Download PDF
Planta Med 2016; 82(16): 1395-1402
DOI: 10.1055/s-0042-105878
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Tabebuia roseoalba: In Vivo Hypouricemic and Anti-inflammatory Effects of Its Ethanolic Extract and Constituents

Zilma Schimith Ferraz-Filha
2   Departamento de Química, Instituto Federal de Minas Gerais-Campus Ouro Preto, Ouro Preto, Minas Gerais, Brazil
,
Marcela Carolina de Paula Michel Araújo
1   Laboratório de Plantas Medicinais, Escola de Farmácia, Universidade Federal de Ouro Preto, Ouro Preto, Minas Gerais, Brazil
,
Fernanda Cristina Ferrari
1   Laboratório de Plantas Medicinais, Escola de Farmácia, Universidade Federal de Ouro Preto, Ouro Preto, Minas Gerais, Brazil
,
Iális Paiva Andrade Rodrigues Dutra
1   Laboratório de Plantas Medicinais, Escola de Farmácia, Universidade Federal de Ouro Preto, Ouro Preto, Minas Gerais, Brazil
,
Dênia Antunes Saúde-Guimarães
1   Laboratório de Plantas Medicinais, Escola de Farmácia, Universidade Federal de Ouro Preto, Ouro Preto, Minas Gerais, Brazil
› Author Affiliations
Further Information

Publication History

received 16 October 2015
revised 21 March 2016

accepted 22 March 2016

Publication Date:
09 May 2016 (online)

    Permissions and Reprints

Abstract

Tabebuia species have several uses in folk medicine, including their use to treat inflammation and rheumatism. The aim of this study was to investigate whether the ethanolic extract of leaves from Tabebuia roseoalba and isolated compounds could be useful to decrease serum uric acid levels and restrain the gout inflammatory process. The compounds α-amyrin, β-amyrin, sitosterol, and stigmasterol were isolated from the ethanolic extract. Rutin and caffeic acid were identified in the ethanolic extract by HPLC analysis. The anti-hyperuricemic effect, liver xanthine oxidoreductase inhibition, and anti-inflammatory activity of the ethanolic extract and isolated compounds were evaluated on hyperuricemic mice and on paw edema induced by monosodium urate crystals in mice. The ethanolic extract of leaves from T. roseoalba, β-amyrin, and stigmasterol were able to reduce serum uric acid levels in hyperuricemic mice through inhibition of liver xanthine oxidase activity and significantly decreased the paw edema induced by monosodium urate crystals. The antioxidant activity of the ethanolic extract and its ability to inhibit xanthine oxidase were also evaluated in vitro. The ethanolic extract of leaves from T. roseoalba showed significant antioxidant activity in the three evaluated assays. Results were analyzed using GraphPad Prism 5.01. One-way ANOVA followed by Studentʼs Newman-Keulʼs test was used to determine the significant differences between groups. The results show that the ethanolic extract of leaves from T. roseoalba, β-amyrin, and stigmasterol can be promising agents for the treatment for gouty arthritis, hyperuricemia, and inflammation. Stigmasterol, β-amyrin, and rutin contribute to the observed effects of the ethanolic extract of leaves from T. roseoalba.

Key words

Tabebuia roseoalba - Bignoniaceae - gout - inflammation - hyperuricemia - antioxidant
 

  • References

  • 1 Bhansing KJ, van Bon LV, Janssen M, Radstake TRDJ. Gout: a clinical syndrome illustrated and discussed. Neth J Med 2010; 68: 352-359
    PubMedGoogle Scholar
  • 2 Sabina EP, Nagar S, Rasool M. A role of piperine on monosodium urate crystal-induced inflammation-an experimental model of gouty arthritis. Inflammation 2011; 34: 184-192
    CrossrefPubMedGoogle Scholar
  • 3 Haidari F, Rashidi MR, Keshavarz SA, Mahboob SA, Eshraghian MR, Shahi MM. Effects of onion on serum uric acid levels and hepatic xanthine dehydrogenase/xanthine oxidase activities in hyperuricemic rats. Pak J Biol Sci 2008; 11: 1779-1784
    CrossrefPubMedGoogle Scholar
  • 4 Xu Z, Zhou J, Cai J, Zhu Z, Sun X, Chunlei J. Anti-inflammation effects of hydrogen saline in LPS activated macrophages and carrageenan induced paw oedema. J Inflamm (Lond) 2012; 9: 2
    CrossrefPubMedGoogle Scholar
  • 5 Liu X, Chen R, Shang Y, Jiao B, Huang C. Lithospermic acid as a novel xanthine oxidase inhibitor has anti-inflammatory and hypouricemic effects in rats. Chem Biol Interact 2008; 176: 137-142
    CrossrefPubMedGoogle Scholar
  • 6 Grose SO, Olmstead RG. Taxonomic revisions in the polyphyletic genus Tabebuia s.l. (Bignoniaceae). Syst Bot 2007; 32: 660-670
    CrossrefPubMedGoogle Scholar
  • 7 Costa FN, Leitão GG. Evaluation of different solvent systems for the isolation of Sparattosperma leucanthum flavonoids by counter-current chromatography. J Chromatogr A 2011; 1218: 6200-6205
    CrossrefPubMedGoogle Scholar
  • 8 Ospina LAF, Guerrero JPC, Buendia YCO, Bolivar IBP, Castillo FD. [Antiinflammatory, antioxidant and antibacterial activity of two species of Tabebuia genus]. Rev Cubana Plant Med 2013; 18: 34-46
    PubMedGoogle Scholar
  • 9 Byeon SE, Chung JY, Lee YG, Kim BH, Kim KH, Cho JY. In vitro and in vivo anti-inflammatory effects of taheebo, a water extract from the inner bark of Tabebuia avellanedae . J Ethnopharmacol 2008; 119: 145-152
    CrossrefPubMedGoogle Scholar
  • 10 Budni P, Petronilho FC, Citadini-Zanete V, Marcondes C, Zoch AN, Reginatto FH, Dal-Pizzol F. [Preliminary studies of the antioxidant activity of adult and young leaf extract hydroethanolic of Tabebuia heptaphylla (Vell.) Toledo (ipê-roxo)]. Lat Am J Pharm 2007; 26: 394-398
    PubMedGoogle Scholar
  • 11 Hajdu Z, Hohmann J. An ethnopharmacological survey of the traditional medicine utilized in the community of Porvenir, Bajo Paragua Indian Reservation, Bolivia. J Ethnopharmacol 2012; 139: 838-857
    CrossrefPubMedGoogle Scholar
  • 12 Vera Saltos MB, Naranjo Puente BF, Milella L, De Tommasi N, Dal Piaz F, Braca A. Antioxidant and free radical scavenging activity of phenolics from Bidens humilis . Planta Med 2015; 81: 1056-1064
    Article in Thieme ConnectPubMedGoogle Scholar
  • 13 Duarte-Almeida JM, Santos RJ, Genovese MI, Lajolo FM. Avaliação da atividade antioxidante utilizando sistema β-caroteno/ácido linoléico e método de seqüestro de radicais DPPH. Ciênc Tecnol Aliment (Campinas) 2006; 26: 446-452
    CrossrefPubMedGoogle Scholar
  • 14 Rufino MSM, Alves RE, de Brito AVB, Marcini Filho J, Moreira AVB. Metodologia Científica: Determinação da atividade antioxidante total em frutas no sistema β-caroteno/ácido linoléico (Comunicado técnico 126). Fortaleza: Embrapa Agroindústria Tropical; 2006
    Google Scholar
  • 15 Rufino MSM, Alves RE, Brito ES, Morais SM, Sampaio CG, Jimenez-Perez J, Calixto-Satura FD. Metodologia científica: determinação da atividade antioxidante total em frutas pela captura do radical livre ABTS (Comunicado técnico 128). Fortaleza: Embrapa Agroindústria Tropical; 2007
    Google Scholar
  • 16 Panda S, Jafri M, Kar A, Meheta BK. Thyroid inhibitory, antiperoxidative and hypoglycemic effects of stigmasterol isolated from Butea monosperma . Fitoterapia 2009; 80: 123-126
    CrossrefPubMedGoogle Scholar
  • 17 Krishnan K, Mathew LE, Vijayalakshmi NR, Helen A. Anti-inflammatory potential of β-amyrin, a triterpenoid isolated from Costus igneus . Inflammopharmacology 2014; 22: 373-385
    CrossrefPubMedGoogle Scholar
  • 18 Singh D, Arya PV, Sharma A, Dobhal MP, Gupta RS. Modulatory potential of α-amyrin against hepatic oxidative stress through antioxidant status in wistar albino rats. J Ethnopharmacol 2015; 161: 186-193
    CrossrefPubMedGoogle Scholar
  • 19 Gulcin I. Antioxidant activity of caffeic acid (3, 4-dihydroxycinnamic acid). Toxicology 2006; 217: 213-220
    CrossrefPubMedGoogle Scholar
  • 20 Vivancos M, Moreno JJ. β-Sitosterol modulates antioxidant enzyme response in RAW 264.7 macrophages. Free Radic Biol Med 2005; 39: 91-97
    CrossrefPubMedGoogle Scholar
  • 21 Krishnan E. Interaction of inflammation, hyperuricemia, and the prevalence of hypertension among adults free of metabolic syndrome: NHANES 2009–2010. J Am Heart Assoc 2014; 3: e000157
    CrossrefPubMedGoogle Scholar
  • 22 Jiang Y, You XY, Fu KL, Yin WL. Effect of extract from Mangifera indica leaf on monossodium urate crystal-induced gouty arthritis in rats. J Evid Based Complementary Altern Med 2012; 2012: 967573
    PubMedGoogle Scholar
  • 23 Tausche AK, Richter K, Grässler A, Hänsel S, Roch B, Schröder HE. Severe gouty arthritis refractory to anti-inflammatory drugs: treatment with anti-tumour necrosis factor α as a new therapeutic option. Ann Rheum Dis 2004; 63: 1351-1352
    CrossrefPubMedGoogle Scholar
  • 24 Recio MC, Giner RM, Manez S, Rios JL. Structural requirements for the anti-inflammatory activity of natural triterpenoids. Planta Med 1995; 61: 182-185
    Article in Thieme ConnectPubMedGoogle Scholar
  • 25 Otuki MF, Vieira-Lima F, Malheiros A, Yunes RA, Calixto JB. Topical antiinflammatory effects of the ether extract from Protium kleinii and alpha-amyrin pentacyclic triterpene. Eur J Pharmacol 2005; 507: 253-259
    CrossrefPubMedGoogle Scholar
  • 26 Kweifio-Okai G, De Munk F, Rumble BA, Macrides TA, Cropley M. Antiarthritic mechanisms of amyrin triterpenes. Res Commun Mol Pathol Pharmacol 1994; 85: 45-55
    PubMedGoogle Scholar
  • 27 Kathryn AB, Silva S, Paszcuk AF, Passos GF, Silva ES, Bento AF, Meotti FC, Calixto JB. Activation of cannabinoid receptors by the pentacyclic triterpene α,β-amyrin inhibits inflammatory and neuropathic persistente pain in mice. Pain 2011; 152: 1872-1887
    CrossrefPubMedGoogle Scholar
  • 28 Gomez MA, Sáenz MT, Garcia MD, Fernández MA. Study of the topical anti-inflammatory activity of Achillea ageratum on chronic and acute inflammation models. Z Naturforsch C 1999; 54: 937-941
    PubMedGoogle Scholar
  • 29 Bouic PJ, Clark A, Lamprecht J, Freestone M, Pool EJ, Liebenberg RW, Kotze D, van Jaarsveld PP. The effects of β-sitosterol (BSS) and β-sitosterol glucoside (BSSG) mixture on selected immune parameters of marathon runners: inhibition of post marathon immune suppression and inflammation. Int J Sports Med 1999; 20: 258-262
    Article in Thieme ConnectPubMedGoogle Scholar
  • 30 De Souza MR, de Paula CA, Pereira de Resende ML, Grabe-Guimarães A, de Souza Filho JD, Saúde-Guimarães DA. Pharmacological basis for use of Lychnophora trichocarpha in gouty arthritis: anti-hyperuricemic and anti-inflammatory effects of its extract, fraction and constituents. J Ethnopharmacol 2012; 142: 845-850
    CrossrefPubMedGoogle Scholar
  • 31 Zhu JX, Wang Y, Kong LD, Yang C, Zhang X. Effects of Biota orientalis extract and its flavonoid constituents, quercetin and rutin on serum uric acid levels in oxonate-induced mice and xanthine dehydrogenase and xanthine oxidase activities in mouse liver. J Ethnopharmacol 2004; 93: 133-140
    CrossrefPubMedGoogle Scholar
  • 32 Umar S, Mishra NK, Pal K, Sajad M, Neha AMM, Ahmad S, Katiyar CK, Khan HA. Protective effect of rutin in attenuation of collagen-induced arthritis in Wistar rat by inhibiting inflammation and oxidative stress. Indian J Rheumatol 2012; 7: 191-198
    CrossrefPubMedGoogle Scholar
  • 33 Khan AQ, Khan R, Qamar W, Lateef A, Ali F, Tahir M, Muneeb UR, Sultana S. Caffeic acid attenuates 12-O-tetradecanoyl-phorbol-13-acetate (TPA)-induced NF-κB and COX-2 expression in mouse skin: abrogation of oxidative stress, inflammatory responses and proinflammatory cytokine production. Food Chem Toxicol 2012; 50: 175-183
    CrossrefPubMedGoogle Scholar
  • 34 Chen L, Yin H, Lan Z, Ma S, Zhang C, Yang Z, Li P, Lin B. Anti-hyperuricemic and nephroprotective effects of Smilax china L. J Ethnopharmacol 2011; 135: 399-405
    CrossrefPubMedGoogle Scholar
  • 35 Jaiswal R, Karaköse H, Rühmann S, Goldner K, Neumüller M, Treutter D, Kuhnert N. Identification of phenolic compounds in plum fruits (Prunus salicina L. and Prunus domestica L.) by high-performance liquid chromatography/tandem mass spectrometry and characterization of varieties by quantitative phenolic fingerprints. J Agric Food Chem 2013; 61: 12020-12031
    CrossrefPubMedGoogle Scholar
  • 36 Santos CA. Estudo químico de Jacaranda macrantha Cham. e síntese de piranonaftoquinonas hidroxiladas no anel benzóide [dissertation]. Belo Horizonte: Universidade Federal de Minas Gerais; 1999
    PubMedGoogle Scholar
  • 37 Chaves MH, Lopes Citó AMG, Dantas Lopes JA, da Costa DA, de Oliveira CAA, Costa AF, Brito Júnior FEM. Fenóis totais, atividade antioxidante e constituintes químicos de extratos de Anacardium occidentale L., Anacardiaceae. Rev Bras Pharmacogn 2010; 20: 106-112
    CrossrefPubMedGoogle Scholar
  • 38 Gallegos Olea RS, Roque NF. Análise de misturas de triterpenos por RMN de 13C. Quim Nova 1990; 13: 278-281
    PubMedGoogle Scholar
  • 39 Campanini MZ, Custódio DL, Ivan ALM, Martins SM, Paranzini MJR, Martinez RM, Verri jr. WA, Vicentini FTMC, Arakawa NS, Faria TJ, Baracat MM, Casagrande R, Georgetti SR. Topical formulations containing Pimenta pseudocaryophyllus extract: in vitro antioxidant activity and in vivo efficacy against UV-B-induced oxidative stress. AAPS PharmSciTech 2014; 15: 86-95
    CrossrefPubMedGoogle Scholar
  • 40 Singh RP, Murthy KNC, Jayaprakasha GK. Studies on the antioxidant activity of Pormegranate (Punica granatum) peel and seed extracts using in vitro models. J Agric Food Chem 2002; 50: 81-86
    CrossrefPubMedGoogle Scholar
  • 41 Ferraz-Filha ZS, Vitolo IF, Fietto LG, Lombardi JA, Saúde Guimarães DA. Xanthine oxidase inhibitory activity of Lychnophora species from Brazil (“Arnica”). J Ethnopharmacol 2006; 107: 79-82
    CrossrefPubMedGoogle Scholar
  • 42 Lima RCL, Ferrari FC, Souza MR, Pereira BMS, Paula CA, Saúde-Guimarães DA. Effects of extracts of leaves from Sparattosperma leucanthum on hyperuricemia and gouty arthritis. J Ethnopharmcol 2015; 161: 194-199
    CrossrefPubMedGoogle Scholar