Fibrinolytic and coagulative activities of Yersinia pestis

Frontiers in Cellular and Infection Microbiology

Volumn 4, Issue JUL, 2013, Pages

  Korhonen, Timo K ^a   Haiko, Johanna ^a   Laakkonen, Liisa ^a   Järvinen, Hanna M ^a,b   Westerlund Wikström, Benita ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Coagulation; Fibrinolysis; Hemostasis; Plague; Plasminogen; Proteolysis; Yersinia pestis

Indexed keywords

BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 7A; ELASTASE; FIBRIN; LIPOPOLYSACCHARIDE; MATRIX METALLOPROTEINASE; PLASMIN; PLASMINOGEN; PLASMINOGEN ACTIVATOR INHIBITOR 1; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; THROMBIN; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; TISSUE FACTOR PATHWAY INHIBITOR; TOLL LIKE RECEPTOR 4; UROKINASE; BACTERIAL PROTEIN; ENDOTOXIN; PLA PROTEASE, YERSINIA PESTIS; PLASMINOGEN ACTIVATOR; VIRULENCE FACTOR;

BIOLOGICAL ACTIVITY; BLOOD CLOTTING; ENZYME ACTIVITY; FIBRINOLYSIS; FUNGAL STRUCTURES; HUMAN; INFLAMMATION; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN MODIFICATION; REVIEW; SIGNAL TRANSDUCTION; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS; ANIMAL; COAGULATION; ENZYMOLOGY; HEMOSTASIS; METABOLISM; MOUSE; PATHOGENICITY; PLAGUE;

COAGULATION; FIBRINOLYSIS; HEMOSTASIS; PLAGUE; PLASMINOGEN; PROTEOLYSIS; YERSINIA PESTIS;

ANIMALS; BACTERIAL PROTEINS; BLOOD COAGULATION; ENDOTOXINS; FIBRINOLYSIS; HUMANS; LIPOPOLYSACCHARIDES; MICE; PLASMINOGEN ACTIVATORS; VIRULENCE FACTORS; YERSINIA PESTIS;

EID: 84891425884     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00035     Document Type: Review

References (77)

1. Agarkov, A., Chauhan, S., Lory, P. J., Gilbertson, S. R., and Motin, V. L. (2008). Substrate specificity and screening of the integral membrane protease Pla. Bioorg. Med. Chem. Lett. 18, 427-431. doi:10.1016/j.bmcl.2007.09.104
2. Akopyan, K., Edgren, T., Wang-Edgren, H., Rosqvist, R., Fahlgren, A., Wolf-Watz, H., et al. (2011). Translocation of surface-localized effectors in type III secretion. Proc. Natl. Acad. Sci. U.S.A. 4, 1639-1644. doi:10.1073/pnas.1013888108
3. Beaufort, N., Seweryn, P., de Bentzmann, S., Tang, A., Kellermann, J., Grebenchtchikov, N., et al. (2010). Activation of human pro-urokinase by unrelated proteases secreted by Pseudomonas aeruginosa. Biochem. J. 428, 473-482. doi:10.1042/BJ20091806
4. Beaufort, N., Wojciechowski, P., Sommerhof, C. P., Szmyd, G., Dunin, G., Eick, S., et al. (2008). The human fibrinolytic system is a target for the staphylococcal metalloprotease aureolysin. Biochem. J. 410, 157-165. doi:10.1042/BJ20070650
5. Brandenburg, K., Garidel, P., Schromm, A. B., Andra, J., Kramer, A., Egmond, M., et al. (2005). Investigation into the interaction of the bacterial protease OmpT with outer membrane lipids and biological activity of OmpT:lipopolysaccharide complexes. Eur. Biophys. J. 34, 28-41. doi:10.1007/s00249-004-0422-3
6. Broze, G. J. Jr. (2003) "The tissue factor pathway of coagulation," in Thrombosis and Hemorrhage eds J. Loscalzo and A. I. Schafer (Philadelphia, PA: Lippincott Williams and Wilkins), 62-80.
7. Busch, J. D., Van Andel, R., Cordova, J., Colman, R. E., Keim, P., Rocke, T. E., et al. (2011). Population dofference in host immune factors may influence survival of Gunnison's prairie dogs (Cynomys gunnisoni) during plague outbreaks. J. Wildl. Dis. 47, 968-973.
8. Caruso, R. (1986). Fibrinogen/fibrin deposits in mesenteric lymphadenitis due to Yersinia pseudotuberculosis type I: morphologic, immunohistochemical and electron microscopic studies of one case. Basic Appl. Histochem. 30, 333-341.
9. Caulfield, A. J., and Lathem, W. W. (2012). Substrates of the plasminogen activator protease of Yersinia pestis. Adv. Exp. Med. Biol. 954, 253-260. doi:10.1007/978-1-4614-3561-7_32
10. Chromy, B. A., Choi, M. W., Murphy, G. A., Gonzales, A. D., Corzett, C. H., Chang, B. C., et al. (2005). Proteomic characterization of Yersinia pestis virulence. J. Bacteriol. 187, 8172-8180. doi:10.1128/JB.187.23.8172-8180.2005
11. Chung, M. C., Jörgensen, S. C., Tonry, J. H., Kaschanci, E., Bailey, C., and Popov, S. (2011). Secreted Bacillus anthracis taget the host fibrinolytic system. FEMS Immunol. Med. Microbiol. 62, 173-181. doi:10.1111/j.1574-695X.2011.00798.x
12. Comer, J. E., Sturdevant, D. E., Carmody, A. B., Virtaneva, K., Gardner, D., Long, D., et al. (2010). Transcriptomic and innate immune responses to Yersinia pestis in the lymph node during bubonic plague. Infect. Immun. 78, 5086-5098. doi:10.1128/IAI.00256-10
13. Crippa, M. P. (2007). Urokinase-type plasminogen activator. Int. J. Biochem. Cell Biol. 39, 690-694. doi:10.1016/j.biocel.2006.10.008
14. Degen, J. L., Bugge, T. H., and Goguen, J. D. (2007). Fibrin and fibrinolysis in infection and host defence. J. Thromb. Haemost. 5(Suppl. 1), 24-31. doi:10.1111/j.1538-7836.2007.02519.x
15. Dekker, N., Cox, R. C., Kramer, R. A., and Egmond, M. R. (2001). Substrate specificity of the integral membrane protease OmpT determined by spatially addressed peptide libraries. Biochemistry 40, 1694-1701. doi: 10.1021/bi0014195
16. Eppinger, M., Worsham, P. L., Nikolich, M. P., Riley, D. R., Sebastian, Y., Mou, S., et al. (2010). Genome sequence of the deep-rooted Yersinia pestis strain Angola reveals new insight into the evolution and pangenome of the plague bacterium. J. Bacteriol. 192, 1685-1699. doi:10.1128/JB.01518-09
17. Eren, E., Murphy, M., Goguen, J., and van den Berg, B. (2010). An active site network in the plasminogen activator Pla from Yersinia pestis. Structure 18, 809-818. doi: 10.1016/j.str.2010.03.013
18. Eren, E., and van den Berg, B. (2012). Structural basis for activation of an integral membrane protease by lipopolysaccharide. J. Biol. Chem. 287, 23971-23976. doi: 10.1074/jbc.M112.376418
19. Ferguson, A. D., Welte, W., Hofmann, E., Lindner, B., Holst, O., Coulton, J. W., et al. (2000). A conserved structural motif for lipopolysaccharide recognition by prokaryotic and eukaryotic proteins. Structure 8, 585-592. doi: 10.1016/S0969-2126(00)00143-X
20. Fisher, M. L., Castillo, C., and Mecsas, J. (2007). Intranasal inoculation of mice with Yersinia pseudotuberculosis causes a lethal lung infection that is dependent on Yersinia outer proteins and PhoP. Infect. Immun. 75, 429-442. doi: 10.1128/IAI.01287-06
21. Flick, M. J., Du, X., Witte, D. P., Jirousková, M., Soloviev, D. A., Busuttil, S. J., et al. (2004). Leukocyte engagement of fibrin(ogen) via the integrin aMß2/MAC-1 receptor is critical for host inflammatory response in vivo. J. Clin. Invest. 113, 1596-1606.
22. Galvan, E. M., Lasaro, M. A., and Schifferli, D. M. (2008). Capsular antigen fraction 1 and Pla modulae the susceptibility of Yersinia pestis to pulmonary antimicrobial peptides such as cathelicidin. Infect. Immun. 76, 1456-1464. doi: 10.1128/IAI.01197-07
23. Goolaerts, A., Lafargue, M., Song, Y., Miyazawa, B., Arjomandi, M., Carlés, M., et al. (2011). PAI-1 is an essential component of the pulmonary response during Pseudomonas aeruginosa pneumoniae in mice. Thorax 66, 788-796. doi: 10.1136/thx.2010.155788
24. Greenberg, C. S., and Lai, T.S. (2003). "Fibrin formation and stabilization," in Thrombosis and Hemorrhage, eds J. Loscalzo and A. I. Schafer (Philadelphia, PA: Lippincott Williams and Wilkins), 81-104.
25. Guinet, F., Avé, P., Jones, L., Huerre, M., and Carniel, E. (2008). Defective innate cell response and lymph node infiltration specify Yesinia pestis infection. PLoS ONE 3:e1688. doi: 10.1371/journal.pone.0001688
26. Haiko, J., Kukkonen, M., Ravantti, J. J., Westerlund-Wikström, B., and Korhonen, T. K. (2009a). The single substitution I259T, conserved in the plasminogen activator Pla of pandemic Yersinia pestis branches, enhances fibrinolytic activity. J. Bacteriol. 191, 4758-4766. doi: 10.1128/JB.00489-09
27. Haiko, J., Suomalainen, M., Ojala, T., Lähteenmäki, K., and Korhonen, T. K. (2009b). Breaking barriers-attack on innate immune defences by omptin surface proteases of enterobacterial pathogens. Innate Immun. 15, 67-80. doi: 10.1177/1753425909102559
28. Haiko, J., Laakkonen, L., Juuti, K., Kalkkinen, N., and Korhonen, T. K. (2010). The omptins of Yersinia pestis and Salmonella enterica cleave the reactive center loop of plasminogen activator inhibitor 1. J. Bacteriol. 192, 4553-4561. doi: 10.1128/JB.00458-10
29. Haiko, J., Laakkonen, L., Westerlund-Wikström, B., and Korhonen, T. K. (2011). Molecular adaptation of a plant-bacterium outer membrane protease towards plague virulence factor Pla. BMC Evol. Biol. 11:43. doi: 10.1186/1471-2148-11-43
30. Hua, F., Ren, W., and Zhu, L. (2011). Plasminogen activator inhibitor type-1 deficiency exaggerates LPS-induced acute lung injury through enhancing Toll-like receptor 4 signalling pathway. Blood Coagul. Fibrinolysis 22, 480-486. doi: 10.1097/MBC.0b013e328346ef56
31. Hwang, B.Y., Varadarajan, N., Li, H., Rodriguez, S., Iverson, B. L., and Georgiou, G. (2007). Substrate specificity of the Escherichia coli outer membrane protease OmpP. J. Bacteriol. 189, 522-530. doi: 10.1128/JB.01493-06
32. Järvinen, H. M., Laakkonen, L., Haiko, J., Johansson, T., Juuti, K., Suomalainen, M., et al. (2013). Human single-chain urokinase is activated by the omptins PgtE of Salmonella enterica and Pla of Yersinia pestis despite mutations of active site residues. Mol. Microbiol. doi: 10.1111/mmi.12293. [Epub ahead of print].
33. Kager, L. M., Wiersinga, W. J., Roelofs, T. H., Meijers, J. C. M., Levi, M., Van't Veer, C., et al. (2011). Plasminogen activator inhibitor type 1 contributes to protective immunity during experimental Gram-negative sepsis (melioidosis). J. Thromb. Haemost. 9, 2020-2028. doi: 10.1111/j.1538-7836.2011.04473.x
34. Kawahara, K., Tsukano, H., Watanabe, H., Lindner, B., and Matsuura, M. (2002). Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect. Immun. 70, 4092-4098. doi: 10.1128/IAI.70.8.4092-4098.2002
35. Kawamura, T., Okada, N., and Okada, H. (2002). Elastase from activated human neutrophils activates procarboxypeptidase R. Microbiol. Immunol. 46, 225-230.
36. Knirel, Y. A., Lindner, B., Vinogradov, E. V., Kocharova, N. A., Senchenkova, S. N., Shaikhutdinova, R. Z., et al. (2005). Temperature-dependent variations and intraspecies diversity of the structure of the lipopolysaccharide of Yersinia pestis. Biochemistry 44, 1731-1743. doi: 10.1021/bi048430f
37. Kramer, R. A., Brandenburg, K., Vandeputee-Rutten, L., Werkhoven, M., Gros, P., Dekker, N., et al. (2002). Lipopolysaccharide regions involved in the activation of Escherichia coli outer membrane protease OmpT. Eur. J. Biochem. 269, 1746-1752. doi: 10.1046/j.1432-1327.2002.02820.x
38. Kramer, R. A., Vandeputte-Rutten, L., de Roon, G. J., Gros, P., Dekker, N., and Egmond, M. R. (2001). Identification of essential acidic residues of outer membrane protease OmpT supports a novel active site. FEBS Lett. 505, 426-430. doi: 10.1016/S0014-5793(01)02863-0
39. Kramer, R. A., Zandwijken, D., Egmond, M. R., and Dekker, N. (2000). In vitro folding, purification and characterization of Escherichia coli outer membrane protease OmpT. Eur. J. Biochem. 267, 885-893. doi: 10.1046/j.1432-1327.2000.01073.x
40. Kukkonen, M., Lähteenmäki, K., Suomalainen, M., Kalkkinen, N., Emödy, L., Lång, H., et al. (2001). Protein regions important for plasminogen activation and inactivation of a2-antiplasmin in the surface protease Pla of Yersinia pestis. Mol. Microbiol. 40, 1097-1111. doi: 10.1046/j.1365-2958.2001.02451.x
41. Kukkonen, M., Suomalainen, M., Kyllönen, P., Lähteenmäki, K., Lång, H., Virkola, R., et al. (2004). Lack of O-antigen is essential for plasminogen activation by Yersinia pestis and Salmonella enterica. Mol. Microbiol. 51, 215-225. doi: 10.1046/j.1365-2958.2003.03817.x
42. Lähteenmäki, K., Edelman, S., and Korhonen, T. K. (2005a). Bacterial metastasis: the host plasminogen system in bacterial infections. Trends Microbiol. 13, 79-85. doi: 10.1016/j.tim.2004.12.003
43. Lähteenmäki, K., Kyllönen, P., Partanen, L., and Korhonen, T. K. (2005b). Antiprotease inactivation by Salmonella enterica released from infected macrophages. Cell. Microbiol. 7, 529-538. doi: 10.1111/j.1462-5822.2004.00483.x
44. Lathem, W. W., Price, P. A., Miller, V. L., and Goldman, W. E. (2007). A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 315, 509-513. doi: 10.1126/science.1137195
45. Lawrence, M. B., Pennington, J., and Miller, V. L. (2013). Acquisition of omptin reveals cryptic virulence function of autotransporter YapE in Yersinia pestis. Mol. Microbiol. 89, 276-287. doi: 10.1111/mmi.12273
46. Lijnen, H. R. (2005). Pleitropic functions of plasminogen activator inhibitor-1. J. Thromb. Haemost. 3, 35-45. doi: 10.1111/j.1538-7836.2004.00827.x
47. Lim, J. H., Woo, C. H., and Li, J.D. (2011). Critical role of type 1 plasminogen activator inhibitor (PAI-1) in ealy host defence against nontypeable Haemophilus influenzae (NTHi) infection. Biochem. Biophys. Res. Commun. 414, 67-72. doi: 10.1016/j.bbrc.2011.09.023
48. Liu, H., Wang, H., Qiu, J., Wang, X., Guo, Z., Zhou, D., et al. (2009). Transcriptional profiling of a mice plague model: insight into interaction between Yersinia pestis and its host. J. Basic Microbiol. 49, 92-99. doi: 10.1002/jobm.200800027
49. Luo, D., Lin, J. S., Parent, M. A., Mullarky-Kanevsky, I., Szaba, F. M., Kummer, L. W., et al. (2013). Fibrin facilitates both innate and T cell-mediated defense against Yersinia pestis. J. Immunol. 190, 4149-4161. doi: 10.4049/jimmunol.1203253
50. Luo, D., Szaba, F. M., Kummer, L. W., Plow, E. F., Mackman, N., Gailani, D., et al. (2011). Protective roles for fibrin, tissue factor, plasminogen activator inhibitor-1, and thrombin activable fibrinolysis inhibitor, but not factor XI, during defence against the Gram-negative bacterium Yersinia enterocolitica. J. Immunol. 187, 1866-1876. doi: 10.4049/jimmunol.1101094
51. Marx, P. F., Dawson, P. E., Bouma, B. N., and Meijers, J. C. (2002). Plasmin-mediated activation and inactivation of thrombin-activable fibrinolysis inhibitor. Biochemistry 41, 6688-6696. doi: 10.1021/bi015982e
52. McCarter, J. D., Stephens, D., Shoemaker, K., Rosenberg, S., Kirsch, J. F., and Georgiou, G. (2004). Substrate specificity of the Escherichia coli outer membrane protease OmpT. J. Bacteriol. 186, 5919-5925. doi: 10.1128/JB.186.17.5919-5925.2004
53. Montminy, S. W., Khan, N., McGrath, S., Walkowicz, M. J., Sharp, F., Conlon, J. E., et al. (2006). Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat. Immunol. 7, 1066-1073. doi: 10.1038/ni1386
54. Montuori, N., Cosimato, V., Rinaldi, L., Rea, V. E. A., Alfano, D., and Ragno, P. (2013). uPAR regulates pericellular proteolysis through a mechanism involving integrins and fMLF-receptors. Thromb. Haemost. 31, 309-318.
55. Motin, V. L., Georgescu, A. M., Fitch, J. P., Gu, P. P., Nelson, D. O., Mabery, S. L., et al. (2004). Temporal global changes in gene expression during temperature transition in Yesinia pestis. J. Bacteriol. 186, 6298-6305. doi: 10.1128/JB.186.18.6298-6305.2004
56. Myöhänen, H., and Vaheri, A. (2004). Regulations and interactions in the activation of cell-associated plasminogen. Cell. Mol. Life Sci. 61, 2840-2858. doi: 10.1007/s00018-004-4230-9
57. Park, C.G., Goh, Y.J., Kook, S.H., Park, H.K., Kim, B.J., Cha, C.,et al. (1997). Incresed expression of urokinase type plasminogen activator (u-PA), plasminogen activator inhibitor-1 (PAI-1), and collagenases in Caco-2 cells infected by Salmonella typhimurium. JKMS 12, 23-31.
58. Prior, J. L., Parkhill, J., Hitchen, P. G., Mungall, K. L., Baker, S. G., Stevens, K., et al. (2001). The failure of different strains of Yersinia pestis toproduce lipopolysaccharide O-antigen under different growth conditions is due to mutations in the O-antigen gene cluster. FEMS Microbiol. Lett. 197, 229-233. doi: 10.1111/j.1574-6968.2001.tb10608.x
59. Ramu, P., Lobo, L. A., Kukkonen, M., Bjur, E., Suomalainen, M., Raukola, H., et al. (2008). Activation of pro-matrix metalloproteinase-9 and degradation of gelatine by the surface protease PgtE of Salmonella enterica serovar Typhimurium. Int. J. Med. Microbiol. 298, 263-278. doi: 10.1016/j.ijmm.2007.06.004
60. Renckens, R., Roelefs, J. J., Bonta, P. I., Florquin, S., de Vries, C. J., Levi, M., et al. (2007). Plasminogen activator inhibitor type 1 is protective during severe Gram-negative pneumoniae. Blood 109, 1593-1601. doi: 10.1182/blood-2006-05-025197
61. Schaller, J., and Gerber, S. S. (2011). The plasmin-antiplasmin system: structural and functional aspects. Cell. Mol. Life Sci. 68, 785-801. doi: 10.1007/s00018-010-0566-5
62. Sebbane, F., Lemaitre, N., Sturdevant, D. E., Rebeil, R., Virtaneva, K., Porcella, S. F., et al. (2006). Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc. Natl. Acad. sci. U.S.A. 103, 11766-11771. doi: 10.1073/pnas.0601182103
63. Semeraro, N., Ammollo, C. T., Semeraro, F., and Colucci, M. (2012). Sepsis, thrombosis and organ dysfunction. Thromb. Res. 129, 290-295. doi: 10.1016/j.thromres.2011.10.013
64. Skurnik, M., Peippo, A., and Ervelä, E. (2000). Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b. Mol. Microbiol. 37, 316-330. doi: 10.1046/j.1365-2958.2000.01993.x
65. Sodeinde, O. A., Subrahmanyan, Y. V., Stark, K., Quan, T., Bao, Y., and Goguen, J. D. (1992). A surface protease and the invasive character of plague. Science 258, 1004-1007. doi: 10.1126/science.1439793
66. Song, Y., Lynch, S. V., Flanagan, J., Zhuo, H., Tom, W., Dotson, R. H., et al. (2007). Increased plasminogen activator inhibitor-1 concentrations in bronchoalveolar lavage fluids are associated with increased mortality in a cohort of patients with Pseudomonas aeruginosa. Anesthesiology 106, 252-261. doi: 10.1097/00000542-200702000-00012
67. Song, Y., Tong, Z., Wang, J., Wang, L., Guo, Z., Han, Y., et al. (2004). Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res. 11, 179-197. doi: 10.1093/dnares/11.3.179
68. Sun, H. (2006). The interaction between pathogens and the host coagulation system. Physiology 21, 281-288. doi: 10.1152/physiol.00059.2005
69. Suomalainen, M., Lobo, L. A., Brandenburg, K., Lindner, K., Virkola, R., Knirel, Y. A., et al. (2010). Temperature-induced changes in the lipopolysaccharide of Yersinia pestis affect plasminogen activation by the Pla surface protease. Infect. Immun. 78, 2644-2652. doi: 10.1128/IAI.01329-09
70. Valls Serón, M., Haiko, J., Korhonen, T. K., de Groot, P. G., and Meijers, C. M. M. (2010). Thrombin-activable fibrinolysis inhibitor is degraded by Salmonella enterica and Yersinia pestis. J. Thromb. Haemost. 8, 2232-2240. doi: 10.1111/j.1538-7836.2010.04014.x
71. van de Craen, B., Declerck, P. J., and Gils, A. (2012). The biochemistry, physiology and pathological roles of PAI-1 and the requirements for PAI-1 inhibition in vivo. Thromb. Res. 130, 576-585. doi: 10.1016/j.thromres.2012.06.023
72. Vandeputte-Rutten, L., Kramer, R. A., Kroon, J., Dekker, N., Egmond, M. R., and Gros, P. (2001). Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. EMBO J. 20, 5033-5039. doi: 10.1093/emboj/20.18.5033
73. van Gorp, E. C. M., Suhart, C., ten Cate, H., Dolmans, W. M. V., van der Meer, J. W. M., ten Cate, J. W., et al. (1999). Review: Infectious diseases and coagulation disorders. J. Inf. Dis. 180, 176-186. doi: 10.1086/314829
74. Vaughan, D. E., and Declerck, P. J. (2003). "Regulation of fibrinolysis," in Thrombosis and Hemorrhage, eds J. Loscalzo and A. I. Schafer (Philadelphia, PA: Lippincott Williams and Wilkins), 105-119.
75. Yun, T. H., Cott, J. E., Tapping, R. I., Slauch, J. M., and Morrissey, J. H. (2009). Proteolytic inactivation of tissue factor pathway inhibitor by bacterial omptins. Blood 113, 1139-1148. doi: 10.1182/blood-2008-05-157180
76. Yun, T. H., and Morrissey, J. H. (2009). Polyphosphate and omptins: novel bacterial procoagulant agents. J. Cell. Mol. Med. 13, 4146-4153. doi: 10.1111/j.1582-4934.2009.00884.x
77. Zeeleder, S., Schroeder, V., Hack, C. E., Kohler, H. P., and Wuillemin, W. A. (2006). TAFI and PAI-1 levels in human sepsis. Thromb Res. 118, 205-212. doi: 10.1016/j.thromres.2005.06.007