Crossroads of coagulation and innate immunity: The case of deep vein thrombosis

Journal of Thrombosis and Haemostasis

Volumn 11, Issue SUPPL.1, 2013, Pages 233-241

  Schulz, C ^a   Engelmann, B ^b   Massberg, S ^b,c  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

Blood coagulation; Immunity; Innate; Monocytes; Neutrophils; Platelet activation; Venous thrombosis

Indexed keywords

BLOOD CLOTTING FACTOR 12; CHEMOKINE; CYTOKINE; LEUKOCYTE ELASTASE; PADGEM PROTEIN; PROTEIN DISULFIDE ISOMERASE; THROMBOPLASTIN; VON WILLEBRAND FACTOR;

ARTERY THROMBOSIS; BLOOD CLOTTING; BLOOD FLOW; BLOOD VESSEL OCCLUSION; DEEP VEIN THROMBOSIS; ENDOTHELIUM; FIBRIN FORMATION; HEMOSTASIS; HUMAN; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; MONOCYTE; NEUTROPHIL; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; REVIEW; THROMBOCYTE; VEIN THROMBOSIS;

BLOOD COAGULATION; IMMUNITY; INNATE; MONOCYTES; NEUTROPHILS; PLATELET ACTIVATION; VENOUS THROMBOSIS;

ANIMALS; BLOOD PLATELETS; HUMANS; IMMUNITY, INNATE; VENOUS THROMBOSIS;

EID: 84880616430     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12261     Document Type: Review

References (86)

1. Fowkes FJ, Price JF, Fowkes FG. Incidence of diagnosed deep vein thrombosis in the general population: systematic review. Eur J Vasc Endovasc Surg 2003; 25: 1-5.
2. Naess IA, Christiansen SC, Romundstad P, Cannegieter SC, Rosendaal FR, Hammerstrom J. Incidence and mortality of venous thrombosis: a population-based study. J Thromb Haemost 2007; 5: 692-9.
3. Dickson B. Venous thrombosis: on the history of Virchow's triad. Univ Toronto Med J. 2004; 81: 166-171.
4. Wakefield TW, Strieter RM, Wilke CA, Kadell AM, Wrobleski SK, Burdick MD, Schmidt R, Kunkel SL, Greenfield LJ. Venous thrombosis-associated inflammation and attenuation with neutralizing antibodies to cytokines and adhesion molecules. Arterioscler Thromb Vasc Biol 1995; 15: 258-68.
5. Stewart GJ. Neutrophils and deep venous thrombosis. Haemostasis 1993; 23(Suppl. 1): 127-40.
6. Downing LJ, Strieter RM, Kadell AM, Wilke CA, Austin JC, Hare BD, Burdick MD, Greenfield LJ, Wakefield TW. IL-10 regulates thrombus-induced vein wall inflammation and thrombosis. J Immunol 1998; 161: 1471-6.
7. Smeeth L, Cook C, Thomas S, Hall AJ, Hubbard R, Vallance P. Risk of deep vein thrombosis and pulmonary embolism after acute infection in a community setting. Lancet 2006; 367: 1075-9.
8. Esmon CT, Xu J, Lupu F. Innate immunity and coagulation. J Thromb Haemost 2011; 9(Suppl. 1): 182-8.
9. Mackman N. Mouse models, risk factors, and treatments of venous thrombosis. Arterioscler Thromb Vasc Biol 2012; 32: 554-5.
10. von Bruhl ML, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, Khandoga A, Tirniceriu A, Coletti R, Kollnberger M, Byrne RA, Laitinen I, Walch A, Brill A, Pfeiler S, Manukyan D, Braun S, Lange P, Riegger J, Ware J et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012; 209: 819-35.
11. Diaz JA, Obi AT, Myers DD Jr, Wrobleski SK, Henke PK, Mackman N, Wakefield TW. Critical review of mouse models of venous thrombosis. Arterioscler Thromb Vasc Biol 2012; 32: 556-62.
12. Cooley BC. Murine models of thrombosis. Thromb Res 2012; 129(Suppl. 2): S62-4.
13. Brill A, Fuchs TA, Chauhan AK, Yang JJ, De Meyer SF, Kollnberger M, Wakefield TW, Lammle B, Massberg S, Wagner DD. von Willebrand factor-mediated platelet adhesion is critical for deep vein thrombosis in mouse models. Blood 2011; 117: 1400-7.
14. Myers D Jr, Farris D, Hawley A, Wrobleski S, Chapman A, Stoolman L, Knibbs R, Strieter R, Wakefield T. Selectins influence thrombosis in a mouse model of experimental deep venous thrombosis. J Surg Res 2002; 108: 212-21.
15. Myers DD Jr, Rectenwald JE, Bedard PW, Kaila N, Shaw GD, Schaub RG, Farris DM, Hawley AE, Wrobleski SK, Henke PK, Wakefield TW. Decreased venous thrombosis with an oral inhibitor of P selectin. J Vasc Surg 2005; 42: 329-36.
16. Eppihimer MJ, Schaub RG. P-Selectin-dependent inhibition of thrombosis during venous stasis. Arterioscler Thromb Vasc Biol 2000; 20: 2483-8.
17. Burns AR, Bowden RA, Abe Y, Walker DC, Simon SI, Entman ML, Smith CW. P-selectin mediates neutrophil adhesion to endothelial cell borders. J Leukoc Biol 1999; 65: 299-306.
18. McEver RP, Beckstead JH, Moore KL, Marshall-Carlson L, Bainton DF. GMP-140, a platelet alpha-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel-Palade bodies. J Clin Invest 1989; 84: 92-9.
19. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7: 678-89.
20. Hamer JD, Malone PC, Silver IA. The PO2 in venous valve pockets: its possible bearing on thrombogenesis. Br J Surg 1981; 68: 166-70.
21. Pinsky DJ, Naka Y, Liao H, Oz MC, Wagner DD, Mayadas TN, Johnson RC, Hynes RO, Heath M, Lawson CA, Stern DM. Hypoxia-induced exocytosis of endothelial cell Weibel-Palade bodies. A mechanism for rapid neutrophil recruitment after cardiac preservation. J Clin Invest 1996; 97: 493-500.
22. Denis CV, Andre P, Saffaripour S, Wagner DD. Defect in regulated secretion of P-selectin affects leukocyte recruitment in von Willebrand factor-deficient mice. Proc Natl Acad Sci USA 2001; 98: 4072-7.
23. Giesen PL, Rauch U, Bohrmann B, Kling D, Roque M, Fallon JT, Badimon JJ, Himber J, Riederer MA, Nemerson Y. Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci USA 1999; 96: 2311-15.
24. Muller I, Klocke A, Alex M, Kotzsch M, Luther T, Morgenstern E, Zieseniss S, Zahler S, Preissner K, Engelmann B. Intravascular tissue factor initiates coagulation via circulating microvesicles and platelets. FASEB J 2003; 17: 476-8.
25. Chou J, Mackman N, Merrill-Skoloff G, Pedersen B, Furie BC, Furie B. Hematopoietic cell-derived microparticle tissue factor contributes to fibrin formation during thrombus propagation. Blood 2004; 104: 3190-7.
26. Mackman N. New insights into the mechanisms of venous thrombosis. J Clin Invest 2012; 122: 2331-6.
27. Osterud B. Tissue factor expression in blood cells. Thromb Res 2010; 125(Suppl. 1): S31-4.
28. Pawlinski R, Wang JG, Owens AP 3rd, Williams J, Antoniak S, Tencati M, Luther T, Rowley JW, Low EN, Weyrich AS, Mackman N. Hematopoietic and nonhematopoietic cell tissue factor activates the coagulation cascade in endotoxemic mice. Blood 2010; 116: 806-14.
29. Papayannopoulos V, Zychlinsky A. NETs: a new strategy for using old weapons. Trends Immunol 2009; 30: 513-21.
30. Fuchs TA, Bhandari AA, Wagner DD. Histones induce rapid and profound thrombocytopenia in mice. Blood 2011; 118: 3708-14.
31. Kambas K, Mitroulis I, Apostolidou E, Girod A, Chrysanthopoulou A, Pneumatikos I, Skendros P, Kourtzelis I, Koffa M, Kotsianidis I, Ritis K. Autophagy mediates the delivery of thrombogenic tissue factor to neutrophil extracellular traps in human sepsis. PLoS ONE 2012; 7: e45427.
32. Massberg S, Grahl L, von Bruehl ML, Manukyan D, Pfeiler S, Goosmann C, Brinkmann V, Lorenz M, Bidzhekov K, Khandagale AB, Konrad I, Kennerknecht E, Reges K, Holdenrieder S, Braun S, Reinhardt C, Spannagl M, Preissner KT, Engelmann B. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010; 16: 887-96.
33. Glaser CB, Morser J, Clarke JH, Blasko E, McLean K, Kuhn I, Chang RJ, Lin JH, Vilander L, Andrews WH. Oxidation of a specific methionine in thrombomodulin by activated neutrophil products blocks cofactor activity. A potential rapid mechanism for modulation of coagulation. J Clin Invest 1992; 90: 2565-73.
34. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, Wrobleski SK, Wakefield TW, Hartwig JH, Wagner DD. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA 2010; 107: 15880-5.
35. 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: 6388-93.
36. Iwanaga S. The molecular basis of innate immunity in the horseshoe crab. Curr Opin Immunol 2002; 14: 87-95.
37. Hoffmann JA. The immune response of Drosophila. Nature 2003; 426: 33-8.
38. Muta T, Iwanaga S. The role of hemolymph coagulation in innate immunity. Curr Opin Immunol 1996; 8: 41-7.
39. Tzou P, De Gregorio E, Lemaitre B. How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Curr Opin Microbiol 2002; 5: 102-10.
40. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, Patel KD, Chakrabarti S, McAvoy E, Sinclair GD, Keys EM, Allen-Vercoe E, Devinney R, Doig CJ, Green FH, Kubes P. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 13: 463-9.
41. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532-5.
42. Wen F, White GJ, van Etten HD, Xiong Z, Hawes MC. Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 2009; 151: 820-9.
43. Altincicek B, Stotzel S, Wygrecka M, Preissner KT, Vilcinskas A. Host-derived extracellular nucleic acids enhance innate immune responses, induce coagulation, and prolong survival upon infection in insects. J Immunol 2008; 181: 2705-12.
44. Guimaraes-Costa AB, Nascimento MT, Froment GS, Soares RP, Morgado FN, Conceicao-Silva F, Saraiva EM. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci USA 2009; 106: 6748-53.
45. McCormick A, Heesemann L, Wagener J, Marcos V, Hartl D, Loeffler J, Heesemann J, Ebel F. NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microbes Infect 2010; 12: 928-36.
46. Amulic B, Cazalet C, Hayes GL, Metzler KD, Zychlinsky A. Neutrophil function: from mechanisms to disease. Annu Rev Immunol 2012; 30: 459-89.
47. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD, Pittman K, Asaduzzaman M, Wu K, Meijndert HC, Malawista SE, de Boisfleury Chevance A, Zhang K, Conly J, Kubes P. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 2012; 18: 1386-93.
48. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A. Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 2007; 176: 231-41.
49. Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, Zychlinsky A, Reichenbach J. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 2009; 114: 2619-22.
50. Brill A, Fuchs TA, Savchenko AS, Thomas GM, Martinod K, De Meyer SF, Bhandari AA, Wagner DD. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost 2012; 10: 136-44.
51. Fischer S, Preissner KT. Extracellular nucleic acids as novel alarm signals in the vascular system. Mediators of defence and disease. Hamostaseologie 2013; 33: 37-42.
52. Chow OA, von Kockritz-Blickwede M, Bright AT, Hensler ME, Zinkernagel AS, Cogen AL, Gallo RL, Monestier M, Wang Y, Glass CK, Nizet V. Statins enhance formation of phagocyte extracellular traps. Cell Host Microbe 2010; 8: 445-54.
53. Yousefi S, Gold JA, Andina N, Lee JJ, Kelly AM, Kozlowski E, Schmid I, Straumann A, Reichenbach J, Gleich GJ, Simon HU. Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 2008; 14: 949-53.
54. Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F, Taylor FB, Esmon NL, Lupu F, Esmon CT. Extracellular histones are major mediators of death in sepsis. Nat Med 2009; 15: 1318-21.
55. Semeraro F, Ammollo CT, Morrissey JH, Dale GL, Friese P, Esmon NL, Esmon CT. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood 2011; 118: 1952-61.
56. Renne T, Schmaier AH, Nickel KF, Blomback M, Maas C. In vivo roles of factor XII. Blood 2012; 120: 4296-303.
57. Engelmann B. Massberg S. Nat Rev Immunol: Thrombosis as an intravascular effector of innate immunity, 2012.
58. Luo D, Szaba FM, Kummer LW, Plow EF, Mackman N, Gailani D, Smiley ST. Protective roles for fibrin, tissue factor, plasminogen activator inhibitor-1, and thrombin activatable fibrinolysis inhibitor, but not factor XI, during defense against the gram-negative bacterium Yersinia enterocolitica. J Immunol 2011; 187: 1866-76.
59. Flick MJ, Du X, Witte DP, Jirouskova M, Soloviev DA, Busuttil SJ, Plow EF, Degen JL. Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest 2004; 113: 1596-606.
60. Mullarky IK, Szaba FM, Berggren KN, Parent MA, Kummer LW, Chen W, Johnson LL, Smiley ST. Infection-stimulated fibrin deposition controls hemorrhage and limits hepatic bacterial growth during listeriosis. Infect Immun 2005; 73: 3888-95.
61. Newton K, Dixit VM. Signaling in innate immunity and inflammation. Cold Spring Harb Perspect: Biol, 2012:4.
62. Guha M, Mackman N. LPS induction of gene expression in human monocytes. Cell Signal 2001; 13: 85-94.
63. Reinhardt C, von Bruhl ML, Manukyan D, Grahl L, Lorenz M, Altmann B, Dlugai S, Hess S, Konrad I, Orschiedt L, Mackman N, Ruddock L, Massberg S, Engelmann B. Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J Clin Invest 2008; 118: 1110-22.
64. Sun H, Ringdahl U, Homeister JW, Fay WP, Engleberg NC, Yang AY, Rozek LS, Wang X, Sjobring U, Ginsburg D. Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 2004; 305: 1283-6.
65. Sodeinde OA, Subrahmanyam YV, Stark K, Quan T, Bao Y, Goguen JD. A surface protease and the invasive character of plague. Science 1992; 258: 1004-7.
66. Berends ET, Horswill AR, Haste NM, Monestier M, Nizet V, von Kockritz-Blickwede M. Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J Innate Immun 2010; 2: 576-86.
67. Schulz C, Massberg S. Platelets in atherosclerosis and thrombosis. Handb Exp Pharmacol. 2012; 210: 111-33.
68. Semple JW, Italiano JE Jr, Freedman J. Platelets and the immune continuum. Nat Rev Immunol 2011; 11: 264-74.
69. Fitzgerald JR, Foster TJ, Cox D. The interaction of bacterial pathogens with platelets. Nat Rev Microbiol 2006; 4: 445-57.
70. Youssefian T, Drouin A, Masse JM, Guichard J, Cramer EM. Host defense role of platelets: engulfment of HIV and Staphylococcus aureus occurs in a specific subcellular compartment and is enhanced by platelet activation. Blood 2002; 99: 4021-9.
71. Verschoor A, Neuenhahn M, Navarini AA, Graef P, Plaumann A, Seidlmeier A, Nieswandt B, Massberg S, Zinkernagel RM, Hengartner H, Busch DH. A platelet-mediated system for shuttling blood-borne bacteria to CD8alpha+ dendritic cells depends on glycoprotein GPIb and complement C3. Nat Immunol 2011; 12: 1194-201.
72. Urban CF, Reichard U, Brinkmann V, Zychlinsky A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol 2006; 8: 668-76.
73. Muller F, Mutch NJ, Schenk WA, Smith SA, Esterl L, Spronk HM, Schmidbauer S, Gahl WA, Morrissey JH, Renne T. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 2009; 139: 1143-56.
74. Smith SA, Mutch NJ, Baskar D, Rohloff P, Docampo R, Morrissey JH. Polyphosphate modulates blood coagulation and fibrinolysis. Proc Natl Acad Sci USA 2006; 103: 903-8.
75. Lorenz B, Leuck J, Kohl D, Muller WE, Schroder HC. Anti-HIV-1 activity of inorganic polyphosphates. J Acquir Immune Defic Syndr Hum Retrovirol 1997; 14: 110-18.
76. Muller F, Renne T. Platelet polyphosphates: the nexus of primary and secondary hemostasis. Scand J Clin Lab Invest 2011; 71: 82-6.
77. Schulz C, Leuschen NV, Frohlich T, Lorenz M, Pfeiler S, Gleissner CA, Kremmer E, Kessler M, Khandoga AG, Engelmann B, Ley K, Massberg S, Arnold GJ. Identification of novel downstream targets of platelet glycoprotein VI activation by differential proteome analysis: implications for thrombus formation. Blood 2010; 115: 4102-10.
78. Novotny WF, Girard TJ, Miletich JP, Broze GJ Jr. Platelets secrete a coagulation inhibitor functionally and antigenically similar to the lipoprotein associated coagulation inhibitor. Blood 1988; 72: 2020-5.
79. Haselmayer P, Daniel M, Tertilt C, Salih HR, Stassen M, Schild H, Radsak MP. Signaling pathways of the TREM-1- and TLR4-mediated neutrophil oxidative burst. J Innate Immun 2009; 1: 582-91.
80. Nishimura S, Manabe I, Nagasaki M, Kakuta S, Iwakura Y, Takayama N, Ooehara J, Otsu M, Kamiya A, Petrich BG, Urano T, Kadono T, Sato S, Aiba A, Yamashita H, Sugiura S, Kadowaki T, Nakauchi H, Eto K, Nagai R. In vivo imaging visualizes discoid platelet aggregations without endothelium disruption and implicates contribution of inflammatory cytokine and integrin signaling. Blood 2012; 119: e45-56.
81. Saha P, Humphries J, Modarai B, Mattock K, Waltham M, Evans CE, Ahmad A, Patel AS, Premaratne S, Lyons OT, Smith A. Leukocytes and the natural history of deep vein thrombosis: current concepts and future directions. Arterioscler Thromb Vasc Biol 2011; 31: 506-12.
82. Horwitz M, Benson KF, Duan Z, Li FQ, Person RE. Hereditary neutropenia: dogs explain human neutrophil elastase mutations. Trends Mol Med 2004; 10: 163-70.
83. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, Richards DR, McDonald-Smith GP, Gao H, Hennessy L, Finnerty CC, Lopez CM, Honari S, Moore EE, Minei JP, Cuschieri J, Bankey PE, Johnson JL, Sperry J, Nathens AB, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci USA 2013; 110: 3507-12.
84. Hawkey CM. Analysis of hematologic findings in healthy and sick adult chimpanzees (Pan troglodytes). J Med Primatol 1985; 14: 327-43.
85. Knight LC, Romano JE, Bright LT, Agelan A, Kantor S, Maurer AH. Platelet binding and biodistribution of [99mTc]rBitistatin in animal species and humans. Nucl Med Biol 2007; 34: 855-63.
86. van Montfoort ML, Stephan F, Lauw MN, Hutten BA, van Mierlo GJ, Solati S, Middeldorp S, Meijers JC, Zeerleder S. Circulating nucleosomes and neutrophil activation as risk factors for deep vein thrombosis. Arterioscler Thromb Vasc Biol 2013; 33: 147-51.