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- PDB-7b5l: Ubiquitin ligation to F-box protein substrates by SCF-RBR E3-E3 s... -

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Basic information

Entry
Database: PDB / ID: 7b5l
TitleUbiquitin ligation to F-box protein substrates by SCF-RBR E3-E3 super-assembly: NEDD8-CUL1-RBX1-SKP1-SKP2-CKSHS1-Cyclin A-CDK2-p27-UBE2L3~Ub~ARIH1. Transition State 1
Components
  • (Cyclin-dependent kinase ...) x 2
  • (E3 ubiquitin-protein ligase ...) x 2
  • (S-phase kinase-associated protein ...) x 2
  • Cullin-1
  • Cyclin-A2
  • Cyclin-dependent kinases regulatory subunit 1
  • NEDD8
  • Polyubiquitin-C
  • Ubiquitin-conjugating enzyme E2 L3
KeywordsLIGASE / ubiquitin / ubiquitin ligase / E3 ligase / F-box protein / RBR ligase / Cullin-RING-Ligase / CRL / SCF / NEDD8 / Post-translational modification / ubiquitylation
Function / homology
Function and homology information


PKR/eIFalpha signaling / cyclin-dependent protein kinase activating kinase regulator activity / regulation of lens fiber cell differentiation / negative regulation of cyclin-dependent protein kinase activity / negative regulation of cardiac muscle tissue regeneration / positive regulation of protein polyubiquitination / ubiquitin-like protein transferase activity / autophagic cell death / Lewy body / Parkin-FBXW7-Cul1 ubiquitin ligase complex ...PKR/eIFalpha signaling / cyclin-dependent protein kinase activating kinase regulator activity / regulation of lens fiber cell differentiation / negative regulation of cyclin-dependent protein kinase activity / negative regulation of cardiac muscle tissue regeneration / positive regulation of protein polyubiquitination / ubiquitin-like protein transferase activity / autophagic cell death / Lewy body / Parkin-FBXW7-Cul1 ubiquitin ligase complex / FOXO-mediated transcription of cell cycle genes / cell cycle phase transition / negative regulation of epithelial cell proliferation involved in prostate gland development / ubiquitin-protein transferase activator activity / RBR-type E3 ubiquitin transferase / F-box domain binding / Phosphorylation of proteins involved in the G2/M transition by Cyclin A:Cdc2 complexes / cyclin A2-CDK1 complex / Aberrant regulation of mitotic exit in cancer due to RB1 defects / cell cycle G1/S phase transition / negative regulation of phosphorylation / PcG protein complex / regulation of cell cycle G1/S phase transition / cellular response to luteinizing hormone stimulus / regulation of exit from mitosis / mitotic cell cycle phase transition / cullin-RING-type E3 NEDD8 transferase / NEDD8 transferase activity / epithelial cell proliferation involved in prostate gland development / cullin-RING ubiquitin ligase complex / negative regulation of cyclin-dependent protein serine/threonine kinase activity / negative regulation of epithelial cell apoptotic process / cellular response to leptin stimulus / cellular response to chemical stress / Transcription of E2F targets under negative control by p107 (RBL1) and p130 (RBL2) in complex with HDAC1 / ubiquitin ligase activator activity / positive regulation of ubiquitin protein ligase activity / Cul7-RING ubiquitin ligase complex / ubiquitin-dependent protein catabolic process via the C-end degron rule pathway / regulation of proteolysis / cyclin-dependent protein serine/threonine kinase inhibitor activity / maintenance of protein location in nucleus / Loss of Function of FBXW7 in Cancer and NOTCH1 Signaling / positive regulation of protein autoubiquitination / RHO GTPases activate CIT / male pronucleus / protein K11-linked ubiquitination / protein neddylation / cyclin-dependent protein serine/threonine kinase activator activity / female pronucleus / ubiquitin conjugating enzyme binding / nuclear export / cellular response to cocaine / cellular response to glucocorticoid stimulus / NEDD8 ligase activity / response to glucagon / positive regulation of ubiquitin-protein transferase activity / Cul5-RING ubiquitin ligase complex / AKT phosphorylates targets in the cytosol / positive regulation of intracellular estrogen receptor signaling pathway / negative regulation of response to oxidative stress / cyclin-dependent protein serine/threonine kinase regulator activity / ubiquitin-ubiquitin ligase activity / positive regulation of protein targeting to mitochondrion / epithelial cell apoptotic process / cellular response to antibiotic / SCF ubiquitin ligase complex / Cul2-RING ubiquitin ligase complex / Cul4A-RING E3 ubiquitin ligase complex / Cul4B-RING E3 ubiquitin ligase complex / negative regulation of type I interferon production / cellular response to steroid hormone stimulus / SCF-dependent proteasomal ubiquitin-dependent protein catabolic process / positive regulation of DNA biosynthetic process / E2 ubiquitin-conjugating enzyme / cellular response to insulin-like growth factor stimulus / ubiquitin ligase complex scaffold activity / Cul3-RING ubiquitin ligase complex / negative regulation of kinase activity / regulation of cyclin-dependent protein serine/threonine kinase activity / cellular response to lithium ion / molecular function inhibitor activity / cyclin A1-CDK2 complex / cyclin E2-CDK2 complex / cyclin E1-CDK2 complex / cochlea development / cyclin A2-CDK2 complex / positive regulation of DNA-templated DNA replication initiation / G2 Phase / cyclin-dependent protein kinase activity / Y chromosome / Phosphorylation of proteins involved in G1/S transition by active Cyclin E:Cdk2 complexes / RSV-host interactions / positive regulation of heterochromatin formation / p53-Dependent G1 DNA Damage Response / X chromosome / PTK6 Regulates Cell Cycle / protein kinase inhibitor activity / Prolactin receptor signaling / regulation of anaphase-promoting complex-dependent catabolic process
Similarity search - Function
: / E3 ubiquitin-protein ligase ARIH1, UBA-like domain / Ariadne domain / Ariadne domain / Cyclin-dependent kinase inhibitor domain / Cyclin-dependent kinase inhibitor domain superfamily / Cyclin-dependent kinase inhibitor / Cyclin-dependent kinase, regulatory subunit / Cyclin-dependent kinase, regulatory subunit superfamily / Cyclin-dependent kinase regulatory subunit ...: / E3 ubiquitin-protein ligase ARIH1, UBA-like domain / Ariadne domain / Ariadne domain / Cyclin-dependent kinase inhibitor domain / Cyclin-dependent kinase inhibitor domain superfamily / Cyclin-dependent kinase inhibitor / Cyclin-dependent kinase, regulatory subunit / Cyclin-dependent kinase, regulatory subunit superfamily / Cyclin-dependent kinase regulatory subunit / Cyclin-dependent kinases regulatory subunits signature 1. / Cyclin-dependent kinases regulatory subunits signature 2. / Cyclin-dependent kinase regulatory subunit / IBR domain, a half RING-finger domain / Nedd8-like ubiquitin / E3 ubiquitin ligase RBR family / IBR domain / Leucine-rich repeat, cysteine-containing subtype / Leucine-rich repeat - CC (cysteine-containing) subfamily / A Receptor for Ubiquitination Targets / IBR domain / In Between Ring fingers / F-box domain profile. / TRIAD supradomain / TRIAD supradomain profile. / SKP1 component, dimerisation / S-phase kinase-associated protein 1 / F-box-like domain superfamily / SKP1-like, dimerisation domain superfamily / Skp1 family, dimerisation domain / Cyclin-A, N-terminal APC/C binding region / Cyclin-A N-terminal APC/C binding region / F-box-like / : / F-box domain / Cyclin, C-terminal domain / : / Cyclins signature. / Cyclin / Zinc finger, RING-H2-type / RING-H2 zinc finger domain / Cyclin, C-terminal domain / Cyclin_C / Cullin protein neddylation domain / : / Cullin, conserved site / Cullin family signature. / Cullin repeat-like-containing domain superfamily / Cullin protein, neddylation domain / Cullin / Cullin protein neddylation domain / : / Cullin / Cullin, N-terminal / Cullin homology domain / Cullin homology domain superfamily / Cullin family / Cullin family profile. / Zinc finger, C3HC4 RING-type / Zinc finger, C3HC4 type (RING finger) / S-phase kinase-associated protein 1-like / SKP1 component, POZ domain / Skp1 family, tetramerisation domain / Found in Skp1 protein family / Cyclin, N-terminal / Cyclin, N-terminal domain / Ubiquitin-conjugating enzyme, active site / Ubiquitin-conjugating (UBC) active site signature. / Ubiquitin-conjugating enzyme E2 / Ubiquitin-conjugating enzyme / Ubiquitin-conjugating (UBC) core domain profile. / Ubiquitin-conjugating enzyme E2, catalytic domain homologues / Cyclin-like / domain present in cyclins, TFIIB and Retinoblastoma / Ubiquitin-conjugating enzyme/RWD-like / Cyclin-like superfamily / : / SKP1/BTB/POZ domain superfamily / Ring finger / Zinc finger RING-type profile. / Leucine-rich repeat domain superfamily / Zinc finger, RING-type / : / Ubiquitin domain signature. / Ubiquitin conserved site / Ubiquitin domain / Ubiquitin family / Ubiquitin homologues / Ubiquitin domain profile. / Ubiquitin-like domain / Zinc finger, RING/FYVE/PHD-type / Ubiquitin-like domain superfamily / Winged helix DNA-binding domain superfamily / Serine/threonine-protein kinase, active site / Serine/Threonine protein kinases active-site signature. / Winged helix-like DNA-binding domain superfamily / Protein kinase domain / Serine/Threonine protein kinases, catalytic domain / Protein kinase, ATP binding site / Protein kinases ATP-binding region signature.
Similarity search - Domain/homology
5-azanylpentan-2-one / Polyubiquitin-C / Cyclin-A2 / Cyclin-dependent kinase 2 / Cyclin-dependent kinase inhibitor 1B / Cyclin-dependent kinases regulatory subunit 1 / E3 ubiquitin-protein ligase RBX1 / S-phase kinase-associated protein 1 / Ubiquitin-conjugating enzyme E2 L3 / S-phase kinase-associated protein 2 ...5-azanylpentan-2-one / Polyubiquitin-C / Cyclin-A2 / Cyclin-dependent kinase 2 / Cyclin-dependent kinase inhibitor 1B / Cyclin-dependent kinases regulatory subunit 1 / E3 ubiquitin-protein ligase RBX1 / S-phase kinase-associated protein 1 / Ubiquitin-conjugating enzyme E2 L3 / S-phase kinase-associated protein 2 / Cullin-1 / NEDD8 / E3 ubiquitin-protein ligase ARIH1
Similarity search - Component
Biological speciesHomo sapiens (human)
MethodELECTRON MICROSCOPY / single particle reconstruction / cryo EM / Resolution: 3.8 Å
AuthorsHorn-Ghetko, D. / Prabu, J.R. / Schulman, B.A.
Funding support Germany, 2items
OrganizationGrant numberCountry
European Research Council (ERC)H2020 789016-NEDD8Activate Germany
German Research Foundation (DFG)SCHU 3196/1-1 Germany
CitationJournal: Nature / Year: 2021
Title: Ubiquitin ligation to F-box protein targets by SCF-RBR E3-E3 super-assembly.
Authors: Daniel Horn-Ghetko / David T Krist / J Rajan Prabu / Kheewoong Baek / Monique P C Mulder / Maren Klügel / Daniel C Scott / Huib Ovaa / Gary Kleiger / Brenda A Schulman /
Abstract: E3 ligases are typically classified by hallmark domains such as RING and RBR, which are thought to specify unique catalytic mechanisms of ubiquitin transfer to recruited substrates. However, rather ...E3 ligases are typically classified by hallmark domains such as RING and RBR, which are thought to specify unique catalytic mechanisms of ubiquitin transfer to recruited substrates. However, rather than functioning individually, many neddylated cullin-RING E3 ligases (CRLs) and RBR-type E3 ligases in the ARIH family-which together account for nearly half of all ubiquitin ligases in humans-form E3-E3 super-assemblies. Here, by studying CRLs in the SKP1-CUL1-F-box (SCF) family, we show how neddylated SCF ligases and ARIH1 (an RBR-type E3 ligase) co-evolved to ubiquitylate diverse substrates presented on various F-box proteins. We developed activity-based chemical probes that enabled cryo-electron microscopy visualization of steps in E3-E3 ubiquitylation, initiating with ubiquitin linked to the E2 enzyme UBE2L3, then transferred to the catalytic cysteine of ARIH1, and culminating in ubiquitin linkage to a substrate bound to the SCF E3 ligase. The E3-E3 mechanism places the ubiquitin-linked active site of ARIH1 adjacent to substrates bound to F-box proteins (for example, substrates with folded structures or limited length) that are incompatible with previously described conventional RING E3-only mechanisms. The versatile E3-E3 super-assembly may therefore underlie widespread ubiquitylation.
History
DepositionDec 4, 2020Deposition site: PDBE / Processing site: PDBE
Revision 1.0Feb 10, 2021Provider: repository / Type: Initial release
Revision 1.1Feb 17, 2021Group: Database references / Category: citation / citation_author
Item: _citation.pdbx_database_id_PubMed / _citation.title / _citation_author.name
Revision 1.2Mar 10, 2021Group: Database references / Category: citation
Item: _citation.journal_volume / _citation.page_first / _citation.page_last
Revision 1.3Oct 23, 2024Group: Data collection / Database references / Structure summary
Category: chem_comp_atom / chem_comp_bond ...chem_comp_atom / chem_comp_bond / database_2 / em_admin / pdbx_entry_details / pdbx_modification_feature
Item: _database_2.pdbx_DOI / _database_2.pdbx_database_accession ..._database_2.pdbx_DOI / _database_2.pdbx_database_accession / _em_admin.last_update / _pdbx_entry_details.has_protein_modification

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Structure visualization

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Assembly

Deposited unit
C: Cullin-1
H: E3 ubiquitin-protein ligase ARIH1
T: S-phase kinase-associated protein 2
K: Cyclin-dependent kinases regulatory subunit 1
S: S-phase kinase-associated protein 1
U: Polyubiquitin-C
N: NEDD8
R: E3 ubiquitin-protein ligase RBX1
D: Ubiquitin-conjugating enzyme E2 L3
L: Cyclin-dependent kinase 2
Y: Cyclin-A2
P: Cyclin-dependent kinase inhibitor 1B
hetero molecules


Theoretical massNumber of molelcules
Total (without water)382,21822
Polymers381,52812
Non-polymers69010
Water00
1


  • Idetical with deposited unit
  • defined by author&software
  • Evidence: gel filtration
TypeNameSymmetry operationNumber
identity operation1_5551
Buried area29360 Å2
ΔGint-146 kcal/mol
Surface area125860 Å2
MethodPISA

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Components

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Protein , 6 types, 6 molecules CKUNDY

#1: Protein Cullin-1 / CUL-1


Mass: 89800.367 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: CUL1 / Production host: Trichoplusia ni (cabbage looper) / References: UniProt: Q13616
#4: Protein Cyclin-dependent kinases regulatory subunit 1 / CKS-1


Mass: 8968.261 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: CKS1B, CKS1, PNAS-143, PNAS-16 / Production host: Escherichia coli (E. coli) / References: UniProt: P61024
#6: Protein Polyubiquitin-C


Mass: 8519.778 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: UBC / Production host: Escherichia coli (E. coli) / References: UniProt: P0CG48
#7: Protein NEDD8 / Neddylin / Neural precursor cell expressed developmentally down-regulated protein 8 / NEDD-8 / ...Neddylin / Neural precursor cell expressed developmentally down-regulated protein 8 / NEDD-8 / Ubiquitin-like protein Nedd8


Mass: 8573.978 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: NEDD8 / Production host: Escherichia coli (E. coli) / References: UniProt: Q15843
#9: Protein Ubiquitin-conjugating enzyme E2 L3 / E2 ubiquitin-conjugating enzyme L3 / L-UBC / UbcH7 / Ubiquitin carrier protein L3 / Ubiquitin- ...E2 ubiquitin-conjugating enzyme L3 / L-UBC / UbcH7 / Ubiquitin carrier protein L3 / Ubiquitin-conjugating enzyme E2-F1 / Ubiquitin-protein ligase L3


Mass: 17825.459 Da / Num. of mol.: 1 / Mutation: C17A, C137A
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: UBE2L3, UBCE7, UBCH7 / Production host: Escherichia coli (E. coli)
References: UniProt: P68036, E2 ubiquitin-conjugating enzyme
#11: Protein Cyclin-A2 / Cyclin-A / Cyclin A


Mass: 48609.574 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: CCNA2, CCN1, CCNA / Production host: Escherichia coli (E. coli) / References: UniProt: P20248

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E3 ubiquitin-protein ligase ... , 2 types, 2 molecules HR

#2: Protein E3 ubiquitin-protein ligase ARIH1 / H7-AP2 / HHARI / Monocyte protein 6 / MOP-6 / Protein ariadne-1 homolog / ARI-1 / UbcH7-binding ...H7-AP2 / HHARI / Monocyte protein 6 / MOP-6 / Protein ariadne-1 homolog / ARI-1 / UbcH7-binding protein / UbcM4-interacting protein / Ubiquitin-conjugating enzyme E2-binding protein 1


Mass: 64197.777 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: ARIH1, ARI, MOP6, UBCH7BP, HUSSY-27 / Production host: Escherichia coli (E. coli)
References: UniProt: Q9Y4X5, RBR-type E3 ubiquitin transferase
#8: Protein E3 ubiquitin-protein ligase RBX1 / E3 ubiquitin-protein transferase RBX1 / Protein ZYP / RING finger protein 75 / RING-box protein 1 / ...E3 ubiquitin-protein transferase RBX1 / Protein ZYP / RING finger protein 75 / RING-box protein 1 / Rbx1 / Regulator of cullins 1 / ROC1


Mass: 12289.977 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: RBX1, RNF75, ROC1 / Production host: Trichoplusia ni (cabbage looper)
References: UniProt: P62877, RING-type E3 ubiquitin transferase, cullin-RING-type E3 NEDD8 transferase

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S-phase kinase-associated protein ... , 2 types, 2 molecules TS

#3: Protein S-phase kinase-associated protein 2 / Cyclin-A/CDK2-associated protein p45 / F-box protein Skp2 / F-box/LRR-repeat protein 1 / p45skp2


Mass: 47817.785 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: SKP2, FBXL1 / Production host: Escherichia coli (E. coli) / References: UniProt: Q13309
#5: Protein S-phase kinase-associated protein 1 / Cyclin-A/CDK2-associated protein p19 / p19A / Organ of Corti protein 2 / OCP-2 / Organ of Corti ...Cyclin-A/CDK2-associated protein p19 / p19A / Organ of Corti protein 2 / OCP-2 / Organ of Corti protein II / OCP-II / RNA polymerase II elongation factor-like protein / SIII / Transcription elongation factor B polypeptide 1-like / p19skp1


Mass: 18679.965 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: SKP1, EMC19, OCP2, SKP1A, TCEB1L / Production host: Escherichia coli (E. coli) / References: UniProt: P63208

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Cyclin-dependent kinase ... , 2 types, 2 molecules LP

#10: Protein Cyclin-dependent kinase 2 / Cell division protein kinase 2 / p33 protein kinase


Mass: 34056.469 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: CDK2, CDKN2 / Production host: Escherichia coli (E. coli) / References: UniProt: P24941, cyclin-dependent kinase
#12: Protein Cyclin-dependent kinase inhibitor 1B / Cyclin-dependent kinase inhibitor p27 / p27Kip1


Mass: 22188.303 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Details: misaligned sequence / Source: (gene. exp.) Homo sapiens (human) / Gene: CDKN1B, KIP1 / Production host: Escherichia coli (E. coli) / References: UniProt: P46527

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Non-polymers , 2 types, 10 molecules

#13: Chemical
ChemComp-ZN / ZINC ION


Mass: 65.409 Da / Num. of mol.: 9 / Source method: obtained synthetically / Formula: Zn
#14: Chemical ChemComp-SY8 / 5-azanylpentan-2-one


Mass: 101.147 Da / Num. of mol.: 1 / Source method: obtained synthetically / Formula: C5H11NO

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Details

Has ligand of interestN
Has protein modificationY

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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

Component
IDNameTypeEntity IDParent-IDSource
1NEDD8-CUL1-RBX1-SKP1-SKP2-CKSHS1-Cyclin A-CDK2-p27-UBE2L3~Ub~ARIH1. Transition State 1 composite map.COMPLEX#1-#120MULTIPLE SOURCES
2NEDD8-SKP1-SKP2-CKSHS1-Cyclin A-CDK2-p27-UBE2L3~Ub~ARIH1. Transition State 1 composite map.COMPLEX#2-#7, #9-#121RECOMBINANT
3Cullin-1, E3 ubiquitin-protein ligase RBX1COMPLEX#1, #81RECOMBINANT
Molecular weightValue: 0.30 MDa
Source (natural)
IDEntity assembly-IDOrganismNcbi tax-ID
22Homo sapiens (human)9606
33Homo sapiens (human)9606
Source (recombinant)
IDEntity assembly-IDOrganismNcbi tax-ID
22Escherichia coli (E. coli)562
33Trichoplusia ni (cabbage looper)7111
Buffer solutionpH: 7.8
SpecimenEmbedding applied: NO / Shadowing applied: NO / Staining applied: NO / Vitrification applied: YES
VitrificationCryogen name: ETHANE

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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 FIELD
Image recordingElectron dose: 70 e/Å2 / Film or detector model: GATAN K3 BIOQUANTUM (6k x 4k)

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Processing

SoftwareName: PHENIX / Version: 1.18.2_3874: / Classification: refinement
CTF correctionType: PHASE FLIPPING AND AMPLITUDE CORRECTION
3D reconstructionResolution: 3.8 Å / Resolution method: OTHER / Num. of particles: 623409 / Symmetry type: POINT
Refine LS restraints
Refine-IDTypeDev idealNumber
ELECTRON MICROSCOPYf_bond_d0.00621972
ELECTRON MICROSCOPYf_angle_d0.71929701
ELECTRON MICROSCOPYf_dihedral_angle_d9.7212871
ELECTRON MICROSCOPYf_chiral_restr0.0453303
ELECTRON MICROSCOPYf_plane_restr0.0053781

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