Abstract
Hyperinflammatory responses can lead to a variety of diseases, including sepsis. We now report that extracellular histones released in response to inflammatory challenge contribute to endothelial dysfunction, organ failure and death during sepsis. They can be targeted pharmacologically by antibody to histone or by activated protein C (APC). Antibody to histone reduced the mortality of mice in lipopolysaccharide (LPS), tumor necrosis factor (TNF) or cecal ligation and puncture models of sepsis. Extracellular histones are cytotoxic toward endothelium in vitro and are lethal in mice. In vivo, histone administration resulted in neutrophil margination, vacuolated endothelium, intra-alveolar hemorrhage and macro- and microvascular thrombosis. We detected histone in the circulation of baboons challenged with Escherichia coli, and the increase in histone levels was accompanied by the onset of renal dysfunction. APC cleaves histones and reduces their cytotoxicity. Co-infusion of APC with E. coli in baboons or histones in mice prevented lethality. Blockade of protein C activation exacerbated sublethal LPS challenge into lethality, which was reversed by treatment with antibody to histone. We conclude that extracellular histones are potential molecular targets for therapeutics for sepsis and other inflammatory diseases.
MeSH Terms
Animals
Antibodies/pharmacology,therapeutic use
Cattle
Cell Line, Transformed
Disease Models, Animal
Endothelium/drug effects,pathology,ultrastructure
Escherichia coli/physiology
Extracellular Fluid/drug effects,metabolism
Flow Cytometry
Hemorrhage/etiology,pathology
Histones/drug effects,immunology,metabolism,pharmacology
Kidney Diseases/metabolism
Macrophages/drug effects,metabolism,ultrastructure
Mice
Microscopy, Electron, Transmission/methods
Neutrophils/drug effects,pathology
Oligopeptides/pharmacology,therapeutic use
Papio
Polysaccharides/adverse effects
Sepsis/drug therapy,etiology,mortality,pathology
Tumor Necrosis Factor-alpha/adverse effects
Chemicals
Antibodies
Histones
Oligopeptides
Polysaccharides
Tumor Necrosis Factor-alpha
protein C activator peptide
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Xu Jun
Oklahoma Medical Research Foundation, Oklahoma City, OK, USA.
Zhang Xiaomei
Pelayo Rosana
Monestier Marc
Ammollo Concetta T
Semeraro Fabrizio
Taylor Fletcher B
Esmon Naomi L
Lupu Florea
Esmon Charles T
References (21)
21 references, click to expand
-
Structure and binding properties of monoclonal antibodies to core histones from autoimmune mice.
Mol Immunol. 1993 Aug;30(12):1069-75
PMID: 8366857
-
HMG-1 as a late mediator of endotoxin lethality in mice.
Science. 1999 Jul 9;285(5425):248-51
PMID: 10398600
-
Efficacy and safety of recombinant human activated protein C for severe sepsis.
N Engl J Med. 2001 Mar 8;344(10):699-709
PMID: 11236773
-
The cytoprotective protein C pathway.
Blood. 2007 Apr 15;109(8):3161-72
PMID: 17110453
-
Phosphatidylethanolamine incorporation into vesicles selectively enhances factor Va inactivation by activated protein C.
J Biol Chem. 1994 Jan 14;269(2):816-9
PMID: 8288632
-
Neutrophil extracellular traps kill bacteria.
Science. 2004 Mar 5;303(5663):1532-5
PMID: 15001782
-
The history, properties, and biological effects of cachectin.
Biochemistry. 1988 Oct 4;27(20):7575-82
PMID: 3061461
-
Elevated nucleosome levels in systemic inflammation and sepsis.
Crit Care Med. 2003 Jul;31(7):1947-51
PMID: 12847387
-
Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation.
Blood. 2008 Mar 15;111(6):3070-80
PMID: 18182576
-
Reconstitution of the human endothelial cell protein C receptor with thrombomodulin in phosphatidylcholine vesicles enhances protein C activation.
J Biol Chem. 1999 Mar 5;274(10):6704-10
PMID: 10037768
-
The protein C pathway.
Chest. 2003 Sep;124(3 Suppl):26S-32S
PMID: 12970121
-
Endogenous activated protein C signaling is critical to protection of mice from lipopolysaccaride-induced septic shock.
J Thromb Haemost. 2009 May;7(5):851-6
PMID: 19320827
-
Severe protein C deficiency predicts early death in severe sepsis.
Crit Care Med. 2004 May;32(5 Suppl):S223-8
PMID: 15118522
-
Localization and production of plasminogen activator inhibitor-1 in human healthy and atherosclerotic arteries.
Arterioscler Thromb. 1993 Jul;13(7):1090-100
PMID: 7686395
-
Acute inflammation is exacerbated in mice genetically predisposed to a severe protein C deficiency.
Blood. 2007 Mar 1;109(5):1984-91
PMID: 17047151
-
Activation of endothelial cell protease activated receptor 1 by the protein C pathway.
Science. 2002 Jun 7;296(5574):1880-2
PMID: 12052963
-
Management of sepsis.
N Engl J Med. 2006 Oct 19;355(16):1699-713
PMID: 17050894
-
Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood.
Nat Med. 2007 Apr;13(4):463-9
PMID: 17384648
-
Endotoxemia and sepsis mortality reduction by non-anticoagulant activated protein C.
J Exp Med. 2007 Oct 1;204(10):2439-48
PMID: 17893198
-
Immunodesign of experimental sepsis by cecal ligation and puncture.
Nat Protoc. 2009;4(1):31-6
PMID: 19131954
-
Protein C prevents the coagulopathic and lethal effects of Escherichia coli infusion in the baboon.
J Clin Invest. 1987 Mar;79(3):918-25
PMID: 3102560