Architecture of the Rix1-Rea1 Checkpoint Machinery During Pre-60S-ribosome Remodeling

Overview

Journal Nat Struct Mol Biol

Specialties Cell Biology
Molecular Biology

Date 2015 Dec 1

PMID 26619264

Citations 78

Authors

Clara Barrio-Garcia

Matthias Thoms

Dirk Flemming

Lukas Kater

Otto Berninghausen

Jochen Bassler

Roland Beckmann

Ed Hurt

Affiliations

Soon will be listed here.

Abstract

Ribosome synthesis is catalyzed by ∼200 assembly factors, which facilitate efficient production of mature ribosomes. Here, we determined the cryo-EM structure of a Saccharomyces cerevisiae nucleoplasmic pre-60S particle containing the dynein-related 550-kDa Rea1 AAA(+) ATPase and the Rix1 subcomplex. This particle differs from its preceding state, the early Arx1 particle, by two massive structural rearrangements: an ∼180° rotation of the 5S ribonucleoprotein complex and the central protuberance (CP) rRNA helices, and the removal of the 'foot' structure from the 3' end of the 5.8S rRNA. Progression from the Arx1 to the Rix1 particle was blocked by mutational perturbation of the Rix1-Rea1 interaction but not by a dominant-lethal Rea1 AAA(+) ATPase-ring mutant. After remodeling, the Rix1 subcomplex and Rea1 become suitably positioned to sense correct structural maturation of the CP, which allows unidirectional progression toward mature ribosomes.

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References

Oeffinger M, Zenklusen D, Ferguson A, Wei K, El Hage A, Tollervey D . Rrp17p is a eukaryotic exonuclease required for 5' end processing of Pre-60S ribosomal RNA. Mol Cell. 2009; 36(5):768-81. PMC: 2806520. DOI: 10.1016/j.molcel.2009.11.011. View

Mitchell P, Petfalski E, Tollervey D . The 3' end of yeast 5.8S rRNA is generated by an exonuclease processing mechanism. Genes Dev. 1996; 10(4):502-13. DOI: 10.1101/gad.10.4.502. View

Ludtke S, Baldwin P, Chiu W . EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol. 1999; 128(1):82-97. DOI: 10.1006/jsbi.1999.4174. View

Dez C, Houseley J, Tollervey D . Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae. EMBO J. 2006; 25(7):1534-46. PMC: 1440318. DOI: 10.1038/sj.emboj.7601035. View

Waterhouse A, Procter J, Martin D, Clamp M, Barton G . Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009; 25(9):1189-91. PMC: 2672624. DOI: 10.1093/bioinformatics/btp033. View

Janke C, Magiera M, Rathfelder N, Taxis C, Reber S, Maekawa H . A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast. 2004; 21(11):947-62. DOI: 10.1002/yea.1142. View

Zhang J, Harnpicharnchai P, Jakovljevic J, Tang L, Guo Y, Oeffinger M . Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes Dev. 2007; 21(20):2580-92. PMC: 2000323. DOI: 10.1101/gad.1569307. View

Rinner O, Seebacher J, Walzthoeni T, Mueller L, Beck M, Schmidt A . Identification of cross-linked peptides from large sequence databases. Nat Methods. 2008; 5(4):315-8. PMC: 2719781. DOI: 10.1038/nmeth.1192. View

West M, Hedges J, Chen A, Johnson A . Defining the order in which Nmd3p and Rpl10p load onto nascent 60S ribosomal subunits. Mol Cell Biol. 2005; 25(9):3802-13. PMC: 1084314. DOI: 10.1128/MCB.25.9.3802-3813.2005. View

10.

Kappel L, Loibl M, Zisser G, Klein I, Fruhmann G, Gruber C . Rlp24 activates the AAA-ATPase Drg1 to initiate cytoplasmic pre-60S maturation. J Cell Biol. 2012; 199(5):771-82. PMC: 3514788. DOI: 10.1083/jcb.201205021. View

11.

Woolford Jr J, Baserga S . Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics. 2013; 195(3):643-81. PMC: 3813855. DOI: 10.1534/genetics.113.153197. View

12.

Galani K, Nissan T, Petfalski E, Tollervey D, Hurt E . Rea1, a dynein-related nuclear AAA-ATPase, is involved in late rRNA processing and nuclear export of 60 S subunits. J Biol Chem. 2004; 279(53):55411-8. DOI: 10.1074/jbc.M406876200. View

13.

Chu S, Archer R, Zengel J, Lindahl L . The RNA of RNase MRP is required for normal processing of ribosomal RNA. Proc Natl Acad Sci U S A. 1994; 91(2):659-63. PMC: 43008. DOI: 10.1073/pnas.91.2.659. View

14.

Buscemi G, Saracino F, Masnada D, Carbone M . The Saccharomyces cerevisiae SDA1 gene is required for actin cytoskeleton organization and cell cycle progression. J Cell Sci. 2000; 113 ( Pt 7):1199-211. DOI: 10.1242/jcs.113.7.1199. View

15.

Simos G, Segref A, Fasiolo F, Hellmuth K, Shevchenko A, Mann M . The yeast protein Arc1p binds to tRNA and functions as a cofactor for the methionyl- and glutamyl-tRNA synthetases. EMBO J. 1996; 15(19):5437-48. PMC: 452286. View

16.

Demoinet E, Jacquier A, Lutfalla G, Fromont-Racine M . The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae. RNA. 2007; 13(9):1570-81. PMC: 1950757. DOI: 10.1261/rna.585007. View

17.

de la Cruz J, Sanz-Martinez E, Remacha M . The essential WD-repeat protein Rsa4p is required for rRNA processing and intra-nuclear transport of 60S ribosomal subunits. Nucleic Acids Res. 2005; 33(18):5728-39. PMC: 1253832. DOI: 10.1093/nar/gki887. View

18.

Bassler J, Paternoga H, Holdermann I, Thoms M, Granneman S, Barrio-Garcia C . A network of assembly factors is involved in remodeling rRNA elements during preribosome maturation. J Cell Biol. 2014; 207(4):481-98. PMC: 4242840. DOI: 10.1083/jcb.201408111. View

19.

Lamanna A, Karbstein K . Nob1 binds the single-stranded cleavage site D at the 3'-end of 18S rRNA with its PIN domain. Proc Natl Acad Sci U S A. 2009; 106(34):14259-64. PMC: 2732849. DOI: 10.1073/pnas.0905403106. View

20.

Calvino F, Kharde S, Ori A, Hendricks A, Wild K, Kressler D . Symportin 1 chaperones 5S RNP assembly during ribosome biogenesis by occupying an essential rRNA-binding site. Nat Commun. 2015; 6:6510. PMC: 4396368. DOI: 10.1038/ncomms7510. View