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- PDB-7r6k: State E2 nucleolar 60S ribosomal intermediate - Model for Noc2/No... -

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Entry
Database: PDB / ID: 7r6k
TitleState E2 nucleolar 60S ribosomal intermediate - Model for Noc2/Noc3 region
Components
  • (60S ribosomal protein ...) x 4
  • (Ribosome biogenesis protein ...) x 3
  • 25S rRNA
  • 25S rRNA (cytosine(2870)-C(5))-methyltransferase
  • 27S pre-rRNA (guanosine(2922)-2'-O)-methyltransferase
  • 60S ribosomal subunit assembly/export protein LOC1
  • 60S ribosome subunit biogenesis protein NIP7
  • Nucleolar complex protein 2
  • Nucleolar complex-associated protein 3
  • RRP17 isoform 1
  • rRNA-processing protein EBP2
KeywordsRIBOSOME / ribosome biogenesis / DEAD-box ATPases / methyltransferases / nucleolus
Function / homology
Function and homology information


25S rRNA (cytosine2870-C5)-methyltransferase / Noc1p-Noc2p complex / 27S pre-rRNA (guanosine2922-2'-O)-methyltransferase / Noc2p-Noc3p complex / rRNA (guanosine-2'-O-)-methyltransferase activity / nuclear division / exonucleolytic trimming to generate mature 5'-end of 5.8S rRNA from tricistronic rRNA transcript (SSU-rRNA, 5.8S rRNA, LSU-rRNA) / rRNA (uridine-2'-O-)-methyltransferase activity / endonucleolytic cleavage in ITS1 upstream of 5.8S rRNA from tricistronic rRNA transcript (SSU-rRNA, 5.8S rRNA, LSU-rRNA) / rRNA (cytosine-C5-)-methyltransferase activity ...25S rRNA (cytosine2870-C5)-methyltransferase / Noc1p-Noc2p complex / 27S pre-rRNA (guanosine2922-2'-O)-methyltransferase / Noc2p-Noc3p complex / rRNA (guanosine-2'-O-)-methyltransferase activity / nuclear division / exonucleolytic trimming to generate mature 5'-end of 5.8S rRNA from tricistronic rRNA transcript (SSU-rRNA, 5.8S rRNA, LSU-rRNA) / rRNA (uridine-2'-O-)-methyltransferase activity / endonucleolytic cleavage in ITS1 upstream of 5.8S rRNA from tricistronic rRNA transcript (SSU-rRNA, 5.8S rRNA, LSU-rRNA) / rRNA (cytosine-C5-)-methyltransferase activity / rRNA (guanine) methyltransferase activity / endonucleolytic cleavage in 5'-ETS of tricistronic rRNA transcript (SSU-rRNA, 5.8S rRNA, LSU-rRNA) / intracellular mRNA localization / endonucleolytic cleavage to generate mature 5'-end of SSU-rRNA from (SSU-rRNA, 5.8S rRNA, LSU-rRNA) / PeBoW complex / pre-replicative complex assembly involved in nuclear cell cycle DNA replication / nuclear pre-replicative complex / rRNA base methylation / rRNA primary transcript binding / protein folding chaperone complex / maturation of 5.8S rRNA from tricistronic rRNA transcript (SSU-rRNA, 5.8S rRNA, LSU-rRNA) / rRNA methylation / Major pathway of rRNA processing in the nucleolus and cytosol / SRP-dependent cotranslational protein targeting to membrane / GTP hydrolysis and joining of the 60S ribosomal subunit / Formation of a pool of free 40S subunits / Nonsense Mediated Decay (NMD) independent of the Exon Junction Complex (EJC) / Nonsense Mediated Decay (NMD) enhanced by the Exon Junction Complex (EJC) / preribosome, large subunit precursor / L13a-mediated translational silencing of Ceruloplasmin expression / DNA replication initiation / ribosomal large subunit export from nucleus / mRNA transport / endonucleolytic cleavage in ITS1 to separate SSU-rRNA from 5.8S rRNA and LSU-rRNA from tricistronic rRNA transcript (SSU-rRNA, 5.8S rRNA, LSU-rRNA) / ribonucleoprotein complex binding / maturation of LSU-rRNA from tricistronic rRNA transcript (SSU-rRNA, 5.8S rRNA, LSU-rRNA) / maturation of LSU-rRNA / ribosomal large subunit biogenesis / nuclear periphery / assembly of large subunit precursor of preribosome / ribosomal large subunit assembly / rRNA processing / large ribosomal subunit rRNA binding / ribosome biogenesis / cytoplasmic translation / 5S rRNA binding / cytosolic large ribosomal subunit / negative regulation of translation / structural constituent of ribosome / ribonucleoprotein complex / cell division / mRNA binding / chromatin binding / nucleolus / mitochondrion / DNA binding / RNA binding / nucleoplasm / identical protein binding / nucleus / cytosol / cytoplasm
Similarity search - Function
Nucleolar protein 12 / Nucleolar protein 12 (25kDa) / 60S ribosomal subunit assembly/export protein Loc1 / Nucleolar complex protein 2 / Noc2p family / Nucleolar complex-associated protein 3, N-terminal / Nucleolar complex-associated protein 3 / Nucleolar complex-associated protein / Ribosome biogenesis factor, NIP7 / RNA (C5-cytosine) methyltransferase, NOP2 ...Nucleolar protein 12 / Nucleolar protein 12 (25kDa) / 60S ribosomal subunit assembly/export protein Loc1 / Nucleolar complex protein 2 / Noc2p family / Nucleolar complex-associated protein 3, N-terminal / Nucleolar complex-associated protein 3 / Nucleolar complex-associated protein / Ribosome biogenesis factor, NIP7 / RNA (C5-cytosine) methyltransferase, NOP2 / UPF0113, pre-PUA domain / UPF0113 Pre-PUA domain / UPF0113, PUA domain / UPF0113 PUA domain / Ribosomal RNA small subunit methyltransferase F, N-terminal / N-terminal domain of 16S rRNA methyltransferase RsmF / Nop2p / Bacterial Fmu (Sun)/eukaryotic nucleolar NOL1/Nop2p, conserved site / NOL1/NOP2/sun family signature. / Ribosomal RNA methyltransferase, SPB1-like, C-terminal / Ribosomal RNA methyltransferase Spb1, domain of unknown function DUF3381 / AdoMet-dependent rRNA methyltransferase SPB1-like / Spb1 C-terminal domain / Ribosomal RNA methyltransferase Spb1, DUF3381 / Eukaryotic rRNA processing / Eukaryotic rRNA processing protein EBP2 / Ribosomal RNA large subunit methyltransferase E / Ribosome biogenesis protein BRX1 / CCAAT-binding factor / CBF/Mak21 family / : / BOP1, N-terminal domain / WD repeat BOP1/Erb1 / BOP1NT (NUC169) domain / BOP1NT (NUC169) domain / SAM-dependent methyltransferase RsmB/NOP2-type / RNA (C5-cytosine) methyltransferase / 16S rRNA methyltransferase RsmB/F / SAM-dependent MTase RsmB/NOP-type domain profile. / Putative RNA-binding Domain in PseudoUridine synthase and Archaeosine transglycosylase / PUA domain / PUA domain profile. / PUA domain superfamily / Ribosomal biogenesis NSA2 family / Brix domain / Brix domain / Brix domain profile. / Brix / PUA-like superfamily / Ribosomal protein L34e, conserved site / Ribosomal protein L34Ae / Ribosomal protein L34e / Ribosomal protein L36e / Ribosomal protein L36e domain superfamily / Ribosomal protein L36e / Ribosomal protein L7A/L8 / Ribosomal protein L34e signature. / Ribosomal protein L15e, conserved site / Ribosomal RNA methyltransferase, FtsJ domain / FtsJ-like methyltransferase / Ribosomal protein L36e signature. / Ribosomal_L15e / Ribosomal protein L15e / Ribosomal protein L15e core domain superfamily / Ribosomal L15 / Ribosomal protein S8e/ribosomal biogenesis NSA2 / Ribosomal protein S8e / Ribosomal protein L15e signature. / Ribosomal protein L7Ae conserved site / Ribosomal protein L7Ae signature. / Ribosomal protein L7Ae/L8/Nhp2 family / Ribosomal protein L7Ae/L30e/S12e/Gadd45 / Ribosomal protein L7Ae/L30e/S12e/Gadd45 family / 50S ribosomal protein L30e-like / Ribosomal protein L23/L15e core domain superfamily / Armadillo-type fold / WD40 repeat, conserved site / Trp-Asp (WD) repeats signature. / WD domain, G-beta repeat / WD40 repeats / WD40 repeat / Trp-Asp (WD) repeats profile. / Trp-Asp (WD) repeats circular profile. / WD40-repeat-containing domain superfamily / WD40/YVTN repeat-like-containing domain superfamily / S-adenosyl-L-methionine-dependent methyltransferase superfamily
Similarity search - Domain/homology
RNA / RNA (> 10) / RNA (> 100) / RRP17 isoform 1 / Ribosome biogenesis protein NSA2 / Large ribosomal subunit protein eL36A / Large ribosomal subunit protein eL15A / Large ribosomal subunit protein eL8A / 27S pre-rRNA (guanosine(2922)-2'-O)-methyltransferase / rRNA-processing protein EBP2 ...RNA / RNA (> 10) / RNA (> 100) / RRP17 isoform 1 / Ribosome biogenesis protein NSA2 / Large ribosomal subunit protein eL36A / Large ribosomal subunit protein eL15A / Large ribosomal subunit protein eL8A / 27S pre-rRNA (guanosine(2922)-2'-O)-methyltransferase / rRNA-processing protein EBP2 / Nucleolar complex protein 2 / 25S rRNA (cytosine(2870)-C(5))-methyltransferase / 60S ribosomal subunit assembly/export protein LOC1 / Large ribosomal subunit protein eL34A / Ribosome biogenesis protein ERB1 / Nucleolar complex-associated protein 3 / Ribosome biogenesis protein BRX1 / 60S ribosome subunit biogenesis protein NIP7
Similarity search - Component
Biological speciesSaccharomyces cerevisiae BY4741 (yeast)
MethodELECTRON MICROSCOPY / single particle reconstruction / cryo EM / Resolution: 3.17 Å
AuthorsCruz, V.E. / Sekulski, K. / Peddada, N. / Erzberger, J.P.
Funding support United States, 3items
OrganizationGrant numberCountry
National Institutes of Health/National Institute of General Medical Sciences (NIH/NIGMS)GM135617-01 United States
Cancer Prevention and Research Institute of Texas (CPRIT)RR150074 United States
Robert A. Welch FoundationI-1897 United States
CitationJournal: Nat Struct Mol Biol / Year: 2022
Title: Sequence-specific remodeling of a topologically complex RNP substrate by Spb4.
Authors: Victor Emmanuel Cruz / Kamil Sekulski / Nagesh Peddada / Carolin Sailer / Sahana Balasubramanian / Christine S Weirich / Florian Stengel / Jan P Erzberger /
Abstract: DEAD-box ATPases are ubiquitous enzymes essential in all aspects of RNA biology. However, the limited in vitro catalytic activities described for these enzymes are at odds with their complex cellular ...DEAD-box ATPases are ubiquitous enzymes essential in all aspects of RNA biology. However, the limited in vitro catalytic activities described for these enzymes are at odds with their complex cellular roles, most notably in driving large-scale RNA remodeling steps during the assembly of ribonucleoproteins (RNPs). We describe cryo-EM structures of 60S ribosomal biogenesis intermediates that reveal how context-specific RNA unwinding by the DEAD-box ATPase Spb4 results in extensive, sequence-specific remodeling of rRNA secondary structure. Multiple cis and trans interactions stabilize Spb4 in a post-catalytic, high-energy intermediate that drives the organization of the three-way junction at the base of rRNA domain IV. This mechanism explains how limited strand separation by DEAD-box ATPases is leveraged to provide non-equilibrium directionality and ensure efficient and accurate RNP assembly.
History
DepositionJun 22, 2021Deposition site: RCSB / Processing site: RCSB
Revision 1.0Nov 9, 2022Provider: repository / Type: Initial release
Revision 1.1Dec 14, 2022Group: Database references / Refinement description
Category: citation / citation_author / pdbx_initial_refinement_model
Item: _citation.country / _citation.journal_abbrev ..._citation.country / _citation.journal_abbrev / _citation.journal_id_CSD / _citation.journal_id_ISSN / _citation.pdbx_database_id_DOI / _citation.title / _citation.year / _citation_author.identifier_ORCID
Revision 1.2Dec 21, 2022Group: Database references / Category: citation / citation_author
Item: _citation.pdbx_database_id_PubMed / _citation.title / _citation_author.identifier_ORCID
Revision 1.3Dec 28, 2022Group: Database references / Category: citation / citation_author
Item: _citation.journal_volume / _citation.page_first ..._citation.journal_volume / _citation.page_first / _citation.page_last / _citation_author.identifier_ORCID

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Structure visualization

Structure viewerMolecule:
MolmilJmol/JSmol

Downloads & links

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Assembly

Deposited unit
1: 25S rRNA
7: 60S ribosomal subunit assembly/export protein LOC1
8: Nucleolar complex protein 2
A: Ribosome biogenesis protein BRX1
G: 60S ribosomal protein L8-A
I: Nucleolar complex-associated protein 3
J: rRNA-processing protein EBP2
N: 60S ribosomal protein L15-A
g: 60S ribosomal protein L34-A
i: 60S ribosomal protein L36-A
l: 60S ribosome subunit biogenesis protein NIP7
m: Ribosome biogenesis protein ERB1
q: 25S rRNA (cytosine(2870)-C(5))-methyltransferase
r: Ribosome biogenesis protein NSA2
w: 27S pre-rRNA (guanosine(2922)-2'-O)-methyltransferase
5: RRP17 isoform 1


Theoretical massNumber of molelcules
Total (without water)700,93616
Polymers700,93616
Non-polymers00
Water0
1


  • Idetical with deposited unit
  • defined by author
TypeNameSymmetry operationNumber
identity operation1_5551
Buried area56690 Å2
ΔGint-294 kcal/mol
Surface area131880 Å2

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Components

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Protein , 7 types, 7 molecules 78IJlqw

#2: Protein 60S ribosomal subunit assembly/export protein LOC1 / / Localization of ASH1 mRNA protein 1


Mass: 23652.645 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: P43586
#3: Protein Nucleolar complex protein 2


Mass: 81719.289 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: P39744
#6: Protein Nucleolar complex-associated protein 3


Mass: 75689.008 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: Q07896
#7: Protein rRNA-processing protein EBP2 / EBNA1-binding protein homolog


Mass: 49842.613 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: P36049
#11: Protein 60S ribosome subunit biogenesis protein NIP7 / Nuclear import protein 7


Mass: 20411.699 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: Q08962
#13: Protein 25S rRNA (cytosine(2870)-C(5))-methyltransferase / Nucleolar protein 2


Mass: 69912.164 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741
References: UniProt: P40991, 25S rRNA (cytosine2870-C5)-methyltransferase
#15: Protein 27S pre-rRNA (guanosine(2922)-2'-O)-methyltransferase / 2'-O-ribose RNA methyltransferase SPB1 / AdoMet-dependent rRNA methyltransferase SPB1 / S-adenosyl- ...2'-O-ribose RNA methyltransferase SPB1 / AdoMet-dependent rRNA methyltransferase SPB1 / S-adenosyl-L-methionine-dependent methyltransferase / Suppressor of PAB1 protein 1


Mass: 96656.172 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741
References: UniProt: P25582, 27S pre-rRNA (guanosine2922-2'-O)-methyltransferase

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Ribosome biogenesis protein ... , 3 types, 3 molecules Amr

#4: Protein Ribosome biogenesis protein BRX1 /


Mass: 33585.414 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: Q08235
#12: Protein Ribosome biogenesis protein ERB1 / / Eukaryotic ribosome biogenesis protein 1


Mass: 91830.609 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: Q04660
#14: Protein Ribosome biogenesis protein NSA2 / / NOP7-associated protein 2


Mass: 29786.783 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: A6ZR80

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60S ribosomal protein ... , 4 types, 4 molecules GNgi

#5: Protein 60S ribosomal protein L8-A / Ribosome / L4 / L4-2 / L7a-1 / Large ribosomal subunit protein eL8-A / Maintenance of killer protein 7 / RP6 / YL5


Mass: 28175.820 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: P17076
#8: Protein 60S ribosomal protein L15-A / Ribosome / L13 / Large ribosomal subunit protein eL15-A / RP15R / YL10 / YP18


Mass: 24482.357 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: P05748
#9: Protein 60S ribosomal protein L34-A / Ribosome / Large ribosomal subunit protein eL34-A


Mass: 13673.196 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: P87262
#10: Protein 60S ribosomal protein L36-A / Ribosome / L39 / Large ribosomal subunit protein eL36-A / YL39


Mass: 11151.259 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: P05745

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RNA chain / Protein/peptide , 2 types, 2 molecules 15

#16: Protein/peptide RRP17 isoform 1


Mass: 1082.234 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741 / References: UniProt: A0A6A5Q2X9
#1: RNA chain 25S rRNA


Mass: 49285.230 Da / Num. of mol.: 1 / Source method: isolated from a natural source / Source: (natural) Saccharomyces cerevisiae BY4741 (yeast) / Strain: BY4741

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Experimental details

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Experiment

ExperimentMethod: ELECTRON MICROSCOPY
EM experimentAggregation state: PARTICLE / 3D reconstruction method: single particle reconstruction

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Sample preparation

ComponentName: Nucleolar 60S intermediate purified with tags on Ytm1 and Spb4
Type: RIBOSOME / Entity ID: all / Source: NATURAL
Molecular weightValue: 3.3 MDa / Experimental value: NO
Source (natural)Organism: Saccharomyces cerevisiae BY4741 (yeast)
Buffer solutionpH: 8
Buffer component
IDConc.NameFormulaBuffer-ID
150 mMBis-Tris-PropaneCH2[CH2NHC9CH20H03]21
2150 mMSodium ChlorideNaClSodium chloride1
310 mMMagnesium ChlorideMgCl21
41 mMTCEPC9H15O6PHCl1
50.01 % (w/v)NP-401
SpecimenConc.: 0.45 mg/ml / Embedding applied: NO / Shadowing applied: NO / Staining applied: NO / Vitrification applied: YES
Specimen supportGrid material: COPPER / Grid mesh size: 300 divisions/in. / Grid type: Quantifoil R2/2
VitrificationInstrument: FEI VITROBOT MARK IV / Cryogen name: ETHANE / Humidity: 100 % / Chamber temperature: 277 K

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Electron microscopy imaging

Experimental equipment
Model: Titan Krios / Image courtesy: FEI Company
MicroscopyModel: FEI TITAN KRIOS
Electron gunElectron source: FIELD EMISSION GUN / Accelerating voltage: 300 kV / Illumination mode: FLOOD BEAM
Electron lensMode: BRIGHT FIELDBright-field microscopy / Nominal magnification: 81000 X / Nominal defocus max: 2200 nm / Nominal defocus min: 900 nm / C2 aperture diameter: 70 µm / Alignment procedure: COMA FREE
Specimen holderCryogen: NITROGEN / Specimen holder model: FEI TITAN KRIOS AUTOGRID HOLDER
Image recordingAverage exposure time: 0.05 sec. / Electron dose: 1.2 e/Å2 / Film or detector model: GATAN K3 (6k x 4k) / Num. of grids imaged: 1 / Num. of real images: 4523

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Processing

Software
NameVersionClassification
phenix.real_space_refine1.19.2_4158refinement
PHENIX1.19.2_4158refinement
EM software
IDNameCategory
2SerialEMimage acquisition
4GctfCTF correction
7Cootmodel fitting
9RELIONinitial Euler assignment
10RELIONfinal Euler assignment
12RELION3D reconstruction
13PHENIXmodel refinement
CTF correctionType: NONE
Particle selectionNum. of particles selected: 825096
SymmetryPoint symmetry: C1 (asymmetric)
3D reconstructionResolution: 3.17 Å / Resolution method: FSC 0.143 CUT-OFF / Num. of particles: 198000 / Algorithm: FOURIER SPACE / Num. of class averages: 1 / Symmetry type: POINT
Atomic model buildingProtocol: AB INITIO MODEL / Space: REAL
Atomic model buildingPDB-ID: 6ELZ

6elz

RefinementCross valid method: NONE
Stereochemistry target values: GeoStd + Monomer Library + CDL v1.2
Displacement parametersBiso mean: 47.33 Å2
Refine LS restraints
Refine-IDTypeDev idealNumber
ELECTRON MICROSCOPYf_bond_d0.002621182
ELECTRON MICROSCOPYf_angle_d0.524329210
ELECTRON MICROSCOPYf_chiral_restr0.03783421
ELECTRON MICROSCOPYf_plane_restr0.00423160
ELECTRON MICROSCOPYf_dihedral_angle_d14.69868562

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