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- PDB-9cju: Structure of SARS-CoV-2 main protease in complex with Bofutrelvir... -

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Basic information

Entry
Database: PDB / ID: 9cju
TitleStructure of SARS-CoV-2 main protease in complex with Bofutrelvir in orthorhombic form
ComponentsNon-structural protein 7
KeywordsHYDROLASE/INHIBITOR / HYDROLASE-INHIBITOR complex / SARS2
Function / homology
Function and homology information


protein guanylyltransferase activity / RNA endonuclease activity producing 3'-phosphomonoesters, hydrolytic mechanism / mRNA guanylyltransferase activity / 5'-3' RNA helicase activity / Lyases; Phosphorus-oxygen lyases / Assembly of the SARS-CoV-2 Replication-Transcription Complex (RTC) / symbiont-mediated suppression of host cytoplasmic pattern recognition receptor signaling pathway via inhibition of TBK1 activity / Maturation of replicase proteins / TRAF3-dependent IRF activation pathway / ISG15-specific peptidase activity ...protein guanylyltransferase activity / RNA endonuclease activity producing 3'-phosphomonoesters, hydrolytic mechanism / mRNA guanylyltransferase activity / 5'-3' RNA helicase activity / Lyases; Phosphorus-oxygen lyases / Assembly of the SARS-CoV-2 Replication-Transcription Complex (RTC) / symbiont-mediated suppression of host cytoplasmic pattern recognition receptor signaling pathway via inhibition of TBK1 activity / Maturation of replicase proteins / TRAF3-dependent IRF activation pathway / ISG15-specific peptidase activity / Transcription of SARS-CoV-2 sgRNAs / snRNP Assembly / Translation of Replicase and Assembly of the Replication Transcription Complex / Replication of the SARS-CoV-2 genome / Hydrolases; Acting on ester bonds; Exoribonucleases producing 5'-phosphomonoesters / double membrane vesicle viral factory outer membrane / SARS coronavirus main proteinase / host cell endoplasmic reticulum-Golgi intermediate compartment / 5'-3' DNA helicase activity / 3'-5'-RNA exonuclease activity / symbiont-mediated degradation of host mRNA / host cell endosome / mRNA guanylyltransferase / symbiont-mediated suppression of host ISG15-protein conjugation / symbiont-mediated suppression of host toll-like receptor signaling pathway / G-quadruplex RNA binding / symbiont-mediated suppression of host cytoplasmic pattern recognition receptor signaling pathway via inhibition of IRF3 activity / omega peptidase activity / mRNA (guanine-N7)-methyltransferase / methyltransferase cap1 / SARS-CoV-2 modulates host translation machinery / host cell Golgi apparatus / symbiont-mediated suppression of host NF-kappaB cascade / DNA helicase / symbiont-mediated perturbation of host ubiquitin-like protein modification / methyltransferase cap1 activity / ubiquitinyl hydrolase 1 / cysteine-type deubiquitinase activity / mRNA 5'-cap (guanine-N7-)-methyltransferase activity / Hydrolases; Acting on peptide bonds (peptidases); Cysteine endopeptidases / single-stranded RNA binding / regulation of autophagy / lyase activity / viral protein processing / host cell perinuclear region of cytoplasm / host cell endoplasmic reticulum membrane / RNA helicase / symbiont-mediated suppression of host type I interferon-mediated signaling pathway / copper ion binding / symbiont-mediated suppression of host gene expression / symbiont-mediated activation of host autophagy / viral translational frameshifting / RNA-directed RNA polymerase / cysteine-type endopeptidase activity / viral RNA genome replication / RNA-directed RNA polymerase activity / DNA-templated transcription / lipid binding / host cell nucleus / SARS-CoV-2 activates/modulates innate and adaptive immune responses / ATP hydrolysis activity / proteolysis / RNA binding / zinc ion binding / ATP binding / membrane
Similarity search - Function
RNA-dependent RNA polymerase, SARS-CoV-like / Nonstructural protein 14, betacoronavirus / NSP15, NendoU domain, coronavirus / Nonstructural protein 15, middle domain, alpha/betacoronavirus / Nonstructural protein 15, N-terminal domain, alpha/beta-coronavirus / NSP14, guanine-N7-methyltransferase domain, coronavirus / Coronavirus (CoV) guanine-N7-methyltransferase (N7-MTase) domain profile. / Coronavirus (CoV) Nsp15 N-terminal oligomerization domain profile. / NSP12 RNA-dependent RNA polymerase, coronavirus / : ...RNA-dependent RNA polymerase, SARS-CoV-like / Nonstructural protein 14, betacoronavirus / NSP15, NendoU domain, coronavirus / Nonstructural protein 15, middle domain, alpha/betacoronavirus / Nonstructural protein 15, N-terminal domain, alpha/beta-coronavirus / NSP14, guanine-N7-methyltransferase domain, coronavirus / Coronavirus (CoV) guanine-N7-methyltransferase (N7-MTase) domain profile. / Coronavirus (CoV) Nsp15 N-terminal oligomerization domain profile. / NSP12 RNA-dependent RNA polymerase, coronavirus / : / Coronavirus Nsp12 RNA-dependent RNA polymerase (RdRp) domain profile. / Coronavirus Nsp12 Interface domain profile. / : / : / Coronavirus Nonstructural protein 13, 1B domain / Coronavirus Non-structural protein 13, zinc-binding domain / Coronavirus Nonstructural protein 13, stalk domain / Nidovirus 2-O-methyltransferase / Nidovirus 2'-O-methyltransferase (2'-O-MTase) domain profile. / Non-structural protein NSP15, N-terminal domain superfamily, coronavirus / Non-structural protein NSP15, middle domain superfamily / Coronavirus replicase NSP15, N-terminal oligomerization / Nonstructural protein 15, middle domain, coronavirus / Nonstructural protein 13, 1B domain, coronavirus / Coronavirus replicase NSP15, middle domain / Coronavirus replicase NSP15, N-terminal oligomerisation / Nidovirus 3'-5' exoribonuclease domain / Nidovirus 3'-5' exoribonuclease (ExoN) domain profile. / Non-structural protein NSP16, coronavirus-like / Non-structural protein 14, coronavirus / RNA polymerase, N-terminal, coronavirus / Coronavirus 2'-O-methyltransferase / Coronavirus proofreading exoribonuclease / Coronavirus RNA-dependent RNA polymerase, N-terminal / Nonstructural protein 13, zinc-binding domain, coronavirus-like / Coronaviridae zinc-binding (CV ZBD) domain profile. / Arterivirus Nsp11 N-terminal/Coronavirus NSP15 middle domain / Arterivirus Nsp11 N-terminal/coronavirus NSP15 middle (AV-Nsp11N/CoV-Nsp15M) domain profile. / Nidoviral uridylate-specific endoribonuclease (NendoU) domain profile. / Nidovirus RdRp-associated nucleotidyl transferase (NiRAN) domain / Nidovirus RdRp-associated nucleotidyl transferase (NiRAN) domain profile. / Endoribonuclease EndoU-like / NendoU domain, nidovirus / Coronavirus replicase NSP15, uridylate-specific endoribonuclease / : / Lipocalin signature. / DNA2/NAM7 helicase-like, C-terminal / AAA domain / (+) RNA virus helicase core domain / (+)RNA virus helicase core domain profile. / Non-structural protein NSP3, SUD-N (Mac2) domain, betacoronavirus / Sarbecovirus Nsp3c-N domain profile. / Non-structural protein NSP3, N-terminal, betacoronavirus / Polyprotein cleavage domain PL2pro superfamily, betacoronavirus / Non-structural protein NSP3, SUD-N (Mac2) domain superfamily, betacoronavirus / Betacoronavirus SUD-C domain / Betacoronavirus replicase NSP3, N-terminal / NSP1 globular domain superfamily, betacoronavirus / Non-structural protein 2, SARS-CoV-like / Betacoronavirus single-stranded poly(A) binding domain / Betacoronavirus Nsp3c-M domain profile. / NSP1, globular domain, betacoronavirus / Non-structural protein NSP3, SUD-M domain, betacoronavirus / Non-structural protein NSP3, SUD-M domain superfamily, betacoronavirus / Betacoronavirus replicase NSP1 / NSP1, C-terminal domain, betacoronavirus / Betacoronavirus (BetaCoV) Nsp1 C-terminal domain profile. / : / Betacoronavirus Nsp3e group 2-specific marker (G2M) domain profile. / Betacoronavirus Nsp3c-C domain profile. / Betacoronavirus Nsp3e nucleic acid-binding (NAB) domain profile. / DPUP/SUD, C-terminal, betacoronavirus / Non-structural protein NSP3, nucleic acid-binding domain, betacoronavirus / Non-structural protein NSP3A domain-like superfamily / Non-structural protein NSP3, nucleic acid-binding domain superfamily, betacoronavirus / Non-structural protein 6, betacoronavirus / Betacoronavirus nucleic acid-binding (NAB) / Papain-like viral protease, palm and finger domains, coronavirus / Papain-like protease, N-terminal domain superfamily, coronavirus / Carbamoyl-phosphate synthase subdomain signature 2. / Coronavirus replicase NSP2, N-terminal / : / Coronavirus replicase NSP2, C-terminal / Coronavirus (CoV) Nsp2 middle domain profile. / NSP1, globular domain, alpha/betacoronavirus / Coronavirus (CoV) Nsp1 globular domain profile. / Coronavirus (CoV) Nsp2 N-terminal domain profile. / Coronavirus (CoV) Nsp2 C-terminal domain profile. / Nonstructural protein 2, N-terminal domain, coronavirus / Non-structural protein 2, C-terminal domain, coronavirus / NSP3, second ubiquitin-like (Ubl) domain, coronavirus / Coronavirus Nsp3a Ubl domain profile. / Coronavirus Nsp3d Ubl domain profile. / NSP3, first ubiquitin-like (Ubl) domain, coronavirus / Peptidase family C16 domain profile. / Coronavirus replicase NSP7 / : / : / Coronavirus 3Ecto domain profile. / Coronavirus RNA-dependent RNA polymerase (RdRp) Nsp7 cofactor domain profile.
Similarity search - Domain/homology
~{N}-[(2~{S})-3-cyclohexyl-1-oxidanylidene-1-[[(2~{S})-1-oxidanylidene-3-[(3~{S})-2-oxidanylidenepyrrolidin-3-yl]propan-2-yl]amino]propan-2-yl]-1~{H}-indole-2-carboxamide / Chem-FHR / DI(HYDROXYETHYL)ETHER / Replicase polyprotein 1ab
Similarity search - Component
Biological speciesSevere acute respiratory syndrome coronavirus 2
MethodX-RAY DIFFRACTION / SYNCHROTRON / MOLECULAR REPLACEMENT / Resolution: 1.68 Å
AuthorsEsler, M.A. / Shi, K. / Harris, R.S. / Aihara, H.
Funding support United States, 2items
OrganizationGrant numberCountry
National Institutes of Health/National Cancer Institute (NIH/NCI)P01 CA214279 United States
National Institutes of Health/National Institute Of Allergy and Infectious Diseases (NIH/NIAID)R37 AI064064 United States
CitationJournal: Mbio / Year: 2025
Title: Structural basis for varying drug resistance of SARS-CoV-2 M pro E166 variants.
Authors: Esler, M.A. / Shi, K. / Rollie, J.A. / Delgado, R. / Vishwakarma, J. / Dabrowska, A. / Prahlad, J. / Moghadasi, S.A. / Harris, R.S. / Aihara, H.
History
DepositionJul 7, 2024Deposition site: RCSB / Processing site: RCSB
Revision 1.0Jul 9, 2025Provider: repository / Type: Initial release
Revision 1.1Jul 23, 2025Group: Database references / Category: citation / citation_author
Item: _citation.country / _citation.journal_abbrev ..._citation.country / _citation.journal_abbrev / _citation.journal_id_CSD / _citation.journal_id_ISSN / _citation.journal_volume / _citation.page_first / _citation.page_last / _citation.pdbx_database_id_DOI / _citation.pdbx_database_id_PubMed / _citation.title / _citation.year

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Structure visualization

Structure viewerMolecule:
MolmilJmol/JSmol

Downloads & links

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Assembly

Deposited unit
A: Non-structural protein 7
B: Non-structural protein 7
hetero molecules


Theoretical massNumber of molelcules
Total (without water)68,88512
Polymers67,3952
Non-polymers1,49010
Water8,089449
1


  • Idetical with deposited unit
  • defined by author&software
TypeNameSymmetry operationNumber
identity operation1_555x,y,z1
Buried area4830 Å2
ΔGint10 kcal/mol
Surface area25310 Å2
MethodPISA
Unit cell
Length a, b, c (Å)67.848, 99.822, 104.113
Angle α, β, γ (deg.)90.00, 90.00, 90.00
Int Tables number19
Space group name H-MP212121

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Components

#1: Protein Non-structural protein 7 / nsp7


Mass: 33697.418 Da / Num. of mol.: 2
Source method: isolated from a genetically manipulated source
Source: (gene. exp.) Severe acute respiratory syndrome coronavirus 2
Gene: rep, 1a-1b / Production host: Escherichia coli BL21 (bacteria) / References: UniProt: P0DTD1
#2: Chemical ChemComp-FHR / ~{N}-[(2~{S})-3-cyclohexyl-1-oxidanylidene-1-[[(2~{S})-1-oxidanylidene-3-[(3~{S})-2-oxidanylidenepyrrolidin-3-yl]propan-2-yl]amino]propan-2-yl]-1~{H}-indole-2-carboxamide


Type: peptide-like, Peptide-like / Class: Inhibitor / Mass: 452.546 Da / Num. of mol.: 2 / Source method: obtained synthetically / Formula: C25H32N4O4 / Feature type: SUBJECT OF INVESTIGATION
References: ~{N}-[(2~{S})-3-cyclohexyl-1-oxidanylidene-1-[[(2~{S})-1-oxidanylidene-3-[(3~{S})-2-oxidanylidenepyrrolidin-3-yl]propan-2-yl]amino]propan-2-yl]-1~{H}-indole-2-carboxamide
#3: Chemical
ChemComp-EDO / 1,2-ETHANEDIOL / ETHYLENE GLYCOL


Mass: 62.068 Da / Num. of mol.: 6 / Source method: obtained synthetically / Formula: C2H6O2
#4: Chemical ChemComp-PEG / DI(HYDROXYETHYL)ETHER


Mass: 106.120 Da / Num. of mol.: 2 / Source method: obtained synthetically / Formula: C4H10O3
#5: Water ChemComp-HOH / water


Mass: 18.015 Da / Num. of mol.: 449 / Source method: isolated from a natural source / Formula: H2O
Has ligand of interestY
Has protein modificationY

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Experimental details

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Experiment

ExperimentMethod: X-RAY DIFFRACTION / Number of used crystals: 1

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Sample preparation

CrystalDensity Matthews: 2.64 Å3/Da / Density % sol: 53.35 %
Crystal growTemperature: 295 K / Method: vapor diffusion, sitting drop
Details: J000854 E10_10: 0.12 M ethylene glycols, 0.1 M Buffer System 3, pH 8.5, 30% v/v Precipitant Mix 2

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Data collection

DiffractionMean temperature: 100 K / Serial crystal experiment: N
Diffraction sourceSource: SYNCHROTRON / Site: NSLS-II / Beamline: 17-ID-1 / Wavelength: 0.979 Å
DetectorType: DECTRIS EIGER X 9M / Detector: PIXEL / Date: Feb 2, 2024
RadiationProtocol: SINGLE WAVELENGTH / Monochromatic (M) / Laue (L): M / Scattering type: x-ray
Radiation wavelengthWavelength: 0.979 Å / Relative weight: 1
ReflectionResolution: 1.68→33.924 Å / Num. obs: 59620 / % possible obs: 73.6 % / Redundancy: 6.7 % / Rmerge(I) obs: 0.129 / Rpim(I) all: 0.054 / Rrim(I) all: 0.14 / Net I/σ(I): 8.4
Reflection shellResolution: 1.681→1.861 Å / % possible obs: 14.2 % / Redundancy: 6.1 % / Rmerge(I) obs: 1.116 / Num. measured all: 18288 / Num. unique obs: 2981 / Rpim(I) all: 0.487 / Rrim(I) all: 1.22 / Net I/σ(I) obs: 1.7

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Processing

Software
NameVersionClassification
PHENIX(1.20.1_4487: ???)refinement
Aimlessdata scaling
XDSdata reduction
PHASERphasing
RefinementMethod to determine structure: MOLECULAR REPLACEMENT / Resolution: 1.68→33.92 Å / SU ML: 0.18 / Cross valid method: FREE R-VALUE / σ(F): 1.34 / Phase error: 25.29 / Stereochemistry target values: ML
RfactorNum. reflection% reflection
Rfree0.21 2828 4.74 %
Rwork0.1746 --
obs0.1763 59615 73.58 %
Solvent computationShrinkage radii: 0.9 Å / VDW probe radii: 1.1 Å / Solvent model: FLAT BULK SOLVENT MODEL
Refinement stepCycle: LAST / Resolution: 1.68→33.92 Å
ProteinNucleic acidLigandSolventTotal
Num. atoms4689 0 104 449 5242
Refine LS restraints
Refine-IDTypeDev idealNumber
X-RAY DIFFRACTIONf_dihedral_angle_d13.8721797
X-RAY DIFFRACTIONf_chiral_restr0.088751
X-RAY DIFFRACTIONf_plane_restr0.008875
LS refinement shell
Resolution (Å)Rfactor RfreeNum. reflection RfreeRfactor RworkNum. reflection RworkRefine-ID% reflection obs (%)
1.68-1.710.190740.277466X-RAY DIFFRACTION2
1.71-1.740.604860.2673194X-RAY DIFFRACTION5
1.74-1.770.4552130.3126382X-RAY DIFFRACTION10
1.77-1.810.3426330.3023732X-RAY DIFFRACTION19
1.81-1.850.3161630.28181134X-RAY DIFFRACTION30
1.85-1.890.331800.25571694X-RAY DIFFRACTION44
1.89-1.940.27091180.26012668X-RAY DIFFRACTION69
1.94-1.990.29141580.23383370X-RAY DIFFRACTION88
1.99-2.050.26341830.2293803X-RAY DIFFRACTION100
2.05-2.120.22491800.20543856X-RAY DIFFRACTION100
2.12-2.190.24941950.18493823X-RAY DIFFRACTION100
2.19-2.280.23351810.18723851X-RAY DIFFRACTION100
2.28-2.390.21992010.17833829X-RAY DIFFRACTION100
2.39-2.510.23432250.18423826X-RAY DIFFRACTION100
2.51-2.670.20792260.18433823X-RAY DIFFRACTION100
2.67-2.870.22581920.18623871X-RAY DIFFRACTION100
2.87-3.160.20741690.18463911X-RAY DIFFRACTION100
3.16-3.620.20791890.16183916X-RAY DIFFRACTION100
3.62-4.560.14812010.13343941X-RAY DIFFRACTION100
4.56-33.920.19252110.14954097X-RAY DIFFRACTION100
Refinement TLS params.

Method: refined / Refine-ID: X-RAY DIFFRACTION

IDL11 (°2)L12 (°2)L13 (°2)L22 (°2)L23 (°2)L33 (°2)S11 (Å °)S12 (Å °)S13 (Å °)S21 (Å °)S22 (Å °)S23 (Å °)S31 (Å °)S32 (Å °)S33 (Å °)T11 (Å2)T12 (Å2)T13 (Å2)T22 (Å2)T23 (Å2)T33 (Å2)Origin x (Å)Origin y (Å)Origin z (Å)
11.9582-0.009-0.95150.91620.00872.2376-0.0908-0.2279-0.02460.02660.0063-0.12190.12850.4990.04480.10680.0375-0.00410.14350.01560.110321.6563-6.6616-22.2244
22.65620.19750.65990.35540.20170.949-0.02590.09540.0064-0.0467-0.01990.0944-0.0008-0.11980.03860.12180.0052-0.00060.0908-0.00610.115-2.6938-5.8633-31.8673
31.345-0.74810.29361.18380.35681.8813-0.1618-0.1305-0.1912-0.01440.07570.04180.6989-0.24240.03260.2657-0.03740.0190.11640.01510.1432-0.0995-10.8381-1.6846
42.0452-1.04460.38423.547-0.04952.7808-0.0576-0.4255-0.87630.3449-0.06810.68941.258-0.7575-0.01960.6507-0.19670.08310.40560.09930.3507-5.9165-17.38159.3645
52.4011-0.40180.01681.5220.09014.20890.0303-0.10340.0285-0.0135-0.065-0.02580.0468-0.22870.02580.1169-0.01450.02470.08980.0040.106-4.2407-2.8894-3.9626
60.67010.0251-0.14392.0426-0.82953.07090.0637-0.02650.2754-0.00630.2870.4385-0.2931-0.8324-0.1880.17090.0381-0.00450.18180.01040.1801-10.71946.806-7.8695
70.57460.6382-0.19213.9256-1.83551.51430.2804-0.18960.32530.53880.0450.0671-0.8313-0.0924-0.2660.56060.0630.08190.2406-0.0160.2714-4.392723.2117-14.9356
82.0992-0.4618-2.10732.84220.47582.26410.0281-0.00640.0408-0.1250.00180.131-0.6526-0.1780.02990.35830.00010.01220.1183-0.01370.2112-1.508214.6857-18.5765
Refinement TLS group
IDRefine-IDRefine TLS-IDSelection details
1X-RAY DIFFRACTION1chain 'A' and (resid 1 through 139 )
2X-RAY DIFFRACTION2chain 'A' and (resid 140 through 301 )
3X-RAY DIFFRACTION3chain 'B' and (resid 1 through 43 )
4X-RAY DIFFRACTION4chain 'B' and (resid 44 through 100 )
5X-RAY DIFFRACTION5chain 'B' and (resid 101 through 180 )
6X-RAY DIFFRACTION6chain 'B' and (resid 181 through 213 )
7X-RAY DIFFRACTION7chain 'B' and (resid 214 through 260 )
8X-RAY DIFFRACTION8chain 'B' and (resid 261 through 305 )

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