Reduced hind limb ischemia-reperfusion injury in Toll-like receptor-4 mutant mice is associated with decreased neutrophil extracellular traps

Journal of Vascular Surgery

Volumn 58, Issue 6, 2013, Pages 1627-1636

  Oklu, Rahmi ^a   Albadawi, Hassan ^a   Jones, John E ^a   Yoo, Hyung Jin ^a   Watkins, Michael T ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; KERATINOCYTE DERIVED CHEMOKINE; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOPEROXIDASE; TOLL LIKE RECEPTOR 4; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; BLOOD VESSEL INJURY; CELL INFILTRATION; ENHANCER REGION; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; LIMB ISCHEMIA; MONOCYTE; MOUSE; NEUTROPHIL; NEUTROPHIL EXTRACELLULAR TRAP; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; SKELETAL MUSCLE; THROMBOGENICITY; TOURNIQUET;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DNA MUTATIONAL ANALYSIS; HINDLIMB; MICE; MICE, TRANSGENIC; MUTATION; NEUTROPHILS; REPERFUSION INJURY; RNA; TOLL-LIKE RECEPTOR 4;

EID: 84888343739     PISSN: 07415214     EISSN: 10976809     Source Type: Journal    
DOI: 10.1016/j.jvs.2013.02.241     Document Type: Article

References (40)

1. J. Oyama, C. Blais Jr., X. Liu, M. Pu, L. Kobzik, and R.A. Kelly Reduced myocardial ischemia-reperfusion injury in toll-like receptor 4-deficient mice Circulation 109 2004 784 789
2. X.D. Shen, F. Gao, B. Ke, Y. Zhai, C.R. Lassman, and S. Tsuchihashi Inflammatory responses in a new mouse model of prolonged hepatic cold ischemia followed by arterialized orthotopic liver transplantation Liver Transpl 11 2005 1273 1281
3. X.D. Shen, B. Ke, Y. Zhai, F. Gao, R.W. Busuttil, and G. Cheng Toll-like receptor and heme oxygenase-1 signaling in hepatic ischemia/reperfusion injury Am J Transplant 5 2005 1793 1800
4. S.C. Tang, T.V. Arumugam, X. Xu, A. Cheng, M.R. Mughal, and D.G. Jo Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits Proc Natl Acad Sci U S A 104 2007 13798 13803
5. J. Fan, A. Kapus, P.A. Marsden, Y.H. Li, G. Oreopoulos, and J.C. Marshall Regulation of Toll-like receptor 4 expression in the lung following hemorrhagic shock and lipopolysaccharide J Immunol 168 2002 5252 5259
6. A. Tsung, R.A. Hoffman, K. Izuishi, N.D. Critchlow, A. Nakao, and M.H. Chan Hepatic ischemia/reperfusion injury involves functional TLR4 signaling in nonparenchymal cells J Immunol 175 2005 7661 7668
7. H. Wu, G. Chen, K.R. Wyburn, J. Yin, P. Bertolino, and J.M. Eris TLR4 activation mediates kidney ischemia/reperfusion injury J Clin Invest 117 2007 2847 2859
8. T.A. Fuchs, U. Abed, C. Goosmann, R. Hurwitz, I. Schulze, and V. Wahn Novel cell death program leads to neutrophil extracellular traps J Cell Biol 176 2007 231 241
9. A. Brill, T.A. Fuchs, A.S. Savchenko, G.M. Thomas, K. Martinod, and S.F. De Meyer Neutrophil extracellular traps promote deep vein thrombosis in mice J Thromb Haemost 10 2012 136 144
10. V. Brinkmann, U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, and D.S. Weiss Neutrophil extracellular traps kill bacteria Science 303 2004 1532 1535
11. R. Oklu, H. Albadawi, M.T. Watkins, M. Monestier, M. Sillesen, and S. Wicky Detection of extracellular genomic DNA scaffold in human thrombus: implications for the use of deoxyribonuclease enzymes in thrombolysis J Vasc Interv Radiol 23 2012 712 718
12. S.R. Clark, A.C. Ma, S.A. Tavener, B. McDonald, Z. Goodarzi, and M.M. Kelly Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood Nat Med 13 2007 463 469
13. T.A. Fuchs, A. Brill, D. Duerschmied, D. Schatzberg, M. Monestier, and D.D. Myers Jr. Extracellular DNA traps promote thrombosis Proc Natl Acad Sci U S A 107 2010 15880 15885
14. A. Poltorak, X. He, I. Smirnova, M.Y. Liu, C. Van Huffel, and X. Du Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene Science 282 1998 2085 2088
15. R.S. Crawford, F.F. Hashmi, J.E. Jones, H. Albadawi, M. McCormack, and K. Eberlin A novel model of acute murine hindlimb ischemia Am J Physiol Heart Circ Physiol 292 2007 H830 H837
16. M.C. McCormack, E. Kwon, K.R. Eberlin, M. Randolph, D.S. Friend, and A.C. Thomas Development of reproducible histologic injury severity scores: skeletal muscle reperfusion injury Surgery 143 2008 126 133
17. Y. Doring, O. Soehnlein, M. Drechsler, E. Shagdarsuren, S.M. Chaudhari, and S. Meiler Hematopoietic interferon regulatory factor 8-deficiency accelerates atherosclerosis in mice Arterioscler Thromb Vasc Biol 32 2012 1613 1623
18. A. Schreiber, C.T. Pham, Y. Hu, W. Schneider, F.C. Luft, and R. Kettritz Neutrophil serine proteases promote IL-1beta generation and injury in necrotizing crescentic glomerulonephritis J Am Soc Nephrol 23 2012 470 482
19. M.J. Losman, T.M. Fasy, K.E. Novick, and M. Monestier Monoclonal autoantibodies to subnucleosomes from a MRL/Mp(-)+/+ mouse. Oligoclonality of the antibody response and recognition of a determinant composed of histones H2A, H2B, and DNA J Immunol 148 1992 1561 1569
20. P.L. Sappington, R.J. Cruz Jr., T. Harada, R. Yang, Y. Han, and J.A. Englert The ethyl pyruvate analogues, diethyl oxaloproprionate, 2-acetamidoacrylate, and methyl-2-acetamidoacrylate, exhibit anti-inflammatory properties in vivo and/or in vitro Biochem Pharmacol 70 2005 1579 1592
21. P.K. Henke, M. Mitsuya, C.E. Luke, M.A. Elfline, J.F. Baldwin, and K.B. Deatrick Toll-like receptor 9 signaling is critical for early experimental deep vein thrombosis resolution Arterioscler Thromb Vasc Biol 31 2011 43 49
22. S. Akira, and K. Takeda Toll-like receptor signalling Nat Rev Immunol 4 2004 499 511
23. A. Granfeldt, R. Jiang, N.P. Wang, J. Mykytenko, S. Eldaif, and J. Deneve Neutrophil inhibition contributes to cardioprotection by postconditioning Acta Anaesthesiol Scand 56 2012 48 56
24. Y. Liu, T. Kalogeris, M. Wang, M.Y. Zuidema, Q. Wang, and H. Dai Hydrogen sulfide preconditioning or neutrophil depletion attenuates ischemia- reperfusion-induced mitochondrial dysfunction in rat small intestine Am J Physiol Gastrointest Liver Physiol 302 2012 G44 G54
25. V. Marcos, Z. Zhou, A.O. Yildirim, A. Bohla, A. Hector, and L. Vitkov CXCR2 mediates NADPH oxidase-independent neutrophil extracellular trap formation in cystic fibrosis airway inflammation Nat Med 16 2010 1018 1023
26. Y. Wang, M. Li, S. Stadler, S. Correll, P. Li, and D. Wang Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation J Cell Biol 184 2009 205 213
27. S. Massberg, L. Grahl, M.L. von Bruehl, D. Manukyan, S. Pfeiler, and C. Goosmann Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases Nat Med 16 2010 887 896
28. J. Xu, X. Zhang, M. Monestier, N.L. Esmon, and C.T. Esmon Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury J Immunol 187 2011 2626 2631
29. J. Xu, X. Zhang, R. Pelayo, M. Monestier, C.T. Ammollo, and F. Semeraro Extracellular histones are major mediators of death in sepsis Nat Med 15 2009 1318 1321
30. A.V. Dubois, A. Gauthier, D. Brea, F. Varaigne, P. Diot, and F. Gauthier Influence of DNA on the activities and inhibition of neutrophil serine proteases in cystic fibrosis sputum Am J Respir Cell Mol Biol 47 2012 80 86
31. R.S. Crawford, H. Albadawi, M.D. Atkins, J.J. Jones, M.F. Conrad, and W.G. Austen Jr. Postischemic treatment with ethyl pyruvate prevents adenosine triphosphate depletion, ameliorates inflammation, and decreases thrombosis in a murine model of hind-limb ischemia and reperfusion J Trauma 70 2011 103 110
32. S. Muthupalani, Z. Ge, Y. Feng, B. Rickman, M. Mobley, and A. McCabe Systemic macrophage depletion inhibits Helicobacter bilis-induced proinflammatory cytokine-mediated typhlocolitis and impairs bacterial colonization dynamics in a BALB/c Rag2-/- mouse model of inflammatory bowel disease Infect Immun 80 2012 4388 4397
33. P. Riquelme, S. Tomiuk, A. Kammler, F. Fandrich, H.J. Schlitt, and E.K. Geissler IFN-gamma-induced iNOS expression in mouse regulatory macrophages prolongs allograft survival in fully immunocompetent recipients Mol Ther 21 2013 409 422
34. R.S. Crawford, H. Albadawi, M.D. Atkins, J.E. Jones, H.J. Yoo, and M.F. Conrad Postischemic poly (ADP-ribose) polymerase (PARP) inhibition reduces ischemia reperfusion injury in a hind-limb ischemia model Surgery 148 2010 110 118
35. T.A. Abbruzzese, H. Albadawi, J. Kang, V.I. Patel, J.H. Yoo, and G.M. Lamuraglia Enoxaparin does not ameliorate limb ischemia-reperfusion injury J Surg Res 147 2008 260 266
36. M. Mullarkey, J.R. Rose, J. Bristol, T. Kawata, A. Kimura, and S. Kobayashi Inhibition of endotoxin response by e5564, a novel Toll-like receptor 4-directed endotoxin antagonist J Pharmacol Exp Ther 304 2003 1093 1102
37. L.C. Parker, M.K. Whyte, S.N. Vogel, S.K. Dower, and I. Sabroe Toll-like receptor (TLR)2 and TLR4 agonists regulate CCR expression in human monocytic cells J Immunol 172 2004 4977 4986
38. Y. Wu, E.L. Lousberg, L.M. Moldenhauer, J.D. Hayball, J.K. Coller, and K.C. Rice Inhibiting the TLR4-MyD88 signalling cascade by genetic or pharmacological strategies reduces acute alcohol-induced sedation and motor impairment in mice Br J Pharmacol 165 2012 1319 1329
39. X.P. Gao, T.J. Standiford, A. Rahman, M. Newstead, S.M. Holland, and M.C. Dinauer Role of NADPH oxidase in the mechanism of lung neutrophil sequestration and microvessel injury induced by Gram-negative sepsis: studies in p47phox-/- and gp91phox-/- mice J Immunol 168 2002 3974 3982
40. H.X. Nguyen, A.J. Lusis, and J.G. Tidball Null mutation of myeloperoxidase in mice prevents mechanical activation of neutrophil lysis of muscle cell membranes in vitro and in vivo J Physiol 565 2005 403 413