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Analytical and Bioanalytical Chemistry

, Volume 406, Issue 4, pp 1163–1172 | Cite as

Electrochemical transduction of DNA hybridization at modified electrodes by using an electroactive pyridoacridone intercalator

  • Laurent BouffierEmail author
  • Bingquan Stuart Wang
  • André Roget
  • Thierry Livache
  • Martine Demeunynck
  • Pascal Mailley
Research Paper

Abstract

A synthetic redox probe structurally related to natural pyridoacridones was designed and electrochemically characterised. These heterocycles behave as DNA intercalators due to their extended planar structure that promotes stacking in between nucleic acid base pairs. Electrochemical characterization by cyclic voltammetry revealed a quasi-reversible electrochemical behaviour occurring at a mild negative potential in aqueous solution. The study of the mechanism showed that the iminoquinone redox moiety acts similarly to quinone involving a two-electron reduction coupled with proton transfer. The easily accessible potential region with respect to aqueous electro-inactive window makes the pyridoacridone ring suitable for the indirect electrochemical detection of chemically unlabelled DNA. Its usefulness as electrochemical hybridization indicator was assessed on immobilised DNA and compared to doxorubicin. The voltamperometric response of the intercalator acts as an indicator of the presence of double-stranded DNA at the electrode surface and allows the selective transduction of immobilised oligonucleotide hybridization at both macro- and microscale electrodes.

Keywords

DNA hybridization Redox intercalator Pyridoacridone Doxorubicin DNA microsensor 

References

  1. 1.
    Wang J (2000) From DNA biosensors to gene chips. Nucleic Acids Res 28(16):3011–3016CrossRefGoogle Scholar
  2. 2.
    Szunerits S, Bouffier L, Calemczuk R, Corso B, Demeunynck M, Descamps E, Defontaine Y, Fiche J-B, Fortin E, Livache T, Mailley P, Roget A, Vieil E (2005) Comparison of different strategies on DNA chip fabrication and DNA-sensing: optical and electrochemical approaches. Electroanalysis 17(22):2001–2017CrossRefGoogle Scholar
  3. 3.
    Cagnin S, Caraballo M, Guiducci C, Martini P, Ross M, SantaAna M, Danley D, West T, Lanfranchi G (2009) Overview of electrochemical DNA biosensors: new approaches to detect the expression of life. Sensors 9(4):3122–3148CrossRefGoogle Scholar
  4. 4.
    Mikkelsen SR (1996) Electrochemical biosensors for DNA sequence detection. Electroanalysis 8(1):15–19CrossRefGoogle Scholar
  5. 5.
    Mascini M, Palchetti I, Marrazza G (2001) DNA electrochemical biosensors. Fresenius J Anal Chem 369(1):15–22CrossRefGoogle Scholar
  6. 6.
    Gooding JJ (2002) Electrochemical DNA hybridization biosensors. Electroanalysis 14(17):1149–1156CrossRefGoogle Scholar
  7. 7.
    Cosnier S, Mailley P (2008) Recent advances in DNA biosensors. Analyst 133(8):984–991CrossRefGoogle Scholar
  8. 8.
    Sassolas A, Leca-Bouvier BD, Blum LJ (2008) DNA biosensors and microarrays. Chem Rev 108(1):109–139CrossRefGoogle Scholar
  9. 9.
    Paleček E, Bartošík M (2012) Electrochemistry of nucleic acids. Chem Rev 112(6):3427–3481CrossRefGoogle Scholar
  10. 10.
    Lisdat F, Schäfer D (2008) The use of electrochemical impedance spectroscopy for biosensing. Anal Bioanal Chem 391(5):1555–1567CrossRefGoogle Scholar
  11. 11.
    Gebala M, Stoica L, Neugebauer S, Schuhmann W (2009) Label-free detection of DNA hybridization in presence of intercalators using electrochemical impedance spectroscopy. Electroanalysis 21(3–5):325–331CrossRefGoogle Scholar
  12. 12.
    Grützke S, Abdali S, Schuhmann W, Gebala M (2012) Detection of DNA hybridization using electrochemical impedance spectroscopy and surface enhanced Raman scattering. Electrochem Commun 19:59–62CrossRefGoogle Scholar
  13. 13.
    Lassalle N, Mailley P, Vieil E, Livache T, Roget A, Correia JP, Abrantes LM (2001) Electronically conductive polymer grafted with oligonucleotides as electrosensors of DNA: preliminary study of real time monitoring by in situ techniques. J Electroanal Chem 509(1):48–57CrossRefGoogle Scholar
  14. 14.
    Garnier F, Korri-Youssoufi H, Srivastava P, Mandrand B, Delair T (1999) Toward intelligent polymers: DNA sensors based on oligonucleotide-functionalized polypyrroles. Synth Met 100(1):89–94CrossRefGoogle Scholar
  15. 15.
    Reisberg S, Piro B, Noël V, Pham MC (2005) DNA electrochemical sensor based on conducting polymer: dependence of the “signal-on” detection on the probe sequence localization. Anal Chem 77(10):3351–3356CrossRefGoogle Scholar
  16. 16.
    Caruana DJ, Heller A (1999) Enzyme-amplified amperometric detection of hybridization and of a single base pair mutation in an 18-base oligonucleotide on a 7-μm-diameter microelectrode. J Am Chem Soc 121(4):769–774CrossRefGoogle Scholar
  17. 17.
    Patolsky F, Lichtenstein A, Willner I (2001) Detection of single-base DNA mutations by enzyme-amplified electronic transduction. Nat Biotechnol 19(3):253–257CrossRefGoogle Scholar
  18. 18.
    Cosnier S, Ionescu RE, Herrmann S, Bouffier L, Demeunynck M, Marks RS (2006) An electro-enzymatic polypyrrole-intercalator sensor for determination of the West Nile Virus DNA. Anal Chem 78(19):7054–7057CrossRefGoogle Scholar
  19. 19.
    Wang J, Xu D, Kawde A-N, Polsky R (2001) Metal nanoparticle-based electrochemical stripping potentiometric detection of DNA hybridization. Anal Chem 73(22):5576–5581CrossRefGoogle Scholar
  20. 20.
    Authier L, Grossiord C, Brossier P, Limoges B (2001) Gold nanoparticle-based quantitative electrochemical detection of amplified human cytomegalovirus DNA using disposable microband electrodes. Anal Chem 73(18):4450–4456CrossRefGoogle Scholar
  21. 21.
    Erdem A, Ozsoz M (2002) Electrochemical DNA biosensors based on DNA-drug interactions. Electroanalysis 14(14):965–974CrossRefGoogle Scholar
  22. 22.
    Ferapontova E (2011) Electrochemical indicators for DNA electroanalysis. Curr Anal Chem 7(1):51–62CrossRefGoogle Scholar
  23. 23.
    Bouffier L, Demeunynck M, Milet A, Dumy P (2004) Reactivity of pyrido[4,3,2-kl]acridines: regioselective formation of 6-substituted derivatives. J Org Chem 69(23):8144–8147CrossRefGoogle Scholar
  24. 24.
    Bouffier L, Dinica R, Debray J, Dumy P, Demeumynck M (2009) Functionalization of A ring of pyridoacridine as a route toward greater structural diversity. Synthesis of an octacyclic analogue of eilatin. Bioorg Med Chem Lett 19(16):4836–4838CrossRefGoogle Scholar
  25. 25.
    Bouffier L, Baldeyrou B, Hildebrant M-P, Lansiaux A, David-Cordonnier M-H, Carrez D, Croisy A, Renaudet O, Dumy P, Demeunynck M (2006) Amino- and glycoconjugates of pyrido[4,3,2-kl]acridine. Synthesis, antitumor activity and DNA binding. Bioorg Med Chem 14(22):7520–7530CrossRefGoogle Scholar
  26. 26.
    Bouffier L, Gosse I, Demeunynck M, Mailley P, Bioelectrochemistry (2012) Electrochemistry and bioactivity relationship of 6-substituted-4H-pyrido[4,3,2-kl]acridin-4-one antitumor drug candidates. Bioelectrochemistry 88:103–109CrossRefGoogle Scholar
  27. 27.
    Molinski TF (1993) Marine pyridoacridine alkaloids: structure, synthesis, and biological chemistry. Chem Rev 93(5):1825–1838CrossRefGoogle Scholar
  28. 28.
    Ding O, Chichak K, Lown JW (1999) Pyrroloquinoline and pyridoacridine alkaloids from marine sources. Curr Med Chem 6(1):1–28Google Scholar
  29. 29.
    Delfourne E, Bastide J (2003) Marine pyridoacridine alkaloids and synthetic analogues as antitumor agents. Med Res Rev 23(2):234–252CrossRefGoogle Scholar
  30. 30.
    Marshall KM, Barrows LR (2004) Biological activities of pyridoacridines. Nat Prod Rep 21(6):731–751CrossRefGoogle Scholar
  31. 31.
    Wang B, Bouffier L, Demeunynck M, Mailley P, Roget A, Livache T, Dumy P (2004) New acridone derivatives for the electrochemical DNA-hybridisation labelling. Bioelectrochemistry 63(1–2):233–237CrossRefGoogle Scholar
  32. 32.
    Guedon P, Livache T, Martin F, Lesbre F, Roget A, Bidan G, Levy Y (2000) Characterization and optimization of a real-time, parallel, label-free, polypyrrole-based DNA sensor by surface plasmon resonance imaging. Anal Chem 72(24):6003–6009CrossRefGoogle Scholar
  33. 33.
    Livache T, Fouque B, Roget A, Marchand J, Bidan G, Téoule R, Mathis G (1998) Polypyrrole DNA chip on a silicon device: example of hepatitis C virus genotyping. Anal Biochem 255(2):188–194CrossRefGoogle Scholar
  34. 34.
    Crawford PW, Gross F, Lawson K, Chen CC, Dong Q, Liu DF, Luo Y, Szczepankiewicz BG, Heathcock CH (1997) Electrochemical properties of some biologically active quinone derivatives: furanquinones, pyridoquinones, and diplamine, a cytotoxic pyridoacridine alkaloid. J Electrochem Soc 144(11):3710–3715CrossRefGoogle Scholar
  35. 35.
    Matsumoto SS, Biggs J, Copp BR, Holden JA, Barrows LR (2003) Mechanism of ascididemin-induced cytotoxicity. Chem Res Toxicol 16(2):113–122CrossRefGoogle Scholar
  36. 36.
    Bouffier L, Lister K, Higgins SJ, Nichols RJ, Doneux T (2012) Electrochemical investigations of dissolved and surface immobilised 2-amino-1,4-naphthoquinones in aqueous solutions. J Electroanal Chem 664:80–87CrossRefGoogle Scholar
  37. 37.
    Deféver T, Druet M, Evrard D, Marchal D, Limoges B (2011) Real-time electrochemical PCR with a DNA intercalating redox probe. Anal Chem 83(5):1815–1821CrossRefGoogle Scholar
  38. 38.
    Lamm G, Pack GR (1990) Acidic domains around nucleic acids. Proc Natl Acad Sci U S A 87(22):9033–9036CrossRefGoogle Scholar
  39. 39.
    Minehan DS, Marx KA, Tripathy SK (1994) Kinetics of DNA binding to electrically conducting polypyrrole films. Macromolecules 27(3):777–783CrossRefGoogle Scholar
  40. 40.
    Palecek E, Fojta M, Tomschik M, Wang J (1998) Electrochemical biosensors for DNA hybridization and DNA damage. Biosens Bioelectron 13(6):621–628CrossRefGoogle Scholar
  41. 41.
    Piedade JAP, Fernandes IR, Oliveira-Brett AM (2002) Electrochemical sensing of DNA—adriamycin interactions. Bioelectrochemistry 56(1–2):81–83CrossRefGoogle Scholar
  42. 42.
    Oliveira-Brett AM, Vivan M, Fernandes IR, Piedade JAP (2002) Electrochemical detection of in situ adriamycin oxidative damage to DNA. Talanta 56(5):959–970CrossRefGoogle Scholar
  43. 43.
    Chiti G, Marrazza G, Mascini M (2001) Electrochemical DNA biosensor for environmental monitoring. Anal Chim Acta 427(2):155–164CrossRefGoogle Scholar
  44. 44.
    Livache T, Roget A, Dejean E, Barthet C, Bidan G, Teoule R (1994) Preparation of a DNA matrix via an electrochemically directed copolymerization of pyrrole and oligonucleotides bearing a pyrrole group. Nucleic Acids Res 22(15):2915–2921CrossRefGoogle Scholar
  45. 45.
    Bouffier L, Yiu HHP, Rosseinsky MJ (2011) Chemical grafting of a DNA intercalator probe onto functional iron oxide nanoparticles: a physicochemical study. Langmuir 27(10):6185–6192CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Laurent Bouffier
    • 1
    • 2
    Email author
  • Bingquan Stuart Wang
    • 3
    • 4
  • André Roget
    • 3
  • Thierry Livache
    • 3
  • Martine Demeunynck
    • 5
  • Pascal Mailley
    • 3
    • 6
  1. 1.Univ. Bordeaux, ISM, UMR 5255TalenceFrance
  2. 2.CNRS, ISM, UMR 5255TalenceFrance
  3. 3.CREAB/SI3M/DRFMC, UMR 5819, CEA GrenobleGrenoble cedex 9France
  4. 4.Genzyme CorporationFraminghamUSA
  5. 5.Department of Pharmacomolecular ChemistryUMR 5063 & FR 2607 CNRS/Joseph Fourier UniversityGrenoble cedex 9France
  6. 6.Laboratory of Electricity StorageLSE/DTS, CEALe Bourget du Lac cedexFrance

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