Download PDF
Planta Med 2016; 82(05): 407-413
DOI: 10.1055/s-0035-1568200
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Effect of the Hydroethanolic Extract from Echinodorus grandiflorus Leaves and a Fraction Enriched in Flavone-C-Glycosides on Antigen-Induced Arthritis in Mice

Eliana de Faria Garcia
1   Department of Pharmaceutical Products, Faculty of Pharmacy, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
,
Mariana Assíria de Oliveira
1   Department of Pharmaceutical Products, Faculty of Pharmacy, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
,
Luiza C. M. Candido
2   Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
,
Fernanda M. Coelho
2   Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
,
Vivian Vasconcelos Costa
2   Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
3   Department of Microbiology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
,
Celso Martins Queiroz-Junior
2   Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
4   Department of Oral Pathology, Faculty of Odontology, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
,
Daiane Boff
2   Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
,
Flávio Almeida Amaral
2   Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
,
Danielle da Glória de Souza
3   Department of Microbiology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
,
Mauro Martins Teixeira
2   Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
,
Fernão Castro Braga
1   Department of Pharmaceutical Products, Faculty of Pharmacy, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
› Author Affiliations
Further Information

Publication History

received 09 January 2015
revised 04 November 2015

accepted 09 November 2015

Publication Date:
29 January 2016 (online)

    Permissions and Reprints

Abstract

The leaves of Echinodorus grandiflorus are traditionally used in Brazil to treat several inflammatory conditions, including arthritis. This study aimed to investigate the antiarthritis activity of the 70 % ethanol extract of E. grandiflorus leaves and a standardized flavonoid-rich fraction in an antigen-induced arthritis model in mice. Previously immunized mice were treated per os with saline (control group), 70 % ethanol extract (100–1000 mg/kg), or a flavonoid-rich fraction (0.7–7.2 mg/kg) 40 minutes before and 3 and 6 hours after the challenge with antigen into the knee joint. The administration of the 70 % ethanol extract and flavonoid-rich fraction to mice significantly reduced neutrophil recruitment to the joint cavity and in periarticular tissue. The levels of chemokine (C–X-C motif) ligand 1, tumor necrosis factor-α, and interleukin-1β quantified by the enzyme-linked immunosorbent assay (ELISA) in the periarticular tissue were also diminished in mice treated with the 70 % ethanol extract and flavonoid-rich fraction, as well as mechanical hypernociception. Histological analysis confirmed that both the 70 % ethanol extract and flavonoid-rich fraction suppressed joint inflammation and inhibited cartilage and bone destruction when compared to the control group. Our results demonstrate, for the first time, that E. grandiflorus has anti-inflammatory activity in an experimental arthritis model and highlights the role of flavonoids in the observed response.

Key words

Echinodorus grandifloras - Alismataceae - antigen-induced arthritis model - standardized fraction - flavonoids
 

  • References

  • 1 McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011; 365: 2205-2219
    CrossrefPubMedGoogle Scholar
  • 2 Venkatesha SH, Berman BM, Moudgil KD. Herbal medicine products target defined biochemical and molecular mediators of inflammatory autoimmune arthritis. Bioorg Med Chem 2011; 19: 21-29
    CrossrefPubMedGoogle Scholar
  • 3 Cameron M, Gagnier JJ, Little CV, Parsons TJ, Blümle A, Chrubasik S. Evidence of effectiveness of herbal medicinal products in the treatment of arthritis. Phytother Res 2009; 23: 1647-1662
    CrossrefPubMedGoogle Scholar
  • 4 Soeken KL, Miller SA, Ernst E. Herbal medicines for the treatment of rheumatoid arthritis: a systematic review. Rheumatology 2003; 42: 652-659
    CrossrefPubMedGoogle Scholar
  • 5 Lorenzi H, Matos FJA. Plantas Medicinais no Brasil: nativas e exóticas cultivadas. São Paulo: Instituto Plantarum; 2002: 39-40
    Google Scholar
  • 6 Dutra RC, Tavares CZ, Ferraz SO, Sousa OV, Pimenta DS. Investigação das atividades analgésica e anti-inflamatória do extrato metanólico dos rizomas de Echinodorus grandiflorus . Rev Bras Farmacogn 2006; 16: 469-474
    CrossrefPubMedGoogle Scholar
  • 7 Pimenta DS. Ecologia, cultivo e validação do uso de Echinodorus grandiflorus (Cham. & Schltdl.) Micheli (chapeú de couro) [PhD thesis]. Rio de Janeiro: Fundação Oswaldo Cruz; 2002
    PubMedGoogle Scholar
  • 8 Garcia Ede F, de Oliveira MA, Godin AM, Ferreira WC, Bastos LF, Coelho Mde M, Braga FC. Antiedematogenic activity and phytochemical composition of preparations from Echinodorus grandiflorus leaves. Phytomedicine 2010; 18: 80-86
    CrossrefPubMedGoogle Scholar
  • 9 Schnitzler M, Petereit F, Nahrstedt A. Trans-aconitic acid, glucosylflavones and hydroxycinnamoyltartaric acids from the leaves of Echinodorus grandiflorus ssp. aureus, a Brazilian medicinal plant. Rev Bras Farmacogn 2007; 17: 149-154
    CrossrefPubMedGoogle Scholar
  • 10 Costa M, Tanaka CMA, Imamura PM, Marsaioli AJ. Isolation and synthesis of a new clerodane from Echinodorus grandiflorus . Phytochemistry 1999; 50: 117-122
    CrossrefPubMedGoogle Scholar
  • 11 Firestein GS. Evolving concepts of rheumatoid arthritis. Nature 2003; 423: 356-361
    CrossrefPubMedGoogle Scholar
  • 12 Németh T, Mócsai A. The role of neutrophils in autoimmune diseases. Immunol Lett 2012; 143: 9-19
    CrossrefPubMedGoogle Scholar
  • 13 Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 2013; 13: 159-175
    CrossrefPubMedGoogle Scholar
  • 14 Cuzzocrea S, Ayroldi E, Di Paola R, Agostini M, Mazzon E, Bruscoli S, Genovese T, Ronchetti S, Caputi AP, Riccardi C. Role of glucocorticoid-induced TNF receptor family gene (GITR) in collagen-induced arthritis. FASEB J 2005; 19: 1253-1265
    CrossrefPubMedGoogle Scholar
  • 15 Cascão R, Rosário HS, Souto-Carneiro MM, Fonseca JE. Neutrophils in rheumatoid arthritis: More than simple final effectors. Autoimmun Rev 2010; 9: 531-535
    CrossrefPubMedGoogle Scholar
  • 16 Sachs D, Coelho FM, Costa VV, Lopes F, Pinho V, Amaral FA, Silva TA, Teixeira AL, Souza DG, Teixeira MM. Cooperative role of tumour necrosis factor-α, interleukin-1β and neutrophils in a novel behavioural model that concomitantly demonstrates articular inflammation and hypernociception in mice. Br J Pharmacol 2011; 162: 72-83
    CrossrefPubMedGoogle Scholar
  • 17 Coelho FM, Pinho V, Amaral FA, Sachs D, Costa VV, Rodrigues DH, Vieira AT, Silva TA, Souza DG, Bertini R, Teixeira AL, Teixeira MM. The chemokine receptors CXCR1/CXCR2 modulate antigen-induced arthritis by regulating adhesion of neutrophils to the synovial microvasculature. Arthritis Rheum 2008; 58: 2329-2337
    CrossrefPubMedGoogle Scholar
  • 18 Amaral FA, Costa VV, Tavares LD, Sachs D, Coelho FM, Fagundes CT, Soriani FM, Silveira TN, Cunha LD, Zamboni DS, Quesniaux V, Peres RS, Cunha TM, Cunha FQ, Ryffel B, Souza DG, Teixeira MM. NLRP3 inflammasome-mediated neutrophil recruitment and hypernociception depend on leukotriene B(4) in a murine model of gout. Arthritis Rheum 2012; 64: 474-484
    CrossrefPubMedGoogle Scholar
  • 19 Lo HM, Lai TH, Li CH, Wu WB. TNFα-induces CXCL1 chemokine expression and release in human vascular endothelial cells in vitro via two distinct signaling pathways. Acta Pharmacol Sin 2014; 35: 339-350
    CrossrefPubMedGoogle Scholar
  • 20 Moss ML, Sklair-Tavron L, Nudelman R. Drug insight: tumor necrosis factor-converting enzyme as a pharmaceutical target for rheumatoid arthritis. Nat Clin Pract Rheumatol 2008; 4: 300-309
    PubMedGoogle Scholar
  • 21 Klareskog L, Catrina AI, Paget S. Rheumatoid arthritis. Lancet 2009; 373: 659-672
    CrossrefPubMedGoogle Scholar
  • 22 Scott DL, Wolfe F, Huizinga TWJ. Rheumatoid arthritis. Lancet 2010; 376: 1094-1108
    CrossrefPubMedGoogle Scholar
  • 23 Van den Berg WB. Arguments for interleukin 1 as a target in chronic arthritis. Ann Rheum Dis 2000; 59: i81-i84
    CrossrefPubMedGoogle Scholar
  • 24 Dayer JM, Bresnihan B. Targeting interleukin-1 in the treatment of rheumatoid arthritis. Arthritis Rheum 2002; 46: 574-578
    CrossrefPubMedGoogle Scholar
  • 25 Garcia EF, Oliveira MA, Dourado LPA, Souza DGS, Teixeira MM, Braga FC. In vitro TNF-α inhibition elicited by extracts from Echinodorus grandiflorus leaves and correlation with their phytochemical composition. Planta Med advance online publication 21.12.2015; DOI: 10.1055/s-0035-1558290.
    PubMedGoogle Scholar
  • 26 Zucolotto SM, Goulart S, Montanher AB, Reginatto FH, Schenkel EP, Fröde TS. Bioassay-guided isolation of anti-inflammatory C-glucosylflavones from Passiflora edulis . Planta Med 2009; 75: 1221-1226
    Article in Thieme ConnectPubMedGoogle Scholar
  • 27 Lin CM, Huang ST, Liang YC, Lin MS, Shih CM, Chang YC, Chen TY, Chen CT. Isovitexin suppresses lipopolysaccharide-mediated inducible nitric oxide synthase through inhibition of NF-kappa B in mouse macrophages. Planta Med 2005; 71: 748-753
    Article in Thieme ConnectPubMedGoogle Scholar
  • 28 Huang L, Ken N, Ye W. Pharmacological effect of the organic acid of Achillea alpina . Zhong Yao Tong Bao 1985; 10: 38-40
    PubMedGoogle Scholar
  • 29 Quintão NLM, Meyre-Silva C, Silva GF, Antonialli CS, Rocha LW, Lucinda-Silva RM, Malheiros A, Souza MM, Filho VC, Bresolin TMB. Aleurites moluccana (L.) Willd. leaves: mechanical antinociceptive properties of a standardized dried extract and its chemical markers. Evid Based Complement Alternat Med 2011; 2011: 179890
    PubMedGoogle Scholar
  • 30 Zhang L, Li J, Yu S, Jin Y, Lv X, Zou Y, Li Y. Therapeutic effects and mechanisms of total flavonoids of Turpinia arguta seen on adjuvant arthritis in rats. J Ethnopharmacol 2008; 116: 167-172
    CrossrefPubMedGoogle Scholar
  • 31 Larrosa M, Luceri C, Vivoli E, Pagliuca C, Lodovici M, Moneti G, Dolara P. Polyphenol metabolites from colonic microbiota exert anti-inflammatory activity on different inflammation models. Mol Nutr Food Res 2009; 53: 1044-1054
    CrossrefPubMedGoogle Scholar
  • 32 Erdemoglu N, Akkol EK, Yesilada E, Calis I. Bioassay-guided isolation of anti-inflammatory and antinociceptive principles from a folk remedy, Rhododendron ponticum L. leaves. J Ethnopharmacol 2008; 119: 172-178
    CrossrefPubMedGoogle Scholar
  • 33 Da Silva SL, Calgarotto AK, Maso V, Damico DC, Baldasso P, Veber CL, Villar JA, Oliveira AR, Comar jr. M, Oliveira KM, Marangoni S. Molecular modeling and inhibition of phospholipase A2 by polyhydroxy phenolic compounds. Eur J Med Chem 2009; 44: 312-321
    CrossrefPubMedGoogle Scholar
  • 34 Huang ST, Chen CT, Chieng KT, Huang SH, Chiang BH, Wang LF, Kuo HS, Lin CM. Inhibitory effects of a rice hull constituent on tumor necrosis factor alpha, prostaglandin E2, and cyclooxygenase-2 production in lipopolysaccharide-activated mouse macrophages. Ann N Y Acad Sci 2005; 1042: 387-395
    CrossrefPubMedGoogle Scholar
  • 35 Pellati F, Benvenuti S, Melegari M, Lasseigne T. Variability in the composition of anti-oxidant compounds in Echinacea species by HPLC. Phytochem Anal 2005; 16: 77-85
    CrossrefPubMedGoogle Scholar
  • 36 Kauss T, Moynet D, Rambert J, Al-Kharrat A, Brajot S, Thiolat D, Ennemany R, Fawaz F, Mossalayi MD. Rutoside decreases human macrophage-derived inflammatory mediators and improves clinical signs in adjuvant-induced arthritis. Arthritis Res Ther 2008; 10: R19
    CrossrefPubMedGoogle Scholar
  • 37 Li R, Cai L, Xie XF, Yang F, Li J. Hesperidin suppresses adjuvant arthritis in rats by inhibiting synoviocyte activity. Phytother Res 2010; 24: S71-S76
    CrossrefPubMedGoogle Scholar
  • 38 Jiang CP, He X, Yang XL, Zhang SL, Li H, Song ZJ, Zhang CF, Yang ZL, Li P, Wang CZ, Yuan CS. Anti-rheumatoid arthritic activity of flavonoids from Daphne genkwa . Phytomedicine 2014; 21: 830-837
    CrossrefPubMedGoogle Scholar
  • 39 Lee JD, Huh JE, Jeon G, Yang HR, Woo HS, Choi DY, Park DS. Flavonol-rich RVHxR from Rhus verniciflua Stokes and its major compound fisetin inhibits inflammation-related cytokines and angiogenic factor in rheumatoid arthritic fibroblast-like synovial cells and in vivo models. Int Immunopharmacol 2009; 9: 268-276
    CrossrefPubMedGoogle Scholar
  • 40 Jin JH, Kim JS, Kang SS, Son KH, Chang HW, Kim HP. Anti-inflammatory and anti-arthritic activity of total flavonoids of the roots of Sophora flavescens . J Ethnopharmacol 2010; 127: 589-595
    CrossrefPubMedGoogle Scholar
  • 41 Queiroz-Junior CM, Madeira MF, Coelho FM, Costa VV, Bessoni RL, Sousa LF, Garlet GP, Souza Dda G, Teixeira MM, Silva TA. Experimental arthritis triggers periodontal disease in mice: involvement of TNF-α and the oral microbiota. J Immunol 2011; 187: 3821-3830
    CrossrefPubMedGoogle Scholar