Src-family kinases: Rheostats of immune cell signaling

Molecular Immunology

Volumn 41, Issue 6-7, 2004, Pages 631-643

  Lowell, Clifford A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cytokines; Immunoreceptor signaling; Integrins; ITAM; ITIM

Indexed keywords

ADAPTOR PROTEIN; HEMATOPOIETIC CELL KINASE; INTEGRIN; PROTEIN KINASE BLK; PROTEIN KINASE FGR; PROTEIN KINASE FYN; PROTEIN KINASE LCK; PROTEIN KINASE LYN; PROTEIN KINASE YES; PROTEIN KINASE YRK; PROTEIN SUBUNIT; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

B LYMPHOCYTE; CELL INTERACTION; DENDRITIC CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEFECT; ENZYME STRUCTURE; EOSINOPHIL; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; KNOCKOUT GENE; KNOCKOUT MOUSE; LEUKOCYTE; MACROPHAGE; MAST CELL; MOLECULE; MONOCYTE; MUTANT; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; OSTEOCLAST; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THROMBOCYTE;

EID: 3042615397     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2004.04.010     Document Type: Article

References (105)

1. Ardouin L., Bracke M., Mathiot A., Pagakis S.N., Norton T., Hogg N., Tybulewicz V.L. Vav1 transduces TCR signals required for LFA-1 function and cell polarization at the immunological synapse. Eur. J. Immunol. 33:2003;790-797
2. Arias-Salgado E.G., Lizano S., Sarkar S., Brugge J.S., Ginsberg M.H., Shattil S.J. Src kinase activation by direct interaction with the integrin β cytoplasmic domain. Proc. Natl. Acad. Sci. U.S.A. 100:2003;13298-13302
3. Awasthi-Kalia M., Schnetkamp P.P., Deans J.P. Differential effects of filipin and methyl-beta-cyclodextrin on B cell receptor signaling. Biochem. Biophys. Res. Commun. 287:2001;77-82
4. Barlic J., Andrews J.D., Kelvin A.A., Bosinger S.E., DeVries M.E., Xu L., Dobransky T., Feldman R.D., Ferguson S.S., Kelvin D.J. Regulation of tyrosine kinase activation and granule release through β-arrestin by CXCRI. Nat. Immunol. 1:2000;227-233
5. Caveggion E., Continolo S., Pixley F.J., Stanley E.R., Bowtell D.D., Lowell C.A., Berton G. Expression and tyrosine phosphorylation of Cbl regulates macrophage chemokinetic and chemotactic movement. J. Cell. Physiol. 195:2003;276-289
6. Chan V.W., Mecklenbrauker I., Su I., Texido G., Leitges M., Carsetti R., Lowell C.A., Rajewsky K., Miyake K., Tarakhovsky A. The molecular mechanism of B cell activation by toll-like receptor protein RP-105. J. Exp. Med. 188:1998;93-101
7. Chu D.H., van Oers N.S., Malissen M., Harris J., Elder M., Weiss A. Pre-T cell receptor signals are responsible for the down-regulation of Syk protein tyrosine kinase expression. J. Immunol. 163:1999;2610-2620
8. Cowen M.S., Schumann G., Yagi T., Spanagel R. Role of Fyn tyrosine kinase in ethanol consumption by mice. Alcohol Clin. Exp. Res. 27:2003;1213-1219
9. Davidson D., Bakinowski M., Thomas M.L., Horejsi V., Veillette A. Phosphorylation-dependent regulation of T-cell activation by PAG/Cbp, a lipid raft-associated transmembrane adaptor. Mol. Cell. Biol. 23:2003;2017-2028
10. De Franceschi L., Fumagalli L., Olivieri O., Corrocher R., Lowell C.A., Berton G. Deficiency of Src family kinases Fgr and Hck results in activation of erythrocyte K/Cl cotransport. J. Clin. Invest. 99:1997;220-227
11. DeFranco A.L., Chan V.W., Lowell C.A. Positive and negative roles of the tyrosine kinase Lyn in B cell function. Semin. Immunol. 10:1998;299-307
12. Dykstra M., Cherukuri A., Sohn H.W., Tzeng S.J., Pierce S.K. Location is everything: lipid rafts and immune cell signaling. Annu. Rev. Immunol. 21:2003;457-481
13. Ernst M., Inglese M., Scholz G.M., Harder K.W., Clay F.J., Bozinovski S., Waring P., Darwiche R., Kay T., Sly P., Collins R., Turner D., Hibbs M.L., Anderson G.P., Dunn A.R. Constitutive activation of the SRC family kinase Hck results in spontaneous pulmonary inflammation and an enhanced innate immune response. J. Exp. Med. 196:2002;589-604
14. Fang D., Wang H.Y., Fang N., Altman Y., Elly C., Liu Y.C. Cbl-b, a RING-type E3 ubiquitin ligase, targets phosphatidylinositol 3-kinase for ubiquitination in T cells. J. Biol. Chem. 276:2001;4872-4878
15. lck up-regulates VLA-4 integrin affinity. Implications for rapid spontaneous and chemokine-triggered T cell adhesion to VCAM-1 and fibronectin. J. Biol. Chem. 276:2001;13891-13901
16. Fitzer-Attas C.J., Lowry M., Crowley M.T., Finn A.J., Meng F., DeFranco A.L., Lowell C.A. Fcgamma receptor-mediated phagocytosis in macrophages lacking the Src family tyrosine kinases Hck, Fgr, and Lyn. J. Exp. Med. 191:2000;669-682
17. Fuhlbrigge R.C., Chaplin D.D., Kiely J.M., Unanue E.R. Regulation of interleukin 1 gene expression by adherence and lipopolysaccharide. J. Immunol. 138:1987;3799-3802
18. Gardai S., Whitlock B.B., Helgason C., Ambruso D., Fadok V., Bratton D., Henson P.M. Activation of SHIP by NADPH oxidase-stimulated Lyn leads to enhanced apoptosis in neutrophils. J. Biol. Chem. 277:2002;5236-5246
19. Gresham H.D., Dale B.M., Potter J.W., Chang P.W., Vines C.M., Lowell C.A., Lagenaur C.F., Willman C.L. Negative regulation of phagocytosis in murine macrophages by the Src kinase family member. Fgr. J. Exp. Med. 191:2000;515-528
20. Grishin A., Sinha S., Roginskaya V., Boyer M.J., Gomez-Cambronero J., Zuo S., Kurosaki T., Romero G., Corey S.J. Involvement of Shc and Cbl-PI 3-kinase in Lyn-dependent proliferative signaling pathways for G-CSF. Oncogene. 19:2000;97-105
21. Gupta N., DeFranco A.L. Visualizing lipid raft dynamics and early signaling events during antigen receptor-mediated B-lymphocyte activation. Mol. Biol. Cell. 14:2003;432-444
22. Harder K.W., Moller N.P., Peacock J.W., Jirik F.R. Protein-tyrosine phosphatase alpha regulates Src family kinases and alters cell-substratum adhesion. J. Biol. Chem. 273:1998;31890-31900
23. Harder K.W., Parsons L.M., Armes J., Evans N., Kountouri N., Clark R., Quilici C., Grail D., Hodgson G.S., Dunn A.R., Hibbs M.L. Gain- and loss-of-function Lyn mutant mice define a critical inhibitory role for Lyn in the myeloid lineage. Immunity. 15:2001;603-615
24. Hermiston M.L., Xu Z., Majeti R., Weiss A. Reciprocal regulation of lymphocyte activation by tyrosine kinases and phosphatases. J. Clin. Invest. 109:2002;9-14
25. Hermiston M.L., Xu Z., Weiss A. CD45: a critical regulator of signaling thresholds in immune cells. Annu. Rev. Immunol. 21:2003;107-137
26. Hernandez-Hansen V., Mackay G.A., Lowell C.A., Wilson B.S., Oliver J.M. The Src kinase Lyn is a negative regulator of mast cell proliferation. J. Leukoc. Biol. 75:2003;143-151
27. Hibbs M.L., Harder K.W., Armes J., Kountouri N., Quilici C., Casagranda F., Dunn A.R., Tarlinton D.M. Sustained activation of Lyn tyrosine kinase in vivo leads to autoimmunity. J. Exp. Med. 196:2002;1593-1604
28. Hibbs M.L., Tarlinton D.M., Armes J., Grail D., Hodgson G., Maglitto R., Stacker S.A., Dunn A.R. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell. 83:1995;301-311
29. Ho L.H., Uehara T., Chen C.C., Kubagawa H., Cooper M.D. Constitutive tyrosine phosphorylation of the inhibitory paired Ig-like receptor PIR-B. Proc. Natl. Acad. Sci. U.S.A. 96:1999;15086-15090
30. Hogg N., Laschinger M., Giles K., McDowall A. T-cell integrins: more than just sticking points. J. Cell. Sci. 116:2003;4695-4705
31. fyn. J. Immunol. 159:1997;4806-4814
32. Hyduk S.J., Cybulsky M.I. Alpha 4 integrin signaling activates phosphatidylinositol 3-kinase and stimulates T cell adhesion to intercellular adhesion molecule-1 to a similar extent as CD3, but induces a distinct rearrangement of the actin cytoskeleton. J. Immunol. 168:2002;696-704
33. Irie-Sasaki J., Sasaki T., Penninger J.M. CD45 regulated signaling pathways. Curr. Top. Med. Chem. 3:2003;783-796
34. Janes P.W., Ley S.C., Magee A.I., Kabouridis P.S. The role of lipid rafts in T cell antigen receptor (TCR) signalling. Semin. Immunol. 12:2000;23-34
35. Jeschke M., Brandi M.L., Susa M. Expression of Src family kinases and their putative substrates in the human preosteoclastic cell line FLG 29.1. J. Bone Miner. Res. 13:1998;1880-1889
36. Kabuyama Y., Homma M.K., Kurosaki T., Homma Y. Early signaling events induced by 280-nm UV irradiation. Eur. J. Biochem. 269:2002;664-670
37. Katagiri K., Maeda A., Shimonaka M., Kinashi T. RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1. Nat. Immunol. 4:2003;741-748
38. Korade-Mirnics Z., Corey S.J. Src kinase-mediated signaling in leukocytes. J. Leukoc. Biol. 68:2000;603-613
39. Lago Paz F., Galgani M., D'Oro U., Matarese G., Masci A.M., Zappacosta S., Racioppi L. Modulation of CD45 tyrosine phosphatase activity by antigen. Eur. J. Immunol. 31:2001;777-782
40. Latour S., Chow L.M., Veillette A. Differential intrinsic enzymatic activity of Syk and Zap-70 protein-tyrosine kinases. J. Biol. Chem. 271:1996;22782-22790
41. Latour S., Veillette A. Proximal protein tyrosine kinases in immunoreceptor signaling. Curr. Opin. Immunol. 13:2001;299-306
42. Liang X., Nazarian A., Erdjument-Bromage H., Bornmann W., Tempst P., Resh M.D. Heterogeneous fatty acylation of Src family kinases with polyunsaturated fatty acids regulates raft localization and signal transduction. J. Biol. Chem. 276:2001;30987-30994
43. Liang X., Wisniewski D., Strife A., Shivakrupa, Clarkson B., Resh M.D. Phosphatidylinositol 3-kinase and Src family kinases are required for phosphorylation and membrane recruitment of Dok-1 in c-Kit signaling. J. Biol. Chem. 277:2002;13732-13738
44. Lindquist J.A., Simeoni L., Schraven B. Transmembrane adapters: attractants for cytoplasmic effectors. Immunol. Rev. 191:2003;165-182
45. Link D.C., Zutter M. The proto-oncogene c-fgr is expressed in normal mantle zone B lymphocytes and is developmentally regulated during myelomonocytic differentiation in vivo. Blood. 85:1995;472-479
46. Lock P., Ralph S., Stanley E., Boulet I., Ramsay R., Dunn A.R. Two isoforms of murine hck, generated by utilization of alternative translational initiation codons, exhibit different patterns of subcellular localization. Mol. Cell. Biol. 11:1991;4363-4370
47. Lowell C.A., Berton G. Integrin signal transduction in myeloid leukocytes. J. Leukoc. Biol. 65:1999;313-320
48. Lowell C.A., Fumagalli L., Berton G. Deficiency of Src family kinases p59/61hck and p58c-fgr results in defective adhesion-dependent neutrophil functions. J. Cell Biol. 133:1996;895-910
49. Ma Y.C., Huang X.Y. Novel regulation and function of Src tyrosine kinase. Cell. Mole. Life Sci. 59:2002;456-462
50. Marwali M.R., Rey-Ladino J., Dreolini L., Shaw D., Takei F. Membrane cholesterol regulates LFA-1 function and lipid raft heterogeneity. Blood. 102:2003;215-222
51. Melander F., Andersson T., Dib K. Fgr but not Syk tyrosine kinase is a target for β 2 integrin-induced c-Cbl-mediated ubiquitination in adherent human neutrophils. Biochem. J. 370:2003;687-694
52. Meng F., Lowell C.A. Aβ 1 integrin signaling pathway involving Src-family kinases, Cbl and PI-3 kinase is required for macrophage spreading and migration. EMBO J. 17:1998;4391-4403
53. Miller L.A., Hong J.J., Kinch M.S., Harrison M.L., Geahlen R.L. The engagement of b1 integrins on promonocytic cells promotes phosphorylation of Syk and formation of a protein complex containing Lyn and b1 integrin. Eur. J. Immunol. 29:1999;1426-1434
54. Miranti C.K., Leng L., Maschberger P., Brugge J.S., Shattil S.J. Identification of a novel integrin signaling pathway involving the kinase Syk and the guanine nucleotide exchange factor Vav1. Curr. Biol. 8:1998;1289-1299
55. Mocsai A., Jakus Z., Vantus T., Berton G., Lowell C.A., Ligeti E. Kinase pathways in chemoattractant-induced degranulation of neutrophils: the role of p38 mitogen-activated protein kinase activated by Src family kinases. J. Immunol. 164:2000;4321-4331
56. Mocsai A., Ligeti E., Lowell C.A., Berton G. Adhesion-dependent degranulation of neutrophils requires the Src family kinases Fgr and Hck. J. Immunol. 162:1999;1120-1126
57. Mocsai A., Zhou M., Meng F., Tybulewicz V.L., Lowell C.A. Syk is required for integrin signaling in neutrophils. Immunity. 16:2002;547-558
58. Modafferi E.F., Black D.L. Combinatorial control of a neuron-specific exon. RNA. 5:1999;687-706
59. Mustelin T., Tasken K. Positive and negative regulation of T-cell activation through kinases and phosphatases. Biochem. J. 371:2003;15-27
60. Newbrough S.A., Mócsai A., Clemens R.A., Wu J.N., Silverman M.A., Singer A.L., Lowell C.A., Koretzky G.A. SLP-76 regulates Fcγ receptor and integrin signaling in neutrophils. Immunity. 19:2003;761-769
61. Nijhuis E., Lammers J.W., Koenderman L., Coffer P.J. Src kinases regulate PKB activation and modulate cytokine and chemoattractant-controlled neutrophil functioning. J. Leukoc. Biol. 71:2002;115-124
62. Obergfell A., Eto K., Mócsai A., Buensuceso C., Moores S.L., Brugge J.S., Lowell C.A., Shattil S.J. Coordinate interactions of Csk, Src, and Syk kinases with αIIbβ3 initiate integrin signaling to the cytoskeleton. J. Cell Biol. 157:2002;265-275
63. Obergfell A., Judd B.A., del Pozo M.A., Schwartz M.A., Koretzky G.A., Shattil S.J. The molecular adapter SLP-76 relays signals from platelet integrin aIIbb3 to the actin cytoskeleton. J. Biol. Chem. 276:2001;5916-5923
64. cbl links c-Src and phosphatidylinositol 3'-kinase to the integrin signaling pathway. J. Biol. Chem. 272:1997;3780-3787
65. Parravicini V., Gadina M., Kovarova M., Odom S., Gonzalez-Espinosa C., Furumoto Y., Saitoh S., Samelson L.E., O'Shea J.J., Rivera J. Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat. Immunol. 3:2002;741-748
66. Pereira S., Lowell C. The Lyn tyrosine kinase negatively regulates neutrophil integrin signaling. J. Immunol. 171:2003;1319-1327
67. Peterson E.J. The TCR ADAPts to integrin-mediated cell adhesion. Immunol. Rev. 192:2003;113-121
68. Picard C., Gilles A., Pontarotti P., Olive D., Collette Y. Cutting edge: recruitment of the ancestral fyn gene during emergence of the adaptive immune system. J. Immunol. 168:2002;2595-2598
69. Porter J.C., Hogg N. Integrin cross talk: activation of lymphocyte function-associated antigen-1 on human T cells alters α4β1- and α5β1-mediated function. J. Cell Biol. 138:1997;1437-1447
70. Rane S.G., Reddy E.P. JAKs, STATs and Src kinases in hematopoiesis. Oncogene. 21:2002;3334-3358
71. Ravetch J.V., Lanier L.L. Immune inhibitory receptors. Science. 290:2000;84-89
72. Resh M.D. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta. 1451:1999;1-16
73. Rivera J., Cordero J.R., Furumoto Y., Luciano-Montalvo C., Gonzalez-Espinosa C., Kovarova M., Odom S., Parravicini V. Macromolecular protein signaling complexes and mast cell responses: a view of the organization of IgE-dependent mast cell signaling. Mol. Immunol. 38:2002;1253-1258
74. Robbins S.M., Quintrell N.A., Bishop J.M. Myristoylation and differential palmitoylation of the HCK protein-tyrosine kinases govern their attachment to membranes and association with caveolae. Mol. Cell Biol. 15:1995;3507-3515
75. Saijo K., Schmedt C., Su I.H., Karasuyama H., Lowell C.A., Reth M., Adachi T., Patke A., Santana A., Tarakhovsky A. Essential role of Src-family protein tyrosine kinases in NF-κB activation during B cell development. Nat. Immunol. 4:2003;274-279
76. Sampath R., Gallagher P.J., Pavalko F.M. Cytoskeletal interactions with the leukocyte integrin β2 cytoplasmic tail. Activation-dependent regulation of associations with talin and α-actinin. J. Biol. Chem. 273:1998;33588-33594
77. Sanjay A., Houghton A., Neff L., DiDomenico E., Bardelay C., Antoine E., Levy J., Gailit J., Bowtell D., Horne W.C., Baron R. Cbl associates with Pyk2 and Src to regulate Src kinase activity, αvβ3 integrin-mediated signaling, cell adhesion, and osteoclast motility. J. Cell Biol. 152:2001;181-195
78. Shakespeare W.C., Metcalf C.A. III, Wang Y., Sundaramoorthi R., Keenan T., Weigele M., Bohacek R.S., Dalgarno D.C., Sawyer T.K. Novel bone-targeted Src tyrosine kinase inhibitor drug discovery. Curr. Opin. Drug Discov. Dev. 6:2003;729-741
79. Shimizu Y. LFA-1: more than just T cell Velcro. Nat. Immunol. 4:2003;1052-1054
80. Shrivastava P., Katagiri T., Ogimoto M., Mizuno K., Yakura H. Dynamic regulation of Src-family kinases by CD45 in B cells. Blood. 103:2003;1425-1432
81. Sicheri F., Kuriyan J. Structures of Src-family tyrosine kinases. Curr. Opin. Struct. Biol. 7:1997;777-785
82. Smith A., Bracke M., Leitinger B., Porter J.C., Hogg N. LFA-1-induced T cell migration on ICAM-1 involves regulation of MLCK-mediated attachment and ROCK-dependent detachment. J. Cell Sci. 116:2003;3123-3133
83. Songyang Z., Cantley L.C. Recognition and specificity in protein tyrosine kinase-mediated signalling. Trends Biochem. Sci. 20:1995;470-475
84. Soriano P., Montgomery C., Geske R., Bradley A. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell. 64:1991;693-702
85. Stafford S., Lowell C., Sur S., Alam R. Lyn tyrosine kinase is important for IL-5-stimulated eosinophil differentiation. J. Immunol. 168:2002;1978-1983
86. Suen P.W., Ilic D., Caveggion E., Berton G., Damsky C.H., Lowell C.A. Impaired integrin-mediated signal transduction, altered cytoskeletal structure and reduced motility in Hck/Fgr deficient macrophages. J. Cell Sci. 112(Part 22):1999;4067-4078
87. dok-2 as a cytokine-inducible inhibitor of cell proliferation and signal transduction. EMBO J. 19:2000;5114-5422
88. Takagi J., Springer T.A. Integrin activation and structural rearrangement. Immunol. Rev. 186:2002;141-163
89. Tanaka S., Amling M., Neff L., Peyman A., Uhlmann E., Levy J.B., Baron R. c-Cbl is downstream of c-Src in a signalling pathway necessary for bone resorption. Nature. 383:1996;528-531
90. Thomas M.L., Brown E.J. Positive and negative regulation of Src-family membrane kinases by CD45. Immunol. Today. 20:1999;406-411
91. Tohyama Y., Katagiri K., Pardi R., Lu C., Springer T.A., Kinashi T. The critical cytoplasmic regions of the aL/b2 integrin in Rap1-induced adhesion and migration. Mol. Biol. Cell. 14:2003;2570-2582
92. Turner J.M., Brodsky M.H., Irving B.A., Levin S.D., Perlmutter R.M., Littman D.R. Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell. 60:1990;755-765
93. Urzainqui A., Serrador J.M., Viedma F., Yanez-Mo M., Rodriguez A., Corbi A.L., Alonso-Lebrero J.L., Luque A., Deckert M., Vazquez J., Sanchez-Madrid F. ITAM-based interaction of ERM proteins with Syk mediates signaling by the leukocyte adhesion receptor PSGL-1. Immunity. 17:2002;401-412
94. van Oers N.S., Lowin-Kropf B., Finlay D., Connolly K., Weiss A. Aab T cell development is abolished in mice lacking both Lck and Fyn protein tyrosine kinases. Immunity. 5:1996;429-436
95. Van Seventer G.A., Shimizu Y., Horgan K.J., Shaw S. The LFA-1 ligand ICAM-1 provides an important costimulatory signal for T cell receptor-mediated activation of resting T cells. J. Immunol. 144:1990;4579-4586
96. Vines C.M., Potter J.W., Xu Y., Geahlen R.L., Costello P.S., Tybulewicz V.L., Lowell C.A., Chang P.W., Gresham H.D., Willman C.L. Inhibition of β2 integrin receptor and Syk kinase signaling in monocytes by the Src family kinase Fgr. Immunity. 15:2001;507-519
97. Volkov Y., Long A., McGrath S., Ni Eidhin D., Kelleher D. Crucial importance of PKC-β(I) in LFA-1-mediated locomotion of activated T cells. Nat. Immunol. 2:2001;508-514
98. Willeke T., Behrens S., Scharffetter-Kochanek K., Gaehtgens P., Walzog B. AAb2 integrin (CD11/CD18)-mediated signaling involves tyrosine phosphorylation of c-Cbl in human neutrophils. J. Leuk. Biol. 68:2000;284-292
99. Woodside D.G., Obergfell A., Leng L., Wilsbacher J.L., Miranti C.K., Brugge J.S., Shattil S.J., Ginsberg M.H. Activation of Syk protein tyrosine kinase through interaction with integrin β cytoplasmic domains. Curr. Biol. 11:2001;1799-1804
100. Xavier R., Brennan T., Li Q., McCormack C., Seed B. Membrane compartmentation is required for efficient T cell activation. Immunity. 8:1998;723-732
101. Xu J., Wang F., Van Keymeulen A., Herzmark P., Straight A., Kelly K., Takuwa Y., Sugimoto N., Mitchison T., Bourne H.R. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell. 114:2003;201-214
102. dok in negative regulation of B cell receptor-mediated signaling. Genes Dev. 14:2000;11-16
103. Yazawa N., Fujimoto M., Sato S., Miyake K., Asano N., Nagai Y., Takeuchi O., Takeda K., Okochi H., Akira S., Tedder T.F., Tamaki K. CD19 regulates innate immunity by the toll-like receptor RP105 signaling in B lymphocytes. Blood. 102:2003;1374-1380
104. Yi T.L., Bolen J.B., Ihle J.N. Hematopoietic cells express two forms of lyn kinase differing by 21 amino acids in the amino terminus. Mol. Cell. Biol. 11:1991;2391-2398
105. Zell T., Warden C.S., Chan A.S., Cook M.E., Dell C.L., Hunt S.W., Shimizu Y. III Regulation of β1-integrin-mediated cell adhesion by the Cbl adaptor protein. Curr. Biol. 8:1998;814-822