Sequence-selective interaction of the minor-groove interstrand cross-linking agent SJG-136 with naked and cellular DNA: footprinting and enzyme inhibition studies

Biochemistry. 2005 Mar 22;44(11):4135-47. doi: 10.1021/bi0479813.

Abstract

SJG-136 (3) is a novel pyrrolobenzodiazepine (PBD) dimer that is predicted from molecular models to bind in the minor groove of DNA and to form sequence-selective interstrand cross-links at 5'-Pu-GATC-Py-3' (Pu = purine; Py = pyrimidine) sites through covalent bonding between each PBD unit and guanines on opposing strands. Footprinting studies have confirmed that high-affinity adducts do form at 5'-G-GATC-C-3' sequences and that these can inhibit RNA polymerase in a sequence-selective manner. At higher concentrations of SJG-136, bands that migrate more slowly than one of the 5'-G-GATC-C-3' footprint sites show significantly reduced intensity, concomitant with the appearance of higher molecular weight material near the gel origin. This phenomenon is attributed to interstrand cross-linking at the 5'-G-GATC-C-3' site and is the first report of DNA footprinting being used to detect interstrand cross-linked adducts. The control dimer GD113 (4), of similar structure to SJG-136 but unable to cross-link DNA due to its C7/C7'-linkage rather than C8/C8'-linkage, neither produces footprints with the same DNA sequence nor blocks transcription at comparable concentrations. In addition to the two high-affinity 5'-G-GATC-C-3' footprints on the MS2 DNA sequence, other SJG-136 adducts of lower affinity are observed that can still block transcription but with lower efficiency. All these sites contain the 5'-GXXC-3' motif (where XX includes AG, TA, GC, CT, TT, GG, and TC) and represent less-favored cross-link sites. In time-course experiments, SJG-136 blocks transcription if incubated with a double-stranded DNA template before the transcription components are added; addition after transcription is initiated fails to elicit blockage. Single-strand ligation PCR studies on a sequence from the c-jun gene show that SJG-136 binds to 5'-GAAC-3'/5'-GTTC-3' (preferred) or 5'-GAGC-3'/5'-GCTC-3' sequences. Significantly, adducts are obtained at the same sequences following extraction of DNA from drug-treated K562 cells, confirming that the agent reaches the cellular genome and interacts with the DNA in a sequence-selective fashion. Finally, SJG-136 efficiently inhibits the action of restriction endonuclease BglII, which has a 5'-A-GATC-T-3' motif at its cleavage site.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / antagonists & inhibitors
  • Bacterial Proteins / metabolism
  • Bacteriophage T7 / genetics
  • Bacteriophage T7 / metabolism*
  • Base Sequence
  • Benzodiazepinones / metabolism*
  • Benzodiazepinones / pharmacology
  • Capsid Proteins / genetics
  • Capsid Proteins / metabolism*
  • Cross-Linking Reagents / metabolism*
  • Cross-Linking Reagents / pharmacology
  • DNA Footprinting
  • DNA, Single-Stranded / metabolism
  • DNA, Viral / genetics
  • DNA, Viral / metabolism*
  • Deoxyribonuclease I / metabolism
  • Deoxyribonucleases, Type II Site-Specific / antagonists & inhibitors
  • Deoxyribonucleases, Type II Site-Specific / metabolism
  • Enzyme Inhibitors / metabolism
  • Enzyme Inhibitors / pharmacology
  • Molecular Sequence Data
  • Nucleic Acid Conformation*
  • Polymerase Chain Reaction / methods
  • Pyrroles / metabolism*
  • Pyrroles / pharmacology
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*
  • Sequence Analysis, DNA
  • Temperature
  • Transcription, Genetic

Substances

  • 1,1'-((propane-1,3-diyl)dioxy)bis(7-methoxy-2-methylidene-1,2,3,10,11,11a-hexahydro-5H-pyrrolo(2,1-c)(1,4)benzodiazepin-5,11-dione)
  • Bacterial Proteins
  • Benzodiazepinones
  • Capsid Proteins
  • Cross-Linking Reagents
  • DNA, Single-Stranded
  • DNA, Viral
  • Enzyme Inhibitors
  • Pyrroles
  • RNA-Binding Proteins
  • endodeoxyribonuclease MluI
  • Deoxyribonuclease I
  • BglII endonuclease
  • Deoxyribonucleases, Type II Site-Specific