Protein Binding of Benzofuran Derivatives: A CD Spectroscopic and In Silico Comparative Study of the Effects of 4-Nitrophenyl Functionalized Benzofurans and Benzodifurans on BSA Protein Structure
Abstract
:1. Introduction
2. Materials and Methods
2.1. Synthesis of Benzofuran Derivatives BF1 and BDF1
2.2. CD Binding Studies
2.3. CD Denaturation Studies
2.4. CD Spectra Deconvolution
2.5. Fluorescence Studies
2.6. Molecular Docking and in Silico Protein–Protein and Protein–Ligand Interaction Analysis
2.7. Pharmacokinetic Properties
3. Results and Discussion
3.1. CD Binding Studies on BSA in Complex with BF1 and BDF1
3.2. Fluorescence Studies
3.3. In Silico Studies on the Benzofuran/BSA Complexes
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Peters, T., Jr. Serum albumin. Adv. Protein Chem. 1985, 37, 161–245. [Google Scholar] [PubMed]
- Carter, D.C.; Ho, J.X. Structure of serum albumin. Adv. Protein Chem. 1994, 45, 153–203. [Google Scholar] [PubMed]
- Akdogan, Y.; Emrullahoglu, M.; Tatlidil, D.; Ucuncu, M.; Cakan-Akdogan, G. EPR studies of intermolecular interactions and competitive binding of drugs in a drug–BSA binding model. Phys. Chem. Chem. Phys. 2016, 18, 22531–22539. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fik-Jaskółka, M.A.; Mkrtchyan, A.F.; Saghyan, A.S.; Palumbo, R.; Belter, A.; Hayriyan, L.A.; Simonyan, H.; Roviello, V.; Roviello, G.N. Spectroscopic and SEM evidences for G4-DNA binding by a synthetic alkyne-containing amino acid with anticancer activity. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 2020, 229, 117884. [Google Scholar] [CrossRef]
- Fik-Jaskółka, M.A.; Mkrtchyan, A.F.; Saghyan, A.S.; Palumbo, R.; Belter, A.; Hayriyan, L.A.; Simonyan, H.; Roviello, V.; Roviello, G.N. Biological macromolecule binding and anticancer activity of synthetic alkyne-containing l-phenylalanine derivatives. Amino Acids 2020, 52, 755–769. [Google Scholar] [CrossRef]
- Liu, E.-H.; Qi, L.-W.; Li, P. Structural relationship and binding mechanisms of five flavonoids with bovine serum albumin. Molecules 2010, 15, 9092–9103. [Google Scholar] [CrossRef] [Green Version]
- Szymańska, M.; Pospieszna-Markiewicz, I.; Mańka, M.; Insińska-Rak, M.; Dutkiewicz, G.; Patroniak, V.; Fik-Jaskółka, M.A. Synthesis and Spectroscopic Investigations of Schiff Base Ligand and Its Bimetallic Ag (I) Complex as DNA and BSA Binders. Biomolecules 2021, 11, 1449. [Google Scholar] [CrossRef]
- Izawa, H.; Kinai, M.; Ifuku, S.; Morimoto, M.; Saimoto, H. Guanidinylation of Chitooligosaccharides involving internal cyclization of the Guanidino group on the reducing end and effect of Guanidinylation on protein binding ability. Biomolecules 2019, 9, 259. [Google Scholar] [CrossRef] [Green Version]
- Losytskyy, M.; Chornenka, N.; Vakarov, S.; Meier-Menches, S.M.; Gerner, C.; Potocki, S.; Arion, V.B.; Gumienna-Kontecka, E.; Voloshin, Y.; Kovalska, V. Sensing of Proteins by ICD Response of Iron (II) Clathrochelates Functionalized by Carboxyalkylsulfide Groups. Biomolecules 2020, 10, 1602. [Google Scholar] [CrossRef]
- Simard, J.R.; Zunszain, P.A.; Hamilton, J.A.; Curry, S. Location of high and low affinity fatty acid binding sites on human serum albumin revealed by NMR drug-competition analysis. J. Mol. Biol. 2006, 361, 336–351. [Google Scholar] [CrossRef]
- Sugio, S.; Kashima, A.; Mochizuki, S.; Noda, M.; Kobayashi, K. Crystal structure of human serum albumin at 2.5 Å resolution. Protein Eng. 1999, 12, 439–446. [Google Scholar] [CrossRef]
- Loureiro, A.; G. Azoia, N.; C. Gomes, A.; Cavaco-Paulo, A. Albumin-based nanodevices as drug carriers. Curr. Pharm. Des. 2016, 22, 1371–1390. [Google Scholar] [CrossRef]
- Parodi, A.; Miao, J.; Soond, S.M.; Rudzińska, M.; Zamyatnin, A.A. Albumin nanovectors in cancer therapy and imaging. Biomolecules 2019, 9, 218. [Google Scholar] [CrossRef] [Green Version]
- Rubio-Camacho, M.; Encinar, J.A.; Martínez-Tomé, M.J.; Esquembre, R.; Mateo, C.R. The Interaction of Temozolomide with Blood Components Suggests the Potential Use of Human Serum Albumin as a Biomimetic Carrier for the Drug. Biomolecules 2020, 10, 1015. [Google Scholar] [CrossRef]
- Kanal, K.M.; Fullerton, G.D.; Cameron, I.L. A study of the molecular sources of nonideal osmotic pressure of bovine serum albumin solutions as a function of pH. Biophys. J. 1994, 66, 153–160. [Google Scholar] [CrossRef] [Green Version]
- Van Dijk, J.; Smit, J. Size-exclusion chromatography–multiangle laser light scattering analysis of β-lactoglobulin and bovine serum albumin in aqueous solution with added salt. J. Chromatogr. A 2000, 867, 105–112. [Google Scholar] [CrossRef]
- Squire, P.G.; Moser, P.; O’Konski, C.T. Hydrodynamic properties of bovine serum albumin monomer and dimer. Biochemistry 1968, 7, 4261–4272. [Google Scholar] [CrossRef]
- Kovalsky, O.; Lung, F.-D.T.; Roller, P.P.; Fornace, A.J. Oligomerization of human Gadd45a protein. J. Biol. Chem. 2001, 276, 39330–39339. [Google Scholar] [CrossRef] [Green Version]
- Levi, V.; Rossi, J.P.; Castello, P.R.; Flecha, F.L.G. Structural significance of the plasma membrane calcium pump oligomerization. Biophys. J. 2002, 82, 437–446. [Google Scholar] [CrossRef] [Green Version]
- Bowie, J.U. Stabilizing membrane proteins. Curr. Opin. Struct. Biol. 2001, 11, 397–402. [Google Scholar] [CrossRef]
- Sah, H. Stabilization of proteins against methylene chloride/water interface-induced denaturation and aggregation. J. Control. Release 1999, 58, 143–151. [Google Scholar] [CrossRef]
- Chubarov, A.; Spitsyna, A.; Krumkacheva, O.; Mitin, D.; Suvorov, D.; Tormyshev, V.; Fedin, M.; Bowman, M.K.; Bagryanskaya, E. Reversible Dimerization of Human Serum Albumin. Molecules 2020, 26, 108. [Google Scholar] [CrossRef] [PubMed]
- Wetzel, R.; Becker, M.; Behlke, J.; Billwitz, H.; BoHm, S.; Ebert, B.; Hamann, H.; Krumbiegel, J.; Lassmann, G. Temperature Behaviour of Human Serum Albumin. Eur. J. Biochem. 1980, 104, 469–478. [Google Scholar] [CrossRef]
- Taguchi, K.; Giam Chuang, V.T.; Maruyama, T.; Otagiri, M. Pharmaceutical Aspects of the Recombinant Human Serum Albumin Dimer: Structural Characteristics, Biological Properties, and Medical Applications. J. Pharm. Sci. 2012, 101, 3033–3046. [Google Scholar] [CrossRef] [PubMed]
- DeSimone, R.; Currie, K.; Mitchell, S.; Darrow, J.; Pippin, D. Privileged Structures: Applications in Drug Discovery. Comb. Chem. High Throughput Screen. 2004, 7, 473–493. [Google Scholar] [CrossRef]
- D’Errico, S.; Oliviero, G.; Amato, J.; Borbone, N.; Cerullo, V.; Hemminki, A.; Piccialli, V.; Zaccaria, S.; Mayol, L.; Piccialli, G. Synthesis and biological evaluation of unprecedented ring-expanded nucleosides (RENs) containing the imidazo [4,5-d][1,2,6]oxadiazepine ring system. Chem. Commun. 2012, 48, 9310. [Google Scholar] [CrossRef]
- Oliviero, G.; Amato, J.; Borbone, N.; D’Errico, S.; Piccialli, G.; Mayol, L. Synthesis of N-1 and ribose modified inosine analogues on solid support. Tetrahedron Lett. 2007, 48, 397–400. [Google Scholar] [CrossRef]
- Alper-Hayta, S.; Arisoy, M.; Temiz-Arpaci, Ö.; Yildiz, I.; Aki, E.; Özkan, S.; Kaynak, F. Synthesis, antimicrobial activity, pharmacophore analysis of some new 2-(substitutedphenyl/benzyl)-5-[(2-benzofuryl)carboxamido]benzoxazoles. Eur. J. Med. Chem. 2008, 43, 2568–2578. [Google Scholar] [CrossRef]
- Soni, J.N.; Soman, S.S. Synthesis and antimicrobial evaluation of amide derivatives of benzodifuran-2-carboxylic acid. Eur. J. Med. Chem. 2014, 75, 77–81. [Google Scholar] [CrossRef]
- Ashok, D.; Sudershan, K.; Khalilullah, M. Solvent-free microwave-assisted synthesis ofE-(1)-(6-benzoyl-3,5-dimethylfuro[3 ′,2′:4,5]benzo[b]furan-2-yl)-3-(aryl)-2-propen-1-ones and their antibacterial activity. Green Chem. Lett. Rev. 2012, 5, 121–125. [Google Scholar] [CrossRef] [Green Version]
- Feng, Z.; Mohapatra, S.; Klimko, P.G.; Hellberg, M.R.; May, J.A.; Kelly, C.; Williams, G.; McLaughlin, M.A.; Sharif, N.A. Novel benzodifuran analogs as potent 5-HT2A receptor agonists with ocular hypotensive activity. Bioorganic Med. Chem. Lett. 2007, 17, 2998–3002. [Google Scholar] [CrossRef]
- Thévenin, M.; Thoret, S.; Grellier, P.; Dubois, J. Synthesis of polysubstituted benzofuran derivatives as novel inhibitors of parasitic growth. Bioorganic Med. Chem. 2013, 21, 4885–4892. [Google Scholar] [CrossRef]
- Hayakawa, I.; Shioya, R.; Agatsuma, T.; Furukawa, H.; Naruto, S.; Sugano, Y. 4-Hydroxy-3-methyl-6-phenylbenzofuran-2-carboxylic acid ethyl ester derivatives as potent anti-tumor agents. Bioorganic Med. Chem. Lett. 2004, 14, 455–458. [Google Scholar] [CrossRef]
- Xie, F.; Zhu, H.; Zhang, H.; Lang, Q.; Tang, L.; Huang, Q.; Yu, L. In vitro and in vivo characterization of a benzofuran derivative, a potential anticancer agent, as a novel Aurora B kinase inhibitor. Eur. J. Med. Chem. 2015, 89, 310–319. [Google Scholar] [CrossRef]
- Musumeci, D.; Roviello, G.N.; Rigione, G.; Capasso, D.; Di Gaetano, S.; Riccardi, C.; Roviello, V.; Montesarchio, D. Benzodifuran Derivatives as Potential Antiproliferative Agents: Possible Correlation between Their Bioactivity and Aggregation Properties. ChemPlusChem 2017, 82, 251–260. [Google Scholar] [CrossRef]
- Wang, Y.-N.; Liu, M.-F.; Hou, W.-Z.; Xu, R.-M.; Gao, J.; Lu, A.-Q.; Xie, M.-P.; Li, L.; Zhang, J.-J.; Peng, Y.; et al. Bioactive Benzofuran Derivatives from Cortex Mori Radicis, and Their Neuroprotective and Analgesic Activities Mediated by mGluR1. Molecules 2017, 22, 236. [Google Scholar] [CrossRef] [Green Version]
- Roviello, G.N.; Roviello, V.; Musumeci, D.; Pedone, C. Synthesis of a novel benzodifuran derivative and its molecular recognition of poly rA RNA. Biol. Chem. 2013, 394, 1235–1239. [Google Scholar] [CrossRef]
- Carella, A.; Roviello, V.; Iannitti, R.; Palumbo, R.; La Manna, S.; Marasco, D.; Trifuoggi, M.; Diana, R.; Roviello, G.N. Evaluating the biological properties of synthetic 4-nitrophenyl functionalized benzofuran derivatives with telomeric DNA binding and antiproliferative activities. Int. J. Biol. Macromol. 2019, 121, 77–88. [Google Scholar] [CrossRef]
- Musumeci, D.; Mokhir, A.; Roviello, G.N. Synthesis and nucleic acid binding evaluation of a thyminyl l-diaminobutanoic acid-based nucleopeptide. Bioorganic Chem. 2020, 100, 103862. [Google Scholar] [CrossRef]
- D’Atri, V.; Oliviero, G.; Amato, J.; Borbone, N.; D’Errico, S.; Mayol, L.; Piccialli, V.; Haider, S.; Hoorelbeke, B.; Balzarini, J.; et al. New anti-HIV aptamers based on tetra-end-linked DNA G-quadruplexes: Effect of the base sequence on anti-HIV activity. Chem. Commun. 2012, 48, 9516. [Google Scholar] [CrossRef]
- Amato, J.; Oliviero, G.; De Pauw, E.; Gabelica, V. Hybridization of short complementary PNAs to G-quadruplex forming oligonucleotides: An electrospray mass spectrometry study. Biopolymers 2009, 91, 244–255. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Esposito, V.; Virgilio, A.; Pepe, A.; Oliviero, G.; Mayol, L.; Galeone, A. Effects of the introduction of inversion of polarity sites in the quadruplex forming oligonucleotide TGGGT. Bioorganic Med. Chem. 2009, 17, 1997–2001. [Google Scholar] [CrossRef]
- Scuotto, M.; Persico, M.; Bucci, M.; Vellecco, V.; Borbone, N.; Morelli, E.; Oliviero, G.; Novellino, E.; Piccialli, G.; Cirino, G.; et al. Outstanding effects on antithrombin activity of modified TBA diastereomers containing an optically pure acyclic nucleotide analogue. Org. Biomol. Chem. 2014, 12, 5235–5242. [Google Scholar] [CrossRef] [PubMed]
- Abriata, L.A. Online interactive fitting and simulation of protein circular dichroism spectra for use in education and for preliminary spectral analysis. arXiv 2020, arXiv:2006.06275. Available online: https://arxiv.org/abs/2006.06275 (accessed on 31 December 2021).
- Abriata, L.A. A simple spreadsheet program to simulate and analyze the far-UV circular dichroism spectra of proteins. J. Chem. Educ. 2011, 88, 1268–1273. [Google Scholar] [CrossRef]
- Musumeci, D.; Ullah, S.; Ikram, A.; Roviello, G.N. Novel insights on nucleopeptide binding: A spectroscopic and in silico investigation on the interaction of a thymine-bearing tetrapeptide with a homoadenine DNA. J. Mol. Liq. 2022, 347, 117975. [Google Scholar] [CrossRef]
- Roviello, V.; Scognamiglio, P.L.; Caruso, U.; Vicidomini, C.; Roviello, G.N. Evaluating In Silico the Potential Health and Environmental Benefits of Houseplant Volatile Organic Compounds for an Emerging ‘Indoor Forest Bathing’ Approach. Int. J. Environ. Res. Public Health 2022, 19, 273. [Google Scholar] [CrossRef]
- Roviello, V.; Roviello, G.N. Less COVID-19 deaths in southern and insular Italy explained by forest bathing, Mediterranean environment, and antiviral plant volatile organic compounds. Environ. Chem. Lett. 2021. [Google Scholar] [CrossRef]
- Vicidomini, C.; Roviello, V.; Roviello, G.N. In Silico Investigation on the Interaction of Chiral Phytochemicals from Opuntia ficus-indica with SARS-CoV-2 Mpro. Symmetry 2021, 13, 1041. [Google Scholar] [CrossRef]
- Roviello, V.; Musumeci, D.; Mokhir, A.; Roviello, G.N. Evidence of Protein Binding by a Nucleopeptide Based on a Thyminedecorated L-Diaminopropanoic Acid through CD and In Silico Studies. Curr. Med. Chem. 2021, 28, 5004–5015. [Google Scholar] [CrossRef]
- Duhovny, D.; Nussinov, R.; Wolfson, H.J. Efficient unbound docking of rigid molecules. In Proceedings of the International Workshop in Algorithms in Bioinformatics, Rome, Italy, 17–21 September 2002; Springer: Berlin, Germany; pp. 185–200. [Google Scholar]
- Schneidman-Duhovny, D.; Inbar, Y.; Nussinov, R.; Wolfson, H.J. PatchDock and SymmDock: Servers for rigid and symmetric docking. Nucleic Acids Res. 2005, 33, W363–W367. [Google Scholar] [CrossRef] [Green Version]
- Andrusier, N.; Nussinov, R.; Wolfson, H.J. FireDock: Fast interaction refinement in molecular docking. Proteins Struct. Funct. Bioinform. 2007, 69, 139–159. [Google Scholar] [CrossRef]
- Yang, S.L.; Chou, Y.T.; Wu, C.N.; Ho, M.S. Annexin II Binds to Capsid Protein VP1 of Enterovirus 71 and Enhances Viral Infectivity. J. Virol. 2011, 85, 11809–11820. [Google Scholar] [CrossRef] [Green Version]
- Yan, Y.; Huang, S.-Y. Accurate prediction of inter-protein residue–residue contacts for homo-oligomeric protein complexes. Brief. Bioinform. 2021, 22, bbab038. [Google Scholar] [CrossRef]
- Adasme, M.F.; Linnemann, K.L.; Bolz, S.N.; Kaiser, F.; Salentin, S.; Haupt, V.J.; Schroeder, M. PLIP 2021: Expanding the scope of the protein-ligand interaction profiler to DNA and RNA. Nucleic Acids Res. 2021, 49, W530–W534. [Google Scholar] [CrossRef]
- Ye, F.; An, Y.; Qin, D.; Yang, L.; She, L.; Xing, R. Spectroscopic study on the effect of crystallization of the hydroxyapatite on the secondary structure of bovine serum albumin. Guang Pu Xue Yu Guang Pu Fen Xi 2007, 27, 321–324. [Google Scholar]
- Nepal, D.; Geckeler, K.E. pH-sensitive dispersion and debundling of single-walled carbon nanotubes: Lysozyme as a tool. Small 2006, 2, 406–412. [Google Scholar] [CrossRef]
- Sun, C.; Yang, J.; Wu, X.; Huang, X.; Wang, F.; Liu, S. Unfolding and refolding of bovine serum albumin induced by cetylpyridinium bromide. Biophys. J. 2005, 88, 3518–3524. [Google Scholar] [CrossRef] [Green Version]
- Dezhampanah, H.; Esmaili, M.; Jampour, S. Spectroscopic and molecular docking studies on interaction of two Schiff base complexes with bovine serum albumin. J. Biomol. Struct. Dyn. 2020, 38, 2650–2658. [Google Scholar] [CrossRef]
Δ(BF1-BSA) (%) | Δ(BDF1-BSA) (%) | |
---|---|---|
α | +0.06 | −0.79 |
β | +5.70 | +1.00 |
Random coil | −5.76 | −0.21 |
Compound | Tm/°C | ΔT/°C = (Tm − TmBSA) |
---|---|---|
BF1-BSA | 72.9 ± 0.1 | +3.1 ± 0.2 |
BDF1-BSA | 69.0 ± 0.2 | −0.8 ± 0.1 |
Complex | Global Energy | Attractive VDW * | Repulsive VDW * | ACE ** |
---|---|---|---|---|
BF1-BSA(monomer) | −44.20 | −23.90 | 11.00 | −11.16 |
BDF1-BSA(monomer) | −40.05 | −26.40 | 11.37 | −6.94 |
BF1-BSA(dimer) | −36.78 | −22.73 | 17.36 | −10.77 |
BDF1-BSA(dimer) | −35.53 | −23.79 | 11.73 | −6.36 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Scognamiglio, P.L.; Vicidomini, C.; Fontanella, F.; De Stefano, C.; Palumbo, R.; Roviello, G.N. Protein Binding of Benzofuran Derivatives: A CD Spectroscopic and In Silico Comparative Study of the Effects of 4-Nitrophenyl Functionalized Benzofurans and Benzodifurans on BSA Protein Structure. Biomolecules 2022, 12, 262. https://doi.org/10.3390/biom12020262
Scognamiglio PL, Vicidomini C, Fontanella F, De Stefano C, Palumbo R, Roviello GN. Protein Binding of Benzofuran Derivatives: A CD Spectroscopic and In Silico Comparative Study of the Effects of 4-Nitrophenyl Functionalized Benzofurans and Benzodifurans on BSA Protein Structure. Biomolecules. 2022; 12(2):262. https://doi.org/10.3390/biom12020262
Chicago/Turabian StyleScognamiglio, Pasqualina Liana, Caterina Vicidomini, Francesco Fontanella, Claudio De Stefano, Rosanna Palumbo, and Giovanni N. Roviello. 2022. "Protein Binding of Benzofuran Derivatives: A CD Spectroscopic and In Silico Comparative Study of the Effects of 4-Nitrophenyl Functionalized Benzofurans and Benzodifurans on BSA Protein Structure" Biomolecules 12, no. 2: 262. https://doi.org/10.3390/biom12020262
APA StyleScognamiglio, P. L., Vicidomini, C., Fontanella, F., De Stefano, C., Palumbo, R., & Roviello, G. N. (2022). Protein Binding of Benzofuran Derivatives: A CD Spectroscopic and In Silico Comparative Study of the Effects of 4-Nitrophenyl Functionalized Benzofurans and Benzodifurans on BSA Protein Structure. Biomolecules, 12(2), 262. https://doi.org/10.3390/biom12020262