The ATPase Fap7 Tests the Ability to Carry Out Translocation-like Conformational Changes and Releases Dim1 during 40S Ribosome Maturation

Ghalei, Homa; Trepreau, Juliette; Collins, Jason C.; Bhaskaran, Hari; Strunk, Bethany S.; Karbstein, Katrin

doi:10.1016/j.molcel.2017.08.007

Cited by 52 publications

(88 citation statements)

References 62 publications

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“…Nob1 blocks mRNA recruitment to 20S pre-rRNA-containing ribosomes Nascent 40S subunits arrive in the cytoplasm bound to seven assembly factors, which block premature translation initiation on immature assembly intermediates by preventing the association of translation initiation factors (Strunk et al, 2012). These assembly factors are then released in a series of regulated steps that form part of a translation-like cycle, which couples the release of these factors to quality control steps (Collins et al, 2018;Ghalei et al, 2017;Strunk et al, 2012). Furthermore, when pre-mature ribosomes do escape into the translating pool, they are unable to support cell viability (Soudet et al, 2010;Strunk et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

“…To prevent misassembled ribosomes from reaching the translating pool, the premature small (pre-40S) ribosomal subunit undergoes a series of quality control checkpoints during late cytoplasmic maturation that verify proper ribosomal structure and function (Collins et al, 2018;Ghalei et al, 2017;Strunk et al, 2012). The importance of these checkpoints for cellular function is illustrated by the numerous diseases caused by haploinsufficiency or mutations in ribosomal proteins and assembly factors.…”

Section: Introductionmentioning

confidence: 99%

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A kinase-dependent checkpoint prevents escape of immature ribosomes into the translating pool

Parker

Collins

Korona

et al. 2019

Preprint

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Premature release of nascent ribosomes into the translating pool must be prevented, as these do not support viability and may be prone to mistakes. Here we show that the kinase Rio1, the nuclease Nob1, and its binding partner Pno1 cooperate to establish a checkpoint that prevents the escape of immature ribosomes into polysomes. Nob1 blocks mRNA recruitment, and rRNA cleavage is required for its dissociation from nascent 40S subunits, thereby setting up a checkpoint for maturation. Rio1 releases Nob1 and Pno1 from pre-40S ribosomes to discharge nascent 40S into the translating pool. Weakly binding Nob1 and Pno1 mutants can bypass the requirement for Rio1, and Pno1 mutants rescue cell viability. In these strains, immature ribosomes escape into the translating pool, where they cause fidelity defects and perturb protein homeostasis. Thus, the Rio1-Nob1-Pno1 network establishes a checkpoint that safeguards against the release of immature ribosomes into the translating pool.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A kinase-dependent checkpoint prevents escape of immature ribosomes into the translating pool

Parker

Collins

Korona

et al. 2019

Preprint

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“…Similar to YBEY, Fap7 forms a stoichiometric complex with uS11/Rps14 (93) and helps to recruit it to the nascent SSU (94), which represents a final checkpoint before the fully assembled SSU is released for translation (95). In fact, all known uS11 homologues have a long disordered positively charged C-terminal extension, which needs to be correctly positioned in the vicinity of the helix-45 of the SSU rRNA ( Figure 6E) (96).…”

Section: Discussionmentioning

confidence: 99%

YBEY is an essential biogenesis factor for mitochondrial ribosomes

Summer

Smirnova

Gabriele

et al. 2019

Preprint

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Ribosome biogenesis requires numerous trans-acting factors, some of which are deeply conserved. In Bacteria, the endoribonuclease YbeY is believed to be involved in 16S rRNA 3'-end processing and its loss was associated with ribosomal abnormalities. In Eukarya, YBEY appears to generally localize to mitochondria (or chloroplasts). Here we show that the deletion of human YBEY results in a severe respiratory deficiency and morphologically abnormal mitochondria as an apparent consequence of impaired mitochondrial translation. Reduced stability of 12S rRNA and the deficiency of several proteins of the small ribosomal subunit in YBEY knockout cells pointed towards a defect in mitochondrial ribosome biogenesis. The specific interaction of mitoribosomal protein uS11m with YBEY suggests that the latter recruits uS11m to the nascent small subunit in its late assembly stage. This scenario shows similarities with final stages of cytosolic ribosome biogenesis, and may represent a late checkpoint before the mitoribosome engages in translation. INTRODUCTIONRibosome biogenesis is a highly complex process that starts co-transcriptionally and includes ribosomal RNA processing, modification, and binding of ribosomal proteins (1). Each of these steps relies on specific factors, some of which are remarkably conserved. One such factor is the UPF0054 family protein YbeY found in all classified bacteria (2). Based on studies in various bacteria, YbeY has been implicated in ribosome maturation and quality control, with a particularly important role in small subunit (SSU) biogenesis (3-8), and post-transcriptional gene expression regulation (9-14). The deletion of ybeY is often lethal or associated with severe alterations of cellular metabolism and growth, indicating its indispensability for a wide variety of bacterial-type ribosomes (4,6,7,(13)(14)(15)(16)(17).Mechanistically, YbeY has been described as a metal-dependent endoribonuclease (5,12), and in some bacteria, ybeY mutants accumulate 16S rRNA with an unprocessed 3' end (3,5,7,8). Therefore, YbeY was proposed to be the "missing" 3' endoribonuclease required for 16S rRNA maturation to obtain the correct anti-Shine-Dalgarno sequence, which is needed for translation initiation on most bacterial mRNAs. However, this 16S rRNA 3'-misprocessing phenotype could equally be caused by the loss of a ribosome biogenesis factor that is not per se involved in rRNA cleavage (18), and so the precise role of YbeY in ribosome biogenesis remains unclear.By carrying out an in-depth phylogenetic analysis, we found that YBEY is also conserved in many eukaryal lineages, including animals, plants, most stramenopiles and alveolates (Supplementary Figure 1). Indeed, YbeY of Arabidopsis thaliana was reported to be an essential ribosome biogenesis factor in chloroplasts, and its absence was associated with severe misprocessing of nearly all chloroplast rRNAs, resulting in deficiency of organellar translation, and hence, the absence of photosynthesis (16). Human YBEY, which shares 27% of identity with YbeY of...

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“…The sedimentation profile showed that the majority of Tsr1-FPZ pre-40S particles presented a peak position very similar to that of mature 40S ribosomal subunits, thus migrating as "free" pre-40S subunits. A smaller peak of heavier fractions indicates that Tsr1-FPZ could be found in bigger complexes, some of them probably being 80S-like particles [29,30,34,35] (Figure 1a, upper panel). Transmission electron microscopy (TEM) observations after negative staining confirmed that the particles sedimenting on lighter fractions had the overall size and shape of 40S subunits, while heavier fractions contained larger, rounder objects, with dimensions compatible with 80S-like particles (Figure 1a, lower panel).…”

Section: Proteomic Characterization Of Tsr1-purified Pre-40s Particlesmentioning

confidence: 99%

Good Vibrations: Structural Remodeling of Maturing Yeast Pre-40S Ribosomal Particles Followed by Cryo-Electron Microscopy

et al. 2020

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Assembly of eukaryotic ribosomal subunits is a very complex and sequential process that starts in the nucleolus and finishes in the cytoplasm with the formation of functional ribosomes. Over the past few years, characterization of the many molecular events underlying eukaryotic ribosome biogenesis has been drastically improved by the “resolution revolution” of cryo-electron microscopy (cryo-EM). However, if very early maturation events have been well characterized for both yeast ribosomal subunits, little is known regarding the final maturation steps occurring to the small (40S) ribosomal subunit. To try to bridge this gap, we have used proteomics together with cryo-EM and single particle analysis to characterize yeast pre-40S particles containing the ribosome biogenesis factor Tsr1. Our analyses lead us to refine the timing of the early pre-40S particle maturation steps. Furthermore, we suggest that after an early and structurally stable stage, the beak and platform domains of pre-40S particles enter a “vibrating” or “wriggling” stage, that might be involved in the final maturation of 18S rRNA as well as the fitting of late ribosomal proteins into their mature position.

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The ATPase Fap7 Tests the Ability to Carry Out Translocation-like Conformational Changes and Releases Dim1 during 40S Ribosome Maturation

Cited by 52 publications

References 62 publications

A kinase-dependent checkpoint prevents escape of immature ribosomes into the translating pool

A kinase-dependent checkpoint prevents escape of immature ribosomes into the translating pool

YBEY is an essential biogenesis factor for mitochondrial ribosomes

Good Vibrations: Structural Remodeling of Maturing Yeast Pre-40S Ribosomal Particles Followed by Cryo-Electron Microscopy

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