ICAM-1-activated Src and eNOS signaling increase endothelial cell surface PECAM-1 adhesivity and neutrophil transmigration

Blood

Volumn 120, Issue 9, 2012, Pages 1942-1952

  Liu, Guoquan ^a   Place, Aaron T ^a   Chen, Zhenlong ^a   Brovkovych, Viktor M ^a   Vogel, Stephen M ^a,b   Muller, William A ^c   Skidgel, Randal A ^a,b   Malik, Asrar B ^a,b   Minshall, Richard D ^a,b  

^a UNIVERSITY OF ILLINOIS   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; PROTEIN; SRC PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL INFILTRATION; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 84865754557     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-12-397430     Document Type: Article

References (50)

1. Diep BA, Chan L, Tattevin P, et al. Polymorphonuclear leukocytes mediate Staphylococcus aureus Panton-Valentine leukocidin-induced lung inflammation and injury. Proc Natl Acad Sci U S A. 2010;107(12):5587-5592.
2. Lawson C, Wolf S. ICAM-1 signaling in endothelial cells. Pharmacol Rep. 2009;61(1):22-32.
3. Carman CV, Springer TA. A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J Cell Biol. 2004;167(2):377-388.
4. van Buul JD, Allingham MJ, Samson T, et al. RhoG regulates endothelial apical cup assembly downstream from ICAM1 engagement and is involved in leukocyte trans-endothelial migration. J Cell Biol. 2007;178(7):1279-1293.
5. Dasgupta B, Dufour E, Mamdouh Z, Muller WA. A novel and critical role for tyrosine 663 in platelet endothelial cell adhesion molecule-1 trafficking and transendothelial migration. J Immunol. 2009;182(8):5041-5051.
6. Muller WA. Mechanisms of leukocyte transendothelial migration. Annu Rev Pathol. 2011;6:323-344.
7. Pluskota E, Chen Y, D'Souza SE. Src homology domain 2-containing tyrosine phosphatase 2 associates with intercellular adhesion molecule 1 to regulate cell survival. J Biol Chem. 2000;275(39):30029-30036.
8. Liu G, Vogel SM, Gao X, et al. Src phosphorylation of endothelial cell surface intercellular adhesion molecule-1 mediates neutrophil adhesion and contributes to the mechanism of lung inflammation. Arterioscler Thromb Vasc Biol. 2011;31(6):1342-1350.
9. Amos C, Romero IA, Schultze C, et al. Crossinking of brain endothelial intercellular adhesion molecule (ICAM)-1 induces association of ICAM-1 with detergent-insoluble cytoskeletal fraction. Arterioscler Thromb Vasc Biol. 2001;21(5):810-816.
10. 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. 2002;166(6):872-877.
11. Etienne-Manneville S, Manneville JB,Adamson P, Wilbourn B, Greenwood J, Couraud PO. ICAM-1-coupled cytoskeletal rearrangements and trans-endothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J Immunol. 2000;165(6):3375-3383.
12. Wojciak-Stothard B, Williams L, Ridley AJ. Monocyte adhesion and spreading on human endothelial cells is dependent on Rho-regulated receptor clustering. J Cell Biol. 1999;145(6):1293-1307.
13. Adamson P, Etienne S, Couraud PO, Calder V, Greenwood J. Lymphocyte migration through brain endothelial cell monolayers involves signaling through endothelial ICAM-1 via a rhodependent pathway. J Immunol. 1999;162(5):2964-2973.
14. Wang Q, Doerschuk CM. The p38 mitogen-activated protein kinase mediates cytoskeletal remodeling in pulmonary microvascular endothelial cells upon intracellular adhesion molecule-1 ligation. J Immunol. 2001;166(11):6877-6884.
15. Wang Q, Pfeiffer GR 2nd, Gaarde WA. Activation of SRC tyrosine kinases in response to ICAM-1 ligation in pulmonary microvascular endothelial cells. J Biol Chem. 2003;278(48):47731-47743.
16. 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(6):4053-4064.
17. Durieu-Trautmann O, Chaverot N, Cazaubon S, Strosberg AD, Couraud PO. Intercellular adhesion molecule 1 activation induces tyrosine phosphorylation of the cytoskeleton-associated protein cortactin in brain microvessel endothelial cells. J Biol Chem. 1994;269(17):12536-12540.
18. Martinelli R, Gegg M, Longbottom R, Adamson P, Turowski P, Greenwood J. ICAM-1-mediated eNOS activation via calcium and AMPK is required for transendothelial lymphocyte migration. Mol Biol Cell. 2009;20(3):995-1005.
19. Sithu SD, English WR, Olson P, et al. Membrane-type 1-matrix metalloproteinase regulates intracellular adhesion molecule-1 (ICAM-1)-mediated monocyte transmigration. J Biol Chem. 2007;282(34):25010-25019.
20. Cunnick JM, Meng S, Ren Y, et al. Regulation of the mitogen-activated protein kinase signaling pathway by SHP2. J Biol Chem. 2002;277(11):9498-9504.
21. Maniatis NA, Brovkovych V, Allen SE, et al. Novel mechanism of endothelial nitric oxide synthase activation mediated by caveolae internalization in endothelial cells. Circ Res. 2006;99(8):870-877.
22. Lawson C, Ainsworth M, Yacoub M, Rose M. Ligation of ICAM-1 on endothelial cells leads to expression of VCAM-1 via a nuclear factor-kappaB-independent mechanism. J Immunol. 1999;162(5):2990-2996.
23. Hu G, Vogel SM, Schwartz DE, Malik AB, Minshall RD. Intercellular adhesion molecule-1- dependent neutrophil adhesion to endothelial cells induces caveolae-mediated pulmonary vascular hyperpermeability. Circ Res. 2008;102(12):e120-e131.
24. Cuzzocrea S, Mazzon E, Calabro G, et al. Inducible nitric oxide synthase-knockout mice exhibit resistance to pleurisy and lung injury caused by carrageenan. Am J Respir Crit Care Med. 2000;162(5):1859-1866.
25. Rao RM, Yang L, Garcia-Cardena G, Luscinskas FW. Endothelial-dependent mechanisms of leukocyte recruitment to the vascular wall. Circ Res. 2007;101(3):234-247.
26. Springer TA. Adhesion receptors of the immune system. Nature. 1990;346(6283):425-434.
27. Xu W, Harrison SC, Eck MJ. Three-dimensional structure of the tyrosine kinase c-Src. Nature. 1997;385:595-602.
28. Place AT, Chen Z, Bakhshi FR, Liu G, O'Bryan JP, Minshall RD. Cooperative role of Caveolin-1 and C-terminal Src kinase binding protein in C-terminal Src kinase-mediated negative regulation of c-Src. Mol Pharmacol. 2011;80(4):665-672.
29. 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(6736):601-605.
30. Youn JY, Wang T, Cai H. An ezrin/calpain/PI3K/ AMPK/eNOSs1179 signaling cascade mediating VEGF-dependent endothelial nitric oxide production. Circ Res. 2009;104(1):50-59.
31. Peairs A, Radjavi A, Davis S, et al. Activation of AMPK inhibits inflammation in MRL/lpr mouse mesangial cells. Clin Exp Immunol. 2009;156(3):542-551.
32. Wittchen ES. Endothelial signaling in paracellular and transcellular leukocyte transmigration. Front Biosci. 2009;14:2522-2545.
33. Newman PJ. Switched at birth: a new family for PECAM-1. J Clin Invest. 1999;103(1):5-9.
34. Ilan N, Madri JA. PECAM-1: old friend, new partners. Curr Opin Cell Biol. 2003;15(5):515-524.
35. Steiner O, Coisne C, Cecchelli R, et al. Differential roles for endothelial ICAM-1, ICAM-2, and VCAM-1 in shear-resistant T cell arrest, polarization, and directed crawling on blood-brain barrier endothelium. J Immunol. 2010;185(8):4846-4855.
36. Taylor BS, Kim YM, Wang Q, Shapiro RA, Billiar TR, Geller DA. Nitric oxide down-regulates hepatocyte-inducible nitric oxide synthase gene expression. Arch Surg. 1997;132(11):1177-1183.
37. Berendji-Grun D, Kolb-Bachofen V, Kroncke KD. Nitric oxide inhibits endothelial IL-1[beta]-induced ICAM-1 gene expression at the transcriptional level decreasing Sp1 and AP-1 activity. Mol Med. 2001;7(11):748-754.
38. Smart JE, Oppermann H, Czernilofsky AP, Purchio AF, Erikson RL, Bishop JM. Characterization of sites for tyrosine phosphorylation in the transforming protein of Rous sarcoma virus (pp60v-src) and its normal cellular homologue (pp60c-src). Proc Natl Acad Sci U S A. 1981;78(10):6013-6017.
39. Arcaro A, Aubert M, Espinosa del Hierro ME, et al. Critical role for lipid raft-associated Src kinases in activation of PI3K-Akt signalling. Cell Signal. 2007;19(5):1081-1092.
40. Burns AR, Zheng Z, Soubra SH, Chen J, Rumbaut RE. Transendothelial flow inhibits neutrophil transmigration through a nitric oxide-dependent mechanism: potential role for cleft shear stress. Am J Physiol Heart Circ Physiol. 2007;293(5):H2904-H2910.
41. Clancy RM, Leszczynska-Piziak J, Abramson SB. Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on the NADPH oxidase. J Clin Invest. 1992;90(3):1116-1121.
42. Van Uffelen BE, de Koster BM, Van den Broek PJ, Van Steveninck J, Elferink JG. Modulation of neutrophil migration by exogenous gaseous nitric oxide. J Leukoc Biol. 1996;60(1):94-100.
43. Isenberg JS. Inhibition of nitric oxide synthase (NOS) conversion of L-arginine to nitric oxide (NO) decreases low density mononuclear cell (LD MNC) trans-endothelial migration and cytokine output. J Surg Res. 2003;114(1):100-106.
44. Filaire M, Fadel E, Decante B, Seccatore F, Mazmanian GM, Herve P. Inhaled nitric oxide does not prevent postpneumonectomy pulmonary edema in pigs. J Thorac Cardiovasc Surg. 2007;133(3):770-774.
45. Sligh JE Jr, Ballantyne CM, Rich SS, et al. Inflammatory and immune responses are impaired in mice deficient in intercellular adhesion molecule 1. Proc Natl Acad Sci U S A. 1993;90(18):8529-8533.
46. Kevil CG, Orr AW, Langston W, et al. Intercellular adhesion molecule-1 (ICAM-1) regulates endothelial cell motility through a nitric pathway. J Biol Chem. 2004;279(18):19230-19238.
47. Kalra VK, Shen Y, Sultana C, Rattan V. Hypoxia induces PECAM-1 phosphorylation and transendothelial migration of monocytes. Am J Physiol. 1996;271(5):H2025-H2034.
48. Rattan V, Shen Y, Sultana C, Kumar D, Kalra VK. Glucose-induced transmigration of monocytes is linked to phosphorylation of PECAM-1 in cultured endothelial cells. Am J Physiol. 1996;271(4):E711-E717.
49. Dusserre N, L'Heureux N, Bell KS, et al. PECAM-1 interacts with nitric oxide synthase in human endothelial cells: implication for flow-induced nitric oxide synthase activation. Arterioscler Thromb Vasc Biol. 2004;24(10):1796-1802.
50. Couty JP, Rampon C, Leveque M, et al. PECAM-1 engagement counteracts ICAM-1-induced signaling in brain vascular endothelial cells. J Neurochem. 2007;103(2):793-801.