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- PDB-7b5m: Ubiquitin ligation to F-box protein substrates by SCF-RBR E3-E3 s... -

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Entry
Database: PDB / ID: 7b5m
TitleUbiquitin ligation to F-box protein substrates by SCF-RBR E3-E3 super-assembly: CUL1-RBX1-SKP1-SKP2-CKSHS1-p27~Ub~ARIH1. Transition State 2
Components
  • (Cyclin-dependent ...) x 2
  • (E3 ubiquitin-protein ligase ...) x 2
  • (S-phase kinase-associated protein ...) x 2
  • Cullin-1
  • Polyubiquitin-C
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 regulator activity / negative regulation of cardiac muscle tissue regeneration / ubiquitin-like protein transferase activity / autophagic cell death / FOXO-mediated transcription of cell cycle genes / regulation of xenophagy / RBR-type E3 ubiquitin transferase / Parkin-FBXW7-Cul1 ubiquitin ligase complex / F-box domain binding ...PKR/eIFalpha signaling / cyclin-dependent protein kinase regulator activity / negative regulation of cardiac muscle tissue regeneration / ubiquitin-like protein transferase activity / autophagic cell death / FOXO-mediated transcription of cell cycle genes / regulation of xenophagy / RBR-type E3 ubiquitin transferase / Parkin-FBXW7-Cul1 ubiquitin ligase complex / F-box domain binding / synaptic assembly at neuromuscular junction / regulation of cell cycle G1/S phase transition / Aberrant regulation of mitotic exit in cancer due to RB1 defects / regulation of cell cycle process / neural crest cell differentiation / cellular response to lithium ion / negative regulation of mitotic cell cycle / regulation of BMP signaling pathway / PcG protein complex / negative regulation of beige fat cell differentiation / cyclin-dependent protein serine/threonine kinase inhibitor activity / regulation of mitophagy / cullin-RING-type E3 NEDD8 transferase / NEDD8 transferase activity / regulation of centrosome duplication / cullin-RING ubiquitin ligase complex / maintenance of protein location in nucleus / Cul7-RING ubiquitin ligase complex / regulation of cyclin-dependent protein serine/threonine kinase activity / nuclear export / Loss of Function of FBXW7 in Cancer and NOTCH1 Signaling / RHO GTPases activate CIT / cellular response to chemical stress / cyclin-dependent protein serine/threonine kinase activator activity / regulation of TOR signaling / positive regulation of protein autoubiquitination / RNA polymerase II transcription initiation surveillance / Modulation of host responses by IFN-stimulated genes / protein neddylation / AKT phosphorylates targets in the cytosol / ubiquitin ligase activator activity / ubiquitin conjugating enzyme binding / regulation of DNA damage checkpoint / NEDD8 ligase activity / negative regulation of response to oxidative stress / molecular function inhibitor activity / protein K27-linked ubiquitination / VCB complex / Cul5-RING ubiquitin ligase complex / ubiquitin-ubiquitin ligase activity / ubiquitin-dependent protein catabolic process via the C-end degron rule pathway / SCF ubiquitin ligase complex / Cul2-RING ubiquitin ligase complex / Cul3-RING ubiquitin ligase complex / p53-Dependent G1 DNA Damage Response / negative regulation of type I interferon production / PTK6 Regulates Cell Cycle / SCF-dependent proteasomal ubiquitin-dependent protein catabolic process / Constitutive Signaling by AKT1 E17K in Cancer / negative regulation of mitophagy / Prolactin receptor signaling / RSV-host interactions / limb development / Lewy body / Cul4A-RING E3 ubiquitin ligase complex / Cul4-RING E3 ubiquitin ligase complex / Defective binding of RB1 mutants to E2F1,(E2F2, E2F3) / Cul4B-RING E3 ubiquitin ligase complex / protein kinase inhibitor activity / ubiquitin ligase complex scaffold activity / negative regulation of vascular associated smooth muscle cell proliferation / centrosome duplication / Estrogen-dependent nuclear events downstream of ESR-membrane signaling / cilium assembly / protein monoubiquitination / cullin family protein binding / TP53 Regulates Transcription of Genes Involved in G1 Cell Cycle Arrest / ubiquitin ligase complex / Cajal body / protein K63-linked ubiquitination / Cyclin E associated events during G1/S transition / cyclin-dependent protein kinase holoenzyme complex / Cyclin A:Cdk2-associated events at S phase entry / positive regulation of double-strand break repair via homologous recombination / GSK3B-mediated proteasomal degradation of PD-L1(CD274) / ubiquitin-like ligase-substrate adaptor activity / regulation of G1/S transition of mitotic cell cycle / signal transduction in response to DNA damage / site of DNA damage / Nuclear events stimulated by ALK signaling in cancer / protein K48-linked ubiquitination / negative regulation of insulin receptor signaling pathway / regulation of cellular response to insulin stimulus / positive regulation of TORC1 signaling / FLT3 Signaling / animal organ morphogenesis / Maturation of protein E / Maturation of protein E / transcription-coupled nucleotide-excision repair / intrinsic apoptotic signaling pathway
Similarity search - Function
: / E3 ubiquitin-protein ligase ARIH1, UBA-like domain / Cullin Repeats / Ariadne domain / Ariadne domain / Cyclin-dependent kinase inhibitor domain / Cyclin-dependent kinase inhibitor domain superfamily / Cyclin-dependent kinase inhibitor / E3 ubiquitin ligase RBR family / 5 helical Cullin repeat like ...: / E3 ubiquitin-protein ligase ARIH1, UBA-like domain / Cullin Repeats / Ariadne domain / Ariadne domain / Cyclin-dependent kinase inhibitor domain / Cyclin-dependent kinase inhibitor domain superfamily / Cyclin-dependent kinase inhibitor / E3 ubiquitin ligase RBR family / 5 helical Cullin repeat like / 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 / IBR domain / IBR domain / In Between Ring fingers / TRIAD supradomain / TRIAD supradomain profile. / Leucine-rich repeat, cysteine-containing subtype / Leucine-rich repeat - CC (cysteine-containing) subfamily / A Receptor for Ubiquitination Targets / F-box domain profile. / F-box-like / F-box-like domain superfamily / SKP1 component, dimerisation / S-phase kinase-associated protein 1 / SKP1-like, dimerisation domain superfamily / Skp1 family, dimerisation domain / F-box domain / Zinc finger, RING-H2-type / RING-H2 zinc finger domain / : / Cullin protein neddylation domain / Cullin, conserved site / Cullin family signature. / Cullin, N-terminal / Cullin repeat-like-containing domain superfamily / Cullin protein, neddylation domain / Cullin / Cullin protein neddylation domain / Cullin alpha solenoid domain / Cullin / : / Cullin alpha+beta domain / Cullin homology domain / Cullin homology domain superfamily / 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 / Phosphatidylinositol 3-kinase Catalytic Subunit; Chain A, domain 1 / SKP1/BTB/POZ domain superfamily / Ring finger / Leucine-rich repeat domain superfamily / Zinc finger RING-type profile. / Zinc finger, RING-type / Ubiquitin-like (UB roll) / : / 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 / Winged helix-like DNA-binding domain superfamily / Roll / Up-down Bundle / Mainly Alpha / Alpha Beta
Similarity search - Domain/homology
Polyubiquitin-C / Cyclin-dependent kinase inhibitor 1B / Cyclin-dependent kinases regulatory subunit 1 / E3 ubiquitin-protein ligase RBX1 / S-phase kinase-associated protein 1 / S-phase kinase-associated protein 2 / Cullin-1 / E3 ubiquitin-protein ligase ARIH1
Similarity search - Component
Biological speciesHomo sapiens (human)
MethodELECTRON MICROSCOPY / single particle reconstruction / cryo EM / Resolution: 3.91 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 5, 2020Deposition site: PDBE / Processing site: PDBE
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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
R: E3 ubiquitin-protein ligase RBX1
P: Cyclin-dependent kinase inhibitor 1B
hetero molecules


Theoretical massNumber of molelcules
Total (without water)273,30513
Polymers272,9788
Non-polymers3275
Water00
1


  • Idetical with deposited unit
  • defined by author
  • Evidence: gel filtration
TypeNameSymmetry operationNumber
identity operation1_5551

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Components

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Protein , 2 types, 2 molecules CU

#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
#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

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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: 64005.605 Da / Num. of mol.: 1 / Mutation: F430A, E431A, E503A
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
#7: 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 ... , 2 types, 2 molecules KP

#4: Protein Cyclin-dependent kinases regulatory subunit 1 / CKS-1


Mass: 9679.211 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
#8: Protein Cyclin-dependent kinase inhibitor 1B / Cyclin-dependent kinase inhibitor p27 / p27Kip1


Mass: 22185.262 Da / Num. of mol.: 1
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Homo sapiens (human) / Gene: CDKN1B, KIP1 / Production host: synthetic construct (others) / References: UniProt: P46527

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Non-polymers , 1 types, 5 molecules

#9: Chemical
ChemComp-ZN / ZINC ION


Mass: 65.409 Da / Num. of mol.: 5 / Source method: obtained synthetically / Formula: Zn

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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
1CUL1-RBX1-SKP1-SKP2-CKSHS1-p27~Ub~ARIH1COMPLEX#1-#80MULTIPLE SOURCES
2Cullin-1, E3 ubiquitin-protein ligase RBX1COMPLEX#1, #71RECOMBINANT
3ARIH1, SKP2, CKS1B, SKP1, UBCCOMPLEX#2-#61RECOMBINANT
4Cyclin-dependent kinase inhibitor 1BCOMPLEX#81RECOMBINANT
Molecular weightValue: 0.25 MDa
Source (natural)
IDEntity assembly-IDOrganismNcbi tax-ID
22Homo sapiens (human)9606
33Homo sapiens (human)9606
44Homo sapiens (human)9606
Source (recombinant)
IDEntity assembly-IDOrganismNcbi tax-ID
22Trichoplusia ni (cabbage looper)7111
33Escherichia coli (E. coli)562
44synthetic construct (others)32630
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
EM softwareName: PHENIX / Category: model refinement
CTF correctionType: PHASE FLIPPING AND AMPLITUDE CORRECTION
3D reconstructionResolution: 3.91 Å / Resolution method: FSC 0.143 CUT-OFF / Num. of particles: 759489 / Symmetry type: POINT
Refine LS restraints
Refine-IDTypeDev idealNumber
ELECTRON MICROSCOPYf_bond_d0.00413019
ELECTRON MICROSCOPYf_angle_d0.81317603
ELECTRON MICROSCOPYf_dihedral_angle_d10.9211710
ELECTRON MICROSCOPYf_chiral_restr0.0481969
ELECTRON MICROSCOPYf_plane_restr0.0052251

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