Leukocyte rolling and adhesion both contribute to regulation of microvascular permeability to albumin via ligation of ICAM-1

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 4, 2011, Pages

  Sumagin, Ronen ^a   Kuebel, Julia M ^a   Sarelius, Ingrid H ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Adhesion molecules; Leukocyte endothelial signaling; Microvessel barrier function

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; ALBUMIN; BISINDOLYLMALEIMIDE; INTERCELLULAR ADHESION MOLECULE 1; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BLOOD VESSEL PERMEABILITY; CLUSTER ANALYSIS; CONTROLLED STUDY; EDEMA; ENDOTHELIUM CELL; INFLAMMATION; LEUKOCYTE ADHERENCE; LEUKOCYTE ROLLING; LIGATION; MALE; MICROVASCULATURE; MOUSE; NEUTROPHIL; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN CROSS LINKING; REGULATORY MECHANISM; VENULE;

ALBUMINS; ANIMALS; CAPILLARY PERMEABILITY; CELL ADHESION; GENE EXPRESSION REGULATION; INTERCELLULAR ADHESION MOLECULE-1; LEUKOCYTE ROLLING; LEUKOCYTES; MICE; MICE, KNOCKOUT; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

MUS;

EID: 80053181077     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00135.2011     Document Type: Article

References (53)

1. 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 179: 4053-4064, 2007.
2. Amos C, Romero IA, Schultze C, Rousell J, Pearson JD, Greenwood J, Adamson P. Cross-linking of brain endothelial intercellular adhesion molecule (ICAM)-1 induces association of ICAM-1 with detergent-insoluble cytoskeletal fraction. Arterioscler Thromb Vasc Biol 21: 810-816, 2001.
3. Basit A, Reutershan J, Morris MA, Solga M, Rose CE Jr, Ley K. ICAM-1 and LFA-1 play critical roles in LPS-induced neutrophil recruitment into the alveolar space. Am J Physiol Lung Cell Mol Physiol 291: L200-L207, 2006.
4. Bjork J, Hedqvist P, Arfors KE. Increase in vascular permeability induced by leukotriene B4 and the role of polymorphonuclear leukocytes. Inflammation 6: 189-200, 1982.
5. Chiang EY, Hidalgo A, Chang J, Frenette PS. Imaging receptor microdomains on leukocyte subsets in live mice. Nat Methods 4: 219-222, 2007.
6. Clark PR, Manes TD, Pober JS, Kluger MS. Increased ICAM-1 expression causes endothelial cell leakiness, cytoskeletal reorganization and junctional alterations. J Invest Dermatol 127: 762-774, 2007.
7. Czabanka M, Peter C, Martin E, Walther A. Microcirculatory endothelial dysfunction during endotoxemia-insights into pathophysiology, pathologic mechanisms and clinical relevance. Curr Vasc Pharmacol 5: 266-275, 2007.
8. Diamond MS, Staunton DE, de Fougerolles AR, Stacker SA, Garcia- Aguilar J, Hibbs ML, Springer TA. ICAM-1 (CD54): a counter-receptor for Mac-1 (CD11b/CD18). J Cell Biol 111: 3129-3139, 1990.
9. Diamond MS, Staunton DE, Marlin SD, Springer TA. Binding of the integrin Mac-1 (CD11b/CD18) to the third immunoglobulin-like domain of ICAM-1 (CD54) and its regulation by glycosylation. Cell 65: 961-971, 1991.
10. DiStasi MR, Ley K. Opening the flood-gates: how neutrophil-endothelial interactions regulate permeability. Trends Immunol 30: 547-556, 2009.
11. Etienne-Manneville S, Manneville JB, Adamson P, Wilbourn B, Greenwood J, Couraud PO. ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J Immunol 165: 3375-3383, 2000.
12. Ferrero E, Zocchi MR, Magni E, Panzeri MC, Curnis F, Rugarli C, Ferrero ME, Corti A. Roles of tumor necrosis factor p55 and p75 receptors in TNF-α-induced vascular permeability. Am J Physiol Cell Physiol 281: C1173-C1179, 2001.
13. Friedl J, Puhlmann M, Bartlett DL, Libutti SK, Turner EN, Gnant MF, Alexander HR. Induction of permeability across endothelial cell monolayers by tumor necrosis factor (TNF) occurs via a tissue factordependent mechanism: relationship between the procoagulant and permeability effects of TNF. Blood 100: 1334-1339, 2002.
14. Gaudreault N, Perrin RM, Guo M, Clanton CP, Wu MH, Yuan SY. Counter regulatory effects of PKCbetaII and PKCdelta on coronary endothelial permeability. Arterioscler Thromb Vasc Biol 28: 1527-1533, 2008.
15. Gautam N, Herwald H, Hedqvist P, Lindbom L. Signaling via beta(2) integrins triggers neutrophil-dependent alteration in endothelial barrier function. J Exp Med 191: 1829-1839, 2000.
16. Gautam N, Olofsson AM, Herwald H, Iversen LF, Lundgren- Akerlund E, Hedqvist P, Arfors KE, Flodgaard H, Lindbom L. Heparin-binding protein (HBP/CAP37): a missing link in neutrophilevoked alteration of vascular permeability. Nat Med 7: 1123-1127, 2001.
17. He P, Wang J, Zeng M. Leukocyte adhesion and microvessel permeability. Am J Physiol Heart Circ Physiol 278: H1686-H1694, 2000.
18. Hermant B, Bibert S, Concord E, Dublet B, Weidenhaupt M, Vernet T, Gulino-Debrac D. Identification of proteases involved in the proteolysis of vascular endothelium cadherin during neutrophil transmigration. J Biol Chem 278: 14002-14012, 2003.
19. Hippenstiel S, Tannert-Otto S, Vollrath N, Krull M, Just I, Aktories K, von Eichel-Streiber C, Suttorp N. Glucosylation of small GTPbinding Rho proteins disrupts endothelial barrier function. Am J Physiol Lung Cell Mol Physiol 272: L38-L43, 1997.
20. Huxley VH, Curry FE. Differential actions of albumin and plasma on capillary solute permeability. Am J Physiol Heart Circ Physiol 260: H1645-H1654, 1991.
21. Huxley VH, Wang JJ, Sarelius IH. Adaptation of coronary microvascular exchange in arterioles and venules to exercise training and a role for sex in determining permeability responses. Am J Physiol Heart Circ Physiol 293: H1196-H1205, 2007.
22. Huxley VH, Williams DA, Meyer DJ Jr, Laughlin MH. Altered basal and adenosine-mediated protein flux from coronary arterioles isolated from exercise-trained pigs. Acta Physiol Scand 160: 315-325, 1997.
23. Johnson-Leger C, Aurrand-Lions M, Imhof BA. The parting of the endothelium: miracle, or simply a junctional affair? J Cell Sci 113: 921-933, 2000.
24. Jun CD, Shimaoka M, Carman CV, Takagi J, Springer TA. Dimerization and the effectiveness of ICAM-1 in mediating LFA-1-dependent adhesion. Proc Natl Acad Sci USA 98: 6830-6835, 2001.
25. Kim MB, Sarelius IH. Distributions of wall shear stress in venular convergences of mouse cremaster muscle. Microcirculation 10: 167-178, 2003.
26. Kim MB, Sarelius IH. Role of shear forces and adhesion molecule distribution on P-selectin-mediated leukocyte rolling in postcapillary venules. Am J Physiol Heart Circ Physiol 287: H2705-H2711, 2004.
27. Kunkel EJ, Jung U, Ley K. TNF-α induces selectin-mediated leukocyte rolling in mouse cremaster muscle arterioles. Am J Physiol Heart Circ Physiol 272: H1391-H1400, 1997.
28. Lindbom L. Regulation of vascular permeability by neutrophils in acute inflammation. Chem Immunol Allergy 83: 146-166, 2003.
29. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev 86: 279-367, 2006.
30. Miller J, Knorr R, Ferrone M, Houdei R, Carron CP, Dustin ML. Intercellular adhesion molecule-1 dimerization and its consequences for adhesion mediated by lymphocyte function associated-1. J Exp Med 82: 1231-1241, 1995.
31. Phillipson M, Heit B, Colarusso P, Liu L, Ballantyne CM, Kubes P. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J Exp Med 203: 2569-2575, 2006.
32. Rosengren S, Olofsson AM, von Andrian UH, Lundgren-Akerlund E, Arfors KE. Leukotriene B4-induced neutrophil-mediated endothelial leakage in vitro and in vivo. J Appl Physiol 71: 1322-1330, 1991.
33. Sarantos MR, Zhang H, Schaff UY, Dixit N, Hayenga HN, Lowell CA, Simon SI. Transmigration of neutrophils across inflamed endothelium is signaled through LFA-1 and Src family kinase. J Immunol 181: 8660-8669, 2008.
34. Sarelius IH. Cell and oxygen flow in arterioles controlling capillary perfusion. Am J Physiol Heart Circ Physiol 265: H1682-H1687, 1993.
35. Sarelius IH, Kuebel JM, Wang J, Huxley VH. Macromolecule permeability of in situ and excised rodent skeletal muscle arterioles and venules. Am J Physiol Heart Circ Physiol 290: H474-H480, 2006.
36. Soehnlein O, Zernecke A, Eriksson EE, Rothfuchs AG, Pham CT, Herwald H, Bidzhekov K, Rottenberg ME, Weber C, Lindbom L. Neutrophil secretion products pave the way for inflammatory monocytes. Blood 112: 1461-1471, 2008.
37. Stanley P, Hogg N. The I domain of integrin LFA-1 interacts with ICAM-1 domain 1 at residue Glu-34 but not Gln-73. J Biol Chem 273: 3358-3362, 1998.
38. Sumagin R, Lamkin-Kennard KA, Sarelius IH. A separate role for ICAM-1 and fluid shear in regulating leukocyte interactions with straight regions of venular wall and venular convergences. Microcirculation 16: 508-520, 2009.
39. Sumagin R, Lomakina E, Sarelius IH. Leukocyte-endothelial cell interactions are linked to vascular permeability via ICAM-1-mediated signaling. Am J Physiol Heart Circ Physiol 295: H969-H977, 2008.
40. Sumagin R, Prizant H, Lomakina E, Waugh RE, Sarelius IH. LFA-1 and Mac-1 define characteristically different intralumenal crawling and emigration patterns for monocytes and neutrophils in situ. J Immunol 185: 7057-7066, 2010.
41. Sumagin R, Sarelius IH. Intercellular adhesion molecule-1 enrichment near tricellular endothelial junctions is preferentially associated with leukocyte transmigration and signals for reorganization of these junctions to accommodate leukocyte passage. J Immunol 184: 5242-5252, 2010.
42. Sumagin R, Sarelius IH. A role for ICAM-1 in maintenance of leukocyte- endothelial cell rolling interactions in inflamed arterioles. Am J Physiol Heart Circ Physiol 293: H2786-H2798, 2007.
43. Sumagin R, Sarelius IH. TNF-α activation of arterioles and venules alters distribution and levels of ICAM-1 and affects leukocyte-endothelial cell interactions. Am J Physiol Heart Circ Physiol 291: H2116-H2125, 2006.
44. Tilghman RW, Hoover RL. The Src-cortactin pathway is required for clustering of E-selectin and ICAM-1 in endothelial cells. FASEB J 16: 1257-1259, 2002.
45. Van Buul JD, Allingham MJ, Samson T, Meller J, Boulter E, Garcia- Mata R, Burridge K. RhoG regulates endothelial apical cup assembly downstream from ICAM1 engagement and is involved in leukocyte trans-endothelial migration. J Cell Biol 178: 1279-1293, 2007.
46. Van Buul JD, van Rijssel J, van Alphen FP, Hoogenboezem M, Tol S, Hoeben KA, van Marle J, Mul EP, Hordijk PL. Inside-out regulation of ICAM-1 dynamics in TNF-alpha-activated endothelium. PLoS One 5: e11336, 2010.
47. Venkiteswaran K, Xiao K, Summers S, Calkins CC, Vincent PA, Pumiglia K, Kowalczyk AP. Regulation of endothelial barrier function and growth by VE-cadherin, plakoglobin, and beta-catenin. Am J Physiol Cell Physiol 283: C811-C821, 2002.
48. Wang Q, Doerschuk CM. The signaling pathways induced by neutrophilendothelial cell adhesion. Antioxid Redox Signal 4: 39-47, 2002.
49. Wang Q, Pfeiffer GR 2nd, Stevens T, Doerschuk CM. Lung microvascular and arterial endothelial cells differ in their responses to intercellular adhesion molecule-1 ligation. Am J Respir Crit Care Med 166: 872-77, 2002.
50. Williams MR, Luscinskas FW. Leukocyte rolling and adhesion via ICAM-1 signals to endothelial permeability. Focus on "Leukocyte rolling and adhesion both contribute to regulation of microvascular permeability to albumin via ligation of ICAM-1" (July 20, 2011). doi:10.1152/ajpcell.00250.2011.
51. Yang L, Froio RM, Sciuto TE, Dvorak AM, Alon R, Luscinskas FW. ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow. Blood 106: 584-592, 2005.
52. Yang L, Kowalski JR, Yacono P, Bajmoczi M, Shaw SK, Froio RM, Golan DE, Thomas SM, Luscinskas FW. Endothelial cell cortactin coordinates intercellular adhesion molecule-1 clustering and actin cytoskeleton remodeling during polymorphonuclear leukocyte adhesion and transmigration. J Immunol 177: 6440-6449, 2006.
53. Zhu L, He P. fMLP-stimulated release of reactive oxygen species from adherent leukocytes increases microvessel permeability. Am J Physiol Heart Circ Physiol 290: H365-H372, 2006.