The KRAB-associated co-repressor KAP-1 is a coiled-coil binding partner, substrate and activator of the c-Fes protein tyrosine kinase

Biochemical Journal

Volumn 399, Issue 1, 2006, Pages 141-150

  Delfino, Frank J ^a   Shaffer, Jonathan M ^a   Smithgall, Thomas E ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

c Fes; Coiled coil; KAP 1; Non receptor protein tyrosine kinase; Protein protein interaction; Yeast two hybrid system

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; CELLS; CLONING; DNA; ENZYME KINETICS; YEAST;

C-FES; COILED-COIL BINDING PARTNER; KAP-1; PROTEIN-PROTEIN INTERACTION; YEAST TWO-HYBRID SYSTEMS;

ENZYMES;

PROTEIN KINASE; PROTEIN KINASE FES; PROTEIN KRUPPEL ASSOCIATED BOX ASSOCIATED PROTEIN 1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL LINE; DNA-BINDING PROTEINS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INSECTS; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-FES; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SUBSTRATE SPECIFICITY;

EID: 33749389961     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20060194     Document Type: Article

References (54)

1. Lee, W. H., Bister, K., Pawson, A., Robins, T., Moscovici, C. and Duesberg, P. H. (1980) Fujinami sarcoma virus: an avian RNA tumor virus with a unique transforming gene. Proc. Natl. Acad. Sci. U.S.A. 77, 2018-2022
2. Groffen, J., Heisterkamp, N., Shibuya, M., Hanafusa, H. and Stephenson, J. R. (1983) Transforming genes of avian (v-fps) and mammalian (v-fes) retroviruses correspond to a common cellular locus. Virology 125, 480-486
3. Hampe, A., Laprevotte, I., Galibert, F., Fedele, L. A. and Sherr, C. J. (1982) Nucleotide sequences of feline retroviral oncogenes (v-fes) provide evidence for a family of tyrosine-specific protein kinase genes. Cell 30, 775-785
4. Hanafusa, T., Wang, L. H., Anderson, S. M., Karess, R. E., Hayward, W. S. and Hanafusa, H. (1980) Characterization of the transforming gene of Fujinami sarcoma virus. Proc. Natl. Acad. Sci. U.S.A. 77, 3009-3013
5. Huang, C. C., Hammond, C. and Bishop, J. M. (1984) Nucleotide sequence of v-fps in the PRCII strain of avian sarcoma virus. J. Virol. 50, 125-131
6. Smithgall, T. E., Yu, G. and Glazer, R. I. (1988) Identification of the differentiation-associated p93 tyrosine protein kinase of HL-60 leukaemia cells as the product of the human c-fes locus and its expression in myelomonocytic cells. J. Biol. Chem. 263, 15050-15055
7. MacDonald, I., Levy, J. and Pawson, T. (1985) Expression of the mammalian c-fes protein in hematopoietic cells and identification of a distinct fes-related protein. Mol. Cell. Biol. 5, 2543-2551
8. Feldman, R. A., Gabrilove, J. L., Tam, J. P., Moore, M. A. and Hanafusa, H. (1985) Specific expression of the human cellular fps/fes-encoded protein NCP92 in normal and leukemic myeloid cells. Proc. Natl. Acad. Sci. U.S.A. 82, 2379-2383
9. Greer, P., Haigh, J., Mbamalu, G., Khoo, W., Bernstein, A. and Pawson, T. (1994) The Fps/Fes protein-tyrosine kinase promotes angiogenesis in transgenic mice. Mol. Cell. Biol. 14, 6755-6763
10. Haigh, J., McVeigh, J. and Greer, P. (1996) The fps/fes tyrosine kinase is expressed in myeloid, vascular endothelial, epithelial and neuronal cells and is localized in the trans-golgi network. Cell Growth Differ. 7, 931-944
11. Shibata, A., Laurent, C. E. and Smithgall, T. E. (2003) The c-Fes protein-tyrosine kinase accelerates NGF-induced differentiation of PC12 cells through a PI3K-dependent mechanism. Cell. Signal. 15, 279-288
12. Park, W. Y., Ahn, J. H., Feldman, R. A. and Seo, J. S. (1998) c-Fes tyrosine kinase binds to and activates STAT3 after granulocyte-macrophage colony-stimulating factor stimulation. Cancer Lett. 129, 29-37
13. Matsuda, T., Fukada, T., Takahashi-Tezuka, M., Okuyama, Y., Fujitani, Y., Hanazono, Y., Hirai, H. and Hirano, T. (1995) Activation of Fes tyrosine kinase by gp130, an interleukin-6 family cytokine signal transducer, and their association. J. Biol. Chem. 270, 11037-11039
14. Kanda, S., Lerner, E. C., Tsuda, S., Shono, T., Kanetake, H. and Smithgall, T. E. (2000) The nonreceptor protein-tyrosine kinase c-Fes is involved in fibroblast growth factor-2-induced chemotaxis of murine brain capillary endothelial cells. J. Biol. Chem. 275, 10105-10111
15. Jiang, H., Foltenyi, K., Kashiwada, M., Donahue, L., Vuong, B., Hehn, B. and Rothman, P. (2001) Fes mediates the IL-4 activation of insulin receptor substrate-2 and cellular proliferation. J. Immunol. 166, 2627-2634
16. Izuhara, K., Feldman, R. A., Greer, P. and Harada, N. (1994) Interaction of the c-fes proto-oncogene product with the interleukin-4 receptor. J. Biol. Chem. 269, 18623-18629
17. Hanazono, Y., Chiba, S., Sasaki, K., Mano, H., Miyajima, A., Arai, K., Yazaki, Y. and Hirai, H. (1993) c-fps/fes protein-tyrosine kinase is implicated in a signalling pathway triggered by granulocyte-macrophage colony-stimulating factor and interleukin-3. EMBO J. 12, 1641-1646
18. Brizzi, M. F., Aronica, M. G., Rosso, A., Bagnara, G. P., Yarden, Y. and Pegoraro, L. (1996) Granulocyte-macrophage colony-stimulating factor stimulates JAK2 signalling pathway and rapidly activates p93fes, STAT1 p91, and STAT3 p92 in polymorphonuclear leukocytes. J. Biol. Chem. 271, 3562-3567
19. Greer, P. (2002) Closing in on the biological functions of Fps/Fes and Fer. Nat. Rev. Mol. Cell. Biol. 3, 278-289
20. Smithgall, T. E., Rogers, J. A., Peters, K. L., Li, J., Briggs, S. D., Lionberger, J. M., Cheng, H., Shibata, A., Scholtz, B., Schreiner, S. and Dunham, N. (1998) The c-Fes family of protein-tyrosine kinases. Crit. Rev. Oncog. 9, 43-62
21. Manfredini, R., Balestri, R., Tagliafico, E., Trevisan, F., Pizzanelli, M., Grande, A., Barbieri, D., Zucchini, P., Citro, G., Franceschi, C. and Ferrari, S. (1997) Antisense inhibition of c-fes proto-oncogene blocks PMA-induced macrophage differentiation in HL60 and in FDC-P1/MAC-11 cells. Blood 89, 135-145
22. Cheng, H. Y., Schiavone, A. P. and Smithgall, T. E. (2001) A point mutation in the N-terminal CC domain releases c-Fes tyrosine kinase activity and survival signalling in myeloid leukemia cells. Mol. Cell. Biol. 21, 6170-6180
23. Kim, J. and Feldman, R. A. (2002) Activated Fes protein tyrosine kinase induces terminal macrophage differentiation of myeloid progenitors (U937 cells) and activation of the transcription factor PU.1. Mol. Cell. Biol. 22, 1903-1918
24. Cheng, H., Rogers, J. A., Dunham, N. A. and Smithgall, T. E. (1999) Regulation of c-Fes tyrosine kinase and biological activities by N-terminal coiled-coil oligomerization domains. Mol. Cell. Biol. 19, 8335-8343
25. Yu, G., Smithgall, T. E. and Glazer, R. I. (1989) K562 leukemia cells transfected with the human c-fes gene acquire the ability to undergo myeloid differentiation. J. Biol. Chem. 264, 10276-10281
26. Smithgall, T. E. (1998) Signal transduction pathways regulating hematopoietic differentiation. Pharmacol. Rev. 50, 1-19
27. Read, R. D., Lionberger, J. M. and Smithgall, T. E. (1997) Oligomerization of the Fes tyrosine kinase. Evidence for a coiled-coil domain in the unique N-terminal region. J. Biol. Chem. 272, 18498-18503
28. Lupas, A. (1996) Coiled coils: new structures and new functions. Trends Biochem. Sci. 21, 375-382
29. Kim, S. S., Chen, Y. M., O'Leary, E., Witzgall, R., Vidal, M. and Bonventre, J. V. (1996) A novel member of the RING finger family, KRIP-1, associates with the KRAB-A transcriptional repressor domain of zinc finger proteins. Proc. Natl. Acad. Sci. U.S.A. 93, 15299-15304
30. Moosmann, P., Georgiev, O., Le Douarin, B., Bourquin, J. P. and Schaffner, W. (1996) Transcriptional repression by RING finger protein TIF1 beta that interacts with the KRAB repressor domain of KOX1. Nucleic Acids Res. 24, 4859-4867
31. Friedman, J. R., Fredericks, W. J., Jensen, D. E., Speicher, D. W., Huang, X. P., Neilson, E. G. and Rauscher, III, F. J. (1996) KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes Dev. 10, 2067-2078
32. Nielsen, A. L., Ortiz, J. A., You, J., Oulad-Abdelghani, M., Khechumian, R., Gansmuller, A., Chambon, P. and Losson, R. (1999) Interaction with members of the heterochromatin protein 1 (HP1) family and histone deacetylation are differentially involved in transcriptional silencing by members of the TIF1 family. EMBO J. 18, 6385-6395
33. Lechner, M. S., Begg, G. E., Speicher, D. W. and Rauscher, III, F. J. (2000) Molecular determinants for targeting heterochromatin protein 1-mediated gene silencing: direct chromoshadow domain-KAP-1 corepressor interaction is essential. Mol. Cell. Biol. 20, 6449-6465
34. Underbill, C., Qutob, M. S., Yee, S. P. and Torchia, J. (2000) A novel nuclear receptor corepressor complex, N-CoR, contains components of the mammalian SWI/SNF complex and the corepressor KAP-1. J. Biol. Chem. 275, 40463-40470
35. Schultz, D. C., Friedman, J. R. and Rauscher, III, F. J. (2001) Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2α subunit of NuRD. Genes Dev. 15, 428-443
36. Schultz, D. C., Ayyanathan, K., Negorev, D., Maul, G. G. and Rauscher, III, F. J. (2002) SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 16, 919-932
37. Kushnirov, V. V. (2000) Rapid and reliable protein extraction from yeast. Yeast 16, 857-860
38. Rogers, J. A., Read, R. D., Li, J., Peters, K. L. and Smithgall, T. E. (1996) Autophosphorylation of the Fes tyrosine kinase. Evidence for an intermolecular mechanism involving two kinase domain tyrosine residues. J. Biol. Chem. 271, 17519-17525
39. Lozzio, B. B., Lozzio, C. B., Bamberger, E. G. and Feliu, A. S. (1981) A multipotential leukemia cell line (K-562) of human origin. Proc. Soc. Exp. Biol. Med. 166, 546-550
40. Lupas, A. (1996) Prediction and analysis of coiled-coil structures. Methods Enzymol. 266, 513-525
41. Li, J. and Smithgall, T. E. (1996) Co-expression with BCR induces activation of the FES tyrosine kinase and phosphorylation of specific N-terminal BCR tyrosine residues. J. Biol. Chem. 271, 32930-32936
42. O'Shea, E. K., Klemm, J. D., Kim, P. S. and Alber, T. (1991) X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science 254, 539-544
43. Takashima, Y., Delfino, F. J., Engen, J. R., Superti-Furga, G. and Smithgall, T. E. (2003) Regulation of c-Fes tyrosine kinase activity by coiled-coil and SH2 domains: analysis with Saccharomyces cerevisiae. Biochemistry 42, 3567-3574
44. Peng, H., Begg, G. E., Schultz, D. C., Friedman, J. R., Jensen, D. E., Speicher, D. W. and Rauscher, III, F. J. (2000) Reconstitution of the KRAB-KAP-1 repressor complex: a model system for defining the molecular anatomy of RING-B box-coiled-coil domain-mediated protein-protein interactions. J. Mol. Biol. 295, 1139-1162
45. Lionberger, J. M. and Smithgall, T. E. (2000) The c-Fes protein-tyrosine kinase suppresses cytokine-independent outgrowth of myeloid leukemia cells induced by Bcr-Abl. Cancer Res. 60, 1097-1103
46. Zhao, X., Ghaffari, S., Lodish, H., Malashkevich, V. N. and Kim, P. S. (2002) Structure of the Bcr-Abl oncoprotein oligomerization domain. Nat. Struct. Biol. 9, 117-120
47. Nelson, K. L., Rogers, J. A., Bowman, T. L., Jove, R. and Smithgall, T. E. (1998) Activation of STAT3 by the c-Fes protein-tyrosine kinase. J. Biol. Chem. 273, 7072-7077
48. Senis, Y., Zirngibl, R., McVeigh, J., Haman, A., Hoang, T. and Greer, P. A. (1999) Targeted disruption of the murine fps/fes proto-oncogene reveals that Fps/Fes kinase activity is dispensable for hematopoiesis. Mol. Cell. Biol. 19, 7436-7446
49. Kim, J., Ogata, Y., Ali, H. and Feldman, R. A. (2004) The Fes tyrosine kinase: a signal transducer that regulates myeloid-specific gene expression through transcriptional activation. Blood Cells Mol. Dis. 32, 302-308
50. McLemore, M. L., Grewal, S., Liu, F., Archambault, A., Poursine-Laurent, J., Haug, J. and Link, D. C. (2001) STAT-3 activation is required for normal G-CSF-dependent proliferation and granulocytic differentiation. Immunity 14, 193-204
51. Zhang, D. E., Zhang, P., Wang, N. D., Hetherington, C. J., Darlington, G. J. and Tenen, D. G. (1997) Absence of granulocyte colony-stimulating factor signalling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 94, 569-574
52. Henkel, G. W., McKercher, S. R., Yamamoto, H., Anderson, K. L., Oshima, R. G. and Maki, R. A. (1996) PU.1 but not ets-2 is essential for macrophage development from embryonic stem cells. Blood 88, 2917-2926
53. Tagliafico, E., Siena, M., Zanocco-Marani, T., Manfredini, R., Tenedini, E., Montanari, M., Grande, A. and Ferrari, S. (2003) Requirement of the coiled-coil domains of p92 c-Fes for nuclear localization in myeloid cells upon induction of differentiation. Oncogene 22, 1712-1723
54. Schwartz, Y., Ben-Dor, I., Navon, A., Motro, B. and Nir, U. (1998) Tyrosine phosphorylation of the TATA element modulatory factor by the FER nuclear tyrosine kinases. FEBS Lett. 434, 339-345