The GTPase Nog1 co-ordinates the assembly, maturation and quality control of distant ribosomal functional centers

Abstract

Eukaryotic ribosome precursors acquire translation competence in the cytoplasm through stepwise release of bound assembly factors, and proofreading of their functional centers. In case of the pre-60S, these steps include removal of placeholders Rlp24, Arx1 and Mrt4 that prevent premature loading of the ribosomal protein eL24, the protein-folding machinery at the polypeptide exit tunnel (PET), and the ribosomal stalk, respectively. Here, we reveal that sequential ATPase and GTPase activities license release factors Rei1 and Yvh1 to trigger Arx1 and Mrt4 removal. Drg1-ATPase activity removes Rlp24 from the GTPase Nog1 on the pre-60S; consequently, the C-terminal tail of Nog1 is extracted from the PET. These events enable Rei1 to probe PET integrity and catalyze Arx1 release. Concomitantly, Nog1 eviction from the pre-60S permits peptidyl transferase center maturation, and allows Yvh1 to mediate Mrt4 release for stalk assembly. Thus, Nog1 co-ordinates the assembly, maturation and quality control of distant functional centers during ribosome formation.

Characterization of Single Gene Deletion Mutants Affecting Alternative Oxidase Production in Neurospora crassa: Role of the yvh1 Gene

“…Interactions of Yvh1 with other proteins required for 60S ribosome maturation have also been detected [ 86 , 87 , 88 ]. Recently, details of the role, structure, and point of action of Yvh1 in the process of ribosome assembly have been defined more precisely [ 89 , 90 , 91 ].…”

From Snapshots to Flipbook—Resolving the Dynamics of Ribosome Biogenesis with Chemical Probes

“…As mentioned above, Nog1 is released in the cytoplasm shortly after Rlp24 [42]. Consequently, only a very minor Nog1-containing particle population lacking Rlp24 has to exist which could undergo maturation after diazaborine treatment and liberate Nog1 for recycling into the nucleus.…”

“…Only those particles, which passed all nuclear maturation stages gain export competence and are, hence, efficiently transported through the nuclear pore complexes by dedicated export factors (recently reviewed in [32]). In the cytoplasm the remaining assembly factors are released and eventually replaced by the last r-proteins before the subunits can join to fulfill their role in translation [33][34][35][36][37][38][39][40][41][42].…”

“…Nog1 joins the maturation cascade at the nucleolar stage, in serts its C-terminal tail into the polypeptide exit tunnel and accompanies the particle until its export into the cytoplasm [58,87]. In the cytoplasm, Nog1 is released from the particle shortly after Rlp24 in a reaction that requires GTP hydrolysis [42]. Given the fact that Nog1 is among the factors that get trapped on the exported cytoplasmic particle upon inhibition of Drg1, it is an ideal candidate to follow the maturation pathway of the pre-60S particle from the nucleolar to the first cytoplasmic step after diazaborine treatment.…”

Spatially Enriched Paralog Rearrangements Argue Functionally Diverse Ribosomes Arise during Cold Acclimation in Arabidopsis

“…In agreement with the indispensability of cold-induced ribosome assembly, RBFs such as REIL proteins are essential to activate biogenesis only during cold in both yeast and in Arabidopsis [ 34 , 38 , 39 , 40 , 41 , 42 , 43 ]. These temperature-specialized proteins mediate the final LSU subunit maturation events in the cytoplasm, which happen concomitantly with the polypeptide exit tunnel (PET) quality control and the P-Stalk assembly [ 44 , 45 ]. PET assembly occurs much earlier in the nucleolus when pre-ribosomal particles are slowly processed and crafted [ 46 ].…”