Prefabrication of a ribosomal protein subcomplex essential for eukaryotic ribosome formation

Peña, Cohue; Schütz, Sabina; Fischer, Ute; Chang, Yeon Soo; Panse, Vikram Govind

doi:10.7554/elife.21755

Cited by 25 publications

(38 citation statements)

References 72 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…It has recently been suggested that Fap7 also plays a role in the nuclear incorporation of Rps14 (Pena et al, 2016), consistent with previously reported nuclear and cytoplasmic localization of Fap7 (Huh et al, 2003). This role could be in addition to the role in promoting the rotated state described herein, and is therefore fully consistent with this report, although alternative explanations for the genetic interaction between Fap7 and Tsr2 have been described (Ferretti et al, 2017).…”

Section: Discussionsupporting

confidence: 91%

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

et al. 2017

View full text Add to dashboard Cite

SUMMARY Late in their maturation, nascent small (40S) ribosomal subunits bind 60S subunits to produce 80S-like ribosomes. Due to the analogy of this translation-like cycle to actual translation, and because 80S-like ribosomes do not produce any protein, it was suggested that this represents a quality-control mechanism for subunit functionality. Here, we use genetic and biochemical experiments to show that the essential ATPase Fap7 promotes formation of the rotated state, a key intermediate in translocation, thereby releasing the essential assembly factor Dim1 from pre-40S subunits. Bypassing this quality control step produces defects in reading frame maintenance. These results show how progress in the maturation cascade is linked to a test for a key functionality of 40S ribosomes, their ability to translocate the mRNA•tRNA pair. Furthermore, our data demonstrate for the first time that the translation-like cycle is a quality control mechanism that ensures the fidelity of the cellular ribosome pool.

show abstract

Section: Discussionsupporting

confidence: 91%

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

et al. 2017

View full text Add to dashboard Cite

show abstract

“…This requires the action of a dedicated chaperone (93). Fap7 also facilitates the association of the cytosolic uS11 with eS26 (97), which, by blocking the 3'-end of the 18S rRNA, is positionally and functionally analogous to the mitochondrial mS37 (84). Therefore, it appears that in human cells conceptually similar mechanisms operate to accomplish the assembly of both cytosolic and mitochondrial SSUs.…”

Section: Discussionmentioning

confidence: 99%

YBEY is an essential biogenesis factor for mitochondrial ribosomes

Summer

Smirnova

Gabriele

et al. 2019

Preprint

View full text Add to dashboard Cite

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...

show abstract

“…In this way, Fap7 might protect S14 from aggregation and/or nonspecific interaction with other RNAs and regulate the correct timing of S14 assembly into pre-40S r-particles. In agreement with this, recombinant S14 from E. coli showed poor solubility unless it is co-expressed with Fap7 185; moreover, depletion of Fap7 causes a strong decrease in the in vivo protein levels of S14 in S. cerevisiae 171. However, there is so far no evidence for co-translational capturing of S14 by Fap7 (discussed in 151).…”

Section: Placeholding By Molecular Mimicrymentioning

confidence: 84%

“…In the Fap7-containing complex, S26 and S14 might interact with each other similarly as they do in the context of the mature SSU 171. Thus, it was concluded that Fap7 is an example of a factor enabling nucleation a module of two r-proteins, which then assemble en bloc into relatively early pre-40S r-particles 171.…”

Section: Placeholding By Molecular Mimicrymentioning

confidence: 98%

Placeholder factors in ribosome biogenesis: please, pave my way

Espinar-Marchena¹,

Babiano²,

Cruz³

2017

Microb Cell

View full text Add to dashboard Cite

The synthesis of cytoplasmic eukaryotic ribosomes is an extraordinarily energy-demanding cellular activity that occurs progressively from the nucleolus to the cytoplasm. In the nucleolus, precursor rRNAs associate with a myriad of trans-acting factors and some ribosomal proteins to form pre-ribosomal particles. These factors include snoRNPs, nucleases, ATPases, GTPases, RNA helicases, and a vast list of proteins with no predicted enzymatic activity. Their coordinate activity orchestrates in a spatiotemporal manner the modification and processing of precursor rRNAs, the rearrangement reactions required for the formation of productive RNA folding intermediates, the ordered assembly of the ribosomal proteins, and the export of pre-ribosomal particles to the cytoplasm; thus, providing speed, directionality and accuracy to the overall process of formation of translation-competent ribosomes. Here, we review a particular class of trans-acting factors known as "placeholders". Placeholder factors temporarily bind selected ribosomal sites until these have achieved a structural context that is appropriate for exchanging the placeholder with another site-specific binding factor. By this strategy, placeholders sterically prevent premature recruitment of subsequently binding factors, premature formation of structures, avoid possible folding traps, and act as molecular clocks that supervise the correct progression of pre-ribosomal particles into functional ribosomal subunits. We summarize the current understanding of those factors that delay the assembly of distinct ribosomal proteins or subsequently bind key sites in pre-ribosomal particles. We also discuss recurrent examples of RNA-protein and protein-protein mimicry between rRNAs and/or factors, which have clear functional implications for the ribosome biogenesis pathway.

show abstract

Prefabrication of a ribosomal protein subcomplex essential for eukaryotic ribosome formation

Cited by 25 publications

References 72 publications

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

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

YBEY is an essential biogenesis factor for mitochondrial ribosomes

Placeholder factors in ribosome biogenesis: please, pave my way

Contact Info

Product

Resources

About