A deletion mutation in the SH2-N domain of Shp-2 severely suppresses hematopoietic cell development

Molecular and Cellular Biology

Volumn 17, Issue 9, 1997, Pages 5499-5507

  Qu, Cheng Kui ^a   Shi, Zhong Qing ^a   Shen, Randy ^a   Tsai, Fong Ying ^b,d   Orkin, Stuart H ^b   Feng, Gen Sheng ^a,c  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c INDIANA UNIVERSITY   (United States)

^d MILLENNIUM PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TYROSINE PHOSPHATASE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DELETION MUTANT; EMBRYO DEATH; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; LETHALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN;

ANIMALIA; MAMMALIA;

EID: 0030797548     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.9.5499     Document Type: Article

References (77)

1. Adachi, M., E. H. Fischer, J. Ihle, K. Imai, F. Jirik, B. Neel, T. Pawson, S. Shen, M. Thomas, A. Ullrich, and Z. Zhao. 1996. Mammalian SH2-containine protein tyrosine phosphatases. Cell 85:15. (Letter.)
2. Allard, J. D., H. C. Chang, R. Herbst, H. McNeill, and M. A. Simon. 1996. The SH2-containing tyrosine phosphatase corkscrew is required during signaling by sevenless, Ras1 and Raf. Development 122:1137-1146.
3. Amaya, E., T. J. Musci, and M. W. Kirschner. 1991. Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell 66:257-270.
4. Arrandale, J. M., A. Gore-Willse, S. Rocks, J. M. Ren, J. Zhu, A. Davis, J. N. Livingston, and D. U. Rabin. 1996. Insulin signaling in mice expressing reduced levels of Syp. J. Biol. Chem. 271:21353-21358.
5. Bennett, A. M., S. F. Hausdorff, A. M. O'Reilly, R. M. Freeman, and B. G. Neel. 1996. Multiple requirements for SHPTP2 in epidermal growth factor-mediated cell cycle progression. Mol. Cell. Biol. 16:1189-1202.
6. Bennett, A. M., T. L. Tang, S. Sugimoto, C. T. Walsh, and B. G. Neel. 1994. Protein-tyrosine-phosphatase SHPTP2 couples platelet-derived growth factor receptor beta to Ras. Proc. Natl. Acad. Sci. USA 91:7335-7339.
7. Brady-Kalnay, S. M., and N. K. Tonks. 1995. Protein tyrosine phosphatases as adhesion receptors. Curr. Opin. Cell Biol. 7:650-657.
8. Brown, M. T., and J. A. Cooper. 1996. Regulation, substrates and functions of src. Biochim. Biophys. Acta 1287:121-149.
9. Burkert, U., T. von Ruden, and E. F. Wagner. 1991. Early fetal hematopoietic development from in vitro differentiated embryonic stem cells. New Biol. 3:698-708.
10. Burshtyn, D. N., A. M. Scharenberg, N. Wagtmann, S. Rajagopalan, K. Berrada, T. Yi, J. P. Kinet, and E. O. Long. 1996. Recruitment of tyrosine phosphatase HCP by the killer cell inhibitor receptor. Immunity 4:77-85.
11. Chen, H. E., S. Chang, T. Trub, and B. G. Neel. 1996. Regulation of colony-stimulating factor 1 receptor signaling by the SH2 domain-containing tyrosine phosphatase SHPTP1, Mol. Cell. Biol. 16:3685-3697.
12. Cyster, J. G., J. I. Healy, K. Kishihara, T. W. Mak, M. L. Thomas, and C. C. Goodnow. 1996. Regulation of B-lymphocyte negative and positive selection by tyrosine phosphatase CD45. Nature 381:325-328.
13. D'Ambrosio, D., K. L. Hippen, S. A. Minskoff, I. Mellman, G. Pani, K. A. Siminovitch, and J. C. Cambier. 1945. Recruitment and activation of PTP1C in negative regulation of antigen receptor signaling hy Fc gamma RIIB1. Science 268:293-297.
14. Dechert, U., M. Adam, K. W. Harder, I. Clark-Lewis, and F. Jirik. 1994. Characterization of protein tyrosine phosphatase SH-PTP2. Study of phosphopeptide substrates and possible regulatory role of SH2 domains. J. Biol. Chem. 269:5602-5611.
15. Deng, C. X., A. Wynshaw-Boris, M. M. Shen, C. Daugherty, D. M. Ornitz, and P. Leder. 1994. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 8:3045-3057.
16. Dixon, J. E. 1996. Protein tyrosine phosphatases: their roles in signal transduction. Recent Prog. Horm. Res. 51:405-414.
17. Doetschman, T. C., H. Eistetter, M. Katz, W. Schmidt, and R. Kemler. 1985. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J. Embryol. Exp. Morphol. 87:27-45.
18. Doody, G. M., L. B. Justement, C. C. Delibrias, R. J. Matthews, J. Lin, M. L. Thomas, and D. T. Fearon. 1995. A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP. Science 269:242-244.
19. Etienne-Julan, M., A. Gotoh, G. S. Feng, and H. E. Broxmeyer. Involvement of the Shp-2 phosphatase in proliferation and differentiation of TF1 cells and cord blood myeloid progenitor cells. Unpublished data.
20. Feng, G. S., C. C. Hui, and T. Pawson. 1993. SH2-containing phosphotyrosine phosphatase as a target of protein-tyrosine kinases. Science 259:1607-1611.
21. Feng, G. S., and T. Pawson. 1994. Phosphotyrosine phosphatases with SH2 domains: regulators of signal transduction. Trends Genet. 10:54-58.
22. Feng, G. S., R. Shen, H. H. Heng, L. C. Tsui, A. Kazlauskas, and T. Pawson. 1994. Receptor-binding, tyrosine phosphorylation and chromosome localization of the mouse SH2-containing phosphotyrosine phosphatase Syp. Oncogene 9:1545-1550.
23. Fuhrer, D. K., G. S. Feng, and Y. C. Yang. 1995. Syp associates with gp130 and Janus kinase 2 in response to interleukin-11 in 3T3-L1 mouse preadipocytes. J. Biol. Chem. 270:24826-24830.
24. Herbst, R., P. M. Carroll, J. D. Allard, J. Schilling, T. Raabe, and M. A. Simon. 1996. Daughter of sevenless is a substrate of the phosphotyrosine phosphatase Corkscrew and functions during sevenless signaling. Cell 85: 899-909.
25. Kazlauskas, A., G. S. Feng, T. Pawson, and M. Valius. 1993. The 64-kDa protein that associates with the platelet-derived growth factor receptor beta subunit via Tyr-1009 is the SH2-containing phosphotyrosine phosphatase Syp. Proc. Natl. Acad. Sci. USA 90:6939-6943.
26. Keller, G., M. Kennedy, T. Papayannopoulou, and M. V. Wiles. 1993. Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol. Cell. Biol. 13:473-486.
27. Klingmuller, U., U. Lorenz, L. C. Cantley, B. G. Neel, and H. F. Lodish. 1995. Specific recruitment of SH-PTP1 to the erythropoietin receptor causes inactivation of JAK2 and termination of proliferative signals. Cell 80:729-738.
28. Kozlowski, M., I. Mlinaric-Rascan, G. S. Feng, R. Shen, T. Pawson, and K. A. Siminovitch. 1993. Expression and catalytic activity of the tyrosine phosphatase PTP1C is severely impaired in motheaten and viable motheaten mice. J. Exp. Med. 178:2157-2163.
29. Kuhne, M. R., T. Pawson, G. E. Lienhard, and G. S. Feng. 1993. The insulin receptor substrate 1 associates with the SH2-containing phosphotyrosine phosphatase Syp. J. Biol. Chem. 268:11479-11481.
30. Lechleider, R. J., R. Freeman, Jr., and B. G. Neel. 1993. Tyrosyl phosphorylation and arowth factor receptor association of the human corkscrew homologue, SH-PTP2. J. Biol. Chem. 268:13434-13438.
31. Lechleider, R. J., S. Sugimoto, A. M. Bennett, A. S. Kashishian, J. A. Cooper, S. E. Shoelson, C. T. Walsh, and B. G. Neel. 1993. Activation of the SH2-containing phosphotyrosine phosphatase SH-PTP2 by its binding site, phosphotyrosine 1009, on the human platelet-derived growth factor receptor. J. Biol. Chem 268:21478-21481.
32. Li, W., R. Nishimura, A. Kashishian, A. G. Batzer, W. J. Kim, J. A. Cooper, and J. Schlessinger. 1994. A new function for a phosphotyrosine phosphatase: linking GRB2-Sos to a receptor tyrosine kinase. Mol. Cell. Biol. 14: 509-517.
33. Lu, L., Y. Ge, Z. H. Li, M. Etienne-Julan, G. S. Feng, and H. E. Broxmeyer. Unpublished data.
34. Marengere, L. E., P. Waterhouse, G. S. Duncan, H. W. Mittrucker, G. S. Feng, and T. W. Mak. 1996. Regulation of T cell receptor signaling by tyrosine phosphatase SYP association with CTLA-4. Science 272:1170-1173.
35. McClanahan, T., S. Dalrymple, M. Barkett, and F. Lee. 1993. Hematopoietic growth factor receptor genes as markers of lineage commitment during in vitro development of hematopoietic cells. Blood 81:2903-2915.
36. Milarski, K. L., and A. R. Saltiel. 1994. Expression of catalytically inactive Syp phosphatase in 3T3 cells blocks stimulation of mitogen-activated protein kinase by insulin. J. Biol. Chem. 269:21239-21243.
37. Mortensen, R. M., D. A. Conner, S. Chao, A. A. Geisterfer-Lowrance, and J. G. Scidman. 1992. Production of homozygous mutant ES cells with a single targeting construct. Mol. Cell. Biol. 12:2391-2395.
38. Neel, B. G. 1993. Structure and function of SH2-domain containing tyrosine phosphatases. Semin. Cell Biol. 4:419-432.
39. Noguchi, T., T. Matozaki, K. Horita, Y. Fujioka, and M. Kasuga. 1994. Role of SH-PTP2, a protein-tyrosine phosphatase with Src homology 2 domains, in insulin-stimulated Ras activation. Mol. Cell. Biol. 14:6674-6682.
40. Pei, D., U. Lorenz, U. Klingmuller, B. G. Neel, and C. T. Walsh. 1994. Intramolecular regulation of protein tyrosine phosphatase SH-PTP1: a new function for Src homology 2 domains. Biochemistry 33:15483-15493.
41. Pei, D., B. G. Neel, and C. T. Walsh. 1993. Overexpression, purification, and characterization of SHPTP1, a Src homology 2-containing protein-tyrosine-phosphatase. Proc. Natl. Acad. Sci. USA 90:1092-1096.
42. Perkins, L. A., I. Larsen, and N. Perrimon. 1992. corkscrew encodes a putative protein tyrosine phosphatase that functions to transduce the terminal signal from the receptor tyrosine kinase torso. Cell 70:225-236.
43. Plas, D. R., R. Johnson, J. T. Pingel, R. J. Matthews, M. Dalton, G. Roy, A. C. Chan, and M. L. Thomas. 1996. Direct regulation of ZAP-70 by SHP-1 in T cell antigen receptor signaling. Science 272:1173-1176.
44. Pluskey, S., T. J. Wandless, C. T. Walsh, and S. E. Shoelson. 1995. Potent stimulation of SH-PTP2 phosphatase activity by simultaneous occupancy of both SH2 domains. J. Biol. Chem. 270:2897-2900.
45. Porcher, C., W. Swat, K. Rockwell, Y. Fujiwara, F. W. Alt, and S. H. Orkin. 1996. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 86:47-57.
46. Raabe, T., J. Riesgo-Escovar, X. Liu, B. S. Bausenwein, P. Deak, P. Maroy, and E. Hafen. 1996. DOS, a novel pleckstrin homology domain-containing protein required for signal transduction between sevenless and Ras1 in Drosophila. Cell 85:911-920.
47. Robb, L., N. J. Elwood, A. G. Elefanty, F. Kontgen, R. Li, L. D. Barnett, and C. G. Begley. 1996. The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J. 15:4123-4129.
48. Saxton, T. M., M. Henkemeyer, S. Gasca, R. Shen, F. Shalaby, G. S. Feng, and T. Pawson. 1997. Abnormal mesoderm patterning and tyrosine kinase signalling in mouse embryos mutant for the SH2 tyrosine phosphatase Shp-2. EMBO J. 16:2352-2364.
49. Schmitt, R. M., E. Bruyns, and H. R. Snodgrass. 1991. Hematopoietic development of embryonic stem cells in vitro: cytokine and receptor gene expression. Genes Dev. 5:728-740.
50. Shultz, L. D. 1988. Pleiotropic effects of deleterious alleles at the "motheaten" locus. Curr. Top. Microbiol. Immunol. 137:216-222.
51. Shultz, L. D., C. L. Bailey, and D. R. Coman. 1983. Hematopoietic stem cell function in motheaten mice. Exp. Hematol. 11:667-680.
52. Shultz, L. D., P. A. Schweitzer, T. V. Rajan, T. Yi, J. N. Ihle, R. J. Matthews, M. L. Thomas, and D. R. Beier. 1993. Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene. Cell 73:1445-1454.
53. Sugimoto, S., T. J. Wandless, S. E. Shoelson, B. G. Neel, and C. T. Walsh. 1994. Activation of the SH2-containing protein tyrosine phosphatase, SH-PTP2, by phosphotyrosine-containing peptides derived from insulin receptor substrate-1. J. Biol. Chem. 269:13614-13622.
54. Sun, H., and N. K. Tonks. 1994. The coordinated action of protein tyrosine phosphatases and kinases in cell signaling. Trends Biochem. Sci. 19:480-485.
55. Tang, T. L., R. Freeman, Jr., A. M. O'Reilly, B. G. Neel, and S. Y. Sokol. 1995. The SH2-containing protein-tyrosine phosphatase SH-PTP2 is required upstream of MAP kinase for early Xenopus development. Cell 80: 473-483.
56. Tauchi, T., J. E. Damen, K. Toyama, G. S. Feng, H. E. Broxmeyer, and G. Krystal. 1996. Tyrosine 425 within the activated erythropoietin receptor binds Syp, reduces the erythropoietin required for Syp tyrosine phosphorylation, and promotes mitogenesis. Blood 87:4495-4501.
57. Tauchi, T., G. S. Feng, M. S. Marshall, R. Shen, C. Mantel, T. Pawson, and H. E. Broxmeyer. 1994. The ubiquitously expressed Syp phosphatase interacts with c-kit and Grb2 in hematopoietic cells. J. Biol. Chem. 269:25206-25211.
58. Tauchi, T., G. S. Feng, R. Shen, M. Hoatlin, G. Bagby, Jr., D. Rabat, L. Lu, and H. E. Broxmeyer. 1995. Involvement of SH2-containing phosphotyrosine phosphatase Syp in erythropoietin receptor signal transduction pathways. J. Biol. Chem. 270:5631-5635.
59. Townley, R., S. H. Shen, D. Banville, and C. Ramachandran. 1993. Inhibition of the activity of protein tyrosine phosphate 1C by its SH2 domains. Biochemistry 32:13414-13418.
60. Tsai, F. Y., G. Keller, F. C. Kuo, M. Weiss, J. Chen, M. Rosenblatt, F. W. Alt, and S. H. Orkin. 1994. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371:221-226.
61. Tsui, F. W., and H. W. Tsui. 1994. Molecular basis of the motheaten phenotype. Immunol. Rev. 138:185-206.
62. Tsui, H. W., K. A. Siminovitch, L. de Souza, and F. W. Tsui. 1993. Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene. Nat. Genet. 4:124-129.
63. Vogel, W., R. Lammers, J. Huang, and A. Ullrich. 1993. Activation of a phosphotyrosine phosphatase by tyrosine phosphorylation. Science 259:1611-1614.
64. Weiss, M. J., G. Keller, and S. H. Orkin. 1994. Novel insights into erythroid development revealed through in vitro differentiation of GATA-1 embryonic stem cells. Genes Dev. 8:1184-1197.
65. Weiss, M. J., and S. H. Orkin. 1996. In vitro differentiation of murine embryonic stem cells. New approaches to old problems. J. Clin. Invest. 97:591-595.
66. Welham, M. J., U. Dechert, K. B. Leslie, F. Jirik, and J. W. Schrader. 1994. Interleukin (IL)-3 and granulocyte/macrophage colony-stimulating factor, but not IL-4, induce tyrosine phosphorylation, activation, and association of SHPTP2 with Grb2 and phosphatidylinositol 3′-kinase. J. Biol. Chem. 269: 23764-23768.
67. Wiles, M. V., and G. Keller. 1991. Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development 111:259-267.
68. Wulf, G. M., C. N. Adra, and B. Lim. 1993. Inhibition of hematopoietic development from embryonic stem cells by antisense vav RNA. EMBO J. 12:5065-5074.
69. Wurst, W., and A. L. Joyner. 1993. Production of targeted embryonic stem cell clones, p. 33-62. In A. L. Joyner (ed.), Gene targeting: a practical approach. IRL Press, Oxford, United Kingdom.
70. Xiao, S., D. W. Rose, T. Sasaoka, H. Maegawa, T. Burke, Jr., P. P. Roller, S. E. Shoelson, and J. M. Olefsky. 1994. Syp (SH-PTP2) is a positive mediator of growth factor-stimulated mitogenic signal transduction. J. Biol. Chem. 269:21244-21248.
71. Yamaguchi, T. P., K. Harpal, M. Henkemeyer, and J. Rossant. 1994. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 8:3032-3044.
72. Yamauchi, K., K. L. Milarski, A. R. Saltiel, and J. E. Pessin. 1995. Protein-tyrosine-phosphatase SHPTP2 is a required positive effector for insulin downstream signaling. Proc. Natl. Acad. Sci. USA 92:664-668.
73. Yi, T., A. L. Mui, G. Krystal, and J. N. Ihle. 1993. Hematopoietic cell phosphatase associates with the interleukin-3 (IL-3) receptor beta chain and down-regulates IL-3-induced tyrosine phosphorylation and mitogenesis. Mol. Cell. Biol. 13:7577-7586.
74. Yi, T., J. Zhang, O. Miura, and J. N. Ihle. 1995. Hematopoietic cell phosphatase associates with erythropoietin (Epo) receptor after Epo-induced receptor tyrosine phosphorylation: identification of potential binding sites. Blood 85:87-95.
75. Yin, T., R. Shen, G. S. Feng, and Y. C. Yang. 1997. Molecular characterization of domains required for the specific interactions between Shp-2 phosphatase and JAK tyrosine kinase. J. Biol. Chem. 272:1032-1037.
76. Zhang, R., F. Y. Tsai, and S. H. Orkin. 1994. Hematopoietic development of vav-/-mouse embryonic stem cells. Proc. Natl. Acad. Sci. USA 91:12755-12759.
77. Zmuidzinas, A., K. D. Fischer, S. A. Lira, L. Forrester, S. Bryant, A. Bernstein, and M. Barbacid. 1995. The vav proto-oncogene is required early in embryogenesis but not for hematopoietic development in vitro. EMBO J. 14:1-11.