Gab2 requires membrane targeting and the met binding motif to promote lamellipodia, cell scatter, and epithelial morphogenesis downstream from the met receptor

Journal of Cellular Physiology

Volumn 214, Issue 3, 2008, Pages 694-705

  Frigault, Melanie M ^a   Naujokas, Monica A ^a   Park, Morag ^a  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GAB1 PROTEIN; GAB2 PROTEIN; GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SCAFFOLD PROTEIN; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; EPIDERMAL GROWTH FACTOR RECEPTOR; HYBRID PROTEIN; PROTEIN TYROSINE PHOSPHATASE SHP 2; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; GENE ACTIVATION; GENE AMPLIFICATION; GENE IDENTIFICATION; GENE OVEREXPRESSION; LAMELLIPODIUM; MORPHOGENESIS; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TARGETING; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; CELL MEMBRANE; CELL SHAPE; CHEMISTRY; CHICKEN; CYTOLOGY; DOG; ENZYMOLOGY; METABOLISM; PHOSPHORYLATION; PROTEIN TRANSPORT; PSEUDOPODIUM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; ANIMALS; CELL LINE; CELL MEMBRANE; CELL SHAPE; CHICKENS; DOGS; ENZYME ACTIVATION; EPITHELIAL CELLS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; PROTO-ONCOGENE PROTEINS C-MET; PSEUDOPODIA; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION;

EID: 38449120668     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21264     Document Type: Article

References (91)

1. Aplin AE, Stewart SA, Assoian RK, Juliano RL. 2001. Integrin-mediated adhesion regulates ERK nuclear translocation and phosphorylation of Elk-1. J Cell Biol 153:273-282.
2. Bardelli A, Longati P, Gramaglia D, Stella MC, Comoglio PM. 1997. Gab1 coupling to the HGF/ Met receptor multifunctional docking site requires binding of Grb2 and correlates with the transforming potential. Oncogene 15:3103-3111.
3. Bentires-Alj M, Gil SG, Chan R, Wang ZC, Wang Y, Imanaka N, Harris LN, Richardson A, Neel BG, Gu H. 2006. A role for the scaffolding adapter GAB2 in breast cancer. Nat Med 12:114-121.
4. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. 2003. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 4:915-925.
5. Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C. 1995. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376:768-771.
6. Bouscary D, Lecoq-Lafon C, Chretien S, Zompi S, Fichelson S, Muller O, Porteu F. Dusanter-Fourt I, Gisselbrecht S, Mayeux P, Lacombe C. 2001. Role of Gab proteins in phosphatidylinositol 3-kinase activation by thrombopoietin. Oncogene 20:2197-2204.
7. Brahmbhatt AA, Klemke RL. 2003. ERK and RhoA differentially regulate pseudopodia growth and retraction during chemotaxis. J Biol Chem 278:13016-13025.
8. Brummer T, Schramek D, Hayes VM, Bennett HL, Caldon CE, Musgrove EA, Daly RJ. 2006. Increased proliferation and altered growth factor dependence of human mammary epithelial cells overexpressing the Gab2 docking protein. J Biol Chem 281:626-637.
9. Crouin C, Arnaud M, Gesbert F, Camonis J, Bertoglio J. 2001. A yeast two-hybrid study of human p97/Gab2 interactions with its SH2 domain-containing binding partners. FEBS Lett 495:148-153.
10. Daly RJ, Gu H, Parmar J, Malaney S, Lyons RJ, Kairouz R, Head DR, Henshall SM, Neel BG, Sutherland RL. 2002. The docking protein Gab2 is overexpressed and estrogen regulated in human breast cancer. Oncogene 21:5175-5181.
11. Ebisuya M, Kondoh K, Nishida E. 2005. The duration, magnitude and compartmentalization of ERK MAP kinase activity: Mechanisms for providing signaling specificity. J Cell Sci 118:2997-3002.
12. Fixman ED, Holgado-Madruga M, Nguyen L, Kamikura DM, Fournier TM, Wong AJ, Park M. 1997. Efficient cellular transformation by the Met oncoprotein requires a functional Grb2 binding site and correlates with phosphorylation of the Grb2-associated proteins, Cb1 and Gab1. J Biol Chem 272:20167-20172.
13. Fournier TM, Kamikura D, Teng K, Park M. 1996. Branching tubulogenesis but not scatter of madin-darby canine kidney cells requires a functional Grb2 binding site in the Met receptor tyrosine kinase. J Biol Chem 271:22211-22217.
14. Garcia-Guzman M, Dolfi F, Zeh K, Vuori K. 1999. Met-induced JNK activation is mediated by the adapter protein Crk and correlates with the Gab1 - Crk signaling complex formation. Oncogene 18:7775-7786.
15. Gherardi E, Gray J, Stoker M, Perryman M. Furlong R. 1989. Purification of scatter factor, a fibroblast-derived basic protein that modulates epithelial interactions and movement. Proc Natl Acad Sci USA 86:5844-5848.
16. Giovannone B, Scaldaferri ML, Federici M, Porzio O, Lauro D, Fusco A, Sbraccia P, Borboni P, Lauro R, Sesti G. 2000. Insulin receptor substrate (IRS) transduction system: Distinct and overlapping signaling potential. Diabetes Metab Res Rev 16:434-441.
17. Glading A, Uberall F, Keyse SM, Lauffenburger DA, Wells A. 2001. Membrane proximal ERK signaling is required for M-calpain activation downstream of epidermal growth factor receptor signaling. J Biol Chem 276:23341-23348.
18. Gu H, Neel BG. 2003. The "Gab" in signal transduction. Trends Cell Biol 13:122-130.
19. Gu H, Pratt JC, Burakoff SJ, Neel BG. 1998. Cloning of p97/Gab2, the major SHP2-binding protein in hematopoietic cells, reveals a novel pathway for cytokine-induced gene activation. Mol Cell 2:729-740.
20. Gu H, Saito K, Klaman LD, Shen J, Fleming T, Wang Y, Pratt JC, Lin G, Lim B, Kinet JP, Neel BG. 2001. Essential role for Gab2 in the allergic response. Nature 412:186-190.
21. Gual P, Giordano S, Williams TA, Rocchi S, Van Obberghen E, Comoglio PM. 2000. Sustained recruitment of phospholipase C-gamma to Gab1 is required for HGF-induced branching tubulogenesis. Oncogene 19:1509-1518.
22. Guy GR, Yusoff P, Bangarusamy D, Fong CW, Wong ES. 2002. Dockers at the crossroads. Cell Signal 14:11-20.
23. Hoffmann KM, Tapia JA, Jensen RT. 2006. Activation of Gab1 in pancreatic acinar cells: Effects of gastrointestinal growth factors/hormones on stimulation, phosphospecific phosphorylation, translocation and interaction with downstream signaling molecules. Cell Signal 18:942-954.
24. Hong T, Grabel LB. 2006. Migration of F9 parietal endoderm cells is regulated by the ERK pathway. J Cell Biochem 97:1339-1349.
25. Honma N, Genda T, Matsuda Y, Yamagiwa S, Takamura M, Ichida T, Aoyagi Y. 2006. MEK/ ERK signaling is a critical mediator for integrin-induced cell scattering in highly metastatic hepatocellular carcinoma cells. Lab Invest 86:687-696.
26. Isakoff SJ, Cardozo T, Andreev J, Li Z, Ferguson KM, Abagyan R, Lemmon MA, Aronheim A, Skolnik EY. 1998. Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. Embo J 17:5374-5387.
27. Ischenko I, Petrenko O, Gu H, Hayman MJ. 2003. Scaffolding protein Gab2 mediates fibroblast transformation by the SEA tyrosine kinase. Oncogene 22:6311-6318.
28. Ishibe S, Joly D, Liu ZX, Cantley LG. 2004. Paxillin serves as an ERK-regulated scaffold for coordinating FAK and Rac activation in epithelial morphogenesis. Mol Cell 16:257-267.
29. Itoh M, Yoshida Y, Nishida K, Narimatsu M, Hibi M, Hirano T. 2000. Role of Gabi in heart, placenta, and skin development and growth factor- and cytokine-induced extracellular signal-regulated kinase mitogen-activated protein kinase activation. Mol Cell Biol 20:3695-3704.
30. Kallin A, Demoulin JB, Nishida K, Hirano T, Ronnstrand L, Heldin CH. 2004. Gab1 contributes to cytoskeletal reorganization and chemotaxis in response to platelet-derived growth factor. J Biol Chem 279:17897-17904.
31. Kameda H, Ishigami H, Suzuki M, Abe T, Takeuchi T. 2006. Imatinib mesylate inhibits proliferation of rheumatoid synovial fibroblast-like cells and phosphorylation of Gab adapter proteins activated by platelet-de rived growth factor. Clin Exp Immunol 144:335-341.
32. Ke Y, Wu D, Princen F, Nguyen T, Pang Y, Lesperance J, Muller WJ, Oshima RG, Feng GS. 2007. Role of Gab2 in mammary tumorigenesis and metastasis. Oncogene.
33. Klemke RL, Cai S, Giannini AL, Gallagher PJ, de Lanerolle P, Cheresh DA. 1997. Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol 137:481-492.
34. Kong M, Mounier C, Balbis A, Baquiran G, Posner BI. 2003. Gab2 tyrosine phosphorylation by a pleckstrin homology domain-independent mechanism: Role in epidermal growth factor-induced mitogenesis. Mol Endocrinol 17:935-944.
35. Kubler E, Dohlman HG, Lisanti MP. 1996. Identification of Triton X-100 insoluble membrane domains in the yeast Saccharomyces cerevisiae. Lipid requirements for targeting of heterotrimeric G-protein subunits. J Biol Chem 271:32975-32980.
36. Lamorte L, Kamikura DM, Park M. 2000. A switch from p130Cas/Crk to Gab1/Crk signaling correlates with anchorage independent growth and JNK activation in cells transformed by the Met receptor oncoprotein. Oncogene 19:5973-5981.
37. Lehr S, Kotzka J, Avci H, Sickmann A, Meyer HE, Herkner A, Muller-Wieland D. 2004. Identification of major ERK-related phosphorylation sites in Gab1. Biochemistry 43:12133-12140.
38. Lewitzky M, Kardinal C, Gehring NH, Schmidt EK, Konkol B, Eulitz M, Birchmeier W, Schaeper U, Feller SM. 2001. The C-terminal SH3 domain of the adapter protein Grb2 binds with high affinity to sequences in Gab1 and SLP-76 which lack the SH3-typical P-x-x-P core motif. Oncogene 20:1052-1062.
39. Liu Y, Rohrschneider LR. 2002. The gift of Gab. FEBS Lett 515:1-7.
40. Lock LS, Royal I, Naujokas MA, Park M. 2000. Identification of an atypical Grb2 carboxyl-terminal SH3 domain binding site in Gab docking proteins reveals Grb2-dependent and -independent recruitment of Gab1 to receptor tyrosine kinases. J Biol Chem 275:31536-31545.
41. Lock LS, Maroun CR, Naujokas MA, Park M. 2002. Distinct recruitment and function of Gab1 and Gab2 in Met receptor-mediated epithelial morphogenesis. Mol Biol Cell 13:2132-2146.
42. Maroun CR, Holgado-Madruga M, Royal I, Naujokas MA, Fournier TM, Wong AJ, Park M. 1999a. The Gab1 PH domain is required for localization of Gab1 at sites of cell-cell contact and epithelial morphogenesis downstream from the met receptor tyrosine kinase. Mol Cell Biol 19:1784-1799.
43. Maroun CR, Moscatello DK, Naujokas MA, Holgado-Madruga M, Wong AJ, Park M. 1999b. A conserved inositol phospholipid binding site within the pleckstrin homology domain of the Gab1 docking protein is required for epithelial morphogenesis. J Biol Chem 274:31719-31726.
44. Maroun CR, Naujokas MA, Holgado-Madruga M, Wong AJ, Park M. 2000. The tyrosine phosphatase SHP-2 is required for sustained activation of extracellular signal-regulated kinase and epithelial morphogenesis downstream from the met receptor tyrosine kinase. Mol Cell Biol 20:8513-8525.
45. Maroun CR, Naujokas MA, Park M. 2003. Membrane targeting of Grb2-associated binder-1 (Gab1) scaffolding protein through Src myristoylation sequence substitutes for Gab1 pleckstrin homology domain and switches an epidermal growth factor response to an invasive morphogenic program. Mol Biol Cell 14:1691-1708.
46. Martinez-Quiles N, Ho HY, Kirschner MW, Ramesh N, Geha RS. 2004. Erk/Src phosphorylation of cortactin acts as a switch on-switch off mechanism that controls its ability to activate N-WASP. Mol Cell Biol 24:5269-5280.
47. Matsubayashi Y, Ebisuya M, Honjoh S, Nishida E. 2004. ERK activation propagates in epithelial cell sheets and regulates their migration during wound healing. Curr Biol 14:731-735.
48. Matsumoto K, Nakamura T. 1997. HGF: Its organotrophic role and therapeutic potential. Ciba Found Symp 212:198-211 discussion 211-194.
49. Meng S, Chen Z, Munoz-Antonia T, Wu J. 2005. Participation of both Gab1 and Gab2 in the activation of the ERK/MAPK pathway by epidermal growth factor. Biochem J 391:143-151.
50. Million RP, Harakawa N, Roumiantsev S, Varticovski L, Van Etten RA. 2004. A direct binding site for Grb2 contributes to transformation and leukemogenesis is by the Tel-Abl (ETV6-Ab1) tyrosine kinase. Mol Cell Biol 24:4685-4695.
51. Montesano R, Matsumoto K, Nakamura T, Orci L. 1991. Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67:901-908.
52. Nakamura T. 1991. Structure and function of hepatocyte growth factor. Prog Growth Factor Res 3:67-85.
53. Nguyen L, Holgado-Madruga M, Maroun C, Fixman ED, Kamikura D, Fournier T, Charest A, Tremblay ML, Wong AJ, Park M. 1997. Association of the multisubstrate docking protein Gab1 with the hepatocyte growth factor receptor requires a functional Grb2 binding site involving tyrosine 1356. J Biol Chem 272:20811-20819.
54. Nishida K, Hirano T. 2003. The role of Gab family scaffolding adapter proteins in the signal transduction of cytokine and growth factor receptors. Cancer Sci 94:1029-1033.
55. Nishida K, Yoshida Y, Itoh M, Fukada T, Ohtani T, Shirogane T, Atsumi T, Takahashi-Tezuka M, Ishihara K, Hibi M, Hirano T. 1999. Gab-family adapter proteins act downstream of cytokine and growth factor receptors and T- and B-cell antigen receptors. Blood 93:1809-1816.
56. Nishida K, Wang L, Morii E, Park SJ, Narimatsu M, Itoh S, Yamasaki S, Fujishima M, Ishihara K, Hibi M, Kitamura Y, Hirano T. 2002. Requirement of Gab2 for mast cell development and KitL/c-Kit signaling. Blood 99:1866-1869.
57. O'Brien LE, Zegers MM, Mostov KE. 2002. Opinion: Building epithelial architecture: Insights from three-dimensional culture models. Nat Rev Mol Cell Biol 3:531-537.
58. O'Brien LE, Tang K, Kats ES, Schutz-Geschwender A, Lipschutz JH, Mostov KE. 2004. ERK and MMPs sequentially regulate distinct stages of epithelial tubule development. Dev Cell 7:21-32.
59. Podar K, Mostoslavsky G, Sattler M, Tai YT, Hayashi T, Catley LP, Hideshima T, Mulligan RC, Chauhan D, Anderson KC. 2004. Critical role for hematopoietic cell kinase (Hck)-mediated phosphorylation of Gab1 and Gab2 docking proteins in interleukin 6-induced proliferation and survival of multiple myeloma cells. J Biol Chem 279:21658-21665.
60. Potempa S, Ridley AJ. 1998. Activation of both MAP kinase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/scatter factor-induced adherens junction disassembly. Mol Biol Cell 9:2185-2200.
61. Pratt JC, Igras VE, Maeda H, Baksh S, Gelfand EW, Burakoff SJ, Neel BG, Gu H. 2000. Cutting edge: Gab2 mediates an inhibitory phosphatidylinositol 3′-kinase pathway in T cell antigen receptor signaling. J Immunol 165:4158-4163.
62. Pullar CE, Grahn JC, Liu W, Isseroff RR. 2006. Beta2-adrenergic receptor activation delays wound healing. FASEB J 20:76-86.
63. Ren SY, Bolton E, Mohi MG, Morrione A, Neel BG, Skorski T. 2005. Phosphatidylinositol 3-kinase p85{alpha} subunit-dependent interaction with BCR/ABL-related fusion tyrosine kinases: Molecular mechanisms and biological consequences. Mol Cell Biol 25:8001-8008.
64. Renshaw MW, Price LS, Schwartz MA. 1999. Focal adhesion kinase mediates the integrin signaling requirement for growth factor activation of MAP kinase. J Cell Biol 147:611-618.
65. Ridley AJ, Comoglio PM, Hall A. 1995. Regulation of scatter factor/hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells. Mol Cell Biol 15:1110-1122.
66. Rodrigues GA, Naujokas MA, Park M. 1991. Alternative splicing generates isoforms of the met receptor tyrosine kinase which undergo differential processing. Mol Cell Biol 11:2962-2970.
67. Rodrigues GA, Falasca M, Zhang Z, Ong SH, Schlessinger J. 2000. A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol Cell Biol 20:1448-1459.
68. Royal I, Lamarche-Vane N, Lamorte L, Kaibuchi K, Park M. 2000. Activation of cdc42, rac, PAK, and rho-kinase in response to hepatocyte growth factor differentially regulates epithelial cell colony spreading and dissociation. Mol Biol Cell 11:1709-1725.
69. Sachs M, Brohmann H, Zechner D, Muller T, Hulsken J, Walther I, Schaeper U, Birchmeier C, Birchmeier W. 2000. Essential role of Gab1 for signaling by the c-Met receptor in vivo. J Cell Biol 150:1375-1384.
70. Sakkab D, Lewitzky M, Posern G, Schaeper U, Sachs M, Birchmeier W, Feller SM. 2000. Signaling of hepatocyte growth factor/scatter factor (HGF) to the small GTPase Rap1 via the large docking protein Gab1 and the adapter protein CRKL. J Biol Chem 275:10772-10778.
71. Sattler M, Mohi MG, Pride YB, Quinnan LR, Malouf NA, Podar K, Gesbert F, Iwasaki H, Li S, Van Etten RA, Gu H, Griffin JD, Neel BG. 2002. Critical role for Gab2 in transformation by BCR/ABL. Cancer Cell 1:479-492.
72. Schaeper U, Gehring NH, Fuchs KP, Sachs M, Kempkes B, Birchmeier W. 2000. Coupling of Gab1 to c-Met, Grb2, and Shp2 mediates biological responses. J Cell Biol 149:1419-1432.
73. Scherr M, Chaturvedi A, Battmer K, Dallmann I, Schultheis B, Ganser A, Eder M. 2006. Enhanced sensitivity to inhibition of SHP2, STAT5, and Gab2 expression in chronic myeloid leukemia (CML). Blood 107:3279-3287.
74. Sharma GD, He J, Bazan HE. 2003. p38 and ERK1/2 coordinate cellular migration and proliferation in epithelial wound healing: Evidence of cross-talk activation between MAP kinase cascades. J Biol Chem 278:21989-21997.
75. Vaidya RJ, Ray RM, Johnson LR. 2005. MEK1 restores migration of polyamine-depleted cells by retention and activation of Rac1 in the cytoplasm. Am J Physiol Cell Physiol 288:C350-C359.
76. Vande Woude GF, Jeffers M, Cortner J, Alvord G, Tsarfaty I, Resau J. 1997. Met-HGF/SF: Tumorigenesis, invasion and metastasis. Ciba Found Symp 212:119-130 discussion 130-112. 148-154.
77. Wada T, Nakashima T, Oliveira-dos-Santos AJ, Gasser J, Hara H, Schett G, Penninger JM. 2005. The molecular scaffold Gab2 is a crucial component of RANK signaling and osteoclastogenesis. Nat Med 11:394-399.
78. Watanabe T, Tsuda M, Makino Y, Ichihara S, Sawa H, Minami A, Mochizuki N, Nagashima K, Tanaka S. 2006. Adaptor molecule Crk is required for sustained phosphorylation of Grb2-associated binder I and hepatocyte growth factor-induced cell motility of human synovial sarcoma cell lines. Mol Cancer Res 4:499-510.
79. Weidner KM, Sachs M, Birchmeier W. 1993. The Met receptor tyrosine kinase transduces motility, proliferation, and morphogenic signals of scatter factor/hepatocyte growth factor in epithelial cells. J Cell Biol 121:145-154.
80. White MF. 1998. The IRS-signalling system: A network of docking proteins that mediate insulin action. Mol Cell Biochem 182:3-11.
81. Wickrema A, Uddin S, Sharma A, Chen F, Alsayed Y, Ahmad S, Sawyer ST, Krystal G, Yi T, Nishada K, Hibi M, Hirano T, Platanias LC. 1999. Engagement of Gab1 and Gab2 in erythropoietin signaling. J Biol Chem 274:24469-24474.
82. Wolf I, Jenkins BJ, Liu Y, Seiffert M, Custodio JM, Young P, Rohrschneider LR. 2002. Gab3, a new DOS/Gab family member, facilitates macrophage differentiation. Mol Cell Biol 22:231-244.
83. Yu CF, Basson MD. 2000. Matrix-specific FAK and MAPK reorganization during Caco-2 cell motility. Microsc Res Tech 51:191-203.
84. Yu CF, Roshan B, Liu ZX, Cantley LG. 2001. ERK regulates the hepatocyte growth factor-mediated interaction of Gab1 and the phosphatidylinositol 3-kinase. J Biol Chem 276:32552-32558.
85. Yu CF, Liu ZX, Cantley LG. 2002a. ERK negatively regulates the epidermal growth factor-mediated interaction of Gab1 and the phosphatidylinositol 3-kinase. J Biol Chem 277:19382-19388.
86. Yu WM, Hawley TS, Hawley RG, Qu CK. 2002b. Role of the docking protein Gab2 in beta(1)-integrin signaling pathway-mediated hematopoietic cell adhesion and migration. Blood 99:2351-2359.
87. Zhang S, Broxmeyer HE. 2000. Flt3 ligand induces tyrosine phosphorylation of gab1 and gab2 and their association with shp-2, grb2, and PI3 kinase. Biochem Biophys Res Commun 277:195-199.
88. Zhao C, Yu DH, Shen R, Feng GS. 1999. Gab2, a new pleckstrin homology domain-containing adapter protein, acts to uncouple signaling from ERK kinase to Elk-1. J Biol Chem 274:19649-19654.
89. Zhao C, Ma H, Bossy-Wetzel E, Lipton SA, Zhang Z, Feng GS. 2003. GC-GAP, a Rho family GTPase-activating protein that interacts with signaling adapters Gab1 and Gab2. J Biol Chem 278:34641-34653.
90. Zhu H, Naujokas MA, Park M. 1994. Receptor chimeras indicate that the met tyrosine kinase mediates the motility and morphogenic responses of hepatocyte growth/scatter factor. Cell Growth Differ 5:359-366.
91. Zompi S, Gu H, Colucci F. 2004. The absence of Grb2-associated binder 2 (Gab2) does not disrupt NK cell development and functions. J Leukoc Biol 76:896-903.