Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions

Molecular Biology of the Cell

Volumn 16, Issue 1, 2005, Pages 260-269

  Pendle, Alison F ^a   Clark, Gillian P ^b   Boon, Reinier ^a   Lewandowska, Dominika ^b   Lam, Yun Wah ^c   Andersen, Jens ^d   Mann, Matthias ^d   Lamond, Angus I ^c   Brown, John W S ^b   Shaw, Peter J ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MESSENGER RNA; PROTEOME; RNA;

ARABIDOPSIS; ARTICLE; CELLULAR DISTRIBUTION; NONHUMAN; NUCLEOLUS; PHYTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEOMICS; RNA TRANSPORT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL NUCLEOLUS; CELL NUCLEUS; EXONS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GREEN FLUORESCENT PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; MASS SPECTROMETRY; MICROSCOPY, FLUORESCENCE; PROTEOMICS; RECOMBINANT FUSION PROTEINS; RNA; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 19944400417     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-09-0791     Document Type: Article

References (78)

1. Aebersold, R., and Mann, M. (2003). Mass spectrometry-based proteomics. Nature 422, 198-207.
2. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
3. Andersen, J. S., Lyon, C. E., Fox, A. H., Leung, A.K.L., Lam, Y. W., Steen, H., Mann, M., and Lamond, A. I. (2002). Directed proteomic analysis of the human nucleolus. Curr. Biol. 12, 1-11.
4. Barakat, A., Szick-Miranda, K., Chang, I.-F., Guyot, R., Blanc, G., Cooke, R., Delseny, M., and Bailey-Serres, J. (2001). The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome. Plant Physiol. 127, 398-415.
5. Barneche, F., Steinmetz, F., and Echeverria, M. (2000). Fibrillarin genes encode both a conserved nucleolar protein and a novel small nucleolar RNA involved in ribosomal RNA methylation in Arabidopsis thaliana. J. Biol. Chem. 275, 27212-27220.
6. Beven, A. F., Simpson, G. G., Brown, J.W.S., and Shaw, P. J. (1995). The organization of spliceosomal components in the nuclei of higher plants. J. Cell Sci. 108, 509-518.
7. Beven, A. F., Lee, R., Razaz, M., Leader, D. J., Brown, J.W.S., and Shaw, P. J. (1996). The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs. J. Cell Sci. 109, 1241-1251.
8. Brown, J.W.S., and Shaw, P. J. (1998). Small nucleolar RNAs and pre-rRNA processing in plants. Plant Cell 10, 649-657.
9. Calikowski, T. T., Meulia, T., and Meier, I. (2003). A proteomic study of the Arabidopsis nuclear matrix. J. Cell. Biochem. 90, 361-378.
10. Carmo-Fonseca, M., Mendez-Soares, L., and Campos, I. (2000). To be or not to be in the nucleolus. Nat. Cell Biol. 2, E107-E112.
11. Chan, C. C., Dostie, J., Diem, M. D., Feng, W., Mann, M., Rappsilber, J., and Dreyfuss, G. (2004). eIF4A3 is a novel component of the exon junction complex. RNA 10, 200-209.
12. Chen, D., and Huang, S. (2001). Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. J. Cell Biol. 153, 169-176.
13. Chen, M., Schwab, R., and Chory, J. (2003). Characterization of the requirements for localization of phytochrome B to nuclear bodies. Proc. Natl. Acad. Sci. USA 100, 14493-14498.
14. Cockell, M. M., and Gasser, S. M. (1999). Nucleolar space for RENT. Curr. Biol. 9, R575-R576.
15. Custódio, N., Carvalho, C., Condado, I., Antoniou, M., Blencowe, B. J., and Carmo-Fonseca, M. (2004). In vivo recruitment of exon junction complex proteins to transcription sites in mammalian cell nuclei. RNA 10, 622-633.
16. Darzacq, X., Jady, B. E., Verheggen, C., Kiss, A. M., Bertrand, E., and Kiss, T. (2002). Cajal body-specific small nuclear RNAs: a novel class of 2′-O-methylation and pseudouridylation guide RNAs. EMBO J. 21, 2746-2756.
17. Dragon, F. et al. (2002). A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417, 967-970.
18. Dreyfuss, G., Kim, V. N., and Kataoka, N. (2002). messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell. Biol. 3, 195-205.
19. Fatica, A., and Tollervey, D. (2002). Making ribosomes. Curr. Opin. Cell Biol. 14, 313-318.
20. Filipowicz, W., and Pogacic, V. (2002). Biogenesis of small nucleolar ribonucleoproteins. Curr. Opin. Cell Biol. 14, 319-327.
21. Fox, A. H., Lam, Y. W., Leung, A.K.L., Lyon, C. E., Andersen, J., Mann, M., and Lamond, A. I. (2002). Paraspeckles: a novel nuclear domain. Curr. Biol. 12, 13-25.
22. Gonzalez-Melendi, P., Wells, B., Beven, A. F., and Shaw, P. J. (2001). Single ribosomal transcription units are linear, compacted Christmas trees in plant nucleoli. Plant J. 27, 223-233.
23. Gunning, B.E.S. Plant Cell Biology on CD - information for students and a resource for teachers, Part 1. World Wide Web URL: www.plantcellbiologyonCD. com. Accessed November 18, 2004.
24. Han, M. H., Goud, S., Song, L., and Fedoroff, N. (2004). The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc. Natl. Acad. Sci. USA 101, 1093-1098.
25. Hayano, T., Yanagida, M., Yamauchi, Y., Shinkawa, T., Isobe, T., and Takahashi, N. (2003). Proteomic analysis of human Nop56p-associated pre-ribosomal ribonucleoprotein complexes. J. Biol. Chem. 278, 34309-34319.
26. Horn, H. F., and Vousden, K. H. (2004). Guarding the guardian. Nature 427, 110-111.
27. Ishigaki, Y., Li., X. Serin, G., and Maquat, L. E. (2001). Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106, 607-617.
28. Jady, B. E., Darzacq, X., Tucker, K. E., Matera, A. G., Bertrand, E., and Kiss, T. (2003). Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm. EMBO J. 22, 1878-1888.
29. Jady, B., and Kiss, T. (2001). A small nucleolar guide RNA functions in 2′-O-ribose methylation and pseudouridylation of the U5 spliceosomal RNA. EMBO J. 20, 541-551.
30. Kataoka, N., Diem, M. D., Kim, V. N., Yong, J., and Dreyfuss, G. (2001). Magoh, a human homologue of Drosophila mago nashi protein, is a component of the splicing-dependent exon-exon junction complex. EMBO J. 20, 6424-6433.
31. Kircher, S., Gil, P., Kozma-Bognar, L., Fejes, E., Speth, V., Husselstein-Muller, T., Bauer, D., Adam, E., Schafer, E. and Nagy, F. (2002). Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell, 14, 1541-1555.
32. Kiss, T. (2002). Small nucleolar RNAs: an abundant group of non-coding RNAs with diverse cellular functions. Cell 109, 145-148.
33. Koberna, K., Malinsky, J., Pliss, A., Masata, M., Vecerova, J., Fialova, M., Bednar, J., and Raska, I. (2002). Ribosomal genes in focus: new transcripts label the dense fibrillar components and form clusters indicative of "Christmas trees" in situ. J. Cell Biol. 157, 743-748.
34. Koroleva, O., Tomlinson, M., Leader, D., Shaw, P., and Doonan, J. (2005). High-throughput protein localization in Arabidopsis using Agrobacterium- mediated transient expression of GFP-ORF fusions. Plant J. (in press).
35. Lafontaine, D.L.J., and Tollervey, D. (2001). The function and synthesis of ribosomes. Nat. Rev. Mol. Cell. Biol. 2, 514-520.
36. Lamond, A. I., and Earnshaw, W. C. (1998). Structure and function in the nucleolus. Science 291, 843-847.
37. Lamond, A. I., and Spector, D.L. (2003). Nuclear speckles: a model for nuclear organelles. Nat. Rev. Mol. Cell. Biol. 4, 605-612.
38. Le Hir, H., Gatfield, D., Izauralde, E., and Moore, M. J. (2001a). The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay. EMBO J. 20, 4987-4997.
39. Le Hir, H., Gatfield, D., Braun, I. C., Forler, D., and Izzuralde, E. (2001b). The protein Mago provides a link between splicing and mRNA localization. EMBO Rep. 2, 1119-1124.
40. Lejeune, F., Ishigaki, Y., Li, X., and Maquat, L. E. (2002). The exon junction complex is detected on CBP80-bound but not eIF4E-bound mRNA in mammalian cells: dynamics of mRNP remodelling. EMBO J. 21, 3536-3545.
41. Leung, A.K.L., and Lamond, A. I. (2002). In vivo analysis of NHPX reveals a novel nucleolar localization pathway involving a transient accumulation in splicing speckles. J. Cell Biol. 157, 615-629.
42. Leung, A.K.L., Andersen, J. S., Mann, M., and Lamond, A. I. (2003). Bioinformatics analysis of the nucleolus. Biochem. J. 376, 553-569.
43. Lorkovic, Z. J., Hilscher, J., and Barta, A. (2004a). Use of fluorescent protein tags to study nuclear organization of the spliceosomal machinery in transiently transformed living plant cells. Mol. Biol. Cell 15, 3233-3243.
44. Lorkovic, Z. J., Lopato, S., Pexa, M., Lehner, R., and Barta, A. (2004b). Interactions of arabidopsis RS domain containing cyclophilins with SR proteins and U1 and U11 snRNP-specific proteins suggest their involvement in pre-mRNA splicing. J. Biol. Chem. 279, 33890-33898.
45. Lykke-Andersen, J., Shu, M. D., and Steitz, J. A. (2001). Communication of the position of exon-exon junctions to the mRNA surveillance machinery by the protein RNPS1. Science 293, 1836-1839.
46. Lytle, J. R., and Stietz, J. A. (2004). Premature termination codons do not affect the rate of splicing of neighbouring introns. RNA 10, 657-668.
47. Macknight, S. (2003). Gene switching by metabolic enzymes-how did you get on the invitation list? Cell 114, 150-152.
48. Maquat, L. E. (2004). Nonsense-mediated mRNA decay: splicing, translation and mRNA dynamics. Nat. Rev. Mol. Cell. Biol. 5, 89-99.
49. Matera, A. G. (1999). Nuclear bodies: multifaceted sub-domains of the interchromatin space. Trends Cell Biol. 9, 302-309.
50. Mazzola, J. L., and Sirover, M. A. (2002). Alteration of intracellular structure and function of glyceraldehydes-3-phosphate dehydrogenase: a common phenotype of neurodegenerative disorders? Neurotoxicology 23, 603-609.
51. Mo, B., Tse, Y. C., and Jiang, L. (2003). Organelle identification and proteomics in plant cells. Trends Biotechnol. 21, 331-332.
52. Olsen, M. O., Dundr, M., and Szebeni, A. (2000). The nucleolus: an old factory with unexpected capabilities. Trends Cell Biol. 10, 189-196.
53. Palacios, I. M., Gatfield, G., St. Johnston, D., and Izaurralde, E. (2004). An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427, 753-757.
54. Pedersen, T. (1998). The plurifunctional nucleolus. Nucleic Acids Res. 26, 3871-3876.
55. Phair, R. D., and Misteli, T. (2000). High mobility of proteins in the mammalian cell nucleus. Nature 404, 604-609.
56. Pluk, H., Soffner, J., Luhrmann, R., and van Venrooij, W. J. (1998). cDNA cloning and characterization of the human U3 small nucleolar ribonucleoprotein complex-associated 55-kilodalton protein Mol. Cell. Biol. 18, 488-498.
57. Rappsilber, J., and Mann, M. (2002). What does it mean to identify a protein in proteomics? Trends Biochem. Sci. 27, 74-78.
58. Reed, R., and Hurt, E. A. (2002). A conserved mRNA export machinery coupled to pre-mRNA splicing. Cell 108, 523-531.
59. Rocak, S., and Linder, P. (2004). DEAD-box proteins: the driving forces behind RNA metabolism. Nat. Rev. Mol. Cell. Biol. 5, 232-241.
60. Rubbi, C. P., and Milner, J. (2003). Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J. 22, 6068-6077.
61. Saxena, P.K., Fowke, L. C., and King, J. (1985). An efficient procedure for isolation of nuclei from plant protoplasts. Protoplasma 128, 184-189.
62. Scherl, A., Couté, Y., Déon, C., Callé, A., Kindbeiter, K., Sanchez, J.-C., Greco, A., Hochstrasse, D., and Diaz, J.-J. (2002). Functional proteomics analysis of human nucleolus. Mol. Biol. Cell 13, 4100-4109.
63. Scheer, U., and Hock, R. (1999). Structure and function of the nucleolus. Curr. Opin. Cell Biol. 11, 385-390.
64. Shaw, P. J. (2004). The nucleolus. In: Nature Encyclopaedia of Life Sciences/ www.els.net. Edited by: Nature Publishing Group.
65. Shaw, P. J. and Brown, J.W.S. (2004). Plant nuclear bodies. Curr. Opin. Plant Biol. 7, 614-620.
66. Shaw, P. J., and Jordan, E. G. (1995). The nucleolus. Annu. Rev. Cell Dev. Biol. 11, 93-121.
67. Sleeman, J. E., and Lamond, A. I. (1999). Newly assembled snRNPs associate with coiled bodies before speckles, suggesting a nuclear snRNP maturation pathway. Curr. Biol. 9, 1065-1074.
68. Stutz, F., and Izauralde, E. (2003). The interplay of nuclear mRNP assembly, mRNA surveillance and export. Trends Cell Biol. 13, 319-327.
69. Taylor, S. W., Fahy, E., and Ghosh, S. S. (2003). Global organellar proteomics. Trends Biotechnol. 21, 82-87.
70. Visintin, R., and Amon, A. (2000). The nucleolus: the magician's hat for cell cycle tricks. Curr. Opin. Cell Biol. 12, 372-377.
71. Wang, C., and Meier, U. T. (2004). Architecture and assembly of mammalian H/ACA small nucleolar and telomerase ribonucleoproteins. EMBO J. 23, 1857-1867.
72. Watkins, N. J., Segault, V., Charpentier, B., Nottrott, S., Fabrizio, P., Bachi, A., Wilm, M., Rosbash, M., Branlant, C., and Lührmann, R. (2000). A common core RNP structure shared between the small nucleolar box C/D RNPs and the spliceosomal U4 snRNP. Cell 103, 457-466.
73. Watkins, N. J., Dickmanns, A., and Lührmann, R. (2002). Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5K protein, for the hierarchical assembly of the box C/D snoRNP. Mol. Cell. Biol. 22, 8342-8352.
74. Wendel, J. F. (2000). Genome evolution in polyploids. Plant Mol. Biol. 42, 225-249.
75. Wilkinson, M. F., and Shyu, A.-B. (2002). RNA surveillance by nuclear scanning? Nat. Cell Biol. 4, E144-E147.
76. Westendorf, J. M., Konstantinov, K. N., Wormsley, S., Shu, M. D., Matsumoto-Taniura, N., Pirollet, F., Klier, F. G., Gerace, L. and Baserga, S. J. (1998). M phase phosphoprotein 10 is a human U3 small nucleolar ribonucleoprotein component. Mol. Biol. Cell 9, 437-449.
77. Zheng, L., Roeder, R. G., and Luo, Y. (2003). S phase activation of the histone promoter OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 114, 255-266.
78. Zhou, Z., Luo, M. J., Straesser, K., Katahira, J., Hurt, E., and Reed, R. (2000). The protein Aly links pre-messenger RNA splicing to nuclear export in metazoans. Nature 407, 401-405.