Sequence specific binding of beta carboline alkaloid harmalol with deoxyribonucleotides: Binding heterogeneity, conformational, thermodynamic and cytotoxic aspects

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Sarkar, Sarita ^a   Pandya, Prateek ^a,b   Bhadra, Kakali ^a  

^a UNIVERSITY OF KALYANI   (India)

^b UNIVERSITY OF RAJASTHAN   (India)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEOTIDE; HARMALOL; POLYMER; POLYNUCLEOTIDE; HARMALINE;

ARTICLE; BASE PAIRING; BINDING KINETICS; CELL VIABILITY; CHEMOTHERAPY; CIRCULAR DICHROISM; CONCENTRATION RESPONSE; CYTOTOXICITY; DRUG PROTEIN BINDING; ENTHALPY; HUMAN; HUMAN CELL; HYDROPHOBICITY; IC50; IN VITRO STUDY; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR DOCKING; MTT ASSAY; PHYSICAL CHEMISTRY; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STRUCTURE; QUANTUM YIELD; SPECTROPHOTOMETRY; THERMODYNAMICS; VISCOSITY; ANALOGS AND DERIVATIVES; CONFORMATION; METABOLISM; TUMOR CELL LINE;

CELL LINE, TUMOR; CIRCULAR DICHROISM; HARMALINE; HUMANS; MOLECULAR CONFORMATION;

EID: 84907452622     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108022     Document Type: Article

References (73)

1. Hurley LH (2001) Secondary DNA structures as molecular targets for cancer therapeutics. Biochem Soc Trans 29: 692-696.
2. Dervan PB (2001) Molecular recognition of DNA by small molecules. Bioorg Med Chem 9: 2215-2235.
3. Neidle S (2001) DNA minor-groove recognition by small-molecules. Nat Prod Rep 18: 291-309.
4. Maiti M, Suresh Kumar G (2007) Molecular aspects on the interaction of protoberberine, benzophenanthridine and aristolochia group of alkaloids with nucleic acid structures and biological perspectives. Med Res Rev 27: 649-695.
5. Bhadra K, Suresh Kumar G (2011) Therapeutic potential of nucleic acid binding isoquinoline alkaloids: Binding aspects and implications for drug design. Med Res Rev 31: 821-862.
6. Cao R, Peng W, Wang Z, Xu A (2007) β-Carboline alkaloids: Biochemical and pharmacological functions. Curr Med Chem 14: 479-500.
7. Patel K, Gadewar M, Tripathi R, Prasad SK, Patel DK (2012) A review on medicinal importance, pharmacological activity and bioanalytical aspects of β-carboline alkaloid "Harmine". Asian Pacific J Trop Biomed 2: 660-664.
8. Tweedie DJ, Burke MD (1986) Metabolism of the β-carbolines, harmine and harmol, by liver microsomes from phenobarbitone or 3-methylcholantrene-treated mice; identification and quantitation of two novel harmine metabolites. Drug Metab Dispos 15: 74-82.
9. Kim H, Sablin SO, Ramsay RR (1997) Inhibition of monoamine oxidase A by β-carboline de rivates. Arch Biochem Biophys 337: 137-142.
10. Glennon RA, Dukat M, Brella B, Hong SS, Constantino L, et al. (2000) Binding of β-carbolines and relating agents at serotonin (5-HT2and 5-HT1A) dopamine (D2) and benzodiazepines receptors. Drug Alcohol Depend 60: 121-132.
11. Funayama Y, Nishi K, Wakabayashi K, Nagao M, Simio K, et al. (1996) Effects of β and γ carboline derivatives on DNA topoisomerase activities. Mutat Res 349: 183-191.
12. De Meester C (1995) Genotoxic potential of β-carbolines: a review. Mutat Res 339: 139-153.
13. Taira Z, Kanzawas S, Dohara C, Ishida S, Matsumoto M, et al. (1997) Intercalation of six beta-carboline derivatives into DNA. Jpn J Toxocol Environ Health 43: 83-91.
14. Remsen JF, Cerutti PA (1979) Inhibition of DNA-repair and DNA synthesis by Harman in human alveolar tumor cells. Biochem Biophys Res Commun 86: 135-149.
15. Lamchouri F, Settaf A, Cherrah Y, Zemzami M, Lyoussi B, et al. (1999) Antitumor principles from Paganum harmala seeds. Therapy 54: 753-758.
16. Uezono T, Maruyama W, Matsubara K, Naoi M, Shimizu K, et al. (2001) Norharman an indoleamine-derived betacarboline, but not Trp-P-2, a gamma-carboline, induces apoptotic cell death in human neuroblantoma SH-SY5Y cells. J Neural Transm 108: 943-953.
17. Hayashi K, Nagao M, Sugimura T (1977) Interactions of norharman and harman with DNA. Nucl Acids Res 4: 3679-3685.
18. Pezzuto JM, Lau PP, Luh Y, Moore PD, Wogan GN, et al. (1980) There is a correlation between the DNA affinity and mutagenicity of several 3-amino-1-methyl-5H-pyrido[4,3-b]indoles. Proc Natl Acad Sci USA 77: 1427-1431.
19. Duportail G (1981) Linear and circular dichroism of harmine and harmaline interacting with DNA Inter J Biol Macro 3: 188-192.
20. Xiao S, Lin W, Wang C, Yang M (2001) Synthesis and biological evaluation of DNA targeting flexible side-chain substituted β-carboline derivatives. Bioorg Med Chem Lett 11: 437-441.
21. Du W, Cao R, Peng W, Chen H, Ma Y, et al. (2005) DNA binding properties of 9-substituted harmine derivatives. Biochem Biophys Res Comm 338: 1557-1563.
22. Guan H, Liu X, Peng W, Cao R, Ma Y, et al. (2006) β-carboline derivatives: Novel photosensitizers that intercalate into DNA to cause direct DNA damage in photodynamic therapy. Biochem Biophys Res Comm 342: 894-901
23. Nafisi S, Bonsaii M, Maali P, Khalilzadeh MA, Manouchehri F (2010) β-carboline alkaloids bind DNA. J Photochem Photobiol B Biol 100: 84-91.
24. Sarkar S, Bhadra K (2014) Binding of alkaloid harmalol to DNA Photophysical and calorimetric approach. J Photochem Photobiol B Biol 130: 272-280.
25. Ren J, Chaires JB (1999) Sequence and structural selectivity of nucleic acid binding ligands. Biochemistry 38: 16067-16075.
26. Chaires JB (2005) Competition dialysis: an assay to measure the structural selectivity of drug-nucleic acid interactions. Curr Med Chem Anti Cancer Agents 5: 339-352.
27. Chaires JB (1983) Equilibrium studies on the interaction of daunomycin with deoxypolynucleotides. Biochemistry 22: 4204-4211.
28. Graves DE, Krugh TR (1983) Adriamycin and daunorubicin bind in a cooperative manner to deoxyribonucleic acid. Biochemistry 22: 3941-3947.
29. Wilson WD, Wang YH, Krishnamoorty CR, Smith JC (1985) Poly(dA). poly(dT) exists in an unusual conformation under physiological conditions: propidium binding to poly(dA).poly(dT) and poly[d(A-T)].poly[d(A-T)]. Biochemistry 24: 3991-3999.
30. Wadkin RM, Graves DE (1989) Thermodynamics of the interactions of m-AMSA and o-AMSA with nucleic acids: influence of ionic strength and DNA base composition. Nucleic Acids Res 17: 9933-9946.
31. Scaria PV, Shafer RH (1991) Binding of ethidium bromide to a DNA triple helix. Evidence for intercalation. J Biol Chem 266: 5417-5423.
32. Jones RL, Zon G, Krishnamoorty CR, Wilson WD (1986) Sequence dependent cooperative interactionsin A/T-containing oligo-and polydeoxyribonucleotides. Biochemistry 25: 7431-7439.
33. Marky LA Jr, Macgregor RB (1990) Hydration of dA.dT polymers: role of water in the thermodynamics of ethidium and propidium intercalation. Biochemistry 29: 4805-4811.
34. Rosenberg LS, Carvlin MJ, Krugh TR (1986) The antitumor agent mitoxantrone binds cooperatively to DNA: evidence for heterogeneity in DNA conformation, Biochemistry 25: 1002-1008.
35. Elmore RH, Wadkin RM, Graves DE (1988) Cooperative binding of m-AMSA to nucleic acids. Nucleic Acids Res 16: 9707-9719.
36. Bhadra K, Maiti M, Suresh Kumar G (2007) Molecular recognition of DNA by small molecules: AT base pair specific intercalative binding of cytotoxic plant alkaloid palmatine. Biochim Biophys Acta 1770: 1071-1080.
37. Bhadra K, Maiti M, Suresh G (2008) Berberine-DNA complexation: New insights into the cooperative binding and energetic aspects. Biochim Biophys Acta 1780: 1054-1061.
38. Hogan M, Dattagupta N, Crothers DM (1979) Trasmission of allosteric effects in DNA. Nature 278: 521-524.
39. Qu X, Trent JO, Fokt I, Priebe W, Chaires JB (2000) Allosteric, chiral-selective drug binding to DNA. Proc Natl Acad Sci USA 97: 12032-12037.
40. Saenger W (1993) Principles of Nucleic Acid Structures, Springer-Verlag, New York, 1984.
41. Bohne C, Faulhaber K, Giese B, Häfner A, Hofmann A, et al. (2005) Studies on the mechanism of the photo-induced DNA damage in the presence of acridizinium salts-involvement of singlet oxygen and an unusual source for hydroxyl radicals. J Am Chem Soc, 127: 76-85
42. Basu P, Kumar GS (2014) Elucidation of the DNA binding specificity of the natural plant alkaloid chelerythrine: A biophysical approach. J. Photchem Photobiol B: Biol, 138: 282-294.
43. Waring MJ (1981) DNA modification and cancer. Ann Rev Biochem 50: 159-192.
44. Neidle S, Waring MJ (1981) Molecular Aspects of Anticancer Action, Macmillan Press Ltd., Basingstoke, U.K.
45. Islam MM, Roy Chowdhury S, Suresh Kumar G (2009) Spectroscopic and calorimetric studies on the binding of alkaloids berberine, palmatine and coralyne to double stranded RNA polynucleotides. J Phys Chem B 113: 1210-1224.
46. Brien R O', Haq I, Applications of biocalorimetry: binding, stability and enzyme kinetics, in: Ladbury JE, Doyle M (Eds.), Biocalorimetry, Wiley John and Sons Ltd, West Sussex, England, 2004.
47. Saboury AA (2006) A review of the ligand binding studies by isothermal titration calorimetry. J Iranian Chem Soc 3: 1-21.
48. Buurma NJ, Haq I (2007) Advances in the analysis of isothermal titration calorimetry data for ligand-DNA interactions. Methods 42: 162-172.
49. Breslauer KJ, Remeta DP, Chou WY, Ferrante R, Curry J, et al. (1987) Enthalpy-entropy compensations in drug-DNA binding studies. Proc Natl Acad Sci USA 84: 8922-8926.
50. Herrera JE, Chaires JB (1989) A premelting conformational transition in poly(dA).poly(dT) coupled to daunomycin binding. Biochemistry 28: 1993-2000.
51. Guthrie KM, Parenty ADC, Smith LV, Cromin L, Cooper A (2007) Microcalorimetry of interaction of dihydro-imidazo-phenanthridinium (DIP) based compounds with duplex DNA. Biophys Chem 126: 117-123.
52. Chaires JB (1998) Energetics of drug-DNA interactions. Biopolymers 44: 201-215.
53. Haq I (2002) Thermodynamics of drug-DNA interactions Part II: the thermodynamics of drug-biopolymers interaction. Arch Biochem Biophys 403: 1-15.
54. Ren J, Jenkins TC, Chaires JB (2000) Energetics of DNA intercalation reactions. Biochemistry 39: 8439-8447.
55. Ha JH, Soplar RS Jr, Record MT (1989) Role of the hydrophobic effect in stability of site-specific protein-DNA complexes. J Mol Biol 209: 801-816.
56. Hossain M, Giri P, Suresh Kumar G (2007) DNA intercalation by quinacrine and methylene blue: a comparative binding and thermodynamic characterization study. DNA Cell Biol doi: 10.1089/dna.2007.0652.
57. Pandya P, Islam MM, Kumar GS, Jayaram B, Kumar S (2010) DNA minor groove binding of small molecules: Experimental and computational evidence. J Chem Sci 122: 247-257.
58. Islam MM, Chakraborty M, Pandya P, Al Masum A, Gupta N, et al. (2013) Binding of DNA with Rhodamine B: Spectroscopic and molecular modeling studies. Dyes and Pigments 99: 412-422.
59. El Gendy MAM, Soshilov AA, Denison MS, El Kadi AOS (2012) Harmaline and harmalol inhibit the carcinogen activating enzyme CYP1A1 via transcriptional and posttranslational mechanisms. Food Chem Toxicol 50: 353-362.
60. Moura DL, Richter MF, Boeira JM, Henriques JAP, Saffi J (2007) Antioxidant properties of betacrboline alkaloids are related to antimutagenic and antigenotoxic activities. Mutagenesis 22: 293-302.
61. M. Butler, Animal cell culture and technology, 2ndEdition, Taylor and Francis Publishers, 2004.
62. Biondic CM, Balsells RE (1993) Photochemical reaction of harmalol. Part2. Electronicspectra. J Chem Soc Perkin Trans 2: 887-903.
63. Alomer M L, Gonzalez MM, Balsells RE, Cabrerizo FM. (2014) Comment on "Binding of alkaloid harmalol to DNA: Photophysical and calorimetric approach. J Photochem Photobiol B: Biol 136: 26-28.
64. Sen A, Ray A, Maiti M (1996) Thermodynamics of the interactions of sanguinarine with DNA: influence of ionic strength and base composition. Biophys Chem 59: 155-170.
65. Mosmann T (1983) Rapid calorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63.
66. Tang F, Wang D, Wuan C, Uuang D, Wu Y, et al. (2009) Berberine inhibits metastasis of nasopharyngeal carcinoma 5-8F cells by targeting Rho kinase mediated Ezrin phosphorylation at threonine 567. J Biol Chem 284: 27456-27466.
67. Chaires JB, Dattagupta N, Crothers DM (1982) Studies on interaction of anthracyclin antibiotics and deoxyribonucleic acid: equilibrium binding studies on interaction of daunomycin with deoxyribonucleic acid. Biochemistry 21: 3933-3940.
68. McGhee JD, von Hippel PH (1974) Theoretical aspects of DNA-protein interactions: cooperative and non-cooperative binding of large ligands to one-dimensional homogeneous lattice. J Mol Biol 86: 469-489.
69. Sinha R, Islam MM, Bhadra K, Suresh Kumar G, Banerjee A, et al. (2006) The binding of DNA intercalating and non-intercalating compounds to A-form and protonated form of poly(rC). poly(rG): Spectroscopic and viscometric study. Bioorg Med Chem 14: 800-814.
70. Trott O, Olson A (2010) Auto Dock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comp Chem 31: 455-461.
71. Seeliger D, De Groot BL (2010) Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J Comput Aided Mol Des 24: 417-422.
72. Chang MW, Ayeni C, Breuer S, Torbett BE (2010) Virtual Screening for HIV Protease Inhibitors: A Comparison of AutoDock 4 and Vina, PLoS ONE 5: e11955.doi:10.1371/journal.pone.0011955.
73. Takatsuka Y, Chen C, Nikaido H (2010) Mechanism of recognition of compounds of diverse structures by the multidrug efflux pump AcrB of Escherichia coli. PNAS (USA) 107: 6559-6565.