Detection of snRNP assembly intermediates in Cajal bodies by fluorescence resonance energy transfer

Journal of Cell Biology

Volumn 166, Issue 7, 2004, Pages 1015-1025

  Staněk, David ^a   Neugebauer, Karla M ^a,b  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b NONE   (Germany)

Author keywords

Cajal body; Coilin; FRET; pre mRNA splicing; snRNP

Indexed keywords

CELL PROTEIN; COILIN; MESSENGER RNA PRECURSOR; PROTEIN SART3; SMALL NUCLEAR RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MUTANT; CELL NUCLEUS; COILED BODY; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; RNA SPLICING; SPLICEOSOME; WESTERN BLOTTING;

EID: 4644309827     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200405160     Document Type: Article

References (52)

1. Achsel, T., H. Brahms, B. Kastner, A. Bachi, M. Wilm, and R. Lührmann. 1999. A doughnut-shaped heteromer of human Sm-like proteins binds to the 3′-end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J. 18:5789-5802.
2. Almeida, F., R. Saffrich, W. Ansorge, and M. Carmo-Fonseca. 1998. Microinjection of anti-coilin antibodies affects the structure of coiled bodies. J. Cell Biol. 142:899-912.
3. Andrade, L.E., E.K. Chan, I. Raska, CL. Peebles, G. Roos, and E.M. Tan. 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.
4. Bastiaens, P.I., I.V. Majoul, P.J. Verveer, H.D. Soling, and T.M. Jovin. 1996. Imaging the intracellular trafficking and state of the AB5 quaternary structure of cholera toxin. EMBO J. 15:4246-4253.
5. Bell, M., S. Schreiner, A. Damianov, R. Reddy, and A. Bindereif. 2002. p110, a novel human U6 snRNP protein and U4/U6 snRNP recycling factor. EMBO J. 21:2724-2735.
6. Black, D.L., and A.L. Pinto. 1989. U5 small nuclear ribonucleoprotein: RNA structure analysis and ATP-dependent interaction with U4/U6. Mol. Cell. Biol. 9:3350-3359.
7. Boudonck, K., L. Dolan, and P.J. Shaw. 1998. Coiled body numbers in the Arabidopsis root epidermis are regulated by cell type, developmental stage and cell cycle parameters. J. Cell Sci. 111:3687-3694.
8. Carmo-Fonseca, M., R. Pepperkok, M.T. Carvalho, and A.I. Lamond. 1992. Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 snRNPs in coiled bodies. J. Cell Biol. 117:1-14.
9. Carmo-Fonseca, M., R. Pepperkok, B.S. Sproat, W. Ansorge, M.S. Swanson, and A.I. Lamond. 1991. In vivo detection of snRNP-rich organelles in the nuclei of mammalian cells. EMBO J. 10:1863-1873.
10. Damianov, A., S. Schreiner, and A. Bindereif. 2004. Recycling of the U12-type spliceosome requires p110, a component of the U6atac snRNP. Mol. Cell. Biol. 24:1700-1708.
11. Darzacq, X., B.E. Jady, C. Verheggen, A.M. Kiss, E. Bertrand, and T. Kiss. 2002. Cajal body-specific small nuclear RNAs: a novel class of 2′-O-methylation and pseudouridylation guide RNAs. EMBO J. 21:2746-2756.
12. Dundr, M., M.D. Hebert, T.S. Karpova, D. Stanek, H. Xu, K.B. Shpargel, U.T. Meier, K.M. Neugebauer, A.G. Matera, and T. Misteli. 2004. In vivo kinetics of Cajal body components. J. Cell Biol. 164:831-842.
13. Dundr, M., U. Hoffmann-Rohrer, Q. Hu, I. Grummt, L.I. Rothblum, R.D. Phair, and T. Misteli. 2002. A kinetic framework for a mammalian RNA polymerase in vivo. Science. 298:1623-1626.
14. Dundr, M., and T. Misteli. 2001. Functional architecture in the cell nucleus. Biochem. J. 356:297-310.
15. Gall, J.G. 2000. Cajal bodies: the first 100 years. Annu. Rev. Cell Dev. Biol. 16:273-300.
16. Gall, J.G. 2003. The centennial of the Cajal body. Nat. Rev. Mol. Cell Biol. 4:975-980.
17. Gerbi, S.A., A.V. Borovjagin, F.E. Odreman, and T.S. Lange. 2003. U4 snRNA nucleolar localization requires the NHPX/15.5-kD protein binding site but not Sm protein or U6 snRNA association. J. Cell Biol. 162:821-832.
18. Handwerger, K.E., C. Murphy, and J.G. Gall. 2003. Steady-state dynamics of Cajal body components in the Xenopus germinal vesicle. J. Cell Biol. 160:495-504.
19. Hebert, M.D., and A.G. Matera. 2000. Self-association of coilin reveals a common theme in nuclear body localization. Mol. Biol. Cell. 11:4159-4171.
20. Horowitz, D.S., R. Kobayashi, and A.R. Krainer. 1997. A new cyclophilin and the human homologues of yeast Prp3 and Prp4 form a complex associated with U4/U6 snRNPs. RNA. 3:1374-1387.
21. Ingelfinger, D., D.J. Arndt-Jovin, R. Lührmann, and T. Achsel. 2002. The human LSm1-7 proteins colocalize with the mRNA-degradingenzymes Dcp1/2 and Xrn1 in distinct cytoplasmic foci. RNA. 8:1489-1501.
22. Jady, B.E., X. Darzacq, K.E. Tucker, A.G. Matera, E. Bertrand, and T. Kiss. 2003. Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm. EMBO J. 22:1878-1888.
23. Karpova, T.S., C.T. Baumann, L. He, X. Wu, A. Grammer, P. Lipsky, G.L. Hager, and J.G. McNally. 2003. Fluorescence resonance energy transfer from cyan to yellow fluorescent protein detected by acceptor photobleaching using confocal microscopy and a single laser. J. Microsc. 209:56-70.
24. Lauber, J., G. Plessel, S. Prehn, C.L. Will, P. Fabrizio, K. Groning, W.S. Lane, and R. Lührmann. 1997. The human U4/U6 snRNP contains 60 and 90kD proteins that are structurally homologous to the yeast splicing factors Prp4p and Prp3p. RNA. 3:926-941.
25. Makarova, O.V., E.M. Makarov, S. Liu, H.P. Vornlocher, and R. Lührmann. 2002. Protein 61K, encoded by a gene (PRPF31) linked to autosomal dominant retinitis pigmentosa, is required for U4/U6center dotU5 tri-snRNP formation and pre-mRNA splicing. EMBO J. 21:1148-1157.
26. Matera, A.G. 1999. Nuclear bodies: multifaceted subdomains of the interchromatin space. Trends Cell Biol. 9:302-309.
27. Matera, A.G., and D.C. Ward. 1993. Nucleoplasmic organization of small nuclear ribonucleoproteins in cultured human cells. J. Cell Biol. 121:715-727.
28. Mayes, A.E., L. Verdone, P. Legrain, and J.D. Beggs. 1999. Characterization of Sm-like proteins in yeast and their association with U6 snRNA. EMBO J. 18:4321-4331.
29. Medenbach, S. Schreiner, S. Liu, R. Lührmann, and A. Bindereif. 2004. Human U4/U6 snRNP recycling factor p110: mutational analysis reveals function of TPR domain in recycling. Mol. Cell. Biol. In press.
30. Narayanan, A., W. Speckmann, R. Terns, and M.P. Terns. 1999. Role of the box C/D motif in localization of small nucleolar RNAs to coiled bodies and nucleoli. Mol. Biol. Cell. 10:2131-2147.
31. Neugebauer, K.M. 2002. On the importance of being co-transcriptional. J. Cell Sci. 115:3865-3871.
32. Nottrott, S., K. Hartmuth, P. Fabrizio, H. Urlaub, I. Vidovic, R. Ficner, and R. Lührmann. 1999. Functional interaction of a novel 15.5kD [U4/U6.U5] tri-snRNP protein with the 5′ stem-loop of U4 snRNA. EMBO J. 18:6119-6133.
33. Nottrott, S., H. Urlaub, and R. Lührmann. 2002. Hierarchical, clustered protein interactions with U4/U6 snRNA: a biochemical role for U4/U6 proteins. EMBO J. 21:5527-5538.
34. Ogg, S.C., and A.I. Lamond. 2002. Cajal bodies and coilin-moving towards function. J. Cell Biol. 159:17-21.
35. Patterson, G.H., and J. Lippincott-Schwartz. 2002. A photoactivatable GFP for selective photolabeling of proteins and cells. Science. 297:1873-1877.
36. Pena, E., M.T. Berciano, R. Fernandez, J.L. Ojeda, and M. Lafarga. 2001. Neuronal body size correlates with the number of nucleoli and Cajal bodies, and with the organization of the splicing machinery in rat trigeminal ganglion neurons. J. Comp. Neurol. 430:250-263.
37. Rader, S.D., and C. Guthrie. 2002. A conserved Lsm-interaction motif in Prp24 required for efficient U4/U6 di-snRNP formation. RNA 8:1378-1392.
38. Raghunathan, P.L., and C. Guthrie. 1998. A spliceosomal recycling factor that reanneals U4 and U6 small nuclear ribonucleoprotein particles. Science. 279:857-860.
39. Raska, I., L.E. Andrade, R.L. Ochs, E.K. Chan, C.M. Chang, G. Roos, and E.M. Tan. 1991. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Exp. Cell Res. 195:27-37.
40. Siegel, R.M., F.K. Chan, D.A. Zacharias, R. Swofford, K.L. Holmes, R.Y. Tsien, and M.J. Lenardo. 2000. Measurement of molecular interactions in living cells by fluorescence resonance energy transfer between variants of the green fluorescent protein. Sci STKE. 2000:PL1.
41. Sleeman, J.E., P. Ajuh, and A.I. Lamond. 2001. snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J. Cell Sci. 114:4407-4419.
42. Sleeman, J.E., and A.I. Lamond. 1999. Newly assembled snRNPs associate with coiled bodies before speckles, suggesting a nuclear snRNP maturation pathway. Curr. Biol. 9:1065-1074.
43. Sleeman, J.E., L. Trinkle-Mulcahy, A.R. Prescott, S.C. Ogg, and A.I. Lamond. 2003. Cajal body proteins SMN and Coilin show differential dynamic behaviour in vivo. J. Cell Sci. 116:2039-2050.
44. Spector, D.L. 2001. Nuclear domains. J. Cell Sci. 114:2891-2893.
45. Staley, J.P., and C. Guthrie. 1998. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell. 92:315-326.
46. Stanek, D., K. Koberna, A. Pliss, J. Malinsky, M. Masata, J. Vecerová, M.C. Risueńo, and I. Raska. 2001. Non-isotopic mapping of ribosomal RNA synthesis and processing in the nucleolus. Chromosoma. 110:460-470.
47. Stanek, D., S.D. Rader, M. Klingauf, and K.M. Neugebauer. 2003. Targeting of U4/U6 small nuclear RNP assembly factor SART3/p110 to Cajal bodies. J. Cell Biol. 160:505-516.
48. Stevens, S.W., I. Barta, H.Y. Ge, R.E. Moore, M.K. Young, T.D. Lee, and J. Abelson. 2001. Biochemical and genetic analyses of the U5, U6, and U4/U6 × U5 small nuclear ribonucleoproteins from Saccharomyces cerevisiae. RNA. 7:1543-1553.
49. Tucker, K.E., M.T. Berdano, E.Y. Jacobs, D.F. LePage, K.B. Shpargel, J.J. Rossire, E.K. Chan, M. Lafarga, R.A. Conlon, and A.G. Matera. 2001. Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. J. Cell Biol. 154:293-307.
50. Verheggen, C., D.L. Lafontaine, D. Samarsky, J. Mouaikel, J.M. Blanchard, R. Bordonne, and E. Bertrand. 2002. Mammalian and yeast U3 snoRNPs are matured in specific and related nuclear compartments. EMBO J. 21:2736-2745.
51. Will, C.L., and R. Lührmann. 2001. Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell Biol. 13:290-301.
52. Yong, J., L. Wan, and G. Dreyfuss. 2004. Why do cells need an assembly machine for RNA-prorein complexes? Trends Cell Biol. 14:220-232.