Abstract
Bacterial heat shock proteins (HSPs) from Escherichia coli (GroES, GroEL, and DNAk) were tested for their ability to induce by themselves the expression and release of interleukin-6 (IL-6), tumor necrosis factor alpha (TNF-alpha), and granulocyte-monocyte colony-stimulating factor (GM-CSF) by human monocytes and GM-CSF, IL-6, E-selectin, intercellular adhesion molecule-1 (ICAM-1), and vascular cell adhesion molecule-1 (VCAM-1) by human umbilical vein endothelial cells (HUVEC). Our study demonstrated that treatment of monocytes with DNAk increased IL-6, TNF-alpha, and GM-CSF release in a dose-dependent manner. The same effect was elicited by GroEL but at a lower rate. Treatment of HUVEC cultures with DNAk and GroEL also increased GM-CSF, IL-6, E-selectin, ICAM-1, and VCAM-1 release in a dose-dependent fashion. In any case, the greatest release was obtained by using DNAk and GroEL at a concentration of 1 microg/ml. DNAk and GroEL were also able to up-regulate the surface expression of E-selectin, ICAM-1, and VCAM-1. As detected by reverse transcription-PCR analysis, DNAk and GroEL also increased the steady-state levels of cytokines and adhesion molecules in human monocytes and endothelial cells. In our study GroES showed a significant activity only on the release, surface expression, and mRNA transcription of E-selectin. Adhesion molecule expression seems to be a direct effect of HSPs and not via cytokines. Furthermore, these effects are due to HSPs properties because they are inhibited by specific monoclonal antibodies. These findings support the potential role of HSPs in modulating cell interactions during immunological and inflammatory responses.
Full Text
The Full Text of this article is available as a PDF (433.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bevilacqua M. P. Endothelial-leukocyte adhesion molecules. Annu Rev Immunol. 1993;11:767–804. doi: 10.1146/annurev.iy.11.040193.004003. [DOI] [PubMed] [Google Scholar]
- Buchmeier N. A., Heffron F. Induction of Salmonella stress proteins upon infection of macrophages. Science. 1990 May 11;248(4956):730–732. doi: 10.1126/science.1970672. [DOI] [PubMed] [Google Scholar]
- Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
- Cohen I. R., Young D. B. Autoimmunity, microbial immunity and the immunological homunculus. Immunol Today. 1991 Apr;12(4):105–110. doi: 10.1016/0167-5699(91)90093-9. [DOI] [PubMed] [Google Scholar]
- Cybulsky M. I., Chan M. K., Movat H. Z. Acute inflammation and microthrombosis induced by endotoxin, interleukin-1, and tumor necrosis factor and their implication in gram-negative infection. Lab Invest. 1988 Apr;58(4):365–378. [PubMed] [Google Scholar]
- Ensgraber M., Loos M. A 66-kilodalton heat shock protein of Salmonella typhimurium is responsible for binding of the bacterium to intestinal mucus. Infect Immun. 1992 Aug;60(8):3072–3078. doi: 10.1128/iai.60.8.3072-3078.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Evans D. J., Jr, Evans D. G., Engstrand L., Graham D. Y. Urease-associated heat shock protein of Helicobacter pylori. Infect Immun. 1992 May;60(5):2125–2127. doi: 10.1128/iai.60.5.2125-2127.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fayet O., Ziegelhoffer T., Georgopoulos C. The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J Bacteriol. 1989 Mar;171(3):1379–1385. doi: 10.1128/jb.171.3.1379-1385.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Friedland J. S., Shattock R., Remick D. G., Griffin G. E. Mycobacterial 65-kD heat shock protein induces release of proinflammatory cytokines from human monocytic cells. Clin Exp Immunol. 1993 Jan;91(1):58–62. doi: 10.1111/j.1365-2249.1993.tb03354.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Galdiero F., de L'ero G. C., Benedetto N., Galdiero M., Tufano M. A. Release of cytokines induced by Salmonella typhimurium porins. Infect Immun. 1993 Jan;61(1):155–161. doi: 10.1128/iai.61.1.155-161.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gearing A. J., Hemingway I., Pigott R., Hughes J., Rees A. J., Cashman S. J. Soluble forms of vascular adhesion molecules, E-selectin, ICAM-1, and VCAM-1: pathological significance. Ann N Y Acad Sci. 1992 Dec 4;667:324–331. doi: 10.1111/j.1749-6632.1992.tb51633.x. [DOI] [PubMed] [Google Scholar]
- Georgopoulos C., Welch W. J. Role of the major heat shock proteins as molecular chaperones. Annu Rev Cell Biol. 1993;9:601–634. doi: 10.1146/annurev.cb.09.110193.003125. [DOI] [PubMed] [Google Scholar]
- Gromkowski S. H., Yagi J., Janeway C. A., Jr Elevated temperature regulates tumor necrosis factor-mediated immune killing. Eur J Immunol. 1989 Sep;19(9):1709–1714. doi: 10.1002/eji.1830190927. [DOI] [PubMed] [Google Scholar]
- Karlsson-Parra A., Söderström K., Ferm M., Ivanyi J., Kiessling R., Klareskog L. Presence of human 65 kD heat shock protein (hsp) in inflamed joints and subcutaneous nodules of RA patients. Scand J Immunol. 1990 Jun;31(6):283–288. doi: 10.1111/j.1365-3083.1990.tb02770.x. [DOI] [PubMed] [Google Scholar]
- Kaufmann S. H. Heat shock proteins and the immune response. Immunol Today. 1990 Apr;11(4):129–136. doi: 10.1016/0167-5699(90)90050-j. [DOI] [PubMed] [Google Scholar]
- Kaufmann S. H. Heat-shock proteins: a missing link in the host-parasite relationship? Med Microbiol Immunol. 1990;179(2):61–66. doi: 10.1007/BF00198526. [DOI] [PubMed] [Google Scholar]
- Kaufmann S. H., Schoel B., van Embden J. D., Koga T., Wand-Württenberger A., Munk M. E., Steinhoff U. Heat-shock protein 60: implications for pathogenesis of and protection against bacterial infections. Immunol Rev. 1991 Jun;121:67–90. doi: 10.1111/j.1600-065x.1991.tb00823.x. [DOI] [PubMed] [Google Scholar]
- Klein T. W., Yamamoto Y., Wilson S., Newton C., Friedman H. Legionella pneumophila infection and cytokine production. Adv Exp Med Biol. 1992;319:97–104. doi: 10.1007/978-1-4615-3434-1_11. [DOI] [PubMed] [Google Scholar]
- Lindquist S., Craig E. A. The heat-shock proteins. Annu Rev Genet. 1988;22:631–677. doi: 10.1146/annurev.ge.22.120188.003215. [DOI] [PubMed] [Google Scholar]
- Lo S. K., Lee S., Ramos R. A., Lobb R., Rosa M., Chi-Rosso G., Wright S. D. Endothelial-leukocyte adhesion molecule 1 stimulates the adhesive activity of leukocyte integrin CR3 (CD11b/CD18, Mac-1, alpha m beta 2) on human neutrophils. J Exp Med. 1991 Jun 1;173(6):1493–1500. doi: 10.1084/jem.173.6.1493. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morrison D. C., Ulevitch R. J. The effects of bacterial endotoxins on host mediation systems. A review. Am J Pathol. 1978 Nov;93(2):526–618. [PMC free article] [PubMed] [Google Scholar]
- Nathan C. F. Secretory products of macrophages. J Clin Invest. 1987 Feb;79(2):319–326. doi: 10.1172/JCI112815. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peetermans W. E., D'Haens G. R., Ceuppens J. L., Rutgeerts P., Geboes K. Mucosal expression by B7-positive cells of the 60-kilodalton heat-shock protein in inflammatory bowel disease. Gastroenterology. 1995 Jan;108(1):75–82. doi: 10.1016/0016-5085(95)90010-1. [DOI] [PubMed] [Google Scholar]
- Peetermans W. E., Raats C. J., Langermans J. A., van Furth R. Mycobacterial heat-shock protein 65 induces proinflammatory cytokines but does not activate human mononuclear phagocytes. Scand J Immunol. 1994 Jun;39(6):613–617. doi: 10.1111/j.1365-3083.1994.tb03421.x. [DOI] [PubMed] [Google Scholar]
- Pelham H. Heat-shock proteins. Coming in from the cold. Nature. 1988 Apr 28;332(6167):776–777. doi: 10.1038/332776a0. [DOI] [PubMed] [Google Scholar]
- Polla B. S. A role for heat shock proteins in inflammation? Immunol Today. 1988 May;9(5):134–137. doi: 10.1016/0167-5699(88)91199-1. [DOI] [PubMed] [Google Scholar]
- Retzlaff C., Yamamoto Y., Hoffman P. S., Friedman H., Klein T. W. Bacterial heat shock proteins directly induce cytokine mRNA and interleukin-1 secretion in macrophage cultures. Infect Immun. 1994 Dec;62(12):5689–5693. doi: 10.1128/iai.62.12.5689-5693.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thole J. E., Hindersson P., de Bruyn J., Cremers F., van der Zee J., de Cock H., Tommassen J., van Eden W., van Embden J. D. Antigenic relatedness of a strongly immunogenic 65 kDA mycobacterial protein antigen with a similarly sized ubiquitous bacterial common antigen. Microb Pathog. 1988 Jan;4(1):71–83. doi: 10.1016/0882-4010(88)90049-6. [DOI] [PubMed] [Google Scholar]
- Tsai C. M., Frasch C. E. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem. 1982 Jan 1;119(1):115–119. doi: 10.1016/0003-2697(82)90673-x. [DOI] [PubMed] [Google Scholar]
- Yamamoto Y., Klein T. W., Newton C. A., Widen R., Friedman H. Growth of Legionella pneumophila in thioglycolate-elicited peritoneal macrophages from A/J mice. Infect Immun. 1988 Feb;56(2):370–375. doi: 10.1128/iai.56.2.370-375.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamamoto Y., Okubo S., Klein T. W., Onozaki K., Saito T., Friedman H. Binding of Legionella pneumophila to macrophages increases cellular cytokine mRNA. Infect Immun. 1994 Sep;62(9):3947–3956. doi: 10.1128/iai.62.9.3947-3956.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young R. A. Stress proteins and immunology. Annu Rev Immunol. 1990;8:401–420. doi: 10.1146/annurev.iy.08.040190.002153. [DOI] [PubMed] [Google Scholar]
- Zhang Y., Doerfler M., Lee T. C., Guillemin B., Rom W. N. Mechanisms of stimulation of interleukin-1 beta and tumor necrosis factor-alpha by Mycobacterium tuberculosis components. J Clin Invest. 1993 May;91(5):2076–2083. doi: 10.1172/JCI116430. [DOI] [PMC free article] [PubMed] [Google Scholar]