Toll-like receptor 9 signaling is critical for early experimental deep vein thrombosis resolution

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 1, 2011, Pages 43-49

  Henke, Peter K ^a   Mitsuya, Mayo ^a   Luke, Catherine E ^a   Elfline, Megan A ^a   Baldwin, Joseph F ^a   Barry Deatrick, K ^a   Diaz, Jose A ^a   Sood, Vikram ^a   Upchurch, Gilbert R ^a   Wakefield, Thomas W ^a   Hogaboam, Cory ^a   Kunkel, Steven L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

leukocytes; thrombosis; vascular biology; venous thrombosis

Indexed keywords

ALPHA INTERFERON; COLLAGEN; FIBRINOGEN; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 2; MYELOID DIFFERENTIATION FACTOR 88; NOTCH4 RECEPTOR; THROMBIN ANTITHROMBIN COMPLEX; TOLL LIKE RECEPTOR 9;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; DEEP VEIN THROMBOSIS; INFLAMMATION; INTRACELLULAR SIGNALING; MALE; MONOCYTE; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TH1 CELL; WILD TYPE;

ANIMALS; ANTITHROMBIN III; BLOOD COAGULATION; COLLAGEN; CYTOKINES; DISEASE MODELS, ANIMAL; FIBRINOGEN; INFLAMMATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; MYELOID DIFFERENTIATION FACTOR 88; NEUTROPHILS; OLIGODEOXYRIBONUCLEOTIDES; PEPTIDE HYDROLASES; SIGNAL TRANSDUCTION; TH1 CELLS; THROMBELASTOGRAPHY; TIME FACTORS; TOLL-LIKE RECEPTOR 9; VENOUS THROMBOSIS;

EID: 78650869171     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.216317     Document Type: Article

References (30)

1. Wakefield TW, Myers DD, Henke PK. Mechanisms of venous thrombosis and resolution. Arterioscler Thromb Vasc Biol. 2008;28: 387-391.
2. Gangireddy C, Rectenwald JR, Upchurch GR, Wakefield TW, Khuri S, Henderson WG, Henke PK. Risk factors and clinical impact of postoperative symptomatic venous thromboembolism. J Vasc Surg. 2007;45: 335-341, discussion 341-332.
3. Geerts W. Antithrombotic and thrombolytic therapy. Chest. 2008;133: 381s-451s.
4. Henke PK, Varga A, De S, Deatrick CB, Eliason J, Arenberg DA, Sukheepod P, Thanaporn P, Kunkel SL, Upchurch GR Jr, Wakefield TW. Deep vein thrombosis resolution is modulated by monocyte CXCR2- mediated activity in a mouse model. Arterioscler Thromb Vasc Biol. 2004;24:1130-1137.
5. Henke PK, Varma MR, Moaveni DK, Dewyer NA, Moore AJ, Lynch EM, Longo C, Deatrick CB, Kunkel SL, Upchurch GR Jr, Wakefield TW. Fibrotic injury after experimental deep vein thrombosis is determined by the mechanism of thrombogenesis. Thromb Haemost. 2007;98: 1045-1055.
6. Henke PK, Pearce CG, Moaveni DM, Moore AJ, Lynch EM, Longo C, Varma M, Dewyer NA, Deatrick KB, Upchurch GR Jr, Wakefield TW, Hogaboam C, Kunkel SL. Targeted deletion of CCR2 impairs deep vein thombosis resolution in a mouse model. J Immunol. 2006;177: 3388-3397.
7. Imaeda AB, Watanabe A, Sohail MA, Mahmood S, Mohamadnejad M, Sutterwala FS, Flavell RA, Mehal WZ. Acetaminophen-induced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome. J Clin Invest. 2009;119:305-314.
8. Chen CJ, Kono H, Golenbock D, Reed G, Akira S, Rock KL. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat Med. 2007;13:851-856.
9. Beutler B. Inferences, questions and possibilities in Toll-like receptor signalling. Nature. 2004;430:257-263.
10. Barton GM. A calculated response: control of inflammation by the innate immune system. J Clin Invest. 2008;118:413-420.
11. Wagner H. The immunobiology of the TLR9 subfamily. Trends Immunol. 2004;25:381-386.
12. Krieg AM. CpG motifs: the active ingredient in bacterial extracts? Nat Med. 2003;9:831-835.
13. Stevens SL, Ciesielski TM, Marsh BJ, Yang T, Homen DS, Boule JL, Lessov NS, Simon RP, Stenzel-Poore MP. Toll-like receptor 9: a new target of ischemic preconditioning in the brain. J Cereb Blood Flow Metab. 2008;28:1040-1047.
14. Davis HL, Weeratna R, Waldschmidt TJ, Tygrett L, Schorr J, Krieg AM. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. J Immunol. 1998;160: 870-876.
15. Jozsef L, Khreiss T, El Kebir D, Filep JG. Activation of TLR-9 induces IL-8 secretion through peroxynitrite signaling in human neutrophils. J Immunol. 2006;176:1195-1202.
16. Ito T, Schaller M, Hogaboam CM, Standiford TJ, Sandor M, Lukacs NW, Chensue SW, Kunkel SL. TLR9 regulates the mycobacteria-elicited pulmonary granulomatous immune response in mice through DC-derived Notch ligand delta-like 4. J Clin Invest. 2009;119:33-46.
17. Deatrick KB, Eliason JL, Lynch EM, Moore AJ, Dewyer NA, Varma MR, Pearce CG, Upchurch GR, Wakefield TW, Henke PK. Vein wall remodeling after deep vein thrombosis involves matrix metalloproteinases and late fibrosis in a mouse model. J Vasc Surg. 2005;42: 140-148.
18. Schaller MA, Neupane R, Rudd BD, Kunkel SL, Kallal LE, Lincoln P, Lowe JB, Man Y, Lukacs NW. Notch ligand Delta-like 4 regulates disease pathogenesis during respiratory viral infections by modulating Th2 cytokines. J Exp Med. 2007;204:2925-2934.
19. Gallimore MJ, Harris SL, Tappenden KA, Winter M, Jones DW. Urokinase induced fibrinolysis in thromboelastography: a model for studying fibrinolysis and coagulation in whole blood. J Thromb Haemost. 2005;3:2506-2513.
20. Raymond T, Schaller M, Hogaboam CM, Lukacs NW, Rochford R, Kunkel SL. Toll-like receptors, Notch ligands, and cytokines drive the chronicity of lung inflammation. Proc Am Thorac Soc. 2007;4: 635-641.
21. Henke PK, Varma MR, Deatrick KB, Drewyer NA, Lynch EM, Moore AJ, Dubay DA, Sukheepod P, Pearce CG, Upchurch GR Jr, Kunkel SL, Franz MG, Wakefield TW. Neutrophils modulate post-thrombotic vein wall remodeling but not thrombus neovascularization. Thromb Haemost. 2006;95:272-281.
22. Kannemeier C, Shibamiya A, Nakazawa F, Trusheim H, Ruppert C, Markart P, Song Y, Tzima E, Kennerknecht E, Niepmann M, von Bruehl ML, Sedding D, Massberg S, Gunther A, Engelmann B, Preissner KT. Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci USA. 2007;104:6388-6393.
23. Miles K, Clarke DJ, Lu W, Sibinska Z, Beaumont PE, Davidson DJ, Barr TA, Campopiano DJ, Gray M. Dying and necrotic neutrophils are antiinflammatory secondary to the release of-defensins. J Immunol. 2009; 183:2122-2132.
24. Kawai T, Akira S. TLR signaling. Cell Death Differ. 2006;13:816-825.
25. Baccala R, Hoebe K, Kono DH, Beutler B, Theofilopoulos AN. TLRdependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat Med. 2007;13:543-551.
26. Fung E, Tang SM, Canner JP, Morishige K, Arboleda-Velasquez JF, Cardoso AA, Carlesso N, Aster JC, Aikawa M. Delta-like 4 induces notch signaling in macrophages: implications for inflammation. Circulation. 2007;115:2948-2956.
27. Denis MM, Tolley ND, Bunting M, Schwertz H, Jiang H, Lindemann S, Yost CC, Rubner FJ, Albertine KH, Swoboda KJ, Fratto CM, Tolley E, Kraiss LW, McIntyre TM, Zimmerman GA, Weyrich AS. Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell. 2005;122:379-391.
28. Ishii KJ, Akira S. Innate immune recognition of, and regulation by, DNA. Trends Immunol. 2006;27:525-532. (Pubitemid 44515161)
29. Moaveni DK, Lynch EM, Luke C, Sood V, Upchurch GR, Wakefield TW, Henke PK. Vein wall re-endothelialization after deep vein thrombosis is improved with low-molecular-weight heparin. J Vasc Surg. 2008;47:616-624.
30. Merli G, Spyropoulos AC, Caprini JA. Use of emerging oral anticoagulants in clinical practice: translating results from clinical trials to orthopedic and general surgical patient populations. Ann Surg. 2009;250: 219-228.