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Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases

Blood neutrophils provide the first line of defense against pathogens but have also been implicated in thrombotic processes. This dual function of neutrophils could reflect an evolutionarily conserved association between blood coagulation and antimicrobial defense, although the molecular determinant... Full description

Journal Title: Nature medicine 2010, Vol.16 (8), p.887-896
Main Author: Reges, Katja
Other Authors: Engelmann, Bernd , Bidzhekov, Kiril , Goosmann, Christian , Lorenz, Michael , Pfeiler, Susanne , Konrad, Ildiko , Grahl, Lenka , Massberg, Steffen , von Bruehl, Marie-Luise , Manukyan, Davit , Holdenrieder, Stefan , Braun, Siegmund , Brinkmann, Volker , Kennerknecht, Elisabeth , Preissner, Klaus T , Khandagale, Avinash B , Reinhardt, Christoph , Spannagl, Michael
Format: Electronic Article Electronic Article
Language: English
Subjects:
Publisher: United States: Nature Publishing Group
ID: ISSN: 1078-8956
Link: https://www.ncbi.nlm.nih.gov/pubmed/20676107
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title: Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases
format: Article
creator:
  • Reges, Katja
  • Engelmann, Bernd
  • Bidzhekov, Kiril
  • Goosmann, Christian
  • Lorenz, Michael
  • Pfeiler, Susanne
  • Konrad, Ildiko
  • Grahl, Lenka
  • Massberg, Steffen
  • von Bruehl, Marie-Luise
  • Manukyan, Davit
  • Holdenrieder, Stefan
  • Braun, Siegmund
  • Brinkmann, Volker
  • Kennerknecht, Elisabeth
  • Preissner, Klaus T
  • Khandagale, Avinash B
  • Reinhardt, Christoph
  • Spannagl, Michael
subjects:
  • Animals
  • Blood clots
  • Blood Coagulation - genetics
  • Blood Coagulation - physiology
  • Blood Coagulation Factors - metabolism
  • Blood Coagulation Factors - physiology
  • Cathepsin G - genetics
  • Cathepsin G - metabolism
  • Cathepsin G - physiology
  • Coagulation
  • Fibrin - metabolism
  • Health aspects
  • Immunity, Innate - genetics
  • Immunity, Innate - physiology
  • Immunology
  • Infections
  • Leukocyte Elastase - genetics
  • Leukocyte Elastase - metabolism
  • Leukocyte Elastase - physiology
  • Lipoproteins - metabolism
  • Mice
  • Mice, Knockout
  • Models, Biological
  • Myocardial Infarction - genetics
  • Myocardial Infarction - metabolism
  • Natural immunity
  • Neutrophils
  • Neutrophils - metabolism
  • Neutrophils - physiology
  • Nucleosomes - metabolism
  • Pathology
  • Physiological aspects
  • Proteases
  • Protein Processing, Post-Translational - genetics
  • Protein Processing, Post-Translational - physiology
  • Serine
  • Serine Proteases - genetics
  • Serine Proteases - metabolism
  • Serine Proteases - physiology
  • Signal Transduction - genetics
  • Signal Transduction - physiology
  • Stroke - genetics
  • Stroke - metabolism
ispartof: Nature medicine, 2010, Vol.16 (8), p.887-896
description: Blood neutrophils provide the first line of defense against pathogens but have also been implicated in thrombotic processes. This dual function of neutrophils could reflect an evolutionarily conserved association between blood coagulation and antimicrobial defense, although the molecular determinants and in vivo significance of this association remain unclear. Here we show that major microbicidal effectors of neutrophils, the serine proteases neutrophil elastase and cathepsin G, together with externalized nucleosomes, promote coagulation and intravascular thrombus growth in vivo. The serine proteases and extracellular nucleosomes enhance tissue factor- and factor XII-dependent coagulation in a process involving local proteolysis of the coagulation suppressor tissue factor pathway inhibitor. During systemic infection, activation of coagulation fosters compartmentalization of bacteria in liver microvessels and reduces bacterial invasion into tissue. In the absence of a pathogen challenge, neutrophil-derived serine proteases and nucleosomes can contribute to large-vessel thrombosis, the main trigger of myocardial infarction and stroke. The ability of coagulation to suppress pathogen dissemination indicates that microvessel thrombosis represents a physiological tool of host defense.
language: eng
source:
identifier: ISSN: 1078-8956
fulltext: no_fulltext
issn:
  • 1078-8956
  • 1546-170X
url: Link


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titleReciprocal coupling of coagulation and innate immunity via neutrophil serine proteases
creatorReges, Katja ; Engelmann, Bernd ; Bidzhekov, Kiril ; Goosmann, Christian ; Lorenz, Michael ; Pfeiler, Susanne ; Konrad, Ildiko ; Grahl, Lenka ; Massberg, Steffen ; von Bruehl, Marie-Luise ; Manukyan, Davit ; Holdenrieder, Stefan ; Braun, Siegmund ; Brinkmann, Volker ; Kennerknecht, Elisabeth ; Preissner, Klaus T ; Khandagale, Avinash B ; Reinhardt, Christoph ; Spannagl, Michael
creatorcontribReges, Katja ; Engelmann, Bernd ; Bidzhekov, Kiril ; Goosmann, Christian ; Lorenz, Michael ; Pfeiler, Susanne ; Konrad, Ildiko ; Grahl, Lenka ; Massberg, Steffen ; von Bruehl, Marie-Luise ; Manukyan, Davit ; Holdenrieder, Stefan ; Braun, Siegmund ; Brinkmann, Volker ; Kennerknecht, Elisabeth ; Preissner, Klaus T ; Khandagale, Avinash B ; Reinhardt, Christoph ; Spannagl, Michael
descriptionBlood neutrophils provide the first line of defense against pathogens but have also been implicated in thrombotic processes. This dual function of neutrophils could reflect an evolutionarily conserved association between blood coagulation and antimicrobial defense, although the molecular determinants and in vivo significance of this association remain unclear. Here we show that major microbicidal effectors of neutrophils, the serine proteases neutrophil elastase and cathepsin G, together with externalized nucleosomes, promote coagulation and intravascular thrombus growth in vivo. The serine proteases and extracellular nucleosomes enhance tissue factor- and factor XII-dependent coagulation in a process involving local proteolysis of the coagulation suppressor tissue factor pathway inhibitor. During systemic infection, activation of coagulation fosters compartmentalization of bacteria in liver microvessels and reduces bacterial invasion into tissue. In the absence of a pathogen challenge, neutrophil-derived serine proteases and nucleosomes can contribute to large-vessel thrombosis, the main trigger of myocardial infarction and stroke. The ability of coagulation to suppress pathogen dissemination indicates that microvessel thrombosis represents a physiological tool of host defense.
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languageeng
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subjectAnimals ; Blood clots ; Blood Coagulation - genetics ; Blood Coagulation - physiology ; Blood Coagulation Factors - metabolism ; Blood Coagulation Factors - physiology ; Cathepsin G - genetics ; Cathepsin G - metabolism ; Cathepsin G - physiology ; Coagulation ; Fibrin - metabolism ; Health aspects ; Immunity, Innate - genetics ; Immunity, Innate - physiology ; Immunology ; Infections ; Leukocyte Elastase - genetics ; Leukocyte Elastase - metabolism ; Leukocyte Elastase - physiology ; Lipoproteins - metabolism ; Mice ; Mice, Knockout ; Models, Biological ; Myocardial Infarction - genetics ; Myocardial Infarction - metabolism ; Natural immunity ; Neutrophils ; Neutrophils - metabolism ; Neutrophils - physiology ; Nucleosomes - metabolism ; Pathology ; Physiological aspects ; Proteases ; Protein Processing, Post-Translational - genetics ; Protein Processing, Post-Translational - physiology ; Serine ; Serine Proteases - genetics ; Serine Proteases - metabolism ; Serine Proteases - physiology ; Signal Transduction - genetics ; Signal Transduction - physiology ; Stroke - genetics ; Stroke - metabolism
ispartofNature medicine, 2010, Vol.16 (8), p.887-896
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1Engelmann, Bernd
2Bidzhekov, Kiril
3Goosmann, Christian
4Lorenz, Michael
5Pfeiler, Susanne
6Konrad, Ildiko
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8Massberg, Steffen
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12Braun, Siegmund
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14Kennerknecht, Elisabeth
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16Khandagale, Avinash B
17Reinhardt, Christoph
18Spannagl, Michael
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descriptionBlood neutrophils provide the first line of defense against pathogens but have also been implicated in thrombotic processes. This dual function of neutrophils could reflect an evolutionarily conserved association between blood coagulation and antimicrobial defense, although the molecular determinants and in vivo significance of this association remain unclear. Here we show that major microbicidal effectors of neutrophils, the serine proteases neutrophil elastase and cathepsin G, together with externalized nucleosomes, promote coagulation and intravascular thrombus growth in vivo. The serine proteases and extracellular nucleosomes enhance tissue factor- and factor XII-dependent coagulation in a process involving local proteolysis of the coagulation suppressor tissue factor pathway inhibitor. During systemic infection, activation of coagulation fosters compartmentalization of bacteria in liver microvessels and reduces bacterial invasion into tissue. In the absence of a pathogen challenge, neutrophil-derived serine proteases and nucleosomes can contribute to large-vessel thrombosis, the main trigger of myocardial infarction and stroke. The ability of coagulation to suppress pathogen dissemination indicates that microvessel thrombosis represents a physiological tool of host defense.
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2Blood Coagulation - genetics
3Blood Coagulation - physiology
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13Immunity, Innate - physiology
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16Leukocyte Elastase - genetics
17Leukocyte Elastase - metabolism
18Leukocyte Elastase - physiology
19Lipoproteins - metabolism
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21Mice, Knockout
22Models, Biological
23Myocardial Infarction - genetics
24Myocardial Infarction - metabolism
25Natural immunity
26Neutrophils
27Neutrophils - metabolism
28Neutrophils - physiology
29Nucleosomes - metabolism
30Pathology
31Physiological aspects
32Proteases
33Protein Processing, Post-Translational - genetics
34Protein Processing, Post-Translational - physiology
35Serine
36Serine Proteases - genetics
37Serine Proteases - metabolism
38Serine Proteases - physiology
39Signal Transduction - genetics
40Signal Transduction - physiology
41Stroke - genetics
42Stroke - metabolism
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titleReciprocal coupling of coagulation and innate immunity via neutrophil serine proteases
authorReges, Katja ; Engelmann, Bernd ; Bidzhekov, Kiril ; Goosmann, Christian ; Lorenz, Michael ; Pfeiler, Susanne ; Konrad, Ildiko ; Grahl, Lenka ; Massberg, Steffen ; von Bruehl, Marie-Luise ; Manukyan, Davit ; Holdenrieder, Stefan ; Braun, Siegmund ; Brinkmann, Volker ; Kennerknecht, Elisabeth ; Preissner, Klaus T ; Khandagale, Avinash B ; Reinhardt, Christoph ; Spannagl, Michael
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1Blood clots
2Blood Coagulation - genetics
3Blood Coagulation - physiology
4Blood Coagulation Factors - metabolism
5Blood Coagulation Factors - physiology
6Cathepsin G - genetics
7Cathepsin G - metabolism
8Cathepsin G - physiology
9Coagulation
10Fibrin - metabolism
11Health aspects
12Immunity, Innate - genetics
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14Immunology
15Infections
16Leukocyte Elastase - genetics
17Leukocyte Elastase - metabolism
18Leukocyte Elastase - physiology
19Lipoproteins - metabolism
20Mice
21Mice, Knockout
22Models, Biological
23Myocardial Infarction - genetics
24Myocardial Infarction - metabolism
25Natural immunity
26Neutrophils
27Neutrophils - metabolism
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29Nucleosomes - metabolism
30Pathology
31Physiological aspects
32Proteases
33Protein Processing, Post-Translational - genetics
34Protein Processing, Post-Translational - physiology
35Serine
36Serine Proteases - genetics
37Serine Proteases - metabolism
38Serine Proteases - physiology
39Signal Transduction - genetics
40Signal Transduction - physiology
41Stroke - genetics
42Stroke - metabolism
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8Massberg, Steffen
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10Manukyan, Davit
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12Braun, Siegmund
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14Kennerknecht, Elisabeth
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16Khandagale, Avinash B
17Reinhardt, Christoph
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7Grahl, Lenka
8Massberg, Steffen
9von Bruehl, Marie-Luise
10Manukyan, Davit
11Holdenrieder, Stefan
12Braun, Siegmund
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14Kennerknecht, Elisabeth
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abstractBlood neutrophils provide the first line of defense against pathogens but have also been implicated in thrombotic processes. This dual function of neutrophils could reflect an evolutionarily conserved association between blood coagulation and antimicrobial defense, although the molecular determinants and in vivo significance of this association remain unclear. Here we show that major microbicidal effectors of neutrophils, the serine proteases neutrophil elastase and cathepsin G, together with externalized nucleosomes, promote coagulation and intravascular thrombus growth in vivo. The serine proteases and extracellular nucleosomes enhance tissue factor- and factor XII-dependent coagulation in a process involving local proteolysis of the coagulation suppressor tissue factor pathway inhibitor. During systemic infection, activation of coagulation fosters compartmentalization of bacteria in liver microvessels and reduces bacterial invasion into tissue. In the absence of a pathogen challenge, neutrophil-derived serine proteases and nucleosomes can contribute to large-vessel thrombosis, the main trigger of myocardial infarction and stroke. The ability of coagulation to suppress pathogen dissemination indicates that microvessel thrombosis represents a physiological tool of host defense.
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