Molecular basis for disassembly of an importin:ribosomal protein complex by the escortin Tsr2

Schütz, Sabina; Michel, Erich; Damberger, Fred F.; Oplová, Michaela; Peña, Cohue; Leitner, Alexander; Aebersold, Ruedi; Allain, Frédéric H.‐T.; Panse, Vikram Govind

doi:10.1038/s41467-018-06160-x

Cited by 21 publications

(37 citation statements)

References 68 publications

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“…Both Tsr4 and Nap1 have in common that they preferentially bind to eukaryote-specific regions of their r-protein clients. Similar observations have also been made for Acl4 and Tsr2 (13,16,69,70). Moreover, also the N-terminal region of Rpl3, where Rrb1 binds (30), and most of the Sqt1- and Syo1-binding regions within the Rpl10 and Rpl5 N-termini (21,30), respectively, are specific to eukaryotes (71).…”

Section: Discussionsupporting

confidence: 85%

Tsr4 and Nap1, two novel members of the ribosomal protein chaperOME

Rössler

Embacher

Pillet

et al. 2019

Nucleic Acids Research

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Dedicated chaperones protect newly synthesized ribosomal proteins (r-proteins) from aggregation and accompany them on their way to assembly into nascent ribosomes. Currently, only nine of the ∼80 eukaryotic r-proteins are known to be guarded by such chaperones. In search of new dedicated r-protein chaperones, we performed a tandem-affinity purification based screen and looked for factors co-enriched with individual small subunit r-proteins. We report the identification of Nap1 and Tsr4 as direct binding partners of Rps6 and Rps2, respectively. Both factors promote the solubility of their r-protein clients in vitro. While Tsr4 is specific for Rps2, Nap1 has several interaction partners including Rps6 and two other r-proteins. Tsr4 binds co-translationally to the essential, eukaryote-specific N-terminal extension of Rps2, whereas Nap1 interacts with a large, mostly eukaryote-specific binding surface of Rps6. Mutation of the essential Tsr4 and deletion of the non-essential Nap1 both enhance the 40S synthesis defects of the corresponding r-protein mutants. Our findings highlight that the acquisition of eukaryote-specific domains in r-proteins was accompanied by the co-evolution of proteins specialized to protect these domains and emphasize the critical role of r-protein chaperones for the synthesis of eukaryotic ribosomes.

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Section: Discussionsupporting

confidence: 85%

Tsr4 and Nap1, two novel members of the ribosomal protein chaperOME

Rössler

Embacher

Pillet

et al. 2019

Nucleic Acids Research

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“…These differences illustrate how eukaryotic and euryarchaeal ribosomes evolved different binding modes of the mRNA in the exit pocket, in relation with the canonical eukaryotic scanning mode vs. the SD-assisted AUG recognition mode occurring in many genes in the archaeal domain. In this view, it is notable that eS26 is absent in euryarchaotes but present in crenarchaeota/lokiarchaeota genomes 7,81 . Because the archaeal version of the exit chamber is a simplified version of the eukaryotic one, this argues in favor of the controversial hypothesis that eukaryotic ribosomes have evolved from within the archaeal version 10,82 .…”

Section: Discussionmentioning

confidence: 98%

Cryo-EM study of an archaeal 30S initiation complex gives insights into evolution of translation initiation

et al. 2020

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Archaeal translation initiation occurs within a macromolecular complex containing the small ribosomal subunit (30S) bound to mRNA, initiation factors aIF1, aIF1A and the ternary complex aIF2:GDPNP:Met-tRNA i Met. Here, we determine the cryo-EM structure of a 30S: mRNA:aIF1A:aIF2:GTP:Met-tRNA i Met complex from Pyrococcus abyssi at 3.2 Å resolution. It highlights archaeal features in ribosomal proteins and rRNA modifications. We find an aS21 protein, at the location of eS21 in eukaryotic ribosomes. Moreover, we identify an N-terminal extension of archaeal eL41 contacting the P site. We characterize 34 N 4-acetylcytidines distributed throughout 16S rRNA, likely contributing to hyperthermostability. Without aIF1, the 30S head is stabilized and initiator tRNA is tightly bound to the P site. A network of interactions involving tRNA, mRNA, rRNA modified nucleotides and C-terminal tails of uS9, uS13 and uS19 is observed. Universal features and domain-specific idiosyncrasies of translation initiation are discussed in light of ribosomal structures from representatives of each domain of life.

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“…Cells can even evolve a specialized chaperone system to interact with ribosomal proteins specifically. These dedicated chaperones could regulate the stability, transport, stoichiometry, and orientation of ribosomal proteins during the assembly process [14,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33].…”

Section: Introductionmentioning

confidence: 99%

Puf6 and Loc1 Are the Dedicated Chaperones of Ribosomal Protein Rpl43 in Saccharomyces cerevisiae

Liang

Yueh

Hsu

et al. 2019

IJMS

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Ribosomal proteins are highly expressed, and the quality of ribosomal proteins must be rigorously controlled to build up a functional ribosome. Rpl43, ribosomal protein large subunit 43, is located nearby the E-site of ribosomes. In our previous study, we found that Puf6, Loc1, and Rpl43 form a trimeric complex in Saccharomyces cerevisiae. Rpl43 protein levels are under-accumulated in the absence of PUF6 or LOC1. However, why the loss of Puf6 or Loc1 decreased the protein levels of Rpl43 remained unclear. In the present study, we further dissected the connections among these three proteins and found that the processing defects of pre-ribosomal RNA in puf6Δ and loc1Δ are similar to those of the mutant with depletion of Rpl43. The stability of newly synthesized Rpl43 protein decreased slightly in puf6Δ and significantly in loc1Δ. We also found that Puf6 and Loc1 could interact with nascent Rpl43 co-translationally via the N-terminus of Rpl43. While the association and dissociation of Rpl43 with karyopherins did not depend on Puf6 and Loc1, Puf6 and Loc1 interacted with nascent Rpl43 in collaboration. While the N-terminus of Puf6 contained nuclear localization signals for transport, the PUF (Pumilio) domain was essential to interaction with Loc1, Rpl43, and 60S subunits. The C-terminus of Loc1 is more important for interaction with Puf6 and Rpl43. In this study, we found that Puf6 and Loc1 are the dedicated chaperones of ribosomal protein Rpl43 and also analyzed the potential interaction domains among the three proteins. Correct formation of the Puf6, Loc1, and Rpl43 ternary complex is required to properly proceed to the next step in 60S biogenesis.

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Molecular basis for disassembly of an importin:ribosomal protein complex by the escortin Tsr2

Cited by 21 publications

References 68 publications

Tsr4 and Nap1, two novel members of the ribosomal protein chaperOME

Tsr4 and Nap1, two novel members of the ribosomal protein chaperOME

Cryo-EM study of an archaeal 30S initiation complex gives insights into evolution of translation initiation

Puf6 and Loc1 Are the Dedicated Chaperones of Ribosomal Protein Rpl43 in Saccharomyces cerevisiae

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