G protein-coupled receptor kinase 2 moderates recruitment of THP-1 cells to the endothelium by limiting histamine-invoked weibel-palade body exocytosis

Journal of Thrombosis and Haemostasis

Volumn 12, Issue 2, 2014, Pages 261-272

  Stevenson, N L ^a   Martin Martin, B ^a   Freeman, J ^a   Kriston Vizi, J ^a   Ketteler, R ^a   Cutler, D F ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

G protein coupled receptor kinase 2; Human umbilical vein endothelial cells; P selectin; Von Willebrand factor; Weibel Palade bodies

Indexed keywords

CALCIUM; G PROTEIN COUPLED RECEPTOR KINASE 2; HISTAMINE; HISTAMINE RECEPTOR; PADGEM PROTEIN; SMALL INTERFERING RNA; VON WILLEBRAND FACTOR;

ARTICLE; BIOGENESIS; CALCIUM CELL LEVEL; CELL ADHESION; CELL LYSATE; CELL POPULATION; CELL SURFACE; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOTHELIUM; ENDOTHELIUM CELL; EXOCYTOSIS; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; MONOCYTE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; SECRETORY PATHWAY; STEADY STATE; THP 1 CELL; TRANS GOLGI NETWORK; UMBILICAL VEIN ENDOTHELIAL CELL; WEIBEL PALADE BODY;

BASE SEQUENCE; CELL LINE; DNA PRIMERS; ENDOTHELIUM; EXOCYTOSIS; G-PROTEIN-COUPLED RECEPTOR KINASE 2; HISTAMINE; HUMANS; POLYMERASE CHAIN REACTION; WEIBEL-PALADE BODIES;

EID: 84893542709     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12470     Document Type: Article

References (66)

1. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7: 678-89.
2. Vroon A, Heijnen CJ, Kavelaars A. GRKs and arrestins: regulators of migration and inflammation. J Leukoc Biol 2006; 6: 1214-21.
3. Shenoy SK, Lefkowitz RJ. β-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol Sci 2011; 32: 521-33.
4. Moore CA, Milano SK, Benovic JL. Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol 2007; 69: 451-82.
5. Pitcher JA, Freedman NJ, Lefkowitz RJ. G protein-coupled receptor kinases. Annu Rev Biochem 1998; 67: 653-92.
6. Penela P, Murga C, Ribas C, Salcedo A, Jurado-Pueyo M, Rivas V, Aymerich I, Mayor F. G protein-coupled receptor kinase 2 (GRK2) in migration and inflammation. Arch Physiol Biochem 2008; 114: 195-200.
7. Penela P, Murga C, Ribas C, Tutor AS, Peregrín S, Mayor F. Mechanisms of regulation of G protein-coupled receptor kinases (GRKs) and cardiovascular disease. Cardiovasc Res 2006; 69: 46-56.
8. Chuang TT, Sallese M, Ambrosini G, Parruti G, De Blasi A. High expression of beta-adrenergic receptor kinase in human peripheral blood leukocytes. Isoproterenol and platelet activating factor can induce kinase translocation. J Biol Chem 1992; 267: 6886-92.
9. Lombardi MS, Kavelaars A, Schedlowski M, Bijlsma JW, Okihara KL, van de Pol M, Ochsmann S, Pawlak C, Schmidt RE, Heijnen CJ. Decreased expression and activity of G-protein-coupled receptor kinases in peripheral blood mononuclear cells of patients with rheumatoid arthritis. FASEB J 1999; 13: 715-25.
10. Ramos-Ruiz R, Penela P, Penn RB, Mayor F Jr. Analysis of the human G protein-coupled receptor kinase 2 (GRK2) gene promoter: regulation by signal transduction systems in aortic smooth muscle cells. Circulation 2000; 101: 2083-9.
11. Lombardi MS, Kavelaars A, Penela P, Scholtens EJ, Roccio M, Schmidt RE, Schedlowski M, Mayor F Jr, Heijnen CJ. Oxidative stress decreases G protein-coupled receptor kinase 2 in lymphocytes via a calpain-dependent mechanism. Mol Pharmacol 2002; 62: 379-88.
12. Vroon A, Kavelaars A, Limmroth V, Lombardi MS, Goebel MU, van Dam AM, Caron MG, Schedlowski M, Heijnen CJ. G protein-coupled receptor kinase 2 in multiple sclerosis and experimental autoimmune encephalomyelitis. J Immunol 2005; 147: 4400-6.
13. Lombardi MS, Kavelaars A, Cobelens PM, Schmidt RE, Schedlowski M, Heijnen CJ. Adjuvant arthritis induces down-regulation of G protein-coupled receptor kinases in the immune system. J Immunol 2001; 166: 1635-40.
14. Eijkelkamp N, Heijnen CJ, Willemen HL, Deumens R, Joosten EA, Kleibeuker W, den Hartog IJ, van Velthoven CT, Nijboer C, Nassar MA, Dorn GW, Wood JN, Kavelaars A. GRK2: a novel cell-specific regulator of severity and duration of inflammatory pain. J Neurosci 2010; 30: 2138-49.
15. Vroon A, Heijnen CJ, Lombardi MS, Cobelens PM, Mayor F, Caron MG, Kavelaars A. Reduced GRK2 level in T cells potentiates chemotaxis and signaling in response to CCL4. J Leukoc Biol 2004; 75: 901-9.
16. Ciccarelli M, Sorriento D, Franco A, Fusco A, Del Giudice C, Annunziata R, Cipolletta E, Monti MG, Dorn GW 2nd, Trimarco B, Iaccarino G. Endothelial g protein-coupled receptor kinase 2 regulates vascular homeostasis through the control of free radical oxygen species. Arterioscler Thromb Vasc Biol 2013; 33: 2415-24.
17. Wagner DD, Olmsted JB, Marder VJ. Immunolocalization of von Willebrand protein in Weibel-Palade bodies of human endothelial cells. J Cell Biol 1982; 95: 355-60.
18. Metcalf DJ, Nightingale TD, Zenner HL, Lui-Roberts WW, Cutler DF. Formation and function of Weibel-Palade bodies. J Cell Sci 2008; 121: 19-27.
19. Michaux G, Cutler DF. How to roll an endothelial cigar: the biogenesis of Weibel-Palade bodies. Traffic 2004; 5: 69-78.
20. Hannah MJ, Williams R, Kaur J, Hewlett LJ, Cutler DF. Biogenesis of Weibel-Palade bodies. Semin Cell Dev Biol 2002; 13: 313-24.
21. Lui-Roberts WW, Collinson LM, Hewlett LJ, Michaux G, Cutler DF. An AP-1/clathrin coat plays a novel and essential role in forming the Weibel-Palade bodies of endothelial cells. J Cell Biol 2005; 170: 627-36.
22. Nightingale TD, Pattni K, Hume AN, Seabra MC, Cutler DF. Rab27a and MyRIP regulate the amount and multimeric state of VWF released from endothelial cells. Blood 2009; 113: 5010-8.
23. De Ceunynck K, De Meyer SF, Vanhoorelbeke K. Unwinding the von Willebrand factor strings puzzle. Blood 2012; 121: 270-7.
24. Nightingale T, Cutler D. The secretion of von Willebrand factor from endothelial cells; an increasingly complicated story. J Thromb Haemost 2013; 11: 192-201.
25. Doyle EL, Ridger V, Ferraro F, Turmaine M, Saftig P, Cutler DF. CD63 is an essential co-factor to leukocyte recruitment by endothelial P-selectin. Blood 2011; 118: 4265-73.
26. Moore KL, Patel KD, Bruehl RE, Li F, Johnson DA, Lichenstein HS, Cummings RD, Bainton DF, McEver RP. P-selectin glycoprotein ligand-1 mediates rolling of human neutrophils on P-selectin. J Cell Biol 1995; 128: 661-71.
27. Lang C, Sauter M, Szalay G, Racchi G, Grassi G, Rainaldi G, Mercatanti A, Lang F, Kandolf R, Klingel K. Connective tissue growth factor: a crucial cytokine-mediating cardiac fibrosis in ongoing enterovirus myocarditis. J Mol Med (Berl) 2008; 86: 49-60.
28. Connolly CN, Futter CE, Gibson A, Hopkins CR, Cutler DF. Transport into and out of the Golgi complex studied by transfecting cells with cDNAs encoding horseradish peroxidase. J Cell Biol 1994; 127: 641-52.
29. Lui-Roberts WW, Ferraro F, Nightingale TD, Cutler DF. Aftiphilin and gamma-synergin are required for secretagogue sensitivity of Weibel-Palade bodies in endothelial cells. Mol Biol Cell 2008; 19: 5072-81.
30. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008; 3: 1101-8.
31. Harrison-Lavoie KJ, Michaux G, Hewlett L, Kaur J, Hannah MJ, Lui-Roberts WW, Norman KE, Cutler DF. P-selectin and CD63 use different mechanisms for delivery to Weibel-Palade bodies. Traffic 2006; 7: 647-62.
32. Hannah MJ, Hume AN, Arribas M, Williams R, Hewlett LJ, Seabra MC, Cutler DF. Weibel-Palade bodies recruit Rab27 by a content-driven, maturation-dependent mechanism that is independent of cell type. J Cell Sci 2003; 116: 3939-48.
33. Wagner DD, Saffaripour S, Bonfanti R, Sadler JE, Cramer EM, Chapman B, Mayadas TN. Induction of specific storage organelles by von Willebrand factor propolypeptide. Cell 1991; 64: 403-13.
34. Wang JW, Eikenboom J. von Willebrand disease and Weibel-Palade bodies. Hamostaseologie 2010; 30: 150-5.
35. Wang JW, Bouwens EA, Pintao MC, Voorberg J, Safdar H, Valentijn KM, de Boer HC, Mertens K, Reitsma PH, Eikenboom J. Analysis of the storage and secretion of von Willebrand factor in blood outgrowth endothelial cells derived from patients with von Willebrand disease. Blood 2013; 121: 2762-72.
36. Wise RJ, Barr PJ, Wong PA, Kiefer MC, Brake AJ, Kaufman RJ. Expression of a human proprotein processing enzyme: correct cleavage of the von Willebrand factor precursor at a paired basic amino acid site. Proc Natl Acad Sci USA 1990; 87: 9378-82.
37. Iwata K, Luo J, Penn RB, Benovic JL. Bimodal regulation of the human H1 histamine receptor by G protein-coupled receptor kinase 2. J Biol Chem 2005; 280: 2197-204.
38. White JM, Rumbold GR. Behavioural effects of histamine and its antagonists: a review. Psychopharmacology 1988; 95: 1-14.
39. Kubes P, Kanwar S. Histamine induces leukocyte rolling in post-capillary venules. A P-selectin-mediated event. J Immunol 1994; 152: 3570-7.
40. Jiménez-Sainz MC, Murga C, Kavelaars A, Jurado-Pueyo M, Krakstad BF, Heijnen CJ, Mayor F, Aragay AM. G protein-coupled receptor kinase 2 negatively regulates chemokine signaling at a level downstream from G protein subunits. Mol Biol Cell 2006; 17: 25-31.
41. Hamilton KK, Sims PJ. Changes in cytosolic Ca2 + associated with von Willebrand factor release in human endothelial cells exposed to histamine. Study of microcarrier cell monolayers using the fluorescent probe indo-1. J Clin Invest 1987; 79: 600-8.
42. Tiruppathi C, Yan W, Sandoval R, Naqvi T, Pronin AN, Benovic JL, Malik AB. G protein-coupled receptor kinase-5 regulates thrombin-activated signaling in endothelial cells. Proc Natl Acad Sci USA 2000; 97: 7440-5.
43. Asako H, Kurose I, Wolf R, DeFrees S, Zheng ZL, Phillips ML, Paulson JC, Granger DN. Role of H1 receptors and P-selectin in histamine-induced leukocyte rolling and adhesion in postcapillary venules. J Clin Invest 1994; 93: 1508-15.
44. McEver RP. Selectins: lectins that initiate cell adhesion under flow. Curr Opin Cell Biol 2002; 14: 581-6.
45. Mayadas TN, Johnson RC, Rayburn H, Hynes RO, Wagner DD. Leukocyte rolling and extravasation are severely compromised in P selectin-deficient mice. Cell 1993; 74: 541-54.
46. Norman KE, Moore KL, McEver RP, Ley K. Leukocyte rolling in vivo is mediated by P-selectin glycoprotein ligand-1. Blood 1995; 86: 4417-21.
47. Johnson-Tidey RR, McGregor JL, Taylor PR, Poston RN. Increase in the adhesion molecule P-selectin in endothelium overlying atherosclerotic plaques. Coexpression with intercellular adhesion molecule-1. Am J Pathol 1994; 144: 952-61.
48. Detmar M, Brown LF, Schon MP, Elicker BM, Velasco P, Richard L, Fukumura D, Monsky W, Claffey KP, Jain RK. Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. J Invest Dermatol. 1998; 111: 1-6.
49. Telek G, Ducroc R, Scoazec JY, Pasquier C, Feldmann G, Roze C. Differential upregulation of cellular adhesion molecules at the sites of oxidative stress in experimental acute pancreatitis. J Surg Res 2001; 96: 56-67.
50. McMurray RW. Adhesion molecules in autoimmune disease. Semin Arthritis Rheum 1996; 25: 215-33.
51. Grober JS, Bowen BL, Ebling H, Athey B, Thompson CB, Fox DA, Stoolman LM. Monocyte-endothelial adhesion in chronic rheumatoid arthritis. In situ detection of selectin and integrin-dependent interactions. J Clin Invest 1993; 91: 2609-19.
52. Bullard DC, Mobley JM, Justen JM, Sly LM, Chosay JG, Dunn CJ, Lindsey JR, Beaudet AL, Staite ND. Acceleration and increased severity of collagen-induced arthritis in P-selectin mutant mice. J Immunol 1999; 163: 2844-9.
53. Pendu R, Terraube V, Christophe OD, Gahmberg CG, de Groot PG, Lenting PJ, Denis CV. P-selectin glycoprotein ligand 1 and beta2-integrins cooperate in the adhesion of leukocytes to von Willebrand factor. Blood 2006; 108: 3746-52.
54. Dole VS, Bergmeier W, Mitchell HA, Eichenberger SC, Wagner DD. Activated platelets induce Weibel-Palade-body secretion and leukocyte rolling in vivo: role of P-selectin. Blood 2005; 106: 2334-9.
55. Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest 2005; 115: 3378-84.
56. Yeo EL, Sheppard JA, Feuerstein IA. Role of P-selectin and leukocyte activation in polymorphonuclear cell adhesion to surface adherent activated platelets under physiologic shear conditions (an injury vessel wall model). Blood 1994; 83: 2498-507.
57. Giblin JP, Hewlett LJ, Hannah MJ. Basal secretion of von Willebrand factor from human endothelial cells. Blood 2008; 112: 957-64.
58. Ewenstein BM, Warhol MJ, Handin RI, Pober JS. Composition of the von Willebrand factor storage organelle (Weibel-Palade body) isolated from cultured human umbilical vein endothelial cells. J Cell Biol 1987; 104: 1423-33.
59. Howell GJ, Herbert SP, Smith JM, Mittar S, Ewan LC, Mohammed M, Hunter AR, Simpson N, Turner AJ, Zachary I, Walker JH, Ponnambalam S. Endothelial cell confluence regulates Weibel-Palade body formation. Mol Membr Biol 2004; 21: 413-21.
60. Takano M, Meneshian A, Sheikh E, Yamakawa Y, Wilkins KB, Hopkins EA, Bulkley GB. Rapid upregulation of endothelial P-selectin expression via reactive oxygen species generation. Am J Physiol Heart Circ Physiol 2002; 283: H2054-61.
61. Kim J, Ahn S, Ren XR, Whalen EJ, Reiter E, Wei H, Lefkowitz RJ. Functional antagonism of different G protein-coupled receptor kinases for beta-arrestin-mediated angiotensin II receptor signaling. Proc Natl Acad Sci USA 2005; 102: 1442-7.
62. Ren XR, Reiter E, Ahn S, Kim J, Chen W, Lefkowitz RJ. Different G protein-coupled receptor kinases govern G protein and beta-arrestin-mediated signaling of V2 vasopressin receptor. Proc Natl Acad Sci USA 2005; 102: 1448-53.
63. Fredericks ZL, Pitcher JA, Lefkowitz RJ. Identification of the G protein-coupled receptor kinase phosphorylation sites in the human beta2-adrenergic receptor. J Biol Chem 1996; 271: 13796-803.
64. Ge X, Low B, Liang M, Fu J. Angiotensin II directly triggers endothelial exocytosis via protein kinase C-dependent protein kinase D2 activation. J Pharmacol Sci 2007; 105: 168-76.
65. Vischer UM, Wollheim CB. Epinephrine induces von Willebrand factor release from cultured endothelial cells: involvement of cyclic AMP-dependent signalling in exocytosis. Thromb Haemost 1997; 77: 1182-8.
66. Kaufmann JE, Oksche A, Wollheim CB, Gunther G, Rosenthal W, Vischer UM. Vasopressin-induced von Willebrand factor secretion from endothelial cells involves V2 receptors and cAMP. J Clin Invest 2000; 106: 107-16.