Fibrin facilitates both innate and T cell-mediated defense against Yersinia pestis

Journal of Immunology

Volumn 190, Issue 8, 2013, Pages 4149-4161

  Luo, Deyan ^a,f   Lin, Jr Shiuan ^a   Parent, Michelle A ^a,g   Mullarky Kanevsky, Isis ^a,h   Szaba, Frank M ^a   Kummer, Lawrence W ^a   Duso, Debra K ^a   Tighe, Michael ^a   Hill, Jim ^b   Gruber, Andras ^c   Mackman, Nigel ^d   Gailani, David ^e   Smiley, Stephen T ^a  

^a TRUDEAU INSTITUTE   (United States)

^b DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^c Oregon Health and Science University Department of Biomedical Engineering   (United States)

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

^e VANDERBILT UNIVERSITY   (United States)

^f BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^g UNIVERSITY OF DELAWARE   (United States)

^h VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CXCL1 CHEMOKINE; FIBRIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 6; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN FXI; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL GROWTH; BACTERIAL LOAD; BLEEDING; CELL SURVIVAL; CELL VIABILITY; CELLULAR IMMUNITY; CONTROLLED STUDY; HEPATITIS; INFLAMMATORY INFILTRATE; INNATE IMMUNITY; LEUKOCYTE FUNCTION; LUNG INFECTION; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PLAGUE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEPLETION; PROTEIN FUNCTION; SURVIVAL; T LYMPHOCYTE; WILD TYPE; YERSINIA PESTIS;

ANIMALS; BACTERIAL PROTEINS; FIBRIN; FIBRINOGEN; IMMUNITY, INNATE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLAGUE; PLASMINOGEN ACTIVATORS; T-LYMPHOCYTE SUBSETS; YERSINIA PESTIS;

EID: 84875968722     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203253     Document Type: Article

References (93)

1. Perry, R. D., and J. D. Fetherston. 1997. Yersinia pestis - etiologic agent of plague. Clin. Microbiol. Rev. 10: 35-66.
2. Sebbane, F., C. O. Jarrett, D. Gardner, D. Long, and B. J. Hinnebusch. 2006. Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc. Natl. Acad. Sci. USA 103: 5526-5530.
3. Hinnebusch, B. J., and D. L. Erickson. 2008. Yersinia pestis biofilm in the flea vector and its role in the transmission of plague. Curr. Top. Microbiol. Immunol. 322: 229-248.
4. Viboud, G. I., and J. B. Bliska. 2005. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59: 69-89.
5. Du, Y., R. Rosqvist, and A. Forsberg. 2002. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect. Immun. 70: 1453-1460.
6. Montminy, S. W., N. Khan, S. McGrath, M. J. Walkowicz, F. Sharp, J. E. Conlon, K. Fukase, S. Kusumoto, C. Sweet, K. Miyake, et al. 2006. Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat. Immunol. 7: 1066-1073.
7. Telepnev, M. V., G. R. Klimpel, J. Haithcoat, Y. A. Knirel, A. P. Anisimov, and V. L. Motin. 2009. Tetraacylated lipopolysaccharide of Yersinia pestis can inhibit multiple Toll-like receptor-mediated signaling pathways in human dendritic cells. J. Infect. Dis. 200: 1694-1702.
8. Knirel, Y. A., and A. P. Anisimov. 2012. Lipopolysaccharide of Yersinia pestis, the Cause of Plague: Structure, Genetics, Biological Properties. Acta Naturae 4: 46-58.
9. Lien-Teh, W. 1926. A Treatise on Pneumonic Plague. League of Nations Health Organisation, Geneva.
10. Inglesby, T. V., D. T. Dennis, D. A. Henderson, J. G. Bartlett, M. S. Ascher, E. Eitzen, A. D. Fine, A. M. Friedlander, J. Hauer, J. F. Koerner, et al; Working Group on Civilian Biodefense. 2000. Plague as a biological weapon: medical and public health management. JAMA 283: 2281-2290.
11. Kool, J. L. 2005. Risk of person-to-person transmission of pneumonic plague. Clin. Infect. Dis. 40: 1166-1172.
12. Smiley, S. T. 2008. Current challenges in the development of vaccines for pneumonic plague. Expert Rev. Vaccines 7: 209-221.
13. Tilley, R., and N. Mackman. 2006. Tissue factor in hemostasis and thrombosis. Semin. Thromb. Hemost. 32: 5-10.
14. Pawlinski, R., and N. Mackman. 2010. Cellular sources of tissue factor in endotoxemia and sepsis. Thromb. Res. 125(Suppl 1): S70-S73.
15. Rijken, D. C., and H. R. Lijnen. 2009. New insights into the molecular mechanisms of the fibrinolytic system. J. Thromb. Haemost. 7: 4-13.
16. Sun, H. 2006. The interaction between pathogens and the host coagulation system. Physiology (Bethesda) 21: 281-288.
17. Bergmann, S., and S. Hammerschmidt. 2007. Fibrinolysis and host response in bacterial infections. Thromb. Haemost. 98: 512-520.
18. Beesley, E. D., R. R. Brubaker, W. A. Janssen, and M. J. Surgalla. 1967. Pesticins. 3. Expression of coagulase and mechanism of fibrinolysis. J. Bacteriol. 94: 19-26.
19. Sodeinde, O. A., Y. V. Subrahmanyam, K. Stark, T. Quan, Y. Bao, and J. D. Goguen. 1992. A surface protease and the invasive character of plague. Science 258: 1004-1007.
20. Kukkonen, M., K. Lähteenmäki, M. Suomalainen, N. Kalkkinen, L. Emödy, H. Lång, and T. K. Korhonen. 2001. Protein regions important for plasminogen activation and inactivation of alpha2-antiplasmin in the surface protease Pla of Yersinia pestis. Mol. Microbiol. 40: 1097-1111.
21. Haiko, J., L. Laakkonen, K. Juuti, N. Kalkkinen, and T. K. Korhonen. 2010. The omptins of Yersinia pestis and Salmonella enterica cleave the reactive center loop of plasminogen activator inhibitor 1. J. Bacteriol. 192: 4553-4561.
22. Valls Serón, M., J. Haiko, P. G. DE Groot, T. K. Korhonen, and J. C. Meijers. 2010. Thrombin-activatable fibrinolysis inhibitor is degraded by Salmonella enterica and Yersinia pestis. J. Thromb. Haemost. 8: 2232-2240.
23. Welkos, S. L., A. M. Friedlander, and K. J. Davis. 1997. Studies on the role of plasminogen activator in systemic infection by virulent Yersinia pestis strain C092. Microb. Pathog. 23: 211-223.
24. Titball, R. W., and P. C. Oyston. 2007. A plague upon fibrin. Nat. Med. 13: 253-254.
25. Esmon, C. T., J. Xu, and F. Lupu. 2011. Innate immunity and coagulation. J. Thromb. Haemost. 9(Suppl 1): 182-188.
26. Degen, J. L., T. H. Bugge, and J. D. Goguen. 2007. Fibrin and fibrinolysis in infection and host defense. J. Thromb. Haemost. 5(Suppl 1): 24-31.
27. Flick, M. J., X. Du, D. P. Witte, M. Jirousková, D. A. Soloviev, S. J. Busuttil, E. F. Plow, and J. L. Degen. 2004. Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J. Clin. Invest. 113: 1596-1606.
28. Welkos, S., M. L. Pitt, M. Martinez, A. Friedlander, P. Vogel, and R. Tammariello. 2002. Determination of the virulence of the pigmentation-deficient and pigmentation-/plasminogen activator-deficient strains of Yersinia pestis in non-human primate and mouse models of pneumonic plague. Vaccine 20: 2206-2214.
29. Lathem, W. W., P. A. Price, V. L. Miller, and W. E. Goldman. 2007. A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science 315: 509-513.
30. Suh, T. T., K. Holmbäck, N. J. Jensen, C. C. Daugherty, K. Small, D. I. Simon, S. Potter, and J. L. Degen. 1995. Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev. 9: 2020-2033.
31. Gailani, D., N. M. Lasky, and G. J. Broze, Jr. 1997. A murine model of factor XI deficiency. Blood Coagul. Fibrinolysis 8: 134-144.
32. Swaisgood, C. M., D. Schmitt, D. Eaton, and E. F. Plow. 2002. In vivo regulation of plasminogen function by plasma carboxypeptidase B. J. Clin. Invest. 110: 1275-1282.
33. Luo, D., F. M. Szaba, L. W. Kummer, E. F. Plow, N. Mackman, D. Gailani, and S. T. Smiley. 2011. 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. 187: 1866-1876.
34. 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.
35. Mullarky, I. K., F. M. Szaba, K. N. Berggren, M. A. Parent, L. W. Kummer, W. Chen, L. L. Johnson, and S. T. Smiley. 2005. Infection-stimulated fibrin deposition controls hemorrhage and limits hepatic bacterial growth during listeriosis. Infect. Immun. 73: 3888-3895.
36. Szaba, F. M., L. W. Kummer, L. B. Wilhelm, J. S. Lin, M. A. Parent, S. W. Montminy-Paquette, E. Lien, L. L. Johnson, and S. T. Smiley. 2009. D27-pLpxL, an avirulent strain of Yersinia pestis, primes T cells that protect against pneumonic plague. Infect. Immun. 77: 4295-4304.
37. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty per cent endpoints. Am. J. Hyg. 27: 493-497.
38. Anderson, G. W., Jr., P. L. Worsham, C. R. Bolt, G. P. Andrews, S. L. Welkos, A. M. Friedlander, and J. P. Burans. 1997. Protection of mice from fatal bubonic and pneumonic plague by passive immunization with monoclonal antibodies against the F1 protein of Yersinia pestis. Am. J. Trop. Med. Hyg. 56: 471-473.
39. Hill, J., S. E. Leary, K. F. Griffin, E. D. Williamson, and R. W. Titball. 1997. Regions of Yersinia pestis V antigen that contribute to protection against plague identified by passive and active immunization. Infect. Immun. 65: 4476-4482.
40. Kummer, L. W., F. M. Szaba, M. A. Parent, J. J. Adamovicz, J. Hill, L. L. Johnson, and S. T. Smiley. 2008. Antibodies and cytokines independently protect against pneumonic plague. Vaccine 26: 6901-6907.
41. Lin, J. S., S. Park, J. J. Adamovicz, J. Hill, J. B. Bliska, C. K. Cote, D. S. Perlin, K. Amemiya, and S. T. Smiley. 2010. TNFa and IFNg contribute to F1/LcrV-targeted immune defense in mouse models of fully virulent pneumonic plague. Vaccine 29: 357-362.
42. Lin, J. S., F. M. Szaba, L. W. Kummer, B. A. Chromy, and S. T. Smiley. 2011. Yersinia pestis YopE contains a dominant CD8 T cell epitope that confers protection in a mouse model of pneumonic plague. J. Immunol. 187: 897-904.
43. Parent, M. A., K. N. Berggren, L. W. Kummer, L. B. Wilhelm, F. M. Szaba, I. K. Mullarky, and S. T. Smiley. 2005. Cell-mediated protection against pulmonary Yersinia pestis infection. Infect. Immun. 73: 7304-7310.
44. Johnson, L. L., K. N. Berggren, F. M. Szaba, W. Chen, and S. T. Smiley. 2003. Fibrin-mediated protection against infection-stimulated immunopathology. J. Exp. Med. 197: 801-806.
45. Mullarky, I. K., F. M. Szaba, C. G. Winchel, M. A. Parent, L. W. Kummer, N. Mackman, L. L. Johnson, and S. T. Smiley. 2006. In situ assays demonstrate that interferon-gamma suppresses infection-stimulated hepatic fibrin deposition by promoting fibrinolysis. J. Thromb. Haemost. 4: 1580-1587.
46. Ahrenholz, D. H., and R. L. Simmons. 1980. Fibrin in peritonitis. I. Beneficial and adverse effects of fibrin in experimental E. coli peritonitis. Surgery 88: 41-47.
47. Echtenacher, B., K. Weigl, N. Lehn, and D. N. Männel. 2001. Tumor necrosis factor-dependent adhesions as a major protective mechanism early in septic peritonitis in mice. Infect. Immun. 69: 3550-3555.
48. 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.
49. Sun, H., U. Ringdahl, J. W. Homeister, W. P. Fay, N. C. Engleberg, A. Y. Yang, L. S. Rozek, X. Wang, U. Sjöbring, and D. Ginsburg. 2004. Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 305: 1283-1286.
50. Sun, H., X. Wang, J. L. Degen, and D. Ginsburg. 2009. Reduced thrombin generation increases host susceptibility to group A streptococcal infection. Blood 113: 1358-1364.
51. Gailani, D., and G. J. Broze, Jr. 1991. Factor XI activation in a revised model of blood coagulation. Science 253: 909-912.
52. Naito, K., and K. Fujikawa. 1991. Activation of human blood coagulation factor XI independent of factor XII. Factor XI is activated by thrombin and factor XIa in the presence of negatively charged surfaces. J. Biol. Chem. 266: 7353-7358.
53. von dem Borne, P. A., J. C. Meijers, and B. N. Bouma. 1995. Feedback activation of factor XI by thrombin in plasma results in additional formation of thrombin that protects fibrin clots from fibrinolysis. Blood 86: 3035-3042.
54. Gailani, D., and T. Renné. 2007. The intrinsic pathway of coagulation: a target for treating thromboembolic disease? J. Thromb. Haemost. 5: 1106-1112.
55. Lijnen, H. R. 2005. Pleiotropic functions of plasminogen activator inhibitor-1. J. Thromb. Haemost. 3: 35-45.
56. Bajzar, L. 2000. Thrombin activatable fibrinolysis inhibitor and an anti-fibrinolytic pathway. Arterioscler. Thromb. Vasc. Biol. 20: 2511-2518.
57. Morser, J., E. C. Gabazza, T. Myles, and L. L. Leung. 2010. What has been learnt from the thrombin-activatable fibrinolysis inhibitor-deficient mouse? J. Thromb. Haemost. 8: 868-876.
58. Vercauteren, E., M. Peeters, M. F. Hoylaerts, H. R. Lijnen, J. C. Meijers, P. J. Declerck, and A. Gils. 2012. The hyperfibrinolytic state of mice with combined thrombin-activatable fibrinolysis inhibitor (TAFI) and plasminogen activator inhibitor-1 gene deficiency is critically dependent on TAFI deficiency. J. Thromb. Haemost. 10: 2555-2562.
59. Dennis, D. T., K. L. Gage, N. Gratz, J. D. Poland, and E. Tikhomirov. 1999. Plague Manual: Epidemiology, Distribution, Surveillance and Control WHO/CDS/CSR/EDC/99.2. World Health Organization, Geneva.
60. Pollitzer, R. 1954. Plague. World Health Organization, Geneva.
61. Jennewein, C., N. Tran, P. Paulus, P. Ellinghaus, J. A. Eble, and K. Zacharowski. 2011. Novel aspects of fibrin(ogen) fragments during inflammation. Mol. Med. 17: 568-573.
62. Wright, S. D., J. I. Weitz, A. J. Huang, S. M. Levin, S. C. Silverstein, and J. D. Loike. 1988. Complement receptor type three (CD11b/CD18) of human polymorphonuclear leukocytes recognizes fibrinogen. Proc. Natl. Acad. Sci. USA 85: 7734-7738.
63. Loike, J. D., B. Sodeik, L. Cao, S. Leucona, J. I. Weitz, P. A. Detmers, S. D. Wright, and S. C. Silverstein. 1991. CD11c/CD18 on neutrophils recognizes a domain at the N terminus of the A a chain of fibrinogen. Proc. Natl. Acad. Sci. USA 88: 1044-1048.
64. 2, Mac-1) and promotes leukocyte adhesion. J. Biol. Chem. 268: 1847-1853.
65. Weber, C., and T. A. Springer. 1997. Neutrophil accumulation on activated, surface-adherent platelets in flow is mediated by interaction of Mac-1 with fibrinogen bound to alphaIIbbeta3 and stimulated by platelet-activating factor. J. Clin. Invest. 100: 2085-2093.
66. Ugarova, T. P., D. A. Solovjov, L. Zhang, D. I. Loukinov, V. C. Yee, L. V. Medved, and E. F. Plow. 1998. Identification of a novel recognition sequence for integrin alphaM b2 within the gamma-chain of fibrinogen. J. Biol. Chem. 273: 22519-22527.
67. Sitrin, R. G., P. M. Pan, S. Srikanth, and R. F. Todd, III. 1998. Fibrinogen activates NF-kappa B transcription factors in mononuclear phagocytes. J. Immunol. 161: 1462-1470.
68. Forsyth, C. B., D. A. Solovjov, T. P. Ugarova, and E. F. Plow. 2001. Integrin alpha(M)beta(2)-mediated cell migration to fibrinogen and its recognition peptides. J. Exp. Med. 193: 1123-1133.
69. Rubel, C., G. C. Fernández, G. Dran, M. B. Bompadre, M. A. Isturiz, and M. S. Palermo. 2001. Fibrinogen promotes neutrophil activation and delays apoptosis. J. Immunol. 166: 2002-2010.
70. Rubel, C., S. Gómez, G. C. Fernández, M. A. Isturiz, J. Caamaño, and M. S. Palermo. 2003. Fibrinogen-CD11b/CD18 interaction activates the NF-kappa B pathway and delays apoptosis in human neutrophils. Eur. J. Immunol. 33: 1429-1438.
71. Flick, M. J., X. Du, and J. L. Degen. 2004. Fibrin(ogen)-alpha M beta 2 interactions regulate leukocyte function and innate immunity in vivo. Exp. Biol. Med. (Maywood) 229: 1105-1110.
72. Alves, C. S., S. Yakovlev, L. Medved, and K. Konstantopoulos. 2009. Biomolecular characterization of CD44-fibrin(ogen) binding: distinct molecular requirements mediate binding of standard and variant isoforms of CD44 to immobilized fibrin(ogen). J. Biol. Chem. 284: 1177-1189.
73. Szaba, F. M., and S. T. Smiley. 2002. Roles for thrombin and fibrin(ogen) in cytokine/chemokine production and macrophage adhesion in vivo. Blood 99: 1053-1059.
74. Smiley, S. T., J. A. King, and W. W. Hancock. 2001. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J. Immunol. 167: 2887-2894.
75. Barrera, V., O. A. Skorokhod, D. Baci, G. Gremo, P. Arese, and E. Schwarzer. 2011. Host fibrinogen stably bound to hemozoin rapidly activates monocytes via TLR-4 and CD11b/CD18-integrin: a new paradigm of hemozoin action. Blood 117: 5674-5682.
76. 2) integrins (CD11/CD18) in the regulation of cytokine gene expression of polymorphonuclear neutrophils during the inflammatory response. FASEB J. 13: 1855-1865.
77. Sakamoto, K., R. E. Geisel, M. J. Kim, B. T. Wyatt, L. B. Sellers, S. T. Smiley, A. M. Cooper, D. G. Russell, and E. R. Rhoades. 2010. Fibrinogen regulates the cytotoxicity of mycobacterial trehalose dimycolate but is not required for cell recruitment, cytokine response, or control of mycobacterial infection. Infect. Immun. 78: 1004-1011.
78. Walzog, B., F. Jeblonski, A. Zakrzewicz, and P. Gaehtgens. 1997. Beta2 integrins (CD11/CD18) promote apoptosis of human neutrophils. FASEB J. 11: 1177-1186.
79. Whitlock, B. B., S. Gardai, V. Fadok, D. Bratton, and P. M. Henson. 2000. Differential roles for alpha(M)beta(2) integrin clustering or activation in the control of apoptosis via regulation of akt and ERK survival mechanisms. J. Cell Biol. 151: 1305-1320.
80. McCall, T. B., R. M. Palmer, and S. Moncada. 1991. Induction of nitric oxide synthase in rat peritoneal neutrophils and its inhibition by dexamethasone. Eur. J. Immunol. 21: 2523-2527.
81. Evans, T. J., L. D. Buttery, A. Carpenter, D. R. Springall, J. M. Polak, and J. Cohen. 1996. Cytokine-treated human neutrophils contain inducible nitric oxide synthase that produces nitration of ingested bacteria. Proc. Natl. Acad. Sci. USA 93: 9553-9558.
82. Scapini, P., J. A. Lapinet-Vera, S. Gasperini, F. Calzetti, F. Bazzoni, and M. A. Cassatella. 2000. The neutrophil as a cellular source of chemokines. Immunol. Rev. 177: 195-203.
83. Laws, T. R., M. S. Davey, R. W. Titball, and R. Lukaszewski. 2010. Neutrophils are important in early control of lung infection by Yersinia pestis. Microbes Infect. 12: 331-335.
84. Lukaszewski, R. A., D. J. Kenny, R. Taylor, D. G. Rees, M. G. Hartley, and P. C. Oyston. 2005. Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect. Immun. 73: 7142-7150.
85. Levy, Y., Y. Flashner, A. Tidhar, A. Zauberman, M. Aftalion, S. Lazar, D. Gur, A. Shafferman, and E. Mamroud. 2011. T cells play an essential role in anti-F1 mediated rapid protection against bubonic plague. Vaccine 29: 6866-6873.
86. Pettersson, J., A. Holmström, J. Hill, S. Leary, E. Frithz-Lindsten, A. von Euler-Matell, E. Carlsson, R. Titball, A. Forsberg, and H. Wolf-Watz. 1999. The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol. Microbiol. 32: 961-976.
87. Cowan, C., A. V. Philipovskiy, C. R. Wulff-Strobel, Z. Ye, and S. C. Straley. 2005. Anti-LcrV antibody inhibits delivery of Yops by Yersinia pestis KIM5 by directly promoting phagocytosis. Infect. Immun. 73: 6127-6137.
88. Cornelius, C. A., L. E. Quenee, D. Elli, N. A. Ciletti, and O. Schneewind. 2009. Yersinia pestis IS1541 transposition provides for escape from plague immunity. Infect. Immun. 77: 1807-1816.
89. Delvaeye, M., and E. M. Conway. 2009. Coagulation and innate immune responses: can we view them separately? Blood 114: 2367-2374.
90. Levi, M., and T. van der Poll. 2010. Inflammation and coagulation. Crit. Care Med. 38(Suppl): S26-S34.
91. Stearns-Kurosawa, D. J., M. F. Osuchowski, C. Valentine, S. Kurosawa, and D. G. Remick. 2011. The pathogenesis of sepsis. Annu. Rev. Pathol. 6: 19-48.
92. Riedemann, N. C., R. F. Guo, and P. A. Ward. 2003. The enigma of sepsis. J. Clin. Invest. 112: 460-467.
93. Dyson, A., and M. Singer. 2009. Animal models of sepsis: why does preclinical efficacy fail to translate to the clinical setting? Crit. Care Med. 37(Suppl): S30- S37.