Crucial role of SLP-76 and ADAP for neutrophil recruitment in mouse kidney ischemia-reperfusion injury

Journal of Experimental Medicine

Volumn 209, Issue 2, 2012, Pages 407-421

  Block, Helena ^a,b   Herter, Jan M ^a,b   Rossaint, Jan ^a,b   Stadtmann, Anika ^a,b   Kliche, Stefanie ^c   Lowell, Clifford A ^d   Zarbock, Alexander ^a,b  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION AND DEGRANULATION PROMOTING ADAPTOR PROTEIN; BRUTON TYROSINE KINASE; CREATININE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; PERTUSSIS TOXIN; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PHOSPHOLIPASE C GAMMA2; PROTEIN; PROTEIN SH2; SH2 DOMAIN CONTAINING LEUKOCYTE PHOSPHOPROTEIN OF 76 KD; TUMOR NECROSIS FACTOR; TYROSINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL MODEL; ARTICLE; ATTENUATION; BINDING AFFINITY; CELL ADHESION; CELL ISOLATION; CELL SIZE; CELL STIMULATION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; EPITHELIUM CELL; EXTRAVASATION; HEMATOPOIETIC STEM CELL; IN VIVO STUDY; KIDNEY ISCHEMIA; KIDNEY TUBULE; LEUKOCYTE; LEUKOCYTE ROLLING; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; REPERFUSION INJURY; SHEAR RATE; SIGNAL TRANSDUCTION; VIRAL GENE DELIVERY SYSTEM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL LINE, TUMOR; CLASS IB PHOSPHATIDYLINOSITOL 3-KINASE; E-SELECTIN; GENETIC VECTORS; HUMANS; INTEGRINS; KIDNEY; LEUKOCYTE ROLLING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUTROPHILS; PERITONITIS; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEINS; PROTEIN-TYROSINE KINASES; REPERFUSION INJURY; RETROVIRIDAE; THIOGLYCOLATES; TRANSDUCTION, GENETIC;

EID: 84856893681     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20111493     Document Type: Article

References (71)

1. Abtahian, F., A. Guerriero, E. Sebzda, M.M. Lu, R. Zhou, A. Mocsai, E.E. Myers, B. Huang, D.G. Jackson, V.A. Ferrari, et al. 2003. Regulation of blood and lymphatic vascular separation by signaling proteins SLP-76 and Syk. Science. 299:247-251. http://dx.doi.org/10.1126/science.1079477
2. Altavilla, D., F. Squadrito, M. Ioculano, P. Canale, G.M. Campo, B. Zingarelli, and A.P. Caputi. 1994. E-selectin in the pathogenesis of experimental myocardial ischemia-reperfusion injury. Eur. J. Pharmacol. 270:45-51.
3. Baker, R.G., C.J. Hsu, D. Lee, M.S. Jordan, J.S. Maltzman, D.A. Hammer, T. Baumgart, and G.A. Koretzky. 2009. The adapter protein SLP-76 mediates " outside-in" integrin signaling and function in T cells. Mol. Cell. Biol. 29:5578-5589. http://dx.doi.org/10.1128/MCB.00283-09
4. Bezman, N.A., L. Lian, C.S. Abrams, L.F. Brass, M.L. Kahn, M.S. Jordan, and G.A. Koretzky. 2008. Requirements of SLP76 tyrosines in ITAM and integrin receptor signaling and in platelet function in vivo. J. Exp. Med. 205:1775-1788. http://dx.doi.org/10.1084/jem.20080240
5. Bonventre, J.V., and J.M. Weinberg. 2003. Recent advances in the pathophysiology of ischemic acute renal failure. J. Am. Soc. Nephrol. 14:2199-2210. http://dx.doi.org/10.1097/01.ASN.0000079785.13922.F6
6. Bubeck Wardenburg, J., C. Fu, J.K. Jackman, H. Flotow, S.E. Wilkinson, D.H. Williams, R. Johnson, G. Kong, A.C. Chan, and P.R. Findell. 1996. Phosphorylation of SLP-76 by the ZAP-70 protein-tyrosine kinase is required for T-cell receptor function. J. Biol. Chem. 271:19641- 19644. http://dx.doi.org/10.1074/jbc.271.33.19641
7. Bubeck Wardenburg, J., R. Pappu, J.Y. Bu, B. Mayer, J. Chernoff, D. Straus, and A.C. Chan. 1998. Regulation of PAK activation and the T cell cytoskeleton by the linker protein SLP-76. Immunity. 9:607-616. http://dx.doi.org/10.1016/S1074-7613(00)80658-5
8. Clemens, R.A., L.E. Lenox, T. Kambayashi, N. Bezman, J.S. Maltzman, K.E. Nichols, and G.A. Koretzky. 2007. Loss of SLP-76 expression within myeloid cells confers resistance to neutrophil-mediated tissue damage while maintaining effective bacterial killing. J. Immunol. 178:4606-4614.
9. Clements, J.L., J.R. Lee, B. Gross, B. Yang, J.D. Olson, A. Sandra, S.P. Watson, S.R. Lentz, and G.A. Koretzky. 1999. Fetal hemorrhage and platelet dysfunction in SLP-76-deficient mice. J. Clin. Invest. 103:19- 25. http://dx.doi.org/10.1172/JCI5317
10. da Silva, A.J., Z. Li, C. de Vera, E. Canto, P. Findell, and C.E. Rudd. 1997. Cloning of a novel T-cell protein FYB that binds FYN and SH2-domain-containing leukocyte protein 76 and modulates interleukin 2 production. Proc. Natl. Acad. Sci. USA. 94:7493-7498. http://dx.doi.org/10.1073/pnas.94.14.7493
11. Eltzschig, H.K., and P. Carmeliet. 2011. Hypoxia and inflammation. N. Engl. J. Med. 364:656-665. http://dx.doi.org/10.1056/NEJMra0910283
12. Fang, N., D.G. Motto, S.E. Ross, and G.A. Koretzky. 1996. Tyrosines 113, 128, and 145 of SLP-76 are required for optimal augmentation of NFAT promoter activity. J. Immunol. 157:3769-3773.
13. Faust, N., F. Varas, L.M. Kelly, S. Heck, and T. Graf. 2000. Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood. 96:719-726.
14. Geng, L., M. Raab, and C.E. Rudd. 1999. Cutting edge: SLP-76 cooperativity with FYB/FYN-T in the Up-regulation of TCR-driven IL-2 transcription requires SLP-76 binding to FYB at Tyr595 and Tyr651. J. Immunol. 163:5753-5757.
15. Geng, L., S. Pfister, S.K. Kraeft, and C.E. Rudd. 2001. Adaptor FYB (Fynbinding protein) regulates integrin-mediated adhesion and mediator release: Differential involvement of the FYB SH3 domain. Proc. Natl. Acad. Sci. USA. 98:11527-11532. http://dx.doi.org/10.1073/pnas.191378198
16. Green, C.E., D.N. Pearson, R.T. Camphausen, D.E. Staunton, and S.I. Simon. 2004. Shear-dependent capping of L-selectin and P-selectin glycoprotein ligand 1 by E-selectin signals activation of high-avidity beta2-integrin on neutrophils. J. Immunol. 172:7780-7790.
17. Griffiths, E.K., C. Krawczyk, Y.Y. Kong, M. Raab, S.J. Hyduk, D. Bouchard, V.S. Chan, I. Kozieradzki, A.J. Oliveira-Dos-Santos, A. Wakeham, et al. 2001. Positive regulation of T cell activation and integrin adhesion by the adapter Fyb/Slap. Science. 293:2260-2263. http://dx.doi.org/10.1126/science.1063397
18. Gross, B.S., J.R. Lee, J.L. Clements, M. Turner, V.L. Tybulewicz, P.R. Findell, G.A. Koretzky, and S.P. Watson. 1999. Tyrosine phosphorylation of SLP-76 is downstream of Syk following stimulation of the collagen receptor in platelets. J. Biol. Chem. 274:5963-5971. http://dx.doi.org/10.1074/jbc.274.9.5963
19. Heuer, K., A. Arbuzova, H. Strauss, M. Kofler, and C. Freund. 2005. The helically extended SH3 domain of the T cell adaptor protein ADAP is a novel lipid interaction domain. J. Mol. Biol. 348:1025-1035. http://dx.doi.org/10.1016/j.jmb.2005.02.069
20. Hidalgo, A., A.J. Peired, M.K. Wild, D. Vestweber, and P.S. Frenette. 2007. Complete identification of E-selectin ligands on neutrophils reveals distinct functions of PSGL-1, ESL-1, and CD44. Immunity. 26:477-489. http://dx.doi.org/10.1016/j.immuni.2007.03.011
21. Hogg, N., I. Patzak, and F. Willenbrock. 2011. The insider's guide to leukocyte integrin signalling and function. Nat. Rev. Immunol. 11:416-426. http://dx.doi.org/10.1038/nri2986
22. Horn, J., X. Wang, P. Reichardt, T.E. Stradal, N. Warnecke, L. Simeoni, M. Gunzer, D. Yablonski, B. Schraven, and S. Kliche. 2009. Src homology 2-domain containing leukocyte-specific phosphoprotein of 76 kDa is mandatory for TCR-mediated inside-out signaling, but dispensable for CXCR4-mediated LFA-1 activation, adhesion, and migration of T cells. J. Immunol. 183:5756-5767. http://dx.doi.org/10.4049/jimmunol.0900649
23. Jordan, M.S., A.L. Singer, and G.A. Koretzky. 2003. Adaptors as central mediators of signal transduction in immune cells. Nat. Immunol. 4:110-116. http://dx.doi.org/10.1038/ni0203-110
24. Jordan, M.S., J. Sadler, J.E. Austin, L.D. Finkelstein, A.L. Singer, P.L. Schwartzberg, and G.A. Koretzky. 2006. Functional hierarchy of the N-terminal tyrosines of SLP-76. J. Immunol. 176:2430-2438.
25. Jordan, M.S., J.E. Smith, J.C. Burns, J.E. Austin, K.E. Nichols, A.C. Aschenbrenner, and G.A. Koretzky. 2008. Complementation in trans of altered thymocyte development in mice expressing mutant forms of the adaptor molecule SLP76. Immunity. 28:359-369. http://dx.doi.org/10.1016/j.immuni.2008.01.010
26. Judd, B.A., P.S. Myung, L. Leng, A. Obergfell, W.S. Pear, S.J. Shattil, and G.A. Koretzky. 2000. Hematopoietic reconstitution of SLP-76 corrects hemostasis and platelet signaling through alpha IIb beta 3 and collagen receptors. Proc. Natl. Acad. Sci. USA. 97:12056-12061. http://dx.doi.org/10.1073/pnas.97.22.12056
27. Judd, B.A., P.S. Myung, A. Obergfell, E.E. Myers, A.M. Cheng, S.P. Watson, W.S. Pear, D. Allman, S.J. Shattil, and G.A. Koretzky. 2002. Differential requirement for LAT and SLP-76 in GPVI versus T cell receptor signaling. J. Exp. Med. 195:705-717. http://dx.doi.org/10.1084/jem.20011583
28. Kasirer-Friede, A., B. Moran, J. Nagrampa-Orje, K. Swanson, Z.M. Ruggeri, B. Schraven, B.G. Neel, G. Koretzky, and S.J. Shattil. 2007. ADAP is required for normal alphaIIbbeta3 activation by VWF/GP Ib-IX-V and other agonists. Blood. 109:1018-1025. http://dx.doi.org/10.1182/blood-2006-05-022301
29. Kempf, T., A. Zarbock, C. Widera, S. Butz, A. Stadtmann, J. Rossaint, M. Bolomini-Vittori, M. Korf-Klingebiel, L.C. Napp, B. Hansen, et al. 2011. GDF-15 is an inhibitor of leukocyte integrin activation required for survival after myocardial infarction in mice. Nat. Med. 17:581-588. http://dx.doi.org/10.1038/nm.2354
30. Kettner, A., V. Pivniouk, L. Kumar, H. Falet, J.S. Lee, R. Mulligan, and R.S. Geha. 2003. Structural requirements of SLP-76 in signaling via the high-affinity immunoglobulin E receptor (Fc epsilon RI) in mast cells. Mol. Cell. Biol. 23:2395-2406. http://dx.doi.org/10.1128/MCB.23.7.2395-2406.2003
31. Kliche, S., D. Breitling, M. Togni, R. Pusch, K. Heuer, X. Wang, C. Freund, A. Kasirer-Friede, G. Menasche, G.A. Koretzky, and B. Schraven. 2006. The ADAP/SKAP55 signaling module regulates T-cell receptor-mediated integrin activation through plasma membrane targeting of Rap1. Mol. Cell. Biol. 26:7130-7144. http://dx.doi.org/10.1128/MCB.00331-06
32. Koretzky, G.A., and P.S. Myung. 2001. Positive and negative regulation of T-cell activation by adaptor proteins. Nat. Rev. Immunol. 1:95-107. http://dx.doi.org/10.1038/35100523
33. Koretzky, G.A., F. Abtahian, and M.A. Silverman. 2006. SLP76 and SLP65: complex regulation of signalling in lymphocytes and beyond. Nat. Rev. Immunol. 6:67-78. http://dx.doi.org/10.1038/nri1750
34. Krause, M., A.S. Sechi, M. Konradt, D. Monner, F.B. Gertler, and J. Wehland. 2000. Fyn-binding protein (Fyb)/SLP-76-associated protein (SLAP), Ena/ vasodilator-stimulated phosphoprotein (VASP) proteins and the Arp2/3 complex link T cell receptor (TCR) signaling to the actin cytoskeleton. J. Cell Biol. 149:181-194. http://dx.doi.org/10.1083/jcb.149.1.181
35. Kuwano, Y., O. Spelten, H. Zhang, K. Ley, and A. Zarbock. 2010. Rolling on E- or P-selectin induces the extended but not high-affinity conformation of LFA-1 in neutrophils. Blood. 116:617-624. http://dx.doi.org/10.1182/blood-2010-01-266122
36. Lenox, L.E., T. Kambayashi, M. Okumura, C. Prieto, K. Sauer, R.M. Bunte, M.S. Jordan, G.A. Koretzky, and K.E. Nichols. 2009. Mutation of tyrosine 145 of lymphocyte cytosolic protein 2 protects mice from anaphylaxis and arthritis. J. Allergy Clin. Immunol. 124:1088-1098. http://dx.doi.org/10.1016/j.jaci.2009.08.038
37. 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. http://dx.doi.org/10.1038/nri2156
38. Ménasché, G., S. Kliche, E.J. Chen, T.E. Stradal, B. Schraven, and G. Koretzky. 2007. RIAM links the ADAP/SKAP-55 signaling module to Rap1, facilitating T-cell-receptor-mediated integrin activation. Mol. Cell. Biol. 27:4070-4081. http://dx.doi.org/10.1128/MCB.02011-06
39. Miner, J.J., L. Xia, T. Yago, J. Kappelmayer, Z. Liu, A.G. Klopocki, B. Shao, J.M. McDaniel, H. Setiadi, D.W. Schmidtke, and R.P. McEver. 2008. Separable requirements for cytoplasmic domain of PSGL-1 in leukocyte rolling and signaling under flow. Blood. 112:2035-2045. http://dx.doi.org/10.1182/blood-2008-04-149468
40. Mócsai, A., C.L. Abram, Z. Jakus, Y. Hu, L.L. Lanier, and C.A. Lowell. 2006. Integrin signaling in neutrophils and macrophages uses adaptors containing immunoreceptor tyrosine-based activation motifs. Nat. Immunol. 7:1326-1333. http://dx.doi.org/10.1038/ni1407
41. Motto, D.G., S.E. Ross, J. Wu, L.R. Hendricks-Taylor, and G.A. Koretzky. 1996. Implication of the GRB2-associated phosphoprotein SLP-76 in T cell receptor-mediated interleukin 2 production. J. Exp. Med. 183:1937-1943. http://dx.doi.org/10.1084/jem.183.4.1937
42. Mueller, H., A. Stadtmann, H. Van Aken, E. Hirsch, D. Wang, K. Ley, and A. Zarbock. 2010. Tyrosine kinase Btk regulates E-selectin-mediated integrin activation and neutrophil recruitment by controlling phospholipase C (PLC) gamma2 and PI3Kgamma pathways. Blood. 115:3118-3127. http://dx.doi.org/10.1182/blood-2009-11-254185
43. Murugan, R., and J.A. Kellum. 2011. Acute kidney injury: what's the prognosis? Nat. Rev. Nephrol. 7:209-217. http://dx.doi.org/10.1038/nrneph.2011.13
44. Musci, M.A., L.R. Hendricks-Taylor, D.G. Motto, M. Paskind, J. Kamens, C.W. Turck, and G.A. Koretzky. 1997. Molecular cloning of SLAP-130, an SLP-76-associated substrate of the T cell antigen receptor-stimulated protein tyrosine kinases. J. Biol. Chem. 272:11674-11677. http://dx.doi.org/10.1074/jbc.272.18.11674
45. Myung, P.S., G.S. Derimanov, M.S. Jordan, J.A. Punt, Q.H. Liu, B.A. Judd, E.E. Meyers, C.D. Sigmund, B.D. Freedman, and G.A. Koretzky. 2001. Differential requirement for SLP-76 domains in T cell development and function. Immunity. 15:1011-1026. http://dx.doi.org/10.1016/S1074-7613(01)00253-9
46. Nathan, C. 2006. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6:173-182. http://dx.doi.org/10.1038/nri1785
47. Newbrough, S.A., A. Mocsai, R.A. Clemens, J.N. Wu, M.A. Silverman, A.L. Singer, C.A. Lowell, and G.A. Koretzky. 2003. SLP-76 regulates Fcgamma receptor and integrin signaling in neutrophils. Immunity. 19:761-769. http://dx.doi.org/10.1016/S1074-7613(03)00305-4
48. O'Shea, J.J., and P.J. Murray. 2008. Cytokine signaling modules in inflammatory responses. Immunity. 28:477-487. http://dx.doi.org/10.1016/j.immuni.2008.03.002
49. Peterson, E.J., M.L. Woods, S.A. Dmowski, G. Derimanov, M.S. Jordan, J.N. Wu, P.S. Myung, Q.H. Liu, J.T. Pribila, B.D. Freedman, et al. 2001. Coupling of the TCR to integrin activation by Slap-130/Fyb. Science. 293:2263-2265. http://dx.doi.org/10.1126/science.1063486
50. Prorock, A.J., A. Hafezi-Moghadam, V.E. Laubach, J.K. Liao, and K. Ley. 2003. Vascular protection by estrogen in ischemia-reperfusion injury requires endothelial nitric oxide synthase. Am. J. Physiol. Heart Circ. Physiol. 284:H133-H140.
51. Raab, M., A.J. da Silva, P.R. Findell, and C.E. Rudd. 1997. Regulation of Vav-SLP-76 binding by ZAP-70 and its relevance to TCR zeta/CD3 induction of interleukin-2. Immunity. 6:155-164. http://dx.doi.org/10.1016/S1074-7613(00)80422-7
52. Raab, M., H. Kang, A. da Silva, X. Zhu, and C.E. Rudd. 1999. FYNT-FYB-SLP-76 interactions define a T-cell receptor zeta/CD3-mediated tyrosine phosphorylation pathway that up-regulates interleukin 2 transcription in T-cells. J. Biol. Chem. 274:21170-21179. http://dx.doi.org/10.1074/jbc.274.30.21170
53. Serhan, C.N., and J. Savill. 2005. Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6:1191-1197. http://dx.doi.org/10.1038/ni1276
54. Simon, S.I., Y. Hu, D. Vestweber, and C.W. Smith. 2000. Neutrophil tethering on E-selectin activates beta 2 integrin binding to ICAM-1 through a mitogen-activated protein kinase signal transduction pathway. J. Immunol. 164:4348-4358.
55. Singbartl, K., and K. Ley. 2000. Protection from ischemia-reperfusion induced severe acute renal failure by blocking E-selectin. Crit. Care Med. 28:2507- 2514. http://dx.doi.org/10.1097/00003246-200007000-00053
56. Singbartl, K., and K. Ley. 2004. Leukocyte recruitment and acute renal failure. J. Mol. Med. 82:91-101. http://dx.doi.org/10.1007/s00109-003-0498-8
57. Singbartl, K., S.A. Green, and K. Ley. 2000. Blocking P-selectin protects from ischemia/reperfusion-induced acute renal failure. FASEB J. 14:48-54.
58. Smith, M.L., T.S. Olson, and K. Ley. 2004. CXCR2- and E-selectin-induced neutrophil arrest during inflammation in vivo. J. Exp. Med. 200:935- 939. http://dx.doi.org/10.1084/jem.20040424
59. Stadtmann, A., L. Brinkhaus, H. Mueller, J. Rossaint, M. Bolomini-Vittori, W. Bergmeier, H. Van Aken, D.D. Wagner, C. Laudanna, K. Ley, and A. Zarbock. 2011. Rap1a activation by CalDAG-GEFI and p38 MAPK is involved in E-selectin-dependent slow leukocyte rolling. Eur. J. Immunol. 41:2074-2085. http://dx.doi.org/10.1002/eji.201041196
60. Su, Y.W., Y. Zhang, J. Schweikert, G.A. Koretzky, M. Reth, and J. Wienands. 1999. Interaction of SLP adaptors with the SH2 domain of Tec family kinases. Eur. J. Immunol. 29:3702-3711. http://dx.doi.org/10.1002/(SICI)1521-4141(199911)29:11<3702::AID-IMMU3702>3.0.CO;2-R
61. Thadhani, R., M. Pascual, and J.V. Bonventre. 1996. Acute renal failure. N. Engl. J. Med. 334:1448-1460. http://dx.doi.org/10.1056/NEJM199605303342207
62. Urzainqui, A., J.M. Serrador, F. Viedma, M. Yáñez-Mó, A. Rodríguez, A.L. Corbí, J.L. Alonso-Lebrero, A. Luque, M. Deckert, J. Vázquez, and F. Sánchez-Madrid. 2002. ITAM-based interaction of ERM proteins with Syk mediates signaling by the leukocyte adhesion receptor PSGL-1. Immunity. 17:401-412. http://dx.doi.org/10.1016/S1074-7613(02)00420-X
63. Veale, M., M. Raab, Z. Li, A.J. da Silva, S.K. Kraeft, S. Weremowicz, C.C. Morton, and C.E. Rudd. 1999. Novel isoform of lymphoid adaptor FYN-T-binding protein (FYB-130) interacts with SLP-76 and upregulates interleukin 2 production. J. Biol. Chem. 274:28427-28435. http://dx.doi.org/10.1074/jbc.274.40.28427
64. Wang, H., F.E. McCann, J.D. Gordan, X. Wu, M. Raab, T.H. Malik, D.M. Davis, and C.E. Rudd. 2004. ADAP-SLP-76 binding differentially regulates supramolecular activation cluster (SMAC) formation relative to T cell-APC conjugation. J. Exp. Med. 200:1063-1074. http://dx.doi.org/10.1084/jem.20040780
65. Wang, H.B., J.T. Wang, L. Zhang, Z.H. Geng, W.L. Xu, T. Xu, Y. Huo, X. Zhu, E.F. Plow, M. Chen, and J.G. Geng. 2007. P-selectin primes leukocyte integrin activation during inflammation. Nat. Immunol. 8:882-892. http://dx.doi.org/10.1038/ni1491
66. Yablonski, D., M.R. Kuhne, T. Kadlecek, and A. Weiss. 1998. Uncoupling of nonreceptor tyrosine kinases from PLC-gamma1 in an SLP-76-deficient T cell. Science. 281:413-416. http://dx.doi.org/10.1126/science.281.5375.413
67. Yago, T., B. Shao, J.J. Miner, L. Yao, A.G. Klopocki, K. Maeda, K.M. Coggeshall, and R.P. McEver. 2010. E-selectin engages PSGL-1 and CD44 through a common signaling pathway to induce integrin alphaLbeta2-mediated slow leukocyte rolling. Blood. 116:485-494. http://dx.doi.org/10.1182/blood-2009-12-259556
68. Zarbock, A., and K. Ley. 2008. Mechanisms and consequences of neutrophil interaction with the endothelium. Am. J. Pathol. 172:1-7. http://dx.doi.org/10.2353/ajpath.2008.070502
69. Zarbock, A., C.A. Lowell, and K. Ley. 2007a. Spleen tyrosine kinase Syk is necessary for E-selectin-induced alpha(L)beta(2) integrin-mediated rolling on intercellular adhesion molecule-1. Immunity. 26:773-783. http://dx.doi.org/10.1016/j.immuni.2007.04.011
70. Zarbock, A., M. Schmolke, S.G. Bockhorn, M. Scharte, K. Buschmann, K. Ley, and K. Singbartl. 2007b. The Duffy antigen receptor for chemokines in acute renal failure: A facilitator of renal chemokine presentation. Crit. Care Med. 35:2156-2163. http://dx.doi.org/10.1097/01.CCM.0000280570.82885.32
71. Zarbock, A., C.L. Abram, M. Hundt, A. Altman, C.A. Lowell, and K. Ley. 2008. PSGL-1 engagement by E-selectin signals through Src kinase Fgr and ITAM adapters DAP12 and FcRγ to induce slow leukocyte rolling. J. Exp. Med. 205:2339-2347. http://dx.doi.org/10.1084/jem.20072660s. sadam2