The roles of Dok family adapters in immunoreceptor signaling
Ryuichi Mashima,
Yukihiro Hishida,
Tohru Tezuka,
Yuji Yamanashi,
Ryuichi Mashima
Division of Genetics, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
Search for more papers by this authorYukihiro Hishida
Division of Genetics, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
Search for more papers by this authorTohru Tezuka
Division of Genetics, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
Search for more papers by this authorYuji Yamanashi
Division of Genetics, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
Search for more papers by this authorRyuichi Mashima,
Yukihiro Hishida,
Tohru Tezuka,
Yuji Yamanashi,
Ryuichi Mashima
Division of Genetics, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
Search for more papers by this authorYukihiro Hishida
Division of Genetics, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
Search for more papers by this authorTohru Tezuka
Division of Genetics, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
Search for more papers by this authorYuji Yamanashi
Division of Genetics, The Institute of Medical Science, The University of Tokyo, Tokyo, Japan.
Search for more papers by this authorYuji Yamanashi
Division of GeneticsThe Institute of Medical ScienceThe University of Tokyo4-6-1 Shirokanedai, Minato-kuTokyo 108-8639, JapanTel.: +81 3 6409 2115Fax: +81 3 6409 2116e-mail: [email protected]
Abstract
Summary: The mammalian Dok protein family has seven members (Dok-1–Dok-7). The Dok proteins share structural similarities characterized by the NH2-terminal pleckstrin homology and phosphotyrosine-binding domains followed by SH2 target motifs in the COOH-terminal moiety, indicating an adapter function. Indeed, Dok-1 was originally identified as a 62 kDa protein that binds with p120 rasGAP, a potent inhibitor of Ras, upon tyrosine phosphorylation by a variety of protein tyrosine kinases. Among the Dok family, only Dok-1, Dok-2, and Dok-3 are preferentially expressed in hematopoietic/immune cells. Dok-1 and its closest relative Dok-2 act as negative regulators of the Ras–Erk pathway downstream of many immunoreceptor-mediated signaling systems, and it is believed that recruitment of p120 rasGAP by Dok-1 and Dok-2 is critical to their negative regulation. By contrast, Dok-3 does not bind with p120 rasGAP. However, accumulating evidence has demonstrated that Dok-3 is a negative regulator of the activation of JNK and mobilization of Ca2+ in B-cell receptor-mediated signaling, where the interaction of Dok-3 with SHIP-1 and Grb2 appears to be important. Here, we review the physiological roles and underlying mechanisms of Dok family proteins.
References
- 1 Manning G, Young SL, Miller WT, Zhai Y. The protist, Monosiga brevicollis, has a tyrosine kinase signaling network more elaborate and diverse than found in any known metazoan. Proc Natl Acad Sci USA 2008; 105: 9674–9679.
- 2 Pincus D, Letunic I, Bork P, Lim WA. Evolution of the phospho-tyrosine signaling machinery in premetazoan lineages. Proc Natl Acad Sci USA 2008; 105: 9680–9684.
- 3 Ellis C, Moran M, McCormick F, Pawson T. Phosphorylation of GAP and GAP-associated proteins by transforming and mitogenic tyrosine kinases. Nature 1990; 343: 377–381.
- 4 DeClue JE, Vass WC, Johnson MR, Stacey DW, Lowy DR. Functional role of GTPase-activating protein in cell transformation by pp60v-src. Mol Cell Biol 1993; 13: 6799–6809.
- 5 Heidaran MA, et al. Activation of the colony-stimulating factor 1 receptor leads to the rapid tyrosine phosphorylation of GTPase-activating protein and activation of cellular p21ras. Oncogene 1992; 7: 147–152.
- 6 Gold MR, Crowley MT, Martin GA, McCormick F, DeFranco AL. Targets of B lymphocyte antigen receptor signal transduction include the p21ras GTPase-activating protein (GAP) and two GAP-associated proteins. J Immunol 1993; 150: 377–386.
- 7 Yamanashi Y, Baltimore D. Identification of the Abl- and rasGAP-associated 62 kDa protein as a docking protein, Dok. Cell 1997; 88: 205–211.
- 8 Carpino N, et al. p62dok: a constitutively tyrosine-phosphorylated, GAP-associated protein in chronic myelogenous leukemia progenitor cells. Cell 1997; 88: 197–204.
- 9 Yasuda T, et al. Role of Dok-1 and Dok-2 in myeloid homeostasis and suppression of leukemia. J Exp Med 2004; 200: 1681–1687.
- 10 Yasuda T, et al. Dok-1 and Dok-2 are negative regulators of T cell receptor signaling. Int Immunol 2007; 19: 487–495.
- 11 Lemay S, Davidson D, Latour S, Veillette A. Dok-3, a novel adapter molecule involved in the negative regulation of immunoreceptor signaling. Mol Cell Biol 2000; 20: 2743–2754.
- 12 Smith A, Wang J, Cheng CM, Zhou J, Weickert CS, Bondy CA. High-level expression of Dok-1 in neurons of the primate prefrontal cortex and hippocampus. J Neurosci Res 2004; 75: 218–224.
- 13 Zhao M, Janas JA, Niki M, Pandolfi PP, Van Aelst L. Dok-1 independently attenuates Ras/mitogen-activated protein kinase and Src/c-myc pathways to inhibit platelet-derived growth factor-induced mitogenesis. Mol Cell Biol 2006; 26: 2479–2489.
- 14 Hosooka T, et al. Dok1 mediates high-fat diet-induced adipocyte hypertrophy and obesity through modulation of PPAR-γ phosphorylation. Nat Med 2008; 14: 188–193.
- 15 Hiragun T, Peng Z, Beaven MA. Dexamethasone up-regulates the inhibitory adaptor protein Dok-1 and suppresses downstream activation of the mitogen-activated protein kinase pathway in antigen-stimulated RBL-2H3 mast cells. Mol Pharmacol 2005; 67: 598–603.
- 16 Suzu S, et al. p56dok−2 as a cytokine-inducible inhibitor of cell proliferation and signal transduction. EMBO J 2000; 19: 5114–5122.
- 17 Shinohara H, et al. Dok-1 and Dok-2 are negative regulators of lipopolysaccharide-induced signaling. J Exp Med 2005; 201: 333–339.
- 18 Grimm J, et al. Novel p62dok family members, dok-4 and dok-5, are substrates of the c-Ret receptor tyrosine kinase and mediate neuronal differentiation. J Cell Biol 2001; 154: 345–354.
- 19 Crowder RJ, Enomoto H, Yang M, Johnson EM, Jr, Milbrandt J. Dok-6, a Novel p62 Dok family member, promotes Ret-mediated neurite outgrowth. J Biol Chem 2004; 279: 42072–42081.
- 20 Favre C, Gerard A, Clauzier E, Pontarotti P, Olive D, Nunes JA. DOK4 and DOK5: new Dok-related genes expressed in human T cells. Genes Immun 2003; 4: 40–45.
- 21 Gerard A, et al. Dok-4 is a novel negative regulator of T cell activation. J Immunol 2009; 182: 7681–7689.
- 22 Okada K, et al. The muscle protein Dok-7 is essential for neuromuscular synaptogenesis. Science 2006; 312: 1802–1805.
- 23 Lemmon MA, Ferguson KM. Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J 2000; 350: 1–18.
- 24 Rebecchi MJ, Scarlata S. Pleckstrin homology domains: a common fold with diverse functions. Annu Rev Biophys Biomol Struct 1998; 27: 503–528.
- 25 Forman-Kay JD, Pawson T. Diversity in protein recognition by PTB domains. Curr Opin Struct Biol 1999; 9: 690–695.
- 26 Uhlik MT, Temple B, Bencharit S, Kimple AJ, Siderovski DP, Johnson GL. Structural and evolutionary division of phosphotyrosine binding (PTB) domains. J Mol Biol 2005; 345: 1–20.
- 27 Songyang Z. Recognition and regulation of primary-sequence motifs by signaling modular domains. Prog Biophys Mol Biol 1999; 71: 359–372.
- 28 Pawson T. Specificity in signal transduction: from phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 2004; 116: 191–203.
- 29 Uchida M, et al. Dok-4 regulates GDNF-dependent neurite outgrowth through downstream activation of Rap1 and mitogen-activated protein kinase. J Cell Sci 2006; 119: 3067–3077.
- 30 Shi L, et al. Dok5 is substrate of TrkB and TrkC receptors and involved in neurotrophin induced MAPK activation. Cell Signal 2006; 18: 1995–2003.
- 31 Inoue A, et al. Dok-7 activates the muscle receptor kinase MuSK and shapes synapse formation. Sci Signal 2009; 2: ra7.
- 32 Campbell SL, Khosravi-Far R, Rossman KL, Clark GJ, Der CJ. Increasing complexity of Ras signaling. Oncogene 1998; 17: 1395–1413.
- 33 Songyang Z, Yamanashi Y, Liu D, Baltimore D. Domain-dependent function of the rasGAP-binding protein p62Dok in cell signaling. J Biol Chem 2001; 276: 2459–2465.
- 34 Di Cristofano A, et al. Molecular cloning and characterization of p56dok−2 defines a new family of RasGAP-binding proteins. J Biol Chem 1998; 273: 4827–4830.
- 35 Woodring PJ, et al. c-Abl phosphorylates Dok1 to promote filopodia during cell spreading. J Cell Biol 2004; 165: 493–503.
- 36 Noguchi T, et al. Tyrosine phosphorylation of p62Dok induced by cell adhesion and insulin: possible role in cell migration. EMBO J 1999; 18: 1748–1760.
- 37 Inoue A, Yasuda T, Yamamoto T, Yamanashi Y. Dok-1 is a positive regulator of IL-4 signalling and IgE response. J Biochem 2007; 142: 257–263.
- 38 Master Z, et al. Dok-R binds c-Abl and regulates Abl kinase activity and mediates cytoskeletal reorganization. J Biol Chem 2003; 278: 30170–30179.
- 39 Van Slyke P, Coll ML, Master Z, Kim H, Filmus J, Dumont DJ. Dok-R mediates attenuation of epidermal growth factor-dependent mitogen-activated protein kinase and Akt activation through processive recruitment of c-Src and Csk. Mol Cell Biol 2005; 25: 3831–3841.
- 40 Cong F, Yuan B, Goff SP. Characterization of a novel member of the DOK family that binds and modulates Abl signaling. Mol Cell Biol 1999; 19: 8314–8325.
- 41 Honma M, et al. Dok-3 sequesters Grb2 and inhibits the Ras–Erk pathway downstream of protein-tyrosine kinases. Genes Cells 2006; 11: 143–151.
- 42 Robson JD, Davidson D, Veillette A. Inhibition of the Jun N-terminal protein kinase pathway by SHIP-1, a lipid phosphatase that interacts with the adaptor molecule Dok-3. Mol Cell Biol 2004; 24: 2332–2343.
- 43 Ng CH, Xu S, Lam KP. Dok-3 plays a nonredundant role in negative regulation of B-cell activation. Blood 2007; 110: 259–266.
- 44 Stork B, et al. Subcellular localization of Grb2 by the adaptor protein Dok-3 restricts the intensity of Ca2+ signaling in B cells. EMBO J 2007; 26: 1140–1149.
- 45 Shi N, et al. Structural basis for the specific recognition of RET by the Dok1 phosphotyrosine binding domain. J Biol Chem 2004; 279: 4962–4969.
- 46 Smith MJ, Hardy WR, Murphy JM, Jones N, Pawson T. Screening for PTB domain binding partners and ligand specificity using proteome-derived NPXY peptide arrays. Mol Cell Biol 2006; 26: 8461–8474.
- 47 Latour S, Gish G, Helgason CD, Humphries RK, Pawson T, Veillette A. Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nat Immunol 2001; 2: 681–690.
- 48 Sattler M, Verma S, Pride YB, Salgia R, Rohrschneider LR, Griffin JD. SHIP1, an SH2 domain containing polyinositol-5-phosphatase, regulates migration through two critical tyrosine residues and forms a novel signaling complex with DOK1 and CRKL. J Biol Chem 2001; 276: 2451–2458.
- 49 Dunant NM, Wisniewski D, Strife A, Clarkson B, Resh MD. The phosphatidylinositol polyphosphate 5-phosphatase SHIP1 associates with the dok1 phosphoprotein in bcr-Abl transformed cells. Cell Signal 2000; 12: 317–326.
- 50 Zhang Y, et al. Molecular basis of distinct interactions between Dok1 PTB domain and tyrosine-phosphorylated EGF receptor. J Mol Biol 2004; 343: 1147–1155.
- 51 Boulay I, Nemorin JG, Duplay P. Phosphotyrosine binding-mediated oligomerization of downstream of tyrosine kinase (Dok)-1 and Dok-2 is involved in CD2-induced Dok phosphorylation. J Immunol 2005; 175: 4483–4489.
- 52 Zhao M, Schmitz AA, Qin Y, Di Cristofano A, Pandolfi PP, Van Aelst L. Phosphoinositide 3-kinase-dependent membrane recruitment of p62dok is essential for its negative effect on mitogen-activated protein (MAP) kinase activation. J Exp Med 2001; 194: 265–274.
- 53 Lemmon MA. Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 2008; 9: 99–111.
- 54 Guittard G, et al. Dok-1 and Dok-2 adaptor molecules are regulated by phosphatidylinositol 5-phosphate production in T cells. J Immunol 2009; 182: 3974–3978.
- 55 Bedirian A, Baldwin C, Abe J, Takano T, Lemay S. Pleckstrin homology and phosphotyrosine-binding domain-dependent membrane association and tyrosine phosphorylation of Dok-4, an inhibitory adapter molecule expressed in epithelial cells. J Biol Chem 2004; 279: 19335–19349.
- 56 Fu G, et al. Constitutive plasma membrane targeting and microdomain localization of Dok5 studied by single-molecule microscopy. Biophys Chem 2008; 136: 13–18.
- 57 Kim N, et al. Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell 2008; 135: 334–342.
- 58 Zhang B, Luo S, Wang Q, Suzuki T, Xiong WC, Mei L. LRP4 serves as a coreceptor of agrin. Neuron 2008; 60: 285–297.
- 59 Beeson D, et al. Dok-7 mutations underlie a neuromuscular junction synaptopathy. Science 2006; 313: 1975–1978.
- 60 Palace J, et al. Clinical features of the DOK7 neuromuscular junction synaptopathy. Brain 2007; 130: 1507–1515.
- 61 Muller JS, et al. Phenotypical spectrum of DOK7 mutations in congenital myasthenic syndromes. Brain 2007; 130: 1497–1506.
- 62 Hamuro J, et al. Mutations causing DOK7 congenital myasthenia ablate functional motifs in Dok-7. J Biol Chem 2008; 283: 5518–5524.
- 63 Yamanashi Y, Higuch O, Beeson D. Dok-7/MuSK signaling and a congenital myasthenic syndrome. Acta Myol 2008; 27: 25–29.
- 64 Yamanashi Y, et al. Role of the rasGAP-associated docking protein p62dok in negative regulation of B cell receptor-mediated signaling. Genes Dev 2000; 14: 11–16.
- 65 Kurosaki T, Hikida M. Tyrosine kinases and their substrates in B lymphocytes. Immunol Rev 2009; 228: 132–148.
- 66 Tamir I, et al. The RasGAP-binding protein p62dok is a mediator of inhibitory FcγRIIB signals in B cells. Immunity 2000; 12: 347–358.
- 67 Coughlin JJ, Stang SL, Dower NA, Stone JC. RasGRP1 and RasGRP3 regulate B cell proliferation by facilitating B cell receptor-Ras signaling. J Immunol 2005; 175: 7179–7184.
- 68 Zheng Y, Liu H, Coughlin J, Zheng J, Li L, Stone JC. Phosphorylation of RasGRP3 on threonine 133 provides a mechanistic link between PKC and Ras signaling systems in B cells. Blood 2005; 105: 3648–3654.
- 69 Aiba Y, et al. Activation of RasGRP3 by phosphorylation of Thr-133 is required for B cell receptor-mediated Ras activation. Proc Natl Acad Sci USA 2004; 101: 16612–16617.
- 70 Imamura Y, et al. BLNK binds active H-Ras to promote B cell receptor-mediated capping and ERK activation. J Biol Chem 2009; 284: 9804–9813.
- 71 Dong S, et al. T cell receptor for antigen induces linker for activation of T cell-dependent activation of a negative signaling complex involving Dok-2, SHIP-1, and Grb-2. J Exp Med 2006; 203: 2509–2518.
- 72 Gugasyan R, et al. Dok-related protein negatively regulates T cell development via its RasGTPase-activating protein and Nck docking sites. J Cell Biol 2002; 158: 115–125.
- 73 Negishi I, et al. Essential role for ZAP-70 in both positive and negative selection of thymocytes. Nature 1995; 376: 435–438.
- 74 Zhang W, et al. Essential role of LAT in T cell development. Immunity 1999; 10: 323–332.
- 75 Smith-Garvin JE, Koretzky GA, Jordan MS. T cell activation. Annu Rev Immunol 2009; 27: 591–619.
- 76 Nemorin JG, Laporte P, Berube G, Duplay P. p62dok negatively regulates CD2 signaling in Jurkat cells. J Immunol 2001; 166: 4408–4415.
- 77 Nemorin JG, Duplay P. Evidence that Lck-mediated phosphorylation of p56dok and p62dok may play a role in CD2 signaling. J Biol Chem 2000; 275: 14590–14597.
- 78 Michel F, Attal-Bonnefoy G, Mangino G, Mise-Omata S, Acuto O. CD28 as a molecular amplifier extending TCR ligation and signaling capabilities. Immunity 2001; 15: 935–945.
- 79 Latour S, et al. Binding of SAP SH2 domain to FynT SH3 domain reveals a novel mechanism of receptor signalling in immune regulation. Nat Cell Biol 2003; 5: 149–154.
- 80 Niki M, et al. Role of Dok-1 and Dok-2 in leukemia suppression. J Exp Med 2004; 200: 1689–1695.
- 81 Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004; 4: 499–511.
- 82 Gilfillan AM, Rivera J. The tyrosine kinase network regulating mast cell activation. Immunol Rev 2009; 228: 149–169.
- 83 Saitoh S, et al. LAT is essential for FcεRI-mediated mast cell activation. Immunity 2000; 12: 525–535.
- 84 Abramson J, Rozenblum G, Pecht I. Dok protein family members are involved in signaling mediated by the type 1 Fcε receptor. Eur J Immunol 2003; 33: 85–91.
- 85 Kepley CL, et al. Co-aggregation of FcγRII with FcεRI on human mast cells inhibits antigen-induced secretion and involves SHIP–Grb2–Dok complexes. J Biol Chem 2004; 279: 35139–35149.
- 86 Ott VL, Tamir I, Niki M, Pandolfi PP, Cambier JC. Downstream of kinase, p62dok, is a mediator of FcγRIIB inhibition of FcεRI signaling. J Immunol 2002; 168: 4430–4439.
- 87 Kashiwada M, et al. Downstream of tyrosine kinases-1 and Src homology 2-containing inositol 5′-phosphatase are required for regulation of CD4+CD25+ T cell development. J Immunol 2006; 176: 3958–3965.
- 88 Henkemeyer M, et al. Vascular system defects and neuronal apoptosis in mice lacking ras GTPase-activating protein. Nature 1995; 377: 695–701.
- 89 Lapinski PE, Bauler TJ, Brown EJ, Hughes ED, Saunders TL, King PD. Generation of mice with a conditional allele of the p120 Ras GTPase-activating protein. Genesis 2007; 45: 762–767.
- 90 Niu Y, et al. A nuclear export signal and phosphorylation regulate Dok1 subcellular localization and functions. Mol Cell Biol 2006; 26: 4288–4301.
- 91 Itoh S, et al. Mitochondrial Dok-4 recruits Src kinase and regulates NF-κB activation in endothelial cells. J Biol Chem 2005; 280: 26383–26396.
- 92 Van Dijk TB, Van Den Akker E, Amelsvoort MP, Mano H, Lowenberg B, Von Lindern M. Stem cell factor induces phosphatidylinositol 3′-kinase-dependent Lyn/Tec/Dok-1 complex formation in hematopoietic cells. Blood 2000; 96: 3406–3413.
- 93 Martelli MP, Boomer J, Bu M, Bierer BE. T cell regulation of p62dok (Dok1) association with Crk-L. J Biol Chem 2001; 276: 45654–45661.
- 94 Shah K, Shokat KM. A chemical genetic screen for direct v-Src substrates reveals ordered assembly of a retrograde signaling pathway. Chem Biol 2002; 9: 35–47.
- 95 Wick MJ, Dong LQ, Hu D, Langlais P, Liu F. Insulin receptor-mediated p62dok tyrosine phosphorylation at residues 362 and 398 plays distinct roles for binding GTPase-activating protein and Nck and is essential for inhibiting insulin-stimulated activation of Ras and Akt. J Biol Chem 2001; 276: 42843–42850.
- 96 Rider DA, et al. A human CD4 monoclonal antibody for the treatment of T-cell lymphoma combines inhibition of T-cell signaling by a dual mechanism with potent Fc-dependent effector activity. Cancer Res 2007; 67: 9945–9953.
- 97 Gerard A, et al. Functional interaction of RasGAP-binding proteins Dok-1 and Dok-2 with the Tec protein tyrosine kinase. Oncogene 2004; 23: 1594–1598.
- 98 Berg KL, Siminovitch KA, Stanley ER. SHP-1 regulation of p62DOK tyrosine phosphorylation in macrophages. J Biol Chem 1999; 274: 35855–35865.
- 99 Zhang S, Phillips JH. Identification of tyrosine residues crucial for CD200R-mediated inhibition of mast cell activation. J Leukoc Biol 2006; 79: 363–368.
- 100 Shinohara H, Yasuda T, Yamanashi Y. Dok-1 tyrosine residues at 336 and 340 are essential for the negative regulation of Ras–Erk signalling, but dispensable for rasGAP-binding. Genes Cells 2004; 9: 601–607.
- 101 Kashige N, Carpino N, Kobayashi R. Tyrosine phosphorylation of p62dok by p210bcr-abl inhibits RasGAP activity. Proc Natl Acad Sci USA 2000; 97: 2093–2098.
- 102 Abramson J, Pecht I. Clustering the mast cell function-associated antigen (MAFA) leads to tyrosine phosphorylation of p62Dok and SHIP and affects RBL-2H3 cell cycle. Immunol Lett 2002; 82: 23–28.
- 103 Sylla BS, Murphy K, Cahir-McFarland E, Lane WS, Mosialos G, Kieff E. The X-linked lymphoproliferative syndrome gene product SH2D1A associates with p62dok (Dok1) and activates NF-κB. Proc Natl Acad Sci USA 2000; 97: 7470–7475.
- 104 Yoshida K, et al. Mediation by the protein-tyrosine kinase Tec of signaling between the B cell antigen receptor and Dok-1. J Biol Chem 2000; 275: 24945–24952.
- 105 Jones N, Dumont DJ. Recruitment of Dok-R to the EGF receptor through its PTB domain is required for attenuation of Erk MAP kinase activation. Curr Biol 1999; 9: 1057–1060.
- 106 Lock P, Casagranda F, Dunn AR. Independent SH2-binding sites mediate interaction of Dok-related protein with RasGTPase-activating protein and Nck. J Biol Chem 1999; 274: 22775–22784.
- 107 Jones N, Dumont DJ. The Tek/Tie2 receptor signals through a novel Dok-related docking protein, Dok-R. Oncogene 1998; 17: 1097–1108.
- 108 Nelms K, Snow AL, Hu-Li J, Paul WE. FRIP, a hematopoietic cell-specific rasGAP-interacting protein phosphorylated in response to cytokine stimulation. Immunity 1998; 9: 13–24.
- 109 Calderwood DA, et al. Integrin β cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc Natl Acad Sci USA 2003; 100: 2272–2277.
- 110 Murakami H, Yamamura Y, Shimono Y, Kawai K, Kurokawa K, Takahashi M. Role of Dok1 in cell signaling mediated by RET tyrosine kinase. J Biol Chem 2002; 277: 32781–32790.
- 111 Okazaki T, Maeda A, Nishimura H, Kurosaki T, Honjo T. PD-1 immunoreceptor inhibits B cell receptor-mediated signaling by recruiting src homology 2-domain-containing tyrosine phosphatase 2 to phosphotyrosine. Proc Natl Acad Sci USA 2001; 98: 13866–13871.
- 112 Yang WC, Ghiotto M, Barbarat B, Olive D. The role of Tec protein-tyrosine kinase in T cell signaling. J Biol Chem 1999; 274: 607–617.
- 113 Oliver-Vila I, Saborit-Villarroya I, Engel P, Martin M. The leukocyte receptor CD84 inhibits FcεRI-mediated signaling through homophilic interaction in transfected RBL-2H3 cells. Mol Immunol 2008; 45: 2138–2149.
- 114 Okabe S, et al. Stromal cell-derived factor-1α/CXCL12-induced chemotaxis of T cells involves activation of the RasGAP-associated docking protein p62Dok-1. Blood 2005; 105: 474–480.
- 115 Kato I, Takai T, Kudo A. The pre-B cell receptor signaling for apoptosis is negatively regulated by FcγRIIB. J Immunol 2002; 168: 629–634.
- 116 Liang X, Wisniewski D, Strife A, Shivakrupa C, Clarkson B, Resh MD. Phosphatidylinositol 3-kinase and Src family kinases are required for phosphorylation and membrane recruitment of Dok-1 in c-Kit signaling. J Biol Chem 2002; 277: 13732–13738.
- 117 Davidson D, et al. Genetic evidence linking SAP, the X-linked lymphoproliferative gene product, to Src-related kinase FynT in TH2 cytokine regulation. Immunity 2004; 21: 707–717.
- 118 Di Cristofano A, et al. p62dok, a negative regulator of Ras and mitogen-activated protein kinase (MAPK) activity, opposes leukemogenesis by p210bcr-abl. J Exp Med 2001; 194: 275–284.
- 119 Helgason CD, et al. Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev 1998; 12: 1610–1620.
- 120 Liu Q, et al. SHIP is a negative regulator of growth factor receptor-mediated PKB/Akt activation and myeloid cell survival. Genes Dev 1999; 13: 786–791.
- 121 Sly LM, Rauh MJ, Kalesnikoff J, Song CH, Krystal G. LPS-induced upregulation of SHIP is essential for endotoxin tolerance. Immunity 2004; 21: 227–239.
- 122 Helgason CD, et al. A dual role for Src homology 2 domain-containing inositol-5-phosphatase (SHIP) in immunity: aberrant development and enhanced function of B lymphocytes in SHIP−/− mice. J Exp Med 2000; 191: 781–794.
