Anthrax lethal and edema toxins produce different patterns of cardiovascular and renal dysfunction and synergistically decrease survival in canines

Journal of Infectious Diseases

Volumn 202, Issue 12, 2010, Pages 1885-1896

  Sweeney, Daniel A ^a   Cui, Xizhong ^a   Solomon, Steven B ^a   Vitberg, David A ^a   Migone, Thi S ^b   Scher, Dara ^a   Danner, Robert L ^a   Natanson, Charles ^a   Subramanian, G Mani ^b   Eichacker, Peter Q ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOTRANSFERASE; ANTHRAX TOXIN; CREATININE; SODIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARDIOVASCULAR DISEASE; CENTRAL VENOUS PRESSURE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DIURESIS; DOG; HEART EJECTION FRACTION; HEART INDEX; HEART RATE; KIDNEY DYSFUNCTION; NONHUMAN; PRIORITY JOURNAL; SODIUM BLOOD LEVEL; SURVIVAL; SYSTEMIC VASCULAR RESISTANCE; UREA NITROGEN BLOOD LEVEL;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; BLOOD PRESSURE; CARDIOVASCULAR SYSTEM; CREATININE; DISEASE MODELS, ANIMAL; DOGS; HEART RATE; KIDNEY; POISONING; SURVIVAL ANALYSIS; TRANSAMINASES; UREA; VASCULAR RESISTANCE;

EID: 78650395903     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/657408     Document Type: Article

References (46)

1. Barakat LA, Quentzel HL, Jernigan JA, et al. Fatal inhalational anthrax in a 94-year-old Connecticut woman. JAMA 2002; 287:863-868.
2. Jernigan JA, Stephens DS, Ashford DA, et al. Bioterrorism-related inhalational anthrax: the first 10 cases reported in the United States. Emerg Infect Dis 2001; 7:933-944.
3. Health Protection Scotland. Anthrax outbreak information. http://www.hps.scot.nhs.uk/anthrax/. Accessed 22 February 2010.
4. BBC News. German death linked to Scots anthrax outbreak. http://news.bbc.co.uk/2/hi/uk-news/scotland/glasgow-and-west/8500848.stm. Accessed 22 February 2010.
5. Collier RJ, Young JA. Anthrax toxin. Annu Rev Cell Dev Biol 2003; 19:45-70.
6. Sherer K, Li Y, Cui X, Eichacker PQ. Lethal and edema toxins in the pathogenesis of Bacillus anthracis septic shock: implications for therapy. Am J Respir Crit Care Med 2007; 175:211-221.
7. Moayeri M, Crown D, Dorward DW, et al. The heart is an early target of anthrax lethal toxin in mice: a protective role for neuronal nitric oxide synthase (nNOS). PLoS Pathog 2009; 5:e1000456.
8. Watson LE, Kuo SR, Katki K, et al. Anthrax toxins induce shock in rats by depressed cardiac ventricular function. PLoS One 2007; 2:e466.
9. Watson LE, Mock J, Lal H, et al. Lethal and edema toxins of anthrax induce distinct hemodynamic dysfunction. Front Biosci 2007; 12:4670-4675.
10. McGee ED, Fritz DL, Ezzell JW, Newcomb HL, Brown RJ, Jaax NK. Anthrax in a dog. Vet Pathol 1994; 31:471-473.
11. Dixon WJ. The up-and-down method for small samples. J Am Stat Assoc 1965; 60:967-978.
12. Minneci PC, Deans KJ, Hansen B, et al. A canine model of septic shock: balancing animal welfare and scientific relevance. Am J Physiol Heart Circ Physiol 2007; 293:H2487-H2500.
13. Cooksey BA, Sampey GC, Pierre JL, et al. Production of biologically active Bacillus anthracis edema factor in Escherichia coli. Biotechnol Prog 2004; 20:1651-1659.
14. Gwinn W, Zhang M, Mon S, et al. Scalable purification of Bacillus anthracis protective antigen from Escherichia coli. Protein Expr Purif 2006; 45:30-36.
15. Laird MW, Zukauskas D, Johnson K, et al. Production and purification of Bacillus anthracis protective antigen from Escherichia coli. Protein Expr Purif 2004; 38:145-152.
16. Cui X, Li Y, Li X, et al. 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 2007; 195:572-580.
17. 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-R709.
18. Lichtman AH. The up-and-down method substantially reduces the number of animals required to determine antinociceptive ED50 values. J Pharmacol Toxicol Methods 1998; 40:81-85.
19. Stanley JL, Smith H. Purification of factor I and recognition of a third factor of the anthrax toxin. J Gen Microbiol 1961; 26:49-63.
20. Bonuccelli G, Sotgia F, Frank PG, et al. 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 2005; 288:C1402-C1410.
21. Young JA, Collier RJ. Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu Rev Biochem 2007; 76:243-265.
22. Stehlik J, Movsesian MA. Inhibitors of cyclic nucleotide phosphodiesterase 3 and 5 as therapeutic agents in heart failure. Expert Opin Investig Drugs 2006; 15:733-742.
23. Benoit JN, Taylor MS. Vascular reactivity following ischemia/reperfusion. Front Biosci 1997; 2:e28-e33.
24. Griffith TM, Taylor HJ. Cyclic AMP mediates EDHF-type relaxations of rabbit jugular vein. Biochem Biophys Res Commun 1999; 263:52-57.
25. Borer JS. Drug insight: if inhibitors as specific heart-rate-reducing agents. Nat Clin Pract Cardiovasc Med 2004; 1:103-109.
26. Katz AM. Physiology of the heart. Philadelphia, PA: Lippincott Williams & Wilkins, 2001:255-286.
27. Friedler RM, Kurokawa K, Coburn JW, Massry SG. Renal action of cholera toxin. I. Effects on urinary excretion of electrolytes and cyclic AMP. Kidney Int 1975; 7:77-85.
28. Kurokawa K, Friedler RM, Massry SG. Renal action of cholera toxin. II. Effects on adenylate cyclase-cyclic AMP system. Kidney Int 1975; 7:137-144.
29. Pierce NF, Graybill JR, Kaplan MM, Bouwman DL. Systemic effects of parenteral cholera enterotoxin in dogs. J Lab Clin Med 1972; 79: 145-156.
30. Firoved AM, Miller GF, Moayeri M, et al. Bacillus anthracis edema toxin causes extensive tissue lesions and rapid lethality in mice. Am J Pathol 2005; 167:1309-1320.
31. Dadachova E, Rivera J, Revskaya E, et al. In vitro evaluation, biodistribution and scintigraphic imaging in mice of radiolabeled anthrax toxins. Nucl Med Biol 2008; 35:755-761.
32. Kim S, BakreM, Yin H, Varner JA. Inhibition of endothelial cell survival and angiogenesis by protein kinase A. J Clin Invest 2002; 110:933-941.
33. Turk BE. Manipulation of host signalling pathways by anthrax toxins. Biochem J 2007; 402:405-417.
34. Xu L, Frucht DM. Bacillus anthracis: a multi-faceted role for anthrax lethal toxin in thwarting host immune defenses. Int J Biochem Cell Biol 2007; 39:20-24.
35. Kirby JE. Anthrax lethal toxin induces human endothelial cell apoptosis. Infect Immun 2004; 72:430-439.
36. Warfel JM, Steele AD, D'Agnillo F. Anthrax lethal toxin induces endothelial barrier dysfunction. Am J Pathol 2005; 166:1871-1881.
37. Horowitz A, Menice CB, Laporte R, Morgan KG. Mechanisms of smooth muscle contraction. Physiol Rev 1996; 76:967-1003.
38. Yamaguchi O,Watanabe T, Nishida K, et al. Cardiac-specific disruption of the c-raf-1 gene induces cardiac dysfunction and apoptosis. J Clin Invest 2004; 114:937-943.
39. Purcell NH, Wilkins BJ, York A, et al. 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 2007; 104: 14074-14079.
40. Lips DJ, Bueno OF, Wilkins BJ, et al. MEK1-ERK2 signaling pathway protects myocardium from ischemic injury in vivo. Circulation 2004; 109:1938-1941.
41. Li Y, Cui X, Su J, et al. Norepinephrine increases blood pressure but not survival with anthrax lethal toxin in rats. Crit Care Med 2009; 37: 1348-1354.
42. 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; 36:148-156.
43. Molin FD, Fasanella A, Simonato M, Garofolo G, Montecucco C, Tonello F. Ratio of lethal and edema factors in rabbit systemic anthrax. Toxicon 2008; 52:824-828.
44. Health Protection Scotland. Anthrax outbreak information: clinical guidelines for use of anthrax immune globulin intravenous (human) (AIGIV) in Scotland. http://www.hps.scot.nhs.uk/anthrax/documents/clinical-guidance-for- use-of-anthrax-immune-globulin-v12-1-2010-03-19.pdf. Accessed 27 October 2010.
45. McDaniel NL, Rembold CM, Richard HM, Murphy RA. Cyclic AMP relaxes swine arterial smooth muscle predominantly by decreasing cell Ca2+ concentration. J Physiol 1991; 439:147-160.
46. Taylor MS, Benoit JN. Effect of milrinone on small mesenteric artery vasoconstriction: role of K(+) channels. Am J Physiol 1999; 277:G69-G78.