Effect of chirality and lipophilicity in the functional activity of evodiamine and its analogues at TRPV1 channels

British Journal of Pharmacology

Volumn 171, Issue 10, 2014, Pages 2608-2620

  De Petrocellis, Luciano ^a   Schiano Moriello, Aniello ^b   Fontana, Gabriele ^c   Sacchetti, Alessandro ^d   Passarella, Daniele ^e   Appendino, Giovanni ^f   Di Marzo, Vincenzo ^b  

^a CNR   (Italy)

^b CNR   (Italy)

^c Research and Development   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

^e POLITECNICO DI MILANO   (Italy)

^f UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

Capsaicin; Evodiamine; Palvanil; TRP channels; TRPV1; Vanilloids

Indexed keywords

ALKALOID DERIVATIVE; CAPSAICIN; EVODIAMINE; VANILLOID RECEPTOR 1; AGENTS AFFECTING WATER, MOLECULE OR ION TRANSPORT; HERBACEOUS AGENT; QUINAZOLINE DERIVATIVE; TRPV1 PROTEIN, HUMAN; TRPV1 PROTEIN, RAT; VANILLOID RECEPTOR;

ARTICLE; CALCIUM CELL LEVEL; CHIRALITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENCY; ENANTIOMER; HEK293 CELL LINE; IC 50; LIPOPHILICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RACEMIC MIXTURE; STRUCTURE ACTIVITY RELATION; AGONISTS; ANIMAL; CALCIUM SIGNALING; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; DOSE RESPONSE; DRUG DESIGN; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; HUMAN; ISOMERISM; METABOLISM; RAT;

ANIMALS; CALCIUM SIGNALING; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DESIGN; DRUGS, CHINESE HERBAL; HEK293 CELLS; HUMANS; ISOMERISM; MEMBRANE TRANSPORT MODULATORS; MOLECULAR STRUCTURE; QUINAZOLINES; RATS; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSFECTION; TRPV CATION CHANNELS;

EID: 84900831327     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12320     Document Type: Article

References (83)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Catterall WA, Spedding M, Peters JA, Harmar AJ, and CGTP Collaborators (2013). The Concise Guide to PHARMACOLOGY 2013/14: Overview. Br J Pharmacol 170: 1449-1867.
2. Appendino G, De Petrocellis L, Trevisani M, Minassi A, Daddario N, Moriello AS, et al. (2005). Development of the first ultra-potent 'capsaicinoid' agonist at transient receptor potential vanilloid type 1 (TRPV1) channels and its therapeutic potential. J Pharmacol Exp Ther 312: 61-70.
3. Appendino G, Cascio MG, Bacchiega S, Moriello AS, Minassi A, Thomas A, et al. (2006). First 'hybrid' ligands of vanilloid TRPV1 and cannabinoid CB2 receptors and non-polyunsaturated fatty acid-derived CB2-selective ligands. FEBS Lett 580: 568-574.
4. Appendino G, Ligresti A, Minassi A, Cascio MG, Allarà M, Taglialatela-Scafati O, et al. (2009). Conformationally constrained fatty acid ethanolamides as cannabinoid and vanilloid receptor probes. J Med Chem 52: 3001-3009.
5. Bak EJ, Park HG, Kim JM, Kim JM, Yoo YJ, Cha JH, (2010). Inhibitory effect of evodiamine alone and in combination with rosiglitazone on in vitro adipocyte differentiation and in vivo obesity related to diabetes. Int J Obes 34: 250-260.
6. Basbaum AI, Bautista DM, Scherrer G, Julius D, (2009). Cellular and molecular mechanisms of pain. Cell 139: 267-284.
7. Bodkin JV, Fernandes ES, (2013). TRPV1 and SP: key elements for sepsis outcome? Br J Pharmacol 170: 1279-1292.
8. Bohlen CJ, Priel A, Zhou S, King D, Siemens J, Julius D, (2010). A bivalent tarantula toxin activates the capsaicin receptor, TRPV1, by targeting the outer pore domain. Cell 141: 834-845.
9. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D, (1997). The capsaicin receptor: a heat-Activated ion channel in the pain pathway. Nature 389: 816-824.
10. Changani K, Hotee S, Campbell S, Pindoria K, Dinnewell L, Saklatvala P, et al. (2013). Effect of the TRPV1 antagonist SB-705498 on the nasal parasympathetic reflex response in the ovalbumin sensitized guinea pig. Br J Pharmacol 169: 580-589.
11. Chen MC, Yu CH, Wang SW, Pu HF, Kan SF, Lin LC, et al. (2010). Anti-proliferative effects of evodiamine on human thyroid cancer cell line ARO. J Cell Biochem 110: 1495-1503.
12. Ching L-C, Kou YR, Shyue S-K, Su K-H, Wei J, Cheng L-C, et al. (2011). Molecular mechanisms of activation of endothelial nitric oxide synthase mediated by transient receptor potential vanilloid type 1. Cardiovasc Res 91: 492-501.
13. Chiou WF, Liao JF, Chen CF, (1996). Comparative study on the vasodilatory effects of three quinazoline alkaloids isolated from Evodia rutaecarpa. J Nat Prod 59: 374-378.
14. Cristino L, de Petrocellis L, Pryce G, Baker D, Guglielmotti V, Di Marzo V, (2006). Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 139: 1405-1415.
15. Czikora Á, Lizanecz E, Bakõ P, Rutkai I, Ruzsnavszky F, Magyar J, et al. (2012). Structure-Activity relationships of vanilloid receptor agonists for arteriolar TRPV1. Br J Pharmacol 165: 1801-1812.
16. Danieli B, Palmisano G, (1978). A new approach to quinazolinocarboline alkaloids: synthesis of (±) evodiamine, rutaecarpine and dehydroevodiamine. Heterocycles 9: 803-806.
17. De Petrocellis L, Di Marzo V, (2005). Lipids as regulators of the activity of transient receptor potential type V1 (TRPV1) channels. Life Sci 77: 1651-1666.
18. De Petrocellis L, Bisogno T, Davis JB, Pertwee RG, Di Marzo V, (2000). Overlap between the ligand recognition properties of the anandamide transporter and the VR1 vanilloid receptor: inhibitors of anandamide uptake with negligible capsaicin-like activity. FEBS Lett 483: 52-56.
19. De Petrocellis L, Bisogno T, Maccarrone M, Davis JB, Finazzi-Agrò A, Di Marzo V, (2001). The activity of anandamide at vanilloid VR1 receptors requires facilitated transport across the cell membrane and is limited by intracellular metabolism. J Biol Chem 276: 12856-12863.
20. De Petrocellis L, Guida F, Moriello AS, De Chiaro M, Piscitelli F, de Novellis V, et al. (2011). N-palmitoyl-vanillamide (palvanil) is a non-pungent analogue of capsaicin with stronger desensitizing capability against the TRPV1 receptor and anti-hyperalgesic activity. Pharmacol Res 63: 294-299.
21. De Petrocellis L, Schiano Moriello A, Imperatore R, Cristino L, Starowicz K, Di Marzo V, (2012). A re-evaluation of 9-HODE activity at TRPV1 channels in comparison to anandamide: enantioselectivity and effects at other TRP channels and in sensory neurons. Br J Pharmacol 167: 1643-1651.
22. Delescluse I, Mace H, Adcock JJ, (2012). Inhibition of airway hyper-responsiveness by TRPV1 antagonists (SB-705498 and PF-04065463) in the unanaesthetized, ovalbumin-sensitized guinea pig. Br J Pharmacol 166: 1822-1832.
23. Domenicali M, Ros J, Fernandez-Varo G, Cejudo-Martin P, Crespo M, Morales-Ruiz M, et al. (2005). Increased anandamide induced relaxation in mesenteric arteries of cirrhotic rats: role of cannabinoid and vanilloid receptors. Gut 54: 522-527.
24. Dong G, Wang S, Miao Z, Yao J, Zhang Y, Guo Z, et al. (2012). New tricks for an old natural product: discovery of highly potent evodiamine derivatives as novel antitumor agents by systemic structure-Activity relationship analysis and biological evaluations. J Med Chem 55: 7593-7613.
25. Ferrer-Montiel A, Fernández-Carvajal A, Planells-Cases R, Fernández-Ballester G, González-Ros JM, Messeguer A, et al. (2012). Advances in modulating thermosensory TRP channels. Expert Opin Ther Pat 22: 999-1017.
26. Gavva NR, Klionsky L, Qu Y, Shi L, Tamir R, Edenson S, et al. (2004). Molecular determinants of vanilloid sensitivity in TRPV1. J Biol Chem 279: 20283-20295.
27. Gijsen HJ, Berthelot D, De Cleyn MA, Geuens I, Brône B, Mercken M, (2012). Tricyclic 3,4-dihydropyrimidine-2-thione derivatives as potent TRPA1 antagonists. Bioorg Med Chem Lett 22: 797-800.
28. Gomtsyan A, Bayburt EK, Keddy R, Turner SC, Jinkerson TK, Didomenico S, et al. (2007). Alpha-methylation at benzylic fragment of N-Aryl-N′-benzyl ureas provides TRPV1 antagonists with better pharmacokinetic properties and higher efficacy in inflammatory pain model. Bioorg Med Chem Lett 17: 3894-3899.
29. Hwang SW, Cho H, Kwak J, Lee SY, Kang CJ, Jung J, et al. (2000). Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci U S A 97: 6155-6160.
30. Jara-Oseguera A, Simon SA, Rosenbaum T, (2008). TRPV1: on the road to pain relief. Curr Mol Pharmacol 1: 255-269.
31. Jiang J, Hu C, (2009). Evodiamine: a novel anti-cancer alkaloid from Evodia rutaecarpa. Molecules 14: 1852-1859.
32. Jordt SE, Julius D, (2002). Molecular basis for species-specific sensitivity to 'hot' chili peppers. Cell 108: 421-430.
33. Jung J, Hwang SW, Kwak J, Lee SY, Kang CJ, Kim WB, et al. (1999). Capsaicin binds to the intracellular domain of the capsaicin-Activated ion channel. J Neurosci 19: 529-538.
34. Jung J, Lee SY, Hwang SW, Cho H, Shin J, Kang YS, et al. (2002). Agonist recognition sites in the cytosolic tails of vanilloid receptor 1. J Biol Chem 277: 44448-44454.
35. Kan SF, Huang WJ, Lin LC, Wang PS, (2004). Inhibitory effects of evodiamine on the growth of human prostate cancer cell line LNCaP. Int J Cancer 110: 641-651.
36. Kan SF, Yu CH, Pu HF, Hsu JM, Chen MJ, Wang PS, (2007). Anti-proliferative effects of evodiamine on human prostate cancer cell lines DU145 and PC3. J Cell Biochem 101: 44-56.
37. Ko HC, Wang YH, Liou KT, Chen CM, Chen CH, Wang WY, et al. (2007). Anti-inflammatory effects and mechanisms of the ethanol extract of Evodia rutaecarpa and its bioactive components on neutrophils and microglial cells. Eur J Pharmacol 555: 211-217.
38. Kobayashi Y, (2003). The nociceptive and anti-nociceptive effects of evodiamine from fruits of Evodia rutaecarpa in mice. Planta Med 69: 425-428.
39. Kobayashi Y, Nakano Y, Hoshikuma K, Yokoo Y, Kamiya T, (2000). The bronchoconstrictive action of evodiamine, an indoloquinazoline alkaloid isolated from the fruits of Evodia rutaecarpa, on guinea-pig isolated bronchus: possible involvement on vanilloid receptors. Planta Med 66: 526-530.
40. Kobayashi Y, Hoshikuma K, Nakano Y, Yokoo Y, Kamiya T, (2001a). The positive inotropic and chronotropic effects of evodiamine and rutaecarpine, indoloquinazoline alkaloids isolated from the fruits of Evodia rutaecarpa, on the guinea-pig isolated right atria: possible involvement of vanilloid receptors. Planta Med 67: 244-248.
41. Kobayashi Y, Nakano Y, Kizaki M, Hoshikuma K, Yokoo Y, Kamiya T, (2001b). Capsaicin-like anti-obese activities of evodiamine from fruits of Evodia rutaecarpa, a vanilloid receptor agonist. Planta Med 67: 628-633.
42. Kym PR, Kort ME, Hutchins CW, (2009). Analgesic potential of TRPV1 antagonists. Biochem Pharmacol 78: 211-216.
43. Lazar J, Braun DC, Tõth A, Wang Y, Pearce LV, Pavlyukovets VA, et al. (2006). Kinetics of penetration influence the apparent potency of vanilloids on TRPV1. Mol Pharmacol 69: 1166-1173.
44. Lee JH, Lee Y, Ryu H, Kang DW, Lee J, Lazar J, et al. (2011). Structural insights into transient receptor potential vanilloid type 1 (TRPV1) from homology modeling, flexible docking, and mutational studies. J Comput Aided Mol Des 25: 317-327.
45. Lee TJ, Kim EJ, Kim S, Jung EM, Park JW, Jeong SH, et al. (2006). Caspase-dependent and caspase-independent apoptosis induced by evodiamine in human leukemic U937 cells. Mol Cancer Ther 5: 2398-2407.
46. Liao C-H, Pan S-L, Guh J-H, Chang Y-L, Pai H-C, Lin C-H, et al. (2005). Antitumor mechanism of evodiamine, a constituent from Chinese herb Evodiae fructus, in human multiple-drug resistant breast cancer NCI/ADR-RES cells in vitro and in vivo. Carcinogenesis 26: 968-975.
47. Lu J-J, Bao J-L, Chen X-P, Huang M, Wang Y-T, (2012). Alkaloids isolated from natural herbs as the anticancer agents. Evid Based Complement Alternat Med 2012: 485042, 1-12.
48. Melck D, Bisogno T, De Petrocellis L, Chuang H, Julius D, Bifulco M, et al. (1999). Unsaturated long-chain N-Acyl-vanillyl-Amides (N-AVAMs): vanilloid receptor ligands that inhibit anandamide-facilitated transport and bind to CB1 cannabinoid receptors. Biochem Biophys Res Commun 262: 275-284.
49. Moran MM, McAlexander MA, Biro T, Szallasi A, (2011). Transient receptor potential channels as therapeutic targets. Nat Rev Drug Discov 10: 601-620.
50. Movahed P, Jönsson BA, Birnir B, Wingstrand JA, Jørgensen TD, Ermund A, et al. (2005). Endogenous unsaturated C18 N-Acylethanolamines are vanilloid receptor (TRPV1) agonists. J Biol Chem 280: 38496-38504.
51. Myers BR, Bohlen CJ, Julius D, (2008). A yeast genetic screen reveals a critical role for the pore helix domain in TRP channel gating. Neuron 58: 362-373.
52. Nilius B, Owsianik G, (2010). Transient receptor potential channelopathies. Pflugers Arch 460: 437-450.
53. O'Dell DK, Rimmerman N, Pickens SR, Walker JM, (2007). Fatty acyl amides of endogenous tetrahydroisoquinolines are active at the recombinant human TRPV1 receptor. Bioorg Med Chem 15: 6164-6169.
54. Ortar G, De Petrocellis L, Schiano Moriello A, Allarà M, Morera E, Nalli M, et al. (2013). Tetrahydro-β-carboline derivatives targeting fatty acid amide hydrolase (FAAH) and transient receptor potential (TRP) channels. Bioorg Med Chem Lett 23: 138-142.
55. Patapoutian A, Tate S, Woolf CJ, (2009). Transient receptor potential channels: targeting pain at the source. Nat Rev Drug Discov 8: 55-68.
56. Pearce LV, Petukhov PA, Szabo T, Kedei N, Bizik F, Kozikowski AP, et al. (2004). Evodiamine functions as an agonist for the vanilloid receptor TRPV1. Org Biomol Chem 2: 2281-2286.
57. Phillips E, Reeve A, Bevan S, McIntyre P, (2004). Identification of species-specific determinants of the action of the antagonist capsazepine and the agonist PPAHV on TRPV1. J Biol Chem 279: 17165-17172.
58. Rang WQ, Du YH, Hu CP, Ye F, Tan GS, Deng HW, et al. (2003). Protective effects of calcitonin gene-related peptide-mediated evodiamine on guinea-pig cardiac anaphylaxis. Naunyn Schmiedebergs Arch Pharmacol 367: 306-311.
59. Rang WQ, Du YH, Hu CP, Ye F, Xu KP, Peng J, et al. (2004). Protective effects of evodiamine on myocardial ischemia-reperfusion injury in rats. Planta Med 70: 1140-1143.
60. Sanchez JF, Krause JE, Cortright DN, (2001). The distribution and regulation of vanilloid receptor VR1 and VR1 5′ splice variant RNA expression in rat. Neuroscience 107: 373-381.
61. 2+-dependent desensitization of TRPV1 targets the receptor to lysosomes for degradation. J Biol Chem 287: 19462-19471.
62. Shyu KG, Lin S, Lee CC, Chen E, Lin LC, Wang BW, et al. (2006). Evodiamine inhibits in vitro angiogenesis: implication for antitumorgenicity. Life Sci 78: 2234-2243.
63. Siemens J, Siemens J, Zhou S, Piskorowski R, Nikai T, Lumpkin EA, et al. (2006). Spider toxins activate the capsaicin receptor to produce inflammatory pain. Nature 444: 208-212.
64. Tetko IV, Gasteiger J, Todeschini R, Mauri A, Livingstone D, Ertl P, et al. (2005). Virtual computational chemistry laboratory-design and description. J Comput Aid Mol Des 19: 453-463.
65. Tu YJ, Fan X, Yang X, Zhang C, Liang HP, (2013). Evodiamine activates autophagy as a cytoprotective response in murine Lewis lung carcinoma cells. Oncol Rep 29: 481-490.
66. Ursu D, Knopp K, Beattie RE, Liu B, Sher E, (2010). Pungency of TRPV1 agonists is directly correlated with kinetics of receptor activation and lipophilicity. Eur J Pharmacol 641: 114-122.
67. Vallin KS, Sterky KJ, Nyman E, Bernström J, From R, Linde C, et al. (2012). N-1-Alkyl-2-oxo-2-Aryl amides as novel antagonists of the TRPA1 receptor. Bioorg Med Chem Lett 22: 5485-5492.
68. Venkatachalam K, Montell C, (2007). TRP channels. Annu Rev Biochem 76: 387-417.
69. Vriens J, Appendino G, Nilius B, (2009). Pharmacology of vanilloid transient receptor potential cation channels. Mol Pharmacol 75: 1262-1279.
70. Wahl P, Foged C, Tullin S, Thomsen C, (2001). Iodo-resiniferatoxin, a new potent vanilloid receptor antagonist. Mol Pharmacol 59: 9-15.
71. Wang C, Li S, Wang MW, (2010). Evodiamine-induced human melanoma A375-S2 cell death was mediated by PI3K/Akt/caspase and Fas-L/NF-kappaB signaling pathways and augmented by ubiquitin-proteasome inhibition. Toxicol In Vitro 24: 898-904.
72. Wang L, Wang DH, (2005). TRPV1 gene knockout impairs post-ischemic recovery in isolated perfused heart in mice. Circulation 112: 3617-3623.
73. Wang T, Wang Y, Kontani Y, Kobayashi Y, Sato Y, Mori N, et al. (2008). Evodiamine improves diet-induced obesity in a uncoupling protein-1-independent manner: involvement of antiadipogenic mechanism and extracellularly regulated kinase/mitogen-Activated protein kinase signaling. Endocrinology 149: 358-366.
74. Wang Z, Sun L, Yu H, Zhang Y, Gong W, Jin H, et al. (2012). Binding mode prediction of evodiamine within vanilloid receptor TRPV1. Int J Mol Sci 13: 8958-8969.
75. Wei J, Ching L-C, Zhao JF, Shyue SK, Lee HF, Kou YR, et al. (2013). Essential role of transient receptor potential vanilloid type 1 in evodiamine-mediated protection against atherosclerosis. Acta Physiol 207: 299-307.
76. Wen H, Östman J, Bubb KJ, Panayiotou C, Priestley JV, Baker MD, et al. (2012). 20-Hydroxyeicosatetraenoic acid (20-HETE) is a novel activator of transient receptor potential vanilloid 1 (TRPV1) channel. J Biol Chem 287: 13868-13876.
77. Yang J, Wu LJ, Tashino S, Onodera S, Ikejima T, (2008). Reactive oxygen species and nitric oxide regulate mitochondria-dependent apoptosis and autophagy in evodiamine-treated human cervix carcinoma HeLa cells. Free Radic Res 42: 492-504.
78. Yang J, Cai X, Lu W, Hu C, Xu X, Yu Q, et al. (2013). Evodiamine inhibits STAT3 signaling by inducing phosphatase shatterproof 1 in hepatocellular carcinoma cells. Cancer Lett 328: 243-251.
79. Yang ZG, Chen AQ, Liu B, (2009). Antiproliferation and apoptosis induced by evodiamine in human colorectal carcinoma cells (COLO-205). Chem Biodivers 6: 924-933.
80. Yao X, Garland CJ, (2005). Recent developments in vascular endothelial cell transient receptor potential channels. Circ Res 97: 853-863.
81. Zhang C, Fan X, Xu X, Yang X, Wang X, Liang HP, (2010). Evodiamine induces caspase-dependent apoptosis and S phase arrest in human colon lovo cells. Anticancer Drugs 21: 766-776.
82. Zhu B, Xia M, Xu X, Ludovici DW, Tennakoon M, Youngman MA, et al. (2013). Arylglycine derivatives as potent transient receptor potential melastatin 8 (TRPM8) antagonists. Bioorg Med Chem Lett 23: 2234-2237.
83. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sørgård M, Di Marzo V, et al. (1999). Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400: 452-457.