Mast cells mediate neutrophil recruitment during atherosclerotic plaque progression
Activated mast cells have been identified in the intima and perivascular tissue of human atherosclerotic plaques. As mast cells have been described to release a number of chemokines that mediate leukocyte fluxes, we propose that activated mast cells may play a pivotal role in leukocyte recruitment d...
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| Vydáno v: | Atherosclerosis Ročník 241; číslo 2; s. 289 - 296 |
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| Médium: | Journal Article |
| Jazyk: | angličtina |
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Ireland
Elsevier Ireland Ltd
01.08.2015
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| ISSN: | 0021-9150, 1879-1484, 1879-1484 |
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| Abstract | Activated mast cells have been identified in the intima and perivascular tissue of human atherosclerotic plaques. As mast cells have been described to release a number of chemokines that mediate leukocyte fluxes, we propose that activated mast cells may play a pivotal role in leukocyte recruitment during atherosclerotic plaque progression.
Systemic IgE-mediated mast cell activation in apoE−/−μMT mice resulted in an increase in atherosclerotic lesion size as compared to control mice, and interestingly, the number of neutrophils was highly increased in these lesions. In addition, peritoneal mast cell activation led to a massive neutrophil influx into the peritoneal cavity in C57Bl6 mice, whereas neutrophil numbers in mast cell deficient Kit(W-sh/W-sh) mice were not affected. Within the newly recruited neutrophil population, increased levels of CXCR2+ and CXCR4+ neutrophils were observed after mast cell activation. Indeed, mast cells were seen to contain and release CXCL1 and CXCL12, the ligands for CXCR2 and CXCR4. Intriguingly, peritoneal mast cell activation in combination with anti-CXCR2 receptor antagonist resulted in decreased neutrophil recruitment, thus establishing a prominent role for the CXCL1/CXCR2 axis in mast cell-mediated neutrophil recruitment.
Our data suggest that chemokines, and in particular CXCL1, released from activated mast cells induce neutrophil recruitment to the site of inflammation, thereby aggravating the ongoing inflammatory response and thus affecting plaque progression and destabilization.
•Systemic mast cell activation increased atherosclerotic plaque development.•Systemic mast cell activation induces neutrophil accumulation.•Peritoneal mast cell activation caused an influx of CXCR2+ and CXCR4+ neutrophils.•Mast cells express and secrete CXCL1 or CXCL12, the ligands for CXCR2 and CXCR4.•CXCR2 inhibition significantly reduced mast cell-mediated neutrophil recruitment. |
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| AbstractList | Abstract Aims Activated mast cells have been identified in the intima and perivascular tissue of human atherosclerotic plaques. As mast cells have been described to release a number of chemokines that mediate leukocyte fluxes, we propose that activated mast cells may play a pivotal role in leukocyte recruitment during atherosclerotic plaque progression. Methods and results Systemic IgE-mediated mast cell activation in apoE−/− μMT mice resulted in an increase in atherosclerotic lesion size as compared to control mice, and interestingly, the number of neutrophils was highly increased in these lesions. In addition, peritoneal mast cell activation led to a massive neutrophil influx into the peritoneal cavity in C57Bl6 mice, whereas neutrophil numbers in mast cell deficient Kit(W-sh /W-sh ) mice were not affected. Within the newly recruited neutrophil population, increased levels of CXCR2+ and CXCR4+ neutrophils were observed after mast cell activation. Indeed, mast cells were seen to contain and release CXCL1 and CXCL12, the ligands for CXCR2 and CXCR4. Intriguingly, peritoneal mast cell activation in combination with anti-CXCR2 receptor antagonist resulted in decreased neutrophil recruitment, thus establishing a prominent role for the CXCL1/CXCR2 axis in mast cell-mediated neutrophil recruitment. Conclusions Our data suggest that chemokines, and in particular CXCL1, released from activated mast cells induce neutrophil recruitment to the site of inflammation, thereby aggravating the ongoing inflammatory response and thus affecting plaque progression and destabilization. Activated mast cells have been identified in the intima and perivascular tissue of human atherosclerotic plaques. As mast cells have been described to release a number of chemokines that mediate leukocyte fluxes, we propose that activated mast cells may play a pivotal role in leukocyte recruitment during atherosclerotic plaque progression.AIMSActivated mast cells have been identified in the intima and perivascular tissue of human atherosclerotic plaques. As mast cells have been described to release a number of chemokines that mediate leukocyte fluxes, we propose that activated mast cells may play a pivotal role in leukocyte recruitment during atherosclerotic plaque progression.Systemic IgE-mediated mast cell activation in apoE(-/-)μMT mice resulted in an increase in atherosclerotic lesion size as compared to control mice, and interestingly, the number of neutrophils was highly increased in these lesions. In addition, peritoneal mast cell activation led to a massive neutrophil influx into the peritoneal cavity in C57Bl6 mice, whereas neutrophil numbers in mast cell deficient Kit(W(-sh)/W(-sh)) mice were not affected. Within the newly recruited neutrophil population, increased levels of CXCR2(+) and CXCR4(+) neutrophils were observed after mast cell activation. Indeed, mast cells were seen to contain and release CXCL1 and CXCL12, the ligands for CXCR2 and CXCR4. Intriguingly, peritoneal mast cell activation in combination with anti-CXCR2 receptor antagonist resulted in decreased neutrophil recruitment, thus establishing a prominent role for the CXCL1/CXCR2 axis in mast cell-mediated neutrophil recruitment.METHODS AND RESULTSSystemic IgE-mediated mast cell activation in apoE(-/-)μMT mice resulted in an increase in atherosclerotic lesion size as compared to control mice, and interestingly, the number of neutrophils was highly increased in these lesions. In addition, peritoneal mast cell activation led to a massive neutrophil influx into the peritoneal cavity in C57Bl6 mice, whereas neutrophil numbers in mast cell deficient Kit(W(-sh)/W(-sh)) mice were not affected. Within the newly recruited neutrophil population, increased levels of CXCR2(+) and CXCR4(+) neutrophils were observed after mast cell activation. Indeed, mast cells were seen to contain and release CXCL1 and CXCL12, the ligands for CXCR2 and CXCR4. Intriguingly, peritoneal mast cell activation in combination with anti-CXCR2 receptor antagonist resulted in decreased neutrophil recruitment, thus establishing a prominent role for the CXCL1/CXCR2 axis in mast cell-mediated neutrophil recruitment.Our data suggest that chemokines, and in particular CXCL1, released from activated mast cells induce neutrophil recruitment to the site of inflammation, thereby aggravating the ongoing inflammatory response and thus affecting plaque progression and destabilization.CONCLUSIONSOur data suggest that chemokines, and in particular CXCL1, released from activated mast cells induce neutrophil recruitment to the site of inflammation, thereby aggravating the ongoing inflammatory response and thus affecting plaque progression and destabilization. Activated mast cells have been identified in the intima and perivascular tissue of human atherosclerotic plaques. As mast cells have been described to release a number of chemokines that mediate leukocyte fluxes, we propose that activated mast cells may play a pivotal role in leukocyte recruitment during atherosclerotic plaque progression. Systemic IgE-mediated mast cell activation in apoE−/−μMT mice resulted in an increase in atherosclerotic lesion size as compared to control mice, and interestingly, the number of neutrophils was highly increased in these lesions. In addition, peritoneal mast cell activation led to a massive neutrophil influx into the peritoneal cavity in C57Bl6 mice, whereas neutrophil numbers in mast cell deficient Kit(W-sh/W-sh) mice were not affected. Within the newly recruited neutrophil population, increased levels of CXCR2+ and CXCR4+ neutrophils were observed after mast cell activation. Indeed, mast cells were seen to contain and release CXCL1 and CXCL12, the ligands for CXCR2 and CXCR4. Intriguingly, peritoneal mast cell activation in combination with anti-CXCR2 receptor antagonist resulted in decreased neutrophil recruitment, thus establishing a prominent role for the CXCL1/CXCR2 axis in mast cell-mediated neutrophil recruitment. Our data suggest that chemokines, and in particular CXCL1, released from activated mast cells induce neutrophil recruitment to the site of inflammation, thereby aggravating the ongoing inflammatory response and thus affecting plaque progression and destabilization. •Systemic mast cell activation increased atherosclerotic plaque development.•Systemic mast cell activation induces neutrophil accumulation.•Peritoneal mast cell activation caused an influx of CXCR2+ and CXCR4+ neutrophils.•Mast cells express and secrete CXCL1 or CXCL12, the ligands for CXCR2 and CXCR4.•CXCR2 inhibition significantly reduced mast cell-mediated neutrophil recruitment. Activated mast cells have been identified in the intima and perivascular tissue of human atherosclerotic plaques. As mast cells have been described to release a number of chemokines that mediate leukocyte fluxes, we propose that activated mast cells may play a pivotal role in leukocyte recruitment during atherosclerotic plaque progression. Systemic IgE-mediated mast cell activation in apoE(-/-)μMT mice resulted in an increase in atherosclerotic lesion size as compared to control mice, and interestingly, the number of neutrophils was highly increased in these lesions. In addition, peritoneal mast cell activation led to a massive neutrophil influx into the peritoneal cavity in C57Bl6 mice, whereas neutrophil numbers in mast cell deficient Kit(W(-sh)/W(-sh)) mice were not affected. Within the newly recruited neutrophil population, increased levels of CXCR2(+) and CXCR4(+) neutrophils were observed after mast cell activation. Indeed, mast cells were seen to contain and release CXCL1 and CXCL12, the ligands for CXCR2 and CXCR4. Intriguingly, peritoneal mast cell activation in combination with anti-CXCR2 receptor antagonist resulted in decreased neutrophil recruitment, thus establishing a prominent role for the CXCL1/CXCR2 axis in mast cell-mediated neutrophil recruitment. Our data suggest that chemokines, and in particular CXCL1, released from activated mast cells induce neutrophil recruitment to the site of inflammation, thereby aggravating the ongoing inflammatory response and thus affecting plaque progression and destabilization. |
| Author | de Jager, Saskia C.A. Kuiper, Johan Quax, Paul H.A. van der Velden, Daniël Lagraauw, H. Maxime Wezel, Anouk Bot, Ilze |
| Author_xml | – sequence: 1 givenname: Anouk surname: Wezel fullname: Wezel, Anouk organization: Division of Biopharmaceutics, Leiden Academic Centre for Drug Research, Leiden University, Leiden, The Netherlands – sequence: 2 givenname: H. Maxime surname: Lagraauw fullname: Lagraauw, H. Maxime organization: Division of Biopharmaceutics, Leiden Academic Centre for Drug Research, Leiden University, Leiden, The Netherlands – sequence: 3 givenname: Daniël surname: van der Velden fullname: van der Velden, Daniël organization: Division of Biopharmaceutics, Leiden Academic Centre for Drug Research, Leiden University, Leiden, The Netherlands – sequence: 4 givenname: Saskia C.A. surname: de Jager fullname: de Jager, Saskia C.A. organization: Laboratory of Experimental Cardiology, University Medical Center Utrecht, Utrecht, The Netherlands – sequence: 5 givenname: Paul H.A. surname: Quax fullname: Quax, Paul H.A. organization: Department of Surgery, Leiden University Medical Center, Leiden, The Netherlands – sequence: 6 givenname: Johan surname: Kuiper fullname: Kuiper, Johan organization: Division of Biopharmaceutics, Leiden Academic Centre for Drug Research, Leiden University, Leiden, The Netherlands – sequence: 7 givenname: Ilze surname: Bot fullname: Bot, Ilze email: i.bot@lacdr.leidenuniv.nl organization: Division of Biopharmaceutics, Leiden Academic Centre for Drug Research, Leiden University, Leiden, The Netherlands |
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| Keywords | Atherosclerotic plaque development and progression Influx Mast cells Chemokines Neutrophils Recruitment |
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| Snippet | Activated mast cells have been identified in the intima and perivascular tissue of human atherosclerotic plaques. As mast cells have been described to release... Abstract Aims Activated mast cells have been identified in the intima and perivascular tissue of human atherosclerotic plaques. As mast cells have been... |
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| SubjectTerms | Animals Aorta - immunology Aorta - metabolism Aorta - pathology Aortic Diseases - genetics Aortic Diseases - immunology Aortic Diseases - metabolism Aortic Diseases - pathology Apolipoproteins E - deficiency Apolipoproteins E - genetics Atherosclerosis - genetics Atherosclerosis - immunology Atherosclerosis - metabolism Atherosclerosis - pathology Atherosclerotic plaque development and progression Cardiovascular Cells, Cultured Chemokine CXCL1 - immunology Chemokine CXCL1 - metabolism Chemokine CXCL12 - immunology Chemokine CXCL12 - metabolism Chemokines Disease Models, Animal Disease Progression Immunoglobulin E - administration & dosage Immunoglobulin E - immunology Influx Male Mast cells Mast Cells - drug effects Mast Cells - immunology Mast Cells - pathology Mice, Inbred C57BL Mice, Knockout Neutrophil Infiltration - drug effects Neutrophils Neutrophils - drug effects Neutrophils - immunology Neutrophils - metabolism Paracrine Communication Plaque, Atherosclerotic Receptors, CXCR4 - immunology Receptors, CXCR4 - metabolism Receptors, Interleukin-8B - antagonists & inhibitors Receptors, Interleukin-8B - immunology Receptors, Interleukin-8B - metabolism Recruitment Signal Transduction |
| Title | Mast cells mediate neutrophil recruitment during atherosclerotic plaque progression |
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