Symportin 1 chaperones 5S RNP assembly during ribosome biogenesis by occupying an essential rRNA-binding site

Calviño, Fabiola R.; Kharde, Satyavati; Ori, Alessandro; Hendricks, Astrid; Wild, Klemens; Kressler, Dieter; Bange, Gert; Hurt, Ed; Beck, Martin; Sinning, Irmgard

doi:10.1038/ncomms7510

Cited by 54 publications

(76 citation statements)

References 30 publications

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“…A specific feature of LSU assembly is the incorporation of a preformed 5S RNP ( Figure 2J) comprising the 5S RNA and the rproteins uL5 and uL18. Formation of the 5S RNP is facilitated by the transport adaptor Syo1, which couples nuclear import of uL5 and uL18 with 5S rRNA association [90,91]. The subsequent incorporation of the 5S RNP module involves the Rpf2-Rrs1 heterodimer and has already occurred within the Nsa1-defined particle [25,86,[92][93][94] (Figure 2K).…”

Section: Assembly Of the Lsumentioning

confidence: 99%

A Puzzle of Life: Crafting Ribosomal Subunits

Kressler

Hurt

Baßler

2017

Trends in Biochemical Sciences

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165

127

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The biogenesis of eukaryotic ribosomes is a complicated process during which the transcription, modification, folding, and processing of the rRNA is coupled with the ordered assembly of $80 ribosomal proteins (r-proteins). Ribosome synthesis is catalyzed and coordinated by more than 200 biogenesis factors as the preribosomal subunits acquire maturity on their path from the nucleolus to the cytoplasm. Several biogenesis factors also interconnect the progression of ribosome assembly with quality control of important domains, ensuring that only functional subunits engage in translation. With the recent visualization of several assembly intermediates by cryoelectron microscopy (cryo-EM), a structural view of ribosome assembly begins to emerge. In this review we integrate these first structural insights into an updated overview of the consecutive ribosome assembly steps. Synopsis of Eukaryotic Ribosome AssemblyRibosomes are the molecular machines that translate the genetic information from the intermediary mRNA templates into proteins [1]. Eukaryotic 80S ribosomes comprise two unequal subunits that contain four different rRNAs and around 80 r-proteins ( Figure 1). The small 40S subunit (SSU) comprises the 18S rRNA and 33 r-proteins (referred to as RPS or S). The large 60S subunit (LSU) comprises the 25S/28S, 5.8S, and 5S rRNA and, in most eukaryotic species, 47 r-proteins (RPL or L); a notable exception is budding yeasts, which lack eL28The act of building a ribosome begins in the nucleolus, where the ribosomal DNA (rDNA) is transcribed into a long pre-rRNA precursor (35S pre-rRNA in yeast) and involves the ordered assembly of the r-proteins with the pre-rRNA, which is concomitantly processed into the mature rRNA species [5][6][7][8] (Figure 1 and Box 1). These assembly and processing events are tightly coupled and occur within preribosomal particles (see Glossary) that travel, as maturation progresses, from the nucleus across nuclear pore complexes (NPCs) to the cytoplasm, where they are ultimately converted into translation-competent ribosomal subunits [5,[9][10][11][12][13] (Figure 2, Key Figure). Given the gargantuan complexity of this process, it is unsurprising that the assembly of eukaryotic ribosomes strictly requires the assistance of a plethora (>200) of mostly essential ribosome biogenesis factors, which are also called trans-acting or assembly factors [5,14,15].Our current knowledge has been mainly obtained by studying ribosome biogenesis in the yeast Saccharomyces cerevisiae. Research conducted in the 1970s defined the r-protein composition of ribosomes, revealed the major pre-rRNA processing intermediates, and uncovered the existence of the 90S, 43S, and 66S preribosomal particles. The following 25 years witnessed the identification of numerous biogenesis factors and attributed functional roles TrendsCryoelectron microscopy analyses of the 90S preribosome show that the biogenesis factors create a casting mold that encloses the nascent pre-40S subunit.Structures of nuclear pre-60S particles reveal that a...

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Section: Assembly Of the Lsumentioning

confidence: 99%

A Puzzle of Life: Crafting Ribosomal Subunits

Kressler

Hurt

Baßler

2017

Trends in Biochemical Sciences

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165

127

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“…It has been shown that karyopherins or chaperones interact with ribosomal proteins to maintain their solubility and also facilitate their loading into nascent ribosomal subunits (33)(34)(35)(36)(37)(38)(39)(40)(41)(42).…”

Section: Figure 2 the Function Of Bcp1 Is Tightly Connected With Manmentioning

confidence: 99%

“…Rrb1 has direct interaction with Rpl3 (uL3), and overexpression of Rrb1 increased the level and nuclear accumulation of Rpl3 (36). Syo1 facilitates coimport of Rpl5 (uL18) and Rpl11 (uL5) and chaperones 5S RNP assembly (33,38). Acl4 is a chaperone of Rpl4 (uL4) and accompanies Rpl4 from the cytoplasm to the loading onto the pre-60S in the nucleus (39,41).…”

Section: Bcp1 Is a Chaperone Of Rpl23 And Required To Maintain Thementioning

confidence: 99%

Bcp1 Is the Nuclear Chaperone of Rpl23 in Saccharomyces cerevisiae

Ting

Johnson

et al. 2017

Journal of Biological Chemistry

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Edited by Linda SpremulliEukaryotic ribosomes are composed of rRNAs and ribosomal proteins. Ribosomal proteins are translated in the cytoplasm and imported into the nucleus for assembly with the rRNAs. It has been shown that chaperones or karyopherins responsible for import can maintain the stability of ribosomal proteins by neutralizing unfavorable positive charges and thus facilitate their transports. Among 79 ribosomal proteins in yeast, only a few are identified with specific chaperones. Besides the classic role in maintaining protein stability, chaperones have additional roles in transport, chaperoning the assembly site, and dissociation of ribosomal proteins from karyopherins. Bcp1 has been shown to be necessary for the export of Mss4, a phosphatidylinositol 4-phosphate 5-kinase, and required for ribosome biogenesis. However, its specific function in ribosome biogenesis has not been described. Here, we show that Bcp1 dissociates Rpl23 from the karyopherins and associates with Rpl23 afterward. Loss of Bcp1 causes instability of Rpl23 and deficiency of 60S subunits. In summary, Bcp1 is a novel 60S biogenesis factor via chaperoning Rpl23 in the nucleus.The ribosome is a large macromolecular complex responsible for decoding cellular genetic information into proteins. There are two ribosomal subunits; in the eukaryotes, they are the (60S) large subunit and the small (40S) subunit, each composed of both rRNAs and ribosomal proteins. In eukaryotic cells, the assembly of ribosomes occurs in the nucleolus, a subcompartment of the nucleus devoted to ribosome biogenesis. rRNAs are transcribed by RNA polymerase I and III, and the initial assembly and processing events occur co-transcriptionally. The mRNAs of ribosomal proteins are transcribed in the nucleus by RNA polymerase II and translated in the cytoplasm. Consequently, the ribosomal proteins must be imported into the nucleus for assembly with the rRNAs. After ribosome assemblies have achieved a certain stage of maturation, export factors are loaded to direct these huge complexes to cross the nuclear membrane through the nuclear pore complexes (1-6). In the cytoplasm, ribosomes undergo additional steps in the maturation process; the trans-acting factors that are exported with nascent ribosomal subunits need to be stripped off, additional ribosomal proteins are added, and in the case of the 40S subunit, the final rRNA processing occurs (7,8). The synthesis of ribosomes requires the coordination of many non-ribosomal trans-acting factors at different stages for this pathway to be completed. About 200 trans-acting factors are involved in rRNA processing, rRNA folding, protein loading, and export. To date, more trans-acting factors have continued to be identified (7, 9, 10).BCP1 is an essential gene involved in the export of Mss4 (11), a phosphatidylinositol (PI) 2 4-phosphate 5-kinase that catalyzes the phosphorylation of PI4-phosphate and acts with the PI4-kinase, Stt4p, at the plasma membrane to generate PI4,5P 2 (12, 13). Phosphoinositols are critical small signal...

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“…4A,B; Leidig et al 2014). Notably, rRNA H84 engages in a native-like interaction with protein uL5 of the 5S RNP, indicating that it may serve as an initial docking site during assembly (Leidig et al 2014;Calviño et al 2015).…”

Section: The Architecture Of the Immature Central Protuberance In Nucmentioning

confidence: 99%

Mechanistic insight into eukaryotic 60S ribosomal subunit biogenesis by cryo-electron microscopy

Greber

2016

RNA

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Eukaryotic ribosomes, the protein-producing factories of the cell, are composed of four ribosomal RNA molecules and roughly 80 proteins. Their biogenesis is a complex process that involves more than 200 biogenesis factors that facilitate the production, modification, and assembly of ribosomal components and the structural transitions along the maturation pathways of the preribosomal particles. Here, I review recent structural and mechanistic insights into the biogenesis of the large ribosomal subunit that were furthered by cryo-electron microscopy of natively purified pre-60S particles and in vitro reconstituted ribosome assembly factor complexes. Combined with biochemical, genetic, and previous structural data, these structures have provided detailed insights into the assembly and maturation of the central protuberance of the 60S subunit, the network of biogenesis factors near the ribosomal tunnel exit, and the functional activation of the large ribosomal subunit during cytoplasmic maturation.

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Symportin 1 chaperones 5S RNP assembly during ribosome biogenesis by occupying an essential rRNA-binding site

Cited by 54 publications

References 30 publications

A Puzzle of Life: Crafting Ribosomal Subunits

A Puzzle of Life: Crafting Ribosomal Subunits

Bcp1 Is the Nuclear Chaperone of Rpl23 in Saccharomyces cerevisiae

Mechanistic insight into eukaryotic 60S ribosomal subunit biogenesis by cryo-electron microscopy

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