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Structure paper

TitlePrinciples of human pre-60 biogenesis.
Journal, issue, pagesScience, Vol. 381, Issue 6653, Page eadh3892, Year 2023
Publish dateJul 7, 2023
AuthorsArnaud Vanden Broeck / Sebastian Klinge /
PubMed AbstractDuring the early stages of human large ribosomal subunit (60) biogenesis, an ensemble of assembly factors establishes and fine-tunes the essential RNA functional centers of pre-60 particles by an ...During the early stages of human large ribosomal subunit (60) biogenesis, an ensemble of assembly factors establishes and fine-tunes the essential RNA functional centers of pre-60 particles by an unknown mechanism. Here, we report a series of cryo-electron microscopy structures of human nucleolar and nuclear pre-60 assembly intermediates at resolutions of 2.5 to 3.2 angstroms. These structures show how protein interaction hubs tether assembly factor complexes to nucleolar particles and how guanosine triphosphatases and adenosine triphosphatase couple irreversible nucleotide hydrolysis steps to the installation of functional centers. Nuclear stages highlight how a conserved RNA-processing complex, the rixosome, couples large-scale RNA conformational changes with pre-ribosomal RNA processing by the RNA degradation machinery. Our ensemble of human pre-60 particles provides a rich foundation with which to elucidate the molecular principles of ribosome formation.
External linksScience / PubMed:37410842
MethodsEM (single particle)
Resolution2.33 - 3.75 Å
Structure data

EMDB-29104: Human nucleolar pre-60S ribosomal subunit (State A1) - Overall map
Method: EM (single particle) / Resolution: 3.0 Å

EMDB-29105: Human nucleolar pre-60S ribosomal subunit (State A2) - Overall map
Method: EM (single particle) / Resolution: 2.85 Å

EMDB-29106: Human nucleolar pre-60S ribosomal subunit (State B1) - Overall map
Method: EM (single particle) / Resolution: 3.09 Å

EMDB-29107: Human nucleolar pre-60S ribosomal subunit (State B2) - Overall map
Method: EM (single particle) / Resolution: 3.06 Å

EMDB-29108: Human nucleolar pre-60S ribosomal subunit (State C1) - Overall map
Method: EM (single particle) / Resolution: 2.98 Å

EMDB-29109: Human nucleolar pre-60S ribosomal subunit (State C2) - Overall map
Method: EM (single particle) / Resolution: 3.03 Å

EMDB-29110: Human nucleolar pre-60S ribosomal subunit (State D1) - Overall map
Method: EM (single particle) / Resolution: 2.6 Å

EMDB-29111: Human nucleolar pre-60S ribosomal subunit (State D2) - Overall map
Method: EM (single particle) / Resolution: 2.63 Å

EMDB-29112: Human nucleolar pre-60S ribosomal subunit (State E) - Overall map
Method: EM (single particle) / Resolution: 2.75 Å

EMDB-29113: Human nucleolar pre-60S ribosomal subunit (State F) - Overall map
Method: EM (single particle) / Resolution: 2.84 Å

EMDB-29114: Human nucleolar pre-60S ribosomal subunit (State G) - Overall map
Method: EM (single particle) / Resolution: 3.19 Å

EMDB-29115: Human nucleolar pre-60S ribosomal subunit (State H) - Overall map
Method: EM (single particle) / Resolution: 2.96 Å

EMDB-29116: Human nuclear pre-60S ribosomal subunit (State I1) - Overall map
Method: EM (single particle) / Resolution: 2.71 Å

EMDB-29117: Human nuclear pre-60S ribosomal subunit (State I2) - Overall map
Method: EM (single particle) / Resolution: 2.53 Å

EMDB-29118: Human nuclear pre-60S ribosomal subunit (State I3) - Overall map
Method: EM (single particle) / Resolution: 3.05 Å

EMDB-29119: Human nuclear pre-60S ribosomal subunit (State J1) - Overall map
Method: EM (single particle) / Resolution: 2.76 Å

EMDB-29120: Human nuclear pre-60S ribosomal subunit (State J2) - Overall map
Method: EM (single particle) / Resolution: 2.66 Å

EMDB-29121: Human nuclear pre-60S ribosomal subunit (State J3) - Overall map
Method: EM (single particle) / Resolution: 2.99 Å

EMDB-29122: Human nuclear pre-60S ribosomal subunit (State K1) - Overall map
Method: EM (single particle) / Resolution: 2.84 Å

EMDB-29123: Human nuclear pre-60S ribosomal subunit (State K2) - Overall map
Method: EM (single particle) / Resolution: 2.64 Å

EMDB-29124: Human nuclear pre-60S ribosomal subunit (State K3) - Overall map
Method: EM (single particle) / Resolution: 3.05 Å

EMDB-29125: Human nuclear pre-60S ribosomal subunit (State L1) - Overall map
Method: EM (single particle) / Resolution: 2.72 Å

EMDB-29126: Human nuclear pre-60S ribosomal subunit (State L2) - Overall map
Method: EM (single particle) / Resolution: 2.49 Å

EMDB-29127: Human nuclear pre-60S ribosomal subunit (State L3) - Overall map
Method: EM (single particle) / Resolution: 2.83 Å

EMDB-29128: Human nucleolar pre-60S ribosomal subunit (States A1,A2 & B1,B2 combined) - Domain VI root helix focused map
Method: EM (single particle) / Resolution: 3.46 Å

EMDB-29129: Human nucleolar pre-60S ribosomal subunit (States A1,A2 & B1,B2 combined) - Domain VI helix 96 focused map
Method: EM (single particle) / Resolution: 3.07 Å

EMDB-29130: Human nucleolar pre-60S ribosomal subunit (State A1) - Domain I focused map
Method: EM (single particle) / Resolution: 2.87 Å

EMDB-29131: Human nucleolar pre-60S ribosomal subunit (State A1) - Domain II focused map
Method: EM (single particle) / Resolution: 2.87 Å

EMDB-29132: Human nucleolar pre-60S ribosomal subunit (State A2) - Domain I focused map
Method: EM (single particle) / Resolution: 2.73 Å

EMDB-29133: Human nucleolar pre-60S ribosomal subunit (State A2) - Domain II focused map
Method: EM (single particle) / Resolution: 2.73 Å

EMDB-29134: Human nucleolar pre-60S ribosomal subunit (States A1,A2 combined) - Domain VI focused map
Method: EM (single particle) / Resolution: 3.05 Å

EMDB-29135: Human nucleolar pre-60S ribosomal subunit (States A1,A2 combined) - ITS2 module focused map
Method: EM (single particle) / Resolution: 2.87 Å

EMDB-29136: Human nucleolar pre-60S ribosomal subunit (State B1) - Domain I focused map
Method: EM (single particle) / Resolution: 2.93 Å

EMDB-29137: Human nucleolar pre-60S ribosomal subunit (State B1) - Domain II focused map
Method: EM (single particle) / Resolution: 2.94 Å

EMDB-29138: Human nucleolar pre-60S ribosomal subunit (State B2) - Domain I focused map
Method: EM (single particle) / Resolution: 2.87 Å

EMDB-29139: Human nucleolar pre-60S ribosomal subunit (State B2) - Domain II focused map
Method: EM (single particle) / Resolution: 2.89 Å

EMDB-29140: Human nucleolar pre-60S ribosomal subunit (States B1,B2 combined) - ITS2 module focused map
Method: EM (single particle) / Resolution: 3.08 Å

EMDB-29141: Human nucleolar pre-60S ribosomal subunit (States B1,B2 combined) - Domain VI focused map
Method: EM (single particle) / Resolution: 3.31 Å

EMDB-29142: Human nucleolar pre-60S ribosomal subunit (States B1,B2 combined) - Domain V & GTPB4 focused map
Method: EM (single particle) / Resolution: 3.09 Å

EMDB-29143: Human nucleolar pre-60S ribosomal subunit (State C1) - Domain I focused map
Method: EM (single particle) / Resolution: 2.83 Å

EMDB-29144: Human nucleolar pre-60S ribosomal subunit (State C1) - Domain II focused map
Method: EM (single particle) / Resolution: 2.85 Å

EMDB-29145: Human nucleolar pre-60S ribosomal subunit (State C2) - Domain I focused map
Method: EM (single particle) / Resolution: 2.82 Å

EMDB-29146: Human nucleolar pre-60S ribosomal subunit (State C2) - Domain II focused map
Method: EM (single particle) / Resolution: 2.86 Å

EMDB-29147: Human nucleolar pre-60S ribosomal subunit (States C1,C2 combined) - ITS2 module focused map
Method: EM (single particle) / Resolution: 3.02 Å

EMDB-29148: Human nucleolar pre-60S ribosomal subunit (States C1,C2 combined) - Domains V-VI focused map
Method: EM (single particle) / Resolution: 2.77 Å

EMDB-29149: Human nucleolar pre-60S ribosomal subunit (States C1,C2 combined) - DDX54 focused map
Method: EM (single particle) / Resolution: 2.97 Å

EMDB-29150: Human nucleolar pre-60S ribosomal subunit (States C1,C2 combined) - L1 stalk focused map
Method: EM (single particle) / Resolution: 3.61 Å

EMDB-29151: Human nucleolar pre-60S ribosomal subunit (States A-F combined) - uL15 focused map
Method: EM (single particle) / Resolution: 2.78 Å

EMDB-29152: Human nucleolar pre-60S ribosomal subunit (State D1) - Domain I focused map
Method: EM (single particle) / Resolution: 2.48 Å

EMDB-29153: Human nucleolar pre-60S ribosomal subunit (State D1), Domain II focused map
Method: EM (single particle) / Resolution: 2.46 Å

EMDB-29154: Human nucleolar pre-60S ribosomal subunit (State D1) - Domains V-VI focused map
Method: EM (single particle) / Resolution: 2.5 Å

EMDB-29155: Human nucleolar pre-60S ribosomal subunit (State D1) - GNL3 focused map
Method: EM (single particle) / Resolution: 2.67 Å

EMDB-29156: Human nucleolar pre-60S ribosomal subunit (State D2) - Domain I focused map
Method: EM (single particle) / Resolution: 2.49 Å

EMDB-29157: Human nucleolar pre-60S ribosomal subunit (State D2) - Domain II focused map
Method: EM (single particle) / Resolution: 2.5 Å

EMDB-29158: Human nucleolar pre-60S ribosomal subunit (State D2) - Domains V-VI focused map
Method: EM (single particle) / Resolution: 2.6 Å

EMDB-29159: Human nucleolar pre-60S ribosomal subunit (States D1,D2 combined) - RRS1 focused map
Method: EM (single particle) / Resolution: 2.33 Å

EMDB-29160: Human nucleolar pre-60S ribosomal subunit (States D1,D2 combined) - ITS2 module focused map
Method: EM (single particle) / Resolution: 2.62 Å

EMDB-29161: Human nucleolar pre-60S ribosomal subunit (States D1,D2 combined) - Inter-subunit side focused map
Method: EM (single particle) / Resolution: 2.67 Å

EMDB-29162: Human nucleolar pre-60S ribosomal subunit (States D1,D2 combined) - DDX54 focused map
Method: EM (single particle) / Resolution: 2.59 Å

EMDB-29163: Human nucleolar pre-60S ribosomal subunit (States D1,D2 combined) - L1 stalk focused map
Method: EM (single particle) / Resolution: 2.78 Å

EMDB-29164: Human nucleolar pre-60S ribosomal subunit (States D1,D2 combined) - NOC3L & FTSJ3 focused map
Method: EM (single particle) / Resolution: 3.19 Å

EMDB-29165: Human nucleolar pre-60S ribosomal subunit (States D1,D2 combined) - NOC2L focused map
Method: EM (single particle) / Resolution: 3.08 Å

EMDB-29166: Human nucleolar pre-60S ribosomal subunit (State E) - Domain I focused map
Method: EM (single particle) / Resolution: 2.58 Å

EMDB-29167: Human nucleolar pre-60S ribosomal subunit (State E) - Domain II focused map
Method: EM (single particle) / Resolution: 2.63 Å

EMDB-29168: Human nucleolar pre-60S ribosomal subunit (State E) - ITS2 module focused map
Method: EM (single particle) / Resolution: 2.97 Å

EMDB-29169: Human nucleolar pre-60S ribosomal subunit (State F) - PeBoW-WDR55 focused map
Method: EM (single particle) / Resolution: 3.04 Å

EMDB-29170: Human nucleolar pre-60S ribosomal subunit (State F) - PeBoW complex focused map
Method: EM (single particle) / Resolution: 3.06 Å

EMDB-29171: Human nucleolar pre-60S ribosomal subunit (State F) - WDR55 focused map
Method: EM (single particle) / Resolution: 3.5 Å

EMDB-29173: Human nucleolar pre-60S ribosomal subunit (State F) - Domain III focused map
Method: EM (single particle) / Resolution: 2.84 Å

EMDB-29174: Human nucleolar pre-60S ribosomal subunit (State F) - ITS2 module focused map
Method: EM (single particle) / Resolution: 2.91 Å

EMDB-29175: Human nucleolar pre-60S ribosomal subunit (State F) - Domain I focused map
Method: EM (single particle) / Resolution: 2.71 Å

EMDB-29176: Human nucleolar pre-60S ribosomal subunit (State F) - Domain II focused map
Method: EM (single particle) / Resolution: 2.68 Å

EMDB-29177: Human nucleolar pre-60S ribosomal subunit (States E,F combined) - Inter-subunit side focused map
Method: EM (single particle) / Resolution: 2.86 Å

EMDB-29178: Human nucleolar pre-60S ribosomal subunit (States E,F combined) - DDX54 focused map
Method: EM (single particle) / Resolution: 2.79 Å

EMDB-29179: Human nucleolar pre-60S ribosomal subunit (States E,F combined) - L1 stalk focused map
Method: EM (single particle) / Resolution: 2.92 Å

EMDB-29180: Human nucleolar pre-60S ribosomal subunit (States E,F combined) - NOC3L focused map
Method: EM (single particle) / Resolution: 3.07 Å

EMDB-29181: Human nucleolar pre-60S ribosomal subunit (States E,F combined) - Domain VI focused map
Method: EM (single particle) / Resolution: 2.58 Å

EMDB-29182: Human nucleolar pre-60S ribosomal subunit (States E,F combined) - DDX18 focused map
Method: EM (single particle) / Resolution: 2.56 Å

EMDB-29183: Human nucleolar pre-60S ribosomal subunit (States E,F combined) - Domain V focused map
Method: EM (single particle) / Resolution: 2.58 Å

EMDB-29184: Human nucleolar pre-60S ribosomal subunit (States E,F combined) - RRS1 focused map
Method: EM (single particle) / Resolution: 2.61 Å

EMDB-29185: Human nucleolar pre-60S ribosomal subunit (States E,F combined) - NOC2L focused map
Method: EM (single particle) / Resolution: 3.75 Å

EMDB-29186: Human nucleolar pre-60S ribosomal subunit (State G) - ITS2 module focused map
Method: EM (single particle) / Resolution: 3.35 Å

EMDB-29187: Human nucleolar pre-60S ribosomal subunit (State G) - Domain I focused map
Method: EM (single particle) / Resolution: 3.06 Å

EMDB-29188: Human nucleolar pre-60S ribosomal subunit (State G) - Domain II focused map
Method: EM (single particle) / Resolution: 3.07 Å

EMDB-29189: Human nucleolar pre-60S ribosomal subunit (State G) - Domains V-VI focused map
Method: EM (single particle) / Resolution: 3.13 Å

EMDB-29192: Human nucleolar pre-60S ribosomal subunit (State G) - Domain IV focused map
Method: EM (single particle) / Resolution: 3.1 Å

EMDB-29193: Human nucleolar pre-60S ribosomal subunit (State H) - 5S RNP focused map
Method: EM (single particle) / Resolution: 2.88 Å

EMDB-29194: Human nucleolar pre-60S ribosomal subunit (State H) - Domains V-VI focused map
Method: EM (single particle) / Resolution: 3.0 Å

EMDB-29195: Human nuclear pre-60S ribosomal subunit (States I1,I2,I3 combined) - Central protuberance focused map
Method: EM (single particle) / Resolution: 2.67 Å

EMDB-29196: Human nuclear pre-60S ribosomal subunit (States I1,I2,I3 combined) - TEX10 focused map
Method: EM (single particle) / Resolution: 2.99 Å

EMDB-29197: Human nuclear pre-60S ribosomal subunit (States I1,I2,I3 combined) - Rix1 complex focused map
Method: EM (single particle) / Resolution: 2.87 Å

EMDB-29198: Human nuclear pre-60S ribosomal subunit (States I1,J1,K1,L1 combined) - ITS2 module focused map
Method: EM (single particle) / Resolution: 2.47 Å

EMDB-29199: Human nuclear pre-60S ribosomal subunit (States I2,J2,K2,L2 combined) - ITS2 module focused map
Method: EM (single particle) / Resolution: 2.39 Å

EMDB-29200: Human nuclear pre-60S ribosomal subunit (States J1,J2,J3 combined) - Central protuberance focused map
Method: EM (single particle) / Resolution: 2.52 Å

EMDB-29201: Human nuclear pre-60S ribosomal subunit (States J1,J2,J3 combined) - Domain V focused map
Method: EM (single particle) / Resolution: 2.59 Å

EMDB-29202: Human nuclear pre-60S ribosomal subunit (States K1,K2,K3 combined) - Central protuberance focused map
Method: EM (single particle) / Resolution: 2.51 Å

EMDB-29204: Human nuclear pre-60S ribosomal subunit (States K1,K2,K3 combined) - Domain V focused map
Method: EM (single particle) / Resolution: 2.58 Å

EMDB-29205: Human nuclear pre-60S ribosomal subunit (States L1,L2,L3 combined) - Central protuberance focused map
Method: EM (single particle) / Resolution: 2.45 Å

EMDB-29206: Human nuclear pre-60S ribosomal subunit (States L1,L2,L3 combined) - Domain V focused map
Method: EM (single particle) / Resolution: 2.52 Å

EMDB-29252: Human nucleolar pre-60S ribosomal subunit (State A1) - Composite map
PDB-8fkp: Human nucleolar pre-60S ribosomal subunit (State A1)
Method: EM (single particle) / Resolution: 2.85 Å

EMDB-29253: Human nucleolar pre-60S ribosomal subunit (State A2) - Composite map
PDB-8fkq: Human nucleolar pre-60S ribosomal subunit (State A2)
Method: EM (single particle) / Resolution: 2.76 Å

EMDB-29254: Human nucleolar pre-60S ribosomal subunit (State B1) - Composite map
PDB-8fkr: Human nucleolar pre-60S ribosomal subunit (State B1)
Method: EM (single particle) / Resolution: 2.89 Å

EMDB-29255: Human nucleolar pre-60S ribosomal subunit (State B2) - Composite map
PDB-8fks: Human nucleolar pre-60S ribosomal subunit (State B2)
Method: EM (single particle) / Resolution: 2.88 Å

EMDB-29256: Human nucleolar pre-60S ribosomal subunit (State C1) - Composite map
PDB-8fkt: Human nucleolar pre-60S ribosomal subunit (State C1)
Method: EM (single particle) / Resolution: 2.81 Å

EMDB-29257: Human nucleolar pre-60S ribosomal subunit (State C2) - Composite map
PDB-8fku: Human nucleolar pre-60S ribosomal subunit (State C2)
Method: EM (single particle) / Resolution: 2.82 Å

EMDB-29258: Human nucleolar pre-60S ribosomal subunit (State D1) - Composite map
PDB-8fkv: Human nucleolar pre-60S ribosomal subunit (State D1)
Method: EM (single particle) / Resolution: 2.47 Å

EMDB-29259: Human nucleolar pre-60S ribosomal subunit (State D2) - Composite map
PDB-8fkw: Human nucleolar pre-60S ribosomal subunit (State D2)
Method: EM (single particle) / Resolution: 2.5 Å

EMDB-29260: Human nucleolar pre-60S ribosomal subunit (State E) - Composite map
PDB-8fkx: Human nucleolar pre-60S ribosomal subunit (State E)
Method: EM (single particle) / Resolution: 2.59 Å

EMDB-29261: Human nucleolar pre-60S ribosomal subunit (State F) - Composite map
PDB-8fky: Human nucleolar pre-60S ribosomal subunit (State F)
Method: EM (single particle) / Resolution: 2.67 Å

EMDB-29262: Human nucleolar pre-60S ribosomal subunit (State G) - Composite map
PDB-8fkz: Human nucleolar pre-60S ribosomal subunit (State G)
Method: EM (single particle) / Resolution: 3.04 Å

EMDB-29263: Human nucleolar pre-60S ribosomal subunit (State H) - Composite map
PDB-8fl0: Human nucleolar pre-60S ribosomal subunit (State H)
Method: EM (single particle) / Resolution: 2.91 Å

EMDB-29265: Human nuclear pre-60S ribosomal subunit (State I1) - Composite map
PDB-8fl2: Human nuclear pre-60S ribosomal subunit (State I1)
Method: EM (single particle) / Resolution: 2.67 Å

EMDB-29266: Human nuclear pre-60S ribosomal subunit (State I2) - Composite map
PDB-8fl3: Human nuclear pre-60S ribosomal subunit (State I2)
Method: EM (single particle) / Resolution: 2.53 Å

EMDB-29267: Human nuclear pre-60S ribosomal subunit (State I3) - Composite map
PDB-8fl4: Human nuclear pre-60S ribosomal subunit (State I3)
Method: EM (single particle) / Resolution: 2.89 Å

EMDB-29268: Human nuclear pre-60S ribosomal subunit (State J1) - Composite map
PDB-8fl6: Human nuclear pre-60S ribosomal subunit (State J1)
Method: EM (single particle) / Resolution: 2.62 Å

EMDB-29269: Human nuclear pre-60S ribosomal subunit (State J2) - Composite map
PDB-8fl7: Human nuclear pre-60S ribosomal subunit (State J2)
Method: EM (single particle) / Resolution: 2.55 Å

EMDB-29271: Human nuclear pre-60S ribosomal subunit (State J3) - Composite map
PDB-8fl9: Human nuclear pre-60S ribosomal subunit (State J3)
Method: EM (single particle) / Resolution: 2.75 Å

EMDB-29272: Human nuclear pre-60S ribosomal subunit (State K1) - Composite map
PDB-8fla: Human nuclear pre-60S ribosomal subunit (State K1)
Method: EM (single particle) / Resolution: 2.63 Å

EMDB-29273: Human nuclear pre-60S ribosomal subunit (State K2) - Composite map
PDB-8flb: Human nuclear pre-60S ribosomal subunit (State K2)
Method: EM (single particle) / Resolution: 2.55 Å

EMDB-29274: Human nuclear pre-60S ribosomal subunit (State K3) - Composite map
PDB-8flc: Human nuclear pre-60S ribosomal subunit (State K3)
Method: EM (single particle) / Resolution: 2.76 Å

EMDB-29275: Human nuclear pre-60S ribosomal subunit (State L1) - Composite map
PDB-8fld: Human nuclear pre-60S ribosomal subunit (State L1)
Method: EM (single particle) / Resolution: 2.58 Å

EMDB-29276: Human nuclear pre-60S ribosomal subunit (State L2) - Composite map
PDB-8fle: Human nuclear pre-60S ribosomal subunit (State L2)
Method: EM (single particle) / Resolution: 2.48 Å

EMDB-29277: Human nuclear pre-60S ribosomal subunit (State L3) - Composite map
PDB-8flf: Human nuclear pre-60S ribosomal subunit (State L3)
Method: EM (single particle) / Resolution: 2.65 Å

Chemicals

ChemComp-MG:
Unknown entry

ChemComp-ZN:
Unknown entry

ChemComp-SF4:
IRON/SULFUR CLUSTER

ChemComp-GDP:
GUANOSINE-5'-DIPHOSPHATE / GDP, energy-carrying molecule*YM

ChemComp-K:
Unknown entry

ChemComp-ADP:
ADENOSINE-5'-DIPHOSPHATE / ADP, energy-carrying molecule*YM

ChemComp-GTP:
GUANOSINE-5'-TRIPHOSPHATE / GTP, energy-carrying molecule*YM

Source
  • homo sapiens (human)
  • human (human)
KeywordsRIBOSOME / Pre-60S ribosomal subunit / Assembly intermediate / Nucleoprotein complex

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