Tyrosine Phosphorylation of BCR by FPS/FES Protein-tyrosine Kinases Induces Association of BCR with GRB-2/SOS

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 1995 Feb 1

PMID 7529874

Citations 9

Authors

Y Maru

K L Peters

D E Afar

M Shibuya

O N Witte

T E Smithgall

Affiliations

Soon will be listed here.

Abstract

The human bcr gene encodes a protein with serine/threonine kinase activity, CDC24/dbl homology, a GAP domain, and an SH2-binding region. However, the precise physiological functions of BCR are unknown. Coexpression of BCR with the cytoplasmic protein-tyrosine kinase encoded by the c-fes proto-oncogene in Sf-9 cells resulted in stable BCR-FES protein complex formation and tyrosine phosphorylation of BCR. Association involves the SH2 domain of FES and a novel binding domain localized to the first 347 amino acids of the FES N-terminal region. Deletion of the homologous N-terminal BCR-binding domain from v-fps, a fes-related transforming oncogene, abolished transforming activity and tyrosine phosphorylation of BCR in vivo. Tyrosine phosphorylation of BCR in v-fps-transformed cells induced its association with GRB-2/SOS, the RAS guanine nucleotide exchange factor complex. These data provide evidence that BCR couples the cytoplasmic protein-tyrosine kinase and RAS signaling pathways.

Citing Articles

Molecular processes involved in B cell acute lymphoblastic leukaemia.

Malouf C, Ottersbach K Cell Mol Life Sci. 2017; 75(3):417-446.

PMID: 28819864 PMC: 5765206. DOI: 10.1007/s00018-017-2620-z.

Expression, purification and preliminary crystallographic studies on the catalytic region of the nonreceptor tyrosine kinase Fes.

Gnemmi I, Scotti C, Cappelletti D, Canonico P, Condorelli F, Rosano C Acta Crystallogr Sect F Struct Biol Cryst Commun. 2006; 63(Pt 1):18-20.

PMID: 17183165 PMC: 2330100. DOI: 10.1107/S1744309106051682.

Enhanced endotoxin sensitivity in fps/fes-null mice with minimal defects in hematopoietic homeostasis.

Zirngibl R, Senis Y, Greer P Mol Cell Biol. 2002; 22(8):2472-86.

PMID: 11909942 PMC: 133716. DOI: 10.1128/MCB.22.8.2472-2486.2002.

Activated Fes protein tyrosine kinase induces terminal macrophage differentiation of myeloid progenitors (U937 cells) and activation of the transcription factor PU.1.

Kim J, Feldman R Mol Cell Biol. 2002; 22(6):1903-18.

PMID: 11865067 PMC: 135606. DOI: 10.1128/MCB.22.6.1903-1918.2002.

Regulation of c-Fes tyrosine kinase and biological activities by N-terminal coiled-coil oligomerization domains.

Cheng H, Rogers J, Dunham N, Smithgall T Mol Cell Biol. 1999; 19(12):8335-43.

PMID: 10567558 PMC: 84918. DOI: 10.1128/MCB.19.12.8335.

References

Muller A, Young J, Pendergast A, Pondel M, Landau N, Littman D . BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol Cell Biol. 1991; 11(4):1785-92. PMC: 359845. DOI: 10.1128/mcb.11.4.1785-1792.1991. View

de Klein A, Van Kessel A, Grosveld G, Bartram C, Hagemeijer A, BOOTSMA D . A cellular oncogene is translocated to the Philadelphia chromosome in chronic myelocytic leukaemia. Nature. 1982; 300(5894):765-7. DOI: 10.1038/300765a0. View

Diekmann D, Brill S, Garrett M, Totty N, Hsuan J, Monfries C . Bcr encodes a GTPase-activating protein for p21rac. Nature. 1991; 351(6325):400-2. DOI: 10.1038/351400a0. View

Ron D, Zannini M, Lewis M, Wickner R, Hunt L, Graziani G . A region of proto-dbl essential for its transforming activity shows sequence similarity to a yeast cell cycle gene, CDC24, and the human breakpoint cluster gene, bcr. New Biol. 1991; 3(4):372-9. View

Pendergast A, Muller A, Havlik M, Maru Y, Witte O . BCR sequences essential for transformation by the BCR-ABL oncogene bind to the ABL SH2 regulatory domain in a non-phosphotyrosine-dependent manner. Cell. 1991; 66(1):161-71. DOI: 10.1016/0092-8674(91)90148-r. View

Abo A, Pick E, Hall A, Totty N, Teahan C, Segal A . Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature. 1991; 353(6345):668-70. DOI: 10.1038/353668a0. View

Maru Y, Witte O . The BCR gene encodes a novel serine/threonine kinase activity within a single exon. Cell. 1991; 67(3):459-68. DOI: 10.1016/0092-8674(91)90521-y. View

Shou C, Farnsworth C, Neel B, Feig L . Molecular cloning of cDNAs encoding a guanine-nucleotide-releasing factor for Ras p21. Nature. 1992; 358(6384):351-4. DOI: 10.1038/358351a0. View

Lowenstein E, Daly R, Batzer A, Li W, Margolis B, Lammers R . The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell. 1992; 70(3):431-42. DOI: 10.1016/0092-8674(92)90167-b. View

10.

Muller A, Pendergast A, Havlik M, Puil L, Pawson T, Witte O . A limited set of SH2 domains binds BCR through a high-affinity phosphotyrosine-independent interaction. Mol Cell Biol. 1992; 12(11):5087-93. PMC: 360442. DOI: 10.1128/mcb.12.11.5087-5093.1992. View

11.

McGlade J, Cheng A, Pelicci G, Pelicci P, Pawson T . Shc proteins are phosphorylated and regulated by the v-Src and v-Fps protein-tyrosine kinases. Proc Natl Acad Sci U S A. 1992; 89(19):8869-73. PMC: 50025. DOI: 10.1073/pnas.89.19.8869. View

12.

Matuoka K, Shibata M, Yamakawa A, Takenawa T . Cloning of ASH, a ubiquitous protein composed of one Src homology region (SH) 2 and two SH3 domains, from human and rat cDNA libraries. Proc Natl Acad Sci U S A. 1992; 89(19):9015-9. PMC: 50055. DOI: 10.1073/pnas.89.19.9015. View

13.

Hart M, Maru Y, Leonard D, Witte O, Evans T, Cerione R . A GDP dissociation inhibitor that serves as a GTPase inhibitor for the Ras-like protein CDC42Hs. Science. 1992; 258(5083):812-5. DOI: 10.1126/science.1439791. View

14.

Rozakis-Adcock M, McGlade J, Mbamalu G, Pelicci G, Daly R, Li W . Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature. 1992; 360(6405):689-92. DOI: 10.1038/360689a0. View

15.

Liu J, Campbell M, Guo J, Lu D, Xian Y, Andersson B . BCR-ABL tyrosine kinase is autophosphorylated or transphosphorylates P160 BCR on tyrosine predominantly within the first BCR exon. Oncogene. 1993; 8(1):101-9. View

16.

Hanazono Y, Chiba S, Sasaki K, Mano H, Miyajima A, Arai K . c-fps/fes protein-tyrosine kinase is implicated in a signaling pathway triggered by granulocyte-macrophage colony-stimulating factor and interleukin-3. EMBO J. 1993; 12(4):1641-6. PMC: 413378. DOI: 10.1002/j.1460-2075.1993.tb05809.x. View

17.

Li N, Batzer A, Daly R, Yajnik V, Skolnik E, Chardin P . Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature. 1993; 363(6424):85-8. DOI: 10.1038/363085a0. View

18.

Gulbins E, Coggeshall K, Baier G, Katzav S, Burn P, Altman A . Tyrosine kinase-stimulated guanine nucleotide exchange activity of Vav in T cell activation. Science. 1993; 260(5109):822-5. DOI: 10.1126/science.8484124. View

19.

Hanazono Y, Chiba S, Sasaki K, Mano H, Yazaki Y, Hirai H . Erythropoietin induces tyrosine phosphorylation and kinase activity of the c-fps/fes proto-oncogene product in human erythropoietin-responsive cells. Blood. 1993; 81(12):3193-6. View

20.

Hjermstad S, Peters K, Briggs S, Glazer R, Smithgall T . Regulation of the human c-fes protein tyrosine kinase (p93c-fes) by its src homology 2 domain and major autophosphorylation site (Tyr-713). Oncogene. 1993; 8(8):2283-92. View