Heterogeneity of pulmonary endothelial cyclic nucleotide response to pseudomonas aeruginosa ExoY infection

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 309, Issue 10, 2015, Pages L1199-L1207

  Morrow, K A ^a,b   Seifert, R ^c   Kaever, V ^c   Britain, A L ^b   Sayner, S L ^a,b   Ochoa, C D ^d   Cioffi, E A ^b   Frank, D W ^e   Rich, T C ^b   Stevens, T ^a,b  

^a UNIVERSITY OF SOUTH ALABAMA   (United States)

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

^c HANNOVER MEDICAL SCHOOL   (Germany)

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

^e MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Compartmentation; Microtubule; Permeability; Pneumonia; Second messenger

Indexed keywords

CYCLIC AMP; CYCLIC GMP; CYCLIC UMP; PURINE; PYRIMIDINE; CYCLIC NUCLEOTIDE;

ARTICLE; CAPILLARY ENDOTHELIAL CELL; CELL HETEROGENEITY; CONTROLLED STUDY; ENDOTHELIUM CELL; INTOXICATION; LUNG ENDOTHELIUM; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; TYPE III SECRETION SYSTEM; CAPILLARY PERMEABILITY; CELL CULTURE; CYTOLOGY; ENZYMOLOGY; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MICROVASCULATURE; PHYSIOLOGY; PULMONARY ARTERY;

CAPILLARY PERMEABILITY; CELLS, CULTURED; ENDOTHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; MICROVESSELS; NUCLEOTIDES, CYCLIC; PSEUDOMONAS AERUGINOSA; PULMONARY ARTERY;

EID: 84947231546     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00165.2015     Document Type: Article

References (61)

1. Adamson RH, Liu B, Fry GN, Rubin LL, Curry FE. Microvascular permeability and number of tight junctions are modulated by cAMP. Am J Physiol Heart Circ Physiol 274: H1885-H1894, 1998
2. Anderson DM, Sato H, Dirck AT, Feix JB, Frank DW. Ubiquitin activates patatin-like phospholipases from multiple bacterial species. J Bacteriol 197: 529-541, 2015
3. Bahre H, Danker KY, Stasch JP, Kaever V, Seifert R. Nucleotidyl cyclase activity of soluble guanylyl cyclase in intact cells. Biochem Biophys Res Commun 443: 1195-1199, 2014
4. Bahre H, Hartwig C, Munder A, Wolter S, Stelzer T, Schirmer B, Beckert U, Frank DW, Tummler B, Kaever V, Seifert R. cCMP and cUMP occur in vivo. Biochem Biophys Res Commun 460: 909-914, 2015
5. 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
6. Beavo JA. Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol Rev 75: 725-748, 1995
7. Beckert U, Wolter S, Hartwig C, Bahre H, Kaever V, Ladant D, Frank DW, Seifert R. ExoY from Pseudomonas aeruginosa is a nucleotidyl cyclase with preference for cGMP and cUMP formation. Biochem Biophys Res Commun 450: 870-874, 2014
8. Beste KY, Burhenne H, Kaever V, Stasch JP, Seifert R. Nucleotidyl cyclase activity of soluble guanylyl cyclase alpha1beta1. Biochemistry 51: 194-204, 2012
9. Bloch A. Cytidine 3’,5’-monophosphate (cyclic CMP). I. Isolation from extracts of leukemia L-1210 cells. Biochem Biophys Res Commun 58: 652-659, 1974
10. Bloch A. Uridine 3’,5’-monophosphate (cyclic UMP). I. Isolation from rat liver extracts. Biochem Biophys Res Commun 64: 210-218, 1975
11. Bloch A, Cheng YC. Modulation of cyclic CMP-specific phosphodiesterase activity by polyamines and by cyclic purine nucleotides. Adv Enzyme Regul 17: 283-287, 1978
12. Bonifacio SL, Kitterman JA, Ursell PC. Pseudomonas pneumonia in infants: an autopsy study. Hum Pathol 34: 929-938, 2003
13. Bonilla-Abadia F, Munoz-Buitron E, Ochoa CD, Carrascal E, Canas CA. A rare association of localized scleroderma type morphea, vitiligo, autoimmune hypothyroidism, pneumonitis, autoimmune thrombocytopenic purpura and central nervous system vasculitis. Case report. BMC Res Notes 5: 689, 2012
14. Boyer S, Faure K, Ader F, Husson MO, Kipnis E, Prangere T, Leroy X, Guery BP. Chronic pneumonia with Pseudomonas aeruginosa and impaired alveolar fluid clearance. Respir Res 6: 17, 2005
15. Brigham KL, Woolverton WC, Blake LH, Staub NC. Increased sheep lung vascular permeability caused by pseudomonas bacteremia. J Clin Invest 54: 792-804, 1974
16. Buchan KW, Martin W. Modulation of barrier function of bovine aortic and pulmonary artery endothelial cells: dissociation from cytosolic calcium content. Br J Pharmacol 107: 932-938, 1992
17. Cech SY, Ignarro LJ. Cytidine 3’,5’-monophosphate (cyclic CMP) formation by homogenates of mouse liver. Biochem Biophys Res Commun 80: 119-125, 1978
18. Drummond GI, Perrott-Yee S. Enzymatic hydrolysis of adenosine 3’,5’-phosphoric acid. J Biol Chem 236: 1126-1129, 1961
19. Fan Chung K. Phosphodiesterase inhibitors in airways disease. Eur J Pharmacol 533: 110-117, 2006
20. Fukuhara S, Sakurai A, Sano H, Yamagishi A, Somekawa S, Takakura N, Saito Y, Kangawa K, Mochizuki N. Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol Cell Biol 25: 136-146, 2005
21. 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
22. Hardman JG, Sutherland EW. A cyclic 3’,5’-nucleotide phosphodiesterase from heart with specificity for uridine 3’,5’-phosphate. J Biol Chem 240: 3704-3705, 1965
23. Hartwig C, Bahre H, Wolter S, Beckert U, Kaever V, Seifert R. cAMP, cGMP, cCMP and cUMP concentrations across the tree of life: High cCMP and cUMP levels in astrocytes. Neurosci Lett 579: 183-187, 2014
24. Hasan A, Danker KY, Wolter S, Bahre H, Kaever V, Seifert R. Soluble adenylyl cyclase accounts for high basal cCMP and cUMP concentrations in HEK293 and B103 cells. Biochem Biophys Res Commun 448: 236-240, 2014
25. 2+]i and permeability in microvessels exposed to ATP. Am J Physiol Heart Circ Physiol 265: H1019-H1023, 1993
26. Hewlett EL, Urban MA, Manclark CR, Wolff J. Extracytoplasmic adenylate cyclase of Bordetella pertussis. Proc Natl Acad Sci USA 73: 1926-1930, 1976
27. King J, Hamil T, Creighton J, Wu S, Bhat P, McDonald F, Stevens T. Structural and functional characteristics of lung macro-and microvascular endothelial cell phenotypes. Microvasc Res 67: 139-151, 2004
28. Klinger JR. The nitric oxide/cGMP signaling pathway in pulmonary hypertension. Clin Chest Med 28: 143-167, 2007
29. Klotz U, Stock K. Evidence for a cyclic nucleotide-phosphodiesterase with high specificity for cyclic uridine-3’,5’-monophosphate in rat adipose tissue. Naunyn Schmiedebergs Arch Pharmakol 269: 117-120, 1971
30. Kuo JF, Brackett NL, Shoji M, Tse J. Cytidine 3’:5’-monophosphate phosphodiesterase in mammalian tissues. Occurrence and biological involvement. J Biol Chem 253: 2518-2521, 1978
31. Lange M, Hamahata A, Enkhbaatar P, Esechie A, Connelly R, Nakano Y, Jonkam C, Cox RA, Traber LD, Herndon DN, Traber DL. Assessment of vascular permeability in an ovine model of acute lung injury and pneumonia-induced Pseudomonas aeruginosa sepsis. Crit Care Med 36: 1284-1289, 2008
32. Langeler EG, van Hinsbergh VW. Norepinephrine and iloprost improve barrier function of human endothelial cell monolayers: role of cAMP. Am J Physiol Cell Physiol 260: C1052-C1059, 1991
33. Laue S, Winterhoff M, Kaever V, van den Heuvel JJ, Russel FG, Seifert R. cCMP is a substrate for MRP5. Naunyn Schmiedebergs Arch Pharmacol 387: 893-895, 2014
34. 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
35. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S, Chepenik KP, Waldman SA. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 52: 375-414, 2000
36. Lugnier C, Schoeffter P, Le Bec A, Strouthou E, Stoclet JC. Selective inhibition of cyclic nucleotide phosphodiesterases of human, bovine and rat aorta. Biochem Pharmacol 35: 1743-1751, 1986
37. Maurice DH. Cardiovascular implications in the use of PDE5 inhibitor therapy. Int J Impot Res 16, Suppl 1: S20-S23, 2004
38. Mayer M, Stief CG, Truss MC, Uckert S. Phosphodiesterase inhibitors in female sexual dysfunction. World J Urol 23: 393-397, 2005
39. Monzel M, Kuhn M, Bahre H, Seifert R, Schneider EH. PDE7A1 hydrolyzes cCMP. FEBS Lett 588: 3469-3474, 2014
40. Newton RP, Hakeem NA, Salvage BJ, Wassenaar G, Kingston EE. Cytidylate cyclase activity: identification of cytidine 3’,5’-cyclic monophosphate and four novel cytidine cyclic phosphates as biosynthetic products from cytidine triphosphate. Rapid Commun Mass Spectrom 2: 118-126, 1988
41. Newton RP, Kingston EE, Hakeem NA, Salih SG, Beynon JH, Moyse CD. Extraction, purification, identification and metabolism of 3’,5’-cyclic UMP, 3’,5’-cyclic IMP and 3’,5’-cyclic dTMP from rat tissues. Biochem J 236: 431-439, 1986
42. Obiako B, Calchary W, Xu N, Kunstadt R, Richardson B, Nix J, Sayner SL. Bicarbonate disruption of the pulmonary endothelial barrier via activation of endogenous soluble adenylyl cyclase, isoform 10. Am J Physiol Lung Cell Mol Physiol 305: L185-L192, 2013
43. 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
44. Ochoa CD, Stevens T, Balczon R. Cold exposure reveals two populations of microtubules in pulmonary endothelia. Am J Physiol Lung Cell Mol Physiol 300: L132-L138, 2011
45. 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
46. Reinecke D, Burhenne H, Sandner P, Kaever V, Seifert R. Human cyclic nucleotide phosphodiesterases possess a much broader substratespecificity than previously appreciated. FEBS Lett 585: 3259-3262, 2011
47. Rich TC, Fagan KA, Nakata H, Schaack J, Cooper DM, Karpen JW. Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J Gen Physiol 116: 147-161, 2000
48. Rich TC, Fagan KA, Tse TE, Schaack J, Cooper DM, Karpen JW. A uniform extracellular stimulus triggers distinct cAMP signals in different compartments of a simple cell. Proc Natl Acad Sci USA 98: 13049-13054, 2001
49. Sayner SL. Emerging themes of cAMP regulation of the pulmonary endothelial barrier. Am J Physiol Lung Cell Mol Physiol 300: L667-L678, 2011
50. Sayner SL, Alexeyev M, Dessauer CW, Stevens T. Soluble adenylyl cyclase reveals the significance of cAMP compartmentation on pulmonary microvascular endothelial cell barrier. Circ Res 98: 675-681, 2006
51. 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
52. Schneider EH, Seifert R. Report on the Third Symposium “cCMP and cUMP as New Second Messengers”. Naunyn Schmiedebergs Arch Pharmacol 388: 1-3, 2015
53. Seifert R. cCMP and cUMP: emerging second messengers. Trends Biochem Sci 40: 8-15, 2015
54. Siflinger-Birnboim A, Bode DC, Malik AB. Adenosine 3’,5’-cyclic monophosphate attenuates neutrophil-mediated increase in endothelial permeability. Am J Physiol Heart Circ Physiol 264: H370-H375, 1993
55. Stevens TC, Ochoa CD, Morrow KA, Robson MJ, Prasain N, Zhou C, Alvarez DF, Frank DW, Balczon R, Stevens T. The Pseudomonas aeruginosa exoenzyme Y impairs endothelial cell proliferation and vascular repair following lung injury. Am J Physiol Lung Cell Mol Physiol 306: L915-L924, 2014
56. Swartz MN, Castleman B. Case records of the Massachusetts General Hospital. Case 15-1966. Extensive burn followed by Pseudomonas septicemia, hypotension, anuria, and death. N Engl J Med 274: 736-744, 1966
57. Teplitz C. Pathogenesis of Pseudomonas vasculitis and septic legions. Arch Pathol 80: 297-307, 1965
58. Winn WC, LaSala PR, Leslie KO. Bacterial Infections. In: Pulmonary Pathology, edited by Tomashefski JF, Cagle PT, Farver CF, and Fraire AE. New York, NY: Springer, 2008, p. 228-315
59. Xin W, Tran TM, Richter W, Clark RB, Rich TC. Roles of GRK and PDE4 activities in the regulation of beta2 adrenergic signaling. J Gen Physiol 131: 349-364, 2008
60. 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
61. Zhu B, Zhang L, Creighton J, Alexeyev M, Strada SJ, Stevens T. Protein kinase A phosphorylation of tau-serine 214 reorganizes microtubules and disrupts the endothelial cell barrier. Am J Physiol Lung Cell Mol Physiol 299: L493-L501, 2010