Skip to main content
SpringerLink
Log in

Monocyte adherence to the subendothelial basement membrane increases Interleukin-8 gene expression and antigen release

  • Original Articles
  • Published:
Inflammation Aims and scope Submit manuscript

Abstract

The emigration of peripheral blood monocytes into the interstitium allows for contact with a variety of surfaces which may provide signals important for monocyte function in both normal and inflammatory states. In the present study, we examined the effect of adherence to an endothelial cell-derived basement membrane and to collagen I, the major collagen of the interstitium, on monocyte release and gene expression of the potent chemotactic cytokine Interleukin-8 (IL-8). We further evaluated neutrophil chemotactic activity of the conditioned media containing antigenie IL-8 from monocytes adherent to these same surfaces. Elutriation-purified monocytes were adhered for 1 hour to plastic tissue culture wells either uncoated (PL) or coated with bovine serum albumin (BSA), collagen type I (C-I), or endothelial cellderived basement membrane (BM). Following removal of nonadherent cells, monocytes were further incubated in a serum-free media for 18 hours in the presence or absence of lipopolysaccharide (IPS). Following 18 hrs of incubation there were significantly less monocytes remaining adherent to BM when compared to other surfaces tested. In the absence of LPS, adherent monocytes released significant amounts of IL-8 that was not surface specific. In the presence of LPS, monocytes adherent to BM released significantly more IL-8, when corrected for adherent cell number, than monocytes adherent to PL, BSA, or C-I. Conditioned media from adherent monocytes expressed IL-8 dependent neutrophil chemotactic activity that was not influenced by the surfaces tested. Northern blot analysis indicated greater induction for IL-8 mRNA by monocytes adhered to BM after 18 hrs in the presence of LPS. These results suggest that monocyte adherence to the subendothelial basement membrane provides a priming signal for the induction and secretion of the chemotactic cytokine IL-8 in response to inflammatory stimuli.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Baggiolini, M., A. Walz, andS. L. Kunkel. 1989. Neutrophil activating peptide-Interleukin-8, a novel cytokine that activates neutrophils.J. Clin. Invest. 84:1045–1049.

    PubMed  Google Scholar 

  2. Nourshargh, S., J. A. Perkins, H. J. Showell, K. Matsushima, T. J. Williams, andP. D. Collins. 1992. A comparative study of the neutrophil stimulatory activityin vitro and pro-inflammatory propertiesin vivo of 72 amino acid and 77 amino acid IL-8.J. Immunol. 148:106–111.

    PubMed  Google Scholar 

  3. Walz, A., P. Peveri, H. Aschauer, andM. Baggiolini. 1987. Purification and amino acid sequencing of NAF, a novel neutrophil-activating factor produced by monocytes.Biochem. Biophys. Res. Comm. 149:755–761.

    PubMed  Google Scholar 

  4. Lotz, M., R. Terkeltaub, andP. M. Villiger. 1992. Cartilage and joint inflammation regulation of IL-8 expression by human articular chondrocytes.J. Immunol. 148:466–473.

    PubMed  Google Scholar 

  5. Lynch, J. P., T. J. Standiford, M. W. Rolfe, S. L. Kunkel, andR. M. Strieter. 1992. Neutrophilic alveolitis in idiopathic pulmonary fibrosis. The role of IL-8.Am. Rev. Respir. Dis. 145:1433–1439.

    PubMed  Google Scholar 

  6. Schröder, J. M., H. Gregory, U. S. Young, andE. Christophers. 1992. Neutrophil-activating proteins in psoriasis.J. Invest. Dermatol. 98:241–247.

    PubMed  Google Scholar 

  7. Sekido, N., N. Mukaida, A. Harada, I. Nakanishi, Y. Watanabe, andK. Matsushima. 1993. Prevention of lung reperfusion injury in rabbits by a monoclonal antibody against IL-8.Nature 365:654–657.

    PubMed  Google Scholar 

  8. Windsor, A. C. J., P. G. Mullen, A. A. Fowler, andH. J. Sugerman. 1993. Role of the neutrophil in adult respiratory distress syndrome.Br. J. Surg. 80:10–17.

    PubMed  Google Scholar 

  9. Baggiolini, M. 1992. Neutrophil activation and the role of Interleukin-8 and related cytokines.Int. Arch. Allergy Immunol. 99:196–199.

    Google Scholar 

  10. Baggiolini, M., B. Dewald, andB. Moser. 1994. Interleukin-8 and related chemotactic cytokines — CXC and CC chemokines.Adv. Immunol. 55:97–179.

    PubMed  Google Scholar 

  11. Miller, M. D. andM. S. Krangel. 1992. Biology and biochemistry of the chemokines: a family of chemotactic and inflammatory cytokines.Crit. Rev. Immunol. 12:17–46.

    PubMed  Google Scholar 

  12. Eierman, D. F., C. E. Johnson, andJ. S. Haskill. 1989. Human monocyte inflammatory mediator gene expression is selectively regulated by adherence substrates.J. Immunol. 142:1970–1976.

    PubMed  Google Scholar 

  13. Haskill, S., C. Johnson, D. Eierman, S. Becker, andK. Warren. 1988. Adherence induces selective mRNA expression of monocyte mediators and proto-oncogenes.J. Immunol. 140:1690–1694.

    PubMed  Google Scholar 

  14. Kasahara, K., R. M. Strieter, S. W. Chensue, T. J. Staniford, andS. L. Kunkel. 1991. Mononuclear cell adherence induces neutrophil chemotactic factor/Interleukin-8 gene expression.J. Leukocyte Biol. 50:287–295.

    PubMed  Google Scholar 

  15. Kasahara, K., R. M. Strieter, T. J. Standiford, andS. L. Kunkel. 1993. Adherence in combination with lipopolysaccharide, Tumor Necrosis Factor or Interleukin potentiates the induction of monocyte-derived Interleukin-8.Pathobiology 61:57–66.

    PubMed  Google Scholar 

  16. Sporn, S. A., D. F. Eierman, C. E. Johnson, J. Morris, G. Martin, M. Ladner, andS. Haskill. 1990. Monocyte adherence results in selective induction of novel genes sharing homology with mediators of inflammation and tissue repair.J. Immunol. 144:4434–4441.

    PubMed  Google Scholar 

  17. Strieter, R. M., S. W. Chensue, T. J. Standiford, M. A. Basha, H. J. Showell, andS. L. Kunkel. 1990. Disparate gene expression of chemotactic cytokines by human mononuclear phagocytes.Biochem. Biophy. Res. Comm. 166:886–891.

    Google Scholar 

  18. Gudewicz, P. W., M. B. Frewin, L. A. Heinel, andF. L. Minnear. 1994. Priming of human monocyte superoxide production and arachidonic acid metabolism by adherence to collagen and basement membrane surfaces.J. Leukocyte Biol. 55:423–429.

    PubMed  Google Scholar 

  19. Lennartz, M. R., J. B. Lefkowith, F. A. Bromley, andE. J. Brown. 1993. Immunoglobulin G-mediated phagocytosis activates a calcium-independent, phosphatidylethanolamine-specific phospholipase.J. Leukocyte Biol. 54:389–398.

    PubMed  Google Scholar 

  20. Gudewicz, P. W., M. B. Weaver, P. J. Del Vecchio, andT. M. Saba. 1989. Phorbol myristate acetate-treated endothelium stimulates polymorphonuclear leukocyte adhesion and superoxide secretion.J. Lab. Clin. Med. 113(6):708–716.

    PubMed  Google Scholar 

  21. Gudewicz, P. W., L. E. Odekon, P. J. Del Vecchio, andT. M. Saba. 1988. Generation of neutrophil chemotactic activity by phorbol ester-stimulated calf pulmonary artery endothelial cells.J. Leukocyte Biol. 44:1–7.

    PubMed  Google Scholar 

  22. Harvath, L., W. Falk, andE. J. Leonard. 1980. Rapid quantitation of neutrophil chemotaxis: use of PVP-free polycarbonate membrane in a multiwell assembly.J. Immunol. Methods 37:39–45.

    PubMed  Google Scholar 

  23. Chomczynski, P. andN. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.Anal. Biochem. 162(1):156–159.

    PubMed  Google Scholar 

  24. Gallay, P., C. V. Jongeneel, C. Barras, M. Burnier, J. D. Baumgartner, M. P. Glauser, andD. Heumann. 1993. Short time exposure to lipopolysaccharide is sufficient to activate human monocytes.J. Immunol. 50:5086–5093.

    Google Scholar 

  25. Roth, P. andR. A. Polin. 1990. Lipopolysaccharide enhances monocyte adherence to matrix-bound fibronectin.Clin. Immunol. Immunopath. 57:363–373.

    Google Scholar 

  26. Hailman, E., H. S. Lichenstein, M. M. Wurfel, D. S. Miller, D. A. Johnson, M. Kelley, L. A. Busse, M. M. Zukowski, andS. D. Wright. 1994. Lipopolysaccharide (LPS)-binding protein accelerates the binding of LPS to CD14.J. Exp. Med. 179:269–277.

    PubMed  Google Scholar 

  27. Yurchenco, P. D. andJ. C. Schittny. 1990. Molecular architecture of basement membranes.FASEB J. 4(6):1577–1590.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology and Cell Biology Neil Hellman Medical Research Building, Albany Medical College, 47 New Scotland Avenue, 12208, Albany, New York

    Lynn A. Heinel Ph.D., Demian Singleton, Matthew Miller, Mary Beth Frewin & Paul W. Gudewicz Ph.D.

Authors
  1. Lynn A. Heinel Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Demian Singleton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mary Beth Frewin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paul W. Gudewicz Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heinel, L.A., Singleton, D., Miller, M. et al. Monocyte adherence to the subendothelial basement membrane increases Interleukin-8 gene expression and antigen release. Inflammation 19, 517–527 (1995). https://doi.org/10.1007/BF01539132

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01539132

Keywords

Search

Navigation