Bacillus anthracis cell wall peptidoglycan but not lethal or edema toxins produces changes consistent with disseminated intravascular coagulation in a rat model

Journal of Infectious Diseases

Volumn 208, Issue 6, 2013, Pages 978-989

  Qiu, Ping ^a   Li, Yan ^a   Shiloach, Joseph ^b   Cui, Xizhong ^a   Sun, Junfeng ^a   Trinh, Loc ^b   Kubler Kielb, Joanna ^c   Vinogradov, Evgeny ^e   Mani, Haresh ^d   Al Hamad, Mariam ^a   Fitz, Yvonne ^a   Eichacker, Peter Q ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b National Institute of Diabetes   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d INOVA FAIRFAX HOSPITAL   (United States)

^e NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

anthrax infection; Bacillus anthracis; coagulopathy; disseminated intravascular coagulation; edema toxin; lethal toxin; peptidoglycan; sepsis; thrombocytopenia

Indexed keywords

BACTERIAL TOXIN; EDEMA TOXIN; FIBRINOGEN; LETHAL TOXIN; PEPTIDOGLYCAN; PLASMINOGEN ACTIVATOR INHIBITOR; PROTEIN C; PROTHROMBIN; THROMBIN ANTITHROMBIN COMPLEX; THROMBOPLASTIN; TISSUE FACTOR PATHWAY INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTHRAX; BLOOD CLOTTING; CONFERENCE PAPER; CONTROLLED STUDY; DISSEMINATED INTRAVASCULAR CLOTTING; FIBRINOLYSIS; LETHALITY; NONHUMAN; PARTIAL THROMBOPLASTIN TIME; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; THROMBOCYTE COUNT;

ANTHRAX INFECTION; BACILLUS ANTHRACIS; COAGULOPATHY; DISSEMINATED INTRAVASCULAR COAGULATION; EDEMA TOXIN; LETHAL TOXIN; PEPTIDOGLYCAN; SEPSIS; THROMBOCYTOPENIA;

ANIMALS; ANTHRAX; ANTIGENS, BACTERIAL; ANTITHROMBIN III; BACILLUS ANTHRACIS; BACTERIAL TOXINS; BLOOD COAGULATION; CELL WALL; DISSEMINATED INTRAVASCULAR COAGULATION; FIBRINOGEN; NITRIC OXIDE; PARTIAL THROMBOPLASTIN TIME; PEPTIDE HYDROLASES; PEPTIDOGLYCAN; PLASMINOGEN INACTIVATORS; PROTEIN C; PROTHROMBIN; RATS; RATS, SPRAGUE-DAWLEY; THROMBOPLASTIN;

EID: 84880162172     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jit247     Document Type: Conference Paper

References (50)

1. Sweeney DA, Hicks CW, Cui X, Li Y, Eichacker PQ. Anthrax infection. Am J Respir Crit Care Med 2011; 184:1333-41.
2. Hicks CW, Sweeney DA, Cui X, Li Y, Eichacker PQ. An overview of anthrax infection including the recently identified form of disease in injection drug users. Intensive Care Med 2012; 38:1092-104.
3. Abramova FA, Grinberg LM, Yampolskaya OV, Walker DH. Pathology of inhalational anthrax in 42 cases from the Sverdlovsk outbreak of 1979. Proc Natl Acad Sci USA 1993; 90:2291-4.
4. Grinberg LM, Abramova FA, Yampolskaya OV, Walker DH, Smith JH. Quantitative pathology of inhalational anthrax I: quantitative microscopic findings. Mod Pathol 2001; 14:482-95.
5. Twenhafel NA. Pathology of inhalational anthrax animal models. Vet Pathol 2010; 47:819-30.
6. Stearns-Kurosawa DJ, Lupu F, Taylor FB Jr, Kinasewitz G, Kurosawa S. Sepsis and pathophysiology of anthrax in a nonhuman primate model. Am J Pathol 2006; 169:433-44.
7. Klempner MS, Talbot EA, Lee SI, Zaki S, Ferraro MJ. Case records of the Massachusetts General Hospital. Case 25-2010. A 24-year-old woman with abdominal pain and shock. N Engl J Med 2010; 363: 766-77.
8. Freedman A, Afonja O, Chang MW, et al. Cutaneous anthrax associated with microangiopathic hemolytic anemia and coagulopathy in a 7-month-old infant. JAMA 2002; 287:869-74.
9. Moayeri M, Sastalla I, Leppla SH. Anthrax and the inflammasome. Microbes Infect 2012; 14:392-400.
10. Weidenmaier C, Peschel A. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 2008; 6:276-87.
11. Levi M, van der Poll T, Schultz M. Infection and inflammation as risk factors for thrombosis and atherosclerosis. Semin Thromb Hemost 2012; 38:506-14.
12. Opal SM, Esmon CT. Bench-to-bedside review: functional relationships between coagulation and the innate immune response and their respective roles in the pathogenesis of sepsis. Crit Care 2003; 7:23-38.
13. Tournier JN, Rossi Paccani S, Quesnel-Hellmann A, Baldari CT. Anthrax toxins: a weapon to systematically dismantle the host immune defenses. Mol Aspects Med 2009; 30:456-66.
14. Triantafilou M, Uddin A, Maher S, et al. Anthrax toxin evades Toll-like receptor recognition, whereas its cell wall components trigger activation via TLR2/6 heterodimers. Cell Microbiol 2007; 9:2880-92.
15. Langer M, Malykhin A, Maeda K, et al. Bacillus anthracis peptidoglycan stimulates an inflammatory response in monocytes through the p38 mitogen-activated protein kinase pathway. PloS One 2008; 3:e3706.
16. Iyer JK, Khurana T, Langer M, et al. Inflammatory cytokine response to Bacillus anthracis peptidoglycan requires phagocytosis and lysosomal trafficking. Infect Immun 2010; 78:2418-28.
17. Cui X, Su J, Li Y, et al. Bacillus anthracis cell wall produces injurious inflammation but paradoxically decreases the lethality of anthrax lethal toxin in a rat model. Intensive Care Med 2010; 36:148-56.
18. Ekwunife FS, Singh J, Taylor KG, Doyle RJ. Isolation and purification of cell wall polysaccharide of Bacillus anthracis (delta Sterne). FEMS Microbiol Lett 1991; 66:257-62.
19. Cooksey BA, Sampey GC, Pierre JL, et al. Production of biologically active Bacillus anthracis edema factor in Escherichia coli. Biotechnol Prog 2004; 20:1651-9.
20. Gwinn W, Zhang M, Mon S, et al. Scalable purification of Bacillus anthracis protective antigen from Escherichia coli. Protein Expr Purif 2006; 45:30-6.
21. Laird MW, Zukauskas D, Johnson K, et al. Production and purification of Bacillus anthracis protective antigen from Escherichia coli. Protein Expr Purif 2004; 38:145-52.
22. Chen PS Jr, Toribar TY, Warner H. Microdetermination of phosphorus. Anal Chem 1956; 28:1756-8.
23. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193:265-75.
24. Scott TA ME. Determination of dextran with anthrone. Anal Chem 1953; 25:1656-61.
25. MacKenzie SL. Gas-chromatograpfic analysis of amino acids as the N-heptafluorobutyryl izobutyl esters. J Assoc Off Anal Chem 1987; 70:151-60.
26. Cui X, Moayeri M, Li Y, et al. Lethality during continuous anthrax lethal toxin infusion is associated with circulatory shock but not inflammatory cytokine or nitric oxide release in rats. Am J Physiol Regul Integr Comp Physiol 2004; 286:R699-709.
27. Qiu P, Li Y, Ding Y, et al. The individual survival benefits of tumor necrosis factor soluble receptor and fluid administration are not additive in a rat sepsis model. Intensive Care Med 2011; 37:1688-95.
28. Li Y, Sun JF, Cui X, et al. The effect of heparin administration in animal models of sepsis: a prospective study in Escherichia coli-challenged mice and a systematic review and metaregression analysis of published studies. Crit Care Med 2011; 39:1104-12.
29. Ratney RS. The chemistry of the cell walls of bacillus anthracis: the effect of penicillin. Biochim Biophys Acta 1965; 101:1-5.
30. Bacher G, Korner R, Atrih A, Foster SJ, Roepstorff P, Allmaier G. Negative and positive ion matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and positive ion nano-electrospray ionization quadrupole ion trap mass spectrometry of peptidoglycan fragments isolated from various Bacillus species. J Mass Spectrom 2001; 36:124-39.
31. Levi M, Toh CH, Thachil J, Watson HG. Guidelines for the diagnosis and management of disseminated intravascular coagulation. Br J Haematol. 2009; 145:24-33.
32. Rao LV, Ngyuen M, Pendurthi UR. Lethal toxin of Bacillus anthracis inhibits tissue factor expression in vascular cells. J Thromb Haemost 2004; 2:530-2.
33. Moayeri M, Haines D, Young HA, Leppla SH. Bacillus anthracis lethal toxin induces TNF-alpha-independent hypoxia-mediated toxicity in mice. J Clin Invest 2003; 112:670-82.
34. Trescos Y, Tournier JN. Cytoskeleton as an emerging target of anthrax toxins. Toxins 2012; 4:83-97.
35. Kau JH, Sun DS, Tsai WJ, et al. Antiplatelet activities of anthrax lethal toxin are associated with suppressed p42/44 and p38 mitogen-activated protein kinase pathways in the platelets. J Infect Dis 2005; 192: 1465-74.
36. Alam S, Gupta M, Bhatnagar R. Inhibition of platelet aggregation by anthrax edema toxin. Biochem Biophys Res Commun 2006; 339: 107-14.
37. Chauncey KM, Szarowicz SE, Sidhu GS, During RL, Southwick FS. Anthrax lethal and edema toxins fail to directly impair human platelet function. J Infect Dis 2012; 205:453-7.
38. Culley NC, Pinson DM, Chakrabarty A, Mayo MS, LeVine SM. Pathophysiological manifestations in mice exposed to anthrax lethal toxin. Infect Immun 2005; 73:7006-10.
39. Mattsson E, Herwald H, Bjorck L, Egesten A. Peptidoglycan from Staphylococcus aureus induces tissue factor expression and procoagulant activity in human monocytes. Infect Immun 2002; 70:3033-9.
40. Mattsson E, Heying R, van de Gevel JS, Hartung T, Beekhuizen H. Staphylococcal peptidoglycan initiates an inflammatory response and procoagulant activity in human vascular endothelial cells: a comparison with highly purified lipoteichoic acid and TSST-1. FEMS Immunol Med Microbiol 2008; 52:110-7.
41. Kothari H, Rao LV, Vankayalapati R, Pendurthi UR. Mycobacterium tuberculosis infection and tissue factor expression in macrophages. PloS one 2012; 7:e45700.
42. Chung MC, Popova TG, Jorgensen SC, et al. Degradation of circulating vonWillebrand factor and its regulator ADAMTS13 implicates secreted Bacillus anthracis metalloproteases in anthrax consumptive coagulopathy. J Biol Chem 2008; 283:9531-42.
43. Chung MC, Jorgensen SC, Popova TG, Bailey CL, Popov SG. Neutrophil elastase and syndecan shedding contribute to antithrombin depletion in murine anthrax. FEMS ImmunolMed Microbiol 2008; 54: 309-18.
44. Chung MC, Jorgensen SC, Popova TG, Tonry JH, Bailey CL, Popov SG. Activation of plasminogen activator inhibitor implicates protease InhA in the acute-phase response to Bacillus anthracis infection. J Med Microbiol 2009; 58:737-44.
45. Chung MC, Jorgensen SC, Tonry JH, Kashanchi F, Bailey C, Popov S. Secreted Bacillus anthracis proteases target the host fibrinolytic system. FEMS Immunol Med Microbiol 2011; 62:173-81.
46. Smith H, Keppie J, Stanley JL. Observations on the cause of death in experimental anthrax. Lancet 1954; 267:474-6.
47. Wray GM, Foster SJ, Hinds CJ, Thiemermann C. A cell wall component from pathogenic and non-pathogenic gram-positive bacteria (peptidoglycan) synergises with endotoxin to cause the release of tumour necrosis factor-alpha, nitric oxide production, shock, and multiple organ injury/dysfunction in the rat. Shock 2001; 15:135-42.
48. Guarner J, Jernigan JA, Shieh WJ, et al. Pathology and pathogenesis of bioterrorism-related inhalational anthrax. Am J Pathol 2003; 163: 701-9.
49. Holty JE, Bravata DM, Liu H, Olshen RA, McDonald KM, Owens DK. Systematic review: a century of inhalational anthrax cases from 1900 to 2005. Ann Intern Med 2006; 144:270-80.
50. Quintiliani R Jr, Quintiliani R. Inhalational anthrax and bioterrorism. Curr Opin Pulm Med 2003; 9:221-6.