Translating the Genome in Time and Space: Specialized Ribosomes, RNA Regulons, and RNA-Binding Proteins

Annual Review of Cell and Developmental Biology

Volumn 31, Issue , 2015, Pages 31-54

  Shi, Zhen ^a   Barna, Maria ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Ribosomal proteins; Ribosome centered regulation; RNA regulons; RNA binding proteins; Specialized translation machinery

Indexed keywords

CIS ACTING ELEMENT; MESSENGER RNA; RIBOSOME PROTEIN; RIBOSOME RNA; RNA BINDING PROTEIN; RNA;

ARTICLE; CELL FATE; CELL MATURATION; GENE CONTROL; GENETIC ANALYSIS; GENETIC CODE; GENOME; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULON; RIBOSOME; RNA SEQUENCE; RNA TRANSLATION; TISSUE SPECIFICITY; UNTRANSLATED REGION; ANIMAL; GENE EXPRESSION REGULATION; GENETICS;

ANIMALS; GENE EXPRESSION REGULATION; GENOME; HUMANS; PROTEIN BIOSYNTHESIS; REGULON; RIBOSOMES; RNA; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84947294063     PISSN: 10810706     EISSN: 15308995     Source Type: Book Series    
DOI: 10.1146/annurev-cellbio-100814-125346     Document Type: Article

References (129)

1. Alberts B. 1998. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92(3):291-94
2. Allfrey V, Daly MM, Mirsky AE. 1953. Synthesis of protein in the pancreas. II. The role of ribonucleoprotein in protein synthesis. J. Gen. Physiol. 37(2):157-75
3. Amsterdam A, Sadler KC, Lai K, Farrington S, Bronson RT, et al. 2004. Many ribosomal protein genes are cancer genes in zebrafish. PLOS Biol. 2(5):E139
4. Anderson SJ, Lauritsen JP, Hartman MG, Foushee AM, Lefebvre JM, et al. 2007. Ablation of ribosomal protein L22 selectively impairs αβ T cell development by activation of a p53-dependent checkpoint. Immunity 26(6):759-72
5. Barbosa C, Peixeiro I, Romao L. 2013. Gene expression regulation by upstream open reading frames and human disease. PLOS Genet. 9(8):e1003529
6. Barkic M, Crnomarkovic S, Grabusic K, Bogetic I, Panic L, et al. 2009. The p53 tumor suppressor causes congenital malformations in Rpl24-deficient mice and promotes their survival. Mol. Cell. Biol. 29(10):2489-504
7. Barlow JL,Drynan LF, Hewett DR,Holmes LR, Lorenzo-Abalde S, et al. 2010. A p53-dependentmechanism underlies macrocytic anemia in a mouse model of human 5q-syndrome. Nat. Med. 16(1):59-66
8. Baum S, Bittins M, Frey S, SeedorfM. 2004. Asc1p, aWD40-domain containing adaptor protein, is required for the interaction of the RNA-binding protein Scp160p with polysomes. Biochem. J. 380(Pt. 3):823-30
9. Bellodi C, Kopmar N, Ruggero D. 2010. Deregulation of oncogene-induced senescence and p53 translational control in X-linked dyskeratosis congenita. EMBO J. 29(11):1865-76
10. Bellodi C, McMahon M, Contreras A, Juliano D, Kopmar N, et al. 2013. H/ACA small RNA dysfunctions in disease reveal key roles for noncoding RNA modifications in hematopoietic stem cell differentiation. Cell Rep. 3(5):1493-502
11. Bickle TA, Howard GA, Traut RR. 1973. Ribosome heterogeneity: the nonuniform distribution of specific ribosomal proteins among different functional classes of ribosomes. J. Biol. Chem. 248(13):4862-64
12. Bolze A, Mahlaoui N, Byun M, Turner B, Trede N, et al. 2013. Ribosomal protein SA haploinsufficiency in humans with isolated congenital asplenia. Science 340(6135):976-78
13. Boria I, Garelli E, Gazda HT, Aspesi A, Quarello P, et al. 2010. The ribosomal basis of Diamond-Blackfan anemia: mutation and database update. Hum. Mutat. 31:1269-79
14. Brar GA, Yassour M, Friedman N, Regev A, Ingolia NT, Weissman JS. 2012. High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science 335(6068):552-57
15. BridgesCB, MorganTH.1923. TheThird-ChromosomeGroup ofMutantCharacters of Drosophila Melanogaster. Baltimore, MD: Carnegie Inst
16. Brown V, Jin P, Ceman S, Darnell JC, O'Donnell WT, et al. 2001. Microarray identification of FMRPassociated brain mRNAs and alteredmRNAtranslational profiles in Fragile X syndrome. Cell 107(4):477-87
17. Budde A, Grummt I. 1999. p53 represses ribosomal gene transcription. Oncogene 18(4):1119-24
18. Buszczak M, Signer RAJ, Morrison SJ. 2014. Cellular differences in protein synthesis regulate tissue homeostasis. Cell 159(2):242-51
19. Byrgazov K, Vesper O, Moll I. 2013. Ribosome heterogeneity: another level of complexity in bacterial translation regulation. Curr. Opin. Microbiol. 16(2):133-39
20. Calkhoven CF, Muller C, Leutz A. 2000. Translational control of C/EBPαand C/EBPβisoform expression. Genes Dev. 14:1920-32
21. Calvo SE, Pagliarini DJ, Mootha VK. 2009. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. PNAS 106(18):7507-12
22. Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, et al. 2012. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149:1393-406
23. Ceci M, Gaviraghi C, Gorrini C, Sala LA, Offenhauser N, et al. 2003. Release of eIF6 (p27BBP) from the 60S subunit allows 80S ribosome assembly. Nature 426(6966):579-84
24. Chen E, Sharma MR, Shi X, Agrawal RK, Joseph S. 2014. Fragile X mental retardation protein regulates translation by binding directly to the ribosome. Mol. Cell 54(3):407-17
25. Cho J, Chang H, Kwon SC, Kim B, Kim Y, et al. 2012. LIN28A is a suppressor of ER-associated translation in embryonic stem cells. Cell 151(4):765-77
26. Cornelis S, Bruynooghe Y, Denecker G, Van Huffel S, Tinton S, Beyaert R. 2000. Identification and characterization of a novel cell cycle-regulated internal ribosome entry site. Mol. Cell 5(4):597-605
27. Coyle SM, Gilbert W V, Doudna JA. 2009. Direct link between RACK1 function and localization at the ribosome in vivo. Mol. Cell. Biol. 29(6):1626-34
28. Darnell JC, Jensen KB, Jin P, Brown V,Warren ST, Darnell RB. 2001. Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107(4):489-99
29. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A, et al. 2011. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146(2):247-61
30. De Keersmaecker K, Atak ZK, Li N, Vicente C, Patchett S, et al. 2013. Exome sequencing identifies mutation in CNOT3 and ribosomal genes RPL5 and RPL10 in T-cell acute lymphoblastic leukemia. Nat. Genet. 45(2):186-90
31. Degenhardt RF, Bonham-Smith PC. 2008. Arabidopsis ribosomal proteins RPL23aA and RPL23aB are differentially targeted to the nucleolus and are disparately required for normal development. Plant Physiol. 147(1):128-42
32. Deusser E. 1972. Heterogeneity of ribosomal populations in Escherichia coli cells grown in different media. Mol. Gen. Genet. 119(3):249-58
33. Deusser E,Wittmann HG. 1972. Ribosomal proteins: variation of the protein composition in Escherichia coli ribosomes as function of growth rate. Nature 238(5362):269-70
34. Ding Y, Tang Y, Kwok CK, Zhang Y, Bevilacqua PC, Assmann SM. 2014. In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature 505(7485):696-700
35. Falcone Ferreyra ML, Pezza A, Biarc J, Burlingame AL, Casati P. 2010. Plant L10 ribosomal proteins have different roles during development and translation under ultraviolet-B stress. Plant Physiol. 153(4):1878-94
36. Fleischer TC, Weaver CM, McAfee KJ, Jennings JL, Link AJ. 2006. Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes. Genes Dev. 20(10):1294-307
37. Frank J. 2000. The ribosome-A macromolecular machine par excellence. Chem. Biol. 7(6):R133-41
38. Garlick PJ, McNurlan MA, Preedy VR. 1980. A rapid and convenient technique for measuring the rate of protein synthesis in tissues by injection of phenylalanine. Biochem. J. 192(2):719-23
39. Ghosh A, Rideout EJ, Grewal SS. 2014. TIF-IA-dependent regulation of ribosome synthesis in Drosophila muscle is required tomaintain systemic insulin signaling and larval growth. PLOS Genet. 10(10):e1004750
40. Gingras AC, Svitkin Y, Belsham GJ, Pause A, Sonenberg N. 1996. Activation of the translational suppressor 4E-BP1 following infection with encephalomyocarditis virus and poliovirus. PNAS 93(11):5578-83
41. Golomb L, Bublik DR,Wilder S, Nevo R, Kiss V, et al. 2012. Importin 7 and exportin 1 link c-Myc and p53 to regulation of ribosomal biogenesis. Mol. Cell 45:222-32
42. Gradi A, Svitkin Y V, Imataka H, Sonenberg N. 1998. Proteolysis of human eukaryotic translation initiation factor eIF4GII, but not eIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection. PNAS 95(19):11089-94
43. Gunderson JH, Sogin ML, Wollett G, Hollingdale M, de la Cruz VF, et al. 1987. Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science 238(4829):933-37
44. Holcik M, Lefebvre C, Yeh C, Chow T, Korneluk RG. 1999. A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat. Cell Biol. 1(3):190-92
45. Holcik M, SonenbergN. 2005. Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol. 6(4):318-27
46. Horiguchi G, Van Lijsebettens M, Candela H, Micol JL, Tsukaya H. 2012. Ribosomes and translation in plant developmental control. Plant Sci. 191-192:24-34
47. Hsieh AC, Liu Y, Edlind MP, Ingolia NT, Janes MR, et al. 2012. The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 485(7396):55-61
48. Iacono M, Mignone F, Pesole G. 2005. uAUG and uORFs in human and rodent 5- untranslated mRNAs. Gene 349:97-105
49. Ingolia NT, Lareau LF, Weissman JS. 2011. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147(4):789-802
50. Jang SK, Krausslich HG, Nicklin MJ, Duke GM, Palmenberg AC, Wimmer E. 1988. A segment of the 5- nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62(8):2636-43
51. JannotG, Bajan S, Giguere NJ, Bouasker S, Banville IH, et al. 2011. The ribosomal protein RACK1 is required for microRNA function in both C. elegans and humans. EMBO Rep. 12(6):581-86
52. Kaberdina AC, Szaflarski W, Nierhaus KH, Moll I. 2009. An unexpected type of ribosomes induced by kasugamycin: a look into ancestral times of protein synthesis? Mol. Cell 33(2):227-36
53. Kieft JS. 2008. Viral IRES RNA structures and ribosome interactions. Trends Biochem. Sci. 33(6):274-83
54. Kirn-Safran CB, Oristian DS, Focht RJ, Parker SG, Vivian JL, Carson DD. 2007. Global growth deficiencies in mice lacking the ribosomal protein HIP/RPL29. Dev. Dyn. 236(2):447-60
55. Kladwang W, VanLang CC, Cordero P, Das R. 2011. A two-dimensional mutate-and-map strategy for noncoding RNA structure. Nat. Chem. 3(12):954-62
56. Komar AA, Hatzoglou M. 2011. Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 10(2):229-40
57. Kondrashov N, Pusic A, Stumpf CR, Shimizu K, Hsieh AC, et al. 2011. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145(3):383-97
58. Kozak M. 1987. An analysis of 5-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15:8125-48
59. Krieg J, Hofsteenge J, Thomas G. 1988. Identification of the 40 S ribosomal protein S6 phosphorylation sites induced by cycloheximide. J. Biol. Chem. 263(23):11473-77
60. Kullmann M, Gopfert U, Siewe B, Hengst L. 2002. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5-UTR. Genes Dev. 16(23):3087-99
61. Kurland CG, Voynow P, Hardy SJ, Randall L, Lutter L. 1969. Physical and functional heterogeneity of E. coli ribosomes. Cold Spring Harb. Symp. Quant. Biol. 34:17-24
62. LaiK, AmsterdamA,Farrington S,Bronson RT,HopkinsN,Lees JA. 2009. Manyribosomal proteinmutations are associated with growth impairment and tumor predisposition in zebrafish. Dev. Dyn. 238:76-85
63. Lambertsson A. 1998. The Minute genes in Drosophila and their molecular functions. Adv. Genet. 38:69-134
64. Lee AS, Burdeinick-Kerr R, Whelan SP. 2013. A ribosome-specialized translation initiation pathway is required for cap-dependent translation of vesicular stomatitis virus mRNAs. PNAS 110(1):324-29
65. Levy S, Avni D, HariharanN, Perry RP,Meyuhas O. 1991. Oligopyrimidine tract at the 5- end of mammalian ribosomal protein mRNAs is required for their translational control. PNAS 88:3319-23
66. Liliental J, Chang DD. 1998. Rack1, a receptor for activated protein kinaseC, interactswith integrinβsubunit. J. Biol. Chem. 273(4):2379-83
67. Lincoln AJ, Monczak Y, Williams SC, Johnson PF. 1998. Inhibition of CCAAT/enhancer-binding protein α and βtranslation by upstream open reading frames. J. Biol. Chem. 273:9552-60
68. Link AJ, Eng J, Schieltz DM, Carmack E, Mize GJ, et al. 1999. Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17(7):676-82
69. Liu J, Xu Y, Stoleru D, Salic A. 2012. Imaging protein synthesis in cells and tissues with an alkyne analog of puromycin. PNAS 109(2):413-18
70. Lopes AM, Miguel RN, Sargent CA, Ellis PJ, Amorim A, Affara NA. 2010. The human RPS4 paralogue on Yq11.223 encodes a structurally conserved ribosomal protein and is preferentially expressed during spermatogenesis. BMC Mol. Biol. 11:33
71. Majzoub K, Hafirassou ML, Meignin C, Goto A, Marzi S, et al. 2014. RACK1 controls IRES-mediated translation of viruses. Cell 159(5):1086-95
72. Martin I, Kim JW, Lee BD, Kang HC, Xu JC, et al. 2014. Ribosomal protein s15 phosphorylation mediates LRRK2 neurodegeneration in Parkinson's disease. Cell 157(2):472-85
73. Marygold SJ, Coelho CM, Leevers SJ. 2005. Genetic analysis of RpL38 and RpL5, two Minute genes located in the centric heterochromatin of chromosome 2 of Drosophila melanogaster. Genetics 169(2):683-95
74. Marygold SJ, Roote J, Reuter G, Lambertsson A, AshburnerM, et al. 2007. The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol. 8:R216
75. Mazumder B, Sampath P, SeshadriV,Maitra RK,DiCorleto PE, Fox PL. 2003. Regulated release of L13a from the 60S ribosomal subunit as a mechanism of transcript-specific translational control. Cell 115(2):187-98
76. McGowan KA, Li JZ, Park CY, Beaudry V, Tabor HK, et al. 2008. Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat. Genet. 40(8):963-70
77. Melo JA, Ruvkun G. 2012. Inactivation of conserved C. elegans genes engages pathogen-and xenobioticassociated defenses. Cell 149(2):452-66
78. Milne AN, Mak WW, Wong JT. 1975. Variation of ribosomal proteins with bacterial growth rate. J. Bacteriol. 122(1):89-92
79. Miskimins WK, Wang G, Hawkinson M, Miskimins R. 2001. Control of cyclin-dependent kinase inhibitor p27 expression by cap-independent translation. Mol. Cell. Biol. 21(15):4960-67
80. Moore PB, Traut RR, NollerH, Pearson P, DeliusH. 1968. Ribosomal proteins of Escherichia coli. II. Proteins from the 30 s subunit. J. Mol. Biol. 31(3):441-61
81. Moroz LL, Edwards JR, Puthanveettil S V, Kohn AB, Ha T, et al. 2006. Neuronal transcriptome of Aplysia: neuronal compartments and circuitry. Cell 127(7):1453-67
82. Morris DR, Geballe AP. 2000. Upstream open reading frames as regulators of mRNA translation. Mol. Cell. Biol. 20(23):8635-42
83. Noller HF, Hoffarth V, Zimniak L. 1992. Unusual resistance of peptidyl transferase to protein extraction procedures. Science 256:1416-19
84. Odintsova TI, Muller EC, Ivanov AV, Egorov TA, Bienert R, 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(3):249-58
85. Palade GE. 1955. A small particulate component of the cytoplasm. J. Biophys. Biochem. Cytol. 1(1):59-68
86. Panic L, Tamarut S, Sticker-Jantscheff M, Barkic M, Solter D, et al. 2006. Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation. Mol. Cell. Biol. 26(23):8880-91
87. Parenteau J, Durand M, Morin G, Gagnon J, Lucier JF, et al. 2011. Introns within ribosomal protein genes regulate the production and function of yeast ribosomes. Cell 147(2):320-31
88. Pelletier J, Sonenberg N. 1988. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334:320-25
89. PertzOC, Wang Y, Yang F, Wang W, Gay LJ, et al. 2008. Spatial mapping of the neurite and soma proteomes reveals a functional Cdc42/Rac regulatory network. PNAS 105(6):1931-36
90. Perucho L, Artero-Castro A, Guerrero S, Ramon Y Cajal S, LLeonartME, Wang ZQ. 2014. RPLP1, a crucial ribosomal protein for embryonic development of the nervous system. PLOS ONE 9(6):e99956
91. Ramagopal S. 1991. Covalent modifications of ribosomal proteins in growing and aggregation-competent Dictyostelium discoideum: phosphorylation and methylation. Biochem. Cell Biol. 69(4):263-68
92. Ramji DP, Foka P. 2002. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem. J. 365:561-75
93. Ray PS, Grover R, Das S. 2006. Two internal ribosome entry sites mediate the translation of p53 isoforms. EMBO Rep. 7(4):404-10
94. Reschke M, Clohessy JG, Seitzer N, Goldstein DP, Breitkopf SB, et al. 2013. Characterization and analysis of the composition and dynamics of the mammalian riboproteome. Cell Rep. 4(6):1276-87
95. Rouskin S, Zubradt M, Washietl S, Kellis M, Weissman JS. 2014. Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo. Nature 505(7485):701-5
96. Ruvinsky I, Sharon N, Lerer T, Cohen H, Stolovich-Rain M, et al. 2005. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev. 19(18):2199-211
97. Sampath P, Pritchard DK, Pabon L, Reinecke H, Schwartz SM, et al. 2008. A hierarchical network controls protein translation during murine embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2(5):448-60
98. Schaeffer C, Bardoni B, Mandel JL, Ehresmann B, Ehresmann C, Moine H. 2001. The Fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J. 20(17):4803-13
99. Signer RA,Magee JA, Salic A, Morrison SJ. 2014. Haematopoietic stem cells require a highly regulated protein synthesis rate. Nature 509(7498):49-54
100. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136(4):731-45
101. Spence J, Gali RR, Dittmar G, Sherman F, KarinM, Finley D. 2000. Cell cycle-regulated modification of the ribosome by a variant multiubiquitin chain. Cell 102(1):67-76
102. Spitale RC, Flynn RA, Zhang QC, Crisalli P, Lee B, et al. 2015. Structural imprints in vivo decode RNA regulatory mechanisms. Nature 519(7544):486-90
103. Stewart MJ, Denell R. 1993. Mutations in the Drosophila gene encoding ribosomal protein S6 cause tissue overgrowth. Mol. Cell. Biol. 13:2524-35
104. Sugihara Y, Honda H, Iida T, Morinaga T, Hino S, 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(3):1351-66
105. SuttonMA, Schuman EM. 2006. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127(1):49-58
106. Tcherkezian J, Brittis PA, Thomas F, Roux PP, Flanagan JG. 2010. Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 141(4):632-44
107. Terzian T, Dumble M, Arbab F, Thaller C, Donehower LA, et al. 2011. Rpl27a mutation in the sooty foot ataxia mouse phenocopies high p53 mouse models. J. Pathol. 224(4):540-52
108. Tor ok I, Herrmann-Horle D, Kiss I, Tick G, Speer G, et al. 1999. Down-regulation of RpS21, a putative translation initiation factor interacting with P40, produces viable Minute imagos and larval lethality with overgrown hematopoietic organs and imaginal discs. Mol. Cell. Biol. 19:2308-21
109. Traut RR, Delius H, Ahmad-Zadeh C, Bickle TA, Pearson P, Tissieres A. 1969. Ribosomal proteins of E. coli: stoichiometry and implications for ribosome structure. Cold Spring Harb. Symp. Quant. Biol. 34:25-38
110. Truitt ML, Conn CS, Shi Z, Pang X, Tokuyasu T, et al. 2015. Differential requirements for eIF4E dose in normal development and cancer. Cell 162(1):59-71
111. Uechi T, Nakajima Y, Nakao A, Torihara H, Chakraborty A, et al. 2006. Ribosomal protein gene knockdown causes developmental defects in zebrafish. PLOS ONE 1:e37
112. Volarevic S, Stewart MJ, Ledermann B, Zilberman F,Terracciano L, et al. 2000. Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science 288(5473):2045-47
113. VoltaV, Beugnet A, Gallo S, MagriL, Brina D, et al. 2013.RACK1depletion in a mousemodel causes lethality, pigmentation deficits and reduction in protein synthesis efficiency. Cell. Mol. Life Sci. 70:1439-50
114. Warner JR,McIntosh KB. 2009. How common are extraribosomal functions of ribosomal proteins? Mol. Cell 34(1):3-11
115. Watkins-Chow DE, Cooke J, Pidsley R, Edwards A, Slotkin R, et al. 2013. Mutation of the Diamond-Blackfan anemia gene Rps7 in mouse results in morphological and neuroanatomical phenotypes. PLOS Genet. 9(1):e1003094
116. Watson KL,KonradKD, Woods DF, Bryant PJ. 1992. Drosophila homolog of the human S6 ribosomal protein is required for tumor suppression in the hematopoietic system. PNAS 89:11302-6
117. Weber HJ. 1972. Stoichiometric measurements of 30S and 50S ribosomal proteins from Escherichia coli. Mol. Gen. Genet. 119(3):233-48
118. Wethmar K, Begay V, Smink JJ, Zaragoza K, Wiesenthal V, et al. 2010. C/EBPβ-uORF mice-A genetic model for uORF-mediated translational control in mammals. Genes Dev. 24:15-20
119. WhittleCA, Krochko JE. 2009. Transcript profiling provides evidence of functional divergence and expression networks among ribosomal protein gene paralogs in Brassica napus. Plant Cell 21(8):2203-19
120. Wilkinson KA, Merino EJ, Weeks KM. 2006. Selective 2-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat. Protoc. 1(3):1610-16
121. Xue S, Barna M. 2012. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell Biol. 13(6):355-69
122. Xue S, Tian S, Fujii K, Kladwang W, Das R, Barna M. 2015. RNA regulons in Hox 5- UTRs confer ribosome specificity to gene regulation. Nature 517(7532):33-38
123. Yang DQ, Halaby MJ, Zhang Y. 2006. The identification of an internal ribosomal entry site in the 5-untranslated region of p53 mRNA provides a novel mechanism for the regulation of its translation following DNA damage. Oncogene 25(33):4613-19
124. Yoon A, Peng G, Brandenburger Y, Zollo O, Xu W, et al. 2006. Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science 312(5775):902-6
125. Yu Y, Ji H, Doudna JA, Leary JA. 2005. Mass spectrometric analysis of the human 40S ribosomal subunit: native and HCV IRES-bound complexes. Protein Sci. 14(6):1438-46
126. Zeidan Q, Wang Z, De Maio A, Hart GW. 2010. O-GlcNAc cycling enzymes associate with the translational machinery and modify core ribosomal proteins. Mol. Biol. Cell 21(12):1922-36
127. Zhang Q, Shalaby NA, Buszczak M. 2014. Changes in rRNA transcription influence proliferation and cell fate within a stem cell lineage. Science 343(6168):298-301
128. Zhang Y, Duc ACE, Rao S, Sun XL, Bilbee AN, et al. 2013. Control of hematopoietic stem cell emergence by antagonistic functions of ribosomal protein paralogs. Dev. Cell 24(4):411-25
129. Zhou C, Zang D, Jin Y, Wu H, Liu Z, et al. 2011. Mutation in ribosomal protein L21 underlies hereditary hypotrichosis simplex. Hum. Mutat. 32:710-14