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PMID: 2040686 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Staphylococcus epidermidis induces complement activation, tumor necrosis factor and interleukin-1, a shock-like state and tissue injury in rabbits without endotoxemia. Comparison to Escherichia coli.

The Journal of clinical investigation ·Vol. 87 ·No. 6 ·1991-06-00 ·Pages 1925-35

Wakabayashi G, Gelfand JA, Jung WK, Connolly RJ, Burke JF, Dinarello CA

Abstract

Tumor necrosis factor (TNF) and IL-1 are thought to mediate many of the pathophysiologic changes of endotoxemia and Gram-negative bacteremia. In these studies, heat-killed Staphylococcus epidermidis were infused into rabbits to determine whether an endotoxin (LPS)-free microorganism also elicits cytokinemia and the physiologic abnormalities seen in Gram-negative bacteremia. S. epidermidis induced complement activation, circulating TNF and IL-1, and hypotension to the same degree as did one-twentieth the number of heat-killed Escherichia coli. Circulating IL-1 beta levels had a greater correlation coefficient (r = 0.81, P less than 0.001) with the degree of hypotension than TNF levels (r = 0.48, P less than 0.02). Leukopenia, thrombocytopenia, diffuse pulmonary capillary aggregation of neutrophils, and hepatic necrosis with neutrophil infiltration were observed to the same extent after either S. epidermidis or E. coli infusion. However, S. epidermidis infusion did not induce significant (less than 60 pg/ml) endotoxemia, whereas E. coli infusion resulted in high (11,000 pg/ml) serum endotoxin levels. S. epidermidis, E. coli, LPS, or S. epidermidis-derived lipoteichoic acid (LTA) induced TNF and IL-1 from blood mononuclear cells in vitro. E. coli organisms and LPS were at least 100-fold more potent than S. epidermidis or LTA. Thus, a shock-like state with similar levels of complement activation as well as circulating levels of IL-1 and TNF were observed following either S. epidermidis or E. coli. These data provide further evidence that host factors such as IL-1 and TNF are common mediators of the septic shock syndrome regardless of the organism.

MeSH Terms
Animals Complement Activation Escherichia coli/immunology,pathogenicity Hemodynamics Interleukin-1/blood Leukocytes, Mononuclear/metabolism Lipopolysaccharides/blood,pharmacology Liver Diseases/microbiology,pathology Necrosis Rabbits Shock/microbiology Staphylococcus epidermidis/immunology,pathogenicity Teichoic Acids/pharmacology Tumor Necrosis Factor-alpha/metabolism
Chemicals
Interleukin-1 Lipopolysaccharides Teichoic Acids Tumor Necrosis Factor-alpha lipoteichoic acid
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Wakabayashi G
Department of Medicine, Tufts University, Boston, Massachusetts.
Gelfand J A
Jung W K
Connolly R J
Burke J F
Dinarello C A
References (47)
47 references, click to expand
  1. Coagulase-negative staphylococcal bacteremia. Mortality and hospital stay.
    Ann Intern Med. 1989 Jan 1;110(1):9-16 PMID: 2908834
  2. Interleukin 1 induces a shock-like state in rabbits. Synergism with tumor necrosis factor and the effect of cyclooxygenase inhibition.
    J Clin Invest. 1988 Apr;81(4):1162-72 PMID: 3258319
  3. Role of endotoxemia in cardiovascular dysfunction and mortality. Escherichia coli and Staphylococcus aureus challenges in a canine model of human septic shock.
    J Clin Invest. 1989 Jan;83(1):243-51 PMID: 2642920
  4. Lipoteichoic acids: a new class of bacterial antigen.
    Science. 1975 Mar 28;187(4182):1161-7 PMID: 46620
  5. Activation of the properdin pathway of complement in patients with gram-negative of bacteremia.
    N Engl J Med. 1975 May 1;292(18):937-40 PMID: 47148
  6. Anaphylatoxin-induced shock and two patterns of anaphylactic shock: hemodynamics and mediators.
    Acta Physiol Scand. 1979 Apr;105(4):393-403 PMID: 88165
  7. Endogenous pyrogen production by human blood monocytes stimulated by staphylococcal cell wall components.
    Infect Immun. 1981 Jan;31(1):208-13 PMID: 7216446
  8. Nosocomial septicemia due to multiply antibiotic-resistant Staphylococcus epidermidis.
    Ann Intern Med. 1982 Jan;96(1):1-10 PMID: 7053681
  9. Acute circulatory collapse caused by platelet-activating factor (PAF-acether) in dogs.
    Eur J Pharmacol. 1983 Jan 21;86(3-4):403-13 PMID: 6687572
  10. Septic shock. Hemodynamics and pathogenesis.
    JAMA. 1983 Dec 23-30;250(24):3324-7 PMID: 6196497
  11. Staphylococcus epidermidis sepsis in surgical patients.
    Arch Surg. 1984 Jan;119(1):96-100 PMID: 6418118
  12. Hospital-acquired bloodstream infections with Staphylococcus epidermidis. Review of 100 cases.
    Am J Med. 1984 Oct;77(4):639-44 PMID: 6486140
  13. Observations on the measurement and evaluation of endotoxemia by a quantitative limulus lysate microassay.
    J Infect Dis. 1984 Dec;150(6):916-24 PMID: 6501933
  14. Platelet activating factor (PAF) involvement in endotoxin-induced hypotension in rats. Studies with PAF-receptor antagonist kadsurenone.
    Biochem Biophys Res Commun. 1985 Mar 29;127(3):799-808 PMID: 2985058
  15. Is platelet activating factor (PAF) a mediator of endotoxin shock?
    Eur J Pharmacol. 1985 Feb 26;109(2):257-61 PMID: 3996473
  16. Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin.
    Science. 1985 Aug 30;229(4716):869-71 PMID: 3895437
  17. Experimental Bacteroides fragilis bacteremia in a primate model: evidence that Bacteroides fragilis does not promote the septic shock syndrome.
    J Trauma. 1985 Dec;25(12):1156-62 PMID: 4068069
  18. Effects of anti-C5a antibodies on the adult respiratory distress syndrome in septic primates.
    J Clin Invest. 1986 Jun;77(6):1812-6 PMID: 3711336
  19. An endothelial cell surface factor(s) induced in vitro by lipopolysaccharide, interleukin 1, and tumor necrosis factor-alpha increases neutrophil adherence by a CDw18-dependent mechanism.
    J Immunol. 1986 Jun 15;136(12):4548-53 PMID: 3486903
  20. Detection of circulating tumor necrosis factor after endotoxin administration.
    N Engl J Med. 1988 Jun 9;318(23):1481-6 PMID: 2835680
  21. Participation of tumor necrosis factor in the mediation of gram negative bacterial lipopolysaccharide-induced injury in rabbits.
    J Clin Invest. 1988 Jun;81(6):1925-37 PMID: 3384955
  22. C5a stimulates secretion of tumor necrosis factor from human mononuclear cells in vitro. Comparison with secretion of interleukin 1 beta and interleukin 1 alpha.
    J Exp Med. 1988 Jul 1;168(1):443-8 PMID: 3260938
  23. Tumor necrosis factor and interleukin-1 in the serum of children with severe infectious purpura.
    N Engl J Med. 1988 Aug 18;319(7):397-400 PMID: 3135497
  24. Interleukin-1 and tumour necrosis factor cause hypotension in the conscious rabbit.
    Clin Sci (Lond). 1988 Sep;75(3):251-5 PMID: 3046822
  25. Induction by toxic-shock-syndrome toxin-1 of a circulating tumor necrosis factor-like substance in rabbits and of immunoreactive tumor necrosis factor and interleukin-1 from human mononuclear cells.
    J Infect Dis. 1988 Nov;158(5):1017-25 PMID: 3263446
  26. Tumor necrosis factor (cachectin) is an endogenous pyrogen and induces production of interleukin 1.
    J Exp Med. 1986 Jun 1;163(6):1433-50 PMID: 3486936
  27. Recombinant tumor necrosis factor induces procoagulant activity in cultured human vascular endothelium: characterization and comparison with the actions of interleukin 1.
    Proc Natl Acad Sci U S A. 1986 Jun;83(12):4533-7 PMID: 3487091
  28. Shock and tissue injury induced by recombinant human cachectin.
    Science. 1986 Oct 24;234(4775):470-4 PMID: 3764421
  29. Cachectin/tumor necrosis factor induces lethal shock and stress hormone responses in the dog.
    Surg Gynecol Obstet. 1987 May;164(5):415-22 PMID: 3576418
  30. C5a-induced hemodynamic and hematologic changes in the rabbit. Role of cyclooxygenase products and polymorphonuclear leukocytes.
    Am J Pathol. 1987 Sep;128(3):471-83 PMID: 3115110
  31. C5a induction of human interleukin 1. Synergistic effect with endotoxin or interferon-gamma.
    J Immunol. 1987 Oct 15;139(8):2635-40 PMID: 3116090
  32. Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia.
    Nature. 1987 Dec 17-23;330(6149):662-4 PMID: 3317066
  33. Cytokine appearance in human endotoxemia and primate bacteremia.
    Surg Gynecol Obstet. 1988 Feb;166(2):147-53 PMID: 3122336
  34. Acute inflammation and a Shwartzman-like reaction induced by interleukin-1 and tumor necrosis factor. Synergistic action of the cytokines in the induction of inflammation and microvascular injury.
    Am J Pathol. 1987 Dec;129(3):463-76 PMID: 3501244
  35. Isolation and characterization of a capsular polysaccharide adhesin from Staphylococcus epidermidis.
    J Infect Dis. 1988 Apr;157(4):713-22 PMID: 3279138
  36. Interleukin-1 beta in human plasma: optimization of blood collection, plasma extraction, and radioimmunoassay methods.
    Lymphokine Res. 1988 Winter;7(4):457-67 PMID: 3145372
  37. Rabbit IL-1. Cloning, expression, biologic properties, and transcription during endotoxemia.
    J Immunol. 1989 Apr 1;142(7):2299-306 PMID: 2784458
  38. Sepsis syndrome: a valid clinical entity. Methylprednisolone Severe Sepsis Study Group.
    Crit Care Med. 1989 May;17(5):389-93 PMID: 2651003
  39. Endotoxin-induced shock in the rat. A role for C5a.
    Am J Pathol. 1989 Sep;135(3):489-97 PMID: 2789475
  40. Antibodies to cachectin/tumor necrosis factor reduce interleukin 1 beta and interleukin 6 appearance during lethal bacteremia.
    J Exp Med. 1989 Nov 1;170(5):1627-33 PMID: 2809510
  41. Coagulase-negative staphylococci. Epidemiology, evaluation, and therapy.
    Infect Dis Clin North Am. 1989 Dec;3(4):915-29 PMID: 2687369
  42. Circulating interleukin-1 and tumor necrosis factor in septic shock and experimental endotoxin fever.
    J Infect Dis. 1990 Jan;161(1):79-84 PMID: 2295861
  43. Interleukin-1 induces tumor necrosis factor (TNF) in human peripheral blood mononuclear cells in vitro and a circulating TNF-like activity in rabbits.
    J Infect Dis. 1990 Jul;162(1):215-23 PMID: 2113076
  44. Preliminary report: effects of interleukin-1 on platelet counts.
    Lancet. 1990 Sep 22;336(8717):712-4 PMID: 1975894
  45. Interleukin-1 receptor antagonist reduces mortality from endotoxin shock.
    Nature. 1990 Dec 6;348(6301):550-2 PMID: 2147233
  46. A specific receptor antagonist for interleukin 1 prevents Escherichia coli-induced shock in rabbits.
    FASEB J. 1991 Mar 1;5(3):338-43 PMID: 1825816
  47. Role of interleukin 1 and tumor necrosis factor on energy metabolism in rabbits.
    Am J Physiol. 1988 Dec;255(6 Pt 1):E760-8 PMID: 3144180
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1991-06-00
Pages
1925-35
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC296944
Subset
IM
Grants
NIAID NIH HHS · AI-15614 · United States
NIGMS NIH HHS · GM-21700 · United States
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