Pharmacological Potential of cis-jasmone in Adult Zebrafish (Danio rerio)

Francisca Magnólia Diógenes Holanda Bezerra; Antônio Eufrásio Vieira-Neto; Samara Casemiro Benevides; Kaio César Simiano Tavares; Antonia Deyse de Castro Ribeiro; Sacha Aubrey Alves Rodrigues Santos; Gerlânia de Oliveira Leite; Francisco Ernani Alves Magalhães; Adriana Rolim Campos

doi:10.1055/a-1988-2098

Planta Medica, Table of Contents

Planta Med 2023; 89(05): 539-550
DOI: 10.1055/a-1988-2098

Biological and Pharmacological Activity

Original Papers

Pharmacological Potential of cis-jasmone in Adult Zebrafish (Danio rerio)

Francisca Magnólia Diógenes Holanda Bezerra

¹Universidade de Fortaleza, Núcleo de Biologia Experimental (NUBEX), Fortaleza, Ceará, Brazil

,

Antônio Eufrásio Vieira-Neto

¹Universidade de Fortaleza, Núcleo de Biologia Experimental (NUBEX), Fortaleza, Ceará, Brazil

,

Samara Casemiro Benevides

¹Universidade de Fortaleza, Núcleo de Biologia Experimental (NUBEX), Fortaleza, Ceará, Brazil

,

Kaio César Simiano Tavares

¹Universidade de Fortaleza, Núcleo de Biologia Experimental (NUBEX), Fortaleza, Ceará, Brazil

,

Antonia Deyse de Castro Ribeiro

¹Universidade de Fortaleza, Núcleo de Biologia Experimental (NUBEX), Fortaleza, Ceará, Brazil

,

Sacha Aubrey Alves Rodrigues Santos

¹Universidade de Fortaleza, Núcleo de Biologia Experimental (NUBEX), Fortaleza, Ceará, Brazil

,

Gerlânia de Oliveira Leite

¹Universidade de Fortaleza, Núcleo de Biologia Experimental (NUBEX), Fortaleza, Ceará, Brazil

,

Francisco Ernani Alves Magalhães

¹Universidade de Fortaleza, Núcleo de Biologia Experimental (NUBEX), Fortaleza, Ceará, Brazil

²Universidade Estadual do Ceará (UECE- CECITEC), Laboratório de Bioprospecção de Produtos Naturais e Biotecnologia (LBPNB), Tauá, Ceará, Brazil

,

Adriana Rolim Campos

¹Universidade de Fortaleza, Núcleo de Biologia Experimental (NUBEX), Fortaleza, Ceará, Brazil

› Author Affiliations

Abstract

This study evaluates the pharmacological potential of cis-jasmone (CJ) in adult zebrafish (Danio rerio; aZF). Initially, aZF (n = 6/group) were pretreated (20 µL; p. o.) with CJ (0.1 or 0.3 or 1.0 mg/mL) or vehicle (0.5% Tween 80). The animals were submitted to acute toxicity and locomotion tests, pentylenetetrazole-induced seizure, carrageenan-induced abdominal edema, and cinnamaldehyde-, capsaicin-, menthol-, glutamate-, and acid saline-induced orofacial nociception. The possible mechanisms of anticonvulsant, anxiolytic, and antinociceptive action were evaluated. The involvement of central afferent fibers sensitive to cinnamaldehyde and capsaicin and the effect of CJ on the relative gene expression of TRPA1 and TRPV1 in the brain of aZF were also analyzed, in addition to the study of molecular docking between CJ and TRPA1, TRPV1 channels, and GABA_A receptors. CJ did not alter the locomotor behavior and showed pharmacological potential in all tested models with no toxicity. The anticonvulsant effect of CJ was prevented by flumazenil (GABAergic antagonist). The anxiolytic-like effect of CJ was prevented by flumazenil and serotonergic antagonists. The antinociceptive effect was prevented by TRPA1 and TRPV1 antagonists. Chemical ablation with capsaicin and cinnamaldehyde prevented the orofacial antinociceptive effect of CJ. Molecular docking studies indicate that CJ interacted with TRPA1, TRPV1, and GABA_A receptors. CJ inhibited the relative gene expression of TRPA1 and TRPV1. CJ has pharmacological potential for the treatment of seizures, anxiety, inflammation, and acute orofacial nociception. These effects are obtained by modulating the GABAergic and serotonergic systems, as well as the TRPs and ASIC channels.

Key words

cis-jasmone - seizure - anxiety - inflammation - acute orofacial nociception - GABA_A and TRP receptors

Full Text

References

References
1 Lis-Balchin M, Hart S, Lo BWH. Jasmine absolute (Jasminum grandiflora L.) and its mode of action on guinea-pig ileum in vitro . Phytother Res 2002; 16: 437-439
2 Kaviani M, Maghbool S, Azima S, Tabaei MH. Comparison of the effect of aromatherapy with Jasminum officinale and Salvia officinale on pain severity and labor outcome in nulliparous women. Iran J Nurs Midwifery Res 2014; 19: 666-672
3 Temraz A, Cionib PL, Flaminib G, Bracab A. Chemical composition of the essential oil from Jasminum pubescens Leaves and flowers. Natural Product Communications 2009; 4912: 1729-1732
4 Umukoro S, Olugbemide AS. Antinociceptive effects of methyl jasmonate in experimental animals. J Nat Med 2011; 65: 466-470
5 OʼNeil MJ. (ed) The Merck Index. 15th ed. Cambridge, UK: Royal Society of Chemistry; 2013: 974
6 Ai L, Hu J, Ji X, Zhao H. Structure confirmation and thermal kinetics of the inclusion of cis-jasmone in β-cyclodextrin. RSC advances 2019; 9: 26224-26229
7 Knudsen JT, Eriksson R, Gershenzon J, Stahl B. Diversity and distribution of floral perfume. Bot Rev 2006; 72: 1-120
8 Linares AMP, Hernandes C, Franca SC, Loutenco MV. Atividade fitorreguladora de jasmonatos produzidos por Botryosphaeria rhodina . Horticultura Brasileira 2010; 28: 430-434
9 Silva AM, Soares CCG. A utilização do jasmim (Jasminum officinale) no combate à insônia. In: 54 °CONGRESSO DE QUÍMICA, Natal, Anais … Natal, Rio Grande do Norte, Brasil [s.n.]. 2014. Accessed January 25, 2923 at: http://www.abq.org.br/cbq/2014/trabalhos/7/5230-19365.html
10 Carrera ALC, Moreno IF, Besson JCF, Natali MRM. Análise da resposta tecidual e atividade antineuroinflamatória colônica do metil jasmonato na retocolite ulcerativa crônica induzida por ácido trinitrobenzosulfônico em ratos. Iniciação Científica CESUMAR 2019; 21: 153-162
11 Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assunção JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, Chi J, Fu B, Langley E, Maguire SF, Laird GK, Lloyd D, Kenyon E, Donaldson S, Sehra H, Almeida-King J, Loveland J, Trevanion S, Jones M, Quail M, Willey D, Hunt A, Burton J, Sims S, McLay K, Plumb B, Davis J, Clee C, Oliver K, Clark R, Riddle C, Elliot D, Threadgold G, Harden G, Ware D, Begum S, Mortimore B, Kerry G, Heath P, Phillimore B, Tracey A, Corby N, Dunn M, Johnson C, Wood J, Clark S, Pelan S, Griffiths G, Smith M, Glithero R, Howden P, Barker N, Lloyd C, Stevens C, Harley J, Holt K, Panagiotidis G, Lovell J, Beasley H, Henderson C, Gordon D, Auger K, Wright D, Collins J, Raisen C, Dyer L, Leung K, Robertson L, Ambridge K, Leongamornlert D, McGuire S, Gilderthorp R, Griffiths C, Manthravadi D, Nichol S, Barker G, Whitehead S, Kay M, Brown J, Murnane C, Gray E, Humphries M, Sycamore N, Barker D, Saunders D, Wallis J, Babbage A, Hammond S, Mashreghi-Mohammadi M, Barr L, Martin S, Wray P, Ellington A, Matthews N, Ellwood M, Woodmansey R, Clark G, Cooper J, Tromans A, Grafham D, Skuce C, Pandian R, Andrews R, Harrison E, Kimberley A, Garnett J, Fosker N, Hall R, Garner P, Kelly D, Bird C, Palmer S, Gehring I, Berger A, Dooley CM, Ersan-Ürün Z, Eser C, Geiger H, Geisler M, Karotki L, Kirn A, Konantz J, Konantz M, Oberländer M, Rudolph-Geiger S, Teucke M, Lanz C, Raddatz G, Osoegawa K, Zhu B, Rapp A, Widaa S, Langford C, Yang F, Schuster SC, Carter NP, Harrow J, Ning Z, Herrero J, Searle SM, Enright A, Geisler R, Plasterk RH, Lee C, Westerfield M, de Jong PJ, Zon LI, Postlethwait JH, Nüsslein-Volhard C, Hubbard TJ, Roest Crollius H, Rogers J, Stemple DL. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013; 496: 498-503
12 Magalhães FEA, de Sousa CÁPB, Santos SAAR, Menezes RB, Batista FLA, Abreu ÂO, de Oliveira MV, Moura LFWG, Raposo RDS, Campos AR. Adult zebrafish (Danio rerio): an alternative behavioral model of formalin-Induced nociception. Zebrafish 2017; 14: 422-429
13 Lima MCL, de Araújo JIF, Mota CG, Magalhães FEA, Campos AR, da Silva PT, Rodrigues THS, Matos MGC, de Sousa KC, de Sousa MB, Saker-Sampaio S, Pereira AL, Texeira EH, dos Santos HS. Antinociceptive effect of the essential oil Of Schinus terebinthifolius (female) leaves on adult zebrafish (Danio rerio). Zebrafish 2020; 17: 112-119
14 Magalhães FEA, Batista FLA, Lima LMG, Abrante IA, Batista FLA, Abrante IA, de Araújo JIF, Santos SAAR, de Oliveira BA, Raposo RS, Campos AR. Adult zebrafish (Danio rerio) as a model for the study of corneal antinociceptive compounds. Zebrafish 2018; 5: 566-574
15 do Nascimento JET, de Morais SM, de Lisboa DS, Sousa MO, Santos SAAR, Magalhães FEA, Campos AR. The orofacial antinociceptive effect of kaempferol-3-O-rutinoside, isolated from the plant Ouratea fieldingiana, on adult zebrafish (Danio rerio). Biomed Pharmacother 2018; 107: 1030-1036
16 Soares ICR, Santos SAAR, Coelho RF, Alves YA, Vieira-Neto AE, Tavares KCS, Magalhães FEA, Campos AR. Oleanolic acid promotes orofacial antinociception in adult zebrafish (Danio rerio) through TRPV1 receptors. Chemico-Biological Interactions 2019; 299: 37-43
17 Huang SY, Feng CW, Hung HC, Chakraborty C, Chen CH, Chen WF, Jean YH, Wang HM, Sung CS, Sun YM, Wu CY, Liu W, Hsiao CD, Wen ZH. A novel zebrafish model to provide mechanistic insights into the inflammatory events in carrageenan-induced abdominal edema. PLoS One 2014; 9: e104414
18 Gebauer DL, Pagnussat N, Piato AL, Schaefer IC, Bonan CD, Lara DR. Effects of anxiolytics in zebrafish: similarities and differences between benzodiazepines, buspirone and ethanol. Pharmacol Biochem Behav 2011; 99: 480-486
19 da Silva AW, Ferreira MKA, Rebouças EL, Silva FCO, Holanda CLA, Barroso SM, Batista FLA, Mendes FRS, Campos AR, de Menezes JASA, Magalhães FEA, Siqueira SMC, dos Santos HS. Anxiolytic-like effect of Azadirachta indica A. Juss. (Neem, Meliaceae) bark on adult zebrafish (Danio rerio): participation of the serotoninergic and GABAergic systems. Pharm Pharmacol Int J 2020; 8: 256-263
20 Mrazova A, Sam KA. Application of methyl jasmonate to grey willow (Salix cinerea) attracts insectivorous birds in nature. Arthropod-Plant Interactions 2018; 12: 1-8
21 Cachat J, Stewart A, Utterback E, Hart P, Gaikwad S, Wong K. Three-dimensional neurophenotyping of adult zebrafish behavior. PLoS One 2011; 6: 17597-17610
22 Taylor JC, Dewberry LS, Totsch SK, Yessick LR, DeBerry JJ, Watts SA, Sorge RE. A novel zebrafish-based model of nociception. Physiology and Behavior 2017; 174: 83-88
23 Greenfield jr. LJ. Molecular mechanisms of antiseizure drug activity at GAGA_A receptors. Seizure 2013; 22: 589-600
24 Betts T. Use of aromatherapy (with or without hypnosis) in the treatment of intractable epilepsy a two year follow up study. Seizure 2003; 12: 534-538
25 Hossain SJ, Aoshima H, Koda H, Kiso Y. Fragrances in oolong tea that enhance the response of GABA_A receptors. Biosci Biotechnol Biochem 2004; 68: 1842-1848
26 Bourin M, Hascoet M. The mouse light-dark box test. Eur J Pharmacol 2003; 463: 55-65
27 Barcellos HHA. Efeitos neuroendócrinos e comportamentais do aripiprazol em zebrafish. [Dissertação: Mestrado em Farmacologia]. Santa Maria: Universidade Federal de Santa Maria; 2019
28 de Moura Fé TC. Cis-Jasmona: potencial fitofármaco para o tratamento da dermatite atópica em modelo animal. [Dissertação: Mestrado em Ciências Médica]. Fortaleza: Universidade de Fortaleza; 2019
29 Poluha RL, Grossmann E. Inflammatory mediators related to arthrogenic temporomandibular dysfunctions. Br J Pain 2018; 1: 60-65
30 Saito S, Tominaga M. Evolutionary tuning of TRPA1 and TRPV1 thermal and chemical sensitivity in vertebrates. Temperature 2017; 4: 141-152
31 Ho KW, Ward NJ, Calkins DL. TRPV1: a stress response protein in the central nervous system. Am J Neurodegener Dis 2012; 1: 1-14
32 Meents JE, Ciotu CI, Fischer MJM. TRPA1: a molecular view. J Neurophysiol 2019; 121: 427-443
33 Verleye M, Schlichter R, Gillardin JM. Interactions of etifoxine with the chloride channel coupled to the GABA_A receptor complex. Neuroreport 1999; 10: 3207-3210
34 Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwangs SW, Mcintyre P, Jegla T, Bevan S, Patapoutian A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 2003; 112: 819-829
35 Chung MK, Ro JY. Peripheral glutamate receptor and transient receptor potential channel mechanisms of craniofacial muscle pain. Molecular Pain 2020; 16: 1-10
36 Diogenes A, Akopian AN, Hargreaves KM. NGF up-regulates TRPA1: implications for orofacial pain. J Dent Res 2007; 86: 550-555
37 Hossain MZ, Bakri MM, Yahya F, Ando H, Unno S, Kitagawa J. The role of transient receptor potential (TRP) channels in the transduction of dental pain. International Journal of Molecular Sciences 2019; 20: 526-556
38 Polat H, Erkoç FU, Viran R, Koçak O. Investigation of acute toxicity of beta-cypermethrin on guppies Poecilia reticulata. Chemosphere 2002; 49: 39-44
39 Arellano-Aguilar O, Solis-Angeles S, Serrano-Garcia L, Morales-Sierra E, Mendez-Serrano A, Monteo-Montoya R. Use of the zebrafish embryo toxicity test for risk assessment purpose: Case study. Fish Sci 2015; 9: 52-62
40 Ahmad F, Richardson MK. Exploratory behaviour in the open field test adapted for larval zebrafish: Impact of environmental complexity. Behav Processes 2013; 92: 88-98
41 Siebel AMD, Menezes FP, Schaefer IC, Petersen BD, Bonan DC. Rapamycin suppresses PTZ-induced seizures at different developmental stages of zebrafish. Pharmacol Biochem Behav 2015; 139: 163-168
42 Pineda R, Beattie CE, Hall CW. Recording the adult zebrafish cerebral field potential during pentylenetetrazole seizures. J Neurosci Methods 2011; 200: 20-28
43 Benneh CK, Biney RP, Mante PK, Tandoh A, Adongo DW, Wood E. Maerua angolensis stem bark extract reverses anxiety and related behaviours in zebrafish-Involvement of GABAergic and 5-HT systems. J Ethnopharmacol 2017; 207: 129-145
44 Sakurada T, Matsumura T, Moriyama T, Sakurada C, Ueno S, Sakurada S. Differential effects of intraplantar capsazepine and ruthenium red on capsaicin-induced desensitization in mice. Phamacol Biochem Behav 2003; 75: 115-121
45 McCurley AT, Callard GV. Characterization of housekeeping genes in zebrafish: Male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Molecular Biology 2008; 9: 102-113
46 Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C(T)] Method. Methods 2001; 25: 402-408
47 Macindoe G, Mavridis L, Venkatraman V, Devignes MD, Rritchie DW. HexServer: An FFT-based protein docking server powered by graphics processors. Nucleic Acids Research 2010; 38: 445-449