The Pseudomonas aeruginosa exoenzyme Y impairs endothelial cell proliferation and vascular repair following lung injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 10, 2014, Pages

  Stevens, Trevor C ^a   Ochoa, Cristhiaan D ^c   Morrow, K Adam ^a   Robson, Matthew J ^a   Prasain, Nutan ^d   Zhou, Chun ^a   Alvarez, Diego F ^a   Frank, Dara W ^e   Balczon, Ron ^a,b   Stevens, Troy ^a  

^a UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTH ALABAMA   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Cyclase; Microtubules; Permeability; Pulmonary edema; Tau

Indexed keywords

BACTERIAL ENZYME; EXOENZYME Y; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CYCLIC AMP; EXOY PROTEIN, BACTERIA; GLUCOSYLTRANSFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL ISOLATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; HYDROSTATIC PRESSURE; LUNG INJURY; MALE; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; RAT; VASCULAR SURGERY; ANIMAL; BACTERIAL PNEUMONIA; EDEMA; ENDOTHELIUM CELL; ENZYMOLOGY; HOST PATHOGEN INTERACTION; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; MICROVASCULATURE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSEUDOMONAS INFECTION; VASCULARIZATION;

ANIMALS; BACTERIAL PROTEINS; CELL PROLIFERATION; CYCLIC AMP; EDEMA; ENDOTHELIAL CELLS; GLUCOSYLTRANSFERASES; HOST-PATHOGEN INTERACTIONS; LUNG; LUNG INJURY; MALE; MICROVESSELS; PNEUMONIA, BACTERIAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RATS;

EID: 84900807344     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00135.2013     Document Type: Article

References (35)

1. Ahuja N, Kumar P, Bhatnagar R. The adenylate cyclase toxins. Crit Rev Microbiol 30: 187-196, 2004.
2. Baig S, van Helmond Z, Love S. Tau hyperphosphorylation affects Smad 2/3 translocation. Neuroscience 163: 561-570, 2009.
3. Balczon R, Prasain N, Ochoa C, Prater J, Zhu B, Alexeyev M, Sayner S, Frank DW, Stevens T. Pseudomonas aeruginosa exotoxin Y-mediated tau hyperphosphorylation impairs microtubule assembly in pulmonary microvascular endothelial cells. PLoS One 8: e74343, 2013.
4. Birukova AA, Birukov KG, Smurova K, Adyshev D, Kaibuchi K, Alieva I, Garcia JG, Verin AD. Novel role of microtubules in thrombininduced endothelial barrier dysfunction. FASEB J 18: 1879-1890, 2004.
5. Braun N, Papadopoulos T, Muller-Hermelink HK. Cell cycle dependent distribution of the proliferation-associated Ki-67 antigen in human embryonic lung cells. Virchows Arch B Cell Pathol Incl Mol Pathol 56: 25-33, 1988.
6. Cioffi DL, Moore TM, Schaack J, Creighton JR, Cooper DM, Stevens T. Dominant regulation of interendothelial cell gap formation by calciuminhibited type 6 adenylyl cyclase. J Cell Biol 157: 1267-1278, 2002.
7. 2+-inhibited adenylyl cyclase and phosphodiesterase activities. Am J Physiol Lung Cell Mol Physiol 284: L100-L107, 2003.
8. El-Solh AA, Hattemer A, Hauser AR, Alhajhusain A, Vora H. Clinical outcomes of type III Pseudomonas aeruginosa bacteremia. Crit Care Med 40: 1157-1163, 2012.
9. Engel J, Balachandran P. Role of Pseudomonas aeruginosa type III effectors in disease. Curr Opin Microbiol 12: 61-66, 2009.
10. Glaser P, Sakamoto H, Bellalou J, Ullmann A, Danchin A. Secretion of cyclolysin, the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein of Bordetella pertussis. EMBO J 7: 3997-4004, 1988.
11. Gottle M, Dove S, Kees F, Schlossmann J, Geduhn J, Konig B, Shen Y, Tang WJ, Kaever V, Seifert R. Cytidylyl and uridylyl cyclase activity of bacillus anthracis edema factor and Bordetella pertussis CyaA. Biochemistry 49: 5494-5503, 2010.
12. Gottle M, Dove S, Seifert R. Bacillus anthracis edema factor substrate specificity: evidence for new modes of action. Toxins (Basel) 4: 505-535, 2012.
13. Greenwood JA, Johnson GV. Localization and in situ phosphorylation state of nuclear tau. Exp Cell Res 220: 332-337, 1995.
14. Le Berre R, Nguyen S, Nowak E, Kipnis E, Pierre M, Quenee L, Ader F, Lancel S, Courcol R, Guery BP, Faure K. Relative contribution of three main virulence factors in Pseudomonas aeruginosa pneumonia. Crit Care Med 39: 2113-2120, 2011.
15. Leppla SH. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc Natl Acad Sci USA 79: 3162-3166, 1982.
16. Loomis PA, Howard TH, Castleberry RP, Binder LI. Identification of nuclear tau isoforms in human neuroblastoma cells. Proc Natl Acad Sci USA 87: 8422-8426, 1990.
17. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev 86: 279-367, 2006.
18. Nakamura M, Ito H, Wate R, Nakano S, Hirano A, Kusaka H. Phosphorylated Smad2/3 immunoreactivity in sporadic and familial amyotrophic lateral sclerosis and its mouse model. Acta Neuropathol 115: 327-334, 2008.
19. Ochoa CD, Alexeyev M, Pastukh V, Balczon R, Stevens T. Pseudomonas aeruginosa exotoxin Y is a promiscuous cyclase that increases endothelial tau phosphorylation and permeability. J Biol Chem 287: 25407-25418, 2012.
20. Ochoa CD, Stevens T. Studies on the cell biology of interendothelial cell gaps. Am J Physiol Lung Cell Mol Physiol 302: L275-L286, 2012.
21. Parker JC, Townsley MI. Physiological determinants of the pulmonary filtration coefficient. Am J Physiol Lung Cell Mol Physiol 295: L235-L237, 2008.
22. Parra-Bonilla G, Alvarez DF, Al-Mehdi AB, Alexeyev M, Stevens T. Critical role for lactate dehydrogenase A in aerobic glycolysis that sustains pulmonary microvascular endothelial cell proliferation. Am J Physiol Lung Cell Mol Physiol 299: L513-L522, 2010.
23. Prasain N. Soluble Adenylyl Cyclases Disassemble Microtubules and Disrupt the Pulmonary Endothelial Barrier (PhD Dissertation). Mobile, AL: University of South Alabama, 2009.
24. Prasain N, Alexeyev M, Balczon R, Stevens T. Soluble adenylyl cyclasedependent microtubule disassembly reveals a novel mechanism of endothelial cell retraction. Am J Physiol Lung Cell Mol Physiol 297: L73-L83, 2009.
25. Querfurth HW, LaFerla FM. Alzheimer's disease. N Engl J Med 362: 329-344, 2010.
26. Sayner SL, Frank DW, King J, Chen H, VandeWaa J, Stevens T. Paradoxical cAMP-induced lung endothelial hyperpermeability revealed by Pseudomonas aeruginosa ExoY. Circ Res 95: 196-203, 2004.
27. Seifert R, Hartwig C, Wolter S, Reinecke D, Burhenne H, Kaever V, Munder A, Tummler B, Schwede F, Grundmann M, Kostenis E, Frank DW, Beckert U. Pseudomonas aeruginosa ExoY, a cyclic GMPand cyclic UMP-generating nucleotidyl cyclase. BMC Pharmacol Toxicol 14, Suppl 1: 2013.
28. Sjoberg MK, Shestakova E, Mansuroglu Z, Maccioni RB, Bonnefoy E. Tau protein binds to pericentromeric DNA: a putative role for nuclear tau in nucleolar organization. J Cell Sci 119: 2025-2034, 2006.
29. 2+-inhibitable adenylyl cyclase modulates pulmonary artery endothelial cell cAMP content and barrier function. Proc Natl Acad Sci USA 92: 2696-2700, 1995.
30. Thurston VC, Pena P, Pestell R, Binder LI. Nucleolar localization of the microtubule-associated protein tau in neuroblastomas using sense and anti-sense transfection strategies. Cell Motil Cytoskeleton 38: 100-110, 1997.
31. Thurston VC, Zinkowski RP, Binder LI. Tau as a nucleolar protein in human nonneural cells in vitro and in vivo. Chromosoma 105: 20-30, 1996.
32. Vance RE, Rietsch A, Mekalanos JJ. Role of the type III secreted exoenzymes S, T, and Y in systemic spread of Pseudomonas aeruginosa PAO1 in vivo. Infect Immun 73: 1706-1713, 2005.
33. Verin AD, Birukova A, Wang P, Liu F, Becker P, Birukov K, Garcia JG. Microtubule disassembly increases endothelial cell barrier dysfunction: role of MLC phosphorylation. Am J Physiol Lung Cell Mol Physiol 281: L565-L574, 2001.
34. Winn WC, La Sala PR, Leslie KO. Bacterial infections. In: Pulmonary Pathology, edited by Tomashefski JF, Cagle PT, Farver CF, Fraire AE. New York: Springer, 2008, p. 228-315.
35. Yahr TL, Vallis AJ, Hancock MK, Barbieri JT, Frank DW. ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc Natl Acad Sci USA 95: 13899-13904, 1998.