Induction of the synthesis of the C-X-C chemokine interferon-γ-inducible protein-10 in experimental canine endotoxemia

Nikolaos G. Frangogiannis, Leonardo H. Mendoza, C. Wayne Smith, Lloyd H. Michael, Mark L. Entman

Research output: Contribution to journalArticle

37 Citations (Scopus)

Abstract

Endotoxemia is associated with a systemic inflammatory response leading to organ-specific leukocyte recruitment and tissue injury. Chemokine expression has been demonstrated in various models of sepsis and may mediate tissue infiltration with inflammatory cells. In this study we examined expression of the C-X-C chemokine interferon-γ-inducible protein-10 (IP-10), a potent T-lymphocyte chemoattractant, in a canine model of endotoxemia and investigated mechanisms of cytokine-mediated IP-10 induction in endothelial cells. Control canine tissues showed negligible expression of IP-10 message, with the exception of the spleen. Endotoxemic dogs demonstrated a robust induction of IP-10 mRNA in the heart, lung, kidney, liver, and spleen. Immunohistochemical studies indicated that IP-10 was predominantly localized in cardiac venular endothelial cells, bronchial epithelial cells, renal mesangial cells, and in the splenic red pulp of endotoxemic dogs. In addition, IP-10 expression was associated with T-lymphocyte infiltration in canine tissues. Tumor necrosis factor-α (TNF-α) and interleukin-1β (IL-1β) induced a marked upregulation of IP-10 message in canine venular endothelial cells. IP-10 expression in TNF-α-stimulated endothelial cells peaked at 6 h of stimulation and returned to baseline levels after 24 h. In addition, macrophage colony-stimulating factor (M-CSF) induced a dose-dependent induction of IP-10 mRNA in canine endothelial cells. M-CSF-mediated IP-10 expression peaked after 6 h of incubation and returned to baseline levels after 24 h. Canine endotoxemia is associated with a robust early expression of IP-10 in multiple tissues. IP-10 induction may be important in regulating lymphocyte recruitment and function. TNF-α, IL-1β, and M-CSF are potent inducers of IP-10 in canine endothelial cells and may indirectly mediate lymphocyte chemotaxis and activation in inflammatory processes.

Original languageEnglish (US)
Pages (from-to)365-376
Number of pages12
JournalCell and Tissue Research
Volume302
Issue number3
StatePublished - 2000
Externally publishedYes

Fingerprint

Chemokine CXCL10
CXC Chemokines
Endotoxemia
Canidae
Endothelial cells
Proteins
Endothelial Cells
Macrophage Colony-Stimulating Factor
Tissue
T-cells
Lymphocytes
Tumor Necrosis Factor-alpha
Interleukin-1
Infiltration
Spleen
Dogs
T-Lymphocytes
Messenger RNA
Mesangial Cells
Chemotactic Factors

Keywords

  • Chemokine
  • Cytokine
  • Dog
  • Endothelium
  • Endotoxin
  • Interleukin-1β
  • Lymphocyte
  • Macrophage colony-stimulating factor
  • Tumor necrosis factor-α

ASJC Scopus subject areas

  • Anatomy
  • Clinical Biochemistry
  • Cell Biology

Cite this

Induction of the synthesis of the C-X-C chemokine interferon-γ-inducible protein-10 in experimental canine endotoxemia. / Frangogiannis, Nikolaos G.; Mendoza, Leonardo H.; Smith, C. Wayne; Michael, Lloyd H.; Entman, Mark L.

In: Cell and Tissue Research, Vol. 302, No. 3, 2000, p. 365-376.

Research output: Contribution to journalArticle

Frangogiannis, Nikolaos G. ; Mendoza, Leonardo H. ; Smith, C. Wayne ; Michael, Lloyd H. ; Entman, Mark L. / Induction of the synthesis of the C-X-C chemokine interferon-γ-inducible protein-10 in experimental canine endotoxemia. In: Cell and Tissue Research. 2000 ; Vol. 302, No. 3. pp. 365-376.
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AU - Smith, C. Wayne

AU - Michael, Lloyd H.

AU - Entman, Mark L.

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N2 - Endotoxemia is associated with a systemic inflammatory response leading to organ-specific leukocyte recruitment and tissue injury. Chemokine expression has been demonstrated in various models of sepsis and may mediate tissue infiltration with inflammatory cells. In this study we examined expression of the C-X-C chemokine interferon-γ-inducible protein-10 (IP-10), a potent T-lymphocyte chemoattractant, in a canine model of endotoxemia and investigated mechanisms of cytokine-mediated IP-10 induction in endothelial cells. Control canine tissues showed negligible expression of IP-10 message, with the exception of the spleen. Endotoxemic dogs demonstrated a robust induction of IP-10 mRNA in the heart, lung, kidney, liver, and spleen. Immunohistochemical studies indicated that IP-10 was predominantly localized in cardiac venular endothelial cells, bronchial epithelial cells, renal mesangial cells, and in the splenic red pulp of endotoxemic dogs. In addition, IP-10 expression was associated with T-lymphocyte infiltration in canine tissues. Tumor necrosis factor-α (TNF-α) and interleukin-1β (IL-1β) induced a marked upregulation of IP-10 message in canine venular endothelial cells. IP-10 expression in TNF-α-stimulated endothelial cells peaked at 6 h of stimulation and returned to baseline levels after 24 h. In addition, macrophage colony-stimulating factor (M-CSF) induced a dose-dependent induction of IP-10 mRNA in canine endothelial cells. M-CSF-mediated IP-10 expression peaked after 6 h of incubation and returned to baseline levels after 24 h. Canine endotoxemia is associated with a robust early expression of IP-10 in multiple tissues. IP-10 induction may be important in regulating lymphocyte recruitment and function. TNF-α, IL-1β, and M-CSF are potent inducers of IP-10 in canine endothelial cells and may indirectly mediate lymphocyte chemotaxis and activation in inflammatory processes.

AB - Endotoxemia is associated with a systemic inflammatory response leading to organ-specific leukocyte recruitment and tissue injury. Chemokine expression has been demonstrated in various models of sepsis and may mediate tissue infiltration with inflammatory cells. In this study we examined expression of the C-X-C chemokine interferon-γ-inducible protein-10 (IP-10), a potent T-lymphocyte chemoattractant, in a canine model of endotoxemia and investigated mechanisms of cytokine-mediated IP-10 induction in endothelial cells. Control canine tissues showed negligible expression of IP-10 message, with the exception of the spleen. Endotoxemic dogs demonstrated a robust induction of IP-10 mRNA in the heart, lung, kidney, liver, and spleen. Immunohistochemical studies indicated that IP-10 was predominantly localized in cardiac venular endothelial cells, bronchial epithelial cells, renal mesangial cells, and in the splenic red pulp of endotoxemic dogs. In addition, IP-10 expression was associated with T-lymphocyte infiltration in canine tissues. Tumor necrosis factor-α (TNF-α) and interleukin-1β (IL-1β) induced a marked upregulation of IP-10 message in canine venular endothelial cells. IP-10 expression in TNF-α-stimulated endothelial cells peaked at 6 h of stimulation and returned to baseline levels after 24 h. In addition, macrophage colony-stimulating factor (M-CSF) induced a dose-dependent induction of IP-10 mRNA in canine endothelial cells. M-CSF-mediated IP-10 expression peaked after 6 h of incubation and returned to baseline levels after 24 h. Canine endotoxemia is associated with a robust early expression of IP-10 in multiple tissues. IP-10 induction may be important in regulating lymphocyte recruitment and function. TNF-α, IL-1β, and M-CSF are potent inducers of IP-10 in canine endothelial cells and may indirectly mediate lymphocyte chemotaxis and activation in inflammatory processes.

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KW - Macrophage colony-stimulating factor

KW - Tumor necrosis factor-α

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