Theoretical Coupling and Stability of Boronic Acid Adducts with Catecholamines

Author(s): Eugeniy Demianenko , Alexey Rayevsky , Marvin A. Soriano-Ursúa* , José G. Trujillo-Ferrara* .

Journal Name: Letters in Drug Design & Discovery

Volume 16 , Issue 4 , 2019

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Abstract:

Background: Catecholamines combined with boric/boronic acids are attractive chemical agents in drug design because some of their adducts have shown interesting biological activity. Scant information exists about their stability.

Objective: The aim of the present theoretical study was to explore the role of boron in molecules that combine catecholamines and boric/boronic acids, with a particular interest in examining stability.

Method: The methodology was based on the US GAMESS program using DFT with the B3LYP exchange-correlation functional and the 6-31G (d,p) split-valence basis set.

Results: According to the current findings, the boron-containing compounds (BCCs) exhibit weaker bonding to the hydroxyls on the ethylamine moiety than to those in the aromatic ring. The strongest binding site of a hydroxyl group was often found to be in meta-position (relative to ethylamine moiety) for boron-free compounds and in para-position for BCCs. Nonetheless, the methyl substituent in the amino group was able to induce changes in this pattern. We analyzed feasible boronsubstituted structures and assessed the relative strength of the respective C-B bonds, which allowed for the identification of the favorable points for reaction and stability.

Conclusion: It is feasible to form adducts by bonding on the amine and catechol sides of catecholamines. The presence of boron stabilizes the adducts in para-position. Since some of these BCCs are promising therapeutic agents, understanding the mechanisms of reaction is relevant for drug design.

Keywords: Boron, catecholamine, stability, boron containing compounds, medicinal chemistry, DFT calculations.

[1]
Soriano-Ursúa, M.A.; Das, B.C.; Trujillo-Ferrara, J.G. Boron containing compounds: Chemico-biological properties and expanding medicinal potential in prevention, diagnosis and therapy. Expert Opin. Ther. Pat., 2014, 24, 485-500.
[2]
Ban, H.S.; Nakamura, H. Boron-based drug design. Chem. Rec., 2015, 15, 616-635.
[3]
Leśnikowski, Z.J. Recent developments with boron as a platform for novel drug design. Expert Opin. Drug Discov., 2016, 11, 569-578.
[4]
Del Rosso, J.Q.; Plattner, J.J. From the test tube to the treatment room: Fundamentals of boron-containing compounds and their relevance to dermatology. J. Clin. Aesthet. Dermatol., 2014, 7, 13-21.
[5]
Pizzorno, L. Nothing boring about boron. Integr. Med. (Encinitas), 2015, 14, 35-48.
[6]
Farfán-García, E.D.; Castillo-Mendieta, N.T.; Ciprés-Flores, F.J.; Padilla-Martínez, I.I.; Trujillo-Ferrara, J.G.; Soriano-Ursúa, M.A. Current data regarding the structure-toxicity relationship of boron-containing compounds. Toxicol. Lett., 2016, 258, 115-125.
[7]
Katsamakas, S.; Papadopoulos, A.G.; Hadjipavlou-Litina, D. Boronic acid group: A cumbersome false negative case in the process of drug design. Molecules, 2016, 21, E1185.
[8]
Nocentini, A.; Supuran, C.T.; Winum, J.Y. Benzoxaborole compounds for therapeutic uses: A patent review (2010- 2018). Expert Opin. Ther. Pat., 2018, 28, 493-504.
[9]
Fu, H.; Hu, J.; Zhang, M.; Wang, Y.; Zhang, H.; Hu, P. One-step preparation of phenyl boron-modified magnetic mesoporous silica for selective enrichment of cis-diol-containing substances. Molecules, 2018, 23(3), E603.
[10]
Marfin, Y.S.; Solomonov, A.V.; Timin, A.S.; Rumyantsev, E.V. Recent advances of individual BODIPY and BODIPY-based functional materials in medical diagnostics and treatment. Curr. Med. Chem., 2017, 24, 2745-2772.
[11]
Huang, H.; Yu, C.; Li, X.; Zhang, Y.; Zhang, Y.; Chen, X.; Mariano, P.S.; Xie, H.; Wang, W. Synthesis of aldehydes by organocatalytic formylation reactions of boronic acids with glyoxylic acid. Angew. Chem. Int. Ed. Engl., 2017, 56, 8201-8205.
[12]
Hunter, P. Not boring at all. Boron is the new carbon in the quest for novel drug candidates. EMBO Rep., 2009, 10, 125-128.
[13]
Soriano-Ursúa, M.A.; McNaught-Flores, D.A.; Nieto-Alamilla, G.; Segura-Cabrera, A. A.; Correa-Basurto, J.; Arias-Montaño, J.A.; Trujillo-Ferrara J.G. Cell-based and in-silico studies on the high intrinsic activity of two boron-containing salbutamol derivatives at the human B2-adrenoceptor. Bioorg. Med. Chem., 2012, 20, 933-941.
[14]
Wingelhofer, B.; Kreis, K.; Mairinger, S.; Muchitsch, V.; Stanek, J.; Wanek, T.; Langer, O.; Kuntner, C. Preloading with L-BPA, L-tyrosine and L-DOPA enhances the uptake of [18F]FBPA in human and mouse tumour cell lines. Appl. Radiat. Isot., 2016, 118, 67-72.
[15]
Soriano-Ursúa, M.A.; Arias-Montaño, J.A.; Correa-Basurto, J.; Hernández-Martínez, C.F.; López-Cabrera, Y.; Castillo-Hernández, M.C.; Padilla-Martínez, I.I.; Trujillo-Ferrara, J.G. Insights on the role of boron containing moieties in the design of new potent and efficient agonists targeting the β2 adrenoceptor. Bioorg. Med. Chem. Lett., 2015, 25, 820-825.
[16]
Baker, S.J.; Ding, C.Z.; Akama, T.; Zhang, Y.K.; Hernández, V.; Xia, Y. Therapeutic potential of boron-containing compounds. Future Med. Chem., 2009, 1, 1275-1288.
[17]
Ciani, L.; Ristori, S. Boron as a platform for new drug design. Expert Opin. Drug Discov., 2012, 7, 1017-1027.
[18]
Das, B.C.; Thapa, P.; Karki, R.; Schinke, C.; Das, S.; Kambhampati, S.; Banerjee, S.K.; Van Veldhuizen, P.; Verma, A.; Weiss, L.M.; Evans, T. Boron chemicals in diagnosis and therapeutics. Future Med. Chem., 2013, 5, 653-676.
[19]
Trippier, P.C.; McGuigan, C. Boronic acids in medicinal chemistry: Anticancer, antibacterial and antiviral applications. MedChemComm, 2010, 1, 183-198.
[20]
Diaz, D.B.; Yudin, A.K. The versatility of boron in biological target engagement. Nat. Chem., 2017, 9, 731-742.
[21]
Roy, C.D.; Brown, H.C. Stability of boronic esters - Structural effects on the relative rates of transesterification of 2-(phenyl)-1,3,2-dioxaborolane. J. Organomet. Chem., 2007, 692, 784-790.
[22]
Shonberg, J.; Kling, R.C.; Gmeiner, P.; Löber, S. GPCR crystal structures: Medicinal chemistry in the pocket. Bioorg. Med. Chem., 2015, 23, 3880-3906.
[23]
Tafi, A.; Agamennone, M.; Tortorella, C.; Alcaro, S.; Gallina, C.; Botta, M. AMBER force field implementation of the boronate function to simulate the inhibition of b-lactamases by alkyl and aryl boronic acids. Eur. J. Med. Chem., 2005, 40, 1134-1142.
[24]
Calvaresi, M.; Zerbetto, F.J. In silico carborane docking to proteins and potential drug targets. Chem. Inf. Model, 2011, 51, 1882-1896.
[25]
Aziz-Ketuli, K.; Hadi, A.H. Boronate derivatives of Functionally diverse catechols: Stability studies. Molecules, 2010, 15, 2347-2356.
[26]
Andrade-Jorge, E.; Garcia-Avila, A.K.; Ocampo-Nestor, A.L.; Trujillo-Ferrara, J.G.; Soriano-Ursua, M.A. Advances of bioinformatics applied to development and evaluation of boron-containing compounds. Curr. Org. Chem., 2018, 22, 298-306.
[27]
Ocampo-Néstor, A.L.; Trujillo-Ferrara, J.G.; Reyes-López, C.; Geninatti-Crich, S.; Soriano-Ursúa, M.A. Boron’s journey: Advances in the study and application of pharmacokinetics. Expert Opin. Ther. Pat., 2017, 27, 203-215.
[28]
Soriano-Ursúa, M.A.; Farfán-García, E.D.; López-Cabrera, Y.; Querejeta, E.; Trujillo-Ferrara, J.G. Boron-containing acids: Preliminary evaluation of acute toxicity and access to the brain determined by Raman scattering spectroscopy. Neuro. Toxicol., 2014, 40, 8-15.
[29]
Wehrwein, E.A.; Orer, H.S.; Barman, S.M. Overview of the anatomy, physiology, and pharmacology of the autonomic nervous system. Compr. Physiol., 2016, 6, 1239-1278.
[30]
Vijverman, A.C.; Fox, S.H. New treatments for the motor symptoms of Parkinson’s disease. Expert Rev. Clin. Pharmacol., 2014, 7, 761-777.
[31]
Schmidt, M.W.; Baldridge, K.K.; Boatz, J.A.; Elbert, S.T.; Gordon, M.S.; Jensen, J.H.; Koseki, S.; Matsunaga, N.; Nguyen, K.A.; Su, S.; Windus, T.L.; Dupuis, M.; Montgomery, J.A., Jr General atomic and molecular electronic structure system. J. Comput. Chem., 1993, 14, 1347-1363.
[32]
Becke, A.D. Density functional thermochemistry III. The role of exact exchange. J. Chem. Phys., 1993, 98, 5648-5653.
[33]
Lee, C.; Yang, W.; Parr, R.G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B, 1988, 37, 785-789.
[34]
Wales, D.J.; Berry, R.S. Limitations of the Murrell-Laidler theorem. Faraday Trans, 1992, 88, 543-544.
[35]
CarCabal. P.; Snoek, L.C.; Van Mourik, T. A computational and spectroscopic study of the gas phase conformers of adrenaline. Mol. Phys., 2005, 103, 1633-1639.
[36]
Ramaekers, R.; Pajak, J.; Rospenk, M.; Maes, G. Matrix-isolation FT-IR spectroscopic study and theoretical DFT(B3LYP)/6-31 ++G** calculations of the vibrational and conformational properties of tyrosine. Spectrochimica Acta Part A, 2005, 61, 1347-1356.
[37]
Xu, J.; Wang, X.; Shao, C.; Su, D.; Cheng, G.; Hu, Y. Highly efficient synthesis of phenols by copper-catalyzed oxidative hydroxylation of arylboronic acids at room temperature in water. Org. Lett., 2010, 12, 1964-1967.
[38]
Zhang, L.; Zhang, G.; Zhang, M.; Cheng, J. Cu(OTf)2-mediated Chan-Lam reaction of carboxylic acids to access phenolic esters. J. Org. Chem., 2010, 75, 7472-7474.
[39]
Qi, H.L.; Chen, D.S.; Ye, J.S.; Huang, J.M. Electrochemical technique and copper-promoted transformations: Selective hydroxylation and amination of arylboronic acids. J. Org. Chem., 2013, 78, 7482-7487.
[40]
Zhu, C.; Wang, R.; Falck, J.R. Mild and rapid hydroxylation of aryl/heteroaryl boronic acids and boronate esters with N-oxides. Org. Lett., 2012, 14, 3494-3497.
[41]
Yi, H.; Lei, A. Pd-Catalyzed hydroxylation of aryl boronic acids using in situ generated hydrogen peroxide. Chemistry, 2017, 23, 10023-10027.
[42]
Gennari, A.; Gujral, C.; Hohn, E.; Lallana, E.; Cellesi, F.; Tirelli, N. Revisiting boronate/diol complexation as a double stimulus-responsive bioconjugation. Bioconjug. Chem., 2017, 28, 1391-1402.
[43]
Montanari, E.; Gennari, A.; Pelliccia, M.; Gourmel, C.; Lallana, E.; Matricardi, P.; McBain, A.J.; Tirelli, N. Hyaluronan/tannic acid nanoparticles via catechol/boronate complexation as a smart antibacterial system. Macromol. Biosci., 2016, 16, 1815-1823.
[44]
van der Vlies, A.J.; Inubushi, R.; Uyama, H.; Hasegawa, U. Polymeric framboidal nanoparticles loaded with a carbon monoxide donor via phenylboronic acid-catechol complexation. Bioconjug. Chem., 2016, 27, 1500-1508.
[45]
Zhong, M.; Dai, Y.; Fan, L.; Lu, X.; Kan, X. A novel substitution -sensing for hydroquinone and catechol based on a poly(3-aminophenylboronic acid)/MWCNTs modified electrode. Analyst, 2015, 140, 6047-6053.
[46]
Zhu, C.; Li, G.; Ess, D.H.; Falck, J.R.; Kürti, L. Elusive metal-free primary amination of arylboronic acids: Synthetic studies and mechanism by density functional theory. J. Am. Chem. Soc., 2012, 134, 18253-18256.
[47]
Bjerglund, K.M.; Skrydstrup, T.; Molander, G.A. Carbonylative Suzuki couplings of aryl bromides with boronic acid derivatives underbase-free conditions. Org. Lett., 2014, 16, 1888-1891.
[48]
Deng, C.C.; Brooks, W.L.A.; Abboud, K.A.; Sumerlin, B.S. Boronic acid-based hydrogels undergo self-healing at neutral and acidic pH. ACS Macro Lett., 2015, 4, 220-224.
[49]
Brooks, W.L.A.; Sumerlin, B.S. Synthesis and applications of boronic acid-containing polymers: From materials to medicine. Chem. Rev., 2016, 116, 1375-1397.
[50]
Özdemir, N.; Cakin, A.; Somtür, B. Boronic acid functionalized polymeric microspheres for catecholamine isolation. Colloid Surf. A., 2014, 445, 40-47.
[51]
Ueno, H.; Iwata, T.; Koshiba, N.; Takahashi, D.; Toshima, K. Design, synthesis and evaluation of a boronic acid based artificial receptor for (L)-DOPA in aqueous media. Chem. Commun. , 2013, 49, 10403-10405.
[52]
Bull, S.D.; Davidson, M.G.; van den Elsen, J.M.; Fossey, J.S.; Jenkins, A.T.; Jiang, Y.B.; Kubo, Y.; Marken, F.; Sakurai, K.; Zhao, J.; James, T.D. Exploiting the reversible covalent bonding of boronic acids: Recognition, sensing, and assembly. Acc. Chem. Res., 2013, 46, 312-326.
[53]
Rizi, R.N.; Noei, M. A theoretical study on monoatomic BN nanochains and nanorings. J. Mol. Model., 2016, 22, 205.
[54]
Li, Y.; Hao, J.; Liu, H.; Lu, S.; Tse, J.S. High-energy density and superhard nitrogen-rich B-N compounds. Phys. Rev. Lett., 2015, 115, 105502.
[55]
Karanjit, S.; Ehara, M.; Sakurai, H. Mechanism of the aerobic homocoupling of phenylboronic acid on Au20-: A DFT study. Chem. Asian J., 2015, 10, 2397-2403.
[56]
Chen, X.; Bartolotti, L.; Ishaq, K.; Tropsha, A. Molecular simulation of alkyl boronic acids: Molecular mechanics and solvation free energy calculations. J. Comput. Chem., 1994, 15, 333-345.
[57]
Essafi, S.; Tomasi, S.; Aggarwal, V.K.; Harvey, J.N. Homologation of boronic esters with organolithium compounds: A computational assessment of mechanism. J. Org. Chem., 2014, 79, 12148-12158.
[58]
Higa, S.; Suzuki, T.; Hayashi, A.; Tsuge, I.; Yamamura, Y. Isolation of catecholamines in biological fluids by boric acid gel. Anal. Biochem., 1977, 77, 18-24.
[59]
Lee, Z.S.; Critchley, J.A. Simultaneous measurement of catecholamines and kallikrein in urine using boric acid preservative. Clin. Chim. Acta, 1998, 276, 89-102.
[60]
Axthelm, J. Askes SHC, Elstner M, G UR, Görls H, Bellstedt P, Schiller A. Fluorinated boronic acid-appended pyridinium salts and 19F NMR spectroscopy for diol sensing. J. Am. Chem. Soc., 2017, 139(33), 11413-11420.
[61]
Li, X.S.; Li, S.; Kellermann, G. Simultaneous extraction and determination of monoamine neurotransmitters in human urine for clinical routine testing based on a dual functional solid phase extraction assisted by phenylboronic acid coupled with liquid chromatography-tandem mass spectrometry. Anal. Bioanal. Chem., 2017, 409, 2859-2871.
[62]
Li, H.; Zhang, X.; Zhang, L.; Wang, X.; Kong, F.; Fan, D.; Li, L.; Wang, W. Preparation of a boronate affinity silica stationary phase with enhanced binding properties towards cis-diol compounds. J. Chromatogr. A, 2016, 1473, 90-98.
[63]
He, H.; Zhou, Z.; Dong, C.; Wang, X.; Yu, Q.W.; Lei, Y.; Luo, L.; Feng, Y. Facile synthesis of a boronate affinity sorbent from mesoporous nanomagnetic polyhedral oligomeric silsesquioxanes composite and its application for enrichment of catecholamines in human urine. Anal. Chim. Acta, 2016, 944, 1-13.
[64]
Tossell, J.A. Boric acid adsorption on humic acids: Ab initio calculation of structures, stabilities, 11B NMR and 11B, 10B isotopic fractionations of surface complexes. Geochim. Cosmochim. Acta, 2006, 70, 5089-5103.
[65]
Saylor, R.A.; Reid, E.A.; Lunte, S.M. Microchip electrophoresis with electrochemical detection for the determination of analytes in the dopamine metabolic pathway. Electrophoresis, 2015, 36, 1912-1919.
[66]
Hollenbach, E.; Schulz, C.; Lehnert, H. Rapid and sensitive determination of catecholamines and the metabolite 3-methoxy-4-hydroxyphen-ethyleneglycol using HPLC following novel extraction procedures. Life Sci., 1998, 63, 737-750.
[67]
Ma, R.; Shi, L. Phenylboronic acid-based glucose-responsive polymeric nanoparticles: Synthesis and applications in drug delivery. Polym. Chem., 2014, 5, 1503-1518.
[68]
Furikado, Y.; Nagahata, T.; Okamoto, T.; Sugaya, T.; Iwatsuki, S.; Inamo, M.; Takagi, H.D.; Odani, A.; Ishihara, K. Universal reaction mechanism of boronic acids with diols in aqueous solution: Kinetics and the basic concept of a conditional formation constant. Chemistry, 2014, 20, 13194-13202.
[69]
Chen, G.; Qiu, J.; Fang, X.; Xu, J.; Cai, S.; Chen, Q.; Liu, Y.; Zhu, F.; Ouyang, G. Boronate affinity-molecularly imprinted biocompatible probe: An alternative for specific glucose monitoring. Chem. Asian J., 2016, 11, 2240-2245.
[70]
Cheng, T.; Li, H.; Ma, Y.; Liu, X.; Zhang, H. Synthesis of boronic-acid-functionalized magnetic attapulgite for selective enrichment of nucleosides. Anal. Bioanal. Chem., 2015, 407, 3525-3529.
[71]
Jiang, H.P.; Qi, C.B.; Chu, J.M.; Yuan, B.F.; Feng, Y.Q. Profiling of cis-diol-containing nucleosides and ribosylated metabolites by boronate-affinity organic-silica hybrid monolithic capillary liquid chromatography/mass spectrometry. Sci. Rep., 2015, 5, 7785.
[72]
Sobel, D.O.; Shakir, K.M. Determination of glycated plasma proteins in normal and diabetic subjects utilizing aminophenylboronic acid columns. Diabete Metab., 1987, 13, 575-581.
[73]
Duret, G.; Quinlan, R.; Bisseret, P.; Blanchard, N. Boron chemistry in a new light. Chem. Sci. , 2015, 6, 5366-5382.
[74]
Bernat, V.; Admas, T.H.; Brox, R.; Heinemann, F.W.; Tschammer, N. Boronic acids as probes for investigation of allosteric modulation of the chemokine receptor CXCR3. ACS Chem. Biol., 2014, 9, 2664-2677.
[75]
Du, J.; He, M.; Wang, X.; Fan, H.; Wei, Y. Facile preparation of boronic acid-functionalized magnetic nanoparticles with a high capacity and their use in the enrichment of cis-diol-containing compounds from plasma. Biomed. Chromatogr., 2015, 29, 312-320.
[76]
Zhai, W.; Sun, X.; James, T.D.; Fossey, J.S. Boronic acid‐based carbohydrate sensing. Chem. Asian J., 2015, 10, 1836-1848.
[77]
Schiefner, A.; Nästle, L.; Landgraf, M.; Reichert, A.J.; Skerra, A. Structural basis for the specific cotranslational incorporation of p-boronophenylalanine into biosynthetic proteins. Biochemistry, 2018, 57, 2597-2600.


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VOLUME: 16
ISSUE: 4
Year: 2019
Page: [467 - 475]
Pages: 9
DOI: 10.2174/1570180815666180710101604
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