Anthrax Lethal Toxin Downregulates Claudin-5 Expression in Human Endothelial Tight Junctions

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  D'Agnillo, Felice ^a   Williams, Matthew C ^a   Moayeri, Mahtab ^b   Warfel, Jason M ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ANTHRAX TOXIN; CLAUDIN 5; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; OCCLUDIN; PROTEASOME; PROTEIN ZO1; PROTEIN ZO2; VASCULAR ENDOTHELIAL CADHERIN; BACTERIAL ANTIGEN; BACTERIAL TOXIN; CADHERIN; LEUKOCYTE ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTHRAX; ARTICLE; CELL ADHESION; CELL COMPONENT; CELL DEATH; CELL JUNCTION; CELL STRUCTURE; CLDN5 GENE; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; ELECTRIC RESISTANCE; ENZYME INACTIVATION; ENZYME INHIBITION; FEMALE; GAPDH GENE; HUMAN; HUMAN CELL; LYSOSOME; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STRESS FIBER; TIGHT JUNCTION; TRANSENDOTHELIAL ELECTRIC RESISTANCE; ANIMAL; DRUG EFFECTS; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; LIVER; METABOLISM; VASCULAR ENDOTHELIUM;

MUS;

ANIMALS; ANTIGENS, BACTERIAL; ANTIGENS, CD; BACTERIAL TOXINS; CADHERINS; CELL DEATH; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FEMALE; GENE EXPRESSION REGULATION; LIVER; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; PROTEOLYSIS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS;

EID: 84876518622     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062576     Document Type: Article

References (56)

1. Moayeri M, Leppla S, (2009) Cellular and systemic effects of anthrax lethal toxin and edema toxin. Mol Aspects Med 30: 439-455.
2. van der Goot G, Young JA, (2009) Receptors of anthrax toxin and cell entry. Mol Aspects Med 30: 406-412.
3. Liu S, Crown D, Miller-Randolph S, Moayeri M, Wang H, et al. (2009) Capillary morphogenesis protein-2 is the major receptor mediating lethality of anthrax toxin in vivo. Proc Natl Acad Sci USA 106: 12424-12429.
4. Liu S, Zhang Y, Hoover B, Leppla SH, (2012) The receptors that mediate the direct lethality of anthrax toxin. Toxins (Basel) 5: 1-8.
5. Leppla S, (1982) Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc Natl Acad Sci USA 79: 3162-3166.
6. Walsh J, Pesik N, Quinn C, Urdaneta V, Dykewicz C, et al. (2007) A case of naturally acquired inhalation anthrax: clinical care and analyses of anti-protective antigen immunoglobulin G and lethal factor. Clin Infect Dis 44: 968-971.
7. Shoop W, Xiong Y, Wiltsie J, Woods A, Guo J, et al. (2005) Anthrax lethal factor inhibition. Proc Natl Acad Sci USA 102: 7958-7963.
8. Molin F, Fasanella A, Simonato M, Garofolo G, Montecucco C, et al. (2008) Ratio of lethal and edema factors in rabbit systemic anthrax. Toxicon 52: 824-828.
9. Grinberg L, Abramova F, Yampolskaya O, Walker D, Smith J, (2001) Quantitative pathology of inhalational anthrax I: quantitative microscopic findings. Mod Pathol 14: 482-495.
10. Stearns-Kurosawa D, Lupu F, Taylor FJ, Kinasewitz G, Kurosawa S, (2006) Sepsis and pathophysiology of anthrax in a nonhuman primate model. Am J Pathol 169: 433-444.
11. Guarner J, Jernigan J, Shieh W, Tatti K, Flannagan L, et al. (2003) Pathology and pathogenesis of bioterrorism-related inhalational anthrax. Am J Pathol 163: 701-709.
12. Twenhafel NA, (2010) Pathology of inhalational anthrax animal models. Vet Pathol 47: 819-830.
13. Moayeri M, Haines D, Young H, Leppla S, (2003) Bacillus anthracis lethal toxin induces TNF-alpha-independent hypoxia-mediated toxicity in mice. J Clin Invest 112: 670-682.
14. Kuo S, Willingham M, Bour S, Andreas E, Park S, et al. (2008) Anthrax toxin-induced shock in rats is associated with pulmonary edema and hemorrhage. Microb Pathog 44: 467-472.
15. Moayeri M, Crown D, Dorward D, Gardner D, Ward J, et al. (2009) The heart is an early target of anthrax lethal toxin in mice: a protective role for neuronal nitric oxide synthase (nNOS). PLoS Pathog 5: e1000456.
16. Bolcome Rr, Sullivan S, Zeller R, Barker A, Collier R, et al. (2008) Anthrax lethal toxin induces cell death-independent permeability in zebrafish vasculature. Proc Natl Acad Sci USA 105: 2439-2444.
17. Bolcome RE 3rd, Chan J (2010) Constitutive MEK1 activation rescues anthrax lethal toxin-induced vascular effects in vivo. Infect Immun 78: 5043-5053.
18. Ghosh CC, Mukherjee A, David S, Knaus UG, Stearns-Kurosawa DJ, et al. (2012) Impaired function of the Tie-2 receptor contributes to vascular leakage and lethality in anthrax. Proc Natl Acad Sci USA 109: 10024-10029.
19. Deshpande A, Hammon R, Sanders C, Graves S, (2006) Quantitative analysis of the effect of cell type and cellular differentiation on protective antigen binding to human target cells. FEBS Lett 580: 4172-4175.
20. Dejana E, Giampietro C, (2012) Vascular endothelial-cadherin and vascular stability. Curr Opin Hematol 19: 218-223.
21. Bazzoni G, Dejana E, (2004) Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 84: 869-901.
22. Vandenbroucke E, Mehta D, Minshall R, Malik A, (2008) Regulation of endothelial junctional permeability. Ann N Y Acad Sci 1123: 134-145.
23. Bogatcheva N, Verin A, (2008) The role of cytoskeleton in the regulation of vascular endothelial barrier function. Microvasc Res 76: 202-207.
24. Warfel J, Steele A, D'Agnillo F, (2005) Anthrax lethal toxin induces endothelial barrier dysfunction. Am J Pathol 166: 1871-1881.
25. Warfel JM, D'Agnillo F, (2011) Anthrax Lethal Toxin-Mediated Disruption of Endothelial VE-Cadherin Is Attenuated by Inhibition of the Rho-Associated Kinase Pathway. Toxins (Basel) 3: 1278-1293.
26. Park S, Leppla S, (2000) Optimized production and purification of Bacillus anthracis lethal factor. Protein Expr Purif 18: 293-302.
27. Ramirez D, Leppla S, Schneerson R, Shiloach J, (2002) Production, recovery and immunogenicity of the protective antigen from a recombinant strain of Bacillus anthracis. J Ind Microbiol Biotechnol 28: 232-238.
28. Livak K, Schmittgen T, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
29. Mandel I, Paperna T, Volkowich A, Merhav M, Glass-Marmor L, et al. (2012) The ubiquitin-proteasome pathway regulates claudin 5 degradation. J Cell Biochem 113: 2415-2423.
30. Takahashi S, Iwamoto N, Sasaki H, Ohashi M, Oda Y, et al. (2009) The E3 ubiquitin ligase LNX1p80 promotes the removal of claudins from tight junctions in MDCK cells. J Cell Sci 122: 985-994.
31. Armstrong SM, Wang C, Tigdi J, Si X, Dumpit C, et al. (2012) Influenza infects lung microvascular endothelium leading to microvascular leak: role of apoptosis and claudin-5. PLoS One 7: e47323.
32. Warfel JM, D'Agnillo F, (2009) Anthrax lethal toxin enhances IkappaB kinase activation and differentially regulates pro-inflammatory genes in human endothelium. J Biol Chem 284: 25761-25771.
33. Bogyo M, Verhelst S, Bellingard-Dubouchaud V, Toba S, Greenbaum D, (2000) Selective targeting of lysosomal cysteine proteases with radiolabeled electrophilic substrate analogs. Chem Biol 7: 27-38.
34. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E, (2005) Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1: 84-91.
35. Rolando M, Munro P, Stefani C, Auberger P, Flatau G, et al. (2009) Injection of Staphylococcus aureus EDIN by the Bacillus anthracis protective antigen machinery induces vascular permeability. Infect Immun 77: 3596-3601.
36. Culley NC, Pinson DM, Chakrabarty A, Mayo MS, LeVine SM, (2005) Pathophysiological manifestations in mice exposed to anthrax lethal toxin. Infect Immun 73: 7006-7010.
37. Trescos Y, Tournier JN, (2012) Cytoskeleton as an emerging target of anthrax toxins. Toxins (Basel) 4: 83-97.
38. Yamamoto M, Ramirez SH, Sato S, Kiyota T, Cerny RL, et al. (2008) Phosphorylation of claudin-5 and occludin by rho kinase in brain endothelial cells. Am J Pathol 172: 521-533.
39. Chalmers AD, Whitley P, (2012) Continuous endocytic recycling of tight junction proteins: how and why? Essays Biochem 53: 41-54.
40. Batty S, Chow EM, Kassam A, Der SD, Mogridge J, (2006) Inhibition of mitogen-activated protein kinase signalling by Bacillus anthracis lethal toxin causes destabilization of interleukin-8 mRNA. Cell Microbiol 8: 130-138.
41. Warfel JM, D'Agnillo F, (2008) Anthrax lethal toxin enhances TNF-induced endothelial VCAM-1 expression via an IFN regulatory factor-1-dependent mechanism. J Immunol 180: 7516-7524.
42. Fontijn RD, Volger OL, Fledderus JO, Reijerkerk A, de Vries HE, et al. (2008) SOX-18 controls endothelial-specific claudin-5 gene expression and barrier function. Am J Physiol Heart Circ Physiol 294: H891-900.
43. Aslam M, Ahmad N, Srivastava R, Hemmer B, (2012) TNF-alpha induced NFκB signaling and p65 (RelA) overexpression repress Cldn5 promoter in mouse brain endothelial cells. Cytokine 57: 269-275.
44. Koto T, Takubo K, Ishida S, Shinoda H, Inoue M, et al. (2007) Hypoxia disrupts the barrier function of neural blood vessels through changes in the expression of claudin-5 in endothelial cells. Am J Pathol 170: 1389-1397.
45. Taddei A, Giampietro C, Conti A, Orsenigo F, Breviario F, et al. (2008) Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat Cell Biol 10: 923-934.
46. Yuan L, Le Bras A, Sacharidou A, Itagaki K, Zhan Y, et al. (2012) ETS-related gene (ERG) controls endothelial cell permeability via transcriptional regulation of the claudin 5 (CLDN5) gene. J Biol Chem 287: 6582-6591.
47. Dryden NH, Sperone A, Martin-Almedina S, Hannah RL, Birdsey GM, et al. (2012) The transcription factor Erg controls endothelial cell quiescence by repressing activity of nuclear factor (NF)-κB p65. J Biol Chem 287: 12331-12342.
48. Birdsey GM, Dryden NH, Shah AV, Hannah R, Hall MD, et al. (2012) The transcription factor Erg regulates expression of histone deacetylase 6 and multiple pathways involved in endothelial cell migration and angiogenesis. Blood 119: 894-903.
49. Wasylyk B, Hagman J, Gutierrez-Hartmann A, (1998) Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem Sci 23: 213-216.
50. Hollenhorst PC, (2012) RAS/ERK pathway transcriptional regulation through ETS/AP-1 binding sites. Small GTPases 3: 154-158.
51. Sharrocks AD, (2001) The ETS-domain transcription factor family. Nat Rev Mol Cell Biol 2: 827-837.
52. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, et al. (2003) Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 161: 653-660.
53. Ebrahimi CM, Sheen TR, Renken CW, Gottlieb RA, Doran KS, (2011) Contribution of lethal toxin and edema toxin to the pathogenesis of anthrax meningitis. Infect Immun 79: 2510-2518.
54. Mukherjee DV, Tonry JH, Kim KS, Ramarao N, Popova TG, et al. (2011) Bacillus anthracis protease InhA increases blood-brain barrier permeability and contributes to cerebral hemorrhages. PLoS One 6: e17921.
55. Firoved AM, Miller GF, Moayeri M, Kakkar R, Shen Y, et al. (2005) Bacillus anthracis edema toxin causes extensive tissue lesions and rapid lethality in mice. Am J Pathol 167: 1309-1320.
56. Guichard A, McGillivray SM, Cruz-Moreno B, van Sorge NM, Nizet V, et al. (2010) Anthrax toxins cooperatively inhibit endocytic recycling by the Rab11/Sec15 exocyst. Nature 467: 854-858.