Vascular barrier regulation by PAF, ceramide, caveolae, and no-an intricate signaling network with discrepant effects in the pulmonary and systemic vasculature

Cellular Physiology and Biochemistry

Volumn 26, Issue 1, 2010, Pages 29-40

  Kuebler, Wolfgang M ^a,b   Yang, Yang ^c   Samapati, Rudi ^b   Uhlig, Stefan ^c  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Acid sphingomyelinase; Caveolae; Ceramide; Endothelium; Nitric oxide; Permeability

Indexed keywords

CAVEOLIN 1; CERAMIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MYOSIN LIGHT CHAIN; NITRIC OXIDE; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOSINE 1 PHOSPHATE; THROMBOCYTE ACTIVATING FACTOR;

ACUTE LUNG INJURY; ADULT RESPIRATORY DISTRESS SYNDROME; BLOOD VESSEL PERMEABILITY; CALCIUM SIGNALING; CALCIUM TRANSPORT; CAVEOLA; HUMAN; INTERNALIZATION; LUNG BLOOD VESSEL; LUNG EDEMA; LUNG ENDOTHELIUM; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEPSIS; SIGNAL TRANSDUCTION; SYSTEMIC CIRCULATION; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; VASCULAR ENDOTHELIUM;

EID: 77952927745     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000315103     Document Type: Review

References (87)

1. Michel CC, Curry FE: Microvascular permeability. Physiol Rev 1999;79:703-761.
2. Starling EH: On the absorption of fluids from the connective tissue spaces. J Physiol 1896;19:312-326.
3. Gamble J, Baranov V, Kotov A, Gartside I, Nehring I, Christ F: Microvascular fluid filtration capacity (Kf) assessed with cumulative small venous pressure steps and with various degrees of tilt. J Gravit Physiol 1997;4:35-36.
4. Parker JC, Townsley MI: Physiological determinants of the pulmonary filtration coefficient. Am J Physiol Lung Cell Mol Physiol 2008;295:L235-L237.
5. Uhlig S, von Bethmann AN: Determination of vascular compliance, interstitial compliance, and capillary filtration coefficient in rat isolated perfused lungs. J Pharmacol Toxicol Methods 1997;37:119-127.
6. Guyton AC, Lindsey AW: Effect of elevated left atrial pressure and decreased plasma protein concentration on the development of pulmonary edema. Circ Res 1959;7:649-657.
7. Dhillon SS, Mahadevan K, Bandi V, Zheng Z, Smith CW, Rumbaut RE: Neutrophils, nitric oxide, and microvascular permeability in severe sepsis. Chest 2005;128:1706-1712.
8. Jacobson JR, Garcia JG: Novel therapies for microvascular permeability in sepsis. Curr Drug Targets 2007;8:509-514.
9. Ware LB, Matthay MA: The acute respiratory distress syndrome. N Engl J Med 4-5-2000;342:1334-1349.
10. Minshall RD, Malik AB: Transport across the endothelium: regulation of endothelial permeability. Handb Exp Pharmacol 2006;107-144.
11. 2+ signaling, TRP channels, and endothelial permeability. Micro-circulation 2006;13:693-708.
12. Wang L, Dudek SM: Regulation of vascular permeability by sphingosine 1-phosphate. Microvasc Res 2009;77:39-45.
13. Göggel R, Winoto-Morbach S, Vielhaber G, Imai Y, Lindner K, Brade L, Brade H, Ehlers S, Slutsky AS, Schutze S, Gulbins E, Uhlig S: PAF-mediated pulmonary edema: a new role for acid sphingomyelinase and ceramide. Nat Med 2004;10:155-160.
14. Göggel R, Uhlig S: The inositol trisphosphate pathway mediates platelet-activating-factor-induced pulmonary oedema. Eur Respir J 2005;25:849-857.
15. Uhlig S, Gulbins E: Sphingolipids in the lungs. Am J Respir Crit Care Med 2008;178:1100-1114.
16. Yang Y, Yin J, Baumgartner W, Samapati R, Solymosi EA, Reppien E, Kuebler WM, Uhlig S: Platelet-activating factor reduces endothelial NO production-role of acid sphingomyelinase. Eur Respir J 2009, in press.
17. Simons K, Toomre D: Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000;1:31-39.
18. Pani B, Singh BB: Lipid rafts/caveolae as microdomains of calcium signaling. Cell Calcium 2009;45:625-633.
19. Yin J, Kuebler WM: Mechano-transduction by TRP Channels: General concepts and specific role in the vasculature. Cell Biochem Biophys 2010;56:1-18.
20. Li XA, Everson W, Smart EJ: Nitric oxide, caveolae, and vascular pathology. Cardiovasc Toxicol 2006;6:1-13.
21. Uhlig S, Goggel R, Engel S: Mechanisms of platelet-activating factor (PAF)-mediated responses in the lung. Pharmacol Rep 2005;57 Suppl:206-221.
22. Li S, Stuart L, Zhang Y, Meduri GU, Umberger R, Yates CR: Inter-individual variability of plasma PAF-acetylhydro-lase activity in ARDS patients and PAFAH genotype. J Clin Pharm Ther 2009;34:447-455.
23. Knezevic II, Predescu SA, Neamu RF, Gorovoy MS, Knezevic NM, Easington C, Malik AB, Predescu DN: Tiam1 and Rac1 are required for platelet-activating factor-induced endothelial junctional disassembly and increase in vascular permeability. J Biol Chem 2009;284:5381-5394.
24. Göggel R, Hoffman S, Nüsing R, Narumiya S, Uhlig S: Platelet-activating factor-induced pulmonary edema is partly mediated by prostaglandin E(2), E-prostanoid 3-receptors, and potassium channels. Am J Respir Crit Care Med 2002;166(5):657-662.
25. Uhlig S, Wollin L, Wendel A: Contributions of thromboxane and leukotrienes to PAF-induced impairment of lung function in the rat. J Appl Physiol 1994;77:262-269.
26. Adamson RH, Zeng M, Adamson GN, Lenz JF, Curry FE: PAF-and bradykinin-induced hyperpermeability of rat venules is independent of actin-myosin contraction. Am J Physiol Heart Circ Physiol 2003;285:H406-H417.
27. Lautenschläger I, Dombrowsky H, Frerichs I, Kuchenbecker SC, Bade S, Schultz H, Zabel P, Scholz J, Weiler N, Uhlig S: A model of the isolated perfused rat small intestine. Am J Physiol Gastrointest Liver Physiol 2010;298:G304-G313.
28. Jiang Y, Wen K, Zhou X, Schwegler-Berry D, Castranova V, He P: Three-dimensional localization and quantification of PAF-induced gap formation in intact venular microvessels. Am J Physiol Heart Circ Physiol 2008;295:H898-H906.
29. Tan XD, Chang H, Qu XW, Caplan M, Gonzalez-Crussi F, Hsueh W: Platelet-activating factor increases mucosal permeability in rat intestine via tyrosine phosphorylation of E-cadherin. Br J Pharmacol 2000;129:1522-1529.
30. Hudry-Clergeon H, Stengel D, Ninio E, Vilgrain I: Platelet-activating factor increases VE-cadherin tyrosine phosphorylation in mouse endothelial cells and its association with the PtdIns3'-kinase. FASEB J 2005;19:512-520.
31. Kubes P, Suzuki M, Granger DN: Modulation of PAF-induced leukocyte adherence and increased microvascular permeability. Am J Physiol 1990;259:G859-G864.
32. He P, Zhang H, Zhu L, Jiang Y, Zhou X: Leukocyte-platelet aggregate adhesion and vascular permeability in intact microvessels: role of activated endothe-lial cells. Am J Physiol Heart Circ Physiol 2006;291:H591-H599.
33. Armstrong R: The physiological role and pharmacological potential of nitric oxide in neutrophil activation. Int Immuno-pharmacol 2001;1:1501-1512.
34. Kuebler WM, Uhlig U, Goldmann T, Schael G, Kerem A, Exner K, Martin C, Vollmer E, Uhlig S: Stretch activates nitric oxide production in pulmonary vascular endothelial cells in situ. Am J Respir Crit Care Med 2003;168:1391-1398.
35. Kuebler WM, Parthasarathi K, Lindert J, Bhattacharya J: Real-time lung microscopy. J Appl Physiol 2007;102:1255-1264.
36. Bussolati B, Mariano F, Migliori M, Camussi G: Nitric oxide/platelet activating factor cross-talk in mesangial cells modulates the interaction with leukocytes. Kidney Int 2002;62:1322-1331.
37. Ramirez MM, Quardt SM, Kim D, Oshiro H, Minnicozzi M, Duran WN: Platelet activating factor modulates microvascular permeability through nitric oxide synthesis. Microvasc Res 1995;50:223-234.
38. Kim DD, Kanetaka T, Duran RG, Sanhez FA, Bohlen H G, Dura WN: Independent regulation of periarteriolar and perivenular nitric oxide mechanisms in the in vivo hamster cheek pouch microvasculature. Microcirculation 2009;16:323-330.
39. 2+ ]i and NO production in individually perfused intact microvessels. Am J Physiol Heart Circ Physiol 2005;288:H2869-H2877.
40. Kikuchi M, Shirasaki H, Himi T: Platelet-activating factor (PAF) increases NO production in human endothelial cells-real-time monitoring by DAR-4M AM. Prostaglandins Leukot Essent Fatty Acids 2008;78:305-309.
41. Klabunde RE, Anderson DE: Obligatory role of nitric oxide in platelet-activating factor-induced microvascular leakage. Eur J Pharmacol 2000;404:387-394.
42. Zhu L, Schwegler-Berry D, Castranova V, He P: Internalization of caveolin-1 scaffolding domain facilitated by Antennapedia homeodomain attenuates PAF-induced increase in microvessel permeability. Am J Physiol Heart Circ Physiol 2004;286:H195-H201.
43. Hatakeyama T, Pappas PJ, Hobson RW, Boric MP, Sessa WC, Duran WN: Endothelial nitric oxide synthase regulates microvascular hyper-permeability in vivo. J Physiol 2006;574:275-281.
44. Sanchez FA, Kim DD, Duran RG, Meininger CJ, Duran WN: Internalization of eNOS via caveolae regulates PAF-induced inflammatory hyperpermeability to macromolecules. Am J Physiol Heart Circ Physiol 2008;295:H1642-H1648.
45. Filep JG, Foldes-Filep E: Modulation by nitric oxide of platelet-activating factor-induced albumin extravasation in the conscious rat. Br J Pharmacol 1993;110:1347-1352.
46. Yin J, Hoffmann J, Kaestle SM, Neye N, Wang L, Baeurle J, Liedtke W, Wu S, Kuppe H, Pries AR, Kuebler WM: Negative-feedback loop attenuates hydrostatic lung edema via a cGMP-dependent regulation of transient receptor potential vanilloid 4. Circ Res 2008;102:966-974.
47. Predescu D, Predescu S, Shimizu J, Miyawaki-Shimizu K, Malik AB: Constitutive eNOS-derived nitric oxide is a determinant of endothelial junctional integrity. Am J Physiol Lung Cell Mol Physiol 2005;289:L371-L381.
48. Samapati R, Yang Y, Uhlig S, Kuebler WM. PAF causes vascular barrier failure by acid sphingomyelinase-and ceramide-dependent activation of endothelial TRPC channels. J Vasc Res 46 Suppl. 3, 34. 2009.
49. Kaestle SM, Reich CA, Yin N, Habazettl H, Weimann J, Kuebler WM: Nitric oxide-dependent inhibition of alveolar fluid clearance in hydrostatic lung edema. Am J Physiol Lung Cell Mol Physiol 2007;293:L859-L869.
50. Roth A G, Drescher D, Yang Y, Redmer S, Uhlig S, Arenz C: Potent and selective inhibition of acid sphingomyelinase by bisphosphonates. Angew Chem Int Ed Engl 2009;48:7560-7563.
51. Wong ML, Xie B, Beatini N, Phu P, Marathe S, Johns A, Gold PW, Hirsch E, Williams KJ, Licinio J, Tabas I: Acute systemic inflammation up-regulates secretory sphingomyelinase in vivo: a possible link between inflammatory cytokines and atherogenesis. Proc Natl Acad Sci USA 2000;97:8681-8686.
52. Claus RA, Bunck AC, Bockmeyer CL, Brunkhorst FM, Losche W, Kinscherf R, Deigner HP: Role of increased sphingomyelinase activity in apoptosis and organ failure of patients with severe sepsis. FASEB J 2005;19:1719-1721.
53. Czarny M, Schnitzer JE: Neutral sphingomyelinase inhibitor scyphostatin prevents and ceramide mimics mechano-transduction in vascular endothelium. Am J Physiol Heart Circ Physiol 2004;287:H1344-H1352.
54. Igarashi J, Thatte HS, Prabhakar P, Golan DE, Michel T: Calcium-independent activation of endothelial nitric oxide synthase by ceramide. Proc Natl Acad Sci USA 1999;96:12583-12588. (Pubitemid 29513545)
55. Florio T, Arena S, Pattarozzi A, Thellung S, Corsaro A, Villa V, Massa A, Diana F, Spoto G, Forcella S, Damonte G, Filocamo M, Benatti U, Schettini G: Basic fibroblast growth factor activates endothelial nitric-oxide synthase in CHO-K1 cells via the activation of ceramide synthesis. Mol Pharmacol 2003;63:297-310.
56. Li XA, Titlow WB, Jackson BA, Giltiay N, Nikolova-Karakashian M, Uittenbogaard A, Smart EJ: High density lipoprotein binding to scavenger receptor, Class B, type I activates endothelial nitric-oxide synthase in a ceramide-dependent manner. J Biol Chem 2002;277:11058-11063.
57. Clementi E, Borgese N, Meldolesi J: Interactions between nitric oxide and sphingolipids and the potential consequences in physiology and pathology. Trends Pharmacol Sci 2003;24:518-523.
58. Schlörmann W, Steiniger F, Richter W, Kaufmann R, Hause G, Lemke C, Westermann M: The shape of caveolae is omega-like after glutaraldehyde fixation and cup-like after cryofixation. Histochem Cell Biol 2010;133:223-228.
59. Pike LJ: Lipid rafts: heterogeneity on the high seas. Biochem J 2004;378:281-292.
60. Poisson C, Rollin S, Veronneau S, Bousquet SM, Larrivee JF, Le GC, Boulay G, Stankova J, Rola-Pleszczynski M: Caveolae facilitate but are not essential for platelet-activating factor-mediated calcium mobilization and extracellular signal-regulated kinase activation. J Immunol 2009;183:2747-2757.
61. Sbaa E, Frerart F, Feron O: The double regulation of endothelial nitric oxide synthase by caveolae and caveolin: a paradox solved through the study of angiogenesis. Trends Cardiovasc Med 2005;15:157-162.
62. Dhillon B, Badiwala M V, Li SH, Li RK, Weisel RD, Mickle DA, Fedak PW, Rao V, Verma S: Caveolin: a key target for modulating nitric oxide availability in health and disease. Mol Cell Biochem 2003;247:101-109.
63. Feron O, Balligand JL: Caveolins and the regulation of endothelial nitric oxide synthase in the heart. Cardiovasc Res 2006;69:788-797.
64. Gratton JP, Bernatchez P, Sessa WC: Caveolae and caveolins in the cardiovascular system. Circ Res 2004;94:1408-1417.
65. Dirks WG, MacLeod RA, Drexler HG: ECV304 (endothelial) is really T24 (bladder carcinoma): cell line cross-contamination at source. In Vitro Cell Dev Biol Anim 1999;35:558-559.
66. Sanchez FA, Savalia NB, Duran RG, Lal BK, Boric MP, Duran WN: Functional significance of differential eNOS translocation. Am J Physiol Heart Circ Physiol 2006;291:H1058-H1064.
67. Chatterjee S, Cao S, Peterson TE, Simari RD, Shah V: Inhibition of GTP-dependent vesicle trafficking impairs internalization of plasmalemmal eNOS and cellular nitric oxide production. J Cell Sci 2003;116:3645-3655.
68. Maniatis NA, Brovkovych V, Allen SE, John TA, Shajahan AN, Tiruppathi C, Vogel SM, Skidgel RA, Malik AB, Minshall RD: Novel mechanism of endothelial nitric oxide synthase activation mediated by caveolae internalization in endothelial cells. Circ Res 2006;99:870-877.
69. Sanchez FA, Rana R, Kim DD, Iwahashi T, Zheng R, Lal BK, Gordon DM, Meininger CJ, Duran WN: Internali-zation of eNOS and NO delivery to subcellular targets determine agonist-induced hyperpermeability. Proc Natl Acad Sci USA 2009;106:6849-6853.
70. Fleming I, Busse R: Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am J Physiol Regul Integr Comp Physiol 2003;284:R1-12.
71. Hall CN, Garthwaite J: What is the real physiological NO concentration in vivo? Nitric Oxide 2009;21:92-103.
72. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM: Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999;399:601-605.
73. 2+ -ATPase, and inositol trisphosphate receptor. Proc Natl Acad Sci USA 1995;92:1759-1763.
74. Pei DS, Song YJ, Yu HM, Hu WW, Du Y, Zhang GY: Exogenous nitric oxide negatively regulates c-Jun N-terminal kinase activation via inhibiting endogenous NO-induced S-nitrosylation during cerebral ischemia and reperfusion in rat hippocampus. J Neurochem 2008;106:1952-1963.
75. Feron O, Belhassen L, Kobzik L, Smith TW, Kelly RA, Michel T: Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem 1996;271:22810-22814.
76. Feron O, Saldana F, Michel JB, Michel T: The endothelial nitric-oxide synthase-caveolin regulatory cycle. J Biol Chem 1998;273:3125-3128.
77. Garcia-Cardena G, Fan R, Stern DF, Liu J, Sessa WC: Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem 1996;271:27237-27240.
78. Yao X, Garland CJ: Recent developments in vascular endothelial cell transient receptor potential channels. Circ Res 2005;97:853-863.
79. 2+ influx and endothelial permeability. Am J Physiol Lung Cell Mol Physiol 2004;287:L1303-L1313.
80. Tiruppathi C, Freichel M, Vogel SM, Paria BC, Mehta D, Flockerzi V, Malik AB: Impairment of store-operated Ca2+ entry in TRPC4-/-mice interferes with increase in lung microvascular permeability. Circ Res 2002;91:70-76.
81. Alvarez DF, King JA, Weber D, Addison E, Liedtke W, Townsley MI: Transient receptor potential vanilloid 4-mediated disruption of the alveolar septal barrier: a novel mechanism of acute lung injury. Circ Res 2006;99:988-995.
82. Jian MY, King JA, Al-Mehdi AB, Liedtke W, Townsley MI: High vascular pressure-induced lung injury requires P450 epoxygenase-dependent activation of TRPV4. Am J Respir Cell Mol Biol 2008;38:386-392.
83. Hamanaka K, Jian MY, Weber DS, Alvarez DF, Townsley MI, Al-Mehdi AB, King JA, Liedtke W, Parker JC: TRPV4 initiates the acute calcium-dependent permeability increase during ventilator-induced lung injury in isolated mouse lungs. Am J Physiol Lung Cell Mol Physiol 2007;293:L923-L932.
84. 2+ uptake in bovine vascular endothelial cells. J Physiol 2002;539:77-91.
85. Farhi LE, Sheehan DW: Pulmonary circulation and systemic circulation: similar problems, different solutions. Adv Exp Med Biol 1990;277:579-586.
86. Maron MB: Differential effects of histamine on protein permeability in dog lung and forelimb. Am J Physiol 1982;242:H565-H572.
87. Schubert W, Frank PG, Woodman SE, Hyogo H, Cohen DE, Chow CW, Lisanti MP: Microvascular hyperpermeability in caveolin-1 (-/-) knock-out mice. Treatment with a specific nitric-oxide synthase inhibitor, L-NAME, restores normal microvascular permeability in Cav-1 null mice. J Biol Chem 2002;277:40091-40098.