Anthrax lethal toxin induces acute diastolic dysfunction in rats through disruption of the phospholamban signaling network

International Journal of Cardiology

Volumn 168, Issue 4, 2013, Pages 3884-3895

  Golden, Honey B ^b   Watson, Linley E ^c   Nizamutdinov, Damir ^b   Feng, Hao ^b   Gerilechaogetu, Fnu ^b   Lal, Hind ^d   Verma, Suresh K ^e   Mukhopadhyay, Swagoto ^b   Foster, Donald M ^a   Dillmann, Wolfgang H ^f   Dostal, David E ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b TEXAS A AND M UNIVERSITY SYSTEM   (United States)

^c SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

^d TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Akt; Anthrax lethal toxin; Diastolic dysfunction; JNK1 2; Phospholamban

Indexed keywords

ANTHRAX TOXIN; CALCIUM ION; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; PHOSPHOLAMBAN; PHOSPHOPROTEIN PHOSPHATASE 2A; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; THREONINE; BACTERIAL ANTIGEN; BACTERIAL TOXIN; CALCIUM BINDING PROTEIN;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL PROTECTION; COMPLEX FORMATION; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; DIASTOLIC HEART FAILURE; ECHOCARDIOGRAPHY; ENZYME ACTIVATION; GAIN OF FUNCTION MUTATION; HEART ATRIUM ENLARGEMENT; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; IMMUNOPRECIPITATION; LOSS OF FUNCTION MUTATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; PULMONARY VALVE INSUFFICIENCY; RAT; SARCOPLASMIC RETICULUM; SIGNAL TRANSDUCTION; ACUTE DISEASE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CHEMICALLY INDUCED; DRUG EFFECTS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TOXICITY;

ACUTE DISEASE; ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; HEART FAILURE, DIASTOLIC; MALE; MYOCYTES, CARDIAC; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 84886234937     PISSN: 01675273     EISSN: 18741754     Source Type: Journal    
DOI: 10.1016/j.ijcard.2013.06.050     Document Type: Article

References (44)

1. L. Borio, D. Frank, and V. Mani Death due to bioterrorism-related inhalational anthrax: report of 2 patients JAMA 286 2001 2554 2559
2. B. Mina, J.P. Dym, and F. Kuepper Fatal inhalational anthrax with unknown source of exposure in a 61-year-old woman in New York City JAMA 287 2002 858 862
3. M. Moayeri, D. Haines, H.A. Young, and S.H. Leppla Bacillus anthracis lethal toxin induces TNF-alpha-independent hypoxia-mediated toxicity in mice J Clin Invest 112 2003 670 682
4. L.E. Watson, S.R. Kuo, and K. Katki Anthrax toxins induce shock in rats by depressed cardiac ventricular function PLoS One 2 2007 e466
5. L.E. Watson, J. Mock, and H. Lal Lethal and edema toxins of anthrax induce distinct hemodynamic dysfunction Front Biosci 12 2007 4670 4675
6. N.S. Duesbery, C.P. Webb, and S.H. Leppla Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor Science 280 1998 734 737
7. G. Vitale, L. Bernardi, and G. Napolitani Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor Biochem J 352 Pt 3 2000 739 745
8. A.J. Bardwell, M. Abdollahi, and L. Bardwell Anthrax lethal factor-cleavage products of MAPK (mitogen-activated protein kinase) kinases exhibit reduced binding to their cognate MAPKs Biochem J 378 2004 569 577
9. L.E. Watson, M. Sheth, R.F. Denyer, and D.E. Dostal Baseline echocardiographic values for adult male rats J Am Soc Echocardiogr 17 2004 161 167
10. H.B. Golden, D. Gollapudi, and F. Gerilechaogetu Isolation of cardiac myocytes and fibroblasts from neonatal rat pups Methods Mol Biol 843 2012 205 214
11. H. Lal, S.K. Verma, and M. Smith Stretch-induced MAP kinase activation in cardiac myocytes: differential regulation through beta1-integrin and focal adhesion kinase J Mol Cell Cardiol 43 2007 137 147
12. H. Lal, S.K. Verma, and H.B. Golden Stretch-induced regulation of angiotensinogen gene expression in cardiac myocytes and fibroblasts: opposing roles of JNK1/2 and p38alpha MAP kinases J Mol Cell Cardiol 45 2008 770 778
13. S.W. Burchiel, B.S. Edwards, and F.W. Kuckuck Analysis of free intracellular calcium by flow cytometry: multiparameter and pharmacologic applications Methods 21 2000 221 230
14. M. Moayeri, D. Crown, and D.W. Dorward The heart is an early target of anthrax lethal toxin in mice: a protective role for neuronal nitric oxide synthase (nNOS) PLoS Pathog 5 2009 e1000456
15. G. Vitale, R. Pellizzari, and C. Recchi Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages Biochem Biophys Res Commun 248 1998 706 711
16. D. Marion Crush-related acute kidney injury (acute renal failure) D. Basow, UpToDate 2010 UpToDate Waltham, MA
17. D. Marion Tests of the liver's biosynthetic capacity D. Basow, UpToDate 2010 UpToDate Waltham, MA
18. B.E. Turk, T.Y. Wong, and R. Schwarzenbacher The structural basis for substrate and inhibitor selectivity of the anthrax lethal factor Nat Struct Mol Biol 11 2004 60 66
19. A. Cittadini, M.G. Monti, and G. Iaccarino Adenoviral gene transfer of Akt enhances myocardial contractility and intracellular calcium handling Gene Ther 13 2006 8 19
20. M. Rota, A. Boni, and K. Urbanek Nuclear targeting of Akt enhances ventricular function and myocyte contractility Circ Res 97 2005 1332 1341
21. N. Bhasin, S.R. Cunha, and M. Mudannayake Molecular basis for PP2A regulatory subunit B56alpha targeting in cardiomyocytes Am J Physiol 293 2007 H109 H119
22. A. El-Armouche, A. Bednorz, and T. Pamminger Role of calcineurin and protein phosphatase-2A in the regulation of phosphatase inhibitor-1 in cardiac myocytes Biochem Biophys Res Commun 346 2006 700 706
23. V. De Arcangelis, D. Soto, and Y. Xiang Phosphodiesterase 4 and phosphatase 2A differentially regulate cAMP/protein kinase a signaling for cardiac myocyte contraction under stimulation of beta1 adrenergic receptor Mol Pharmacol 74 2008 1453 1462
24. N.D. Glaser, Y.O. Lukyanenko, and Y. Wang JNK activation decreases PP2A regulatory subunit B56alpha expression and mRNA stability and increases AUF1 expression in cardiomyocytes Am J Physiol 291 2006 H1183 H1192
25. 2 + cycling by direct phosphorylation of phospholamban at Thr17 J Biol Chem 284 2009 28180 28187
26. W. Haeusgen, T. Herdegen, and V. Waetzig The bottleneck of JNK signaling: molecular and functional characteristics of MKK4 and MKK7 Eur J Cell Biol 90 2011 536 544
27. T. Popova, V. Espina, and C. Bailey Anthrax infection inhibits the AKT signaling involved in the E-cadherin-mediated adhesion of lung epithelial cells FEMS Immunol Med Microbiol 56 2009 129 142
28. J.M. Warfel, A.D. Steele, and F. D'Agnillo Anthrax lethal toxin induces endothelial barrier dysfunction Am J Pathol 166 2005 1871 1881
29. J.M. Park, F.R. Greten, Z.W. Li, and M. Karin Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition Science 297 2002 2048 2051
30. L. Xu, H. Fang, and D.M. Frucht Anthrax lethal toxin increases superoxide production in murine neutrophils via differential effects on MAPK signaling pathways J Immunol 180 2008 4139 4147
31. J.E. Comer, A.K. Chopra, J.W. Peterson, and R. Konig Direct inhibition of T-lymphocyte activation by anthrax toxins in vivo Infect Immun 73 2005 8275 8281
32. Q. Liang, and 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 2003 1385 1394
33. X. Cui, Y. Li, and X. Li 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 2007 572 580
34. C.W. Hicks, Y. Li, and S. Okugawa Anthrax edema toxin has cAMP-mediated stimulatory effects and high-dose lethal toxin has depressant effects in an isolated perfused rat heart model Am J Physiol 300 2011 H1108 H1118
35. W.S. Lawrence, J.R. Marshall, and D.L. Zavala Hemodynamic effects of anthrax toxins in the rabbit model and the cardiac pathology induced by lethal toxin Toxins (Basel) 3 2011 721 736
36. D.A. Sweeney, X. Cui, and S.B. Solomon Anthrax lethal and edema toxins produce different patterns of cardiovascular and renal dysfunction and synergistically decrease survival in canines J Infect Dis 202 2010 1885 1896
37. M.B. Jones, R. Jani, and D. Ren Inhibition of Bacillus anthracis growth and virulence-gene expression by inhibitors of quorum-sensing J Infect Dis 191 2005 1881 1888
38. M. Moayeri, and S.H. Leppla Cellular and systemic effects of anthrax lethal toxin and edema toxin Mol Aspects Med 30 2009 439 455
39. A.M. Firoved, G.F. Miller, and M. Moayeri Bacillus anthracis edema toxin causes extensive tissue lesions and rapid lethality in mice Am J Pathol 167 2005 1309 1320
40. I. Falcao-Pires, N. Hamdani, and A. Borbely Diabetes mellitus worsens diastolic left ventricular dysfunction in aortic stenosis through altered myocardial structure and cardiomyocyte stiffness Circulation 124 2011 1151 1159
41. I. Falcao-Pires, G. Palladini, and N. Goncalves Distinct mechanisms for diastolic dysfunction in diabetes mellitus and chronic pressure-overload Basic Res Cardiol 106 2011 801 814
42. M. Marshall, N. Anilkumar, and J. Layland Protein phosphatase 2A contributes to the cardiac dysfunction induced by endotoxemia Cardiovasc Res 82 2009 67 76
43. K.O. Larsen, B. Lygren, and I. Sjaastad Diastolic dysfunction in alveolar hypoxia: a role for interleukin-18-mediated increase in protein phosphatase 2A Cardiovasc Res 80 2008 47 54
44. D. Rittirsch, M.A. Flierl, and P.A. Ward Harmful molecular mechanisms in sepsis Nat Rev Immunol 8 2008 776 787