PAD4-deficiency does not affect bacteremia in polymicrobial sepsis and ameliorates endotoxemic shock

Blood

Volumn 125, Issue 12, 2015, Pages 1948-1956

  Martinod, Kimberly ^a   Fuchs, Tobias A ^a,b,d   Zitomersky, Naamah L ^b   Wong, Siu Ling ^a,b   Demers, Melanie ^a,b   Gallant, Maureen ^b   Wang, Yanming ^c   Wagner, Denisa D ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CELL NUCLEUS DNA; HISTONE; PROTEIN ARGININE DEIMINASE; PROTEIN ARGININE DEIMINASE 4; REACTIVE OXYGEN METABOLITE; THIOGLYCOLIC ACID; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; HYDROLASE; LIPOPOLYSACCHARIDE; PEPTIDYLARGININE DEIMINASE 4, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; BACTERIAL INFECTION; BACTERIAL LOAD; BLOOD CELL COUNT; CONTROLLED STUDY; ENDOTOXEMIA; ENZYME DEFICIENCY; EXTRACELLULAR TRAP; FLOW CYTOMETRY; INFLAMMATION; MOUSE; NEUTROPHIL; NONHUMAN; PERITONITIS; PRIORITY JOURNAL; SALMONELLA ENTERICA; SEPSIS; SEPTIC SHOCK; THROMBOSIS; ANIMAL; C57BL MOUSE; CHEMISTRY; CROSS BREEDING; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LEUKOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTEREMIA; CROSSES, GENETIC; ENDOTOXEMIA; FLOW CYTOMETRY; HISTONES; HYDROLASES; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHIL ACTIVATION; NEUTROPHILS; PERITONITIS; SEPSIS;

EID: 84925357077     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-07-587709     Document Type: Article

References (61)

1. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med. 2001;29(7):1303-1310.
2. th ed. Philadelphia, PA: Saunders-Elsevier; 2010:111-134.
3. Angus DC, van der Poll T. Severe sepsis and septic shock. N Engl J Med. 2013;369(9):840-851.
4. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532-1535.
5. Brinkmann V, Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs. Nat Rev Microbiol. 2007;5(8):577-582.
6. Yipp BG, Kubes P. NETosis: how vital is it? Blood. 2013;122(16):2784-2794.
7. Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13(4):463-469.
8. Gardiner EE, Andrews RK. Neutrophil extracellular traps (NETs) and infection-related vascular dysfunction. Blood Rev. 2012;26(6):255-259.
9. Xu J, Zhang X, Pelayo R, et al. Extracellular histones are major mediators of death in sepsis. Nat Med. 2009;15(11):1318-1321.
10. Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol. 2013;13(1):34-45.
11. Martinod K, Wagner DD. Thrombosis: tangled up in NETs. Blood. 2014;123(18):2768-2776.
12. Margraf S, Lögters T, Reipen J, Altrichter J, Scholz M, Windolf J. Neutrophil-derived circulating free DNA (cf-DNA/NETs): a potential prognostic marker for posttraumatic development of inflammatory second hit and sepsis. Shock. 2008;30(4):352-358.
13. Meng W, Paunel-Görgülü A, Flohé S, et al. Deoxyribonuclease is a potential counter regulator of aberrant neutrophil extracellular traps formation after major trauma. Mediators Inflamm. 2012;2012:149560.
14. Kambas K, Mitroulis I, Apostolidou E, et al. Autophagy mediates the delivery of thrombogenic tissue factor to neutrophil extracellular traps in human sepsis. PLoS ONE. 2012;7(9):e45427.
15. Menegazzi R, Decleva E, Dri P. Killing by neutrophil extracellular traps: fact or folklore? Blood. 2012;119(5):1214-1216.
16. Massberg S, Grahl L, von Bruehl ML, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med. 2010;16(8):887-896.
17. McDonald B, Urrutia R, Yipp BG, Jenne CN, Kubes P. Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe. 2012;12(3):324-333.
18. Yipp BG, Petri B, Salina D, et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med. 2012;18(9):1386-1393.
19. Meng W, Paunel-Görgülü A, Flohé S, et al. Depletion of neutrophil extracellular traps in vivo results in hypersusceptibility to polymicrobial sepsis in mice. Crit Care. 2012;16(4):R137.
20. Cools-Lartigue J, Spicer J, McDonald B, et al. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J Clin Invest. 2013;123(8):3446-3458.
21. Farrera C, Fadeel B. Macrophage clearance of neutrophil extracellular traps is a silent process. J Immunol. 2013;191(5):2647-2656.
22. Luo L, Zhang S, Wang Y, et al. Proinflammatory role of neutrophil extracellular traps in abdominal sepsis. Am J Physiol Lung Cell Mol Physiol. 2014;307(7):L586-L596.
23. Fuchs TA, Brill A, Duerschmied D, et al. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA. 2010;107(36):15880-15885.
24. Brill A, Fuchs TA, Savchenko AS, et al. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost. 2012;10(1):136-144.
25. von Brühl ML, Stark K, Steinhart A, et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med. 2012;209(4):819-835.
26. Li P, Li M, Lindberg MR, Kennett MJ, Xiong N, Wang Y. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med. 2010;207(9):1853-1862.
27. Wang Y, Li M, Stadler S, et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J Cell Biol. 2009;184(2):205-213.
28. Martinod K, Demers M, Fuchs TA, et al. Neutrophil histone modification by peptidylarginine deiminase 4 is critical for deep vein thrombosis in mice. Proc Natl Acad Sci USA. 2013;110(21):8674-8679.
29. Savchenko AS, Borissoff JI, Martinod K, et al. VWF-mediated leukocyte recruitment with chromatin decondensation by PAD4 increases myocardial ischemia/reperfusion injury in mice. Blood. 2014;123(1):141-148.
30. Urban CF, Ermert D, Schmid M, et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 2009;5(10):e1000639.
31. Xu J, Zhang X, Monestier M, Esmon NL, Esmon CT. Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury. J Immunol. 2011;187(5):2626-2631.
32. Semeraro F, Ammollo CT, Morrissey JH, et al. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood. 2011;118(7):1952-1961.
33. Ammollo CT, Semeraro F, Xu J, Esmon NL, Esmon CT. Extracellular histones increase plasma thrombin generation by impairing thrombomodulin-dependent protein C activation. J Thromb Haemost. 2011;9(9):1795-1803.
34. Gupta AK, Hasler P, Holzgreve W, Gebhardt S, Hahn S. Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Hum Immunol. 2005;66(11):1146-1154.
35. Saffarzadeh M, Juenemann C, Queisser MA, et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS ONE. 2012;7(2):e32366.
36. Chen Y, Junger WG. Measurement of oxidative burst in neutrophils. Methods Mol Biol. 2012;844:115-124.
37. Rittirsch D, Huber-Lang MS, Flierl MA, Ward PA. Immunodesign of experimental sepsis by cecal ligation and puncture. Nat Protoc. 2009;4(1):31-36.
38. Demers M, Krause DS, Schatzberg D, et al. Cancers predispose neutrophils to release extracellular DNA traps that contribute to cancer-associated thrombosis. Proc Natl Acad Sci USA. 2012;109(32):13076-13081.
39. Kessenbrock K, Krumbholz M, Schönermarck U, et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med. 2009;15(6):623-625.
40. Radic M, Marion TN. Neutrophil extracellular chromatin traps connect innate immune response to autoimmunity. Semin Immunopathol. 2013;35(4):465-480.
41. De Meyer SF, Suidan GL, Fuchs TA, Monestier M, Wagner DD. Extracellular chromatin is an important mediator of ischemic stroke in mice. Arterioscler Thromb Vasc Biol. 2012;32(8):1884-1891.
42. Fuchs TA, Bhandari AA, Wagner DD. Histones induce rapid and profound thrombocytopenia in mice. Blood. 2011;118(13):3708-3714.
43. Li Y, Liu B, Fukudome EY, et al. Identification of citrullinated histone H3 as a potential serum protein biomarker in a lethal model of lipopolysaccharide-induced shock. Surgery. 2011;150(3):442-451.
44. Remick DG, Newcomb DE, Bolgos GL, Call DR. Comparison of the mortality and inflammatory response of two models of sepsis: lipopolysaccharide vs. cecal ligation and puncture. Shock. 2000;13(2):110-116.
45. Allam R, Scherbaum CR, Darisipudi MN, et al. Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4. J Am Soc Nephrol. 2012;23(8):1375-1388.
46. Thomas GM, Carbo C, Curtis BR, et al. Extracellular DNA traps are associated with the pathogenesis of TRALI in humans and mice. Blood. 2012;119(26):6335-6343.
47. Caudrillier A, Kessenbrock K, Gilliss BM, et al. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest. 2012;122(7):2661-2671.
48. Latifi SQ, O'Riordan MA, Levine AD. Interleukin-10 controls the onset of irreversible septic shock. Infect Immun. 2002;70(8):4441-4446.
49. Kasten KR, Muenzer JT, Caldwell CC. Neutrophils are significant producers of IL-10 during sepsis. Biochem Biophys Res Commun. 2010;393(1):28-31.
50. Zhang X, Majlessi L, Deriaud E, Leclerc C, Lo-Man R. Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity. 2009;31(5):761-771.
51. Esmon CT. Molecular circuits in thrombosis and inflammation. Thromb Haemost. 2013;109(3):416-420.
52. Wildhagen KC, García de Frutos P, Reutelingsperger CP, et al. Nonanticoagulant heparin prevents histone-mediated cytotoxicity in vitro and improves survival in sepsis. Blood. 2014;123(7):1098-1101.
53. Bernard GR, Vincent JL, Laterre PF, et al; Recombinant Human Protein C Worldwide Evaluation in Severe Sepsis (PROWESS) study group. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med. 2001;344(10):699-709.
54. Li Y, Liu Z, Liu B, et al. Citrullinated histone H3: a novel target for the treatment of sepsis. Surgery. 2014;156(2):229-234.
55. Branzk N, Lubojemska A, Hardison SE, et al. Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol. 2014;15(11):1017-1025.
56. Nauseef WM. Proteases, neutrophils, and periodontitis: the NET effect. J Clin Invest. 2014;124(10):4237-4239.
57. Sørensen OE, Clemmensen SN, Dahl SL, et al. Papillon-Lefèvre syndrome patient reveals species-dependent requirements for neutrophil defenses. J Clin Invest. 2014;124(10):4539-4548.
58. Sumby P, Barbian KD, Gardner DJ, et al. Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc Natl Acad Sci USA. 2005;102(5):1679-1684.
59. Beiter K, Wartha F, Albiger B, Normark S, Zychlinsky A, Henriques-Normark B. An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol. 2006;16(4):401-407.
60. Buchanan JT, Simpson AJ, Aziz RK, et al. DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol. 2006;16(4):396-400.
61. Lewis HD, Liddle J, Coote JE, et al. Inhibition of PAD4 activity is sufficient to disrupt mouse and human NET formation. [published online ahead of print January 26, 2015]. Nat Chem Biol.