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Differential induction of stress proteins and functional effects of heat shock in human phagocytes

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Abstract

Induction of specific heat shock (HS) proteins (HSP) has been described as a response of human monocytes to phagocytosis, and HSP may play protective roles in infection and immunity. Here we compared the stress response in monocytes and polymorphonuclear neutrophils during exposure to the classical inducers of HSP, i.e., HS and cadmium. We also investigated the stress response in these two phagocytic cells after particulate (phagocytosis) and nonparticulate [f-Met-Leu-Phe (FMLP)] activation of the respiratory burst enzyme NADPH oxidase. HS and cadmium induced stress protein synthesis in both cell types. In contrast, phagocytosis induced HSP in monocytes only, while FMLP did so in neutrophils only. This differential regulation of stress proteins might relate to physiological and functional differences between monocytes and neutrophils. With respect to functional effects of HS, we examined, in human monocytes and in neutrophils, the effect of HS on NADPH oxidase-mediated O −2 generation as well as on phagocytosis, bacterial killing, and Superoxide dismutase (SOD) activity. In monocytes, as in neutrophils, NADPH oxidase activity was inhibited by HS, while thermotolerance prevented this inhibition. Phagocytosis and bacterial killing were unaltered by HS. SOD activity transiently increased in monocytes but decreased in neutrophils upon exposure to HS. These observations indicate differential induction of HSP in human phagocytes and differential regulation of phagocytes' functions by HS.

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References

  1. Polla, B. S. 1988. A role for heat shock proteins in inflammation?Immunol. Today 9:134–137.

    PubMed  Google Scholar 

  2. Polla, B. S., andS. Kantengwa. 1991. Heat shock proteins and inflammation.Curr. Topics Microbiol. Immunol. 167:93–105.

    Google Scholar 

  3. Bellavite, P. 1988. The superoxide-forming enzymatic system of phagocytes.Free Radic. Biol. Med. 4:225–261.

    PubMed  Google Scholar 

  4. Maridonneau-Parini, I., S. M. Tringale, andA. I. Tauber. 1986. Identification of distinct activation pathways of the human neutrophil NADPH oxidase.J. Immunol. 137:2925–2930.

    PubMed  Google Scholar 

  5. Beaman, L., andB. L. Beaman. 1984. The role of oxygen and its derivates in microbial pathogenesis and host defense.Annu. Rev. Microbiol. 38:27–48.

    PubMed  Google Scholar 

  6. Clerget, M., andB. S. Polla. 1990. Erythrophagocytosis induces heat shock proteins synthesis in human monocytes-macrophages.Proc. Natl. Acad. Sci. U.S.A. 87:1081–1085.

    PubMed  Google Scholar 

  7. Kantengwa, S., andB. S. Polla. 1993. Phagocytosis ofStaphylococcus aureus induces a selective stress response in human monocytes-macrophages: Modulation by macrophage differentiation and by iron.Infect. Immun. 61:1281–1287.

    PubMed  Google Scholar 

  8. Bensaude, O., M. Pinto, M. F. Dubois, V. T. Nguyen, andM. Morange. 1990. Protein denaturation during heat-shock and related stress.In Stress Proteins. Induction and function. M. J. Schlesinger, G. Santoro, and E. Garaci, editors. Springer Verlag, Berlin. 89–99.

    Google Scholar 

  9. Linquist, S. 1986. The heat-shock response.Annu. Rev. Biochem. 55:1151–1191.

    PubMed  Google Scholar 

  10. Welch, W. J., andL. A. Mizzen. 1988. Characterization of the thermotolerant cell. Effects on the intracellular distribution of heat-shock protein 70, intermediate filaments, and small nuclear riboprotein complexes.J. Cell Biol. 106:1117–1130.

    PubMed  Google Scholar 

  11. Polla, B. S., andE. Mariethoz. 1992. More evidence for a case of chaperones in antigen processing.Immunol. Today 13:421–422.

    PubMed  Google Scholar 

  12. Mariethoz, E., F. Tacchini-Cottier, M. R. Jacquier-Sarlin, F. Sinclair, andB. S. Polla. 1994. Exposure of monocytes to heat shock does not increase class II expression but modulates antigen-dependent T cell responses.Int. Immunol. 6:925–930.

    PubMed  Google Scholar 

  13. Young, D. B. 1992. Heat-shock proteins: Immunity and autoimmunity.Curr. Opin. Immunol. 4:396–400.

    PubMed  Google Scholar 

  14. Maridonneau-Parini, I., J. Clerc, andB. S. Polla. 1988. Heat shock inhibits NADPH oxidase in human neutrophils.Biochem. Biophys. Res. Commun. 154:179–186.

    PubMed  Google Scholar 

  15. Reddy, M. V., andP. R. J. Gangadharam. 1992. Heat shock treatment of macrophages causes increased released of Superoxide anion.Infect. Immun. 60:2386–2390.

    PubMed  Google Scholar 

  16. Cohen, M. S., D. E. Mesler, R. G. Snipes, andT. K. Gray. 1986. 1,25-dihydroxyvitamin D3 activates secretion of hydrogen proxide by human monocytes.J. Immunol. 136:1049–1053.

    PubMed  Google Scholar 

  17. Polla, B. S., A. M. Healy, M. Byrne, andS. M. Krane. 1987. Hormone 1α,25-dihydroxy-vitamin D3 modulates heat shock response in monocytes.Am. J. Physiol. (Cell Physiol. 21) 252:C640-C649.

    Google Scholar 

  18. Polla, B. S., A. M. Healy, E. P. Amento, andS. M. Krane. 1986. 1,25-dihydroxyvitamin D3 maintains adherence of human monocytes and protects them from thermal injury.J. Clin. Invest. 77:1332–1339.

    PubMed  Google Scholar 

  19. Polla, B. S., J. V. Bonventre, andS. M. Krane. 1988. 1,25-dihydroxyvitamin D3 increases the toxicity of hydrogen peroxide in the human monocytic line U937: The role of calcium and heat shock.J. Cell. Biol. 107:373–380.

    PubMed  Google Scholar 

  20. Montesano, R., A. Mossaz, P. Vassali, andL. Orci. 1983. Specialization of the macrophage plasma membrane at sites of interaction with opsonized erythrocytes.J. Cell Biol. 96:1227–1233.

    PubMed  Google Scholar 

  21. Pruzanski, W., S. Saito, andD. W. Nitzan. 1983. The influence of lysostaphin on phagocytosis, intracellular bactericidal activity, and chemotaxis of human polymorphonuclear cells.J. Lab. Clin. Med. 102:298–305.

    PubMed  Google Scholar 

  22. Laemmli, U. K. 1970. Cleavage of structural proteins during assembly of the head bacteriophage T4.Nature 227:680–685.

    PubMed  Google Scholar 

  23. Johnston, R. B., Jr. 1984. Measurement of O2 − secreted by monocytes and macrophages.Methods Enzymol. 105:365–369.

    PubMed  Google Scholar 

  24. Bradford, M. M. 1976. A rapid and sensitive method for quantitation of micrograms quantities of proteins utilizing the principle of protein-dye binding.Anal. Biochem. 72:248–254.

    PubMed  Google Scholar 

  25. Crapo, J. D., J. M. McCord, andI. Fridovich. 1978. Preparation and assay of Superoxide dismutases.Methods Enzymol. 53:382–393.

    PubMed  Google Scholar 

  26. Maridonneau-Parini, I., S. E. Malawista, H. Stubbe, F. Russo-Marie, andB. S. Polla. 1993. Heat shock in human neutrophils: Superoxide generation is inhibited by a mechanism distinct from heat-denaturation of NADPH oxidase and is protected by heat shock proteins in thermotolerant cells.J. Cell Physiol. 156:204–211.

    PubMed  Google Scholar 

  27. Loven, D. P., D. B. Leeper, andL. W. Oberley. 1985. Superoxide dismutase levels in Chinese hamster ovary cells and ovarian carcinoma cells after hyperthermia or exposure to cycloheximide.Cancer Res. 45:3029–3033.

    PubMed  Google Scholar 

  28. Wang-Iverson, L., K. B.Pryzwanski, J. K.Spitznagel, and M. H.Cooney. Bactericidal capacity of phorbol myristate acetate-treated human polymorphonuclear leukocytes.Infect. Immun. 22:945–955.

  29. Donati, Y. R. A., S. Kantengwa, andB. S. Polla. 1991. Phagocytosis and heat shock response in human monocytes-macrophages.Pathobiology 59:156–161.

    PubMed  Google Scholar 

  30. Polla, B. S., G. Werlen, M. Clerget, D. Pittet, M. F. Rossier, andA. M. Capponi. 1989. 1,25-dihydroxyvitamin D3 induces responsiveness to the chemotactic peptide f-Met-Leu-Phe in the human monocytic line U937: Dissociation between calcium and oxidative metabolic responses.J. Leukocyte Biol. 45:381–388.

    PubMed  Google Scholar 

  31. Malter, J. S., andY. Hong. 1991. A redox switch and phosphorylation are involved in the post-translational up-regulation of the adenosine-uridine binding factor by phorbol ester and ionophore.J. Biol. Chem. 266:13167–3171.

    Google Scholar 

  32. Malech, H. L., andJ. F. Gallin. 1987. Neutrophils in human disease.N. Engl. J. Med. 317:687–694.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Allergy Unit, University Hospital, Geneva, Switzerland

    Barbara S. Polla, Hiltrud Stubbe, Salomé Kantengwa & Muriel R. Jacquier-Sarlin

  2. Laboratoire de Physiologie respiratoire, UFR Cochin-Port Royal, 24 rue du Faubourg St. Jacques, 75014, Paris, France

    Barbara S. Polla

  3. INSERM U332, ICGM, Paris, France

    Isabelle Maridonneau-Parini

Authors
  1. Barbara S. Polla
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  2. Hiltrud Stubbe
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  3. Salomé Kantengwa
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  4. Isabelle Maridonneau-Parini
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  5. Muriel R. Jacquier-Sarlin
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Additional information

The work presented here was supported by the Fonds National Suisse de la Recherche Scientifique No. 3.960-0.87 and 32-028645.90 to B.S.P. S.K. was supported by the Helmut Horten Foundation, and WHO grant TDR 900538. M.R.J.S. was supported by a grant from INSERM.

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Polla, B.S., Stubbe, H., Kantengwa, S. et al. Differential induction of stress proteins and functional effects of heat shock in human phagocytes. Inflammation 19, 363–378 (1995). https://doi.org/10.1007/BF01534393

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