Apoptotic Cells, through Transforming Growth Factor-β, Coordinately Induce Anti-inflammatory and Suppress Pro-inflammatory Eicosanoid and NO Synthesis in Murine Macrophages
Apoptotic cells are rapidly engulfed by adjacent tissue cells or macrophages before they can release pro-inflammatory/proimmunogenic intracellular contents. In addition, recognition of the apoptotic cells is actively anti-inflammatory and anti-immunogenic with generation of anti-inflammatory mediato...
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Published in | The Journal of biological chemistry Vol. 281; no. 50; pp. 38376 - 38384 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Elsevier Inc
15.12.2006
American Society for Biochemistry and Molecular Biology |
Subjects | |
Online Access | Get full text |
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Abstract | Apoptotic cells are rapidly engulfed by adjacent tissue cells or macrophages before they can release pro-inflammatory/proimmunogenic intracellular contents. In addition, recognition of the apoptotic cells is actively anti-inflammatory and anti-immunogenic with generation of anti-inflammatory mediators such as transforming growth factor-β (TGF-β) and anti-inflammatory eicosanoids. Here, we have investigated the role played by the induction of TGF-β in the coordinate expression of anti-inflammatory eicosanoids or peroxisome proliferator-activated receptor-γ and in the suppression of pro-inflammatory lipid mediators and nitric oxide (NO). By use of a dominant negative TGFβII receptor, TGF-β signaling was blocked, and its participation in the consequences of apoptotic cell stimulation was determined. The induction of TGF-β itself could be attributed to exposed phosphatidylserine on the apoptotic cells, which therefore appears to drive the balanced inflammatory mediator responses. Arachidonic acid release, COX-2, and prostaglandin synthase expression were shown to be significantly dependent on the TGF-β production. On the other hand, a requirement for TGF-β was also shown in the inhibition of thromboxane synthase and thromboxanes, of 5-lipoxygenase and sulfidopeptide leukotrienes, as well as of inducible nitric-oxide synthase and NO. TGF-β-dependent induction of arginase was also found and would further limit the NO generation. Finally, apoptotic cells stimulated production of 15-lipoxygenase and 15-hydroxyeicosatetraenoic acid, a potentially anti-inflammatory pathway acting through peroxisome proliferator-activated receptor-γ, and lipoxin A4 production, which were also up-regulated by a TGF-β-dependent pathway in this system. These results strongly suggest that the apoptotic cell inhibition of pro-inflammatory mediator production is pleiotropic and significantly dependent on the stimulation of TGF-β production. |
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AbstractList | Apoptotic cells are rapidly engulfed by adjacent tissue cells or macrophages before they can release pro-inflammatory/proimmunogenic intracellular contents. In addition, recognition of the apoptotic cells is actively anti-inflammatory and anti-immunogenic with generation of anti-inflammatory mediators such as transforming growth factor-β (TGF-β) and anti-inflammatory eicosanoids. Here, we have investigated the role played by the induction of TGF-β in the coordinate expression of anti-inflammatory eicosanoids or peroxisome proliferator-activated receptor-γ and in the suppression of pro-inflammatory lipid mediators and nitric oxide (NO). By use of a dominant negative TGFβII receptor, TGF-β signaling was blocked, and its participation in the consequences of apoptotic cell stimulation was determined. The induction of TGF-β itself could be attributed to exposed phosphatidylserine on the apoptotic cells, which therefore appears to drive the balanced inflammatory mediator responses. Arachidonic acid release, COX-2, and prostaglandin synthase expression were shown to be significantly dependent on the TGF-β production. On the other hand, a requirement for TGF-β was also shown in the inhibition of thromboxane synthase and thromboxanes, of 5-lipoxygenase and sulfidopeptide leukotrienes, as well as of inducible nitric-oxide synthase and NO. TGF-β-dependent induction of arginase was also found and would further limit the NO generation. Finally, apoptotic cells stimulated production of 15-lipoxygenase and 15-hydroxyeicosatetraenoic acid, a potentially anti-inflammatory pathway acting through peroxisome proliferator-activated receptor-γ, and lipoxin A₄ production, which were also up-regulated by a TGF-β-dependent pathway in this system. These results strongly suggest that the apoptotic cell inhibition of pro-inflammatory mediator production is pleiotropic and significantly dependent on the stimulation of TGF-β production. Apoptotic cells are rapidly engulfed by adjacent tissue cells or macrophages before they can release pro-inflammatory/proimmunogenic intracellular contents. In addition, recognition of the apoptotic cells is actively anti-inflammatory and anti-immunogenic with generation of anti-inflammatory mediators such as transforming growth factor-beta (TGF-beta) and anti-inflammatory eicosanoids. Here, we have investigated the role played by the induction of TGF-beta in the coordinate expression of anti-inflammatory eicosanoids or peroxisome proliferator-activated receptor-gamma and in the suppression of pro-inflammatory lipid mediators and nitric oxide (NO). By use of a dominant negative TGFbetaII receptor, TGF-beta signaling was blocked, and its participation in the consequences of apoptotic cell stimulation was determined. The induction of TGF-beta itself could be attributed to exposed phosphatidylserine on the apoptotic cells, which therefore appears to drive the balanced inflammatory mediator responses. Arachidonic acid release, COX-2, and prostaglandin synthase expression were shown to be significantly dependent on the TGF-beta production. On the other hand, a requirement for TGF-beta was also shown in the inhibition of thromboxane synthase and thromboxanes, of 5-lipoxygenase and sulfidopeptide leukotrienes, as well as of inducible nitric-oxide synthase and NO. TGF-beta-dependent induction of arginase was also found and would further limit the NO generation. Finally, apoptotic cells stimulated production of 15-lipoxygenase and 15-hydroxyeicosatetraenoic acid, a potentially anti-inflammatory pathway acting through peroxisome proliferator-activated receptor-gamma, and lipoxin A(4) production, which were also up-regulated by a TGF-beta-dependent pathway in this system. These results strongly suggest that the apoptotic cell inhibition of pro-inflammatory mediator production is pleiotropic and significantly dependent on the stimulation of TGF-beta production. Apoptotic cells are rapidly engulfed by adjacent tissue cells or macrophages before they can release pro-inflammatory/proimmunogenic intracellular contents. In addition, recognition of the apoptotic cells is actively anti-inflammatory and anti-immunogenic with generation of anti-inflammatory mediators such as transforming growth factor-β (TGF-β) and anti-inflammatory eicosanoids. Here, we have investigated the role played by the induction of TGF-β in the coordinate expression of anti-inflammatory eicosanoids or peroxisome proliferator-activated receptor-γ and in the suppression of pro-inflammatory lipid mediators and nitric oxide (NO). By use of a dominant negative TGFβII receptor, TGF-β signaling was blocked, and its participation in the consequences of apoptotic cell stimulation was determined. The induction of TGF-β itself could be attributed to exposed phosphatidylserine on the apoptotic cells, which therefore appears to drive the balanced inflammatory mediator responses. Arachidonic acid release, COX-2, and prostaglandin synthase expression were shown to be significantly dependent on the TGF-β production. On the other hand, a requirement for TGF-β was also shown in the inhibition of thromboxane synthase and thromboxanes, of 5-lipoxygenase and sulfidopeptide leukotrienes, as well as of inducible nitric-oxide synthase and NO. TGF-β-dependent induction of arginase was also found and would further limit the NO generation. Finally, apoptotic cells stimulated production of 15-lipoxygenase and 15-hydroxyeicosatetraenoic acid, a potentially anti-inflammatory pathway acting through peroxisome proliferator-activated receptor-γ, and lipoxin A4 production, which were also up-regulated by a TGF-β-dependent pathway in this system. These results strongly suggest that the apoptotic cell inhibition of pro-inflammatory mediator production is pleiotropic and significantly dependent on the stimulation of TGF-β production. Apoptotic cells are rapidly engulfed by adjacent tissue cells or macrophages before they can release pro-inflammatory/proimmunogenic intracellular contents. In addition, recognition of the apoptotic cells is actively anti-inflammatory and anti-immunogenic with generation of anti-inflammatory mediators such as transforming growth factor- beta (TGF- beta ) and anti-inflammatory eicosanoids. Here, we have investigated the role played by the induction of TGF- beta in the coordinate expression of anti-inflammatory eicosanoids or peroxisome proliferator-activated receptor- gamma and in the suppression of pro-inflammatory lipid mediators and nitric oxide (NO). By use of a dominant negative TGF beta II receptor, TGF- beta signaling was blocked, and its participation in the consequences of apoptotic cell stimulation was determined. The induction of TGF- beta itself could be attributed to exposed phosphatidylserine on the apoptotic cells, which therefore appears to drive the balanced inflammatory mediator responses. Arachidonic acid release, COX-2, and prostaglandin synthase expression were shown to be significantly dependent on the TGF- beta production. On the other hand, a requirement for TGF- beta was also shown in the inhibition of thromboxane synthase and thromboxanes, of 5-lipoxygenase and sulfidopeptide leukotrienes, as well as of inducible nitric-oxide synthase and NO. TGF- beta -dependent induction of arginase was also found and would further limit the NO generation. Finally, apoptotic cells stimulated production of 15-lipoxygenase and 15-hydroxyeicosatetraenoic acid, a potentially anti-inflammatory pathway acting through peroxisome proliferator-activated receptor- gamma , and lipoxin A sub(4) production, which were also up-regulated by a TGF- beta -dependent pathway in this system. These results strongly suggest that the apoptotic cell inhibition of pro-inflammatory mediator production is pleiotropic and significantly dependent on the stimulation of TGF- beta production. |
Author | Gardai, Shyra J. Henson, Peter M. Schiemann, William P. Freire-de-Lima, Celio G. Xiao, Yi Qun Bratton, Donna L. |
Author_xml | – sequence: 1 givenname: Celio G. surname: Freire-de-Lima fullname: Freire-de-Lima, Celio G. organization: Instituto de Biofísica Carlos Chagas Filho, Federal University of Rio de Janeiro, Rio de Janeiro RJ 21944-970, Brazil – sequence: 2 givenname: Yi Qun surname: Xiao fullname: Xiao, Yi Qun organization: Program in Cell Biology, Department of Pediatrics, National Jewish Medical and Research Center, Denver, Colorado 80206 – sequence: 3 givenname: Shyra J. surname: Gardai fullname: Gardai, Shyra J. organization: Program in Cell Biology, Department of Pediatrics, National Jewish Medical and Research Center, Denver, Colorado 80206 – sequence: 4 givenname: Donna L. surname: Bratton fullname: Bratton, Donna L. organization: Program in Cell Biology, Department of Pediatrics, National Jewish Medical and Research Center, Denver, Colorado 80206 – sequence: 5 givenname: William P. surname: Schiemann fullname: Schiemann, William P. organization: Program in Cell Biology, Department of Pediatrics, National Jewish Medical and Research Center, Denver, Colorado 80206 – sequence: 6 givenname: Peter M. surname: Henson fullname: Henson, Peter M. email: hensonp@njc.org organization: Program in Cell Biology, Department of Pediatrics, National Jewish Medical and Research Center, Denver, Colorado 80206 |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/17056601$$D View this record in MEDLINE/PubMed |
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SubjectTerms | Animals Apoptosis Arachidonic Acid - metabolism Cyclooxygenase 2 - metabolism Eicosanoids - biosynthesis Humans Inflammation Mediators - metabolism Jurkat Cells Macrophages, Peritoneal - metabolism Mice Mice, Inbred BALB C Nitric Oxide - biosynthesis Signal Transduction Transforming Growth Factor beta - physiology |
Title | Apoptotic Cells, through Transforming Growth Factor-β, Coordinately Induce Anti-inflammatory and Suppress Pro-inflammatory Eicosanoid and NO Synthesis in Murine Macrophages |
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