Spatial and temporal changes in the subcellular localization of the nuclear protein-tyrosine kinase, c-Fes

DNA and Cell Biology

Volumn 24, Issue 4, 2005, Pages 225-234

  Carlson, Anne ^a   Yates, Karen E ^b   Slamon, Dennis J ^a   Gasson, Judith C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PROTEASOME; PROTEIN KINASE FES; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL STRAIN HL 60; CELL STRAIN U937; CELL TYPE; CENTROMERE; CHROMOSOME; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HELA CELL; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTERPHASE; METAPHASE; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ANIMALS; CELL NUCLEUS; CELLS, CULTURED; CENTROMERE; CYTOPLASM; DNA PRIMERS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; KINETOCHORES; MICE; MICROSCOPY, CONFOCAL; MITOSIS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-FES;

ANIMALIA;

EID: 16844383754     PISSN: 10445498     EISSN: None     Source Type: Journal    
DOI: 10.1089/dna.2005.24.225     Document Type: Article

References (63)

1. ANDRADE, L.E., CHAN, E.K., RASKA, I., PEEBLES, C.L., ROOS, G., and TAN, E.M. (1991). Human autoantibody to a novel protein of the nuclear coiled body: Immunological characterization and cdna cloning of p80-coilin. J. Exp. Med. 173, 1407-1419.
2. ASPENSTROM, P. (1997). A cdc42 target protein with homology to the non-kinase domain of fer has a potential role in regulating the actin cytoskeleton. Curr. Biol. 7, 479-487.
3. BARBACID, M. (1981). Cellular transformation by subgenomic feline sarcoma virus DNA. J. Virol. 37, 518-523.
4. BEN-DOR, I., BERN, O., TENNENBAUM, T., and NIR, U. (1999). Cell cycle-dependent nuclear accumulation of the p94fer tyrosine kinase is regulated by its nh2 terminus and is affected by kinase domain integrity and atp binding. Cell Growth Differ. 10, 113-129.
5. BOLLEN, M., and BEULLENS, M. (2002). Signaling by protein phosphatases in the nucleus. Trends Cell Biol. 12, 138-145.
6. BORELLINI, F., HE, Y.F., AQUINO, A., YU, G., JOSEPHS, S.F., and GLAZER, R.I. (1991). Increased DNA binding and transcriptional activity associated with transcription factor sp1 in k562 cells transfected with the myeloid-specific c-fes tyrosine kinase gene. J. Biol. Chem. 266, 15850-15854.
7. BRIZZI, M.F., ARONICA, M.G., ROSSO, A., BAGNARA, G.P., YARDEN, Y., and PEGORARO, L. (1996). Granulocyte-macrophage colony-stimulating factor stimulates jak2 signaling pathway and rapidly activates p93fes, stat1 p91, and stat3 p92 in polymorphonuclear leukocytes. J. Biol. Chem. 271, 3562-3567.
8. CANS, C., MANGANO, R., BARILA, D., NEUBAUER, G., and SUPERTI-FURGA, G. (2000). Nuclear tyrosine phosphorylation: The beginning of a map. Biochem. Pharmacol. 60, 1203-1215.
9. CHAN, E.K., TAKANO, S., and VON MUHLEN, C.A. (1994). A microscale method for depleting cross-reactive anti-antibodies used in indirect immunofluorescence microscopy. J. Immunol. Methods 176, 271-273.
10. CRAIG, A.W., ZIRNGIBL, R., and GREER, P. (1999). Disruption of coiled-coil domains in fer protein-tyrosine kinase abolishes trimerization but not kinase activation. J. Biol. Chem. 274, 19934-19942.
11. DAUM, J.R., TUGENDREICH, S., TOPPER, L.M., JORGENSEN, P.M., HOOG, C., HIETER, P., and GORBSKY, G.J. (2000). The 3f3/2 anti-phosphoepitope antibody binds the mitotically phosphorylated anaphase-promoting complex/cyclosome. Curr. Biol. 10, R850-R852.
12. DYCK, J.A., MAUL, G.G., MILLER, W.H., JR., CHEN, J.D., KAKIZUKA, A., and EVANS, R.M. (1994). A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein. Cell 76, 333-343.
13. EARNSHAW, W., BORDWELL, B., MARINO, C., and ROTHFIELD, N. (1986). Three human chromosomal autoantigens are recognized by sera from patients with anti-centromere antibodies. J. Clin. Invest. 77, 426-430.
14. EMILIA, G., DONELLI, A., FERRARI, S., TORELLI, U., SELLERI, L., ZUCCHINI, P., MORETTI, L., VENTURELLI, D., CECCHERELLI, G., and TORELLI, G. (1986). Cellular levels of mrna from c-myc, c-myb and c-fes one-genes in normal myeloid and erythroid precursors of human bone marrow: An in situ hybridization study. Br. J. Haematol. 62, 287-292.
15. 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. USA 82, 2379-2383.
16. FERRARI, S., TORELLI, U., SELLERI, L., DONELLI, A., VENTURELLI, D., MORETTI, L., and TORELLI, G. (1985). Expression of human c-fes one-gene occurs at detectable levels in myeloid but not in lymphoid cell populations. Br. J. Haematol. 59, 21-25.
17. FERRARI, S., DONELLI, A., MANFREDINI, R., SARTI, M., RONCAGLIA, R., TAGLIAFICO, E., ROSSI, E., TORELLI, G., and TORELLI, U. (1990). Differential effects of c-myb and c-fes antisense oligodeoxynucleotides on granulocytic differentiation of human myeloid leukemia hl60 cells. Cell Growth Differ. 1, 543-548.
18. FOSTER, D.A., SHIBUYA, M., and HANAFUSA, H. (1985). Activation of the transformation potential of the cellular fps gene. Cell 42, 105-115.
19. FU, X.D., and MANIATIS, T. (1990). Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature 343, 437-441.
20. GALL, J.G., BELLINI, M., WU, Z., and MURPHY, C. (1999). Assembly of the nuclear transcription and processing machinery: Cajal bodies (coiled bodies) and transcriptosomes. Mol. Biol. Cell 10, 4385-4402.
21. GORBSKY, G.J., and RICKETTS, W.A. (1993). Differential expression of a phosphoepitope at the kinetochores of moving chromosomes. J. Cell Biol. 122, 1311-1321.
22. GREER, P.A., MECKLING-HANSEN, K., and PAWSON, T. (1988). The human c-fps/fes gene product expressed ectopically in rat fibroblasts is nontransforming and has restrained protein-tyrosine kinase activity. Mol. Cell. Biol. 8, 578-587.
23. 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.
24. HACKENMILLER, R., and SIMON, M.C. (2002). Truncation of c-fes via gene targeting results in embryonic lethality and hyperproliferation of hematopoietic cells. Dev. Biol. 245, 255-269.
25. HANAZONO, Y., CHIBA, S., SASAKI, K., MANO, H., MIYAJIMA, A., ARAI, K., YAZAKI, Y., and HIRAI, H. (1993a). C-fps/fes protein-tyrosine kinase is implicated in a signaling pathway triggered by granulocyte-macrophage colony-stimulating factor and interleukin-3. EMBO J. 12, 1641-1646.
26. HANAZONO, Y., CHIBA, S., SASAKI, K., MANO, H., YAZAKI, Y., and HIRAI, H. (1993b). Erythropoietin induces tyrosine phosphorylation and kinase activity of the c-fps/fes proto-oncogene product in human erythropoietin-responsive cells. Blood 81, 3193-3196.
27. HARTMANN, A.M., NAYLER, O., SCHWAIGER, F.W., OBERMEIER, A., and STAMM, S. (1999). The interaction and colocalization of sam68 with the splicing-associated factor yt521-b in nuclear dots is regulated by the src family kinase p59(fyn). Mol. Biol. Cell 10, 3909-3926.
28. HE, Y., BORELLINI, F., KOCH, W.H., HUANG, K.X., and GLAZER, R.I. (1996). Transcriptional regulation of c-fes in myeloid leukemia cells. Biochim. Biophys. Acta 1306, 179-186.
29. 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.
30. KELLER, P., PAYNE, J.L., TREMML, G., GREER, P.A., GABOLI, M., PANDOLFI, P.P., and BESSLER, M. (2001). Fes-cre targets phosphatidylinositol glycan class a (piga) inactivation to hematopoietic stem cells in the bone marrow. J. Exp. Med. 194, 581-589.
31. 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.
32. KIM, J., OGATA, Y., and FELDMAN, R.A. (2003). Fes tyrosine kinase promotes survival and terminal granulocyte differentiation of factor-dependent myeloid progenitors (32d) and activates lineage-specific transcription factors. J. Biol. Chem. 278, 14978-14984.
33. 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.
34. KIM, L., and WONG, T.W. (1995). The cytoplasmic tyrosine kinase fer is associated with the catenin-like substrate pp120 and is activated by growth factors. Mol. Cell Biol. 15, 4553-4561.
35. LAMOND, A.I., and EARNSHAW, W.C. (1998). Structure and function in the nucleus. Science 280, 547-553.
36. LANFRANCONE, L., MANNONI, P., PEBUSQUE, M.J., CARE, A., PESCHLE, C., GRIGNAMI, F., and PELICCI, P.G. (1989). Expression pattern of c-fes oncogene mrna in human myeloid cells. Int. J. Cancer Suppl. 4, 35-38.
37. LIU, Q., and DREYFUSS, G. (1996). A novel nuclear structure containing the survival of motor neurons protein. EMBO J. 15, 3555-3565.
38. 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.
39. MANFREDINI, R., BALESTRI, R., TAGLIAFICO, E., TREVISAN, F., PIZZANELLI, M., GRANDE, A., BARBIERI, D., ZUCCHINI, P., CITRO, G., FRANCESCHI, C., et al. (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.
40. MATERA, A.G. (1999). Nuclear bodies: Multifaceted subdomains of the interchromatin space. Trends Cell Biol. 9, 302-309.
41. 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.
42. MITSUI, N., INATOME, R., TAKAHASHI, S., GOSHIMA, Y., YAMAMURA, H., and YANAGI, S. (2002). Involvement of fes/fps tyrosine kinase in semaphorin3a signaling. EMBO J. 21, 3274-3285.
43. NICKLAS, R.B. (1997). How cells get the right chromosomes. Science 275, 632-637.
44. 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.
45. PENDERGAST, A.M. (1996). Nuclear tyrosine kinases: From abl to wee1. Curr. Opin. Cell Biol. 8, 174-181.
46. PLATANI, M., GOLDBERG, I., SWEDLOW, J.R., and LAMOND, A.I. (2000). In vivo analysis of cajal body movement, separation, and joining in live human cells. J. Cell Biol. 151, 1561-1574.
47. RASKA, I., ANDRADE, L.E., OCHS, R.L., CHAN, E.K., CHANG, C.M., ROOS, G., and TAN, E.M. (1991). Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Exp. Cell Res. 195, 27-37.
48. 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.
49. SANGRAR, W., GAO, Y., ZIRNGIBL, R.A., SCOTT, M.L., and GREER, P.A. (2003). The fps/fes proto-oncogene regulates hematopoietic lineage output. Exp. Hematol. 31, 1259-1267.
50. SENIS, Y.A., CRAIG, A.W., and GREER, P.A. (2003). Fps/fes and fer protein-tyrosinekinases play redundant roles in regulating hematopoiesis. Exp. Hematol. 31, 673-681.
51. 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.
52. SHIBUYA, M., and HANAFUSA, H. (1982). Nucleotide sequence of fujinami sarcoma virus: Evolutionary relationship of its transforming gene with transforming genes of other sarcoma viruses. Cell 30, 787-795.
53. SLAMON, D.J., DEKERNION, J.B., VERMA, I.M., and CLINE, M.J. (1984). Expression of cellular oncogenes in human malignancies. Science 224, 256-262.
54. SMITHGALL, T.E., YU, G., and GLAZER, R.I. (1988). Identification of the differentiation-associated p93 tyrosine protein kinase of hl-60 leukemia cells as the product of the human c-fes locus and its expression in myelomonocytic cells. J. Biol. Chem. 263, 15050-15055.
55. TAAGEPERA, S., RAO, P.N., DRAKE, F.H., and GORBSKY, G.J. (1993). DNA topoisomerase ii alpha is the major chromosome protein recognized by the mitotic phosphoprotein antibody mpm-2. Proc. Natl. Acad. Sci. USA 90, 8407-8411.
56. TAAGEPERA, S., CAMPBELL, M.S., and GORBSKY, G.J. (1995). Cell-cycle-regulated localization of tyrosine and threonine phospho-epitopes at the kinetochores of mitotic chromosomes. Exp. Cell Res. 221, 249-260.
57. 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.
58. TAKAHASHI, S., INATOME, R., HOTTA, A., QIN, Q., HACKENMILLER, R., SIMON, M.C., YAMAMURA, H., and YANAGI, S. (2003). Role for fes/fps tyrosine kinase in microtubule nucleation through is fes/cip4 homology domain. J. Biol. Chem. 278, 49129-49133.
59. WALKER, L., LYNCH, M., SILVERMAN, S., FRASER, J., BOULTER, J., WEINMASTER, G., and GASSON, J.C. (1999). The notch/jagged pathway inhibits proliferation of human hematopoietic progenitors in vitro. Stem Cells 17, 162-171.
60. YATES, K.E., LYNCH, M.R., WONG, S.G., SLAMON, D.J., and GASSON, J.C. (1995). Human c-fes is a nuclear tyrosine kinase. Oncogene 10, 1239-1242.
61. YATES, K.E., CROOKS, G.M., and GASSON, J.C. (1996). Analysis of fes kinase activity in myeloid cell growth and differentiation. Stem Cells 14, 714-724.
62. 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.
63. ZIRNGIBL, R., SCHULZE, D., MIRSKI, S.E., COLE, S.P., and GREER, P.A. (2001). Subcellular localization analysis of the closely related fps/fes and fer protein-tyrosine kinases suggests a distinct role for fps/fes in vesicular trafficking. Exp. Cell. Res. 266, 87-94.