Structural and thermodynamic studies on the interaction of iminium and alkanolamine forms of sanguinarine with hemoglobin

Journal of Physical Chemistry B

Volumn 118, Issue 14, 2014, Pages 3771-3784

  Hazra, Soumitra ^a   Suresh Kumar, Gopinatha ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALOIDS; BINDING ENERGY; DICHROISM; FLUORESCENCE; HEMOGLOBIN; HYDROGEN BONDS; HYDROPHOBICITY; METABOLITES; NITROGEN COMPOUNDS; PROTEINS; SPECTROSCOPIC ANALYSIS;

HYDROGEN BONDING INTERACTIONS; HYDROPHOBIC INTERACTIONS; INTERACTION DYNAMICS; MOLECULAR DISTANCES; SPECTROSCOPIC STUDIES; SYNCHRONOUS FLUORESCENCE; THERMODYNAMIC STUDIES; THREE-DIMENSIONAL FLUORESCENCES;

ALKANOLAMINES;

ALKALOID; AMINE; ANTINEOPLASTIC AGENT; BENZOPHENANTHRIDINE DERIVATIVE; HEMOGLOBIN; IMINE; ISOQUINOLINE DERIVATIVE; PROTEIN BINDING; SANGUINARINE;

CHEMISTRY; HUMAN; HYDROGEN BOND; METABOLISM; PH; SPECTROFLUOROMETRY; TEMPERATURE; THERMODYNAMICS;

ALKALOIDS; AMINES; ANTINEOPLASTIC AGENTS; BENZOPHENANTHRIDINES; HEMOGLOBINS; HUMANS; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; IMINES; ISOQUINOLINES; PROTEIN BINDING; SPECTROMETRY, FLUORESCENCE; TEMPERATURE; THERMODYNAMICS;

EID: 84898466147     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp409764z     Document Type: Article

References (72)

1. Khazaeinia, T.; Ramsey, A. A.; Tam, Y. K. The Effects of Exercise on the Pharmacokinetics of Drugs J. Pharm. Pharm. Sci. 2000, 3, 292-302
2. Martinez, M. N.; Amidon, G. L. A Mechanistic Approach to Understanding the Factors Affecting Drug Absorption: A Review of Fundamentals J. Clin. Pharmacol. 2002, 42, 620-643
3. Connie, C. W.; Hsia, M. D. Respiratory Function of Hemoglobin N. Engl. J. Med. 1998, 338, 239-248
4. Krueger, S.; Nossal, R. SANS Studies of Interacting Hemoglobin in Intact Erythrocytes Biophys. J. 1988, 53, 97-105
5. Perutz, M. F.; Rossmann, M. G.; Cullis, A. F.; Muirhead, H.; Will, G.; North, A. C. T. Structure of Haemoglobin: A Three-Dimensional Fourier Synthesis at 5.5-Å. Resolution, Obtained by X-Ray Analysis Nature 1960, 185, 416-422
6. Perutz, M. F. X-ray Analysis of Hemoglobin Science 1963, 140, 863-869
7. Facchini, P. J.; Hagel, J. M.; Liscombe, D. K.; Loukanina, N.; MacLeod, B. P.; Samanani, N.; Zulak, K. G. Opium Poppy: Blueprint for an Alkaloid Factory Phytochem. Rev. 2007, 6, 97-124
8. Abizov, E. A.; Tolkachev, O. N.; Kopylova, I. E.; Luferov, A. N. Distribution of the Sum of Sanguinarine and Chelerythrine in the Above-Ground Part of Macleaya Microcarpa Pharm. Chem. J. 2003, 37, 413-414
9. Vavrečková, C.; Gawlik, I.; Müller, K. Benzophenanthridine Alkaloids of Chelidonium Majus; I. Inhibition of 5- and 12-Lipoxygenase by a Non-Redox Mechanism Planta Med. 1996, 62, 397-401
10. Mahady, G. B.; Beecher, C. W. W. Quercetin-Induced Benzophenanthridine Alkaloid Production in Suspension Cell Cultures of Sanguinaria canadensis. Planta Med. 1994, 60, 553-557
11. Han, M. H.; Kim, G.-Y.; Yoo, Y. H.; Choi, Y. H. Sanguinarine Induces Apoptosis in Human Colorectal Cancer HCT-116 Cells Through ROS-Mediated Egr-1 Activation and Mitochondrial Dysfunction Toxicol. Lett. 2013, 220, 157-166
12. Han, M. H.; Park, C.; Jin, C.-Y.; Kim, G.-Y.; Chang, Y.-C.; Moon, S.-K.; Kim, W.-J.; Choi, Y. H. Apoptosis Induction of Human Bladder Cancer Cells by Sanguinarine Through Reactive Oxygen Species-Mediated Up-Regulation of Early Growth Response Gene-1 PLoS ONE 2013, 8, e63425
13. Lee, J. S.; Jung, W. K.; Jeong, M. H.; Yoon, T. R.; Kim, H. K. Sanguinarine Induces Apoptosis of HT-29 Human Colon Cancer Cells via the Regulation of Bax/Bcl-2 Ratio and Caspase-9-dependent Pathway Int. J. Toxicol. 2012, 31, 70-77
14. Xu, J.-Y.; Meng, Q.-H.; Chong, Y.; Jiao, Y.; Zhao, L.; Rosen, E. M.; Fan, S. Sanguinarine Inhibits Growth of Human Cervical Cancer Cells Through the Induction of Apoptosis Oncol. Rep. 2012, 28, 2264-2270
15. Sun, M.; Liu, C.; Nadiminty, N.; Lou, W.; Zhu, Y.; Yang, J.; Evans, C. P.; Zhou, Q.; Gao, A. C. Inhibition of Stat3 Activation by Sanguinarine Suppresses Prostate Cancer Cell Growth and Invasion Prostate 2012, 72, 82-89
16. Slaninová, I.; Pěnčíková, K.; Urbanová, J.; Slanina, J.; Táborská, E. Antitumour Activities of Sanguinarine and Related Alkaloids Phytochem. Rev. 2014, 13, 51-58
17. Tsukamoto, H.; Kondo, S.; Mukudai, Y.; Nagumo, T.; Yasuda, A.; Kurihara, Y.; Kamatani, T.; Shintani, S. Evaluation of Anticancer Activities of Benzo[c]phenanthridine Alkaloid Sanguinarine in Oral Squamous Cell Carcinoma Cell Line Anticancer Res. 2011, 31, 2841-2846
18. Janovska, M.; Kubala, M.; Simanek, V.; Ulrichova, J. Fluorescence of Sanguinarine: Fundamental Characteristics and Analysis of Interconversion Between Various Forms Anal. Bioanal. Chem. 2009, 395, 235-240
19. Janovska, M.; Kubala, M.; Simanek, V.; Ulrichova, J. Fluorescence of Sanguinarine: Spectral Changes on Interaction with Amino Acids Phys. Chem. Chem. Phys. 2010, 12, 11335-11341
20. Sen, A.; Maiti, M. Interaction of Sanguinarine Iminium and Alkanolamine Form with Calf Thymus DNA Biochem. Pharmacol. 1994, 48, 2097-2102
21. Hossain, M.; Kabir, A.; Suresh Kumar, G. Binding of the Anticancer Alkaloid Sanguinarine with tRNA(phe): Spectroscopic and Calorimetric Studies J. Biomol. Struct. Dyn. 2012, 30, 223-234
22. Maiti, M.; Suresh Kumar, G. Biophysical Aspects and Biological Implications of the Interaction of Benzophenanthridine Alkaloids with DNA Biophys. Rev. 2009, 1, 119-129
23. Bhadra, K.; Suresh Kumar, G. Therapeutic Potential of Nucleic Acid-Binding Isoquinoline Alkaloids: Binding Aspects and Implications for Drug Design Med. Res. Rev. 2011, 31, 821-862
24. Bessi, I.; Bazzicalupi, C.; Richter, C.; Jonker, H. R. A.; Saxena, K.; Sissi, C.; Chioccioli, M.; Bianco, S.; Bilia, A. R.; Schwalbe, H. Spectroscopic, Molecular Modeling, and NMR-Spectroscopic Investigation of the Binding Mode of the Natural Alkaloids Berberine and Sanguinarine to Human Telomeric G-Quadruplex DNA ACS Chem. Biol. 2012, 7, 1109-1119
25. Giri, P.; Suresh Kumar, G. Molecular Recognition of poly(A) Targeting by Protoberberine Alkaloids: In Vitro Biophysical Studies and Biological Perspectives Mol. BioSyst. 2010, 6, 81-88
26. Roy Chowdhury, S.; Islam, M. M.; Suresh Kumar, G. Binding of the Anticancer Alkaloid Sanguinarine to Double Stranded RNAs: Insights into the Structural and Energetics Aspects Mol. BioSyst. 2010, 6, 1265-1276
27. Hossain, M.; Khan, A. Y.; Suresh Kumar, G. Interaction of the Anticancer Plant Alkaloid Sanguinarine with Bovine Serum Albumin PLoS ONE 2011, 6, e18333
28. Hossain, M.; Khan, A. Y.; Suresh Kumar, G. Study on the Thermodynamics of the Binding of Iminium and Alkanolamine Forms of the Anticancer Agent Sanguinarine to Human Serum Albumin J. Chem. Thermodyn. 2012, 47, 90-99
29. Cox, M. M.; Phillips, Jr., G. N. Handbook of Proteins: Structure, Function and Methods; John Wiley & Sons Ltd.: West Sussex, U.K., 2007; Vol. 2.
30. Hazra, S.; Hossain, M.; Suresh Kumar, G. Binding of Isoquinoline Alkaloids Berberine, Palmatine and Coralyne to Hemoglobin: Structural and Thermodynamic Characterization Studies Mol. BioSyst. 2013, 9, 143-153
31. Jones, R. R.; Harkrader, R. J.; Southard, G. L. The Effect of pH on Sanguinarine Iminium Ion Form J. Nat. Prod. 1986, 49, 1109-1111
32. Hazra, S.; Hossain, M.; Suresh Kumar, G. Studies on α-, β-, and γ-Cyclodextrin Inclusion Complexes of Isoquinoline Alkaloids Berberine, Palmatine and Coralyne J. Incl. Phenom. Macrocycl. Chem. 2014, 78, 311-323
33. Islam, M. M.; Sinha, R.; Suresh Kumar, G. RNA Binding Small Molecules: Studies on t-RNA Binding by Cytotoxic Plant Alkaloids Berberine, Palmatine and the Comparison to Ethidium Biophys. Chem. 2007, 125, 508-520
34. Antonini, E.; Brunori, M. Hemoglobins and Myoglobins in their Reactions with Ligands; North Holland Publishing Co.: Amsterdam, 1971; Chapters 2 and 3.
35. 19F NMR Characterization of the Thermodynamics and Dynamics of the Acid-Alkaline Transition in a Reconstituted Sperm Whale Metmyoglobin J. Am. Chem. Soc. 2005, 127, 4146-4147
36. Shu, F.; Ramakrishnan, V.; Schoenborn, B. P. Enhanced Visibility of Hydrogen Atoms by Neutron Crystallography on Fully Deuterated Myoglobin Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 3872-3877
37. Benesi, H. A.; Hildebrand, J. H. A spectrophotometric investigation of the interaction of iodine with aromatic hydrocarbons J. Am. Chem. Soc. 1949, 71, 2703-2707
38. Alpert, B.; Jameson, D. M.; Weber, G. Tryptophan Emission From Human Hemoglobin and its Isolated Subunits J. Photochem. Photobiol. 1980, 31, 1-4
39. Perutz, M. F.; Fermi, G.; Abraham, D. J.; Poyart, C.; Bursaux, E. Hemoglobin as a Receptor of Drugs and Peptides: X-ray Studies of the Stereochemistry of Binding J. Am. Chem. Soc. 1986, 108, 1064-1078
40. Burstein, E. A.; Vedenkina, N. S.; Ivkova, M. N. Fluorescence and the Location of Tryptophan Residues in Protein Molecules Photochem. Photobiol. 1973, 18, 263-279
41. Lakowicz, J. R. Principles of Fluorescence Spectroscopy; Plenum Press: New York, 1999.
42. MacDonald, B. C.; Lvin, S. J.; Patterson, H. Correction of Fluorescence Inner Filter Effects and the Partitioning of Pyrene to Dissolved Organic Carbon Anal. Chim. Acta 1997, 338, 155-162
43. Lakowicz, J. R. Principles of Fluorescence Spectroscopy, 3 rd ed.; Springer: New York, 2006.
44. Manna, A.; Chakravorti, S. Role of Block Copolymer-Micelle Nanocomposites in Dye-Bovine Serum Albumin Binding: A Combined Experimental and Molecular Docking Study Mol. BioSyst. 2013, 9, 246-257
45. Tong, J.-Q.; Tian, F.-F.; Li, Q.; Li, L.-L.; Xiang, C.; Liu, Y.; Dai, J.; Jiang, F.-L. Probing the Adverse Temperature Dependence in the Static Fluorescence Quenching of BSA Induced by a Novel Anticancer Hydrazone Photochem. Photobiol. Sci. 2012, 11, 1868-1879
46. Tian, F.-F.; Li, J.-H.; Jiang, F.-L.; Han, X.-L.; Xiang, C.; Ge, Y.-S.; Li, L.-L.; Liu, Y. The Adsorption of an Anticancer Hydrazone by Protein: An Unusual Static Quenching Mechanism RSC Adv. 2012, 2, 501-513
47. Tian, F.-F.; Jiang, F.-L.; Han, X.-L.; Xiang, C.; Ge, Y.-S.; Li, J.-H.; Zhang, Y.; Li, R.; Ding, X.-L.; Liu, Y. Synthesis of a Novel Hydrazone Derivative and Biophysical Studies of its Interactions with Bovine Serum Albumin by Spectroscopic, Electrochemical, and Molecular Docking Methods J. Phys. Chem. B 2010, 114, 14842-14853
48. Martin, R. S.; Henningsen, R. A.; Suen, A.; Apparsundaram, S.; Leung, B.; Jia, Z.; Kondru, R. K.; Milla, M. E. Kinetic and Thermodynamic Assessment of Binding of Serotonin Transporter Inhibitors J. Pharmacol. Exp. Ther. 2008, 327, 991-1000
49. Freyer, M. W.; Lewis, E. A. Isothermal Titration Calorimetry: Experimental Design, Data Analysis, and Probing Macromolecule/Ligand Binding and Kinetic Interactions Methods Cell Biol. 2008, 84, 79-113
50. Landau, M. A.; Markovich, M. N.; Piruzyan, L. A. Studies of the Thermodynamics and Nature of Interaction Between Serum Albumin and Penicillins Biochim. Biophys. Acta 1977, 493, 1-9
51. Ross, P. D.; Subramanian, S. Thermodynamics of Protein Association Reactions: Forces Contributing to Stability Biochemistry 1981, 20, 3096-3102
52. Chaires, J. B. Calorimetry and Thermodynamics in Drug Design Annu. Rev. Biophys. 2008, 37, 135-151
53. Spolar, R. S.; Record, M. T., Jr. Coupling of Local Folding to Site-Specific Binding of Proteins to DNA Science 1994, 263, 777-784
54. Chaires, J. B. Energetics of Drug-DNA Interactions Biopolymers 1997, 44, 201-215
55. Guthrie, K. M.; Parenty, A. D.; Smith, L. V.; Cronin, L.; Cooper, A. Microcalorimetry of Interaction of Dihydro-imidazo-phenanthridinium (DIP)-Based Compounds with Duplex DNA Biophys. Chem. 2007, 126, 117-123
56. Kapanidis, A. N.; Laurence, T. A.; Lee, N. K.; Margeat, E.; Kong, X.; Weiss, S. Alternating-Laser Excitation of Single Molecules Acc. Chem. Res. 2005, 38, 523-533
57. Stryer, L.; Haugland, R. P. Energy Transfer: A Spectroscopic Ruler Proc. Natl. Acad. Sci. U.S.A. 1967, 58, 719-726
58. Valeur, B.; Brochon, J. C. New Trends in Fluorescence Spectroscopy; Springer: Berlin, 1999.
59. Haouz, A.; Mohsni, S. E.; Zentz, C.; Merola, F.; Alpert, B. Heterogeneous Motions Within Human Apohemoglobin Eur. J. Biochem. 1999, 264, 250-257
60. Valeur, B. Molecular Fluorescence: Principles and Applications: Wiley VCH Verlag GmbH: Weinheim, Germany, 2001.
61. Lloyd, J. B. F. Synchronized Excitation of Fluorescence Emission Spectra Nat. Phys. Sci. 1971, 231, 64-65
62. Miller, J. N. Recent Advances in Molecular Luminescence Analysis Proc. Anal. Div. Chem. Soc. 1979, 16, 203-208
63. Woody, R. W. Circular Dichroism Method. Enzymol 1995, 246, 34-71
64. Woody, R. W. Theory of Circular Dichroism of Proteins, in Circular Dichroism and the Conformational Analysis of Biomolecules: Plenum Press: New York, 1996; pp 25-30.
65. Chen, Y. H.; Yang, J. T.; Martinez, H. M. Determination of the Secondary Structures of Proteins by Circular Dichroism and Optical Rotatory Dispersion Biochemistry 1972, 11, 4120-4131
66. Mandal, P.; Bardhan, M.; Ganguly, T. A Detailed Spectroscopic Study on the Interaction of Rhodamine 6G with Human Hemoglobin J. Photochem. Photobiol. B 2010, 99, 78-86
67. Lu, Z.; Zhang, Y.; Liu, H.; Yuan, J.; Zheng, Z.; Zou, G. Transport of a Cancer Chemopreventive Polyphenol, Resveratrol: Interaction with Serum Albumin and Hemoglobin J. Fluoresc. 2007, 17, 580-587
68. Kang, J.; Liu, Y.; Xie, M.-X.; Li, S.; Jiang, M.; Wang, Y.-D. Interactions of Human Serum Albumin with Chlorogenic Acid and Ferulic Acid Biochim. Biophys. Acta 2004, 1674, 205-214
69. Stryer, L. The Interaction of a Naphthalene Dye with Apomyoglobin and Apohemoglobin: A fluorescent Probe of Non-polar Binding Sites J. Mol. Biol. 1965, 13, 482-495
70. Parul, D. A.; Bokut, S. B.; Milyutin, A. A.; Petrov, E. P.; Nemkovich, N. A.; Sobchuk, A. N.; Dzhagarov, B. M. Time-resolved Fluorescence Reveals Two Binding Sites of 1,8-ANS in Intact Human Oxyhemoglobin J. Photochem. Photobiol. B 2000, 58, 156-162
71. Matulis, D.; Lovrien, R. 1-Anilino-8-Naphthalene Sulfonate Anion-Protein Binding Depends Primarily on Ion Pair Formation Biophys. J. 1998, 74, 422-429
72. Syakhovich, V. E.; Parul, D. A.; Ruta, E. Y.; Bushuk, B. A.; Bokut, S. B. 1,8-Anilinonaphthalene Sulfonate Binds to Central Cavity of Human Hemoglobin Biochem. Biophys. Res. Commun. 2004, 317, 761-767