Antinociceptive compounds and LC-DAD-ESIMSn profile from Dictyoloma vandellianum leaves

English version

Autoři: Lucas Silva Abreu ^aff001; Iura Muniz Alves ^aff003; Renan Fernandes do Espírito Santo ^aff002; Yuri Mangueira do Nascimento ^aff001; César Augusto Gonçalves Dantas ^aff001; Gisele Graça Leite dos Santos ^aff004; Mireille Le Hyaric ^aff005; Maria Lenise Silva Guedes ^aff006; Marcelo Sobral da Silva ^aff001; Cristiane Flora Villarreal ^aff002; Eudes da Silva Velozo ^aff002; Josean Fechine Tavares ^aff001
Působiště autorů: Programa de Pós-Graduação em Produtos Naturais e Sintéticos Bioativos, Universidade Federal da Paraíba, João Pessoa, Brazil ^aff001; Faculdade de Farmácia, Universidade Federal da Bahia, Salvador, Brazil ^aff002; Instituto de Química, Universidade Federal da Bahia, Salvador, Brazil ^aff003; Instituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, Brazil ^aff004; Departamento de Química, Universidade Federal de Juiz de Fora, Juiz de Fora, Brazil ^aff005; Instituto de Biologia, Universidade Federal da Bahia, Salvador, Brazil ^aff006
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224575

Souhrn

Limonoids, quinolone alkaloids and chromones have been reported as constituents of Dictyoloma vandellianum Adr. Juss. (Rutaceae). Although those compounds are known for their biological activities, only the anti-inflammatory activity of chromones isolated from the underground parts has been evaluated. There are no studies of the pharmacological properties of the aerial parts of D. vandellianum. The present study was carried out to determine the phytochemical profile and antinociceptive activity of the methanol extract, fractions and isolated compounds of leaves of D. vandellianum. The phytochemical profile was performed by HLPC-DAD-ESIMSⁿ and pure substances obtained were characterized by MS and NMR spectroscopy. The antinociceptive activity was assessed using the formalin assay in mice, and the motor function in the rotarod test. ME and all the fractions obtained from ME produced antinociceptive effects. Among them, the ethyl ether fraction was the most active. Data from HPLC-DAD-ESIMSⁿ showed that the ethyl ether fraction presented 42 compounds. The major compounds isolated from this fraction—gallic acid, methyl gallate and 1,2,6-tri-O-galloyl-β-d-glucopyranose–were tested and produced antinociceptive effects. Gallic acid, methyl gallate and 1,2,6-tri-O-galloyl-β-d-glucopyranose at antinociceptive doses did not affect the motor performance in mice in the rotarod test. This work is the first report of the occurrence of gallotanins in D. vandellianum. In addition, the pharmacological study showed that D. vandellianum leaves present antinociceptive activity, probably induced by gallic acid, methyl gallate and 1,2,6-tri-O-galloyl-β-d-glucopyranose.

Klíčová slova:

Inflammation – Leaves – Analgesics – Ethers – Intraperitoneal injections – Phytochemicals – Phase determination – Nociception

Zdroje

1. Sarmento-Neto JF, do Nascimento LG, Felipe CF, de Sousa DP. Analgesic Potential of Essential Oils. Molecules. 2015; 21: 20.

2. Li JX. Combining opioids and non-opioids for pain management: Current status. Neuropharmacology. 2019; https://doi.org/10.1016/j.neuropharm.2019.04.025.

3. Turk DC, Wilson HD, Cahana A. Treatment of chronic non-cancer pain. Lancet. 2011; 377: 2226–2235. doi: 10.1016/S0140-6736(11)60402-9 21704872

4. Calixto JB, Beirith A, Ferreira J, Santos AR, Filho VC, Yunes RA. Naturally occurring antinociceptive substances from plants. Phytother. Res. 2000; 6: 401–418.

5. Sen S, Chakraborty R, De B, Ganesh T, Raghavendra HG, Debnath S. Analgesic and anti-inflammatory herbs: A potential source of modern medicine. Int. J. Pharm. Sci. Res. 2010; 1: 32–44.

6. De Almeida Barros TA, De Freitas LAR, Filho JMB, Nunes XP, Giulietti AM, De Souza GE, et al. Antinociceptive and anti-inflammatory properties of 7-hydroxycoumarin in experimental animal models: Potential therapeutic for the control of inflammatory chronic pain. J. Pharm. Pharmacol. 2010; 62: 205–213. doi: 10.1211/jpp.62.02.0008 20487200

7. De Lima FO, Nonato FR, Couto RD, Barbosa Filho JM, Nunes XP, et al. Mechanisms involved in the antinociceptive effects of 7-hydroxycoumarin. J. Nat. Prod. 2011; 74: 596–602. doi: 10.1021/np100621c 21417376

8. Espírito-Santo RF, Meira CS, Costa RdS, Souza Filho OP, Evangelista AF, Trossini GHG, et al. The anti-inflammatory and immunomodulatory potential of braylin: Pharmacological properties and mechanisms by in silico, in vitro and in vivo approaches. PLoS ONE. 2017; 12(6): e0179174. https://doi.org/10.1371/journal.pone.0179174 28594906

9. Azevedo MI, Pereira AF, Nogueira RB, Rolim FE, Brito GAC, Wong DVT, et al. The antioxidant effects of the flavonoids rutin and quercetin inhibit oxaliplatin-induced chronic painful peripheral neuropathy. Mol. Pain. 2013; 9: 53–53. doi: 10.1186/1744-8069-9-53 24152430

10. Higgs J, Wasowski C, Loscalzo LM, Marder M. In vitro binding affinities of a series of flavonoids for μ-opioid receptors. Antinociceptive effect of the synthetic flavonoid 3,3-dibromoflavanone in mice. Neuropharmacology. 2013; 72: 9–19. doi: 10.1016/j.neuropharm.2013.04.020 23624290

11. De Queiroz AC, Alves HDS, Cavalcante-Silva LHA, Dias TDLMF, Santos MDS, Melo GMDA, et al. Antinociceptive and anti-inflammatory effects of flavonoids PMT1 and PMT2 isolated from Piper montealegreanum Yuncker (Piperaceae) in mice. Nat. Prod. Res. 2014; 28: 403–406. doi: 10.1080/14786419.2013.867444 24479832

12. Waterman PG. Alkaloids of the rutaceae: Their distribution and systematic significance. Biochem. Syst. Ecol. 1975; 3: 149–180.

13. Vieira PC, Lazaro AR, Fernandes JB, Da Silva MFDGF. Limonoids, alkaloids, and chromones from Dictyoloma vandellianum, and their chemosystematic significance. Quim. Nova. 1990; 13: 287–288.

14. Campos AM, Khac DD, Fetizon M. Chromones from Dictyoloma incanescens. Phytochemistry. 1987; 26: 2819–2823.

15. Vieira PC, Lazaro AR, Fernandes JB, Da Silva MFDGF. The chemosystematics of Dictyoloma. Biochem. Syst. Ecol. 1988; 16: 541–544.

16. Sartor CFP, Da Silva MFDGF, Fernandes JB, Vieira PC, Fo ER, Garcia Cortez DA. Alkaloids from Dictyoloma vandellianum: Their chemosystematic significance. Phytochemistry. 2003; 63: 185–192. doi: 10.1016/s0031-9422(03)00006-2 12711140

17. Alves IM, Abreu LS, Costa CO, Le Hyaric M, Guedes ML, Soares MB, et al. Pyranochromones from Dictyoloma vandellianum A. Juss and Their Cytotoxic Evaluation. Chem. Biodiversity. 2017; 14: e1600276.

18. Lavaud C, Massiot G, Vasquez C, Moretti C, Sauvain M, Balderrama L. 4-Quinolinone alkaloids from Dictyoloma peruviana. Phytochemistry. 1995; 40: 317–320. doi: 10.1016/0031-9422(95)00265-9 7546553

19. Michael JP. Quinoline, quinazoline and acridone alkaloids. Nat. Prod. Rep. 1997; 14: 11–20. 9121729

20. Roy A, Saraf S. Limonoids: Overview of significant bioactive triterpenes distributed in plants kingdom. Biol. Pharm. Bull. 2006; 29: 191–201. doi: 10.1248/bpb.29.191 16462017

21. Heeb S, Fletcher MP, Chhabra SR, Diggle SP, Williams P, Cámara M. Quinolones: From antibiotics to autoinducers. Fems. Microbiol. Rev. 2011; 35: 247–274. doi: 10.1111/j.1574-6976.2010.00247.x 20738404

22. Sharma S, Kumar S, Chand K, Kathuria A, Gupta A. An update on natural occurrence and biological activity of chromones. Curr. Med. Chem. 2011; 18: 3825–3852. doi: 10.2174/092986711803414359 21824102

23. Opretzka LCF, Espírito-Santo RF, Nascimento OA, Abreu LS, Alves IM, Döring E, et al. Natural chromones as potential anti-inflammatory agents: Pharmacological properties and related mechanisms. Int. Immunopharm. 2019; 72: 31–39.

24. Dubuisson D, Dennis SG. The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain. 1977; 4: 161–174. doi: 10.1016/0304-3959(77)90130-0 564014

25. Tjolsen A, Berge OG, Hunskaar S, Rosland JH, Hole K. The formalin test: an evaluation of the method. Pain. 1992; 51: 5–17. doi: 10.1016/0304-3959(92)90003-t 1454405

26. Hunskaar S, Hole K. The formalin test in mice: Dissociation between inflammatory and non-inflammatory pain. Pain. 1987; 30: 103–114. doi: 10.1016/0304-3959(87)90088-1 3614974

27. Shibata M, Ohkubo T, Takahashi H, Inoki R. Modified formalin test: Characteristic biphasic pain response. Pain. 1989; 38: 347–352. doi: 10.1016/0304-3959(89)90222-4 2478947

28. Metzker De Oliveira C, Nonato FR, Oliveira De Lima F, Couto RD, David JP, David JM, et al. Antinociceptive properties of bergenin. J. Nat. Prod. 2011; 74: 2062–2068. doi: 10.1021/np200232s 21939182

29. Gama KB, Quintans JSS, Antoniolli AR, Quintans L.J Jr, Santana WA, Branco A, et al. Evidence for the involvement of descending pain-inhibitory mechanisms in the antinociceptive effect of hecogenin acetate. J. Nat. Prod. 2013; 76: 559–563. doi: 10.1021/np3007342 23437926

30. Abu-Reidah IM, Ali-Shtayeh MS, Jamous RM, Arráez-Román D, Segura-carretero A. HPLC–DAD–ESI-MS/MS screening of bioactive components from Rhus coriaria L.(Sumac) fruits. Food Chem. 2015; 166: 179–191. doi: 10.1016/j.foodchem.2014.06.011 25053044

31. Yang B, Kortesniemi M, Liu P, Karonen M, Salminen JP. Analysis of hydrolyzable tannins and other phenolic compounds in emblic leafflower (Phyllanthus emblica L.) fruits by high performance liquid chromatography–electrospray ionization mass spectrometry. J. Agr. Food Chem. 2012; 60: 8672–8683.

32. Clifford MN, Stoupi S, Kuhnert N. Profiling and characterization by LC-MS n of the galloylquinic acids of green tea. tara tannin. and tannic acid. J. Agr. Food Chem. 2007; 5: 2797–2807.

33. Chen H, Li M, Zhang C, Du W, Shao H, Feng Y, et al. Isolation and Identification of the Anti-Oxidant Constituents from Loropetalum chinense (R. Brown) Oliv. Based on UHPLC⁻Q-TOF-MS/MS. Molecules. 2018; 23: 1720.

34. Lin YL, Kuo YH, Shiao MS, Chen CC, Ou JC. Flavonoid glycosides from Terminalia catappa L. J. Chinese Chem. Soci. 2000; 47: 253–256.

35. Fraige K, Dametto AC, Zeraik ML, de Freitas L, Saraiva AC, Medeiros AI, et al. Dereplication by HPLC-DAD-ESI-MS/MS and Screening for Biological Activities of Byrsonima Species (Malpighiaceae). Phytochem. Anal. 2018; 29:196–204. doi: 10.1002/pca.2734 28990237

36. Lee JH, Johnson JV, Talcott ST. Identification of ellagic acid conjugates and other polyphenolics in muscadine grapes by HPLC-ESI-MS. J. Agr. Food Chem. 2005; 53: 6003–6010.

37. Chen G, Li X, Saleri F, Guo M. Analysis of flavonoids in rhamnus davurica and its antiproliferative activities. Molecules. 2016; 21: 1275.

38. Nawwar MAM, Hussein SAM. NMR spectra analysis of polyphenols from Punica granatum. Phytochem. 1994; 36: 793–798.

39. De Bruyn A, Anteunis M, Van Beeumen J. Chemical shifts of aldohexopyranoses revisited and application to gulosylglucose. Bull. Soc. Chim. Belg. 1977; 86: 259–265.

40. Bag A, Bhattacharyya SK, Chattopadhyay RR. Isolation and identification of a gallotannin 1,2,6-tri-O-galloyl-β-d-glucopyranose from hydroalcoholic extract of Terminalia chebula fruits effective against multidrug-resistant uropathogens. J. Appl. Microbiol. 2013; 115: 390–397. doi: 10.1111/jam.12256 23683054

41. Chanwitheesuk A, Teerawutgulrag A, Kilburn JD, Rakariyatham N. Antimicrobial gallic acid from Caesalpinia mimosoides Lamk. Food Chem. 2006; 100: 1044–1048.

42. Wang CR, Zhou R, Ng TB, Wong JH, Qiao WT, Liu F. First report on isolation of methyl gallate with antioxidant, anti-HIV-1 and HIV-1 enzyme inhibitory activities from a mushroom (Pholiota adiposa). Environ. Toxicol. Pharmacol. 2014; 37: 626–637. doi: 10.1016/j.etap.2014.01.023 24572641

43. Le BD, Gozariu M, Cadden SW. Animal models of nociception. Pharmacol. Rev. 2001; 53: 597–652. 11734620

44. Trevisan G, Rossato MF, Tonello R, Hoffmeister C, Klafke JZ, Rosa F, et al. Gallic acid functions as a TRPA1 antagonist with relevant antinociceptive and antiedematogenic effects in mice. Naunyn-Schmiedeberg’s Arch Pharmacol. 2014; 387: 679–689.

45. Kroes BH, Van Den Berg AJJ, Quarles Van Ufford HC, Van Dijk H, Labadie RP. Anti-inflammatory activity of gallic acid. Planta. Med. 1992; 58: 499–504. doi: 10.1055/s-2006-961535 1336604

46. Deng H, Fang Y. Anti-inflammatory gallic acid and wedelolactone are G protein-coupled receptor-35 agonists. Pharmacology. 2012; 89: 211–219. doi: 10.1159/000337184 22488351

47. Hsiang CY, Hseu YC, Chang YC, Kumar KJS, Ho TY, Yang HL. Toona sinensis and its major bioactive compound gallic acid inhibit LPS-induced inflammation in nuclear factor-κB transgenic mice as evaluated by in vivo bioluminescence imaging. Food Chem. 2013; 136: 426–434. doi: 10.1016/j.foodchem.2012.08.009 23122080

48. Kim SJ, Jin M, Lee E, Moon TC, Quan Z, Yang JH, et al. Effects of methyl gallate on arachidonic acid metabolizing enzymes: Cyclooxygenase-2 and 5-lipoxygenase in mouse bone marrow-derived mast cells. Arch Pharmacal. Res. 2006; 29: 874–878.

49. Correa LB, Pádua TA, Seito LN, Costa TE, Silva MA, Candéa AL, et al. Anti-inflammatory effect of methyl gallate on experimental arthritis: Inhibition of neutrophil recruitment, Production of inflammatory mediators, and activation of macrophages. J. Nat. Prod. 2016; 79: 1554–1566. doi: 10.1021/acs.jnatprod.5b01115 27227459

50. Santos AR, De Campos RO, Miguel OG, Cechinel-FilhO V, Yunes RA, Calixto JB. The involvement of K+ channels and Gi/o protein in the antinociceptive action of the gallic acid ethyl ester. Eur. J. Pharmacol. 1999; 379: 7–17. doi: 10.1016/s0014-2999(99)00490-2 10499367

51. Duan D, Li Z, Luo H, Zhang W, Chen L, Xu X. Antiviral compounds from traditional Chinese medicines Galla Chinese as inhibitors of HCV NS3 protease. Bioorg. Med. Chem. Lett. 2004; 14: 6041–6044. doi: 10.1016/j.bmcl.2004.09.067 15546725

52. Bag A, Chattopadhyay RR. Efflux pump inhibitory activity of a gallotannin from Terminalia chebula fruit against multidrug-resistant uropathogenic Escherichia coli. Nat. Pro. Res. 2014; 28: 1280–1283.

53. Bag A, Chattopadhyay RR. Synergistic antibiofilm efficacy of a gallotannin 1,2,6-tri-O-galloyl-β-d-glucopyranose from Terminalia chebula fruit in combination with gentamicin and trimethoprim against multidrug resistant uropathogenic Escherichia coli biofilms. PLoS ONE 2017; 12: e0178712. doi: 10.1371/journal.pone.0178712 28562631

54. Gatis-Carrazzoni ASSG, Mota FVB, Leite TCC. Anti-inflammatory and antinociceptive activities of the leaf methanol extract of Miconia minutiflora (Bonpl.) DC. and characterization of compounds by UPLC-DAD-QTOF-MS/MS. Naunyn-Schmiedeberg’s Arch Pharmacol. 2019; 392: 55–68.

55. Erdelyi K, Kiss A, Bakondi E, Bai P, Szabo C, Gergely P, et al. Gallotannin inhibits the expression of chemokines and inflammatory cytokines in A549 cells. Mol. Pharmacol. 2005; 68: 895–904. doi: 10.1124/mol.105.012518 15976037

56. Wagner H, Ulrich-Merzenich G. Synergy research: Approaching a new generation of phytopharmaceuticals. Phytomed. 2009; 16: 97–110.

57. Filho AW, Filho VC, Olinger L, De Souza MM. Quercetin: Further investigation of its antinociceptive properties and mechanisms of action. Arch. Pharm. Res. 2008; 31: 713–721. doi: 10.1007/s12272-001-1217-2 18563352

58. Maleki-Dizaji N, Fathiazad F, Garjani A. Antinociceptive properties of extracts and two flavonoids isolated from leaves of Danae racemosa. Arch. Pharmacal. Res. 2007; 30: 1536–1542.

59. Javadi F, Ahmadzadeh A, Eghtesadi S, Aryaeian N, Zabihiyeganeh M, Rahimi Foroushani A, Jazayeri S. The Effect of Quercetin on Inflammatory Factors and Clinical Symptoms in Women with Rheumatoid Arthritis: A Double-Blind, Randomized Controlled Trial. J Am Coll Nutr. 2017; 36: 9–15. doi: 10.1080/07315724.2016.1140093 27710596

60. Abu-Salem OM. Kaempferol attenuates the development of diabetic neuropathic pain in mice: possible anti-inflammatory and anti-oxidantmechanisms. Maced J. Med. 2014; 7(3): 424–430.

61. De Melo GO, Malvar DC, Vanderlinde FA, Rocha FF, Pires PA, Costa EA, et al. Antinociceptive and anti-inflammatory kaempferol glycosides from Sedum dendroideum. J. Ethnopharmacol. 2009; 124: 228–232. doi: 10.1016/j.jep.2009.04.024 19397977

Antinociceptive compounds and LC-DAD-ESIMSn profile from Dictyoloma vandellianum leaves

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