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Article

Saccharomyces cerevisiae Ribosomal Protein L26 Is Not Essential for Ribosome Assembly and Function

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Pages 3228-3241 | Received 25 Apr 2012, Accepted 01 Jun 2012, Published online: 20 Mar 2023

REFERENCES

  • Adams CC, et al. 2002. Saccharomyces cerevisiae nucleolar protein Nop7p is necessary for biogenesis of 60S ribosomal subunits. RNA 8:150–165.
  • Albanèse V, Yam AY, Baughman J, Parnot C, Frydman J. 2006. Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells. Cell 124:75–88.
  • Ausubel FM, et al. 1994. Saccharomyces cerevisiae, p 13.0.1–13.14.17. Current protocols in molecular biology, vol 2. John Wiley & Sons, Inc., New York, NY.
  • Babiano R, de la Cruz J. 2010. Ribosomal protein L35 is required for 27SB pre-rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Res. 38:5177–5192.
  • Baronas-Lowell DM, Warner JR. 1990. Ribosomal protein L30 is dispensable in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 10:5235–5243.
  • Belk JP, He F, Jacobson A. 1999. Overexpression of truncated Nmd3p inhibits protein synthesis in yeast. RNA 5:1055–1070.
  • Ben-Shem A, et al. 2011. The structure of the eukaryotic ribosome at 3.0 Å resolution. Science 334:1524–1529.
  • Briones E, Briones C, Remacha M, Ballesta JPG. 1998. The GTPase center protein L12 is required for correct ribosomal stalk assembly but not for Saccharomyces cerevisiae viability. J. Biol. Chem. 273:31956–31961.
  • Bubunenko M, et al. 2006. 30S ribosomal subunits can be assembled in vivo without primary binding ribosomal protein S15. RNA 12:1229–1239.
  • Cabezón T, Herzog A, Petre J, Yaguchi M, Bollen A. 1977. Ribosomal assembly deficiency in an Escherichia coli thermosensitive mutant having an altered L24 ribosomal protein. J. Mol. Biol. 116:361–374.
  • Cannone JJ, et al. 2002. The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3:2. https://doi.org/10.1186/1471-2105-3-2.
  • Cigan AM, Pabich EK, Donahue TF. 1988. Mutational analysis of the HIS4 translational initiator region in Saccharomyces cerevisiae. Mol. Cell. Biol. 8:2964–2975.
  • Connolly K, Culver G. 2009. Deconstructing ribosome construction. Trends Biochem. Sci. 34:256–263.
  • Dabbs ER. 1982. A spontaneous mutant of Escherichia coli with protein L24 lacking from the ribosome. Mol. Gen. Genet. 187:453–458.
  • DeLabre ML, Kessl J, Karamanou S, Trumpower BL. 2002. RPL29 codes for a non-essential protein of the 60S ribosomal subunit in Saccharomyces cerevisiae and exhibits synthetic lethality with mutations in genes for proteins required for subunit coupling. Biochim. Biophys. Acta 1574:255–261.
  • de la Cruz J, Kressler D, Linder P. 2004. Ribosomal subunit assembly, p 258–285. InOlson MOJ (ed), The nucleolus. Landes Bioscience, Austin, TX.
  • de Narvaez CC, Schaup HW. 1979. In vivo transcriptionally coupled assembly of Escherichia coli ribosomal subunits. J. Mol. Biol. 134:1–22.
  • Deshmukh M, et al. 1995. Multiple regions of yeast ribosomal protein L1 are important for its interaction with 5 S rRNA and assembly into ribosomes. J. Biol. Chem. 270:30148–30156.
  • Deshmukh M, Tsay Paulovich Y-FAG, Woolford JLJr. 1993. Yeast ribosomal protein L1 is required for the stability of newly synthesized 5S rRNA and the assembly of 60S ribosomal subunits. Mol. Cell. Biol. 13:2835–2845.
  • Dez C, et al. 2004. Npa1p, a component of very early pre-60S ribosomal particles, associates with a subset of small nucleolar RNPs required for peptidyl transferase center modification. Mol. Cell. Biol. 24:6324–6337.
  • Dez C, Tollervey D. 2004. Ribosome synthesis meets the cell cycle. Curr. Opin. Microbiol. 7:631–637.
  • Dinman JD, Icho T, Wickner RB. 1991. A −1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein. Proc. Natl. Acad. Sci. U. S. A. 88:174–178.
  • Dinman JD, Wickner RB. 1992. Ribosomal frameshifting efficiency and gag/gag-pol ratio are critical for yeast M1 double-stranded RNA virus propagation. J. Virol. 66:3669–3676.
  • Dresios J, Derkatch IL, Liebman SW, Synetos D. 2000. Yeast ribosomal protein L24 affects the kinetics of protein synthesis and ribosomal protein L39 improves translational accuracy, while mutants lacking both remain viable. Biochemistry 39:7236–7244.
  • Dunkle JA, Xiong L, Mankin AS, Cate JH. 2010. Structures of the Escherichia coli ribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action. Proc. Natl. Acad. Sci. U. S. A. 107:17152–17157.
  • Dutca LM, Gallagher JE, Baserga SJ. 2011. The initial U3 snoRNA:pre-rRNA base pairing interaction required for pre-18S rRNA folding revealed by in vivo chemical probing. Nucleic Acids Res. 39:5164–5180.
  • Egebjerg J, Leffers H, Christensen A, Andersen H, Garrett RA. 1987. Structure and accessibility of domain I of Escherichia coli 23 S RNA in free RNA, in the L24-RNA complex and in 50 S subunits. Implications for ribosomal assembly. J. Mol. Biol. 196:125–136.
  • Emery B, de la Cruz J, Rocak S, Deloche O, Linder P. 2004. Has1p, a member of the DEAD-box family, is required for 40S ribosomal subunit biogenesis in Saccharomyces cerevisiae. Mol. Microbiol. 52:141–158.
  • Ferreira-Cerca S, Pöll G, Gleizes PE, Tschochner H, Milkereit P. 2005. Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol. Cell 20:263–275.
  • Ferreira-Cerca S, et al. 2007. Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol. Cell 28:446–457.
  • Fromont-Racine M, Senger B, Saveanu C, Fasiolo F. 2003. Ribosome assembly in eukaryotes. Gene 313:17–42.
  • Fuentes JL, Datta K, Sullivan SM, Walker A, Maddock JR. 2007. In vivo functional characterization of the Saccharomyces cerevisiae 60S biogenesis GTPase Nog1. Mol. Genet. Genomics 278:105–123.
  • Gadal O, et al. 2001. A nuclear AAA-type ATPase (Rix7p) is required for biogenesis and nuclear export of 60S ribosomal subunits. EMBO J. 20:3695–3704.
  • Gadal O, et al. 2001. Nuclear export of 60S ribosomal subunit depends on Xpo1p and requires a nuclear export sequence-containing factor, Nmd3p, that associates with the large subunit protein Rpl10p. Mol. Cell. Biol. 21:3405–3415.
  • Giaever G, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387–391.
  • Grallath S, et al. 2006. L25 functions as a conserved ribosomal docking site shared by nascent chain-associated complex and signal-recognition particle. EMBO Rep. 7:78–84.
  • Grandi P, et al. 2002. 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol. Cell 10:105–115.
  • Granneman S, Petfalski E, Tollervey D. 2011. A cluster of ribosome synthesis factors regulate pre-rRNA folding and 5.8S rRNA maturation by the Rat1 exonuclease. EMBO J. 30:4006–4019.
  • Harnpicharnchai P, et al. 2001. Composition and functional characterization of yeast 66S ribosome assembly intermediates. Mol. Cell 8:505–515.
  • Held WA, Mizushima S, Nomura M. 1973. Reconstitution of Escherichia coli 30 S ribosomal subunits from purified molecular components. J. Biol. Chem. 248:5720–5730.
  • Herold M, Nierhaus KH. 1987. Incorporation of six additional proteins to complete the assembly map of the 50 S subunit from Escherichia coli ribosomes. J. Biol. Chem. 262:8826–8833.
  • Herold M, Nowotny V, Dabbs ER, Nierhaus KH. 1986. Assembly analysis of ribosomes from a mutant lacking the assembly-initiator protein L24: lack of L24 induces temperature sensitivity. Mol. Gen. Genet. 203:281–287.
  • Ho JH-N, Kallstrom G, Johnson AW. 2000. Nmd3p is a Crm1p-dependent adapter protein for nuclear export of the large ribosomal subunit. J. Cell Biol. 151:1057–1066.
  • Hurt E, et al. 1999. A novel in vivo assay reveals inhibition of ribosomal nuclear export in Ran-cycle and nucleoporin mutants. J. Cell Biol. 144:389–401.
  • Jakovljevic J, et al. Ribosomal proteins L7 and L8 function in concert with six A3 assembly factors to propagate assembly of domain I of 25S rRNA in yeast 60S ribosomal subunits. RNA, in press.
  • Kaczanowska M, Ryden-Aulin M. 2007. Ribosome biogenesis and the translation process in Escherichia coli. Microbiol. Mol. Biol. Rev. 71:477–494.
  • Kaiser C, Michaelis S, Mitchell A. 1994. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
  • Kemmler S, Occhipinti L, Veisu M, Panse VG. 2009. Yvh1 is required for a late maturation step in the 60S biogenesis pathway. J. Cell Biol. 186:863–880.
  • Klein DJ, Moore PB, Steitz TA. 2004. The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J. Mol. Biol. 340:141–177.
  • Kosugi S, Hasebe M, Tomita M, Yanagawa H. 2009. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl. Acad. Sci. U. S. A. 106:10171–10176.
  • Kramer G, Boehringer D, Ban N, Bukau B. 2009. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16:589–597.
  • Kressler D, de la Cruz J, Rojo M, Linder P. 1998. Dbp6p is an essential putative ATP-dependent RNA helicase required for 60S-ribosomal-subunit assembly in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:1855–1865.
  • Kressler D, Hurt E, Bassler J. 2010. Driving ribosome assembly. Biochim. Biophys. Acta 1803:673–683.
  • Kruiswijk T, Planta RJ, Krop JM. 1978. The course of the assembly of ribosomal subunits in yeast. Biochim. Biophys. Acta 517:378–389.
  • Lastick SM. 1980. The assembly of ribosomes in HeLa cell nucleoli. Eur. J. Biochem. 113:175–182.
  • Lebreton A, et al. 2008. 60S ribosomal subunit assembly dynamics defined by semi-quantitative mass spectrometry of purified complexes. Nucleic Acids Res. 36:4988–4999.
  • Lebreton A, Saveanu C, Decourty L, Jacquier A, Fromont-Racine M. 2006. Nsa2, an unstable, conserved factor required for the maturation of 27SB pre-rRNAs. J. Biol. Chem. 281:27099–27108.
  • Lecompte O, Ripp R, Thierry JC, Moras D, Poch O. 2002. Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acids Res. 30:5382–5390.
  • Lee B, Udagawa T, Singh CR, Asano K. 2007. Yeast phenotypic assays on translational control. Methods Enzymol. 429:105–137.
  • Lo KY, et al. 2010. Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit. Mol. Cell 39:196–208.
  • Longtine MS, et al. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953–961.
  • Mangiarotti G, Chiaberge S. 1997. Reconstitution of functional eukaryotic ribosomes from Dictyostelium discoideum ribosomal proteins and RNA. J. Biol. Chem. 272:19682–19687.
  • Martín-Marcos P, Hinnebusch AG, Tamame M. 2007. Ribosomal protein L33 is required for ribosome biogenesis, subunit joining, and repression of GCN4 translation. Mol. Cell. Biol. 27:5968–5985.
  • Milkereit P, et al. 2003. A Noc-complex specifically involved in the formation and nuclear export of ribosomal 40S subunits. J. Biol. Chem. 278:4072–4081.
  • Mizushima S, Nomura M. 1970. Assembly mapping of 30S ribosomal proteins in E. coli. Nature 226:1214–1218.
  • Moazed D, Noller HF. 1986. Transfer RNA shields specific nucleotides in 16S ribosomal RNA from attack by chemical probes. Cell 47:985–994.
  • Moritz M, Pulaski BA, Woolford JLJr. 1991. Assembly of 60S ribosomal subunits is perturbed in temperature-sensitive yeast mutants defective in ribosomal protein L16. Mol. Cell. Biol. 11:5681–5692.
  • Mulder AM, et al. 2010. Visualizing ribosome biogenesis: parallel assembly pathways for the 30S subunit. Science 330:673–677.
  • Nierhaus KH. 1991. The assembly of prokaryotic ribosomes. Biochimie 73:739–755.
  • Nierhaus KH, Dohme F. 1974. Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 71:4713–4717.
  • Nissan TA, Bassler J, Petfalski E, Tollervey D, Hurt E. 2002. 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J. 21:5539–5547.
  • Oeffinger M, et al. 2007. Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods 4:951–956.
  • Ofir-Rosenfeld Y, Boggs K, Michael D, Kastan MB, Oren M. 2008. Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26. Mol. Cell 32:180–189.
  • Ohtake Y, Wickner RB. 1995. Yeast virus propagation depends critically on free 60S ribosomal subunit concentration. Mol. Cell. Biol. 15:2772–2781.
  • Peisker K, et al. 2008. Ribosome-associated complex binds to ribosomes in close proximity of Rpl31 at the exit of the polypeptide tunnel in yeast. Mol. Biol. Cell 19:5279–5288.
  • Pettersen EF, et al. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605–1612.
  • Pichon J, Marvaldi J, Marchis-Mouren G. 1975. The in vivo order of protein addition in the course of Escherichia coli 30 S and 50 S subunit biogenesis. J. Mol. Biol. 96:125–137.
  • Pöll G, et al. 2009. rRNA maturation in yeast cells depleted of large ribosomal subunit proteins. PLoS One 4:e8249. https://doi.org/10.1371/journal.pone.0008249.
  • Raue U, Oellerer S, Rospert S. 2007. Association of protein biogenesis factors at the yeast ribosomal tunnel exit is affected by the translational status and nascent polypeptide sequence. J. Biol. Chem. 282:7809–7816.
  • Remacha M, et al. 1995. Ribosomal acidic phosphoproteins P1 and P2 are not required for cell viability but regulate the pattern of protein expression in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:4754–4762.
  • Rigaut G, et al. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17:1030–1032.
  • Robledo S, et al. 2008. The role of human ribosomal proteins in the maturation of rRNA and ribosome production. RNA 14:1918–1929.
  • Rodríguez-Mateos M, et al. 2009. The amino terminal domain from Mrt4 protein can functionally replace the RNA binding domain of the ribosomal P0 protein. Nucleic Acids Res. 37:3514–3521.
  • Rodríguez-Mateos M, et al. 2009. Role and dynamics of the ribosomal protein P0 and its related trans-acting factor Mrt4 during ribosome assembly in Saccharomyces cerevisiae. Nucleic Acids Res. 37:7519–7532.
  • Rosado IV, Kressler D, de la Cruz J. 2007. Functional analysis of Saccharomyces cerevisiae ribosomal protein Rpl3p in ribosome synthesis. Nucleic Acids Res. 35:4203–4213.
  • Sachs AB, Davis RW. 1990. Translation initiation and ribosomal biogenesis: involvement of a putative rRNA helicase and RPL46. Science 247:1077–1079.
  • Sahasranaman A, et al. 2011. Assembly of Saccharomyces cerevisiae 60S ribosomal subunits: role of factors required for 27S pre-rRNA processing. EMBO J. 30:4020–4032.
  • Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
  • Saveanu C, et al. 2001. Nog2p, a putative GTPase associated with pre-60S subunits and required for late 60S maturation steps. EMBO J. 20:6475–6484.
  • Saveanu C, et al. 2003. Sequential protein association with nascent 60S ribosomal particles. Mol. Cell. Biol. 23:4449–4460.
  • Schäfer T, Strauss D, Petfalski E, Tollervey D, Hurt E. 2003. The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J. 22:1370–1380.
  • Senger B, et al. 2001. The nucle(ol)ar Tif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol. Cell 8:1363–1373.
  • Shajani Z, Sykes MT, Williamson JR. 2011. Assembly of bacterial ribosomes. Annu. Rev. Biochem. 80:501–526.
  • Shoji S, Dambacher CM, Shajani Z, Williamson JR, Schultz PG. 2011. Systematic chromosomal deletion of bacterial ribosomal protein genes. J. Mol. Biol. 413:751–761.
  • Spillmann S, Nierhaus KH. 1978. The ribosomal protein L24 of Escherichia coli is an assembly protein. J. Biol. Chem. 253:7047–7050.
  • Steffen KK, et al. 2008. Yeast life span extension by depletion of 60S ribosomal subunits is mediated by Gcn4. Cell 133:292–302.
  • Steffen KK, et al. 2012. Ribosome deficiency protects against ER stress in Saccharomyces cerevisiae. Genetics 191:107–118.
  • Steitz TA, Moore PB. 2003. RNA, the first macromolecular catalyst: the ribosome is a ribozyme. Trends Biochem. Sci. 28:411–418.
  • Sykes MT, Shajani Z, Sperling E, Beck AH, Williamson JR. 2010. Quantitative proteomic analysis of ribosome assembly and turnover in vivo. J. Mol. Biol. 403:331–345.
  • Takagi M, Absalon MJ, McLure KG, Kastan MB. 2005. Regulation of p53 translation and induction after DNA damage by ribosomal protein L26 and nucleolin. Cell 123:49–63.
  • Talkington MW, Siuzdak G, Williamson JR. 2005. An assembly landscape for the 30S ribosomal subunit. Nature 438:628–632.
  • Thomson E, Tollervey D. 2005. Nop53p is required for late 60S ribosome subunit maturation and nuclear export in yeast. RNA 11:1215–1224.
  • Trapman J, Retèl J, Planta RJ. 1975. Ribosomal precursor particles from yeast. Exp. Cell Res. 90:95–104.
  • Tuite MF, Stansfield I, Eurwilaichitr L, Akhmaloka. 1993. Novel ribosome-associated translation factors are required to maintain the fidelity of translation in yeast. Biochem. Soc. Trans. 21:857–862.
  • Ulbrich C, et al. 2009. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell 138:911–922.
  • van Beekvelt CA, de Graaff-Vincent M, Faber AW, van't Riet J, Venema J, Raué HA. 2001. All three functional domains of the large ribosomal subunit protein L25 are required for both early and late pre-rRNA processing steps in Saccharomyces cerevisiae. Nucleic Acids Res. 29:5001–5008.
  • Venema J, Planta RJ, Raué HA. 1998. In vivo mutational analysis of ribosomal RNA in Saccharomyces cerevisiae, p 257–270. InMartin R (ed), Protein synthesis: methods and protocols, vol 77. Humana Press, Totowa, NJ.
  • Venema J, Tollervey D. 1999. Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 33:261–311.
  • Vilardell J, Warner JR. 1997. Ribosomal protein L32 of Saccharomyces cerevisiae influences both the splicing of its own transcript and the processing of rRNA. Mol. Cell. Biol. 17:1959–1965.
  • Wach A, Brachat A, Alberti-Segui C, Rebischung C, Philippsen P. 1997. Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast 13:1065–1075.
  • Warner JR. 1999. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24:437–440.
  • West M, Hedges JB, Chen A, Johnson AW. 2005. Defining the order in which Nmd3p and Rpl10p load onto nascent 60S ribosomal subunits. Mol. Cell. Biol. 25:3802–3813.
  • Williamson JR. 2009. The ribosome at atomic resolution. Cell 139:1041–1043.
  • Xu Z, Culver GM. 2009. Chemical probing of RNA and RNA/protein complexes. Methods Enzymol. 468:147–165.
  • Yonath A. 2005. Antibiotics targeting ribosomes: resistance, selectivity, synergism and cellular regulation. Annu. Rev. Biochem. 74:649–679.
  • Yu X, Warner JR. 2001. Expression of a micro-protein. J. Biol. Chem. 276:33821–33825.
  • Zanchin NIT, Roberts P, DeSilva A, Sherman F, Goldfarb DS. 1997. Saccharomyces cerevisiae Nip7p is required for efficient 60S ribosome subunit biogenesis. Mol. Cell. Biol. 17:5001–5015.
  • Zhang Y, et al. 2010. Negative regulation of HDM2 to attenuate p53 degradation by ribosomal protein L26. Nucleic Acids Res. 38:6544–6554.

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