology by inducing cytokine synthesis. Microbiol Rev. 1996 Jun;60(2):316–341. doi: 10.1128/mr.60.2.316-341.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Klontz K. C., Lieb S., Schreiber M., Janowski H. T., Baldy L. M., Gunn R. A. Syndromes of Vibrio vulnificus infections. Clinical and epidemiologic features in Florida cases, 1981-1987. Ann Intern Med. 1988 Aug 15;109(4):318–323. doi: 10.7326/0003-4819-109-4-318. [DOI] [PubMed] [Google Scholar]
  12. Kothary M. H., Kreger A. S. Purification and characterization of an elastolytic protease of Vibrio vulnificus. J Gen Microbiol. 1987 Jul;133(7):1783–1791. doi: 10.1099/00221287-133-7-1783. [DOI] [PubMed] [Google Scholar]
  13. Kreger A., DeChatelet L., Shirley P. Interaction of Vibrio vulnificus with human polymorphonuclear leukocytes: association of virulence with resistance to phagocytosis. J Infect Dis. 1981 Sep;144(3):244–248. doi: 10.1093/infdis/144.3.244. [DOI] [PubMed] [Google Scholar]
  14. Lagoo-Deenadayalan S., Lagoo A. S., Barber W. H., Hardy K. J. A standardized approach to PCR-based semiquantitation of multiple cytokine gene transcripts from small cell samples. Lymphokine Cytokine Res. 1993 Apr;12(2):59–67. [PubMed] [Google Scholar]
  15. Litwin C. M., Rayback T. W., Skinner J. Role of catechol siderophore synthesis in Vibrio vulnificus virulence. Infect Immun. 1996 Jul;64(7):2834–2838. doi: 10.1128/iai.64.7.2834-2838.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mancuso G., Tomasello F., von Hunolstein C., Orefici G., Teti G. Induction of tumor necrosis factor alpha by the group- and type-specific polysaccharides from type III group B streptococci. Infect Immun. 1994 Jul;62(7):2748–2753. doi: 10.1128/iai.62.7.2748-2753.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. McPherson V. L., Watts J. A., Simpson L. M., Oliver J. D. Physiological effects of the lipopolysaccharide of Vibrio vulnificus on mice and rats. Microbios. 1991;67(272-273):141–149. [PubMed] [Google Scholar]
  18. Mond J. J., Lees A., Snapper C. M. T cell-independent antigens type 2. Annu Rev Immunol. 1995;13:655–692. doi: 10.1146/annurev.iy.13.040195.003255. [DOI] [PubMed] [Google Scholar]
  19. Onderdonk A. B., Markham R. B., Zaleznik D. F., Cisneros R. L., Kasper D. L. Evidence for T cell-dependent immunity to Bacteroides fragilis in an intraabdominal abscess model. J Clin Invest. 1982 Jan;69(1):9–16. doi: 10.1172/JCI110445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pantosti A., Tzianabos A. O., Onderdonk A. B., Kasper D. L. Immunochemical characterization of two surface polysaccharides of Bacteroides fragilis. Infect Immun. 1991 Jun;59(6):2075–2082. doi: 10.1128/iai.59.6.2075-2082.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Reddy G. P., Hayat U., Abeygunawardana C., Fox C., Wright A. C., Maneval D. R., Jr, Bush C. A., Morris J. G., Jr Purification and determination of the structure of capsular polysaccharide of Vibrio vulnificus M06-24. J Bacteriol. 1992 Apr;174(8):2620–2630. doi: 10.1128/jb.174.8.2620-2630.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Reddy G. P., Hayat U., Bush C. A., Morris J. G., Jr Capsular polysaccharide structure of a clinical isolate of Vibrio vulnificus strain BO62316 determined by heteronuclear NMR spectroscopy and high-performance anion-exchange chromatography. Anal Biochem. 1993 Oct;214(1):106–115. doi: 10.1006/abio.1993.1463. [DOI] [PubMed] [Google Scholar]
  23. Salgado A., Bóveda J. L., Monasterio J., Segura R. M., Mourelle M., Gómez-Jiménez J., Peracaula R. Inflammatory mediators and their influence on haemostasis. Haemostasis. 1994 Mar-Apr;24(2):132–138. doi: 10.1159/000217093. [DOI] [PubMed] [Google Scholar]
  24. Shapiro M. E., Kasper D. L., Zaleznik D. F., Spriggs S., Onderdonk A. B., Finberg R. W. Cellular control of abscess formation: role of T cells in the regulation of abscesses formed in response to Bacteroides fragilis. J Immunol. 1986 Jul 1;137(1):341–346. [PubMed] [Google Scholar]
  25. Shinoda S., Kobayashi M., Yamada H., Yoshida S., Ogawa M., Mizuguchi Y. Inhibitory effect of capsular antigen of Vibrio vulnificus on bactericidal activity of human serum. Microbiol Immunol. 1987;31(5):393–401. doi: 10.1111/j.1348-0421.1987.tb03102.x. [DOI] [PubMed] [Google Scholar]
  26. Simonson J. G., Siebeling R. J. Immunogenicity of Vibrio vulnificus capsular polysaccharides and polysaccharide-protein conjugates. Infect Immun. 1993 May;61(5):2053–2058. doi: 10.1128/iai.61.5.2053-2058.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Simpson L. M., White V. K., Zane S. F., Oliver J. D. Correlation between virulence and colony morphology in Vibrio vulnificus. Infect Immun. 1987 Jan;55(1):269–272. doi: 10.1128/iai.55.1.269-272.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Simpson S. Q., Singh R., Bice D. E. Heat-killed pneumococci and pneumococcal capsular polysaccharides stimulate tumor necrosis factor-alpha production by murine macrophages. Am J Respir Cell Mol Biol. 1994 Mar;10(3):284–289. doi: 10.1165/ajrcmb.10.3.8117447. [DOI] [PubMed] [Google Scholar]
  29. Soell M., Diab M., Haan-Archipoff G., Beretz A., Herbelin C., Poutrel B., Klein J. P. Capsular polysaccharide types 5 and 8 of Staphylococcus aureus bind specifically to human epithelial (KB) cells, endothelial cells, and monocytes and induce release of cytokines. Infect Immun. 1995 Apr;63(4):1380–1386. doi: 10.1128/iai.63.4.1380-1386.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Soell M., Lett E., Holveck F., Schöller M., Wachsmann D., Klein J. P. Activation of human monocytes by streptococcal rhamnose glucose polymers is mediated by CD14 antigen, and mannan binding protein inhibits TNF-alpha release. J Immunol. 1995 Jan 15;154(2):851–860. [PubMed] [Google Scholar]
  31. Takahashi T., Nishihara T., Ishihara Y., Amano K., Shibuya N., Moro I., Koga T. Murine macrophage interleukin-1 release by capsularlike serotype-specific polysaccharide antigens of Actinobacillus actinomycetemcomitans. Infect Immun. 1991 Jan;59(1):18–23. doi: 10.1128/iai.59.1.18-23.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tzianabos A. O., Onderdonk A. B., Rosner B., Cisneros R. L., Kasper D. L. Structural features of polysaccharides that induce intra-abdominal abscesses. Science. 1993 Oct 15;262(5132):416–419. doi: 10.1126/science.8211161. [DOI] [PubMed] [Google Scholar]
  33. Wright A. C., Simpson L. M., Oliver J. D., Morris J. G., Jr Phenotypic evaluation of acapsular transposon mutants of Vibrio vulnificus. Infect Immun. 1990 Jun;58(6):1769–1773. doi: 10.1128/iai.58.6.1769-1773.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yoshida S., Ogawa M., Mizuguchi Y. Relation of capsular materials and colony opacity to virulence of Vibrio vulnificus. Infect Immun. 1985 Feb;47(2):446–451. doi: 10.1128/iai.47.2.446-451.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES