The roles of Dok family adapters in immunoreceptor signaling

Immunological Reviews

Volumn 232, Issue 1, 2009, Pages 273-285

  Mashima, Ryuichi ^a   Hishida, Yukihiro ^a   Tezuka, Tohru ^a   Yamanashi, Yuji ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Adapter proteins; Dok; Signal transduction

Indexed keywords

ADAPTOR PROTEIN; CYTOKINE RECEPTOR; FC RECEPTOR; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; PLECKSTRIN; PROTEIN DOK 1; PROTEIN DOK 2; PROTEIN DOK 3; PROTEIN P120; PROTEIN P62; PROTEIN SH2; PROTEIN TYROSINE KINASE; RAS PROTEIN; RECEPTOR; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; B LYMPHOCYTE; BONE MARROW CELL; COLONY FORMING UNIT M; HEMATOPOIETIC CELL; HUMAN; IMMUNOCOMPETENT CELL; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; B-LYMPHOCYTES; DNA-BINDING PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOCYTE ACTIVATION; MAP KINASE KINASE 4; MEMBRANE PROTEINS; P120 GTPASE ACTIVATING PROTEIN; PHOSPHOPROTEINS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS P21(RAS); RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 70350406465     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2009.00844.x     Document Type: Review

References (122)

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. v-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. ras 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. dok: 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. (Pubitemid 38049392)
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. dok-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. dok-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. Dok 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. 2+ 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. dok 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. dok 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. dok 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. dok negatively regulates CD2 signaling in Jurkat cells. J Immunol 2001 166 : 4408 4415.
77. dok 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. dok, is a mediator of FcγRIIB inhibition of FcεRI signaling. J Immunol 2002 168 : 4430 4439.
87. + 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. dok (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. dok 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. DOK 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. bcr-abl inhibits RasGAP activity. Proc Natl Acad Sci USA 2000 97 : 2093 2098.
102. Dok and SHIP and affects RBL-2H3 cell cycle. Immunol Lett 2002 82 : 23 28.
103. dok (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. H2 cytokine regulation. Immunity 2004 21 : 707 717.
118. bcr-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. -/- mice. J Exp Med 2000 191 : 781 794.