1932

Abstract

A central question in cell and developmental biology is how the information encoded in the genome is differentially interpreted to generate a diverse array of cell types. A growing body of research on posttranscriptional gene regulation is revealing that both global protein synthesis rates and the translation of specific mRNAs are highly specialized in different cell types. How this exquisite translational regulation is achieved is the focus of this review. Two levels of regulation are discussed: the translation machinery and -acting elements within mRNAs. Recent evidence shows that the ribosome itself directs how the genome is translated in time and space and reveals surprising functional specificity in individual components of the core translation machinery. We are also just beginning to appreciate the rich regulatory information embedded in the untranslated regions of mRNAs, which direct the selective translation of transcripts. These hidden RNA regulons may interface with a myriad of RNA-binding proteins and specialized translation machinery to provide an additional layer of regulation to how transcripts are spatiotemporally expressed. Understanding this largely unexplored world of translational codes hardwired in the core translation machinery is an exciting new research frontier fundamental to our understanding of gene regulation, organismal development, and evolution.

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2015-11-13
2024-06-12
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Literature Cited

  1. Alberts B. 1998. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92:3291–94 [Google Scholar]
  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. 37:2157–75 [Google Scholar]
  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. 2:5E139 [Google Scholar]
  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 26:6759–72 [Google Scholar]
  5. Barbosa C, Peixeiro I, Romao L. 2013. Gene expression regulation by upstream open reading frames and human disease. PLOS Genet. 9:8e1003529 [Google Scholar]
  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. 29:102489–504 [Google Scholar]
  7. Barlow JL, Drynan LF, Hewett DR, Holmes LR, Lorenzo-Abalde S. et al. 2010. A p53-dependent mechanism underlies macrocytic anemia in a mouse model of human 5q- syndrome. Nat. Med. 16:159–66 [Google Scholar]
  8. Baum S, Bittins M, Frey S, Seedorf M. 2004. Asc1p, a WD40-domain containing adaptor protein, is required for the interaction of the RNA-binding protein Scp160p with polysomes. Biochem. J. 380:Pt. 3823–30 [Google Scholar]
  9. Bellodi C, Kopmar N, Ruggero D. 2010. Deregulation of oncogene-induced senescence and p53 translational control in X-linked dyskeratosis congenita. EMBO J. 29:111865–76 [Google Scholar]
  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. 3:51493–502 [Google Scholar]
  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. 248:134862–64 [Google Scholar]
  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 340:6135976–78 [Google Scholar]
  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 [Google Scholar]
  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 335:6068552–57 [Google Scholar]
  15. Bridges CB, Morgan TH. 1923. The Third-Chromosome Group of Mutant Characters of Drosophila Melanogaster. Baltimore, MD: Carnegie Inst. [Google Scholar]
  16. Brown V, Jin P, Ceman S, Darnell JC, O'Donnell WT. et al. 2001. Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in Fragile X syndrome. Cell 107:4477–87 [Google Scholar]
  17. Budde A, Grummt I. 1999. p53 represses ribosomal gene transcription. Oncogene 18:41119–24 [Google Scholar]
  18. Buszczak M, Signer RAJ, Morrison SJ. 2014. Cellular differences in protein synthesis regulate tissue homeostasis. Cell 159:2242–51 [Google Scholar]
  19. Byrgazov K, Vesper O, Moll I. 2013. Ribosome heterogeneity: another level of complexity in bacterial translation regulation. Curr. Opin. Microbiol. 16:2133–39 [Google Scholar]
  20. Calkhoven CF, Muller C, Leutz A. 2000. Translational control of C/EBPα and C/EBPβ isoform expression. Genes Dev. 14:1920–32 [Google Scholar]
  21. Calvo SE, Pagliarini DJ, Mootha VK. 2009. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. PNAS 106:187507–12 [Google Scholar]
  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 [Google Scholar]
  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 426:6966579–84 [Google Scholar]
  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 54:3407–17 [Google Scholar]
  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 151:4765–77 [Google Scholar]
  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 5:4597–605 [Google Scholar]
  27. Coyle SM, Gilbert W V, Doudna JA. 2009. Direct link between RACK1 function and localization at the ribosome in vivo. Mol. Cell. Biol. 29:61626–34 [Google Scholar]
  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 107:4489–99 [Google Scholar]
  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 146:2247–61 [Google Scholar]
  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. 45:2186–90 [Google Scholar]
  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. 147:1128–42 [Google Scholar]
  32. Deusser E. 1972. Heterogeneity of ribosomal populations in Escherichia coli cells grown in different media. Mol. Gen. Genet. 119:3249–58 [Google Scholar]
  33. Deusser E, Wittmann HG. 1972. Ribosomal proteins: variation of the protein composition in Escherichia coli ribosomes as function of growth rate. Nature 238:5362269–70 [Google Scholar]
  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 505:7485696–700 [Google Scholar]
  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. 153:41878–94 [Google Scholar]
  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. 20:101294–307 [Google Scholar]
  37. Frank J. 2000. The ribosome—a macromolecular machine par excellence. Chem. Biol. 7:6R133–41 [Google Scholar]
  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 [3H]phenylalanine. Biochem. J. 192:2719–23 [Google Scholar]
  39. Ghosh A, Rideout EJ, Grewal SS. 2014. TIF-IA–dependent regulation of ribosome synthesis in Drosophila muscle is required to maintain systemic insulin signaling and larval growth. PLOS Genet. 10:10e1004750 [Google Scholar]
  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 93:115578–83 [Google Scholar]
  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 [Google Scholar]
  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 95:1911089–94 [Google Scholar]
  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 238:4829933–37 [Google Scholar]
  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. 1:3190–92 [Google Scholar]
  45. Holcik M, Sonenberg N. 2005. Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol. 6:4318–27 [Google Scholar]
  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 [Google Scholar]
  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 485:739655–61 [Google Scholar]
  48. Iacono M, Mignone F, Pesole G. 2005. uAUG and uORFs in human and rodent 5′ untranslated mRNAs. Gene 349:97–105 [Google Scholar]
  49. Ingolia NT, Lareau LF, Weissman JS. 2011. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147:4789–802 [Google Scholar]
  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. 62:82636–43 [Google Scholar]
  51. Jannot G, 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. 12:6581–86 [Google Scholar]
  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 33:2227–36 [Google Scholar]
  53. Kieft JS. 2008. Viral IRES RNA structures and ribosome interactions. Trends Biochem. Sci. 33:6274–83 [Google Scholar]
  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. 236:2447–60 [Google Scholar]
  55. Kladwang W, VanLang CC, Cordero P, Das R. 2011. A two-dimensional mutate-and-map strategy for non-coding RNA structure. Nat. Chem. 3:12954–62 [Google Scholar]
  56. Komar AA, Hatzoglou M. 2011. Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 10:2229–40 [Google Scholar]
  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 145:3383–97 [Google Scholar]
  58. Kozak M. 1987. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15:8125–48 [Google Scholar]
  59. Krieg J, Hofsteenge J, Thomas G. 1988. Identification of the 40 S ribosomal protein S6 phosphorylation sites induced by cycloheximide. J. Biol. Chem. 263:2311473–77 [Google Scholar]
  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. 16:233087–99 [Google Scholar]
  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 [Google Scholar]
  62. Lai K, Amsterdam A, Farrington S, Bronson RT, Hopkins N, Lees JA. 2009. Many ribosomal protein mutations are associated with growth impairment and tumor predisposition in zebrafish. Dev. Dyn. 238:76–85 [Google Scholar]
  63. Lambertsson A. 1998. The Minute genes in Drosophila and their molecular functions. Adv. Genet. 38:69–134 [Google Scholar]
  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 110:1324–29 [Google Scholar]
  65. Levy S, Avni D, Hariharan N, 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 [Google Scholar]
  66. Liliental J, Chang DD. 1998. Rack1, a receptor for activated protein kinase C, interacts with integrin β subunit. J. Biol. Chem. 273:42379–83 [Google Scholar]
  67. Lincoln AJ, Monczak Y, Williams SC, Johnson PF. 1998. Inhibition of CCAAT/enhancer-binding protein α and β translation by upstream open reading frames. J. Biol. Chem. 273:9552–60 [Google Scholar]
  68. Link AJ, Eng J, Schieltz DM, Carmack E, Mize GJ. et al. 1999. Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17:7676–82 [Google Scholar]
  69. Liu J, Xu Y, Stoleru D, Salic A. 2012. Imaging protein synthesis in cells and tissues with an alkyne analog of puromycin. PNAS 109:2413–18 [Google Scholar]
  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 [Google Scholar]
  71. Majzoub K, Hafirassou ML, Meignin C, Goto A, Marzi S. et al. 2014. RACK1 controls IRES-mediated translation of viruses. Cell 159:51086–95 [Google Scholar]
  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 157:2472–85 [Google Scholar]
  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 169:2683–95 [Google Scholar]
  74. Marygold SJ, Roote J, Reuter G, Lambertsson A, Ashburner M. et al. 2007. The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome Biol. 8:R216 [Google Scholar]
  75. Mazumder B, Sampath P, Seshadri V, 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 115:2187–98 [Google Scholar]
  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. 40:8963–70 [Google Scholar]
  77. Melo JA, Ruvkun G. 2012. Inactivation of conserved C. elegans genes engages pathogen- and xenobiotic-associated defenses. Cell 149:2452–66 [Google Scholar]
  78. Milne AN, Mak WW, Wong JT. 1975. Variation of ribosomal proteins with bacterial growth rate. J. Bacteriol. 122:189–92 [Google Scholar]
  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. 21:154960–67 [Google Scholar]
  80. Moore PB, Traut RR, Noller H, Pearson P, Delius H. 1968. Ribosomal proteins of Escherichia coli. II. Proteins from the 30 s subunit. J. Mol. Biol. 31:3441–61 [Google Scholar]
  81. Moroz LL, Edwards JR, Puthanveettil S V, Kohn AB, Ha T. et al. 2006. Neuronal transcriptome of Aplysia: neuronal compartments and circuitry. Cell 127:71453–67 [Google Scholar]
  82. Morris DR, Geballe AP. 2000. Upstream open reading frames as regulators of mRNA translation. Mol. Cell. Biol. 20:238635–42 [Google Scholar]
  83. Noller HF, Hoffarth V, Zimniak L. 1992. Unusual resistance of peptidyl transferase to protein extraction procedures. Science 256:1416–19 [Google Scholar]
  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. 22:3249–58 [Google Scholar]
  85. Palade GE. 1955. A small particulate component of the cytoplasm. J. Biophys. Biochem. Cytol. 1:159–68 [Google Scholar]
  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. 26:238880–91 [Google Scholar]
  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 147:2320–31 [Google Scholar]
  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 [Google Scholar]
  89. Pertz OC, 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 105:61931–36 [Google Scholar]
  90. Perucho L, Artero-Castro A, Guerrero S, Ramón Y, Cajal S, LLeonart ME, Wang ZQ. 2014. RPLP1, a crucial ribosomal protein for embryonic development of the nervous system. PLOS ONE 9:6e99956 [Google Scholar]
  91. Ramagopal S. 1991. Covalent modifications of ribosomal proteins in growing and aggregation-competent Dictyostelium discoideum: phosphorylation and methylation. Biochem. Cell Biol. 69:4263–68 [Google Scholar]
  92. Ramji DP, Foka P. 2002. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem. J. 365:561–75 [Google Scholar]
  93. Ray PS, Grover R, Das S. 2006. Two internal ribosome entry sites mediate the translation of p53 isoforms. EMBO Rep. 7:4404–10 [Google Scholar]
  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. 4:61276–87 [Google Scholar]
  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 505:7485701–5 [Google Scholar]
  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. 19:182199–211 [Google Scholar]
  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 2:5448–60 [Google Scholar]
  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. 20:174803–13 [Google Scholar]
  99. Signer RA, Magee JA, Salic A, Morrison SJ. 2014. Haematopoietic stem cells require a highly regulated protein synthesis rate. Nature 509:749849–54 [Google Scholar]
  100. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136:4731–45 [Google Scholar]
  101. Spence J, Gali RR, Dittmar G, Sherman F, Karin M, Finley D. 2000. Cell cycle–regulated modification of the ribosome by a variant multiubiquitin chain. Cell 102:167–76 [Google Scholar]
  102. Spitale RC, Flynn RA, Zhang QC, Crisalli P, Lee B. et al. 2015. Structural imprints in vivo decode RNA regulatory mechanisms. Nature 519:7544486–90 [Google Scholar]
  103. Stewart MJ, Denell R. 1993. Mutations in the Drosophila gene encoding ribosomal protein S6 cause tissue overgrowth. Mol. Cell. Biol. 13:2524–35 [Google Scholar]
  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. 9:31351–66 [Google Scholar]
  105. Sutton MA, Schuman EM. 2006. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127:149–58 [Google Scholar]
  106. Tcherkezian J, Brittis PA, Thomas F, Roux PP, Flanagan JG. 2010. Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 141:4632–44 [Google Scholar]
  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. 224:4540–52 [Google Scholar]
  108. Török 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 [Google Scholar]
  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 [Google Scholar]
  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 162:159–71 [Google Scholar]
  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 [Google Scholar]
  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 288:54732045–47 [Google Scholar]
  113. Volta V, Beugnet A, Gallo S, Magri L, Brina D. et al. 2013. RACK1 depletion in a mouse model causes lethality, pigmentation deficits and reduction in protein synthesis efficiency. Cell. Mol. Life Sci. 70:1439–50 [Google Scholar]
  114. Warner JR, McIntosh KB. 2009. How common are extraribosomal functions of ribosomal proteins?. Mol. Cell 34:13–11 [Google Scholar]
  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. 9:1e1003094 [Google Scholar]
  116. Watson KL, Konrad KD, 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 [Google Scholar]
  117. Weber HJ. 1972. Stoichiometric measurements of 30S and 50S ribosomal proteins from Escherichia coli. Mol. Gen. Genet. 119:3233–48 [Google Scholar]
  118. Wethmar K, Bégay V, Smink JJ, Zaragoza K, Wiesenthal V. et al. 2010. C/EBPβΔuORF mice—a genetic model for uORF-mediated translational control in mammals. Genes Dev. 24:15–20 [Google Scholar]
  119. Whittle CA, Krochko JE. 2009. Transcript profiling provides evidence of functional divergence and expression networks among ribosomal protein gene paralogs in Brassica napus. Plant Cell 21:82203–19 [Google Scholar]
  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. 1:31610–16 [Google Scholar]
  121. Xue S, Barna M. 2012. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell Biol. 13:6355–69 [Google Scholar]
  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 517:753233–38 [Google Scholar]
  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 25:334613–19 [Google Scholar]
  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 312:5775902–6 [Google Scholar]
  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. 14:61438–46 [Google Scholar]
  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 21:121922–36 [Google Scholar]
  127. Zhang Q, Shalaby NA, Buszczak M. 2014. Changes in rRNA transcription influence proliferation and cell fate within a stem cell lineage. Science 343:6168298–301 [Google Scholar]
  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 24:4411–25 [Google Scholar]
  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 [Google Scholar]
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