Abstract
In order to use tetrapyrrolic macrocyclic species in medical applications, the interactions of bovine serum albumin (BSA) with tetrakis-para-carboxyphenyl-porphyrin (H2T(p-COOH) PP or TCPP) and Chlorin e6 (Ce6), under different conditions, were investigated by fluorescence spectroscopy and UV–VIS absorption spectroscopy and contrasted with molecular docking study. The binding constant (Kb) values at three different temperatures were calculated using the modified Stern–Volmer equation. The enthalpy change (ΔH) and entropy change (ΔS) were determined based on the van’t Hoff equation. The results of fluorescence spectroscopy indicate that static quenching is the dominant process resulting from the BSA-TCPP complex formation. In the case of the BSA-Ce6 complex, static quenching was confirmed too. Thermodynamic analysis indicated that hydrogen bonds and van der Waals interactions were the predominant intermolecular forces in the binding process to stabilize the BSA-TCPP and BSA-Ce6 complexes. Molecular docking suggests that the probable binding site of the two macrocyclic species at BSA occurs in the vicinity of the Trp-134 residue. Molecular modeling study further confirmed interactions in the binding mode obtained experimentally.
Graphic abstract
Similar content being viewed by others
References
Adler AD, Longo FR, Shergalis W (1964) Mechanistic investigations of porphyrin syntheses. I. Preliminary studies on ms-tetraphenylporphin. J Am Chem Soc 86:3145–3149. https://doi.org/10.1021/ja01069a035
Arthur OTA, Olson J (2010) Autodock Vina: Improving the speed and accuracy of docking with a new simulación function, efficient optimization, and multithreading. Comput Chem 31:455–461. https://doi.org/10.1002/jcc.21334
Chakraborty B, Basu S (2010) Interaction of BSA with proflavin: a spectroscopic approach. J Lumin 129:34–39. https://doi.org/10.1016/j.jlumin.2008.07.012
Charcosset RAC, Greige-Gerges H (2017) Interaction of triterpenoids with human serum albumin: a review. Chem Phys Lipid 207:260–270
Dmitry K et al (2020) Prediction of Protein–ligand Interaction Based on Sequence Similarity and Ligand Structural Features. Int J Mol Sci 21:8152–8161. https://doi.org/10.3390/ijms21218152
Fayezeh S, Hemmateenejad B, Shamsipur M, Rashidi M, Samouei H (2012) Affinity of two novel five-coordinated anticancer Pt(II) complexes to human and bovine serum albumins: a spectroscopic approach. Inorg Chem 51:3454–3464. https://doi.org/10.1021/ic202141g
Frisch MJ et al (2016) Gaussian 09, Revision A.02
Goma I, Sebak A, Abdel-Kader M (2017) Liposomal delivery of ferrous chlorophyllin: a novel third generation photosensitizer for in vitro PDT of melanoma. Photodiagnosis Photodyn Therapy 18:162–170. https://doi.org/10.1016/j.pdpdt.2017.01.186
Guha D, Das R, Mitra S, Mukherjee S (1997) Fluorescence studies on Luminol in water-organic solvent mixtures. Indian J Chem 36A, 307. http://nopr.niscair.res.in/handle/123456789/15842
Hirano HYA, Arakawa T, Shiraki K (2012) Effects of alcohol on the solubility and structure of native and disulfide-modified bovine serum albumin. Int J Biol Macromol 50:1286–1291. https://doi.org/10.1016/j.ijbiomac.2012.03.014
Horn JR, Brandts JF, Murphy KP (2002) van’t Hoff and calorimetric enthalpies ii: effects of linked equilibrian. Biochemistry 41:7501–7507. https://doi.org/10.1021/bi025626b
Jamie G et al (2005) Structural basis of the drug-binding specificity of human serum albumin. J Mol Biol 353:38–52. https://doi.org/10.1016/j.jmb.2005.07.075
Jones Brunette AM, Farrens DL (2014) Distance mapping in proteins using fluorescence spectroscopy: tyrosine, like tryptophan, quenches bimane fluorescence in a distance-dependent manner. Biochemistry 53:6290–6301. https://doi.org/10.1021/bi500493r
Karolina MA et al (2012) Structural and immunologic characterization of bovine, horse and rabbit serum. Mol Immunol 52:174–182. https://doi.org/10.1016/j.molimm.2012.05.011
Karsima SA, Mochizuki S, Noda M, Kobayashi K (1999) Crystal structure of human serum albumine at 2.5 a resolution. Protein Eng 12:439–446. https://doi.org/10.1093/protein/12.6.439
Kitchen DB, Decornez H, Furr JR, Bajorath J (2004) Applications, docking and scoring in virtual screening for drug discovery. Methods Nat Rev 3:935–949. https://doi.org/10.1038/nrd1549
Klebe G, Krimmergerhard SG (2015) Thermodynamics of protein–ligand interactions as a reference for computational analysis: how to assess accuracy, reliability and relevance of experimental data. J Computer-Aided Mol Des 29:867–883. https://doi.org/10.1007/s10822-015-9867-y
Klein CG et al (2020) Zinc(II), copper(II) and nickel(II) ions improve the selectivity of tetracationic platinum(II) porphyrins in photodynamic therapy and stimulate antioxidant defenses in the metastatic melanoma lineage (A375). Photodiagn Photodyn Ther 31:101942–101956. https://doi.org/10.1016/j.pdpdt.2020.101942
Lakowicz JR (2008) Principles of fluorescence spectroscopy, Third Edition. Vol 13, p 029901
Lebedeva NS et al (2019) Effect of pH on albumin binding with hydrophobic porphyrins. Russian J General Chem 89:565–569. https://doi.org/10.1134/S1070363219030368
Schrödinger Release 2020-2: Maestro, Schrödinger, LLC, New York, NY.
Makoto O et al (2009) Sugar-dependent photodynamic effect of glycoconjugated porphyrins: a study on photocytotoxicity, photophysical properties and binding behavior to bovine serum albumin (BSA). Biochem Biophys Acta 1770:1204–1211. https://doi.org/10.1016/j.bbagen.2007.03.011
Mermer A, Bayrak H, Alyar S, Alagumuthu M (2020) Synthesis, DFT calculations, biological investigation, molecular docking studies of β-lactam derivatives. J Mol Struct 1208:127891. https://doi.org/10.1016/j.molstruc.2020.127891
Miguel ARB, Manuel JEP (1998) Fluorescence quenching data interpretation in biological systems the use of microscopic models for data analysis and interpretation of complex systems. Biochim Biophys Acta 1373:1–16. https://doi.org/10.1016/S0005-2736(98)00081-9
Mocz G, Ross JA (2013) Fluorescence techniques in analysis of protein-ligand interactions. In: Williams MA, Daviter T (eds) Protein-ligand interactions: methods and applications. Humana Press, Totowa, pp 169–210
Mojzisova H, Bonneau S, Vever-Bizet C, Brault D (2007) Cellular uptake and subcellular distribution of chlorin e6 as functions of pH and interactions with membranes and lipoproteins. Biochim Biophys Acta Biomembr 1768:2748–2756. https://doi.org/10.1016/j.bbamem.2007.07.002
Murphy KP (1999) Predicting binding energetics from structure: looking beyond ∆G. John Wiley and Sons, Inc. https://doi.org/10.1002/(SICI)1098-1128(199907)19:4<333::AID-MED6>3.0.CO;2-5
Nonell S, Bresolí Obach R, Ruiz González R, Milán P, Stockert JC, Villanueva A, Cañete M (2017) Photodynamic synergistic effect of pheophorbide a and doxorubicin in combined treatment against tumoral cells. Cancers 9(2):18. https://doi.org/10.3390/cancers9020018
Ogura KIN, Takamiya A (1974) A simple method for extraction and partial purification of chlorophyll from plant material, using dioxane. J Biochem 76:901–904
Orit JJL, Niu G, Lin K-S, Bénard F, Chen X (2019) Bench to bedside: albumin binders for improved cancer radioligand therapies. Bioconjug Chem 30:487–502. https://doi.org/10.1021/acs.bioconjchem.8b00919
Oster G, Broyde SB, Bellin JS (1964) Spectral properties of chlorophyllin a. J Am Chem Soc 86(7):1309–1313. https://doi.org/10.1021/ja01061a010
Ping Z, Huang J-W, Ji L-N (2012) Cationic pyridinium porphyrins appending different peripheral substituents: Spectroscopic studies on their interactions with bovine serum albumin. Spectrochimica Acta Part A 88:130–136. https://doi.org/10.1016/j.saa.2011.12.017
Ross PD, Subramanian S (1981) Thermodynamics of protein association reactions: forces contributing to stability. Biochemistry 20:3096–3102. https://doi.org/10.1021/bi00514a017
Roy R, Mukherje S (1987) Fluorescence quenching of carbazole and indole by ethylenetrithiocarbonate. Chem Phys Lett 140:210–214. https://doi.org/10.1016/0009-2614(87)80816-3
Ryan AJ, Ghuman J, Zunszain PA, Chung C-W, Curry S (2011) Structural basis of binding of fluorescent, site-specific dansylated amino acids. J Struct Biol 174:84–91. https://doi.org/10.1016/j.jsb.2010.10.004
Salentin S, Schreiber S, Joachim Haupt V, Adasme MF, Schroeder M (2015) PLIP: fully automated protein–ligand interaction profiler. Nucleic Acids Res 43(W1):W443–W447
Shen et al (2015) Spectroscopic and molecular docking studies of binding interaction of gefitinib, lapatinib and sunitinib with bovine serum albumin (BSA). J Photochem Photobiol, B 153:380–390. https://doi.org/10.1016/j.jphotobiol.2015.10.023
Singh S, Amit Aggarwal NVS, Bhupathiraju DK, Tiwari GAK, Drain CM (2015) Glycosylated porphyrins, phthalocyanines, and other porphyrinoids for diagnostics and therapeutics. Chem Rev 11:10261–10306. https://doi.org/10.1021/acs.chemrev.5b00244
Theodore P (1995) The Albumin Molecule" Its Structure. All about Albumin. Elsevier, Amsterdam
Theresa B, Cengel KA, Finlay J (2009) Pheophorbide a as a photosensitizer in photodynamic therapy: In vivo considerations. Cancer Biol Ther 8:540–542. https://doi.org/10.4161/cbt.8.6.8067
Wallace AC, Laskowski RA, Thornton JM (1996) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng Des Sel 8:127–134. https://doi.org/10.1093/protein/8.2.127
Williams MA (2013) Protein–ligand interactions: fundamentals. In: Williams M, Daviter T (eds) Protein-ligand interactions. methods in molecular biology (methods and protocols). Humana Press, Totowa https://doi.org/10.1007/978-1-62703-398-5_1
Wu Y, Cheng H, Chen Y, Chen L, Fang Z, Liang, (2017) Formation of a multiligand complex of bovine serum albumin with retinol, resveratrol, and (-)-epigallocatechin-3-gallate for the protection of bioactive components. J Agric Food Chem 65:3019–3030. https://doi.org/10.1021/acs.jafc.7b00326
Xi-Liang Lu, Fan J-J, Liu Yi, Hou A-X (2009) Characterization of the interaction between cationic Erbium (III)–porphyrin complex with bovine serum albumin. J Mol Struct 934:1–8. https://doi.org/10.1016/j.molstruc.2009.05.037
Yan-Jun Hu, Ou-Yang Yu, Dai C-M, Liu Yi, Xiao X-H (2010) Site-selective binding of human serum albumin by palmatine: spectroscopic approach. Biomacromol 11:106–112. https://doi.org/10.1021/bm900961e
Zhong-min W et al (2013) Structural studies of several clinically important oncology drugs in complex with human serum albumin. Biochem Biophys Acta 1830:5356–5374. https://doi.org/10.1016/j.bbagen.2013.06.032
Acknowledgements
J. Osiris Vicente thanks the National Science and Technology Council of Mexico (CONACYT) for the scholarship number 130442.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Vicente-Escobar, J.O., García-Sánchez, M.A., González, F. et al. A spectroscopic and molecular docking study of interactions of tetracarboxyphenyl porphyrin and chlorin e6 with bovine serum albumin. Chem. Pap. 75, 4501–4515 (2021). https://doi.org/10.1007/s11696-021-01670-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11696-021-01670-3