Dimerization of the docking/adaptor protein HEF1 via a carboxy-terminal helix-loop-helix domain

Experimental Cell Research

Volumn 252, Issue 1, 1999, Pages 224-235

  Law, Susan F ^a   Zhang, Yu Zhu ^a   Fashena, Sarah J ^a   Toby, Garabet ^a,b   Estojak, Joanne ^a   Golemis, Erica A ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b MEDITERRANEAN AGRONOMIC INSTITUTE OF CHANIA   (Greece)

Author keywords

Dimerization; HEF1; Helix loop helix (HLH); Id2; Pseudohyphae

Indexed keywords

ADAPTOR PROTEIN; DOCKING PROTEIN; HELIX LOOP HELIX PROTEIN; PROTEIN TYROSINE KINASE;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL DIFFERENTIATION; CELL DIVISION; CONTROLLED STUDY; DIMERIZATION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; YEAST;

EID: 0033544003     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1999.4609     Document Type: Article

References (79)

1. Ishino M., Ohba T., Sasaki H., Sasaki T. Molecular cloning of a cDNA encoding a phosphoprotein, Efs, which contains a Src homology 3 domain and associates with Fyn. Oncogene. 11:1995;2331-2338.
2. Polte T. R., Hanks S. K. Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130Cas. Proc. Natl. Acad. Sci. USA. 92:1995;10678-10682.
3. Law S. F., Estojak J., Wang B., Mysliwiec T., Kruh G. D., Golemis E. A. Human enhancer of filamentation 1 (HEF1), a novel p130Cas-like docking protein, associates with FAK, and induces pseudohyphal growth in yeast. Mol. Cell. Biol. 16:1996;3327-3337.
4. Minegishi M., Tachibana K., Sato T., Iwata S., Nojima Y., Morimoto C. Structure and function of Cas-L, a 105-kD Crk-associated substrate-related protein that is involved in beta-1 integrin-mediated signaling in lymphocytes. J. Exp. Med. 184:1996;1365-1375.
5. Astier A., Manie S., Avraham H., Hirai H., Law S. F., Zhang Y., Golemis E. A., Fu Y., Druker B. J., Haghayeghi N., Freedman A. S., Avraham S. The related adhesion focal tyrosine kinase differentially phosphorylates p130Cas and the Cas-like protein, p105HEF1. J. Biol. Chem. 272:1997;19719-19730.
6. Manie S. N., Beck A. R. P., Astier A., Law S. F., Canty T., Hirai H., Druker B. J., Avraham H., Haghayegi N., Sattler M., Salgia R., Griffin J. D., Golemis E. A., Freedman A. S. Involvement of p130Cas and p105HEF1, a novel Cas-like docking protein, in a cytoskeleton-dependent signaling pathway initiated by ligation of integrin or antigen receptor on human B cells. J. Biol. Chem. 272:1997;4230-4236.
7. Polte T. R., Hanks S. K. Complexes of focal adhesion kinase (FAK) and Crk-associated substrate (p130Cas) are elevated in cytoskeleton-associated fractions following adhesion and Src transformation. J. Biol. Chem. 272:1997;5501-5509.
8. Garton A. J., Flint A. J., Tonks N. K. Identification of p130Cas as a substrate for the cytosolic protein tyrosine phosphatase PTP-PEST. Mol. Cell. Biol. 16:1996;6408-6418.
9. Liu F., Hill D. E., Chernoff J. Direct binding of the proline-rich region of protein tyrosine phosphatase 1B to the Src homology 3 domain of p130Cas. J. Biol. Chem. 271:1996;31290-31295.
10. Garton A. J., Burnham M. R., Bouton A. H., Tonks N. K. Association of PTP-PEST with the SH3 domain of p130Cas; a novel mechanism of protein tyrosine phosphatase substrate recognition. Oncogene. 15:1997;877-885.
11. Ogawa S., Toyoshima H., Kozutsumi H., Hagiwara K., Sakai R., Tanaka T., Hirano N., Mano H., Yazaki Y., Hirai H. The C-terminal SH3 domain of the mouse c-Crk protein negatively regulates tyrosine-phosphorylation of Crk associated p130 in rat 3Y1 cells. Oncogene. 9:1994;1669-1678.
12. Sakai R., Iwamatsu A., Hirano N., Ogawa S., Tanaka T., Mano H., Yazaki Y., Hirai H. A novel signaling molecule, p130, forms stable complexes in vivo with v-Crk and v-Src in a tyrosine phosphorylation-dependent manner. EMBO J. 13:1994;3748-3756.
13. Mayer B. J., Hirai H., Sakai R. Evidence that SH2 domains promote processive phosphorylation by protein-tyrosine kinases. Curr. Biol. 5:1995;296-305.
14. Nojima Y., Morino N., Mimura T., Hamasaki K., Furuya H., Sakai R., Sato T., Tachibana K., Morimoto C., Yazaki Y., Hirai H. Integrin-mediated cell adhesion promotes tyrosine phosphorylation of p130Cas, a Src homology 3-containing molecule having multiple Src homology 2-binding motifs. J. Biol. Chem. 270:1995;15398-15402.
15. Burnham M. R., Harte M. T., Richardson A., Parsons J. T., Bouton A. H. The identification of p130Cas-binding proteins and their role in cellular transformation. Oncogene. 12:1996;2467-2472.
16. Harte M. T., Hildebrand J. D., Burnham M. R., Bouton A. H., Parsons J. T. p130Cas, a substrate associated with v-Src and v-Crk, localizes to focal adhesions and binds to focal adhesion kinase. J. Biol. Chem. 271:1996;13649-13655.
17. Nakamoto T., Sakai R., Ozawa K., Yazaki Y., Hirai H. Direct binding of the C-terminal region of p130-Cas to SH2 and SH3 domains of Src kinase. J. Biol. Chem. 271:1996;8959-8965.
18. Vuori K., Hirai H., Aizawa S., Ruoslahti E. Induction of p130Cas signaling complex formation upon integrin-mediated cell adhesion: a role for Src family kinases. Mol. Cell. Biol. 16:1996;2606-2613.
19. Kron S. J., Styles C. A., Fink G. R. Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Mol. Biol. Cell. 5:1994;1003-1022.
20. Liu H., Styles C. A., Fink G. R. Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science. 262:1993;1741-1744.
21. Roberts R. L., Fink G. R. Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: Mating and invasive growth. Genes Dev. 8:1994;2974-2985.
22. Gimeno C. J., Fink G. R. Induction of pseudohyphal growth by overexpression of PHD1, a Saccharomyces cerevisiae gene related to transcriptional regulators of fungal development. Mol. Cell. Biol. 14:1994;2100-2112.
23. Drubin D. G., Nelson W. J. Origins of cell polarity. Cell. 84:1996;335-344.
24. Biggs J., Murphy E. V., Israel M. A. A human Id-like helix-loop-helix protein expressed during early development. Proc. Natl. Acad. Sci. USA. 89:1992;1512-1516.
25. Hara E., Yamaguchi T., Nojima H., Ide T., Campisi J., Okayama H., Oda K. Id-related genes encoding helix-loop-helix proteins are required for G1 progression and are repressed in senescent human fibroblasts. J. Biol. Chem. 269:1994;2139-2145.
26. Kreider B. L., Benezra R., Rovera G., Kadesch T. Inhibition of myeloid differentiation by the helix-loop-helix protein Id. Science. 255:1992;1700-1702.
27. Barone M. V., Pepperkok R., Peverali F. A., Philipson L. Id proteins control growth induction in mammalian cells. Proc. Natl. Acad. Sci. USA. 91:1994;4985-4988.
28. Iavarone A., Garg P., Lasorella A., Hsu J., Israel M. A. The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev. 8:1994;1270-1284.
29. Peverali F. A., Ramqvist T., Saffrich R., Pepperkok R., Barone M. V., Philipson L. Regulation of G1 progression by E2A and Id helix-loop-helix proteins. EMBO J. 13:1994;4291-4301.
30. Sun X.-H. Constitutive expression of the Id1 gene impairs mouse B cell development. Cell. 79:1994;893-900.
31. Condorelli G., Vitelli L., Valtieri M., Marta I., Montesoro E., Lulli V., Baer R., Peschle C. Coordinate expression and developmental role of Id2 protein and TAL1/E2A heterodimer in erythroid progenitor differentiation. Blood. 86:1995;164-175.
32. Desprez P.-Y., Hara E., Bissell M. J., Campisi J. Suppression of mammary epithelial cell differentiation by the helix-loop-helix protein Id-1. Mol. Cell. Biol. 15:1995;3398-3404.
33. Florio M., Hernandez M. C., Yang H., Shu H. K., Cleveland J. L., Israel M. A. Id2 promotes apoptosis by a novel mechanism independent of dimerization to basic helix-loop-helix factors. Mol. Cell. Biol. 18:1998;5435-5444.
34. Norton J. D., Atherton G. T. Coupling of cell growth control and apoptosis functions of Id proteins. Mol. Cell. Biol. 18:1998;2371-2381.
35. Wary K. K., Mainiero F., Isakoff S. J., Marcantonio E. E., Giancotti F. G. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell. 87:1996;733-743.
36. Law S. F., Zhang Y.-Z., Klein-Szanto A., Golemis E. A. Cell-cycle regulated processing of HEF1 to multiple protein forms differentially targeted to multiple compartments. Mol. Cell. Biol. 18:1998;3540-3551.
37. Gimeno C. J., Ljungdahl P. O., Styles C. A., Fink G. R. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by Starvation and RAS. Cell. 68:1992;1077-1090.
38. Gyuris J., Golemis E. A., Chertkov H., Brent R. Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell. 75:1993;791-803.
39. Estojak J., Brent R., Golemis E. A. Correlation of two-hybrid affinity data with in vitro measurements. Mol. Cell. Biol. 15:1995;5820-5829.
40. Innis M. A., Gelfand D. H., Sninsky J. J., White T. J. Eds. PCR Protocols: A Guide to Methods and Applications. 1990;Academic Press, San Diego.
41. Hu J.-S., Olson E. N., Kingston R. E. HEB, a helix-loop-helix protein related to E2A and ITF2 that can modulate the DNA-binding ability of myogenic regulatory factors. Mol. Cell. Biol. 12:1992;1031-1042.
42. Murre C., McCaw P. S., Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell. 56:1989;777-783.
43. Henthorn P., Kiledjian M., Kadesch T. Two distinct transcription factors that bind the immunoglobulin enhancer μE5/kE2 motif. Science. 247:1990;467-470.
44. Davis R. L., Weintraub H., Lassar A. B. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell. 51:1987;987-1000.
45. Zervos A. S., Gyuris J., Brent R. Mxi1, a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell. 72:1993;223-232.
46. Khazak V., Woychik N., Sadhale P., Brent R., Golemis E. A. Human RNA polymerase II subunit hsRPB7 functions in yeast and influences yeast cell morphology and stress survival. Mol. Biol. Cell. 6:1995;759-775.
47. Kolodziej P. A., Young R. A. Epitope tagging and protein surveillance. Methods Enzymol. 194:1991;508-519.
48. Golemis E. A., Serebriiskii I., Gyuris J., Brent R. Interaction trap/two-hybrid system to identify interacting proteins. Ausubel F. M., Brent R., Kingstonet R. Current Protocols in Molecular Biology. 1997;Wiley, New York.
49. Atchley W. R., Fitch W. M. A natural classification of the basic helix-loop-helix class of transcription factors. Proc. Nat. Acad. Sci. USA. 94:1997;5172-5176.
50. Law, S. F, and, Golemis, E. A, unpublished results.
51. Hamamori Y., Wu H.-Y., Sartorelli V., Kedes L. The basic domain of myogenic basic helix-loop-helix (bHLH) proteins is the novel target for direct inhibition by another bHLH protein, Twist. Mol. Cell. Biol. 17:1997;6563-6573.
52. Zelzer E., Wappner P., Shilo B. Z. The PAS domain confers target gene specificity of Drosophila bHLH/PAS proteins. Genes Dev. 11:1997;2079-2089.
53. Murre C., McCaw P. S., Vaessin H., Caudy M., Jan L. Y., Jan Y. N., Cabrera C. V., Buskin J. N., Hauschka S. D., Lassar A. B., Weintraub H., Baltimore D. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell. 58:1989;537-544.
54. Sun X.-H., Copeland N. G., Jenkins N. A., Baltimore D. Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol. Cell. Biol. 11:1991;5603-5611.
55. Astier A., Manie S. N., Law S. F., Canty T., Hagheyeghi N., Druker B. J., Salgia R., Golemis E. A., Freedman A. S. Association of the Cas-like molecule HEF1 with CrkL following integrin and antigen receptor signaling in B cells. Possible relevance to neoplastic lymphohematopoietic cells. Leukocyte Lymph. 28:1997;65-72.
56. Sattler M., Salgia R., Shrikhande G., Verma S., Uemura N., Law S. F., Golemis E. A., Griffin J. D. Differential signaling after beta1 integrin ligation is mediated through binding of CRKL to p120CBL and p110HEF1. J. Biol. Chem. 272:1997;14320-14326.
57. de Jong R., van Wijk A., Haataja L., Heisterkamp N., Groffen J. BCR/ABL-induced leukemogenesis causes phosphorylation of Hef1 and its association with Crk1. J. Biol. Chem. 272:1997;32649-32655.
58. Ohashi Y., Tachibana K., Kamiguchi K., Fujita H., Morimoto C. T cell receptor-mediated tyrosine phosphorylation of Cas-L, a 105-kDa Crk-associated substrate-related protein, and its association of Crk and C3G. J. Biol. Chem. 273:1998;6446-6451.
59. Reynolds A. B., Kanner S. B., Wang H.-C. R., Parsons J. T. Stable association of activated pp60src with two tyrosine-phosphorylated cellular proteins. Mol. Cell. Biol. 9:1989;3951-3958.
60. Petch L. A., Bockholt S. M., Bouton A., Parsons J. T., Burridge K. Adhesion-induced tyrosine phosphorylation of the p130src substrate. J. Cell Sci. 108:1995;1371-1379.
61. Vuori K., Ruoslahti E. Tyrosine phosphorylation of p130Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J. Biol. Chem. 270:1995;22259-22262.
62. Kanda H., Mimura T., Morino N., Hamasaki K., Nakamoto T., Hirai H., Morimoto C., Yazaki Y., Nojima Y. Ligation of the T cell antigen receptor induces tyrosine phosphorylation of p105CasL, a member of the p130Cas-related docking protein family, and its subsequent binding to the Src homology 2 domain of c-Crk. Eur. J. Immunol. 27:1997;2113-2117.
63. Honda H., Oda H., Nakamoto T., Honda Z., Sakai R., Suzuki T., Saito T., Nakamura K., Nakao K., Ishikawa T., Katsuki M., Yazaki Y., Hirai H. Cardiovascular anomaly, impaired actin bundling and resistance to Src-induced transformation in mice lacking p130Cas. Nature Genet. 19:1998;361-365.
64. Alexandropoulos K., Baltimore D. Coordinate activation of c-Src by SH3- and SH2-binding sites on a novel, p130Cas-related protein, Sin. Genes Dev. 10:1996;1341-1355.
65. Ishino M., Ohba T., Inazawa J., Sasaki H., Ariyama Y., Sasaki T. Identification of an Efs isoform that lacks the SH3 domain and chromosomal mapping of human Efs. Oncogene. 15:1997;1741-1745.
66. Ohba T., Ishino M., Aoto H., Sasaki T. Dot far-Western blot analysis of relative binding affinities of the src homology 3 domains of efs and its related proteins. Anal. Biochem. 262:1998;185-192.
67. Fan C. M., Maniatis T. Generation of the p50 subunit of NF-kappa B by processing of p105 through an ATP-dependent pathway. Nature. 354:1991;395-398.
68. Palombella V. J., Rando O. J., Goldberg A. L., Maniatis T. The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell. 78:1994;773-785.
69. Aza-Blanc P., Ramirez-Weber F.-A., Laget M.-P., Schwartz C., Kornberg T. B. Proteolysis that is inhibited by Hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell. 89:1997;1043-1053.
70. Jiang J., Struhl G. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature. 391:1998;493-496.
71. Ohlmeyer J. T., Kalderon D. Hedgehog stimulates maturation of Cubitus interruptus into a labile transcriptional activator. Nature. 396:1998;749-753.
72. Wang X., Sato R., Brown M. S., Hua X., Goldstein J. L. SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell. 77:1994;53-62.
73. Weintraub H. The MyoD family and myogenesis: Redundancy, networks, and thresholds. Cell. 75:1993;1241-1244.
74. Lasorella A., Iavarone A., Israel M. A. Id2 specifically alters regulation of the cell cycle by tumor suppressor proteins. Mol. Cell. Biol. 16:1996;2570-2578.
75. Nakajima T., Yageta M., Shiotsu K., Morita K., Suzuki M., Tomooka Y., Oda K. Suppression of adenovirus E1A-induced apoptosis by mutated p53 is overcome by coexpression with Id proteins. Proc. Natl. Acad. Sci. USA. 95:1998;10590-10595.
76. Deed R. W., Armitage S., Norton J. D. Nuclear localization and regulation of Id protein through an E protein-mediated chaperone mechanism. J. Biol. Chem. 271:1996;23603-23606.
77. Behrens J., von Kries J. P., Kuhl M., Bruhn L., Wedlich D., Grosschedl R., Birchmeier W. Functional interactions of beta-catenin with the transcription factor LEF-1. Nature. 382:1996;638-642.
78. Stoldt V. R., Sonneborn A., Leuker C. E., Ernst J. F. Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J. 16:1997;1982-1991.
79. Braun B. R., Johnson A. D. Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science. 277:1997;105-109.