Vasodilator-stimulated phosphoprotein regulates inside-out signaling of β2 integrins in neutrophils

Journal of Immunology

Volumn 184, Issue 12, 2010, Pages 6575-6584

  Deevi, Ravi K ^a   Koney Dash, Madhuri ^a   Kissenpfennig, Adrien ^a   Johnston, James A ^a   Schuh, Kai ^b   Walter, Ulrich ^b   Dib, Karim ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 3',5' CYCLIC MONOPHOSPHOTHIOATE; 8 (4 CHLOROPHENYLTHIO) CYCLIC GMP; AMMONIUM DERIVATIVE; BETA2 INTEGRIN; CHEMOATTRACTANT; CYCLIC GMP; FORMYLMETHIONYLLEUCYLPHENYLALANINE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INTEGRIN; N (3 (AMINOMETHYL) BENZYL)ACETAMIDINE; NITRIC OXIDE; RAP1 PROTEIN; SERINE; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN; ACTIN BINDING PROTEIN; BACTERIAL PROTEIN; CD18 ANTIGEN; CELL ADHESION MOLECULE; PHOSPHOPROTEIN; VASODILATOR-STIMULATED PHOSPHOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIUM; CELL DIFFERENTIATION; CELL LINE; CELL MEMBRANE; DOWNSTREAM PROCESSING; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; ISOMER; LEUKOCYTE; MOUSE; MUTANT; NEUTROPHIL; NONHUMAN; PLASMA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; PROTEIN TRANSPORT; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD18; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL ADHESION MOLECULES; GUANINE NUCLEOTIDE-RELEASING FACTOR 2; HUMANS; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; NEUTROPHILS; PHOSPHOPROTEINS; PROTEIN TRANSPORT; RAP1 GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 77953640601     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903910     Document Type: Article

References (51)

1. Evans, R., I. Patzak, L. Svensson, K. De Filippo, K. Jones, A. McDowall, and N. Hogg. 2009. Integrins in immunity. J. Cell Sci. 122: 215-225.
2. Ley, K., C. Laudanna, M. I. Cybulsky, and S. Nourshargh. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7: 678-689.
3. Caron, E., A. J. Self, and A. Hall. 2000. The GTPase Rap1 controls functional activation of macrophage integrin alphaMbeta2 by LPS and other inflammatory mediators. Curr. Biol. 10: 974-978.
4. M'Rabet, L., P. Coffer, F. Zwartkruis, B. Franke, A. W. Segal, L. Koenderman, and J. L. Bos. 1998. Activation of the small GTPase rap1 in human neutrophils. Blood 92: 2133-2140.
5. Bos, J. L., H. Rehmann, and A. Wittinghofer. 2007. GEFs and GAPs: critical elements in the control of small G proteins. Cell 129: 865-877.
6. Lafuente, E. M., A. A. van Puijenbroek, M. Krause, C. V. Carman, G. J. Freeman, A. Berezovskaya, E. Constantine, T. A. Springer, F. B. Gertler, and V. A. Boussiotis. 2004. RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev. Cell 7: 585-595.
7. Katagiri, K., A. Maeda, M. Shimonaka, and T. Kinashi. 2003. RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1. Nat. Immunol. 4: 741-748.
8. Pasvolsky, R., S. W. Feigelson, S. S. Kilic, A. J. Simon, G. Tal-Lapidot, V. Grabovsky, J. R. Crittenden, N. Amariglio, M. Safran, A. M. Graybiel, et al. 2007. A LAD-III syndrome is associated with defective expression of the Rap-1 activator CalDAG-GEFI in lymphocytes, neutrophils, and platelets. J. Exp. Med. 204: 1571-1582.
9. Svensson, L., K. Howarth, A. McDowall, I. Patzak, R. Evans, S. Ussar, M. Moser, A. Metin, M. Fried, I. Tomlinson, and N. Hogg. 2009. Leukocyte adhesion deficiency-III is caused by mutations in KINDLIN3 affecting integrin activation. Nat. Med. 15: 306-312.
10. Selvatici, R., S. Falzarano, A. Mollica, and S. Spisani. 2006. Signal transduction pathways triggered by selective formylpeptide analogues in human neutrophils. Eur. J. Pharmacol. 534: 1-11.
11. Pryzwansky, K. B., T. A. Wyatt, H. Nichols, and T. M. Lincoln. 1990. Compartmentalization of cyclic GMP-dependent protein kinase in formyl-peptide stimulated neutrophils. Blood 76: 612-618.
12. Wanikiat, P., D. F. Woodward, and R. A. Armstrong. 1997. Investigation of the role of nitric oxide and cyclic GMP in both the activation and inhibition of human neutrophils. Br. J. Pharmacol. 122: 1135-1145.
13. Schmidt, H. H., R. Seifert, and E. Böhme. 1989. Formation and release of nitric oxide from human neutrophils and HL-60 cells induced by a chemotactic peptide, platelet activating factor and leukotriene B4. FEBS Lett. 244: 357-360.
14. Werner, C. G., V. Godfrey, R. R. Arnold, G. L. Featherstone, D. Bender, J. Schlossmann, M. Schiemann, F. Hofmann, and K. B. Pryzwansky. 2005. Neutrophil dysfunction in guanosine 3′,5′-cyclic monophosphate-dependent protein kinase I-deficient mice. J. Immunol. 175: 1919-1929.
15. Nanamori, M., J. Chen, X. Du, and R. D. Ye. 2007. Regulation of leukocyte degranulation by cGMP-dependent protein kinase and phosphoinositide 3-kinase: potential roles in phosphorylation of target membrane SNARE complex proteins in rat mast cells. J. Immunol. 178: 416-427.
16. Reinhard, M., T. Jarchau, and U. Walter. 2001. Actin-based motility: stop and go with Ena/VASP proteins. Trends Biochem. Sci. 26: 243-249.
17. Bear, J. E., and F. B. Gertler. 2009. Ena/VASP: towards resolving a pointed controversy at the barbed end. J. Cell Sci. 122: 1947-1953.
18. Walders-Harbeck, B., S. Y. Khaitlina, H. Hinssen, B. M. Jockusch, and S. Illenberger. 2002. The vasodilator-stimulated phosphoprotein promotes actin polymerisation through direct binding to monomeric actin. FEBS Lett. 529: 275-280.
19. Butt, E., K. Abel, M. Krieger, D. Palm, V. Hoppe, J. Hoppe, and U. Walter. 1994. cAMP- and cGMP-dependent protein kinase phosphorylation sites of the focal adhesion vasodilator-stimulated phosphoprotein (VASP) in vitro and in intact human platelets. J. Biol. Chem. 269: 14509-14517.
20. Blume, C., P. M. Benz, U. Walter, J. Ha, B. E. Kemp, and T. Renné. 2007. AMP-activated protein kinase impairs endothelial actin cytoskeleton assembly by phosphorylating vasodilator-stimulated phosphoprotein. J. Biol. Chem. 282: 4601-4612.
21. Barzik, M., T. I. Kotova, H. N. Higgs, L. Hazelwood, D. Hanein, F. B. Gertler, and D. A. Schafer. 2005. Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J. Biol. Chem. 280: 28653-28662.
22. Böyum, A. 1968. Isolation of leucocytes from human blood. Further observations. Methylcellulose, dextran, and ficoll as erythrocyteaggregating agents. Scand. J. Clin. Lab. Invest. Suppl. 97: 31-50.
23. Hauser, W., K. P. Knobeloch, M. Eigenthaler, S. Gambaryan, V. Krenn, J. Geiger, M. Glazova, E. Rhode, I. Horak, U. Walter, and M. Zimmer. 1999. Megakaryocyte hyperplasia and enhanced agonist-induced platelet activation in vasodilator-stimulated phosphoprotein knockout mice. Proc. Natl. Acad. Sci. USA 96: 8120-8125.
24. Ellson, C. D., K. Davidson, G. J. Ferguson, R. O'Connor, L. R. Stephens, and P. T. Hawkins. 2006. Neutrophils from p40phox-/- mice exhibit severe defects in NADPH oxidase regulation and oxidant-dependent bacterial killing. J. Exp. Med. 203: 1927-1937.
25. Schaffner, W., and C. Weissmann. 1973. A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal. Biochem. 56: 502-514.
26. Dib, K., F. Melander, and T. Andersson. 2001. Role of p190RhoGAP in β 2 integrin regulation of RhoA in human neutrophils. J. Immunol. 166: 6311-6322. (Pubitemid 32440764)
27. Jenei, V., R. Deevi, C. Adams, L. Axelsson, D. G. Hirst, T. Andersson, and K. Dib. 2006. Nitric oxide produced in response to engagement of beta2 integrins on human neutrophils activates the monomeric GTPases Rap1 and Rap2 and promotes adhesion. J. Biol. Chem. 281: 35008-35020.
28. Garvey, E. P., J. A. Oplinger, E. S. Furfine, R. J. Kiff, F. Laszlo, B. J. Whittle, and R. G. Knowles. 1997. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J. Biol. Chem. 272: 4959-4963.
29. Butt, E., M. Eigenthaler, and H. G. Genieser. 1994. (Rp)-8-pCPT-cGMPS, a novel cGMP-dependent protein kinase inhibitor. Eur. J. Pharmacol. 269: 265-268.
30. 2 integrin affinity and mobility changes: differential regulation and roles in lymphocyte arrest under flow. Immunity 13: 759-769.
31. Dostmann, W. R., M. S. Taylor, C. K. Nickl, J. E. Brayden, R. Frank, and W. J. Tegge. 2000. Highly specific, membrane-permeant peptide blockers of cGMP-dependent protein kinase Ialpha inhibit NO-induced cerebral dilation. Proc. Natl. Acad. Sci. USA 97: 14772-14777.
32. Pedruzzi, E., M. Fay, C. Elbim, M. Gaudry, and M. A. Gougerot-Pocidalo. 2002. Differentiation of PLB-985 myeloid cells into mature neutrophils, shown by degranulation of terminally differentiated compartments in response to N-formyl peptide and priming of superoxide anion production by granulocyte-macrophage colony-stimulating factor. Br. J. Haematol. 117: 719-726.
33. Garthwaite, J., E. Southam, C. L. Boulton, E. B. Nielsen, K. Schmidt, and B. Mayer. 1995. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol. Pharmacol. 48: 184-188.
34. Franke, B., M. van Triest, K. M. de Bruijn, G. van Willigen, H. K. Nieuwenhuis, C. Negrier, J. W. Akkerman, and J. L. Bos. 2000. Sequential regulation of the small GTPase Rap1 in human platelets. Mol. Cell. Biol. 20: 779-785.
35. Gao, J.-L., and P. M. Murphy. 1993. Species and subtype variants of the N-formyl peptide chemotactic receptor reveal multiple important functional domains. J. Biol. Chem. 268: 25395-25401.
36. Smolenski, A., C. Bachmann, K. Reinhard, P. Hönig-Liedl, T. Jarchau, H. Hoschuetzky, and U. Walter. 1998. Analysis and regulation of vasodilator-stimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J. Biol. Chem. 273: 20029-20035.
37. Dent, E. W., A. V. Kwiatkowski, L. M. Mebane, U. Philippar, M. Barzik, D. A. Rubinson, S. Gupton, J. E. Van Veen, C. Furman, J. Zhang, et al. 2007. Filopodia are required for cortical neurite initiation. Nat. Cell Biol. 9: 1347-1359.
38. Giagulli, C., L. Ottoboni, E. Caveggion, B. Rossi, C. Lowell, G. Constantin, C. Laudanna, and G. Berton. 2006. The Src family kinases Hck and Fgr are dispensable for inside-out, chemoattractant-induced signaling regulating β 2 integrin affinity and valency in neutrophils, but are required for β 2 integrin-mediated outside-in signaling involved in sustained adhesion. J. Immunol. 177: 604-611. (Pubitemid 43939174)
39. Berton, G., S. R. Yan, L. Fumagalli, and C. A. Lowell. 1996. Neutrophil activation by adhesion: mechanisms and pathophysiological implications. Int. J. Clin. Lab. Res. 26: 160-177.
40. Yaroslavskiy, B. B., Y. Zhang, S. E. Kalla, V. García Palacios, A. C. Sharrow, Y. Li, M. Zaidi, C. Wu, and H. C Blair. 2005. NO-dependent osteoclast motility: reliance on cGMP-dependent protein kinase I and VASP. J. Cell Sci. 118: 5479-5487.
41. Kosonen, O., H. Kankaanranta, U. Malo-Ranta, and E. Moilanen. 1999. Nitric oxide-releasing compounds inhibit neutrophil adhesion to endothelial cells. Eur. J. Pharmacol. 382: 111-117.
42. Hwang, T.-L., H.-W. Hung, S.-H. Kao, C.-M. Teng, C.-C. Wu, and S. J.-S. Cheng. 2003. Soluble guanylyl cyclase activator YC-1 inhibits human neutrophil functions through a cGMP-independent but cAMP-dependent pathway. Mol. Pharmacol. 64: 1419-1427.
43. Bloemen, P. G., M. C. van den Tweel, P. A. Henricks, F. Engels, M. H. Kester, P. G. van de Loo, F. J. Blomjous, and F. P. Nijkamp. 1997. Increased cAMP levels in stimulated neutrophils inhibit their adhesion to human bronchial epithelial cells. Am. J. Physiol. 272: L580-L587.
44. Massberg, S., S. Grüner, I. Konrad, M. I. Garcia Arguinzonis, M. Eigenthaler, K. Hemler, J. Kersting, C. Schulz, I. Muller, F. Besta, et al. 2004. Enhanced in vivo platelet adhesion in vasodilator-stimulated phosphoprotein (VASP)-deficient mice. Blood 103: 136-142. (Pubitemid 38029929)
45. Aszódi, A., A. Pfeifer, M. Ahmad, M. Glauner, X. H. Zhou, L. Ny, K. E. Andersson, B. Kehrel, S. Offermanns, and R. Fässler. 1999. The vasodilator-stimulated phosphoprotein (VASP) is involved in cGMP- and cAMP-mediated inhibition of agonist-induced platelet aggregation, but is dispensable for smooth muscle function. EMBO J. 18: 37-48. (Pubitemid 29005021)
46. Henes, J., M. A. Schmit, J. C. Morote-Garcia, V. Mirakaj, D. Köhler, L. Glover, T. Eldh, U. Walter, J. Karhausen, S. P. Colgan, and P. Rosenberger. 2009. Inflammation-associated repression of vasodilator-stimulated phosphoprotein (VASP) reduces alveolar-capillary barrier function during acute lung injury. FASEB J. 23: 4244-4255.
47. Li, Z., X. Xi, M. Gu, R. Feil, R. D. Ye, M. Eigenthaler, F. Hofmann, and X. Du. 2003. A stimulatory role for cGMP-dependent protein kinase in platelet activation. Cell 112: 77-86. (Pubitemid 36106420)
48. Bergmeier, W., T. Goerge, H.-W. Wang, J. R. Crittenden, A. C. W. Baldwin, S. M. Cifuni, D. E. Housman, A. M. Graybiel, and D. D. Wagner. 2007. Mice lacking the signaling molecule CalDAG-GEFI represent a model for leukocyte adhesion deficiency type III. J. Clin. Invest. 117: 1699-1707.
49. Cifuni, S. M., D. D. Wagner, and W. Bergmeier. 2008. CalDAG-GEFI and protein kinase C represent alternative pathways leading to activation of integrin alphaIIbbeta3 in platelets. Blood 112: 1696-1703.
50. Crittenden, J. R., W. Bergmeier, Y. Zhang, C. L. Piffath, Y. Liang, D. D. Wagner, D. E. Housman, and A. M. Graybiel. 2004. CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat. Med. 10: 982-986.
51. Ohba, Y., K. Ikuta, A. Ogura, J. Matsuda, N. Mochizuki, K. Nagashima, K. Kurokawa, B. J. Mayer, K. Maki, J. Miyazaki, and M. Matsuda. 2001. Requirement for C3G-dependent Rap1 activation for cell adhesion and embryogenesis. EMBO J. 20: 3333-3341. (Pubitemid 32634341)