Design and Synthesis of New Transient Receptor Potential Vanilloid Type-1 (TRPV1) Channel Modulators: Identification, Molecular Modeling Analysis, and Pharmacological Characterization of the N-(4-Hydroxy-3-methoxybenzyl)-4-(thiophen-2-yl)butanamide, a Small Molecule Endowed with Agonist TRPV1 Activity and Protective Effects against Oxidative Stress

ACS Chemical Neuroscience

Volumn 7, Issue 6, 2016, Pages 737-748

  Aiello, Francesca ^a   Badolato, Mariateresa ^a   Pessina, Federica ^b   Sticozzi, Claudia ^c   Maestrini, Vanessa ^b   Aldinucci, Carlo ^b   Luongo, Livio ^d   Guida, Francesca ^d   Ligresti, Alessia ^e   Artese, Anna ^f   Allarà, Marco ^e   Costa, Giosué ^f   Frosini, Maria ^b   Schiano Moriello, Aniello ^e   De Petrocellis, Luciano ^e   Valacchi, Giuseppe ^c   Alcaro, Stefano ^f   Maione, Sabatino ^d   Di Marzo, Vincenzo ^e   Corelli, Federico ^b   Brizzi, Antonella ^b   more..

^a UNIVERSITY OF CALABRIA   (Italy)

^b UNIVERSITY OF SIENA   (Italy)

^c UNIVERSITY OF FERRARA   (Italy)

^d SECOND UNIVERSITY OF NAPLES   (Italy)

^e CNR   (Italy)

^f UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

Author keywords

antinociceptive; antioxidant; capsaicin; neuroprotective; oxidative stress; TRPV1 ligands

Indexed keywords

2 [4 (THIOPHEN 2 YL)BUTAMIDO]ETHANESULFONIC ACID; ANALGESIC AGENT; CAPSAICIN; HYDROGEN; N (4 HYDROXY 3 METHOXYBENZYL) 4 (THIOPHEN 2 YL)BUTANAMIDE; N (4 HYDROXYBENZYL) 4 (THIOPHEN 2 YL)BUTANAMIDE; PROTECTIVE AGENT; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR AGONIST; N-(4-HYDROXY-3-METHOXYBENZYL)-4-(THIOPHEN-2-YL)BUTANAMIDE; THIOPHENE DERIVATIVE; TRPV1 PROTEIN, RAT; VANILLOID RECEPTOR;

ANALGESIC ACTIVITY; ARTICLE; CALCIUM CELL LEVEL; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG BINDING; DRUG CYTOTOXICITY; DRUG DESIGN; DRUG EFFICACY; DRUG IDENTIFICATION; DRUG POTENCY; DRUG SCREENING; DRUG SYNTHESIS; EC50; EMBRYO; HUMAN; HUMAN CELL; HYDROGEN BOND; IC50; KERATINOCYTE; LIGAND BINDING; MOLECULAR DOCKING; NEUROBLASTOMA CELL LINE; OXIDATIVE STRESS; PRIORITY JOURNAL; AGONISTS; ANIMAL; CHEMISTRY; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; MALE; METABOLISM; MOLECULAR MODEL; SYNTHESIS; WISTAR RAT;

ANALGESICS; ANIMALS; CAPSAICIN; CHO CELLS; CRICETULUS; MALE; MODELS, MOLECULAR; OXIDATIVE STRESS; RATS, WISTAR; THIOPHENES; TRPV CATION CHANNELS;

EID: 84974834892     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/acschemneuro.5b00333     Document Type: Article

References (41)

1. Di Marzo, V. and De Petrocellis, L. (2010) Endocannabinoids as Regulators of Transient Receptor Potential (TRP) Channels: a Further Opportunity to Develop New Endocannabinoid-Based Therapeutic Drugs Curr. Med. Chem. 17, 1430-1449 10.2174/092986710790980078
2. Rebolledo, C. L., Sotelo-Hitschfeld, P., Brauchi, S., and Olavarría, M. Z. (2013) Design and synthesis of conformationally restricted capsaicin analogues based in 1,3,4-thiadiazole heterocycle reveal a novel family of transient receptor potential vanilloid 1 (TRPV1) antagonists Eur. J. Med. Chem. 66, 193-203 10.1016/j.ejmech.2013.05.001
3. Reyes-Escogido, M. L., Gonzalez-Mondragon, E. G., and Vazquez-Tzompantzi, E. (2011) Chemical and Pharmacological Aspects of Capsaicin Molecules 16, 1253-1270 10.3390/molecules16021253
4. Szallasi, A. and Blumberg, P. M. (1999) Vanilloid (Capsaicin) Receptors and Mechanisms Pharmacol. Rev. 51, 159-211
5. Jancsó, G., Oszlács, O., and Sántha, P. (2011) The Capsaicin Paradox: Pain Relief by an Algesic Agent Anti-Inflammatory Anti-Allergy Agents Med. Chem. 10, 52-65 10.2174/187152311795325514
6. Jansson, E. T., Trkulja, C. L., Ahemaiti, A., Millingen, M., Jeffries, G. DM., Jardemark, K., and Orwar, O. (2013) Effect of cholesterol depletion on the pore dilation of TRPV1 Mol. Pain 9, 1-9 10.1186/1744-8069-9-1
7. Rice-Evans, C. A., Miller, N. J., and Paganga, G. (1997) Antioxidant properties of phenolic compounds Trends Plant Sci. 2, 152-159 10.1016/S1360-1385(97)01018-2
8. Luo, X.-J., Peng, J., and Li, Y.-J. (2011) Recent advances in the study on capsaicinoids and capsinoids Eur. J. Pharmacol. 650, 1-7 10.1016/j.ejphar.2010.09.074
9. Wrigglesworth, R., Walpole, C. S., Bevan, S., Campell, E. A., Dray, A., Hughes, G. A., James, I., Masdin, K. J., and Winter, J. (1996) Analogues of Capsaicin with Agonist Activity as Novel Analgesic Agents: Structure-Activity Studies. 4. Potent, Orally Active Analgesics J. Med. Chem. 39, 4942-4951 10.1021/jm960512h
10. Lee, J. H., Lee, Y., Ryu, H., Kang, D. W., Lee, J., Lazar, J., Pearce, L. V., Pavlyukovets, V. A., Blumberg, P. M., and Choi, S. (2011) Structural insights into transient receptor potential vanilloid type 1 (TRPV1) from homology modelling, flexible docking, and mutational studies J. Comput.-Aided Mol. Des. 25, 317-327 10.1007/s10822-011-9421-5
11. Ursu, D., Knopp, K., Beattie, R. E., Liu, B., and Sher, E. (2010) Pungency of TRPV1 agonists is directly correlated with kinetics of receptor activation and lipophilicity Eur. J. Pharmacol. 641, 114-122 10.1016/j.ejphar.2010.05.029
12. Wong, G. Y. and Gavva, N. R. (2009) Therapeutic potential of vanilloid receptor TRPV1 agonists and antagonists as analgesics: recent advances and setbacks Brain Res. Rev. 60, 267-277 10.1016/j.brainresrev.2008.12.006
13. Jordt, S.-E. and Julius, D. (2002) Molecular basis for Species-Specific Sensitivity to "Hot" Chili Peppers Cell 108, 421-430 10.1016/S0092-8674(02)00637-2
14. Winkler, M., Moraux, T., Khairy, H. A., Scott, R. H., Slawin, A. M. Z., and O'Hagan, D. (2009) Synthesis and Vanilloid Receptor (TRPV1) Activity of the Enantiomers of α-Fluorinated Capsaicin ChemBioChem 10, 823-828 10.1002/cbic.200800709
15. Brizzi, A., Aiello, F., Marini, P., Cascio, M. G., Corelli, F., Brizzi, V., De Petrocellis, L., Ligresti, A., Luongo, L., Lamponi, S., Maione, S., Pertwee, R. G., and Di Marzo, V. (2014) Structure-affinity relationships and pharmacological characterization of new alkyl-resorcinol cannabinoid receptor ligands: Identification of a dual cannabinoid receptor/TRPA1 channel agonist Bioorg. Med. Chem. 22, 4770-4783 10.1016/j.bmc.2014.07.006
16. Sticozzi, C., Belmonte, G., Cervellati, F., Di Capua, A., Maioli, E., Cappelli, A., Giordani, A., Biava, M., Anzini, M., and Valacchi, G. (2013) Antiproliferative effect of two novel COX-2 inhibitors on human keratinocytes Eur. J. Pharm. Sci. 49, 133-141 10.1016/j.ejps.2013.02.009
17. Valacchi, G., Rimbach, G., Saliou, C., Weber, S. U., and Packer, L. (2001) Effect of benzoyl peroxide on antioxidant status, NF-kappaB activity and interleukin-1alpha gene expression in human keratinocytes Toxicology 165, 225-234 10.1016/S0300-483X(01)00430-9
18. Valacchi, G., Davis, P. A., Khan, E. M., Lanir, R., Maioli, E., Pecorelli, A., Cross, C. E., and Goldkorn, T. (2011) Cigarette smoke exposure causes changes in Scavenger Receptor B1 level and distribution in lung cells Int. J. Biochem. Cell Biol. 43, 1065-1070 10.1016/j.biocel.2009.05.014
19. Rao, R. R. and Kisaalita, W. S. (2002) Biochemical and electrophysiological differentiation profile of a human neuroblastoma (IMR-32) cell line In vitro Cell Dev. Biol. Anim. 38, 450-456 10.1290/1071-2690(2002)038<0450:BAEDPO>2.0.CO;2
20. Abdullah, H., Heaney, L. G., Cosby, S. L., and McGarvey, L. P. (2014) Rhinovirus upregulates transient receptor potential channels in a human neuronal cell line: implications for respiratory virus-induced cough reflex sensitivity Thorax 69, 46-54 10.1136/thoraxjnl-2013-203894
21. Brizi, C., Santulli, C., Micucci, M., Budriesi, R., Chiarini, A., Aldinucci, C., and Frosini, M. (2016) Neuroprotective Effects of Castanea sativa Mill. Bark Extract in Human Neuroblastoma Cells Subjected to Oxidative Stress J. Cell. Biochem. 117, 510-520 10.1002/jcb.25302
22. Feng, Z., Pearce, L. V., Xu, X., Yang, X., Yang, P., Blumberg, P. M., and Xie, X. Q. (2015) Structural insight into tetrameric hTRPV1 from homology modeling, molecular docking, molecular dynamics simulation, virtual screening, and bioassay validations J. Chem. Inf. Model. 55, 572-588 10.1021/ci5007189
23. Lee, J. G., Yon, J. M., Lin, C., Jung, A. Y., Jung, K. Y., and Nam, S. Y. (2012) Combined treatment with capsaicin and resveratrol enhances neuroprotection against glutamate-induced toxicity in mouse cerebral cortical neurons Food Chem. Toxicol. 50, 3877-3885 10.1016/j.fct.2012.08.040
24. Marini, E., Magi, G., Mingoia, M., Pugnaloni, A., and Facinelli, B. (2015) Antimicrobial and Anti-Virulence Activity of Capsaicin Against Erythromycin-Resistant, Cell-Invasive Group A Streptococci Front. Microbiol. 6, 1281 10.3389/fmicb.2015.01281
25. Yang, F., Xiao, X., Cheng, W., Yang, W., Yu, P., Song, Z., Yarov-Yarovoy, V., and Zheng, J. (2015) Structural mechanism underlying capsaicin binding and activation of the TRPV1 ion channel Nat. Chem. Biol. 11, 518-524 10.1038/nchembio.1835
26. Schrodinger LLC. ((2015) Maestro, version 10.1, Schrödinger, LLC, New York.
27. Kirchmair, J., Laggner, C., Wolber, G., and Langer, T. (2005) Comparative analysis of protein-bound ligand conformations with respect to catalyst's conformational space subsampling algorithms J. Chem. Inf. Model. 45, 422-430 10.1021/ci049753l
28. Jorgensen, W. L., Maxwell, D. S., and Tirado-Rives, J. (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids J. Am. Chem. Soc. 118, 11225-11236 10.1021/ja9621760
29. Congreve, M., Murray, C. W., and Blundell, T. L. (2005) Structural biology and drug discovery Drug Discovery Today 10, 895-907 10.1016/S1359-6446(05)03484-7
30. Schrodinger LLC. ((2015) S chrödinger Suite 2015-1 Protein Preparation Wizard, Epik version 3.1 Schrödinger, LLC, New York.
31. Schrodinger LLC. ((2015) Impact, version 6.6, Schrödinger, LLC, New York.
32. Schrodinger LLC. ((2015) Prime, version 3.9 Schrödinger, LLC, New York.
33. Schrodinger LLC. ((2015) Glide, version 6.6 Schrödinger, LLC, New York.
34. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935 10.1063/1.445869
35. Jorgensen, W. L. and Madura, J. D. (1985) Temperature and size dependence for monte carlo simulations of TIP4P water Mol. Phys. 56, 1381-1392 10.1080/00268978500103111
36. Desmond Molecular Dynamics System, version 4.1 (2015) D. E. Shaw Research, New York.
37. Schrodinger LLC. ((2015) Maestro-Desmond Interoperability Tools, version 4.1, Schrödinger, New York.
38. Schrodinger LLC. ((2015) The PyMOL Molecular Graphics System, Version 1.7.0.0. Schrödinger, LLC, New York.
39. Quincozes-Santos, A., Bobermin, L. D., Tramontina, A. C., Wartchow, K. M., Tagliari, B., Souza, D. O., Wyse, A. T., and Gonçalves, C. A. (2014) Oxidative stress mediated by NMDA, AMPA/KA channels in acute hippocampal slices: neuroprotective effect of resveratrol Toxicol. In Vitro 28, 544-551 10.1016/j.tiv.2013.12.021
40. Contartese, A., Valoti, M., Corelli, F., Pasquini, S., Mugnaini, C., Pessina, F., Aldinucci, C., Sgaragli, G., and Frosini, M. (2012) A novel CB2 agonist, COR167, potently protects rat brain cortical slices against OGD and reperfusion injury Pharmacol. Res. 66, 555-563 10.1016/j.phrs.2012.08.003
41. Abbott, F. V. and Guy, E. R. (1995) Effects of morphine, pentobarbital and amphetamine on formalin-induced behaviours in infant rats: sedation versus specific suppression of pain Pain 62, 303-312 10.1016/0304-3959(94)00277-L