The pre-mRNA-splicing factor SF3a66 functions as a microtubule-binding and -bundling protein

Biochemical Journal

Volumn 382, Issue 1, 2004, Pages 223-230

  Takenaka, Kei ^a   Nakagawa, Hiroyuki ^b   Miyamoto, Shigeaki ^b   Miki, Hiroaki ^a,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b KYUSHU INSTITUTE OF TECHNOLOGY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Microtubule associated protein (MAP); Neurite extension; RNA splicing; SF3a complex

Indexed keywords

MICROTUBULES; NEUROBLASTOMA CELLS; SPLICING FACTORS;

CELLS; ELECTRON MICROSCOPES; MOLECULES; PROTEINS;

RNA;

BETA TUBULIN; BINDING PROTEIN; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN SUBUNIT; SPLICING FACTOR 3A66; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; ELECTRON MICROSCOPY; MICROTUBULE; MOLECULAR WEIGHT; NERVE FIBER GROWTH; NEUROBLASTOMA CELL; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SPLICING;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NEURITES; NEUROBLASTOMA; PROTEIN BINDING; PROTEIN SUBUNITS; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA PRECURSORS; RNA SPLICING; TUBULIN;

ANIMALIA; STAPHYLOCOCCUS PHAGE 3A;

EID: 4344598748     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040521     Document Type: Article

References (49)

1. Ruskin, B., Krainer, A. R., Maniatis, T. and Green, M. R. (1984) Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro. Cell 38, 317-331
2. Konarska, M. M., Grabowski, P. J., Padgett, R. A. and Sharp, P. A. (1985) Characterization of the branch site in lariat RNAs produced by splicing of mRNA precursors. Nature (London) 313, 552-557
3. Krämer, A. (1996) The structure and function of proteins involved in nuclear pre-mRNA splicing. Annu. Rev. Biochem. 65, 367-409
4. Nilsen, T. (1998) RNA-RNA interactions in nuclear pre-mRNA splicing. In RNA Structure and Function (Simons, R. and Grunberg-Manago, M., eds.), pp. 279-307, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
5. Will, C. and Lührmann, R. (1997) SnRNP structure and function. In Eukaryotic mRNA Processing (Krämer, A., ed.), pp. 130-173, IRL Press, Oxford
6. Madhani, H. D. and Guthrie, C. (1994) Dynamic RNA-RNA interactions in the spliceosome. Annu. Rev. Genet. 28, 1-26
7. Brosi, R., Groning, K., Behrens, S. E., Luhrmann, R. and Krämer, A. (1993) Interaction of mammalian splicing factor SF3a with U2 snRMP and relation of its 60-kD subunit to yeast PRP9. Science 262, 102-105
8. Krämer, A., Grüter, P., Gröning, K. and Kastner, B. (1999) Combined biochemical and electron microscopic analyses reveal the architecture of the mammalian U2 snRMP. J. Cell Biol. 145, 1355-1368
9. Brosi, R., Hauri, H. P. and Krämer, A. (1993) Separation of splicing factor SF3 into two components and purification of SF3a activity. J. Biol. Chem. 268, 17640-17646
10. Bennett, M., Michaud, S., Kingston, J. and Reed, R. (1992) Protein components specifically associated with prespliceosome and spliceosome complexes. Genes Dev. 10, 1986-2000
11. Gozani, O., Patton, J. G. and Reed, R. (1994) A novel set of spliceosome-associated proteins and the essential splicing factor PSF bind stably to pre-mRNA prior to catalytic step II of the splicing reaction. EMBO J. 13, 3356-3367
12. Staknis, D. and Reed, R. (1994) Direct interactions between pre-mRNA and six U2 small nuclear ribonucleoproteins during spliceosome assembly. Mol. Cell Biol. 14, 2994-3005
13. Vijayraghavan, U., Company, M. and Abelson, J. (1989) Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes Dev. 8, 1206-1216
14. Chang, T. H., Clark, M. W., Lustig, A. J., Cusick, M. E. and Abelson, J. (1988) RNA11 protein is associated with the yeast spliceosome and is localized in the periphery of the cell nucleus. Mol. Cell. Biol. 8, 2379-2393
15. Schappert, K. and Friesen, J. D. (1991) Genetic studies of the PRP11 gene of Saccharomyces cerevisiae. Mol. Gen. Genet. 226, 277-282
16. Bennett, M. and Reed, R. (1993) Correspondence between a mammalian spliceosome component and an essential yeast splicing factor. Science 262, 105-108
17. Ruby, S. W., Chang, T. H. and Abelson, J. (1993) Four yeast spliceosomal proteins (PRP5, PRP9, PRP11, and PRP21) interact to promote U2 snRNP binding to pre-mRNA. Genes Dev. 10, 1909-1925
18. Chiara, M. D., Champion-Arnaud, P., Buvoli, M., Nadal-Ginard, B. and Reed, R. (1994) Specific protein-protein interactions between the essential mammalian spliceosome-associated proteins SAP 61 and SAP 114. Proc. Natl. Acad. Sci. U.S.A. 91, 6403-6407
19. Krämer, A., Mulhauser, F., Wersig, C., Groning, K. and Bilbe, G. (1995) Mammalian splicing factor SF3a120 represents a new member of the SURP family of proteins and is homologous to the essential splicing factor PRP21p of Saccharomyces cerevisiae. RNA 3, 260-272
20. Legrain, P. and Chapon, C. (1993) Interaction between PRP11 and SPP91 yeast splicing factors and characterization of a PRP9-PRP11-SPP91 complex. Science 262, 108-110
21. Legrain, P., Chapon, C. and Galisson, F. (1993) Interactions between PRP9 and SPP91 splicing factors identify a protein complex required in prespliceosome assembly. Genes Dev. 7, 1390-1399
22. Wiest, D. K., O'Day, C. L. and Abelson, J. (1996) In vitro studies of the Prp9.Prp11.Prp21 complex indicate a pathway for U2 small nuclear ribonucleoprotein activation. J. Biol. Chem. 271, 33268-33276
23. Miki, H., Yamaguchi, H., Suetsugu, S. and Takenawa, T. (2000) IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature (London) 408, 732-735
24. Krugmann, S., Jordens, I., Gevaert, K., Driessens, M., Vandekerckhove, J. and Hall, A. (2001) Cdc42 induces filopodia by promoting the formation of an IRSp53:Mena complex. Curr. Biol. 11, 1645-1655
25. Miki, H. and Takenawa, T. (2002) WAVE2 serves a functional partner of IRSp53 by regulating its interaction with Rac. Biochem. Biophys. Res. Commun. 293, 93-99
26. Govind, S., Kozma, R., Monfries, C., Lim, L. and Ahmed, S. (2001) Cdc42Hs facilitates cytoskeletal reorganization and neurite outgrowth by localizing the 58-kD insulin receptor substrate to filamentous actin. J. Cell Biol. 152, 579-594
27. Barbee, S. A., Lublin, A. L. and Evans, T. C. (2002) A novel function for the Sm proteins in germ granule localization during C. elegans embryogenesis. Curr. Biol. 12, 1502-1506
28. Schisa, J. A., Pitt, J. N. and Priess, J. R. (2001) Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development 128, 1287-1298
29. Strome, S. and Wood, W. B. (1982) Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 79, 1558-1562
30. Hyman, A., Drechsel, D., Kellogg, D., Salser, S., Sawin, K., Steffen, P., Wordeman, L. and Mitchison, T. (1991) Preparation of modified tubulins. Methods Enzymol. 196, 478-485
31. Nesic, D. and Krämer, A. (2001) Domains in human splicing factors SF3a60 and SF3a66 required for binding to SF3a120, assembly of the 17S U2 snRNP, and prespliceosome formation. Mol. Cell. Biol. 21, 6406-6417
32. Gustke, N., Trinczek, B., Biernat, J., Mandelkow, E. M. and Mandelkow, E. (1994) Domains of tau protein and interactions with microtubules. Biochemistry 33, 9511-9522
33. Wallis, K. T., Azhar, S., Rho, M. B., Lewis, S. A., Cowan, N. J. and Murphy, D. B. (1993) The mechanism of equilibrium binding of microtubule-associated protein 2 to microtubules. Binding is a multi-phasic process and exhibits positive cooperativity. J. Biol. Chem. 268, 5158-5167
34. Aizawa, H., Kawasaki, H., Murofushi, H., Kotani, S., Suzuki, K. and Sakai, H. (1989) A common amino acid sequence in 190-kDa microtubule-associated protein and tau for the promotion of microtubule assembly. J. Biol. Chem. 264, 5885-5890
35. Butner, K. A. and Kirschner, M. W. (1991) Tau protein binds to microtubules through a flexible array of distributed weak sites. J. Cell Biol. 115, 717-730
36. Hirokawa, N., Shiomura, Y. and Okabe, S. (1988) Tau proteins: the molecular structure and mode of binding on microtubules. J. Cell Biol. 107, 1449-1459
37. Kanai, Y., Chen, J. and Hirokawa, N. (1992) Microtubule bundling by tau proteins in vivo: analysis of functional domains. EMBO J. 11, 3953-3961
38. Kanai, Y., Takemura, R., Oshima, T., Mori, H., Ihara, Y., Yanagisawa, M., Masaki, T. and Hirokawa, N. (1989) Expression of multiple tau isoforms and microtubule bundle formation in fibroblasts transfected with a single tau cDMA. J. Cell Biol. 109, 1173-1184
39. Umeyama, T., Okabe, S., Kanai, Y. and Hirokawa, N. (1993) Dynamics of microtubules bundled by microtubule associated protein 2C (MAP2C). J. Cell Biol. 120, 451-465
40. Weisshaar, B., Doll, T. and Matus, A. (1992) Reorganisation of the microtubular cytoskeleton by embryonic microtubule-associated protein 2 (MAP2c). Development 116, 1151-1161
41. Ferhat, L., Represa, A., Bernard, A., Ben-Ari, Y. and Khrestchatisky, M. (1996) MAP2d promotes bundling and stabilization of both microtubules and microfilaments. J. Cell Sci. 109, 1095-1103
42. Fukata, Y., Itoh, T. J., Kimura, T., Menager, C., Nishimura, T., Shiromizu, T., Watanabe, H., Inagaki, N., Iwamatsu, A., Hotani, H. and Kaibuchi, K. (2002) CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4, 583-591
43. Hong, W., Bennett, M., Xiao, Y., Feld Kramer, R., Wang, C. and Reed, R. (1997) Association of U2 snRNP with the spliceosomal complex E. Nucleic Acids Res. 15, 354-361
44. Schmidt-Zachmann, M. S., Knecht, S. and Krämer, A. (1998) Molecular characterization of a novel, widespread nuclear protein that colocalizes with spliceosome components. Mol. Biol. Cell 9, 143-160
45. Mollinari, C., Kleman, J. P., Jiang, W., Schoehn, G., Hunter, T. and Margolis, R. L. (2002) PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 157, 1175-1186
46. Jiang, W., Jimenez, G., Wells, N. J., Hope, T. J., Wahl, G. M., Hunter, T. and Fukunaga, R. (1998) PRC1: a human mitotic spindle-associated CDK substrate protein required for cytokinesis. Mol. Cell 2, 877-885
47. Yen, I. T. and Luduena, R. F. (2004) The βII isotype of tubulin is present in the cell nuclei of a variety of cancers. Cell Motil. Cytoskeleton 57, 96-106
48. Xu, K. and Luduena, R. F. (2002) Characterization of nuclear βII-tubulin in tumor cells: a possible novel target for taxol. Cell Motil. Cytoskeleton 53, 39-52
49. Walss, C., Kreisberg, J. I. and Luduena, R. F. (1999) Presence of the βII isotype of tubulin in the nuclei of cultured mesangial cells from rat kidney. Cell Motil. Cytoskeleton 42, 274-284