Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo

Journal of Experimental Medicine

Volumn 209, Issue 4, 2012, Pages 819-835

  von Brühl, Marie Luise ^a,c   Stark, Konstantin ^a,c   Steinhart, Alexander ^a,c   Chandraratne, Sue ^a,c   Konrad, Ildiko ^a,c   Lorenz, Michael ^a,c   Khandoga, Alexander ^a,c   Tirniceriu, Anca ^a,c   Coletti, Raffaele ^a,c   Köllnberger, Maria ^a,c   Byrne, Robert A ^a,c   Laitinen, Iina ^b   Walch, Axel ^d   Brill, Alexander ^e   Pfeiler, Susanne ^f   Manukyan, Davit ^f   Braun, Siegmund ^a   Lange, Philipp ^g   Riegger, Julia ^a,c   Ware, Jerry ^h   Eckart, Annekathrin ^a,c   Haidari, Selgai ^a,c   Rudelius, Martina ^a   Schulz, Christian ^a,c,i   Echtler, Katrin ^a,c   Brinkmann, Volker ^j   Schwaiger, Markus ^b   Preissner, Klaus T ^k   Wagner, Denisa D ^e   Mackman, Nigel ^l   Engelmann, Bernd ^f   Massberg, Steffen ^a,c   more..

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c Munich Heart Alliance   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f Institut fur Klinische Chemie   (Germany)

^g LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^h UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

ⁱ KING'S COLLEGE LONDON   (United Kingdom)

^j MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^k JUSTUS LIEBIG UNIVERSITY   (Germany)

^l UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 12; FIBRIN; GLYCOPROTEIN IB ALPHA; THROMBOPLASTIN; PADGEM PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL FEATURE; DEEP VEIN THROMBOSIS; EPIFLUORESCENCE MICROSCOPY; IMMUNOPATHOGENESIS; INNATE IMMUNITY; MONOCYTE; MOUSE; NEUTROPENIA; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; THROMBOCYTE; ANIMAL; C57BL MOUSE; CELL COMMUNICATION; METABOLISM; PHYSIOLOGY; VEIN THROMBOSIS;

ANIMALS; BLOOD PLATELETS; CELL COMMUNICATION; FACTOR XII; MICE; MICE, INBRED C57BL; MONOCYTES; NEUTROPHILS; P-SELECTIN; THROMBOPLASTIN; VENOUS THROMBOSIS;

EID: 84861750668     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20112322     Document Type: Article

References (60)

1. Ammollo, C.T., F. Semeraro, J. Xu, N.L. Esmon, and C.T. Esmon. 2011. Extracellular histones increase plasma thrombin generation by impairing thrombomodulin-dependent protein C activation. J. Thromb. Haemost. 9:1795-1803. http://dx.doi.org/10.1111/j.1538-7836.2011.04422.x
2. Angelillo-Scherrer, A., P. de Frutos, C. Aparicio, E. Melis, P. Savi, F. Lupu, J. Arnout, M. Dewerchin, M. Hoylaerts, J. Herbert, et al. 2001. Deficiency or inhibition of Gas6 causes platelet dysfunction and protects mice against thrombosis. Nat. Med. 7:215-221. http://dx.doi.org/10.1038/84667
3. Brill, A., T.A. Fuchs, A.K. Chauhan, J.J. Yang, S.F. De Meyer, M. Köllnberger, T.W. Wakefield, B. Lämmle, S. Massberg, and D.D. Wagner. 2011. von Willebrand factor-mediated platelet adhesion is critical for deep vein thrombosis in mouse models. Blood. 117:1400-1407. http://dx.doi.org/10.1182/blood-2010-05-287623
4. Brinkmann, V., U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, D.S. Weiss, Y. Weinrauch, and A. Zychlinsky. 2004. Neutrophil extracellular traps kill bacteria. Science. 303:1532-1535. http://dx.doi.org/10.1126/science.1092385
5. Bucek, R.A., M. Reiter, P. Quehenberger, and E. Minar. 2002. C-reactive protein in the diagnosis of deep vein thrombosis. Br. J. Haematol. 119:385-389. http://dx.doi.org/10.1046/j.1365-2141.2002.03886.x
6. Cheng, Q., E.I. Tucker, M.S. Pine, I. Sisler, A. Matafonov, M.F. Sun, T.C. White-Adams, S.A. Smith, S.R. Hanson, O.J. McCarty, et al. 2010. A role for factor XIIa-mediated factor XI activation in thrombus formation in vivo. Blood. 116:3981-3989. http://dx.doi.org/10.1182/blood-2010-02-270918
7. Clark, S.R., A.C. Ma, S.A. Tavener, B. McDonald, Z. Goodarzi, M.M. Kelly, K.D. Patel, S. Chakrabarti, E. McAvoy, G.D. Sinclair, et al. 2007. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat. Med. 13:463-469. http://dx.doi.org/10.1038/nm1565
8. Clausen, B.E., C. Burkhardt, W. Reith, R. Renkawitz, and I. Förster. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8:265-277. http://dx.doi.org/10.1023/A:1008942828960
9. Cohen, A.T., G. Agnelli, F.A. Anderson, J.I. Arcelus, D. Bergqvist, J.G. Brecht, I.A. Greer, J.A. Heit, J.L. Hutchinson, A.K. Kakkar, et al; VTE Impact Assessment Group in Europe (VITAE). 2007. Venous thromboembolism (VTE) in Europe. The number of VTE events and associated morbidity and mortality. Thromb. Haemost. 98:756-764.
10. Day, S.M., J.L. Reeve, B. Pedersen, D.M. Farris, D.D. Myers, M. Im, T.W. Wakefield, N. Mackman, and W.P. Fay. 2005. Macrovascular thrombosis is driven by tissue factor derived primarily from the blood vessel wall. Blood. 105:192-198. http://dx.doi.org/10.1182/blood-2004-06-2225
11. Diaz, J.A., A.E. Hawley, C.M. Alvarado, A.M. Berguer, N.K. Baker, S.K. Wrobleski, T.W. Wakefield, B.R. Lucchesi, and D.D. Myers Jr. 2010. Thrombogenesis with continuous blood flow in the inferior vena cava. A novel mouse model. Thromb. Haemost. 104:366-375. http://dx.doi.org/10.1160/TH09-09-0672
12. Eitzman, D.T., R.J. Westrick, E.G. Nabel, and D. Ginsburg. 2000. Plasminogen activator inhibitor-1 and vitronectin promote vascular thrombosis in mice. Blood. 95:577-580.
13. Esmon, C.T. 2009. Basic mechanisms and pathogenesis of venous thrombosis. Blood Rev. 23:225-229. http://dx.doi.org/10.1016/j.blre.2009.07.002
14. Faust, N., F. Varas, L.M. Kelly, S. Heck, and T. Graf. 2000. Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood. 96:719-726.
15. Fuchs, T.A., A. Brill, D. Duerschmied, D. Schatzberg, M. Monestier, D.D. Myers Jr., S.K. Wrobleski, T.W. Wakefield, J.H. Hartwig, and D.D. Wagner. 2010. Extracellular DNA traps promote thrombosis. Proc. Natl. Acad. Sci. USA. 107:15880-15885. http://dx.doi.org/10.1073/pnas.1005743107
16. Furie, B., and B.C. Furie. 2007. In vivo thrombus formation. J. Thromb. Haemost. 5:12-17. http://dx.doi.org/10.1111/j.1538-7836.2007.02482.x
17. Gailani, D., N.M. Lasky, and G.J.J. Broze Jr. 1997. A murine model of factor XI deficiency. Blood Coagul. Fibrinolysis. 8:134-144. http://dx.doi.org/10.1097/00001721-199703000-00008
18. Garcia-Romo, G.S., S. Caielli, B. Vega, J. Connolly, F. Allantaz, Z. Xu, M. Punaro, J. Baisch, C. Guiducci, R.L. Coffman, et al. 2011. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 3:ra20. http://dx.doi.org/10.1126/scitranslmed.3001201
19. Geerts, W.H., K.I. Code, R.M. Jay, E. Chen, and J.P. Szalai. 1994. A prospective study of venous thromboembolism after major trauma. N. Engl. J. Med. 331:1601-1606. http://dx.doi.org/10.1056/NEJM199412153312401
20. Griep, M.A., K. Fujikawa, and G.L. Nelsestuen. 1985. Binding and activation properties of human factor XII, prekallikrein, and derived peptides with acidic lipid vesicles. Biochemistry. 24:4124-4130. http://dx.doi.org/10.1021/bi00336a047
21. Heit, J.A. 2008. The epidemiology of venous thromboembolism in the community. Arterioscler. Thromb. Vasc. Biol. 28:370-372. http://dx.doi.org/10.1161/ATVBAHA.108.162545
22. Heit, J.A., C.E. Kobbervig, A.H. James, T.M. Petterson, K.R. Bailey, and L.J. Melton III. 2005. Trends in the incidence of venous thromboembolism during pregnancy or postpartum: a 30-year population-based study. Ann. Intern. Med. 143:697-706.
23. Hughes, R.J., R.J. Hopkins, S. Hill, M. Weatherall, N. Van de Water, M. Nowitz, D. Milne, J. Ayling, M. Wilsher, and R. Beasley. 2003. Frequency of venous thromboembolism in low to moderate risk long distance air travellers: the New Zealand Air Traveller's Thrombosis (NZATT) study. Lancet. 362:2039-2044. http://dx.doi.org/10.1016/S0140-6736(03)15097-0
24. Jung, S., J. Aliberti, P. Graemmel, M.J. Sunshine, G.W. Kreutzberg, A. Sher, and D.R. Littman. 2000. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20:4106-4114. http://dx.doi.org/10.1128/MCB.20.11.4106-4114.2000
25. Kanaji, T., S. Russell, and J. Ware. 2002. Amelioration of the macrothrombocytopenia associated with the murine Bernard-Soulier syndrome. Blood. 100:2102-2107. http://dx.doi.org/10.1182/blood-2002-03-0997
26. Konings, J., J.W. Govers-Riemslag, H. Philippou, N.J. Mutch, J.I. Borissoff, P. Allan, S. Mohan, G. Tans, H. Ten Cate, and R.A. Ariëns. 2011. Factor XIIa regulates the structure of the fibrin clot independently of thrombin generation through direct interaction with fibrin. Blood. 118:3942-3951. http://dx.doi.org/10.1182/blood-2011-03-339572
27. Livak, K.J., and T.D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Δ Δ C(T)) Method. Methods. 25:402-408. http://dx.doi.org/10.1006/meth.2001.1262
28. Losman, M.J., T.M. Fasy, K.E. Novick, and M. Monestier. 1992. 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. 148:1561-1569.
29. Mackman, N. 2008. Triggers, targets and treatments for thrombosis. Nature. 451:914-918. http://dx.doi.org/10.1038/nature06797
30. Mammen, E.F. 1992. Pathogenesis of venous thrombosis. Chest. 102:640S- 644S. http://dx.doi.org/10.1378/chest.102.6.640S
31. Manly, D.A., J. Boles, and N. Mackman. 2011. Role of tissue factor in venous thrombosis. Annu. Rev. Physiol. 73:515-525. http://dx.doi.org/10.1146/annurev-physiol-042210-121137
32. Massberg, S., G. Enders, R. Leiderer, S. Eisenmenger, D. Vestweber, F. Krombach, and K. Messmer. 1998. Platelet-endothelial cell interactions during ischemia/reperfusion: the role of P-selectin. Blood. 92:507-515.
33. Massberg, S., K. Brand, S. Grüner, S. Page, E. Müller, I. Müller, W. Bergmeier, T. Richter, M. Lorenz, I. Konrad, et al. 2002. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J. Exp. Med. 196:887-896. http://dx.doi.org/10.1084/jem.20012044
34. Massberg, S., M. Gawaz, S. Grüner, V. Schulte, I. Konrad, D. Zohlnhöfer, U. Heinzmann, and B. Nieswandt. 2003. A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo. J. Exp. Med. 197:41-49. http://dx.doi.org/10.1084/jem.20020945
35. Massberg, S., L. Grahl, M.L. von Bruehl, D. Manukyan, S. Pfeiler, C. Goosmann, V. Brinkmann, M. Lorenz, K. Bidzhekov, A.B. Khandagale, et al. 2010. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat. Med. 16:887-896. http://dx.doi.org/10.1038/nm.2184
36. Moll, S., and N. Mackman. 2008. Venous thromboembolism: a need for more public awareness and research into mechanisms. Arterioscler. Thromb. Vasc. Biol. 28:367-369. http://dx.doi.org/10.1161/ATVBAHA.108.163097
37. Myers, D. Jr., D. Farris, A. Hawley, S. Wrobleski, A. Chapman, L. Stoolman, R. Knibbs, R. Strieter, and T. Wakefield. 2002. Selectins influence thrombosis in a mouse model of experimental deep venous thrombosis. J. Surg. Res. 108:212-221. http://dx.doi.org/10.1006/jsre.2002.6552
38. Pal, P.K., T. Starr, and M.M. Gertler. 1983. Neutralization of heparin by histone and its subfractions. Thromb. Res. 31:69-79. http://dx.doi.org/10.1016/0049-3848(83)90008-7
39. Parry, G.C., J.H. Erlich, P. Carmeliet, T. Luther, and N. Mackman. 1998. Low levels of tissue factor are compatible with development and hemostasis in mice. J. Clin. Invest. 101:560-569. http://dx.doi.org/10.1172/JCI814
40. Pauer, H.U., T. Renné, B. Hemmerlein, T. Legler, S. Fritzlar, I. Adham, W. Müller-Esterl, G. Emons, U. Sancken, W. Engel, and P. Burfeind. 2004. Targeted deletion of murine coagulation factor XII gene-a model for contact phase activation in vivo. Thromb. Haemost. 92:503-508.
41. Pawlinski, R., M. Tencati, T. Holscher, B. Pedersen, T. Voet, R.E. Tilley, P. Marynen, and N. Mackman. 2007. Role of cardiac myocyte tissue factor in heart hemostasis. J. Thromb. Haemost. 5:1693-1700. http://dx.doi.org/10.1111/j.1538-7836.2007.02649.x
42. Pawlinski, R., J.G. Wang, A.P. Owens III, J. Williams, S. Antoniak, M. Tencati, T. Luther, J.W. Rowley, E.N. Low, A.S. Weyrich, and N. Mackman. 2010. Hematopoietic and nonhematopoietic cell tissue factor activates the coagulation cascade in endotoxemic mice. Blood. 116:806-814. http://dx.doi.org/10.1182/blood-2009-12-259267
43. Payling Weight, H., S.B. Osborn, and D. Edmonds. 1951. Effect of postoperative bed rest and early ambulation on the rate of venous blood-flow. Lancet. 257:22-25. http://dx.doi.org/10.1016/S0140-6736(51)93496-4
44. PEP-Group. 2000. Prevention of pulmonary embolism and deep vein thrombosis with low dose aspirin: Pulmonary Embolism Prevention (PEP) trial. Lancet. 355:1295-1302. http://dx.doi.org/10.1016/S0140-6736(00)02110-3
45. Ramacciotti, E., S. Blackburn, A.E. Hawley, F. Vandy, N. Ballard-Lipka, C. Stabler, N. Baker, K.E. Guire, J.E. Rectenwald, P.K. Henke, et al. 2011. Evaluation of soluble P-selectin as a marker for the diagnosis of deep venous thrombosis. Clin. Appl. Thromb. Hemost. 17:425-431. http://dx.doi.org/10.1177/1076029611405032
46. Reinhardt, C., M.L. von Brühl, D. Manukyan, L. Grahl, M. Lorenz, B. Altmann, S. Dlugai, S. Hess, I. Konrad, L. Orschiedt, et al. 2008. Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J. Clin. Invest. 118:1110-1122.
47. Roger, V.L., A.S. Go, D.M. Lloyd-Jones, R.J. Adams, J.D. Berry, T.M. Brown, M.R. Carnethon, S. Dai, G. de Simone, E.S. Ford, et al; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. 2011. Heart disease and stroke statistics-2011 update: a report from the American Heart Association. Circulation. 123:e18-e209. http://dx.doi.org/10.1161/CIR.0b013e3182009701
48. Roumen-Klappe, E.M., M.C. Janssen, J. Van Rossum, S. Holewijn, M.M. Van Bokhoven, K. Kaasjager, H. Wollersheim, and M. Den Heijer. 2009. Inflammation in deep vein thrombosis and the development of post-thrombotic syndrome: a prospective study. J. Thromb. Haemost. 7:582-587. http://dx.doi.org/10.1111/j.1538-7836.2009.03286.x
49. Sevitt, S. 1970. Organic canalisation and vascularisation of deep vein thrombi studied with dyed-micropaque injected at necropsy. J. Pathol. Pi.
50. Sevitt, S. 1974. The structure and growth of valve-pocket thrombi in femoral veins. J. Clin. Pathol. 27:517-528. http://dx.doi.org/10.1136/jcp.27.7.517
51. Silverstein, M.D., J.A. Heit, D.N. Mohr, T.M. Petterson, W.M. O'Fallon, and L.J. Melton III. 1998. Trends in the incidence of deep vein thrombosis and pulmonary embolism: a 25-year population-based study. Arch. Intern. Med. 158:585-593. http://dx.doi.org/10.1001/archinte.158.6.585
52. Smeeth, L., C. Cook, S. Thomas, A.J. Hall, R. Hubbard, and P. Vallance. 2006. Risk of deep vein thrombosis and pulmonary embolism after acute infection in a community setting. Lancet. 367:1075-1079. http://dx.doi.org/10.1016/S0140-6736(06)68474-2
53. Stewart, G.J., W.G. Ritchie, and P.R. Lynch. 1974. Venous endothelial damage produced by massive sticking and emigration of leukocytes. Am. J. Pathol. 74:507-532.
54. Varma, M.R., A.J. Varga, B.S. Knipp, P. Sukheepod, G.R. Upchurch, S.L. Kunkel, T.W. Wakefield, and P.K. Henke. 2003. Neutropenia impairs venous thrombosis resolution in the rat. J. Vasc. Surg. 38:1090-1098. http://dx.doi.org/10.1016/S0741-5214(03)00431-2
55. Wakefield, T.W., R.M. Strieter, C.A. Wilke, A.M. Kadell, S.K. Wrobleski, M.D. Burdick, R. Schmidt, S.L. Kunkel, and L.J. Greenfield. 1995. Venous thrombosis-associated inflammation and attenuation with neutralizing antibodies to cytokines and adhesion molecules. Arterioscler. Thromb. Vasc. Biol. 15:258-268. http://dx.doi.org/10.1161/01.ATV.15.2.258
56. Wang, X., P.L. Smith, M.Y. Hsu, M.L. Ogletree, and W.A. Schumacher. 2006. Murine model of ferric chloride-induced vena cava thrombosis: evidence for effect of potato carboxypeptidase inhibitor. J. Thromb. Haemost. 4:403-410. http://dx.doi.org/10.1111/j.1538-7836.2006.01703.x
57. Ward, C.M., T.J. Tetaz, R.K. Andrews, and M.C. Berndt. 1997. Binding of the von Willebrand factor A1 domain to histone. Thromb. Res. 86:469-477. http://dx.doi.org/10.1016/S0049-3848(97)00096-0
58. Warlow, C., D. Ogston, and A.S. Douglas. 1976. Deep venous thrombosis of the legs after strokes: Part 2-Natural history. BMJ. 1:1181-1183. http://dx.doi.org/10.1136/bmj.1.6019.1181
59. Wright, H.P., S.B. Osborn, and M. Hayden. 1952. Venous velocity in bedridden medical patients. Lancet. 2:699-700. http://dx.doi.org/10.1016/S0140-6736(52)91318-4
60. Zhou, J., L. May, P. Liao, P.L. Gross, and J.I. Weitz. 2009. Inferior vena cava ligation rapidly induces tissue factor expression and venous thrombosis in rats. Arterioscler. Thromb. Vasc. Biol. 29:863-869. http://dx.doi.org/10.1161/ATVBAHA.109.185678