Nbeal2 Deficiency Increases Organ Damage but Does Not Affect Host Defense During Gram-Negative Pneumonia-Derived Sepsis
OBJECTIVE—Nbeal2 mice, a model of human gray platelet syndrome, have reduced neutrophil granularity and impaired host defense against systemic Staphylococcus aureus infection. We here aimed to study the role of Nbeal2 deficiency in both leukocytes and platelets during gram-negative pneumonia and sep...
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Veröffentlicht in: | Arteriosclerosis, thrombosis, and vascular biology thrombosis, and vascular biology, 2018-08, Vol.38 (8), p.1772-1784 |
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creator | Claushuis, Theodora A.M de Stoppelaar, Sacha F de Vos, Alex F Grootemaat, Anita E van der Wel, Nicole N Roelofs, Joris J.T.H Ware, Jerry van‘t Veer, Cornelis van der Poll, Tom |
description | OBJECTIVE—Nbeal2 mice, a model of human gray platelet syndrome, have reduced neutrophil granularity and impaired host defense against systemic Staphylococcus aureus infection. We here aimed to study the role of Nbeal2 deficiency in both leukocytes and platelets during gram-negative pneumonia and sepsis.
APPROACH AND RESULTS—We studied the role of Nbeal2 in platelets and leukocytes during murine pneumonia and sepsis by Klebsiella pneumoniae. Apart from platelet α-granule deficiency and reduced neutrophil granularity, also monocyte granularity was reduced in Nbeal2 mice, whereas plasma levels of MPO (myeloperoxidase), elastase, NGAL (neutrophil gelatinase–associated lipocalin), and MMP-9 (matrix metalloproteinase 9), and leukocyte CD11b expression were increased. Nbeal2 leukocytes showed unaltered in vitro antibacterial response and phagocytosis capacity against Klebsiella, and unchanged reactive nitrogen species and cytokine production. Also during Klebsiella pneumonia and sepsis, Nbeal2 mice had similar bacterial growth in lung and distant body sites, with enhanced leukocyte migration to the bronchoalveolar space. Despite similar infection-induced inflammation, organ damage was increased in Nbeal2 mice, which was also seen during endotoxemia. Platelet-specific Nbeal2 deficiency did not influence leukocyte functions, indicating that Nbeal2 directly modifies leukocytes. Transfusion of Nbeal2 but not of Nbeal2 platelets into thrombocytopenic mice was associated with bleeding in the lung but similar host defense, pointing at a role for platelet α-granules in maintaining vascular integrity but not host defense during Klebsiella pneumosepsis.
CONCLUSIONS—These data show that Nbeal2 deficiency—resulting in gray platelet syndrome—affects platelets, neutrophils, and monocytes, with intact host defense but increased organ damage during gram-negative pneumosepsis. |
doi_str_mv | 10.1161/ATVBAHA.118.311332 |
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APPROACH AND RESULTS—We studied the role of Nbeal2 in platelets and leukocytes during murine pneumonia and sepsis by Klebsiella pneumoniae. Apart from platelet α-granule deficiency and reduced neutrophil granularity, also monocyte granularity was reduced in Nbeal2 mice, whereas plasma levels of MPO (myeloperoxidase), elastase, NGAL (neutrophil gelatinase–associated lipocalin), and MMP-9 (matrix metalloproteinase 9), and leukocyte CD11b expression were increased. Nbeal2 leukocytes showed unaltered in vitro antibacterial response and phagocytosis capacity against Klebsiella, and unchanged reactive nitrogen species and cytokine production. Also during Klebsiella pneumonia and sepsis, Nbeal2 mice had similar bacterial growth in lung and distant body sites, with enhanced leukocyte migration to the bronchoalveolar space. Despite similar infection-induced inflammation, organ damage was increased in Nbeal2 mice, which was also seen during endotoxemia. Platelet-specific Nbeal2 deficiency did not influence leukocyte functions, indicating that Nbeal2 directly modifies leukocytes. Transfusion of Nbeal2 but not of Nbeal2 platelets into thrombocytopenic mice was associated with bleeding in the lung but similar host defense, pointing at a role for platelet α-granules in maintaining vascular integrity but not host defense during Klebsiella pneumosepsis.
CONCLUSIONS—These data show that Nbeal2 deficiency—resulting in gray platelet syndrome—affects platelets, neutrophils, and monocytes, with intact host defense but increased organ damage during gram-negative pneumosepsis.</description><identifier>ISSN: 1079-5642</identifier><identifier>EISSN: 1524-4636</identifier><identifier>DOI: 10.1161/ATVBAHA.118.311332</identifier><identifier>PMID: 29930006</identifier><language>eng</language><publisher>United States: American Heart Association, Inc</publisher><subject>Animals ; Blood Platelets - metabolism ; Blood Platelets - microbiology ; Blood Proteins - deficiency ; Blood Proteins - genetics ; CD11b Antigen - blood ; Disease Models, Animal ; Female ; Gray Platelet Syndrome - blood ; Gray Platelet Syndrome - genetics ; Gray Platelet Syndrome - metabolism ; Host-Pathogen Interactions ; Klebsiella Infections - blood ; Klebsiella Infections - genetics ; Klebsiella Infections - metabolism ; Klebsiella Infections - microbiology ; Klebsiella pneumoniae - growth & development ; Klebsiella pneumoniae - pathogenicity ; Lipocalin-2 - blood ; Male ; Matrix Metalloproteinase 9 - blood ; Mice, Inbred C57BL ; Mice, Knockout ; Monocytes - metabolism ; Monocytes - microbiology ; Multiple Organ Failure - blood ; Multiple Organ Failure - genetics ; Multiple Organ Failure - metabolism ; Multiple Organ Failure - microbiology ; Neutrophils - metabolism ; Neutrophils - microbiology ; Pancreatic Elastase - blood ; Peroxidase - blood ; Platelet Glycoprotein GPIb-IX Complex - genetics ; Platelet Glycoprotein GPIb-IX Complex - metabolism ; Platelet Transfusion ; Pneumonia, Bacterial - blood ; Pneumonia, Bacterial - genetics ; Pneumonia, Bacterial - metabolism ; Pneumonia, Bacterial - microbiology ; Sepsis - blood ; Sepsis - genetics ; Sepsis - metabolism ; Sepsis - microbiology</subject><ispartof>Arteriosclerosis, thrombosis, and vascular biology, 2018-08, Vol.38 (8), p.1772-1784</ispartof><rights>2018 American Heart Association, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3942-c259e48105eab3af54707134764a99d9cef5993fa3ecdddfff49754edf398b163</citedby><cites>FETCH-LOGICAL-c3942-c259e48105eab3af54707134764a99d9cef5993fa3ecdddfff49754edf398b163</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29930006$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Claushuis, Theodora A.M</creatorcontrib><creatorcontrib>de Stoppelaar, Sacha F</creatorcontrib><creatorcontrib>de Vos, Alex F</creatorcontrib><creatorcontrib>Grootemaat, Anita E</creatorcontrib><creatorcontrib>van der Wel, Nicole N</creatorcontrib><creatorcontrib>Roelofs, Joris J.T.H</creatorcontrib><creatorcontrib>Ware, Jerry</creatorcontrib><creatorcontrib>van‘t Veer, Cornelis</creatorcontrib><creatorcontrib>van der Poll, Tom</creatorcontrib><title>Nbeal2 Deficiency Increases Organ Damage but Does Not Affect Host Defense During Gram-Negative Pneumonia-Derived Sepsis</title><title>Arteriosclerosis, thrombosis, and vascular biology</title><addtitle>Arterioscler Thromb Vasc Biol</addtitle><description>OBJECTIVE—Nbeal2 mice, a model of human gray platelet syndrome, have reduced neutrophil granularity and impaired host defense against systemic Staphylococcus aureus infection. We here aimed to study the role of Nbeal2 deficiency in both leukocytes and platelets during gram-negative pneumonia and sepsis.
APPROACH AND RESULTS—We studied the role of Nbeal2 in platelets and leukocytes during murine pneumonia and sepsis by Klebsiella pneumoniae. Apart from platelet α-granule deficiency and reduced neutrophil granularity, also monocyte granularity was reduced in Nbeal2 mice, whereas plasma levels of MPO (myeloperoxidase), elastase, NGAL (neutrophil gelatinase–associated lipocalin), and MMP-9 (matrix metalloproteinase 9), and leukocyte CD11b expression were increased. Nbeal2 leukocytes showed unaltered in vitro antibacterial response and phagocytosis capacity against Klebsiella, and unchanged reactive nitrogen species and cytokine production. Also during Klebsiella pneumonia and sepsis, Nbeal2 mice had similar bacterial growth in lung and distant body sites, with enhanced leukocyte migration to the bronchoalveolar space. Despite similar infection-induced inflammation, organ damage was increased in Nbeal2 mice, which was also seen during endotoxemia. Platelet-specific Nbeal2 deficiency did not influence leukocyte functions, indicating that Nbeal2 directly modifies leukocytes. Transfusion of Nbeal2 but not of Nbeal2 platelets into thrombocytopenic mice was associated with bleeding in the lung but similar host defense, pointing at a role for platelet α-granules in maintaining vascular integrity but not host defense during Klebsiella pneumosepsis.
CONCLUSIONS—These data show that Nbeal2 deficiency—resulting in gray platelet syndrome—affects platelets, neutrophils, and monocytes, with intact host defense but increased organ damage during gram-negative pneumosepsis.</description><subject>Animals</subject><subject>Blood Platelets - metabolism</subject><subject>Blood Platelets - microbiology</subject><subject>Blood Proteins - deficiency</subject><subject>Blood Proteins - genetics</subject><subject>CD11b Antigen - blood</subject><subject>Disease Models, Animal</subject><subject>Female</subject><subject>Gray Platelet Syndrome - blood</subject><subject>Gray Platelet Syndrome - genetics</subject><subject>Gray Platelet Syndrome - metabolism</subject><subject>Host-Pathogen Interactions</subject><subject>Klebsiella Infections - blood</subject><subject>Klebsiella Infections - genetics</subject><subject>Klebsiella Infections - metabolism</subject><subject>Klebsiella Infections - microbiology</subject><subject>Klebsiella pneumoniae - growth & development</subject><subject>Klebsiella pneumoniae - pathogenicity</subject><subject>Lipocalin-2 - blood</subject><subject>Male</subject><subject>Matrix Metalloproteinase 9 - blood</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Monocytes - metabolism</subject><subject>Monocytes - microbiology</subject><subject>Multiple Organ Failure - blood</subject><subject>Multiple Organ Failure - genetics</subject><subject>Multiple Organ Failure - metabolism</subject><subject>Multiple Organ Failure - microbiology</subject><subject>Neutrophils - metabolism</subject><subject>Neutrophils - microbiology</subject><subject>Pancreatic Elastase - blood</subject><subject>Peroxidase - blood</subject><subject>Platelet Glycoprotein GPIb-IX Complex - genetics</subject><subject>Platelet Glycoprotein GPIb-IX Complex - metabolism</subject><subject>Platelet Transfusion</subject><subject>Pneumonia, Bacterial - blood</subject><subject>Pneumonia, Bacterial - genetics</subject><subject>Pneumonia, Bacterial - metabolism</subject><subject>Pneumonia, Bacterial - microbiology</subject><subject>Sepsis - blood</subject><subject>Sepsis - genetics</subject><subject>Sepsis - metabolism</subject><subject>Sepsis - microbiology</subject><issn>1079-5642</issn><issn>1524-4636</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kEtPwzAQhC0E4v0HOCAfuQT8TOJjIECRUItE4Ro5zroE8ih2QsW_x1ULR067s5oZaT-Ezii5pDSmV9n89TqbZEGkl5xSztkOOqSSiUjEPN4NO0lUJGPBDtCR9--EEMEY2UcHTCkeVHyIVtMSdMNwDrY2NXTmGz90xoH24PHMLXSHc93qBeByHHDeh-u0H3BmLZgBT3o_rKPQecD56Opuge-dbqMpLPRQfwF-6mBs-67WUQ4uHCr8DEtf-xO0Z3Xj4XQ7j9HL3e38ZhI9zu4fbrLHyHAlWGSYVCBSSiTokmsrRUISykUSC61UpQxYGX6xmoOpqspaK1QiBVSWq7SkMT9GF5vepes_R_BD0dbeQNPoDvrRF4zIVBLJ1NrKNlbjeu8d2GLp6la774KSYg282AIPIi02wEPofNs_li1Uf5FfwsEQbwyrvhnA-Y9mXIEr3gL14e2_5h8r_I1g</recordid><startdate>201808</startdate><enddate>201808</enddate><creator>Claushuis, Theodora A.M</creator><creator>de Stoppelaar, Sacha F</creator><creator>de Vos, Alex F</creator><creator>Grootemaat, Anita E</creator><creator>van der Wel, Nicole N</creator><creator>Roelofs, Joris J.T.H</creator><creator>Ware, Jerry</creator><creator>van‘t Veer, Cornelis</creator><creator>van der Poll, Tom</creator><general>American Heart Association, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>201808</creationdate><title>Nbeal2 Deficiency Increases Organ Damage but Does Not Affect Host Defense During Gram-Negative Pneumonia-Derived Sepsis</title><author>Claushuis, Theodora A.M ; de Stoppelaar, Sacha F ; de Vos, Alex F ; Grootemaat, Anita E ; van der Wel, Nicole N ; Roelofs, Joris J.T.H ; Ware, Jerry ; van‘t Veer, Cornelis ; van der Poll, Tom</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3942-c259e48105eab3af54707134764a99d9cef5993fa3ecdddfff49754edf398b163</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animals</topic><topic>Blood Platelets - metabolism</topic><topic>Blood Platelets - microbiology</topic><topic>Blood Proteins - deficiency</topic><topic>Blood Proteins - genetics</topic><topic>CD11b Antigen - blood</topic><topic>Disease Models, Animal</topic><topic>Female</topic><topic>Gray Platelet Syndrome - blood</topic><topic>Gray Platelet Syndrome - genetics</topic><topic>Gray Platelet Syndrome - metabolism</topic><topic>Host-Pathogen Interactions</topic><topic>Klebsiella Infections - blood</topic><topic>Klebsiella Infections - genetics</topic><topic>Klebsiella Infections - metabolism</topic><topic>Klebsiella Infections - microbiology</topic><topic>Klebsiella pneumoniae - growth & development</topic><topic>Klebsiella pneumoniae - pathogenicity</topic><topic>Lipocalin-2 - blood</topic><topic>Male</topic><topic>Matrix Metalloproteinase 9 - blood</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Monocytes - metabolism</topic><topic>Monocytes - microbiology</topic><topic>Multiple Organ Failure - blood</topic><topic>Multiple Organ Failure - genetics</topic><topic>Multiple Organ Failure - metabolism</topic><topic>Multiple Organ Failure - microbiology</topic><topic>Neutrophils - metabolism</topic><topic>Neutrophils - microbiology</topic><topic>Pancreatic Elastase - blood</topic><topic>Peroxidase - blood</topic><topic>Platelet Glycoprotein GPIb-IX Complex - genetics</topic><topic>Platelet Glycoprotein GPIb-IX Complex - metabolism</topic><topic>Platelet Transfusion</topic><topic>Pneumonia, Bacterial - blood</topic><topic>Pneumonia, Bacterial - genetics</topic><topic>Pneumonia, Bacterial - metabolism</topic><topic>Pneumonia, Bacterial - microbiology</topic><topic>Sepsis - blood</topic><topic>Sepsis - genetics</topic><topic>Sepsis - metabolism</topic><topic>Sepsis - microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Claushuis, Theodora A.M</creatorcontrib><creatorcontrib>de Stoppelaar, Sacha F</creatorcontrib><creatorcontrib>de Vos, Alex F</creatorcontrib><creatorcontrib>Grootemaat, Anita E</creatorcontrib><creatorcontrib>van der Wel, Nicole N</creatorcontrib><creatorcontrib>Roelofs, Joris J.T.H</creatorcontrib><creatorcontrib>Ware, Jerry</creatorcontrib><creatorcontrib>van‘t Veer, Cornelis</creatorcontrib><creatorcontrib>van der Poll, Tom</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Arteriosclerosis, thrombosis, and vascular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Claushuis, Theodora A.M</au><au>de Stoppelaar, Sacha F</au><au>de Vos, Alex F</au><au>Grootemaat, Anita E</au><au>van der Wel, Nicole N</au><au>Roelofs, Joris J.T.H</au><au>Ware, Jerry</au><au>van‘t Veer, Cornelis</au><au>van der Poll, Tom</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Nbeal2 Deficiency Increases Organ Damage but Does Not Affect Host Defense During Gram-Negative Pneumonia-Derived Sepsis</atitle><jtitle>Arteriosclerosis, thrombosis, and vascular biology</jtitle><addtitle>Arterioscler Thromb Vasc Biol</addtitle><date>2018-08</date><risdate>2018</risdate><volume>38</volume><issue>8</issue><spage>1772</spage><epage>1784</epage><pages>1772-1784</pages><issn>1079-5642</issn><eissn>1524-4636</eissn><abstract>OBJECTIVE—Nbeal2 mice, a model of human gray platelet syndrome, have reduced neutrophil granularity and impaired host defense against systemic Staphylococcus aureus infection. We here aimed to study the role of Nbeal2 deficiency in both leukocytes and platelets during gram-negative pneumonia and sepsis.
APPROACH AND RESULTS—We studied the role of Nbeal2 in platelets and leukocytes during murine pneumonia and sepsis by Klebsiella pneumoniae. Apart from platelet α-granule deficiency and reduced neutrophil granularity, also monocyte granularity was reduced in Nbeal2 mice, whereas plasma levels of MPO (myeloperoxidase), elastase, NGAL (neutrophil gelatinase–associated lipocalin), and MMP-9 (matrix metalloproteinase 9), and leukocyte CD11b expression were increased. Nbeal2 leukocytes showed unaltered in vitro antibacterial response and phagocytosis capacity against Klebsiella, and unchanged reactive nitrogen species and cytokine production. Also during Klebsiella pneumonia and sepsis, Nbeal2 mice had similar bacterial growth in lung and distant body sites, with enhanced leukocyte migration to the bronchoalveolar space. Despite similar infection-induced inflammation, organ damage was increased in Nbeal2 mice, which was also seen during endotoxemia. Platelet-specific Nbeal2 deficiency did not influence leukocyte functions, indicating that Nbeal2 directly modifies leukocytes. Transfusion of Nbeal2 but not of Nbeal2 platelets into thrombocytopenic mice was associated with bleeding in the lung but similar host defense, pointing at a role for platelet α-granules in maintaining vascular integrity but not host defense during Klebsiella pneumosepsis.
CONCLUSIONS—These data show that Nbeal2 deficiency—resulting in gray platelet syndrome—affects platelets, neutrophils, and monocytes, with intact host defense but increased organ damage during gram-negative pneumosepsis.</abstract><cop>United States</cop><pub>American Heart Association, Inc</pub><pmid>29930006</pmid><doi>10.1161/ATVBAHA.118.311332</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Blood Platelets - metabolism Blood Platelets - microbiology Blood Proteins - deficiency Blood Proteins - genetics CD11b Antigen - blood Disease Models, Animal Female Gray Platelet Syndrome - blood Gray Platelet Syndrome - genetics Gray Platelet Syndrome - metabolism Host-Pathogen Interactions Klebsiella Infections - blood Klebsiella Infections - genetics Klebsiella Infections - metabolism Klebsiella Infections - microbiology Klebsiella pneumoniae - growth & development Klebsiella pneumoniae - pathogenicity Lipocalin-2 - blood Male Matrix Metalloproteinase 9 - blood Mice, Inbred C57BL Mice, Knockout Monocytes - metabolism Monocytes - microbiology Multiple Organ Failure - blood Multiple Organ Failure - genetics Multiple Organ Failure - metabolism Multiple Organ Failure - microbiology Neutrophils - metabolism Neutrophils - microbiology Pancreatic Elastase - blood Peroxidase - blood Platelet Glycoprotein GPIb-IX Complex - genetics Platelet Glycoprotein GPIb-IX Complex - metabolism Platelet Transfusion Pneumonia, Bacterial - blood Pneumonia, Bacterial - genetics Pneumonia, Bacterial - metabolism Pneumonia, Bacterial - microbiology Sepsis - blood Sepsis - genetics Sepsis - metabolism Sepsis - microbiology |
title | Nbeal2 Deficiency Increases Organ Damage but Does Not Affect Host Defense During Gram-Negative Pneumonia-Derived Sepsis |
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