Integrin activation by P-Rex1 is required for selectin-mediated slow leukocyte rolling and intravascular crawling

Blood

Volumn 121, Issue 12, 2013, Pages 2301-2310

  Herter, Jan M ^a,b   Rossaint, Jan ^a,b   Block, Helena ^a,b   Welch, Heidi ^c   Zarbock, Alexander ^a,b  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^c BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTEGRIN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; PROTEIN PREX 1; RAC PROTEIN; UNCLASSIFIED DRUG; CD11B ANTIGEN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INTERCELLULAR ADHESION MOLECULE 1; PREX1 PROTEIN, MOUSE;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE; IN VIVO STUDY; LEUKOCYTE ROLLING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEFICIENCY; REPERFUSION INJURY; SIGNAL TRANSDUCTION; ANIMAL; BLOOD VESSEL; C57BL MOUSE; CELL CULTURE; CELL STRAIN HL 60; DRUG EFFECT; GENETICS; HUMAN; IMMUNOLOGY; LEUKOCYTE; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ACUTE KIDNEY INJURY; ANIMALS; BLOOD VESSELS; CELLS, CULTURED; CHEMOTAXIS, LEUKOCYTE; E-SELECTIN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HL-60 CELLS; HUMANS; INTEGRINS; INTERCELLULAR ADHESION MOLECULE-1; LEUKOCYTE ROLLING; LEUKOCYTES; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MACROPHAGE-1 ANTIGEN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUTROPHIL INFILTRATION; REPERFUSION INJURY;

MLCS; MLOWN;

EID: 84877930031     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-09-457085     Document Type: Article

References (44)

1. Carman CV, Springer TA. Integrin avidity regulation: Are changes in affinity and conformation underemphasized?. Curr Opin Cell Biol. 2003;15(5):547-556.
2. Ley K, Laudanna C, Cybulsky MI, et al. Getting to the site of inflammation: The leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7(9): 678-689.
3. Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol. 2007;25:619-647.
4. Takagi J, Petre BM, Walz T, et al. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell. 2002;110(5):599-11.
5. Nishida N, Xie C, Shimaoka M, et al. Activation of leukocyte beta2 integrins by conversion from bent to extended conformations. Immunity. 2006;25(4): 583-594.
6. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell. 1994;76(2):301-314.
7. Zarbock A, Lowell CA, Ley K. Spleen tyrosine kinase Syk is necessary for E-selectin-induced alpha(L)beta(2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity. 2007;26(6):773-783.
8. Block H, Herter JM, Rossaint J, et al. Crucial role of SLP-76 and ADAP for neutrophil recruitment in mouse kidney ischemia-reperfusion injury. J Exp Med. 2012;209(2):407-421.
9. Zarbock A, Abram CL, Hundt M, et al. PSGL-1 engagement by E-selectin signals through Src kinase Fgr and ITAM adapters DAP12 and FcR gamma to induce slow leukocyte rolling. J Exp Med. 2008;205(10):2339-2347.
10. Kuwano Y, Spelten O, Zhang H, et al. Rolling on E- or P-selectin induces the extended but not high-affinity conformation of LFA-1 in neutrophils. Blood. 2010;116(4):617-624.
11. Mueller H, Stadtmann A, Van Aken H, et al. Tyrosine kinase Btk regulates E-selectinmediated integrin activation and neutrophil recruitment by controlling phospholipase C (PLC) gamma2 and PI3Kgamma pathways. Blood. 2010;115(15):3118-3127.
12. Zarbock A, Ley K, McEver RP, et al. Leukocyte ligands for endothelial selectins: Specialized glycoconjugates that mediate rolling and signaling under flow. Blood. 2011;118(26):6743-6751.
13. Stadtmann A, Brinkhaus L, Mueller H, et al. Rap1a activation by CalDAG-GEFI and p38 MAPK is involved in E-selectin-dependent slow leukocyte rolling. Eur J Immunol. 2011;41(7): 2074-2085.
14. Yago T, Shao B, Miner JJ, et al. E-selectin engages PSGL-1 and CD44 through a common signaling pathway to induce integrin alphaLbeta2- mediated slow leukocyte rolling. Blood. 2010; 116(3):485-494.
15. Campbell JJ, Hedrick J, Zlotnik A, et al. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science. 1998;279(5349): 381-384.
16. Lefort CT, Ley K. Neutrophil arrest by LFA-1 activation. Front Immunol. 2012;3:157.
17. Phillipson M, Heit B, Colarusso P, et al. Intraluminal crawling of neutrophils to emigration sites: A molecularly distinct process from adhesion in the recruitment cascade. J Exp Med. 2006;203(12):2569-2575.
18. Ryschich E, Kerkadze V, Lizdenis P, et al. Active leukocyte crawling in microvessels assessed by digital time-lapse intravital microscopy. J Surg Res. 2006;135(2):291-296.
19. Wojciechowski JC, Sarelius IH. Preferential binding of leukocytes to the endothelial junction region in venules in situ. Microcirculation. 2005; 12(4):349-359.
20. Lawson CD, Donald S, Anderson KE, et al. P-Rex1 and Vav1 cooperate in the regulation of formyl-methionyl-leucyl-phenylalanine-dependent neutrophil responses. J Immunol. 2011;186(3): 1467-1476.
21. Hill K, Welch HC. Purification of P-Rex1 from neutrophils and nucleotide exchange assay. Methods Enzymol. 2006;406:26-41.
22. Mayeenuddin LH, Garrison JC. Phosphorylation of P-Rex1 by the cyclic AMP-dependent protein kinase inhibits the phosphatidylinositiol (3,4,5)- trisphosphate and Gbetagamma-mediated regulation of its activity. J Biol Chem. 2006; 281(4):1921-1928.
23. Hill K, Krugmann S, Andrews SR, et al. Regulation of P-Rex1 by phosphatidylinositol (3,4,5)-trisphosphate and Gbetagamma subunits. J Biol Chem. 2005;280(6):4166-4173.
24. Welch HC, Condliffe AM, Milne LJ, et al. P-Rex1 regulates neutrophil function. Curr Biol. 2005; 15(20):1867-1873.
25. Faust N, Varas F, Kelly LM, et al. Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood. 2000;96(2):719-726.
26. Welch HC, Coadwell WJ, Ellson CD, et al. P-Rex1, a PtdIns(3,4,5)P3- and Gbetagammaregulated guanine-nucleotide exchange factor for Rac. Cell. 2002;108(6):809-821.
27. Spaargaren M, Beuling EA, Rurup ML, et al. The B cell antigen receptor controls integrin activity through Btk and PLCgamma2. J Exp Med. 2003; 198(10):1539-1550.
28. Gomez-Rodriguez J, Readinger JA, Viorritto IC, et al. Tec kinases, actin, and cell adhesion. Immunol Rev. 2007;218:45-64.
29. Shimaoka M, Xiao T, Liu JH, et al. Structures of the alpha L I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell. 2003;112(1):99-111.
30. Phillipson M, Heit B, Parsons SA, et al. Vav1 is essential for mechanotactic crawling and migration of neutrophils out of the inflamed microvasculature. J Immunol. 2009;182(11): 6870-6878.
31. Diamond MS, Springer TA. A subpopulation of Mac-1 (CD11b/CD18) molecules mediates neutrophil adhesion to ICAM-1 and fibrinogen. J Cell Biol. 1993;120(2):545-556.
32. Walzog B, Weinmann P, Jeblonski F, et al. A role for beta(2) integrins (CD11/CD18) in the regulation of cytokine gene expression of polymorphonuclear neutrophils during the inflammatory response. FASEB J. 1999;13(13): 1855-1865.
33. Pinho V, Russo RC, Amaral FA, et al. Tissue- and stimulus-dependent role of phosphatidylinositol 3-kinase isoforms for neutrophil recruitment induced by chemoattractants in vivo. J Immunol. 2007;179(11):7891-7898.
34. Simoẽs S, Denholm B, Azevedo D, et al. Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development. 2006;133(21):4257-4267.
35. Kempf T, Zarbock A, Widera C, et al. GDF-15 is an inhibitor of leukocyte integrin activation required for survival after myocardial infarction in mice. Nat Med. 2011;17(5):581-588.
36. Gakidis MA, Cullere X, Olson T, et al. Vav GEFs are required for beta2 integrin-dependent functions of neutrophils. J Cell Biol. 2004;166(2): 273-282.
37. Roberts AW, Kim C, Zhen L, et al. Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity. 1999;10(2):183-196.
38. Glogauer M, Marchal CC, Zhu F, et al. Rac1 deletion in mouse neutrophils has selective effects on neutrophil functions. J Immunol. 2003; 170(11):5652-5657.
39. Gu Y, Filippi MD, Cancelas JA, et al. Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Science. 2003; 302(5644):445-449.
40. Singbartl K, Ley K. Leukocyte recruitment and acute renal failure. J Mol Med (Berl). 2004;82(2): 91-101.
41. Bonventre JV, Weinberg JM. Recent advances in the pathophysiology of ischemic acute renal failure. J Am Soc Nephrol. 2003;14(8):2199-2210.
42. Singbartl K, Ley K. Protection from ischemiareperfusion induced severe acute renal failure by blocking E-selectin. Crit Care Med. 2000;28(7): 2507-2514.
43. Altavilla D, Squadrito F, Ioculano M, et al. E-selectin in the pathogenesis of experimental myocardial ischemia-reperfusion injury. Eur J Pharmacol. 1994;270(1):45-51.
44. Eltzschig HK, Carmeliet P. Hypoxia and inflammation. N Engl J Med. 2011;364(7): 656-665.