Ribosome-associated Complex Binds to Ribosomes in Close Proximity of Rpl31 at the Exit of the Polypeptide Tunnel in Yeast

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2008 Oct 3

PMID 18829863

Citations 55

Authors

Kristin Peisker

Daniel Braun

Tina Wolfle

Jendrik Hentschel

Ursula Funfschilling

Gunter Fischer

Albert Sickmann

Sabine Rospert

Affiliations

Soon will be listed here.

Abstract

Ribosome-associated complex (RAC) consists of the Hsp40 homolog Zuo1 and the Hsp70 homolog Ssz1. The chaperone participates in the biogenesis of newly synthesized polypeptides. Here we have identified yeast Rpl31, a component of the large ribosomal subunit, as a contact point of RAC at the polypeptide tunnel exit. Rpl31 is encoded by RPL31a and RPL31b, two closely related genes. Delta rpl31a Delta rpl31b displayed slow growth and sensitivity to low as well as high temperatures. In addition, Delta rpl31a Delta rpl31b was highly sensitive toward aminoglycoside antibiotics and suffered from defects in translational fidelity. With the exception of sensitivity at elevated temperature, the phenotype resembled yeast strains lacking one of the RAC subunits or Rpl39, another protein localized at the tunnel exit. Defects of Delta rpl31a Delta rpl31b Delta zuo1 did not exceed that of Delta rpl31a Delta rpl31b or Delta zuo1. However, the combined deletion of RPL31a, RPL31b, and RPL39 was lethal. Moreover, RPL39 was a multicopy suppressor, whereas overexpression of RAC failed to rescue growth defects of Delta rpl31a Delta rpl31b. The findings are consistent with a model in that Rpl31 and Rpl39 independently affect a common ribosome function, whereas Rpl31 and RAC are functionally interdependent. Rpl31, while not essential for binding of RAC to the ribosome, might be involved in proper function of the chaperone complex.

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References

Gautschi M, Lilie H, Funfschilling U, Mun A, Ross S, Lithgow T . RAC, a stable ribosome-associated complex in yeast formed by the DnaK-DnaJ homologs Ssz1p and zuotin. Proc Natl Acad Sci U S A. 2001; 98(7):3762-7. PMC: 31126. DOI: 10.1073/pnas.071057198. View

Bidou L, Stahl G, Hatin I, Namy O, Rousset J, Farabaugh P . Nonsense-mediated decay mutants do not affect programmed -1 frameshifting. RNA. 2000; 6(7):952-61. PMC: 1369972. DOI: 10.1017/s1355838200000443. View

Klein D, Schmeing T, Moore P, Steitz T . The kink-turn: a new RNA secondary structure motif. EMBO J. 2001; 20(15):4214-21. PMC: 149158. DOI: 10.1093/emboj/20.15.4214. View

Harms J, Schluenzen F, Zarivach R, Bashan A, Gat S, AGMON I . High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell. 2001; 107(5):679-88. DOI: 10.1016/s0092-8674(01)00546-3. View

Hundley H, Eisenman H, Walter W, Evans T, Hotokezaka Y, Wiedmann M . The in vivo function of the ribosome-associated Hsp70, Ssz1, does not require its putative peptide-binding domain. Proc Natl Acad Sci U S A. 2002; 99(7):4203-8. PMC: 123626. DOI: 10.1073/pnas.062048399. View

Gautschi M, Mun A, Ross S, Rospert S . A functional chaperone triad on the yeast ribosome. Proc Natl Acad Sci U S A. 2002; 99(7):4209-14. PMC: 123627. DOI: 10.1073/pnas.062048599. View

Dudek J, Volkmer J, Bies C, Guth S, Muller A, Lerner M . A novel type of co-chaperone mediates transmembrane recruitment of DnaK-like chaperones to ribosomes. EMBO J. 2002; 21(12):2958-67. PMC: 126068. DOI: 10.1093/emboj/cdf315. View

Pool M, Stumm J, Fulga T, Sinning I, Dobberstein B . Distinct modes of signal recognition particle interaction with the ribosome. Science. 2002; 297(5585):1345-8. DOI: 10.1126/science.1072366. View

Kramer G, Rauch T, Rist W, Vorderwulbecke S, Patzelt H, Schulze-Specking A . L23 protein functions as a chaperone docking site on the ribosome. Nature. 2002; 419(6903):171-4. DOI: 10.1038/nature01047. View

10.

Lecompte O, Ripp R, Thierry J, Moras D, Poch O . Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acids Res. 2002; 30(24):5382-90. PMC: 140077. DOI: 10.1093/nar/gkf693. View

11.

Blaha G, Wilson D, Stoller G, Fischer G, Willumeit R, Nierhaus K . Localization of the trigger factor binding site on the ribosomal 50S subunit. J Mol Biol. 2003; 326(3):887-97. DOI: 10.1016/s0022-2836(02)01436-5. View

12.

Enyenihi A, Saunders W . Large-scale functional genomic analysis of sporulation and meiosis in Saccharomyces cerevisiae. Genetics. 2003; 163(1):47-54. PMC: 1462418. DOI: 10.1093/genetics/163.1.47. View

13.

Gu S, Peske F, Wieden H, Rodnina M, Wintermeyer W . The signal recognition particle binds to protein L23 at the peptide exit of the Escherichia coli ribosome. RNA. 2003; 9(5):566-73. PMC: 1370422. DOI: 10.1261/rna.2196403. View

14.

Ullers R, Houben E, Raine A, Ten Hagen-Jongman C, Ehrenberg M, Brunner J . Interplay of signal recognition particle and trigger factor at L23 near the nascent chain exit site on the Escherichia coli ribosome. J Cell Biol. 2003; 161(4):679-84. PMC: 2199365. DOI: 10.1083/jcb.200302130. View

15.

Fromont-Racine M, Senger B, Saveanu C, Fasiolo F . Ribosome assembly in eukaryotes. Gene. 2003; 313:17-42. DOI: 10.1016/s0378-1119(03)00629-2. View

16.

Gautschi M, Just S, Mun A, Ross S, Rucknagel P, Dubaquie Y . The yeast N(alpha)-acetyltransferase NatA is quantitatively anchored to the ribosome and interacts with nascent polypeptides. Mol Cell Biol. 2003; 23(20):7403-14. PMC: 230319. DOI: 10.1128/MCB.23.20.7403-7414.2003. View

17.

Halic M, Becker T, Pool M, Spahn C, Grassucci R, Frank J . Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature. 2004; 427(6977):808-14. DOI: 10.1038/nature02342. View

18.

Klein D, Moore P, Steitz T . The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J Mol Biol. 2004; 340(1):141-77. DOI: 10.1016/j.jmb.2004.03.076. View

19.

Rospert S . Ribosome function: governing the fate of a nascent polypeptide. Curr Biol. 2004; 14(10):R386-8. DOI: 10.1016/j.cub.2004.05.013. View

20.

Rakwalska M, Rospert S . The ribosome-bound chaperones RAC and Ssb1/2p are required for accurate translation in Saccharomyces cerevisiae. Mol Cell Biol. 2004; 24(20):9186-97. PMC: 517888. DOI: 10.1128/MCB.24.20.9186-9197.2004. View