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PMID: 22471443 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Mechanistic studies on the application of DNA aptamers as inhibitors of 2-oxoglutarate-dependent oxygenases.

Journal of medicinal chemistry ·Vol. 55 ·No. 7 ·2012-04-12 ·Pages 3546-52

Krylova SM, Koshkin V, Bagg E, Schofield CJ, Krylov SN

Abstract

The Escherichia coli (E. coli) AlkB protein and its functional human homologues belong to a subfamily of 2-oxoglutarate (2OG) dependent oxygenases (2OG oxygenases for simplicity) that enable the repair of cytotoxic methylation damage in nucleic acids and that catalyze t-RNA oxidations. DNA alkylation is a major mechanism of action for cytotoxic anticancer drugs. Thus, the inhibition of oxidative demethylation, catalyzed by these enzymes, has the potential to improve the efficacy of chemotherapies. Here we report that oligonucleotide aptamers constitute a new class of potent inhibitors of 2OG oxygenases. DNA aptamers can selectively bind to AlkB, with nanomolar affinity, and efficiently inhibit catalysis. The mechanism of inhibition was studied by capillary electrophoresis (CE) with laser-induced fluorescence (LIF) detection. Inhibition constants of the aptamers were determined and shown to correlate well with K(d) values. The results of kinetic analyses imply that the aptamers bind AlkB away from the active site. Our findings should stimulate the development of oligonucleotide aptamers for human homologues of AlkB and further their study as potential enhancers of chemotherapy efficiency.

MeSH Terms
Amino Acids, Dicarboxylic/chemistry Aptamers, Nucleotide/chemistry Biocatalysis DNA/chemistry DNA Methylation Enzyme Assays Escherichia coli Proteins/antagonists & inhibitors,chemistry,metabolism Ferrous Compounds/chemistry Humans Ketoglutaric Acids/metabolism Kinetics Mixed Function Oxygenases/antagonists & inhibitors,chemistry,metabolism Protein Binding Structure-Activity Relationship
Chemicals
Amino Acids, Dicarboxylic Aptamers, Nucleotide Escherichia coli Proteins Ferrous Compounds Ketoglutaric Acids DNA Mixed Function Oxygenases AlkB protein, E coli oxalylglycine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Krylova Svetlana M
Department of Chemistry and Centre for Research on Biomolecular Interactions, York University, Toronto, Ontario, M3J 1P3, Canada.
Koshkin Vasilij
Bagg Eleanor
Schofield Christopher J
Krylov Sergey N
References (34)
34 references, click to expand
  1. Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes.
    Curr Opin Struct Biol. 1999 Dec;9(6):722-31 PMID: 10607676
  2. The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases.
    Genome Biol. 2001;2(3):RESEARCH0007 PMID: 11276424
  3. Kinetic studies of Escherichia coli AlkB using a new fluorescence-based assay for DNA demethylation.
    Nucleic Acids Res. 2007;35(21):e147 PMID: 18003660
  4. Repair of methyl lesions in DNA and RNA by oxidative demethylation.
    Neuroscience. 2007 Apr 14;145(4):1222-32 PMID: 17175108
  5. Direct analysis of enzyme-catalyzed DNA demethylation.
    Anal Chem. 2009 Jul 15;81(14):5871-5 PMID: 19518090
  6. Kinetics of the reversible inhibition of enzyme-catalysed reactions by tight-binding inhibitors.
    Biochim Biophys Acta. 1969;185(2):269-86 PMID: 4980133
  7. Human AlkB homolog ABH8 Is a tRNA methyltransferase required for wobble uridine modification and DNA damage survival.
    Mol Cell Biol. 2010 May;30(10):2449-59 PMID: 20308323
  8. Direct reversal of DNA alkylation damage.
    Chem Rev. 2006 Feb;106(2):215-32 PMID: 16464003
  9. Dynamic states of the DNA repair enzyme AlkB regulate product release.
    EMBO Rep. 2008 Sep;9(9):872-7 PMID: 18617893
  10. A novel human AlkB homologue, ALKBH8, contributes to human bladder cancer progression.
    Cancer Res. 2009 Apr 1;69(7):3157-64 PMID: 19293182
  11. Minimal methylated substrate and extended substrate range of Escherichia coli AlkB protein, a 1-methyladenine-DNA dioxygenase.
    J Biol Chem. 2003 Nov 7;278(45):44348-54 PMID: 12944387
  12. Targeted modulation of MGMT: clinical implications.
    Clin Cancer Res. 2006 Jan 15;12(2):328-31 PMID: 16428468
  13. The selectivity and inhibition of AlkB.
    J Biol Chem. 2003 Mar 21;278(12):10157-61 PMID: 12517755
  14. ALKBH3, a human AlkB homologue, contributes to cell survival in human non-small-cell lung cancer.
    Br J Cancer. 2011 Feb 15;104(4):700-6 PMID: 21285982
  15. Selection of smart small-molecule ligands: the proof of principle.
    Anal Chem. 2009 Jan 1;81(1):490-4 PMID: 19055427
  16. Nonequilibrium capillary electrophoresis of equilibrium mixtures: a universal tool for development of aptamers.
    J Am Chem Soc. 2005 Mar 9;127(9):3165-71 PMID: 15740156
  17. DNA aptamers for as analytical tools for the quantitative analysis of DNA-dealkylating enzymes.
    Anal Biochem. 2011 Jul 15;414(2):261-5 PMID: 21402046
  18. Repair of methylation damage in DNA and RNA by mammalian AlkB homologues.
    J Biol Chem. 2005 Nov 25;280(47):39448-59 PMID: 16174769
  19. Inhibition of 2-oxoglutarate dependent oxygenases.
    Chem Soc Rev. 2011 Aug;40(8):4364-97 PMID: 21390379
  20. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase.
    Science. 1990 Aug 3;249(4968):505-10 PMID: 2200121
  21. Mammalian ALKBH8 possesses tRNA methyltransferase activity required for the biogenesis of multiple wobble uridine modifications implicated in translational decoding.
    Mol Cell Biol. 2010 Apr;30(7):1814-27 PMID: 20123966
  22. Non-SELEX: selection of aptamers without intermediate amplification of candidate oligonucleotides.
    Nat Protoc. 2006;1(3):1359-69 PMID: 17406423
  23. The obesity-associated FTO gene encodes a 2-oxoglutarate-dependent nucleic acid demethylase.
    Science. 2007 Nov 30;318(5855):1469-72 PMID: 17991826
  24. Expression and sub-cellular localization of human ABH family molecules.
    J Cell Mol Med. 2007 Sep-Oct;11(5):1105-16 PMID: 17979886
  25. In vitro selection of RNA molecules that bind specific ligands.
    Nature. 1990 Aug 30;346(6287):818-22 PMID: 1697402
  26. Smart aptamers facilitate multi-probe affinity analysis of proteins with ultra-wide dynamic range of measured concentrations.
    J Am Chem Soc. 2007 Jun 13;129(23):7260-1 PMID: 17503828
  27. Down-regulation of ALKBH2 increases cisplatin sensitivity in H1299 lung cancer cells.
    Acta Pharmacol Sin. 2011 Mar;32(3):393-8 PMID: 21278781
  28. Frequent down-regulation of hABH2 in gastric cancer and its involvement in growth of cancer cells.
    J Gastroenterol Hepatol. 2011 Mar;26(3):577-84 PMID: 21155885
  29. Physiological and biochemical aspects of hydroxylations and demethylations catalyzed by human 2-oxoglutarate oxygenases.
    Trends Biochem Sci. 2011 Jan;36(1):7-18 PMID: 20728359
  30. A non-heme iron-mediated chemical demethylation in DNA and RNA.
    Acc Chem Res. 2009 Apr 21;42(4):519-29 PMID: 19852088
  31. Controlling protein activity with ligand-regulated RNA aptamers.
    Chem Biol. 2002 Aug;9(8):907-13 PMID: 12204690
  32. Human AlkB homolog 1 is a mitochondrial protein that demethylates 3-methylcytosine in DNA and RNA.
    J Biol Chem. 2008 Sep 5;283(36):25046-56 PMID: 18603530
  33. Nonequilibrium capillary electrophoresis of equilibrium mixtures--a single experiment reveals equilibrium and kinetic parameters of protein-DNA interactions.
    J Am Chem Soc. 2002 Nov 20;124(46):13674-5 PMID: 12431087
  34. Structural and mutational analysis of Escherichia coli AlkB provides insight into substrate specificity and DNA damage searching.
    PLoS One. 2010 Jan 13;5(1):e8680 PMID: 20084272
Article Info
Journal
Journal of medicinal chemistry
Abbr.
J Med Chem
ISSN
1520-4804
Published
2012-04-12
Epub
2012-00-03
Pages
3546-52
Language
English
Region
United States
NLM ID
9716531
PMCID
PMC4681096
Subset
IM
Grants
Wellcome Trust · 086482 · United Kingdom
Biotechnology and Biological Sciences Research Council · United Kingdom
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