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Structure paper

Title	Principles of human pre-60 biogenesis.
Journal, issue, pages	Science, Vol. 381, Issue 6653, Page eadh3892, Year 2023
Publish date	Jul 7, 2023
Authors	Arnaud Vanden Broeck / Sebastian Klinge /
PubMed Abstract	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 ...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 links	Science / PubMed:37410842
Methods	EM (single particle)
Resolution	2.33 - 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 29252 8fkp 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 29253 8fkq 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 29254 8fkr 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 29255 8fks 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 29256 8fkt 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 29257 8fku 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 29258 8fkv 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 29259 8fkw 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 29260 8fkx 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 29261 8fky 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 29262 8fkz 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 29263 8fl0 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 29265 8fl2 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 29266 8fl3 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 29267 8fl4 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 29268 8fl6 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 29269 8fl7 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 29271 8fl9 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 29272 8fla 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 29273 8flb 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 29274 8flc 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 29275 8fld 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 29276 8fle 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 29277 8flf 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 / Iron–sulfur cluster ChemComp-GDP: GUANOSINE-5'-DIPHOSPHATE / GDP, energy-carrying moleculeYM / Guanosine diphosphate ChemComp-K: Unknown entry ChemComp-ADP: ADENOSINE-5'-DIPHOSPHATE / ADP, energy-carrying moleculeYM / Adenosine diphosphate ChemComp-GTP: GUANOSINE-5'-TRIPHOSPHATE / GTP, energy-carrying molecule*YM / Guanosine triphosphate
Source	homo sapiens (human) human (human)
Keywords	RIBOSOME / Pre-60S ribosomal subunit / Assembly intermediate / Nucleoprotein complex

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