Developmentally Essential Protein Flightless I Is a Nuclear Receptor Coactivator with Actin Binding Activity

Molecular and Cellular Biology

Volumn 24, Issue 5, 2004, Pages 2103-2117

  Lee, Young Ho ^a   Campbell, Hugh D ^b   Stallcup, Michael R ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; ARGININE; CARM1 PROTEIN; CELL NUCLEUS RECEPTOR; COACTIVATOR PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; ESTROGEN; ESTROGEN RECEPTOR; GELSOLIN; HISTONE; HISTONE ACETYLTRANSFERASE PCAF; METHYLTRANSFERASE; NUCLEAR RECEPTOR COACTIVATOR 2; PRMT1 PROTEIN; PROTEIN; PROTEIN FLIGHTLESS I; PROTEIN P160; REGULATOR PROTEIN; STEROID RECEPTOR COACTIVATOR 1; STEROID RECEPTOR COACTIVATOR 3; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN MCF 7; DEVELOPMENT; DROSOPHILA; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; HORMONAL REGULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PS2 GENE; RECEPTOR BINDING; RECEPTOR UPREGULATION; TWO HYBRID SYSTEM;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARRIER PROTEINS; CELL LINE, TUMOR; DROSOPHILA PROTEINS; ESTRADIOL; GELSOLIN; GENES, REPORTER; HUMANS; MACROMOLECULAR SUBSTANCES; MICE; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-ARGININE N-METHYLTRANSFERASE; RECEPTORS, AMPA; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; TWO-HYBRID SYSTEM TECHNIQUES;

ANIMALIA; MINK CELL FOCUS-FORMING VIRUS;

EID: 1342325341     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.5.2103-2117.2004     Document Type: Article

References (72)

1. Ankenbauer, T., J. A. Kleinschmidt, M. J. Walsh, O. H. Weiner, and W. W. Franke. 1989. Identification of a widespread nuclear actin binding protein. Nature 342:822-825.
2. Anzick, S. L., J. Kononen, R. L. Walker, D. O. Azorsa, M. M. Tanner, X.-Y. Guan, G. Sauter, O.-P. Kallioniemi, J. M. Trent, and P. S. Meltzer. 1997. AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science 277:965-968.
3. Beato, M., P. Herrlich, and G. Schütz. 1995. Steroid hormone receptors: many actors in search of a plot. Cell 83:851-857.
4. Belandia, B., R. L. Orford, H. C. Hurst, and M. G. Parker. 2002. Targeting of SWI/SNF chromatin remodelling complexes to estrogen-responsive genes. EMBO J. 21:4094-4103.
5. Belandia, B., and M. G. Parker. 2000. Functional interaction between the p160 coactivator proteins and the transcriptional enhancer factor family of transcription factors. J. Biol. Chem. 275:30801-30805.
6. Campbell, H. D., S. Fountain, I. S. McLennan, L. A. Berven, M. F. Crouch, D. A. Davy, J. A. Hooper, K. Waterford, K. S. Chen, J. R. Lupski, B. Ledermann, I. G. Young, and K. I. Matthaei. 2002. Fliih, a gelsolin-related cytoskeletal regulator essential for early mammalian embryonic development. Mol. Cell. Biol. 22:3518-3526.
7. Campbell, H. D., S. Fountain, I. G. Young, S. Weitz, P. Lichter, and J. D. Hoheisel. 2000. Fliih, the murine homologue of the Drosophila melanogaster flightless I gene: nucleotide sequence, chromosomal mapping and overlap with Llglh. DNA Seq. 11:29-40.
8. Campbell, H. D., T. Schimansky, C. Claudianos, N. Ozsarac, A. B. Kasprzak, J. N. Cotsell, I. G. Young, H. G. de Couet, and G. L. Miklos. 1993. The Drosophila melanogaster flightless-I gene involved in gastrulation and muscle degeneration encodes gelsolin-like and leucine-rich repeat domains and is conserved in Caenorhabditis elegans and humans. Proc. Natl. Acad. Sci. USA 90:11386-11390.
9. Campbell, H. D., I. G. Young, and K. I. Matthaei. 2000. Mammalian homologues of the Drosophila melanogaster flightless I gene involved in early development. Curr. Genom. 1:59-70.
10. Chen, D., S.-M. Huang, and M. R. Stallcup. 2000. Synergistic, p160 coactivator-dependent enhancement of estrogen receptor function by CARM1 and p300. J. Biol. Chem. 275:40810-40816.
11. Chen, D., H. Ma, H. Hong, S. S. Koh, S.-M. Huang, B. T. Schurter, D. W. Aswad, and M. R. Stallcup. 1999. Regulation of transcription by a protein methyltransferase. Science 284:2174-2177.
12. Chen, H., R. J. Lin, R. L. Schiltz, D. Chakravarti, A. Nash, L. Nagy, M. L. Privalsky, Y. Nakatani, and R. M. Evans. 1997. Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 90:569-580.
13. Chen, K. S., P. H. Gunaratne, J. D. Hoheisel, I. G. Young, G. L. Miklos, F. Greenberg, L. G. Shaffer, H. D. Campbell, and J. R. Lupski. 1995. The human homologue of the Drosophila melanogaster flightless-I gene (fliI) maps within the Smith-Magenis microdeletion critical region in 17p11.2. Am. J. Hum. Genet. 56:175-182.
14. Chen, S. L., D. H. Dowhan, B. M. Hosking, and G. E. Muscat. 2000. The steroid receptor coactivator, GRIP-1, is necessary for MEF-2C-dependent gene expression and skeletal muscle differentiation. Genes Dev. 14:1209-1228.
15. Darimont, B. D., R. L. Wagner, J. W. Apriletti, M. R. Stallcup, P. J. Kushner, J. D. Baxter, R. J. Fletterick, and K. R. Yamamoto. 1998. Structure and specificity of nuclear receptor-coactivator interactions. Genes Dev. 12:3343-3356.
16. Davy, D. A., E. E. Ball, K. I. Matthaei, H. D. Campbell, and M. F. Crouch. 2000. The flightless I protein localizes to actin-based structures during embryonic development. Immunol. Cell Biol. 78:423-429.
17. Davy, D. A., H. D. Campbell, S. Fountain, D. de Jong, and M. F. Crouch. 2001. The flightless I protein colocalizes with actin- and microtubule-based structures in motile Swiss 3T3 fibroblasts: evidence for the involvement of PI 3-kinase and Ras-related small GTPases. J. Cell Sci. 114:549-562.
18. de Couet, H. G., K. S. Fong, A. G. Weeds, P. J. McLaughlin, and G. L. Miklos. 1995. Molecular and mutational analysis of a gelsolin-family member encoded by the flightless I gene of Drosophila melanogaster. Genetics 141:1049-1059.
19. Ding, X. F., C. M. Anderson, H. Ma, H. Hong, R. M. Uht, P. J. Kushner, and M. R. Stallcup. 1998. Nuclear receptor-binding sites of coactivators glucocorticoid receptor interacting protein 1 (GRIP1) and steroid receptor coactivator 1 (SRC-1): multiple motifs with different binding specificities. Mol. Endocrinol. 12:302-313.
20. Eastman, Q., and R. Grosschedl. 1999. Regulation of LEF-1/TCF transcription factors by Wnt and other signals. Curr. Opin. Cell Biol. 11:233-240.
21. Egly, J. M., N. G. Miyamoto, V. Moncollin, and P. Chambon. 1984. Is actin a transcription initiation factor for RNA polymerase B? EMBO J. 3:2363-2371.
22. Fields, S., and O. Song. 1989. A novel genetic system to detect protein-protein interactions. Nature 340:245-246.
23. Frankel, A., N. Yadav, J. Lee, T. L. Branscombe, S. Clarke, and M. T. Bedford. 2002. The novel human protein arginine N-methyltransferase PRMT6 is a nuclear enzyme displaying unique substrate specificity. J. Biol. Chem. 277:3537-3543.
24. Gehin, M., M. Mark, C. Dennefeld, A. Dierich, H. Gronemeyer, and P. Chambon. 2002. The function of TIF2/GRIP1 in mouse reproduction is distinct from those of SRC-1 and p/CIP. Mol. Cell. Biol. 22:5923-5937.
25. Glass, C. K., and M. G. Rosenfeld. 2000. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 14:121-141.
26. Goshima, M., K. Kariya, Y. Yamawaki-Kataoka, T. Okada, M. Shibatohge, F. Shima, E. Fujimoto, and T. Kataoka. 1999. Characterization of a novel Ras-binding protein Ce-FLI-1 comprising leucine-rich repeats and gelsolin-like domains. Biochem. Biophys. Res. Commun. 257:111-116.
27. Heery, D. M., E. Kalkhoven, S. Hoare, and M. G. Parker. 1997. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387:733-736.
28. Heinlein, C. A., and C. Chang. 2002. Androgen receptor (AR) coregulators: an overview. Endocr. Rev. 23:175-200.
29. Hong, H., K. Kohli, A. Trivedi, D. L. Johnson, and M. R. Stallcup. 1996. GRIP1, a novel mouse protein that serves as a transcriptional co-activator in yeast for the hormone binding domains of steroid receptors. Proc. Natl. Acad. Sci. USA 93:4948-4952.
30. Huang, S.-M., and M. R. Stallcup. 2000. Mouse Zac1, a transcriptional coactivator and repressor for nuclear receptors. Mol. Cell. Biol. 20:1855-1867.
31. Kobe, B., and A. V. Kajava. 2001. The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol. 11:725-732.
32. Koh, S. S., D. Chen, Y.-H. Lee, and M. R. Stallcup. 2001. Synergistic enhancement of nuclear receptor function by p160 coactivators and two coactivators with protein methyltransferase activities. J. Biol. Chem. 276:1089-1098.
33. Koh, S. S., H. Li, Y. H. Lee, R. B. Widelitz, C. M. Chuong, and M. R. Stallcup. 2002. Synergistic coactivator function by coactivator-associated arginine methyltransferase (CARM) 1 and beta-catenin with two different classes of DNA-binding transcriptional activators. J. Biol. Chem. 277:26031-26035.
34. Kwiatkowski, D. J. 1999. Functions of gelsolin: motility, signaling, apoptosis, cancer. Curr. Opin. Cell Biol. 11:103-108.
35. Lee, Y.-H., S. S. Koh, X. Zhang, X. Cheng, and M. R. Stallcup. 2002. Synergy among nuclear receptor coactivators: selective requirement for protein methyltransferase and acetyltransferase activities. Mol. Cell. Biol. 22:3621-3632.
36. Li, H., S. Park, B. Kilburn, M. A. Jelinek, A. Henschen-Edman, D. W. Aswad, M. R. Stallcup, and I. A. Laird-Offringa. 2002. Lipopolysaccharide-induced methylation of HuR, an mRNA-stabilizing protein, by CARM1. J. Biol. Chem. 277:44623-44630.
37. Li, J., B. W. O'Malley, and J. Wong. 2000. p300 requires its histone acetyltransferase activity and SRC-1 interaction domain to facilitate thyroid hormone receptor activation in chromatin. Mol. Cell. Biol. 20:2031-2042.
38. Lin, W.-J., J. D. Gary, M. C. Yang, S. Clarke, and H. R. Herschman. 1996. The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J. Biol. Chem. 271:15034-15044.
39. Liu, Y. T., and H. L. Yin. 1998. Identification of the binding partners for flightless I, a novel protein bridging the leucine-rich repeat and the gelsolin superfamilies. J. Biol. Chem. 273:7920-7927.
40. Liu, Z., J. Wong, S. Y. Tsai, M. J. Tsai, and B. W. O'Malley. 2001. Sequential recruitment of steroid receptor coactivator-1 (SRC-1) and p300 enhances progesterone receptor-dependent initiation and reinitiation of transcription from chromatin. Proc. Natl. Acad. Sci. USA 98:12426-12431.
41. Ma, H., C. T. Baumann, H. Li, B. D. Strahl, R. Rice, M. A. Jelinek, D. W. Aswad, C. D. Allis, G. L. Hager, and M. R. Stallcup. 2001. Hormone-dependent, CARM1-directed, arginine-specific methylation of histone H3 on the mouse mammary tumor virus promoter. Curr. Biol. 11:1981-1985.
42. Ma, H., H. Hong, S.-M. Huang, R. A. Irvine, P. Webb, P. J. Kushner, G. A. Coetzee, and M. R. Stallcup. 1999. Multiple signal input and output domains of the 160-kDa nuclear receptor coactivator proteins. Mol. Cell. Biol. 19:6164-6173.
43. Ma, H., Y. Shang, D. Y. Lee, and M. R. Stallcup. 2003. Study of nuclear receptor-induced transcription complex assembly and histone modification by chromatin immunoprecipitation. Methods Enzymol. 364:284-296.
44. Mangelsdorf, D. J., and R. M. Evans. 1995. The RXR heterodimers and orphan receptors. Cell 83:841-850.
45. McBride, A. E., V. H. Weiss, H. K. Kim, J. M. Hogle, and P. A. Silver. 2000. Analysis of the yeast arginine methyltransferase Hmt1p/Rmt1p and its in vivo function. Cofactor binding and substrate interactions. J. Biol. Chem. 275:3128-3136.
46. McKenna, N. J., and B. W. O'Malley. 2002. Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 108:465-474.
47. Morin, P. J. 1999. Beta-catenin signaling and cancer. Bioessays 21:1021-1030.
48. Nolte, R. T., G. B. Wisely, S. Westin, J. E. Cobb, M. H. Lambert, R. Kurokawa, M. G. Rosenfeld, T. M. Willson, C. K. Glass, and M. V. Milburn. 1998. Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. Nature 395:137-143.
49. Oñate, S. A., S. Y. Tsai, M.-J. Tsai, and B. W. O'Malley. 1995. Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science 270:1354-1357.
50. Park, J., M. A. Wood, and M. D. Cole. 2002. BAF53 forms distinct nuclear complexes and functions as a critical c-Myc-interacting nuclear cofactor for oncogenic transformation. Mol. Cell. Biol. 22:1307-1316.
51. Puri, P. L., V. Sartorelli, X. J. Yang, Y. Hamamori, V. V. Ogryzko, B. H. Howard, L. Kedes, J. Y. Wang, A. Graessmann, Y. Nakatani, and M. Levrero. 1997. Differential roles of p300 and PCAF acetyltransferases in muscle differentiation. Mol. Cell 1:35-45.
52. Rando, O. J., K. Zhao, and G. R. Crabtree. 2000. Searching for a function for nuclear actin. Trends Cell Biol. 10:92-97.
53. Rando, O. J., K. Zhao, P. Janmey, and G. R. Crabtree. 2002. Phosphatidylinositol-dependent actin filament binding by the SWI/SNF-like BAF chromatin remodeling complex. Proc. Natl. Acad. Sci. USA 99:2824-2829.
54. Scheer, U., H. Hinssen, W. W. Franke, and B. M. Jockusch. 1984. Microinjection of actin-binding proteins and actin antibodies demonstrates involvement of nuclear actin in transcription of lampbrush chromosomes. Cell 39:111-122.
55. Shang, Y., and M. Brown. 2002. Molecular determinants for the tissue specificity of SERMs. Science 295:2465-2468.
56. Shang, Y., X. Hu, J. DiRenzo, M. A. Lazar, and M. Brown. 2000. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103:843-852.
57. Stallcup, M. R. 2001. Role of protein methylation in chromatin remodeling and transcriptional regulation. Oncogene 20:3014-3020.
58. Teyssier, C., D. Chen, and M. R. Stallcup. 2002. Requirement for multiple domains of the protein arginine methyltransferase CARM1 in its transcriptional coactivator function. J. Biol. Chem. 277:46066-46072.
59. Ting, H. J., S. Yeh, K. Nishimura, and C. Chang. 2002. Supervillin associates with androgen receptor and modulates its transcriptional activity. Proc. Natl. Acad. Sci. USA 99:661-666.
60. Torchia, J., D. W. Rose, J. Inostroza, Y. Kamei, S. Westin, C. K. Glass, and M. G. Rosenfeld. 1997. The transcriptional co-activator p/CIP binds CBP and mediates nuclear receptor function. Nature 387:677-684.
61. Truica, C. I., S. Byers, and E. P. Gelmann. 2000. Beta-catenin affects androgen receptor transcriptional activity and ligand specificity. Cancer Res. 60:4709-4713.
62. Tsai, M.-J., and B. W. O'Malley. 1994. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 63:451-486.
63. Voegel, J. J., M. J. S. Heine, M. Tini, V. Vivat, P. Chambon, and H. Gronemeyer. 1998. The coactivator TIF2 contains three nuclear receptor binding motifs and mediates transactivation through CBP binding-dependent and -independent pathways. EMBO J. 17:507-519.
64. Way, M., B. Pope, and A. G. Weeds. 1992. Are the conserved sequences in segment 1 of gelsolin important for binding actin? J. Cell Biol. 116:1135-1143.
65. Webb, P., G. N. Lopez, R. M. Uht, and P. J. Kushner. 1995. Tamoxifen activation of the estrogen receptor/AP-1 pathway: potential origin for the cell-specific estrogen-like effects of antiestrogens. Mol. Endocrinol. 9:443-456.
66. Wu, X., H. Li, and J. D. Chen. 2001. The human homologue of the yeast DNA repair and TFIIH regulator MMS19 is an AF-1-specific coactivator of estrogen receptor. J. Biol. Chem. 276:23962-23968.
67. Xu, J., L. Liao, G. Ning, H. Yoshida-Komiya, C. Deng, and B. W. O'Malley. 2000. The steroid receptor coactivator SRC-3 (p/CIP/RAC3/AIB1/ACTR/TRAM-1) is required for normal growth, puberty, female reproductive function, and mammary gland development. Proc. Natl. Acad. Sci. USA 97:6379-6384.
68. Xu, J., Y. Qiu, F. J. DeMayo, S. Y. Tsai, M. J. Tsai, and B. W. O'Malley. 1998. Partial hormone resistance in mice with disruption of the steroid receptor coactivator-1 (SRC-1) gene. Science 279:1922-1925.
69. Xu, W., H. Chen, K. Du, H. Asahara, M. Tini, B. M. Emerson, M. Montminy, and R. M. Evans. 2001. A transcriptional switch mediated by cofactor methylation. Science 294:2507-2511.
70. Xue, Y., J. C. Canman, C. S. Lee, Z. Nie, D. Yang, G. T. Moreno, M. K. Young, E. D. Salmon, and W. Wang. 2000. The human SWI/SNF-B chromatin-remodeling complex is related to yeast rsc and localizes at kinetochores of mitotic chromosomes. Proc. Natl. Acad. Sci. USA 97:13015-13020.
71. Zhang, X., L. Zhou, and X. Cheng. 2000. Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. EMBO J. 19:3509-3519.
72. Zhao, K., W. Wang, O. J. Rando, Y. Xue, K. Swiderek, A. Kuo, and G. R. Crabtree. 1998. Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 95:625-636.