Intercellular adhesion molecule-1-dependent neutrophil adhesion to endothelial cells induces caveolae-mediated pulmonary vascular hyperpermeability

Circulation Research

Volumn 102, Issue 12, 2008, Pages

  Hu, Guochang ^a   Vogel, Stephen M ^a   Schwartz, David E ^a   Malik, Asrar B ^a   Minshall, Richard D ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Albumin transport; Caveolin 1; Endothelial permeability; Lung edema; Src

Indexed keywords

ALBUMIN; CAVEOLIN 1; INTERCELLULAR ADHESION MOLECULE 1; MONOCLONAL ANTIBODY; BETA CYCLODEXTRIN; BETA CYCLODEXTRIN DERIVATIVE; ICAM1 PROTEIN, MOUSE; PROTEIN KINASE P60; SERUM ALBUMIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; BLOOD VESSEL WALL; CAVEOLA; CELL ADHESION; CONTROLLED STUDY; CROSS LINKING; ENDOCYTOSIS; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; KNOCKOUT MOUSE; LUNG EDEMA; LUNG VASCULAR HYPERPERMEABILITY; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RAT; TRANSCYTOSIS; ANIMAL; BIOSYNTHESIS; CAPILLARY PERMEABILITY; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; LUNG; MOUSE MUTANT; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; SPRAGUE DAWLEY RAT; VASCULARIZATION;

ANIMALS; ANTIBODIES, MONOCLONAL; BETA-CYCLODEXTRINS; CAPILLARY PERMEABILITY; CAVEOLAE; CAVEOLIN 1; CELL ADHESION; CELLS, CULTURED; ENDOCYTOSIS; ENDOTHELIAL CELLS; INTERCELLULAR ADHESION MOLECULE-1; LUNG; MICE; MICE, KNOCKOUT; NEUTROPHILS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS PP60(C-SRC); PULMONARY EDEMA; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SERUM ALBUMIN;

EID: 48249117901     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.107.167486     Document Type: Article

References (45)

1. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev. 2006;86:279-367.
2. Matthay MA, Wiener-Kronish JP. Intact epithelial barrier function is critical for the resolution of alveolar edema in humans. Am Rev Respir Dis. 1990;142:1250-1257.
3. Matthay MA, Zimmerman GA. Acute lung injury and the acute respiratory distress syndrome: four decades of inquiry into pathogenesis and rational management. Am J Respir Cell Mol Biol. 2005;33:319-327.
4. Lo SK, Everitt J, Gu J, Malik AB. Tumor necrosis factor mediates experimental pulmonary edema by ICAM-1 and CD18-dependent mechanisms. J Clin Invest. 1992;89:981-988.
5. Lindbom L. Regulation of vascular permeability by neutrophils in acute inflammation. Chem Immunol Allergy. 2003;83:146-166.
6. Tinsley JH, Ustinova EE, Xu W, Yuan SY. Src-dependent, neutrophil-mediated vascular hyperpermeability and β-catenin modification. Am J Physiol. 2002;283:C1745-C1751.
7. Cepinskas G, Noseworthy R, Kvietys PR. Transendothelial neutrophil migration. Role of neutrophil-derived proteases and relationship to transendothelial protein movement. Circ Res. 1997;81:618-626.
8. Lum H, Malik AB. Mechanisms of increased endothelial permeability. Can J Physiol Pharmacol. 1996;74:787-800.
9. Gibbs LS, Lai L, Malik AB. Tumor necrosis factor enhances the neutrophil-dependent increase in endothelial permeability. J Cell Physiol. 1990;145:496-500.
10. Minshall RD, Tiruppathi C, Vogel SM, Malik AB. Vesicle formation and trafficking in endothelial cells and regulation of endothelial barrier function. Histochem Cell Biol. 2002;117:105-112.
11. Predescu SA, Predescu DN, Palade GE. Plasmalemmal vesicles function as transcytotic carriers for small proteins in the continuous endothelium. Am J Physiol. 1997;272:H937-H949.
12. Bachofen H, Bachofen M, Weibel ER. 1988. Ultrastructural aspects of pulmonary edema. J Thorac Imaging. 1988;3:1-7.
13. Minshall RD, Sessa WC, Stan RV, Anderson RG, Malik AB. Caveolin regulation of endothelial function. Am J Physiol. 2003;285: L1179-L1183.
14. Rothberg KG, Heuser JE, Donzell WC, Ying Y-S, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell. 1992;68:673-682.
15. Pelkmans L, Helenius A. Endocytosis via caveolae. Traffic. 2002;3: 311-320.
16. Stan RV. Structure and function of endothelial caveolae. Microsc Res Tech. 2002;57:350-364.
17. Bazzoni G, Dejana E. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev. 2004;84:869-901.
18. Schubert W, Frank PG, Razani B, Park DS, Chow CW, Lisanti MP. Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J Biol Chem. 2001;276:48619-48622.
19. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science. 2001;293:2449-2452.
20. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, Di Vizio D, Hou H Jr, Kneitz B, Lagaud G, Christ GJ, Edelmann W, Lisanti MP. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem. 2001;276:38121-38138.
21. Shajahan AN, Timblin BK, Sandoval R, Tiruppathi C, Malik AB, Minshall RD. Role of Src-induced dynamin-2 phosphorylation in caveolae-mediated endocytosis in endothelial cells. J Biol Chem. 2004; 279:20392-20400.
22. Tiruppathi C, Song W, Bergenfeldt M, Sass P, Malik AB. Gp60 activation mediates albumin transcytosis in endothelial cells by a tyrosine kinasedependent pathway. J Biol Chem. 1997;272:25968-25975.
23. i-coupled Src kinase signaling pathway. J Cell Biol. 2000;150:1057-1070.
24. Shajahan AN, Tiruppathi C, Smrcka AV, Malik AB, Minshall RD. Gβγ activation of Src induces caveolae-mediated endocytosis in endothelial cells. J Biol Chem. 2004;279:48055-48062.
25. Parton RG, Joggerst B, Simons K. Regulated internalization of caveolae. J Cell Biol. 1994;127:1199-1215.
26. Li S, Seitz R, Lisanti MP. Phosphorylation of caveolin by Src tyrosine kinases. The α-isoform of caveolin is selectively phosphorylated by v-Src in vivo. J Biol Chem. 1996;271:3863-3868.
27. Glenney JR Jr. Tyrosine phosphorylation of a 22-kDa protein is correlated with transformation by Rous sarcoma virus. J Biol Chem. 1989;264: 20163-20166.
28. 2-mediated permeability II: importance of tyrosine phosphatase and kinase activity. Am J Physiol. 2001;281:C1940-C1947.
29. Wang Q, Pfeiffer GR II, Gaarde WA. Activation of Src tyrosine kinases in response to ICAM-1 ligation in pulmonary microvascular endothelial cells. J Biol Chem. 2003;278:47731-47743.
30. Tilghman RW, Hoover RL. The Src-cortactin pathway is required for clustering of E-selectin and ICAM-1 in endothelial cells. FASEB J. 2002;16:1257-1259.
31. Brumell JH, Burkhardt AL, Bolen JB, Grinstein S. Endogenous reactive oxygen intermediates activate tyrosine kinases in human neutrophils. J Biol Chem. 1996;271:1455-1461.
32. Volonte D, Galbiati F, Pestell RG, Lisanti MP. Cellular stress induces the tyrosine phosphorylation of caveolin-1 (Tyr-14) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress. J Biol Chem. 2001;276:8094-8103.
33. John TA, Vogel SM, Tiruppathi C, Malik AB, Minshall RD. Quantitative analysis of albumin uptake and transport in the rat microvessel endothelial monolayer. Am J Physiol. 2003;284:L187-L196.
34. Tiruppathi C, Malik AB, Del Vecchio PJ, Keese CR, Giaever I. Electrical method for detection of endothelial cell shape change in real time: assessment of endothelial barrier function. Proc Natl Acad Sci U S A. 1992;89:7919-7923.
35. Williams JH Jr, Moser KM, Ulich T, Cairo MS. Harvesting the noncirculating pool of polymorphonuclear leukocytes in rats by hetastarch exchange transfusion (HET): yield and functional assessment. J Leukoc Biol. 1987;42:455-462.
36. Xu N, Rahman A, Minshall RD, Tiruppathi C, Malik AB. β2-Integrin blockade driven by E-selectin promoter prevents neutrophil sequestration and lung injury in mice. Circ Res. 2000;87:254-260.
37. Vogel SM, Minshall RD, Pilipovic M, Tiruppathi C, Malik AB. Albumin uptake and transcytosis in endothelial cells in vivo induced by albuminbinding protein. Am J Physiol. 2001;281:L1512-L1522.
38. Parker JC, Townsley MI. Evaluation of lung injury in rats and mice. Am J Physiol. 2004;286:L231-L246.
39. Keller P, Simons K. Cholesterol is required for surface transport of influenza virus hemagglutinin. J Cell Biol. 1998;140:1357-1367.
40. Schnitzer JE, Oh P, Pinney E, J Allard J. Filipin-sensitive caveolaemediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol. 1994;127:1217-1232.
41. Sano H, Nakagawa N, Chiba R, Kurasawa K, Saito Y, Iwamoto I. Cross-linking of intercellular adhesion molecule-1 induces interleukin-8 and RANTES production through the activation of MAP kinases in human vascular endothelial cells. Biochem Biophys Res Commun. 1998; 250:694-698.
42. Harlan JM, Schwartz BR, Reidy MA, Schwartz SM, Ochs HD, Harker LA. Activated neutrophils disrupt endothelial monolayer integrity by an oxygen radical-independent mechanism. Lab Invest. 1985;52: 141-150.
43. Burns AR, Bowden RA, MacDonell SD, Walker DC, Odebunmi TO, Donnachie EM, Simon SI, Entman ML, Smith CW. Analysis of tight junctions during neutrophil transendothelial migration. J Cell Sci. 2000; 113:45-57.
44. Miyawaki-Shimizu K, Predescu D, Shimizu J, Broman M, Predescu S, Malik AB. siRNA-induced caveolin-1 knockdown in mice increases lung vascular permeability via the junctional pathway. Am J Physiol. 2006; 290:L405-L413.
45. Allingham MJ, van Buul JD, Burridge K. ICAM-1-mediated, Src-and Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J Immunol. 2007;179: 4053-4064.