Perturbation of mouse retinal vascular morphogenesis by anthrax lethal toxin

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Bromberg White, Jennifer L ^a   Boguslawski, Elissa ^a   Duesbery, Nicholas S ^a  

^a VAN ANDEL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; BASIC FIBROBLAST GROWTH FACTOR; EPIDERMAL GROWTH FACTOR; GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; VASCULOTROPIN; BACTERIAL ANTIGEN; BACTERIAL TOXIN; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; GROWTH RETARDATION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; RETINA BLOOD VESSEL; RETINA CELL; RETINA DEVELOPMENT; RETINA NEOVASCULARIZATION; SIGNAL TRANSDUCTION; VITREOUS BODY; ANIMAL; ANTHRAX; C57BL MOUSE; DRUG EFFECT; FLUORESCENCE MICROSCOPY; METABOLISM; MORPHOGENESIS; PATHOPHYSIOLOGY; RETINA; TIME;

MURINAE;

ANIMALS; ANTHRAX; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; IMMUNOBLOTTING; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; MORPHOGENESIS; NEOVASCULARIZATION, PHYSIOLOGIC; RETINA; RETINAL VESSELS; SIGNAL TRANSDUCTION; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 70349193385     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006956     Document Type: Article

References (52)

1. Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR, et al. (1998) Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280: 734-737.
2. Singh Y, Leppla SH, Bhatnagar R, Friedlander AM (1989) Internalization and processing of Bacillus anthracis lethal toxin by toxin-sensitive and -resistant cells. J Biol Chem 264: 11099-11102.
3. Vitale G, Pellizzari R, Recchi C, Napolitani G, Mock M, et al. (1998) Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages. Biochem Biophys Res Commun 248: 706-711.
4. Pellizzari R, Guidi-Rontani C, Vitale G, Mock M, Montecucco C (1999) Anthrax lethal factor cleaves MKK3 in macrophages and inhibits the LPS/ IFN gamma-induced release of NO and TNFalpha. FEBS Lett 462: 199-204.
5. Vitale G, Bernardi L, Napolitani G, Mock M, Montecucco C (2000) Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor. Biochem J 352 Pt 3: 739-745.
6. Chopra AP, Boone SA, Liang X, Duesbery NS (2003) Anthrax lethal factor proteolysis and inactivation of MAPK kinase. J Biol Chem 278: 9402-9406.
7. Bardwell AJ, Abdollahi M, Bardwell L (2004) Anthrax lethal factor-cleavage products of MAPK (mitogen-activated protein kinase) kinases exhibit reduced binding to their cognate MAPKs. Biochem J 378: 569-577.
8. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, et al. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22: 153-183.
9. Duesbery NS, Resau J, Webb CP, Koochekpour S, Koo HM, et al. (2001) Suppression of ras-mediated transformation and inhibition of tumor growth and angiogenesis by anthrax lethal factor, a proteolytic inhibitor of multiple MEK pathways. Proc Natl Acad Sci U S A 98: 4089-4094.
10. Depeille P, Young JJ, Boguslawski EA, Berghuis BD, Kort EJ, et al. (2007) Anthrax lethal toxin inhibits growth of and vascular endothelial growth factor release from endothelial cells expressing the human herpes virus 8 viral G protein coupled receptor. Clin Cancer Res 13: 5926-5934.
11. Ding Y, Boguslawski EA, Berghuis BD, Young JJ, Zhang Z, et al. (2008) Mitogen-activated protein kinase kinase signaling promotes growth and vascularization of fibrosarcoma. Mol Cancer Ther 7: 648-658.
12. Liu S, Wang H, Currie BM, Molinolo A, Leung HJ, et al. (2008) Matrix metalloproteinase-activated anthrax lethal toxin demonstrates high potency in targeting tumor vasculature. J Biol Chem 283: 529-540.
13. Alfano RW, Leppla SH, Liu S, Bugge TH, Meininger CJ, et al. (2009) Matrix metalloproteinase-activated anthrax lethal toxin inhibits endothelial invasion and neovasculature formation during in vitro morphogenesis. Mol Cancer Res 7: 452-461.
14. Saint-Geniez M, D'Amore PA (2004) Development and pathology of the hyaloid, choroidal and retinal vasculature. Int J Dev Biol 48: 1045-1058.
15. Dorrell MI, Friedlander M, Smith LEH (2007) Retinal Vascular Devleopment. In: Joussen AM, Gardner TW, Kirchhof B, Ryan SJ, eds (2007) Retinal Vascular Disease. Berlin: Springer 24-37.
16. Young JA, Collier RJ (2007) Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu Rev Biochem 76: 243-265.
17. Arora N, Klimpel KR, Singh Y, Leppla SH (1992) Fusions of anthrax toxin lethal factor to the ADP-ribosylation domain of Pseudomonas exotoxin A are potent cytotoxins which are translocated to the cytosol of mammalian cells. J Biol Chem 267: 15542-15548.
18. Koo HM, VanBrocklin M, McWilliams MJ, Leppla SH, Duesbery NS, et al. (2002) Apoptosis and melanogenesis in human melanoma cells induced by anthrax lethal factor inactivation of mitogen-activated protein kinase kinase. Proc Natl Acad Sci U S A 99: 3052-3057.
19. Klimpel KR, Arora N, Leppla SH (1994) Anthrax toxin lethal factor contains a zinc metalloprotease consensus sequence which is required for lethal toxin activity. Mol Microbiol 13: 1093-1100.
20. Milanini J, Vinals F, Pouyssegur J, Pages G (1998) p42/p44 MAP kinase module plays a key role in the transcriptional regulation of the vascular endothelial growth factor gene in fibroblasts. J Biol Chem 273: 18165-18172.
21. Pages G, Milanini J, Richard DE, Berra E, Gothie E, et al. (2000) Signaling angiogenesis via p42/p44 MAP kinase cascade. Ann N Y Acad Sci 902: 187-200.
22. Berra E, Pages G, Pouyssegur J (2000) MAP kinases and hypoxia in the control of VEGF expression. Cancer Metastasis Rev 19: 139-145.
23. Gariano RF, Gardner TW (2005) Retinal angiogenesis in development and disease. Nature 438: 960-966.
24. Dorrell MI, Friedlander M (2006) Mechanisms of endothelial cell guidance and vascular patterning in the developing mouse retina. Prog Retin Eye Res 25: 277-295.
25. Stone J, Itin A, Alon T, Pe'er J, Gnessin H, et al. (1995) Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15: 4738-4747.
26. Dorrell MI, Aguilar E, Friedlander M (2002) Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest Ophthalmol Vis Sci 43: 3500-3510.
27. Yafai Y, Lange J, Wiedemann P, Reichenbach A, Eichler W (2007) Pigment epithelium-derived factor acts as an opponent of growth-stimulatory factors in retinal glial-endothelial cell interactions. Glia 55: 642-651.
28. Tobe T, Okamoto N, Vinores MA, Derevjanik NL, Vinores SA, et al. (1998) Evolution of neovascularization in mice with overexpression of vascular endothelial growth factor in photoreceptors. Invest Ophthalmol Vis Sci 39: 180-188.
29. Bullard LE, Qi X, Penn JS (2003) Role for extracellular signal-responsive kinase-1 and -2 in retinal angiogenesis. Invest Ophthalmol Vis Sci 44: 1722-1731.
30. Hayashi A, Koroma BM, Imai K, de Juan E Jr (1996) Increase of protein tyrosine phosphorylation in rat retina after ischemia-reperfusion injury. Invest Ophthalmol Vis Sci 37: 2146-2156.
31. Hayashi A, Imai K, Kim HC, de Juan E Jr (1997) Activation of protein tyrosine phosphorylation after retinal branch vein occlusion in cats. Invest Ophthalmol Vis Sci 38: 372-380.
32. Guma M, Rius J, Duong-Polk KX, Haddad GG, Lindsey JD, et al. (2009) Genetic and pharmacological inhibition of JNK ameliorates hypoxia-induced retinopathy through interference with VEGF expression. Proc Natl Acad Sci U S A.
33. Bolcome RE 3rd, Sullivan SE, Zeller R, Barker AP, Collier RJ, et al. (2008) Anthrax lethal toxin induces cell death-independent permeability in zebrafish vasculature. Proc Natl Acad Sci U S A 105: 2439-2444.
34. D'Angelo G, Struman I, Martial J, Weiner RI (1995) Activation of mitogen-activated protein kinases by vascular endothelial growth factor and basic fibroblast growth factor in capillary endothelial cells is inhibited by the antiangiogenic factor 16-kDa N-terminal fragment of prolactin. Proc Natl Acad Sci U S A 92: 6374-6378.
35. Rousseau S, Houle F, Landry J, Huot J (1997) p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene 15: 2169-2177.
36. Pedram A, Razandi M, Levin ER (1998) Extracellular signal-regulated protein kinase/Jun kinase cross-talk underlies vascular endothelial cell growth factor-induced endothelial cell proliferation. J Biol Chem 273: 26722-26728.
37. Pages G, Berra E, Milanini J, Levy AP, Pouyssegur J (2000) Stress-activated protein kinases (JNK and p38/HOG) are essential for vascular endothelial growth factor mRNA stability. J Biol Chem 275: 26484-26491.
38. Ennis BW, Fultz KE, Smith KA, Westwick JK, Zhu D, et al. (2005) Inhibition of tumor growth, angiogenesis, and tumor cell proliferation by a small molecule inhibitor of c-Jun N-terminal kinase. J Pharmacol Exp Ther 313: 325-332.
39. Mavria G, Vercoulen Y, Yeo M, Paterson H, Karasarides M, et al. (2006) ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9: 33-44.
40. Moayeri M, Leppla SH (2004) The roles of anthrax toxin in pathogenesis. Curr Opin Microbiol 7: 19-24.
41. Sherer K, Li Y, Cui X, Eichacker PQ (2007) Lethal and edema toxins in the pathogenesis of Bacillus anthracis septic shock: implications for therapy. Am J Respir Crit Care Med 175: 211-221.
42. Guarner J, Jernigan JA, Shieh WJ, Tatti K, Flannagan LM, et al. (2003) Pathology and pathogenesis of bioterrorism-related inhalational anthrax. Am J Pathol 163: 701-709.
43. Kirby JE (2004) Anthrax lethal toxin induces human endothelial cell apoptosis. Infect Immun 72: 430-439.
44. Warfel JM, Steele AD, D'Agnillo F (2005) Anthrax lethal toxin induces endothelial barrier dysfunction. Am J Pathol 166: 1871-1881.
45. Kuo SR, Willingham MC, Bour SH, Andreas EA, Park SK, et al. (2008) Anthrax toxin-induced shock in rats is associated with pulmonary edema and hemorrhage. Microb Pathog 44: 467-472.
46. Su X, Sorenson CM, Sheibani N (2003) Isolation and characterization of murine retinal endothelial cells. Mol Vis 9: 171-178.
47. Park S, Leppla SH (2000) Optimized production and purification of Bacillus anthracis lethal factor. Protein Expr Purif 18: 293-302.
48. Bromberg-White JL, Duesbery NS (2008) Biological and biochemical characterization of anthrax lethal factor, a proteolytic inhibitor of MEK signaling pathways. Methods Enzymol 438: 355-365.
49. Arora N, Leppla SH (1993) Residues 1-254 of anthrax toxin lethal factor are sufficient to cause cellular uptake of fused polypeptides. J Biol Chem 268: 3334-3341.
50. Pang J, Cheng M, Haire SE, Barker E, Planelles V, et al. (2006) Efficiency of lentiviral transduction during development in normal and rd mice. Mol Vis 12: 756-767.
51. Aiello LP, Pierce EA, Foley ED, Takagi H, Chen H, et al. (1995) Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc Natl Acad Sci U S A 92: 10457-10461.
52. Qiao H, Sonoda KH, Ikeda Y, Yoshimura T, Hijioka K, et al. (2007) Interleukin-18 regulates pathological intraocular neovascularization. J Leukoc Biol 81: 1012-1021.