The Arabidopsis cytosolic ribosomal proteome: From form to function

Frontiers in Plant Science

Volumn 4, Issue MAR, 2013, Pages

  Carroll, Adam J ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

80S ribosomes; Arabidopsis; Cytosolic ribosomes; Plants; Proteomics; Ribosomes; Sub cellular proteomics; Translation

Indexed keywords

EID: 84883224766     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00032     Document Type: Review

References (113)

1. Adams, K. L., Daley, D. O., Whelan, J., and Palmer, J. D. (2002). Genes for two mitochondrial ribosomal proteins in flowering plants are derived from their chloroplast or cytosolic counterparts. Plant Cell 14, 931-943.
2. Arnold, R. J., Polevoda, B., Reilly, J. P., and Sherman, F. (1999). The action of N-terminal acetyltransferases on yeast ribosomal proteins. J. Biol. Chem. 274, 37035-37040.
3. Bachand, F., and Silver, P. A. (2004). PRMT3 is a ribosomal protein methyltransferase that affects the cellular levels of ribosomal subunits. EMBO J. 23, 2641-2650.
4. Bain, J. D., Switzer, C., Chamberlin, R., and Bennert, S. A. (1992). Ribosome-mediated incorporation of a non-standard amino acid into a peptide through expansion of the genetic code. Nature 356, 537-539.
5. Barakat, A., Szick-Miranda, K., Chang, I.-F., Guyot, R., Blanc, G., Cooke, R., et al. (2001). The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome. Plant Physiol. 127, 398-415.
6. Benner, S. A. (1994). Expanding the genetic lexicon: incorporating non-standard amino acids into proteins by ribosome-based synthesis. Trends Biotechnol. 12, 158-163.
7. Branco-Price, C., Kaiser, K. A., Jang, C. J., Larive, C. K., and Bailey-Serres, J. (2008). Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J. 56, 743-755.
8. Branco-Price, C., Kawaguchi, R., Ferreira, R. B., and Bailey-Serres, J. (2005). Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann. Bot. 96, 647-660.
9. Byrne, M. E. (2009). A role for the ribosome in development. Trends Plant Sci. 14, 512-519.
10. Carroll, A. J., Heazlewood, J. L., Ito, J., and Millar, A. H. (2008). Analysis of the Arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol. Cell. Proteomics 7, 347-369.
11. Ceci, M., Gaviraghi, C., Gorrini, C., Sala, L. A., Offenhauser, N., Carlo Marchisio, P., et al. (2003). Release of eIF6 (p27BBP) from the 60S subunit allows 80S ribosome assembly. Nature 426, 579-584.
12. Chang, I.-F. (2006). Mass spectrometry-based proteomic analysis of the epitope-tag affinity purified protein complexes in eukaryotes. Proteomics 6, 6158-6166.
13. Chang, I.-F., Szick-Miranda, K., Pan, S., and Bailey-Serres, J. (2005). Proteomic characterization of evolutionarily conserved and variable proteins of Arabidopsis cytosolic ribosomes. Plant Physiol. 137, 848-862.
14. Chen, J.-G., Ullah, H., Temple, B., Liang, J., Guo, J., Alonso, J. M., et al. (2006). RACK1 mediates multiple hormone responsiveness and developmental processes in Arabidopsis. J. Exp. Bot. 57, 2697-2708.
15. Choi, H., Lee, H.-S., and Park, Z.-Y. (2008). Detection of multiphosphorylated peptides in LC-MS/MS analysis under low pH conditions. Anal. Chem. 80, 3007-3015.
16. Degenhardt, R. F., and Bonham-Smith, P. C. (2008). Arabidopsis ribosomal proteins RPL23aA and RPL23aB are differentially targeted to the nucleolus and are disparately required for normal development. Plant Physiol. 147, 128-142.
17. Ferreyra, M. L. F., Biarc, J., Burlingame, A. L., and Casati, P. (2010a). Arabidopsis L10 ribosomal proteins in UV-B responses. Plant Signal. Behav. 5, 1222-1225.
18. Ferreyra, M. L. F., Pezza, A., Biarc, J., Burlingame, A. L., and Casati, P. (2010b). Plant L10 ribosomal proteins have different roles during development and translation under ultraviolet-B stress. Plant Physiol. 153, 1878-1894.
19. Finnie, C., and Svensson, B. (2002). Proteolysis during the isoelectric focusing step of two-dimensional gel electrophoresis may be a common problem. Anal. Biochem. 311, 182-186.
20. Forte, G. M. A., Pool, M. R., and Stirling, C. J. (2011). N-terminal acetylation inhibits protein targeting to the endoplasmic reticulum. PLoS Biol. 9:e1001073. doi:10.1371/journal.pbio.1001073
21. Fu, S., Fan, J., Blanco, J., Gimenez-Cassina, A., Danial, N. N., Watkins, S. M., et al. (2012). Polysome profiling in liver identifies dynamic regulation of endoplasmic reticulum translatome by obesity and fasting. PLoS Genet.8:e1002902. doi:10.1371/journal.pgen.1002902
22. Giavalisco, P., Wilson, D., Kreitler, T., Lehrach, H., Klose, J., Gobom, J., et al. (2005). High heterogeneity within the ribosomal proteins of the Arabidopsis thaliana 80S ribosome. Plant Mol. Biol. 57, 577-591.
23. Gilbert, W. V. (2011). Functional specialization of ribosomes? Trends Biochem. Sci. 36, 127-132.
24. Guo, J., and Chen, J.-G. (2008). RACK1 genes regulate plant development with unequal genetic redundancy inArabidopsis. BMC Plant Biol. 8:108. doi:10.1186/1471-2229-8-108
25. Guo, J., Wang, J., Xi, L., Huang, W.-D., Liang, J., and Chen, J.-G. (2009a). RACK1 is a negative regulator of ABA responses in Arabidopsis. J. Exp. Bot. 60, 3819-3833.
26. Guo, J., Wang, S., Wang, J., Huang, W.-D., Liang, J., and Chen, J.-G. (2009b). Dissection of the relationship between RACK1 and heterotrimeric G-proteins in Arabidopsis. Plant Cell Physiol. 50, 1681-1694.
27. Guo, J., Wang, S., Valerius, O., Hall, H., Zeng, Q., Li, J.-F., et al. (2011). Involvement of Arabidopsis RACK1 in protein translation and its regulation by abscisic acid. Plant Physiol. 155, 370-383.
28. Gurtubay, J. I. G., Goñi, F. M., Gómez-Fernández, J. C., Otamendi, J. J., and MacArulla, J. M. (1980). Triton X-100 solubilization of mitochondrial inner and outer membranes. J. Bioenerg. Biomembr. 12, 47-70.
29. Heazlewood, J. L., Verboom, R. E., Tonti-Filippini, J., Small, I., and Millar, A. H. (2007). SUBA: the Arabidopsissubcellular database. Nucleic Acids Res. 35, D213-D218.
30. Horiguchi, G., Molla-Morales, A., Perez-Perez, J. M., Kojima, K., Robles, P., Ponce, M. R., et al. (2011). Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development. Plant J. 65, 724-736.
31. Hummel, M., Cordewener, J. H. G., De Groot, J. C. M., Smeekens, S., America, A. H. P., and Hanson, J. (2012). Dynamic protein composition of Arabidopsis thaliana cytosolic ribosomes in response to sucrose feeding as revealed by label free MSE proteomics. Proteomics 12, 1024-1038.
32. Imai, A., Komura, M., Kawano, E., Kuwashiro, Y., and Takahashi, T. (2008). A semi-dominant mutation in the ribosomal protein L10 gene suppresses the dwarf phenotype of the acl5 mutant in Arabidopsis thaliana. Plant J.56, 881-890.
33. Ingolia, N. T., Ghaemmaghami, S., Newman, J. R. S., and Weissman, J. S. (2009). Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324, 218-223.
34. Ishihama, Y., Oda, Y., Tabata, T., Sato, T., Nagasu, T., Rappsilber, J., et al. (2005). Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics 4, 1265-1272.
35. Ito, T., Kim, G. T., and Shinozaki, K. (2000). Disruption of an Arabidopsis cytoplasmic ribosomal protein S13-homologous gene by transposon-mediated mutagenesis causes aberrant growth and development. Plant J. 22, 257-264.
36. Jakob, N., Jayati, S., Joachim, F., and Poul, N. (2004). Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO Rep. 5, 1137-1141.
37. Kaltimbacher, V., Bonnet, C., Lecoeuvre, G., Forster, V., Sahel, J.-A., and Corral-Debrinski, M. (2006). mRNA localization to the mitochondrial surface allows the efficient translocation inside the organelle of a nuclear recoded ATP6 protein. RNA 12, 1408-1417.
38. Kannan, K., Vázquez-Laslop, N., and Mankin, A. S. (2012). Selective protein synthesis by ribosomes with a drug-obstructed exit tunnel. Cell 151, 508-520.
39. Kapp, L. D., and Lorsch, J. R. (2004). The molecular mechanics of eukaryotic translation. Annu. Rev. Biochem. 73, 657-704.
40. Kawaguchi, R., Williams, A. J., Bray, E. A., and Bailey-Serres, J. (2003). Water-deficit-induced translational control in Nicotiana tabacum. Plant Cell Environ. 26, 221-229.
41. Komili, S., Farny, N. G., Roth, F. P., and Silver, P. A. (2007). Functional specificity among ribosomal proteins regulates gene expression. Cell 131, 557-571.
42. Laby, R. J., Kincaid, M. S., Kim, D., and Gibson, S. I. (2000). The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J. 23, 587-596.
43. Leaver, C. J., and Harmey, M. A. (1973). Plant mitochondrial nucleic acids. Biochem. Soc. Symp. 175-193.
44. Leaver, C. J., and Harmey, M. A. (1976). Higher-plant mitochondrial ribosomes contain a 5S ribosomal ribonucleic acid component. Biochem. J. 157, 275-277.
45. Lee, S., Liu, B., Lee, S., Huang, S.-X., Shen, B., and Qian, S.-B. (2012). Global mapping of translation initiation sites in mammalian cells at single-nucleotide resolution. Proc. Natl. Acad. Sci. U.S.A. 109, E2424-E2432.
46. Lee, S. W., Berger, S. J., Martinovic, S., Pasa-Tolic, L., Anderson, G. A., Shen, Y., et al. (2002). Direct mass spectrometric analysis of intact proteins of the yeast large ribosomal subunit using capillary LC/FTICR. Proc. Natl. Acad. Sci. U.S.A. 99, 5942-5947.
47. Liu, M.-J., Wu, S.-H., Chen, H.-M., and Wu, S.-H. (2012). Widespread translational control contributes to the regulation of Arabidopsis photomorphogenesis. Mol. Syst. Biol. 8, 566.
48. Louie, D. F., Resing, K. A., Lewis, T. S., and Ahn, N. G. (1996). Mass spectrometric analysis of 40 S ribosomal proteins from Rat-1 fibroblasts. J. Biol. Chem. 271, 28189-28198.
49. Mager, W. H., Planta, R. J., Ballesta, J.-P. G., Lee, J. C., Mizuta, K., Suzuki, K., et al. (1997). A new nomenclature for the cytoplasmic ribosomal proteins of Saccharomyces cerevisiae. Nucleic Acids Res. 25, 4872-4875.
50. Mahfouz, M. M., Kim, S., Delauney, A. J., and Verma, D. P. S. (2006). Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18, 477-490.
51. Manuell, A. L., Yamaguchi, K., Haynes, P. A., Milligan, R. A., and Mayfield, S. P. (2005). Composition and structure of the 80S ribosome from the green alga Chlamydomonas reinhardtii: 80S ribosomes are conserved in plants and animals. J. Mol. Biol. 351, 266-279.
52. Mazumder, B., Sampath, P., Seshadri, V., Maitra, R. K., Dicorleto, P. E., and Fox, P. L. (2003). Regulated release of L13a from the 60S ribosomal subunit as a mechanism of transcript-specific translational control. Cell 115, 187-198.
53. McIntosh, K. B., and Warner, J. R. (2007). Yeast ribosomes: variety is the spice of life. Cell 131, 450-451.
54. Mizoguchi, T., Hayashida, N., Yamaguchi-Shinozaki, K., Kamada, H., and Shinozaki, K. (1995). Two genes that encode ribosomal-protein S6 kinase homologs are induced by cold or salinity stress in Arabidopsis thaliana. FEBS Lett. 358, 199-204.
55. Molina, H., Horn, D. M., Tang, N., Mathivanan, S., and Pandey, A. (2007). Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 104, 2199-2204.
56. Morimoto, T., Suzuki, Y., and Yamaguchi, I. (2002). Effects of partial suppression of ribosomal protein S6 on organ formation in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 66, 2437-2443.
57. Mustroph, A., Zanetti, M. E., Jang, C. J., Holtan, H. E., Repetti, P. P., Galbraith, D. W., et al. (2009). Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 106, 18843-18848.
58. Neumann, H. (2012). Rewiring translation-genetic code expansion and its applications. FEBS Lett. 586, 2057-2064.
59. Neumann, H., Wang, K., Davis, L., Garcia-Alai, M., and Chin, J. W. (2010). Encoding multiple unnatural amino acids via evolution of a quadruplet-decoding ribosome. Nature 464, 441-444.
60. Nishimura, T., Wada, T., and Okada, K. (2004). A key factor of translation reinitiation, ribosomal protein L24, is involved in gynoecium development in Arabidopsis. Biochem. Soc. Trans. 32, 611-613.
61. Nishimura, T., Wada, T., Yamamoto, K. T., and Okada, K. (2005). The Arabidopsis STV1 protein, responsible for translation reinitiation, is required for auxin-mediated gynoecium patterning. Plant Cell 17, 2940-2953.
62. Odintsova, T. I., Muller, E. C., Ivanov, A. V., Egorov, T. A., Bienert, R., Vladimirov, S. N., et al. (2003). Characterization and analysis of posttranslational modifications of the human large cytoplasmic ribosomal subunit proteins by mass spectrometry and Edman sequencing. J. Protein Chem. 22, 249-258.
63. Piekna-Przybylska, D., Przybylski, P., Baudin-Baillieu, A., Rousset, J.-P., and Fournier, M. J. (2008). Ribosome performance is enhanced by a rich cluster of pseudouridines in the A-site finger region of the large subunit. J. Biol. Chem. 283, 26026-26036.
64. Pinel, C., Douce, R., and Mache, R. (1986). A study of mitochondrial ribosomes from the higher plant Solanum tuberosum L. Mol. Biol. Rep. 11, 93-97.
65. Pinon, V., Etchells, J. P., Rossignol, P., Collier, S. A., Arroyo, J. M., Martienssen, R. A., et al. (2008). Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 135, 1315-1324.
66. Piques, M., Schulze, W. X., Hohne, M., Usadel, B., Gibon, Y., Rohwer, J., et al. (2009). Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis. Mol. Syst. Biol. 5, 314.
67. Porras-Yakushi, T. R., Whitelegge, J. P., and Clarke, S. (2008). A novel SET domain methyltransferase in yeast: Rkm2-dependent trimethylation of ribosomal protein L12ab at the N terminus. VOLUME 281 (2006) PAGES 35835-35845. J. Biol. Chem. 283, 15512.
68. Porras-Yakushi, T. R., Whitelegge, J. P., Miranda, T. B., and Clarke, S. (2005). A novel SET domain methyltransferase modifies ribosomal protein Rpl23ab in yeast. J. Biol. Chem. 280, 34590-34598.
69. Pring, D. R. (1974). Maize mitochondria: purification and characterization of ribosomes and ribosomal ribonucleic acid. Plant Physiol. 53, 677-683.
70. Rackham, O., and Chin, J. W. (2005). A network of orthogonal ribosome x mRNA pairs. Nat. Chem. Biol. 1, 159-166.
71. Rackham, O., and Chin, J. W. (2006). Synthesizing cellular networks from evolved ribosome-mRNA pairs. Biochem. Soc. Trans. 34, 328-329.
72. Ren, J., Wang, Y., Liang, Y., Zhang, Y., Bao, S., and Xu, Z. (2010). Methylation of ribosomal protein S10 by protein-arginine methyltransferase 5 regulates ribosome biogenesis. J. Biol. Chem. 285, 12695-12705.
73. Revenkova, E., Masson, J., Koncz, C., Afsar, K., Jakovleva, L., and Paszkowski, J. (1999). Involvement ofArabidopsis thaliana ribosomal protein S27 in mRNA degradation triggered by genotoxic stress. EMBO J. 18, 490-499.
74. Santoro, R., Lienemann, P., and Fussenegger, M. (2009). Epigenetic engineering of ribosomal RNA genes enhances protein production. PLoS ONE 4:e6653. doi:10.1371/journal.pone.0006653
75. Scharf, K. D., and Nover, L. (1982). Heat-shock-induced alterations of ribosomal protein phosphorylation in plant cell cultures. Cell 30, 427-437.
76. Shor, B., Calaycay, J., Rushbrook, J., and McLeod, M. (2003). Cpc2/RACK1 is a ribosome-associated protein that promotes efficient translation in Schizosaccharomyces pombe. J. Biol. Chem. 278, 49119-49128.
77. Stapels, M. D., and Barofsky, D. F. (2004). Complementary use of MALDI and ESI for the HPLC-MS/MS analysis of DNA-binding proteins. Anal. Chem. 76, 5423-5430.
78. Stavreva, D. A., Kawasaki, M., Dundr, M., Koberna, K., Müller, W. G., Tsujimura-Takahashi, T., et al. (2006). Potential roles for ubiquitin and the proteasome during ribosome biogenesis. Mol. Cell. Biol. 26, 5131-5145.
79. Stirnberg, P., Liu, J. P., Ward, S., Kendall, S. L., and Leyser, O. (2012). Mutation of the cytosolic ribosomal protein-encoding RPS10B gene affects shoot meristematic function in Arabidopsis. BMC Plant Biol. 12:160. doi:10.1186/1471-2229-12-160
80. Sugihara, Y., Honda, H., Iida, T., Morinaga, T., Hino, S., Okajima, T., et al. (2010). Proteomic analysis of rodent ribosomes revealed heterogeneity including ribosomal proteins L10-like, L22-like 1, and L39-like. J. Proteome Res.9, 1351-1366.
81. Suissa, M., and Schatz, G. (1982). Import of proteins into mitochondria. Translatable mRNAs for imported mitochondrial proteins are present in free as well as mitochondria-bound cytoplasmic polysomes. J. Biol. Chem.257, 13048-13055.
82. Szakonyi, D., and Byrne, M. E. (2011). Ribosomal protein L27a is required for growth and patterning in Arabidopsis thaliana. Plant J. 65, 269-281.
83. Szick, K., Springer, M., and Bailey-Serres, J. (1998). Evolutionary analyses of the 12-kDa acidic ribosomal P-proteins reveal a distinct protein of higher plant ribosomes. Proc. Natl. Acad. Sci. U.S.A. 95, 2378-2383.
84. Szick-Miranda, K., and Bailey-Serres, J. (2001). Regulated heterogeneity in 12-kDa P-protein phosphorylation and composition of ribosomes in Maize (Zea mays L.). J. Biol. Chem. 276, 10921-10928.
85. Szick-Miranda, K., Zanial, A., Zanial, A., Abidayo, S., and Slater, K. C. (2010). Analysis of RPS15aE, an isoform of a plant-specific evolutionarily distinct ribosomal protein in Arabidopsis thaliana, reveals its potential role as a growth regulator. Plant Mol. Biol. Rep. 28, 239-252.
86. Taira, H., Fukushima, M., Hohsaka, T., and Sisido, M. (2005). Four-base codon-mediated incorporation of nonnatural amino acids into proteins in a eukaryotic cell-free translation system. J. Biosci. Bioeng. 99, 473-476.
87. Turck, F., Zilbermann, F., Kozma, S. C., Thomas, G., and Nagy, F. (2004). Phytohormones participate in an S6 kinase signal transduction pathway in Arabidopsis. Plant Physiol. 134, 1527-1535.
88. Turkina, M. V., Klang Årstrand, H., and Vener, A. V. (2011). Differential phosphorylation of ribosomal proteins inArabidopsis thaliana plants during day and night. PLoS ONE 6:e29307. doi:10.1371/journal.pone.0029307
89. Van Lijsebettens, M., Vanderhaeghen, R., De Block, M., Bauw, G., Villarroel, R., and Van Montagu, M. (1994). An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J. 13, 3378.
90. Vasconcelos, A. C., and Bogorad, L. (1971). Proteins of cytoplasmic, chloroplast, and mitochondrial ribosomes of some plants. Biochim. Biophys. Acta 228, 492-502.
91. Vohradsky, J., Branny, P., Li, X.-M., and Thompson, C. J. (2008). Effect of protein degradation on spot Mr distribution in 2-D gels-a case study of proteolysis during development of Streptomyces coelicolor cultures. Proteomics 8, 2371-2375.
92. Wagner, H. (1989). Free-flow electrophoresis. Nature 341, 669-670.
93. Wang, B., Malik, R., Nigg, E. A., and KöRner, R. (2008). Evaluation of the low-specificity protease elastase for large-scale phosphoproteome analysis. Anal. Chem. 80, 9526-9533.
94. Warner, J. R. (1999). The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24, 437-440.
95. Webb, K. J., Al-Hadid, Q., Zurita-Lopez, C. I., Young, B. D., Lipson, R. S., and Clarke, S. G. (2011). The ribosomal L1 protuberance in yeast is methylated on a lysine residue catalyzed by a seven-β-strand methyltransferase. J. Biol. Chem. 286, 18405-18413.
96. Webb, K. J., Lipson, R. S., Al-Hadid, Q., Whitelegge, J. P., and Clarke, S. G. (2010a). Identification of protein N-terminal methyltransferases in yeast and humans. Biochemistry 49, 5225-5235.
97. Webb, K. J., Zurita-Lopez, C. I., Al-Hadid, Q., Laganowsky, A., Young, B. D., Lipson, R. S., et al. (2010b). A novel 3-methylhistidine modification of yeast ribosomal protein Rpl3 is dependent upon the YIL110W methyltransferase.J. Biol. Chem. 285, 37598-37606.
98. Weijers, D., Franke-Van Dijk, M., Vencken, R. J., Quint, A., Hooykaas, P., and Offringa, R. (2001). An Arabidopsisminute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128, 4289-4299.
99. Williams, A. J., Werner-Fraczek, J., Chang, I.-F., and Bailey-Serres, J. (2003). Regulated phosphorylation of 40S ribosomal protein S6 in root tips of maize. Plant Physiol. 132, 2086-2097.
100. Williams, M. E., and Sussex, I. M. (1995). Developmental regulation of ribosomal protein L16 genes in Arabidopsis thaliana. Plant J. 8, 65-76.
101. Wilson, D. N., and Doudna Cate, J. H. (2012). The structure and function of the eukaryotic ribosome. Cold Spring Harb. Perspect. Biol. 4, pii: a011536.
102. Woeller, C. F., Fox, J. T., Perry, C., and Stover, P. J. (2007). A ferritin-responsive internal ribosome entry site regulates folate metabolism. J. Biol. Chem. 282, 29927-29935.
103. Wool, I. G., Chan, Y.-L., and Glück, A. (1995). Structure and evolution of mammalian ribosomal proteins. Biochem. Cell Biol. 73, 933-947.
104. Xue, S., and Barna, M. (2012). Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell Biol. 13, 355-369.
105. Yamaguchi, K. (2011). "Preparation and proteomic analysis of chloroplast ribosomes, " in Chloroplast Research in Arabidopsis, ed. R. P. Jarvis (New York: Humana Press), 241-264.
106. Yamaguchi, K., Beligni, M. V., Prieto, S., Haynes, P. A., Mcdonald, W. H., Yates, J. R., et al. (2003). Proteomic characterization of the Chlamydomonas reinhardtii chloroplast ribosome. J. Biol. Chem. 278, 33774-33785.
107. Yang, P., Fu, H., Walker, J., Papa, C. M., Smalle, J., Ju, Y.-M., et al. (2004). Purification of the Arabidopsis 26 S proteasome: biochemical and molecular analyses revealed the presence of multiple isoforms. J. Biol. Chem. 279, 6401-6413.
108. Yao, Y., Ling, Q., Wang, H., and Huang, H. (2008). Ribosomal proteins promote leaf adaxial identity. Development135, 1325-1334.
109. Yu, Y., Ji, H., Doudna, J. A., and Leary, J. A. (2005). Mass spectrometric analysis of the human 40S ribosomal subunit: native and HCV IRES-bound complexes. Protein Sci. 14, 1438-1446.
110. Zanetti, M. E., Chang, I.-F., Gong, F., Galbraith, D. W., and Bailey-Serres, J. (2005). Immunopurification of polyribosomal complexes of Arabidopsis for global analysis of gene expression. Plant Physiol. 138, 624-635.
111. Zhang, H., and Ge, Y. (2011). Comprehensive analysis of protein modifications by top-down mass spectrometry. Circ. Cardiovasc. Genet. 4, 711.
112. Zhou, H., Ning, Z. E., Starr, A., Abu-Farha, M., and Figeys, D. (2011). Advancements in top-down proteomics. Anal. Chem. 84, 720-734.
113. Zorca, S. M., and Zorca, C. E. (2011). The legacy of a founding father of modern cell biology: George Emil Palade (1912-2008). Yale J. Biol. Med. 84, 113-116.