Anthrax toxin: Pathologic effects on the cardiovascular system

Frontiers in Bioscience

Volumn 14, Issue 6, 2009, Pages 2335-2357

  Golden, Honey B ^a   Watson, Linley E ^b   Lal, Hind ^a   Verma, Suresh K ^a   Foster, Donald M ^c   Kuo, Shu Ru ^b   Sharma, Avadhesh ^d   Frankel, Arthur ^b   Dostal, David E ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

^b SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

Anthrax; Anthrax receptor 1 2; Calmodulin; Cardiomyocytes; Edema factor; Heart failure; Hypotension; Lethal factor; Mitogen activated protein kinase; Phospholamban; Protective antigen; Reivew

Indexed keywords

BACILLUS ANTHRACIS; BACTERIA (MICROORGANISMS);

ANTHRAX TOXIN; BACTERIAL ANTIGEN; BACTERIAL TOXIN;

ANTHRAX; CARDIOVASCULAR SYSTEM; CHEMISTRY; DRUG EFFECT; HUMAN; METABOLISM; PATHOPHYSIOLOGY; REVIEW;

ANTHRAX; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; CARDIOVASCULAR SYSTEM; HUMANS;

EID: 63849240549     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3382     Document Type: Article

References (141)

1. Pannifer, A. D., T. Y. Wong, R. Schwarzenbacher, M. Renatus, C. Petosa, J. Bienkowska, D. B. Lacy, R. J. Collier, S. Park, S. H. Leppla, P. Hanna & R. C. Liddington: Crystal structure of the anthrax lethal factor. Nature 414, 229-33 (2001). (Pubitemid 33051240)
2. Jones, M. B., R. Jani, D. Ren, T. K. Wood & M. J. Blaser: Inhibition of Bacillus anthracis growth and virulence-gene expression by inhibitors of quorum-sensing. J Infect Dis 191, 1881-8 (2005). (Pubitemid 40705396)
3. Lacy, D. B. & R. J. Collier: Structure and function of anthrax toxin. Curr Top Microbiol Immunol 271, 61-85 (2002). (Pubitemid 34847395)
4. Arora, N. & S. H. Leppla: Residues 1-254 of anthrax toxin lethal factor are sufficient to cause cellular uptake of fused polypeptides. J Biol Chem 268, 3334-41 (1993). (Pubitemid 23070965)
5. Tonello, F., P. Ascenzi & C. Montecucco: The metalloproteolytic activity of the anthrax lethal factor is substrate-inhibited. J Biol Chem 278, 40075-8 (2003). (Pubitemid 37248573)
6. Turk, B. E., T. Y. Wong, R. Schwarzenbacher, E. T. Jarrell, S. H. Leppla, R. J. Collier, R. C. Liddington & L. C. Cantley: The structural basis for substrate and inhibitor selectivity of the anthrax lethal factor. Nat Struct Mol Biol 11, 60-6 (2004). (Pubitemid 38173442)
7. Shen, Y., N. L. Zhukovskaya, Q. Guo, J. Florian & W. J. Tang: Calcium-independent calmodulin binding and two metalion catalytic mechanism of anthrax edema factor. Embo J 24, 929-41 (2005). (Pubitemid 40470142)
8. Drum, C. L., S. Z. Yan, J. Bard, Y. Q. Shen, D. Lu, S. Soelaiman, Z. Grabarek, A. Bohm & W. J. Tang: Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin. Nature 415, 396-402 (2002). (Pubitemid 34100945)
9. Leppla, S. H.: Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc Natl Acad Sci U S A 79, 3162-6 (1982). (Pubitemid 12008374)
10. Lacy, D. B., M. Mourez, A. Fouassier & R. J. Collier: Mapping the anthrax protective antigen binding site on the lethal and edema factors. J Biol Chem 277, 3006-10 (2002). (Pubitemid 34953337)
11. Kumar, P., N. Ahuja & R. Bhatnagar: Purification of anthrax edema factor from Escherichia coli and identification of residues required for binding to anthrax protective antigen. Infect Immun 69, 6532-6 (2001). (Pubitemid 32885222)
12. Bradley, K. A., J. Mogridge, G. Jonah, A. Rainey, S. Batty & J. A. Young: Binding of anthrax toxin to its receptor is similar to alpha integrin-ligand interactions. J Biol Chem 278, 49342-7 (2003).
13. Bradley, K. A., J. Mogridge, M. Mourez, R. J. Collier & J. A. Young: Identification of the cellular receptor for anthrax toxin. Nature 414, 225-9 (2001). (Pubitemid 33051239)
14. Scobie, H. M., G. J. Rainey, K. A. Bradley & J. A. Young: Human capillary morphogenesis protein 2 functions as an anthrax toxin receptor. Proc Natl Acad Sci U S A 100, 5170-4 (2003). (Pubitemid 36542677)
15. Bell, S. E., A. Mavila, R. Salazar, K. J. Bayless, S. Kanagala, S. A. Maxwell & G. E. Davis: Differential gene expression during capillary morphogenesis in 3D collagen matrices: regulated expression of genes involved in basement membrane matrix assembly, cell cycle progression, cellular differentiation and G-protein signaling. J Cell Sci 114, 2755-73 (2001). (Pubitemid 32785455)
16. Nanda, A., E. B. Carson-Walter, S. Seaman, T. D. Barber, J. Stampfl, S. Singh, B. Vogelstein, K. W. Kinzler & B. St Croix: TEM8 interacts with the cleaved C5 domain of collagen alpha 3 (VI). Cancer Res 64, 817-20 (2004). (Pubitemid 38176877)
17. Dowling, O., A. Difeo, M. C. Ramirez, T. Tukel, G. Narla, L. Bonafe, H. Kayserili, M. Yuksel-Apak, A. S. Paller, K. Norton, A. S. Teebi, V. Grum-Tokars, G. S. Martin, G. E. Davis, M. J. Glucksman & J. A. Martignetti: Mutations in capillary morphogenesis gene-2 result in the allelic disorders juvenile hyaline fibromatosis and infantile systemic hyalinosis. Am J Hum Genet 73, 957-66 (2003). (Pubitemid 37271897)
18. Hanks, S., S. Adams, J. Douglas, L. Arbour, D. J. Atherton, S. Balci, H. Bode, M. E. Campbell, M. Feingold, G. Keser, W. Kleijer, G. Mancini, J. A. McGrath, F. Muntoni, A. Nanda, M. D. Teare, M. Warman, F. M. Pope, A. Superti-Furga, P. A. Futreal & N. Rahman: Mutations in the gene encoding capillary morphogenesis protein 2 cause juvenile hyaline fibromatosis and infantile systemic hyalinosis. Am J Hum Genet 73, 791-800 (2003). (Pubitemid 37271883)
19. Bonuccelli, G., F. Sotgia, P. G. Frank, T. M. Williams, C. J. de Almeida, H. B. Tanowitz, P. E. Scherer, K. A. Hotchkiss, B. I. Terman, B. Rollman, A. Alileche, J. Brojatsch & M. P. Lisanti: ATR/TEM8 is highly expressed in epithelial cells lining Bacillus anthracis' three sites of entry: implications for the pathogenesis of anthrax infection. Am J Physiol Cell Physiol 288, C1402-10 (2005). (Pubitemid 40991077)
20. Hotchkiss, K. A., C. M. Basile, S. C. Spring, G. Bonuccelli, M. P. Lisanti & B. I. Terman: TEM8 expression stimulates endothelial cell adhesion and migration by regulating cell-matrix interactions on collagen. Exp Cell Res 305, 133-44 (2005). (Pubitemid 40380660)
21. Werner, E., A. P. Kowalczyk & V. Faundez: Anthrax toxin receptor 1/tumor endothelium marker 8 mediates cell spreading by coupling extracellular ligands to the actin cytoskeleton. J Biol Chem 281, 23227-36 (2006).
22. Lee, J. O., P. Rieu, M. A. Arnaout & R. Liddington: Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11b/CD18). Cell 80, 631-8 (1995).
23. Shimaoka, M., J. Takagi & T. A. Springer: Conformational regulation of integrin structure and function. Annu Rev Biophys Biomol Struct 31, 485-516 (2002). (Pubitemid 34666842)
24. Triantafilou, M., A. Uddin, S. Maher, N. Charalambous, T. S. Hamm, A. Alsumaiti & K. Triantafilou: Anthrax toxin evades Toll-like receptor recognition, whereas its cell wall components trigger activation via TLR2/6 heterodimers. Cell Microbiol (2007).
25. Wei, W., Q. Lu, G. J. Chaudry, S. H. Leppla & S. N. Cohen: The LDL receptor-related protein LRP6 mediates internalization and lethality of anthrax toxin. Cell 124, 1141-54 (2006).
26. Schneider, W. J. & J. Nimpf: LDL receptor relatives at the crossroad of endocytosis and signaling. Cell Mol Life Sci 60, 892-903 (2003). (Pubitemid 36735120)
27. Willnow, T. E. & J. Herz: Genetic deficiency in low density lipoprotein receptor-related protein confers cellular resistance to Pseudomonas exotoxin A. Evidence that this protein is required for uptake and degradation of multiple ligands. J Cell Sci 107 ( Pt 3), 719-26 (1994).
28. Young, J. J., J. L. Bromberg-White, C. Zylstra, J. T. Church, E. Boguslawski, J. H. Resau, B. O. Williams & N. S. Duesbery: LRP5 and LRP6 are not required for protective antigen-mediated internalization or lethality of anthrax lethal toxin. PLoS Pathog 3, e27 (2007).
29. Mao, B., W. Wu, Y. Li, D. Hoppe, P. Stannek, A. Glinka & C. Niehrs: LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 411, 321-5 (2001). (Pubitemid 32467039)
30. Young, J. A. & R. J. Collier: Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu Rev Biochem 76, 243-65 (2007).
31. Collier, R. J. & J. A. Young: Anthrax toxin. Annu Rev Cell Dev Biol 19, 45-70 (2003). (Pubitemid 37487342)
32. Rainey, G. J., D. J. Wigelsworth, P. L. Ryan, H. M. Scobie, R. J. Collier & J. A. Young: Receptor-specific requirements for anthrax toxin delivery into cells. Proc Natl Acad Sci U S A 102, 13278-83 (2005). (Pubitemid 41325014)
33. Wolfe, J. T., B. A. Krantz, G. J. Rainey, J. A. Young & R. J. Collier: Whole-cell voltage clamp measurements of anthrax toxin pore current. J Biol Chem 280, 39417-22 (2005). (Pubitemid 41713899)
34. Abrami, L., M. Lindsay, R. G. Parton, S. H. Leppla & F. G. van der Goot: Membrane insertion of anthrax protective antigen and cytoplasmic delivery of lethal factor occur at different stages of the endocytic pathway. J Cell Biol 166, 645-51 (2004). (Pubitemid 39181002)
35. Lacy, D. B., D. J. Wigelsworth, R. A. Melnyk, S. C. Harrison & R. J. Collier: Structure of heptameric protective antigen bound to an anthrax toxin receptor: a role for receptor in pH-dependent pore formation. Proc Natl Acad Sci USA 101, 13147-51 (2004). (Pubitemid 39209633)
36. Gao, M. & K. Schulten: Onset of anthrax toxin pore formation. Biophys J 90, 3267-79 (2006).
37. Scobie, H. M., J. M. Marlett, G. J. Rainey, D. B. Lacy, R. J. Collier & J. A. Young: Anthrax toxin receptor 2 determinants that dictate the pH threshold of toxin pore formation. PLoS ONE 2, e329 (2007).
38. Krantz, B. A., R. A. Melnyk, S. Zhang, S. J. Juris, D. B. Lacy, Z. Wu, A. Finkelstein & R. J. Collier: A phenylalanine clamp catalyzes protein translocation through the anthrax toxin pore. Science 309, 777-81 (2005). (Pubitemid 41077325)
39. Shadomy, S. V. & A. R. Hoffmaster: Clinical manifestations and diagnosis of anthrax. 15.3 ed. (2007).
40. Borio, L., D. Frank, V. Mani, C. Chiriboga, M. Pollanen, M. Ripple, S. Ali, C. DiAngelo, J. Lee, J. Arden, J. Titus, D. Fowler, T. O'Toole, H. Masur, J. Bartlett & T. Inglesby: Death due to bioterrorism-related inhalational anthrax: report of 2 patients. Jama 286, 2554-9 (2001). (Pubitemid 33096806)
41. Mina, B., J. P. Dym, F. Kuepper, R. Tso, C. Arrastia, I. Kaplounova, H. Faraj, A. Kwapniewski, C. M. Krol, M. Grosser, J. Glick, S. Fochios, A. Remolina, L. Vasovic, J. Moses, T. Robin, M. DeVita & M. L. Tapper: Fatal inhalational anthrax with unknown source of exposure in a 61-year-old woman in New York City. Jama 287, 858-62 (2002). (Pubitemid 34252032)
42. Mayer, T. A., S. Bersoff-Matcha, C. Murphy, J. Earls, S. Harper, D. Pauze, M. Nguyen, J. Rosenthal, D. Cerva, Jr., G. Druckenbrod, D. Hanfling, N. Fatteh, A. Napoli, A. Nayyar & E. L. Berman: Clinical presentation of inhalational anthrax following bioterrorism exposure: report of 2 surviving patients. Jama 286, 2549-53 (2001). (Pubitemid 33096805)
43. Malecki, J., S. Wiersma, T. Cahill, M. Grossman, H. Hochman, M. Tapper, M. Pomeranz, A. Friedman-Kien, A. Gurtman, E. Bresnitz, G. DiFernando, P. Lurie, K. Nalluswami, D. Frank, L. Siegel, S. Adams, I. Walks, J. Davies-Coles, C. Chiriboga & R. Brechner: Update: Investigation of Bioterrorism-Related Anthrax and Interim Guidelines for Clinical Evaluation of Persons with Possible Anthrax. Morbidity and Mortality Weekly Report 941-8 (2001).
44. Beall, F. A. & F. G. Dalldorf: The pathogenesis of the lethal effect of anthrax toxin in the rat. J Infect Dis 116, 377-89 (1966).
45. Beall, F. A., M. J. Taylor & C. B. Thorne: Rapid lethal effect in rats of a third component found upon fractionating the toxin of Bacillus anthracis. J Bacteriol 83, 1274-80 (1962).
46. Moayeri, M. & S. H. Leppla: The roles of anthrax toxin in pathogenesis. Curr Opin Microbiol 7, 19-24 (2004). (Pubitemid 38223950)
47. Moayeri, M., D. Haines, H. A. Young & S. H. Leppla: Bacillus anthracis lethal toxin induces TNF-alphaindependent hypoxia-mediated toxicity in mice. J Clin Invest 112, 670-82 (2003). (Pubitemid 38057708)
48. Watson, L. E., S. R. Kuo, K. Katki, T. Dang, S. K. Park, D. E. Dostal, W. J. Tang, S. H. Leppla & A. E. Frankel: Anthrax toxins induce shock in rats by depressed cardiac ventricular function. PLoS ONE 2, e466 (2007).
49. Watson, L. E., J. Mock, H. Lal, G. Lu, R. W. Bourdeau, W. J. Tang, S. H. Leppla, D. E. Dostal & A. E. Frankel: Lethal and edema toxins of anthrax induce distinct hemodynamic dysfunction. Front Biosci 12, 4670-5 (2007).
50. Cui, X., M. Moayeri, Y. Li, X. Li, M. Haley, Y. Fitz, R. Correa-Araujo, S. M. Banks, S. H. Leppla & P. Q. Eichacker: 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 286, R699-709 (2004). (Pubitemid 38375001)
51. Cui, X., Y. Li, M. Moayeri, G. H. Choi, G. M. Subramanian, X. Li, M. Haley, Y. Fitz, J. Feng, S. M. Banks, S. H. Leppla & P. Q. Eichacker: Late treatment with a protective antigen-directed monoclonal antibody improves hemodynamic function and survival in a lethal toxin-infused rat model of anthrax sepsis. J Infect Dis 191, 422-34 (2005). (Pubitemid 40139768)
52. Popov, S. G., T. G. Popova, S. Hopkins, R. S. Weinstein, R. MacAfee, K. J. Fryxell, V. Chandhoke, C. Bailey & K. Alibek: Effective antiprotease-antibiotic treatment of experimental anthrax. BMC Infect Dis 5, 25 (2005).
53. Cheng, C. & S. Masutani: The Causal Role of Left Ventricular Dysfunction and Heart Failure in the Lethality of Anthrax Lethal Toxin in Dog. D. L. Watson, Ed. (2005).
54. Vick, J. A., R. E. Lincoln, F. Klein, B. G. Mahlandt, J. S. Walker & D. C. Fish: Neurological and physiological responses of the primate to anthrax toxin. J Infect Dis 118, 85- 96 (1968).
55. Remmele, N. S., F. Klein, J. A. Vick, J. S. Walker, B. G. Mahlandt & R. E. Lincoln: Anthrax toxin: primary site of action. J Infect Dis 118, 104-13 (1968).
56. Cui, X., Y. Li, X. Li, M. W. Laird, M. Subramanian, M. Moayeri, S. H. Leppla, Y. Fitz, J. Su, K. Sherer & P. Q. Eichacker: Bacillus anthracis edema and lethal toxin have different hemodynamic effects but function together to worsen shock and outcome in a rat model. J Infect Dis 195, 572-80 (2007). (Pubitemid 46214400)
57. Murray, K. J.: Cyclic AMP and mechanisms of vasodilation. Pharmacol Ther 47, 329-45 (1990). (Pubitemid 20309555)
58. Wegener, A. D., H. K. Simmerman, J. Liepnieks & L. R. Jones: Proteolytic cleavage of phospholamban purified from canine cardiac sarcoplasmic reticulum vesicles. Generation of a low resolution model of phospholamban structure. J Biol Chem 261, 5154-9 (1986). (Pubitemid 17204313)
59. Fujii, J., A. Ueno, K. Kitano, S. Tanaka, M. Kadoma & M. Tada: Complete complementary DNA-derived amino acid sequence of canine cardiac phospholamban. J Clin Invest 79, 301-4 (1987). (Pubitemid 17232533)
60. Toyofuku, T., K. Kurzydlowski, M. Tada & D. H. MacLennan: Amino acids Glu2 to Ile18 in the cytoplasmic domain of phospholamban are essential for functional association with the Ca (2+)-ATPase of sarcoplasmic reticulum. J Biol Chem 269, 3088-94 (1994).
61. Voss, J., L. R. Jones & D. D. Thomas: The physical mechanism of calcium pump regulation in the heart. Biophys J 67, 190-6 (1994). (Pubitemid 24197884)
62. Wang, Y.: Mitogen-activated protein kinases in heart development and diseases. Circulation 116, 1413- 23 (2007). (Pubitemid 47417568)
63. Fukuda, M., Y. Gotoh & E. Nishida: Interaction of MAP kinase with MAP kinase kinase: its possible role in the control of nucleocytoplasmic transport of MAP kinase. Embo J 16, 1901-8 (1997). (Pubitemid 27170951)
64. Fukuda, M., I. Gotoh, Y. Gotoh & E. Nishida: Cytoplasmic localization of mitogen-activated protein kinase kinase directed by its NH2-terminal, leucine-rich short amino acid sequence, which acts as a nuclear export signal. J Biol Chem 271, 20024-8 (1996). (Pubitemid 26281751)
65. Fukuda, M., I. Gotoh, M. Adachi, Y. Gotoh & E. Nishida: A novel regulatory mechanism in the mitogenactivated protein (MAP) kinase cascade. Role of nuclear export signal of MAP kinase kinase. J Biol Chem 272, 32642-8 (1997). (Pubitemid 28011955)
66. Vitale, G., L. Bernardi, G. Napolitani, M. Mock & C. Montecucco: Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochem J 352 Pt 3, 739-45 (2000). (Pubitemid 32015030)
67. Duesbery, N. S., C. P. Webb, S. H. Leppla, V. M. Gordon, K. R. Klimpel, T. D. Copeland, N. G. Ahn, M. K. Oskarsson, K. Fukasawa, K. D. Paull & G. F. Vande Woude: Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280, 734-7 (1998). (Pubitemid 28243347)
68. Park, J. M., F. R. Greten, Z. W. Li & M. Karin: Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science 297, 2048-51 (2002).
69. Kau, J. H., D. S. Sun, W. J. Tsai, H. F. Shyu, H. H. Huang, H. C. Lin & H. H. Chang: 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 192, 1465-74 (2005).
70. Fang, H., R. Cordoba-Rodriguez, C. S. Lankford & D. M. Frucht: Anthrax lethal toxin blocks MAPK kinasedependent IL-2 production in CD4+ T cells. J Immunol 174, 4966-71 (2005).
71. Bardwell, A. J., M. Abdollahi & L. Bardwell: Anthrax lethal factor-cleavage products of MAPK (mitogenactivated protein kinase) kinases exhibit reduced binding to their cognate MAPKs. Biochem J 378, 569-77 (2004). (Pubitemid 38367246)
72. Biondi, R. M. & A. R. Nebreda: Signalling specificity of Ser/Thr protein kinases through dockingsite- mediated interactions. Biochem J 372, 1-13 (2003). (Pubitemid 36609602)
73. Tanoue, T. & E. Nishida: Molecular recognitions in the MAP kinase cascades. Cell Signal 15, 455-62 (2003). (Pubitemid 36287667)
74. Dixon, T. C., M. Meselson, J. Guillemin & P. C. Hanna: Anthrax. N Engl J Med 341, 815-26 (1999).
75. Vitale, G., R. Pellizzari, C. Recchi, G. Napolitani, M. Mock & C. Montecucco: Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages. Biochem Biophys Res Commun 248, 706-11 (1998). (Pubitemid 28404486)
76. Montecucco, C., F. Tonello & G. Zanotti: Stop the killer: how to inhibit the anthrax lethal factor metalloprotease. Trends Biochem Sci 29, 282-5 (2004). (Pubitemid 38968757)
77. Chopra, A. P., S. A. Boone, X. Liang & N. S. Duesbery: Anthrax lethal factor proteolysis and inactivation of MAPK kinase. J Biol Chem 278, 9402-6 (2003). (Pubitemid 36800429)
78. During, R. L., B. G. Gibson, W. Li, E. A. Bishai, G. S. Sidhu, J. Landry & F. S. Southwick: Anthrax lethal toxin paralyzes actin-based motility by blocking Hsp27 phosphorylation. Embo J 26, 2240-50 (2007). (Pubitemid 46685867)
79. Friedlander, A. M.: Anthrax: clinical features, pathogenesis, and potential biological warfare threat. Curr Clin Top Infect Dis 20, 335-49 (2000).
80. Culley, N. C., D. M. Pinson, A. Chakrabarty, M. S. Mayo & S. M. Levine: Pathophysiological manifestations in mice exposed to anthrax lethal toxin. Infect Immun 73, 7006-10 (2005). (Pubitemid 41368870)
81. Clerk, A., T. E. Cullingford, S. J. Fuller, A. Giraldo, T. Markou, S. Pikkarainen & P. H. Sugden: Signaling pathways mediating cardiac myocyte gene expression in physiological and stress responses. J Cell Physiol 212, 311-22 (2007). (Pubitemid 47025620)
82. Heineke, J. & J. D. Molkentin: Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 7, 589-600 (2006). (Pubitemid 44325350)
83. Kerkela, R. & T. Force: p38 mitogen-activated protein kinase: a future target for heart failure therapy? J Am Coll Cardiol 48, 556-8 (2006).
84. Baines, C. P. & J. D. Molkentin: STRESS signaling pathways that modulate cardiac myocyte apoptosis. J Mol Cell Cardiol 38, 47-62 (2005). (Pubitemid 40038651)
85. Bueno, O. F. & J. D. Molkentin: Involvement of extracellular signal-regulated kinases 1/2 in cardiac hypertrophy and cell death. Circ Res 91, 776-81 (2002). (Pubitemid 35285074)
86. Purcell, N. H., B. J. Wilkins, A. York, M. K. Saba-El-Leil, S. Meloche, J. Robbins & J. D. Molkentin: Genetic inhibition of cardiac ERK1/2 promotes stress-induced apoptosis and heart failure but has no effect on hypertrophy in vivo. Proc Natl Acad Sci U S A 104, 14074-9 (2007). (Pubitemid 350003337)
87. Lips, D. J., O. F. Bueno, B. J. Wilkins, N. H. Purcell, R. A. Kaiser, J. N. Lorenz, L. Voisin, M. K. Saba-El-Leil, S. Meloche, J. Pouyssegur, G. Pages, L. J. De Windt, P. A. Doevendans & J. D. Molkentin: MEK1-ERK2 signaling pathway protects myocardium from ischemic injury in vivo. Circulation 109, 1938-41 (2004). (Pubitemid 38544482)
88. Harris, I. S., S. Zhang, I. Treskov, A. Kovacs, C. Weinheimer & A. J. Muslin: Raf-1 kinase is required for cardiac hypertrophy and cardiomyocyte survival in response to pressure overload. Circulation 110, 718-23 (2004). (Pubitemid 39056272)
89. Yamaguchi, O., T. Watanabe, K. Nishida, K. Kashiwase, Y. Higuchi, T. Takeda, S. Hikoso, S. Hirotani, M. Asahi, M. Taniike, A. Nakai, I. Tsujimoto, Y. Matsumura, J. Miyazaki, K. R. Chien, A. Matsuzawa, C. Sadamitsu, H. Ichijo, M. Baccarini, M. Hori & K. Otsu: Cardiac-specific disruption of the c-raf-1 gene induces cardiac dysfunction and apoptosis. J Clin Invest 114, 937- 43 (2004). (Pubitemid 39578721)
90. Liang, Q. & J. D. Molkentin: Redefining the roles of p38 and JNK signaling in cardiac hypertrophy: dichotomy between cultured myocytes and animal models. J Mol Cell Cardiol 35, 1385-94 (2003). (Pubitemid 37491181)
91. Lal, H., S. K. Verma, M. Smith, R. S. Guleria, G. Lu, D. M. Foster & D. E. Dostal: Stretch-induced MAP kinase activation in cardiac myocytes: differential regulation through beta1-integrin and focal adhesion kinase. J Mol Cell Cardiol 43, 137-47 (2007). (Pubitemid 47069384)
92. Braz, J. C., O. F. Bueno, Q. Liang, B. J. Wilkins, Y. S. Dai, S. Parsons, J. Braunwart, B. J. Glascock, R. Klevitsky, T. F. Kimball, T. E. Hewett & J. D. Molkentin: Targeted inhibition of p38 MAPK promotes hypertrophic cardiomyopathy through upregulation of calcineurin-NFAT signaling. J Clin Invest 111, 1475-86 (2003). (Pubitemid 38063280)
93. Sadoshima, J., O. Montagne, Q. Wang, G. Yang, J. Warden, J. Liu, G. Takagi, V. Karoor, C. Hong, G. L. Johnson, D. E. Vatner & S. F. Vatner: The MEKK1-JNK pathway plays a protective role in pressure overload but does not mediate cardiac hypertrophy. J Clin Invest 110, 271-9 (2002). (Pubitemid 34787364)
94. Tachibana, H., C. Perrino, H. Takaoka, R. J. Davis, S. V. Naga Prasad & H. A. Rockman: JNK1 is required to preserve cardiac function in the early response to pressure overload. Biochem Biophys Res Commun 343, 1060-6 (2006).
95. Liang, Q., O. F. Bueno, B. J. Wilkins, C. Y. Kuan, Y. Xia & J. D. Molkentin: c-Jun N-terminal kinases (JNK) antagonize cardiac growth through cross-talk with calcineurin-NFAT signaling. Embo J 22, 5079-89 (2003). (Pubitemid 37222028)
96. Duesbery, N. S. & G. F. Vande Woude: Anthrax toxins. Cell Mol Life Sci 55, 1599-609 (1999). (Pubitemid 29445825)
97. Hoover, D. L., A. M. Friedlander, L. C. Rogers, I. K. Yoon, R. L. Warren & A. S. Cross: Anthrax edema toxin differentially regulates lipopolysaccharide-induced monocyte production of tumor necrosis factor alpha and interleukin-6 by increasing intracellular cyclic AMP. Infect Immun 62, 4432-9 (1994). (Pubitemid 24301974)
98. O'Brien, J., A. Friedlander, T. Dreier, J. Ezzell & S. Leppla: Effects of anthrax toxin components on human neutrophils. Infect Immun 47, 306-10 (1985). (Pubitemid 15194628)
99. Crawford, M. A., C. V. Aylott, R. W. Bourdeau & G. M. Bokoch: Bacillus anthracis toxins inhibit human neutrophil NADPH oxidase activity. J Immunol 176, 7557- 65 (2006). (Pubitemid 43849059)
100. Tournier, J. N., A. Quesnel-Hellmann, J. Mathieu, C. Montecucco, W. J. Tang, M. Mock, D. R. Vidal & P. L. Goossens: Anthrax edema toxin cooperates with lethal toxin to impair cytokine secretion during infection of dendritic cells. J Immunol 174, 4934-41 (2005).
101. Tessier, J., C. Green, D. Padgett, W. Zhao, L. Schwartz, M. Hughes & E. Hewlett: Contributions of histamine, prostanoids, and neurokinins to edema elicited by edema toxin from Bacillus anthracis. Infect Immun 75, 1895-903 (2007). (Pubitemid 46559459)
102. Green, B. D., L. Battisti, T. M. Koehler, C. B. Thorne & B. E. Ivins: Demonstration of a capsule plasmid in Bacillus anthracis. Infect Immun 49, 291-7 (1985). (Pubitemid 15004855)
103. Klimpel, K. R., S. S. Molloy, G. Thomas & S. H. Leppla: Anthrax toxin protective antigen is activated by a cell surface protease with the sequence specificity and catalytic properties of furin. Proc Natl Acad Sci U S A 89, 10277-81 (1992).
104. Mock, M. & A. Fouet: Anthrax. Annu Rev Microbiol 55, 647-71 (2001). (Pubitemid 32978119)
105. Turnbull, P. C., M. G. Broster, J. A. Carman, R. J. Manchee & J. Melling: Development of antibodies to protective antigen and lethal factor components of anthrax toxin in humans and guinea pigs and their relevance to protective immunity. Infect Immun 52, 356-63 (1986). (Pubitemid 16117786)
106. Cote, C. K., C. A. Rossi, A. S. Kang, P. R. Morrow, J. S. Lee & S. L. Welkos: The detection of protective antigen (PA) associated with spores of Bacillus anthracis and the effects of anti-PA antibodies on spore germination and macrophage interactions. Microb Pathog 38, 209-25 (2005). (Pubitemid 40733551)
107. Welkos, S., A. Friedlander, S. Weeks, S. Little & I. Mendelson: In-vitro characterisation of the phagocytosis and fate of anthrax spores in macrophages and the effects of anti-PA antibody. J Med Microbiol 51, 821-31 (2002). (Pubitemid 35222782)
108. Welkos, S., S. Little, A. Friedlander, D. Fritz & P. Fellows: The role of antibodies to Bacillus anthracis and anthrax toxin components in inhibiting the early stages of infection by anthrax spores. Microbiology 147, 1677-85 (2001). (Pubitemid 32544833)
109. Muniz, A. E.: Lymphocytic vasculitis associated with the anthrax vaccine: case report and review of anthrax vaccination. J Emerg Med 25, 271-6 (2003). (Pubitemid 37324663)
110. Brey, R. N.: Molecular basis for improved anthrax vaccines. Adv Drug Deliv Rev 57, 1266-92 (2005). (Pubitemid 40796126)
111. Baillie, L.: The development of new vaccines against Bacillus anthracis. J Appl Microbiol 91, 609-13 (2001). (Pubitemid 32948383)
112. McBride, B. W., A. Mogg, J. L. Telfer, M. S. Lever, J. Miller, P. C. Turnbull & L. Baillie: Protective efficacy of a recombinant protective antigen against Bacillus anthracis challenge and assessment of immunological markers. Vaccine 16, 810-7 (1998). (Pubitemid 28236650)
113. Leppla, S. H., J. B. Robbins, R. Schneerson & J. Shiloach: Development of an improved vaccine for anthrax. J Clin Invest 110, 141-4 (2002). (Pubitemid 34787347)
114. Swartz, M. N.: Recognition and management of anthrax-an update. N Engl J Med 345, 1621-6 (2001).
115. Spencer, R. C.: Bacillus anthracis. J Clin Pathol 56, 182-7 (2003). (Pubitemid 36308031)
116. Gorse, G. J., W. Keitel, H. Keyserling, D. N. Taylor, M. Lock, K. Alves, J. Kenner, L. Deans & M. Gurwith: Immunogenicity and tolerance of ascending doses of a recombinant protective antigen (rPA102) anthrax vaccine: a randomized, double-blinded, controlled, multicenter trial. Vaccine 24, 5950-9 (2006). (Pubitemid 44080366)
117. Borio, L. L. & J. G. Bartlet: CBN Report: Safety and Immunogenicity of the Second Generation Anthrax Vaccine Candidate. Center for Biosecurity, Clinicians' Biosecurity network, University of Pittsburgh Medical Center (2006).
118. (HHS), U. S. D. o. H. H. S.: News Release: HHS Buys New Anthrax Vaccine for Stockpile. (2004).
119. Quinn, C. P., P. M. Dull, V. Semenova, H. Li, S. Crotty, T. H. Taylor, E. Steward-Clark, K. L. Stamey, D. S. Schmidt, K. W. Stinson, A. E. Freeman, C. M. Elie, S. K. Martin, C. Greene, R. D. Aubert, J. Glidewell, B. A. Perkins, R. Ahmed & D. S. Stephens: Immune responses to Bacillus anthracis protective antigen in patients with bioterrorism-related cutaneous or inhalation anthrax. J Infect Dis 190, 1228-36 (2004). (Pubitemid 39287748)
120. Stepanov, A. V., L. I. Marinin, A. P. Pomerantsev & N. A. Staritsin: Development of novel vaccines against anthrax in man. J Biotechnol 44, 155-60 (1996). (Pubitemid 26056574)
121. Casadevall, A.: Passive antibody administration (immediate immunity) as a specific defense against biological weapons. Emerg Infect Dis 8, 833-41 (2002).
122. Beedham, R. J., P. C. Turnbull & E. D. Williamson: Passive transfer of protection against Bacillus anthracis infection in a murine model. Vaccine 19, 4409-16 (2001). (Pubitemid 32718664)
123. Little, S. F., B. E. Ivins, P. F. Fellows & A. M. Friedlander: Passive protection by polyclonal antibodies against Bacillus a nthracis infection in guinea pigs. Infect Immun 65, 5171-5 (1997). (Pubitemid 27513566)
124. Henderson, D. W., S. Peacock & F. C. Belton: Observations on the prophylaxis of experimental pulmonary anthrax in the monkey. J Hyg (Lond) 54, 28-36 (1956).
125. Center, N. I. o. H. C.: Plasmapheresis of Anthrax- Vaccinated Subjects for Production of Anthrax Immune Globulin. ClinicalTrials.gov (2002).
126. Pittman, P. R., S. F. Leitman, J. G. Oro, S. L. Norris, N. M. Marano, M. V. Ranadive, B. S. Sink & K. T. McKee, Jr.: Protective antigen and toxin neutralization antibody patterns in anthrax vaccinees undergoing serial plasmapheresis. Clin Diagn Lab Immunol 12, 713-21 (2005). (Pubitemid 41175300)
127. Rainey, G. J. & J. A. Young: Antitoxins: novel strategies to target agents of bioterrorism. Nat Rev Microbiol 2, 721-6 (2004). (Pubitemid 39200063)
128. Dubois, C. M., F. Blanchette, M. H. Laprise, R. Leduc, F. Grondin & N. G. Seidah: Evidence that furin is an authentic transforming growth factor-beta1-converting enzyme. Am J Pathol 158, 305-16 (2001). (Pubitemid 32096497)
129. Peinado, J. R., M. M. Kacprzak, S. H. Leppla & I. Lindberg: Cross-inhibition between furin and lethal factor inhibitors. Biochem Biophys Res Commun 321, 601-5 (2004). (Pubitemid 39118382)
130. Tonello, F., M. Seveso, O. Marin, M. Mock & C. Montecucco: Screening inhibitors of anthrax lethal factor. Nature 418, 386 (2002). (Pubitemid 34826833)
131. Gujraty, K. V., A. Joshi, A. Saraph, V. Poon, J. Mogridge & R. S. Kane: Synthesis of polyvalent inhibitors of controlled molecular weight: structure-activity relationship for inhibitors of anthrax toxin. Biomacromolecules 7, 2082-5 (2006). (Pubitemid 44103346)
132. Scobie, H. M., D. Thomas, J. M. Marlett, G. Destito, D. J. Wigelsworth, R. J. Collier, J. A. Young & M. Manchester: A soluble receptor decoy protects rats against anthrax lethal toxin challenge. J Infect Dis 192, 1047-51 (2005). (Pubitemid 41266802)
133. Karginov, V. A., E. M. Nestorovich, M. Moayeri, S. H. Leppla & S. M. Bezrukov: Blocking anthrax lethal toxin at the protective antigen channel by using structure-inspired drug design. Proc Natl Acad Sci U S A 102, 15075-80 (2005). (Pubitemid 41513337)
134. Sanchez, A. M., D. Thomas, E. J. Gillespie, R. Damoiseaux, J. Rogers, J. P. Saxe, J. Huang, M. Manchester & K. A. Bradley: Amiodarone and bepridil inhibit anthrax toxin entry into host cells. Antimicrob Agents Chemother 51, 2403-11 (2007). (Pubitemid 47047317)
135. Xiong, Y., J. Wiltsie, A. Woods, J. Guo, J. V. Pivnichny, W. Tang, A. Bansal, R. T. Cummings, B. R. Cunningham, A. M. Friedlander, C. M. Douglas, S. P. Salowe, D. M. Zaller, E. M. Scolnick, D. M. Schmatz, K. Bartizal, J. D. Hermes, M. MacCoss & K. T. Chapman: The discovery of a potent and selective lethal factor inhibitor for adjunct therapy of anthrax infection. Bioorg Med Chem Lett 16, 964-8 (2006). (Pubitemid 43059861)
136. Dell'Aica, I., M. Dona, F. Tonello, A. Piris, M. Mock, C. Montecucco & S. Garbisa: Potent inhibitors of anthrax lethal factor from green tea. EMBO Rep 5, 418-22 (2004). (Pubitemid 38618286)
137. Numa, M. M., L. V. Lee, C. C. Hsu, K. E. Bower & C. H. Wong:
138. Cummings, R. T., S. P. Salowe, B. R. Cunningham, J. Wiltsie, Y. W. Park, L. M. Sonatore, D. Wisniewski, C. M. Douglas, J. D. Hermes & E. M. Scolnick: A peptide-based fluorescence resonance energy transfer assay for Bacillus anthracis lethal factor protease. Proc Natl Acad Sci U S A 99, 6603-6 (2002). (Pubitemid 34526179)
139. Gupta, M., S. Alam & R. Bhatnagar: Catalytically inactive anthrax toxin (s) are potential prophylactic agents. Vaccine 25, 8410-9 (2007). (Pubitemid 350137601)
140. Abergel, R. J., M. K. Wilson, J. E. Arceneaux, T. M. Hoette, R. K. Strong, B. R. Byers & K. N. Raymond: Anthrax pathogen evades the mammalian immune system through stealth siderophore production. Proc Natl Acad Sci U S A 103, 18499-503 (2006). (Pubitemid 44913439)
141. Petosa, C., R. J. Collier, K. R. Klimpel, S. H. Leppla & R. C. Liddington: Crystal structure of the anthrax toxin protective antigen. Nature 385, 833-8 (1997). (Pubitemid 27106075)