Bidens pilosa (Black Jack) Standardized Extract Ameliorates Acute TNBS-induced Intestinal Inflammation in Rats

 

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Abstract

Bidens pilosa is an herb popularly used to treat inflammation, hemorrhoids, fever, and gastric ulcers with reported pharmacological activities and chemical composition that sustain its selection as a potential intestinal anti-inflammatory product. Based on this, we examined the effects of a B. pilosa fatty acid-standardized supercritical preparation on the intestinal inflammatory process induced by trinitrobenzenesulphonic acid in rats, using either preventative or curative treatments. We also investigated the safety of plant extract by acute and sub-chronic toxicological analysis. The intestinal anti-inflammatory activity was related to modulation of the immune response, increasing IL-10 production and reducing IL-1β, IL-6, and TNF-α level, the oxidative stress, and the MUC production in the inflamed colon. Optic, scanning, and transmission electron microscopy (TEM) analysis supported the beneficial effects promoted by B. pilosa, which were closely related to downregulation of heparanase, Hsp70, Mapk 3, and NF-κB signaling and with the presence of long-chain fatty acids in extract. Our data suggest that B. pilosa supercritical preparation is a chemically standardized preparation potentially useful as complementary intestinal anti-inflammatory agent to treat inflammatory bowel disease.

• References

• 1 Ghosh S, Pariente B, Mould DR, Schreiber S, Peterson J, Hommes D. New tools and approaches for improved management of inflammatory bowel diseases. J Crohn Colitis 2014; 8: 1246-1253
  CrossrefPubMedGoogle Scholar
• 2 Aloi M, Nuti F, Stronati L, Cucchiara S. Advances in the medical management of paediatric IBD. Nat Rev Gastroenterol Hepatol 2014; 11: 99-108
  PubMedGoogle Scholar
• 3 Di Stasi LC, Costa CARA, Witaicenis A. Products for the treatment of inflammatory bowel disease: a patent review (2013–2014). Expert Opin Ther Pat 2015; 6: 629-642
  PubMedGoogle Scholar
• 4 Longuefosse JL, Nossin E. Medical ethnobotany survey in Martinique. J Ethnopharmacol 1996; 53: 117-142
  CrossrefPubMedGoogle Scholar
• 5 Di Stasi LC, Oliveira GP, Carvalhaes MA, Queiroz-Junior M, Tien OS, Kakinami SH, Reis MS. Medicinal plants popularly used in the Brazilian Tropical Atlantic Forest. Fitoterapia 2002; 73: 69-91
  CrossrefPubMedGoogle Scholar
• 6 Di Stasi LC, Hiruma CA, Guimarães EM, Santos CM. Medicinal plants popularly used in Brazilian Amazon. Fitoterapia 1994; 65: 529-540
  PubMedGoogle Scholar
• 7 Brasil, Ministerio da Saúde. Política e Programa Nacional de Plantas Medicinais e Fitoterápicos. 1st edition. Brasília: Ministério da Saúde/SCTIE/DAF; 2016
  Google Scholar
• 8 Brasil, Ministerio da Saúde. Relação Nacional de Plantas Medicinais de Interesse ao SUS. Espécies vegetais. 1st edition. Brasília: Ministério da Saúde/SCTIE/DAF; 2009: 1-2.. Available. at. http://portalarquivos2.saude.gov.br/images/pdf/2014/maio/07/renisus.pdf.. Accessed. January. 21. 2020
  Google Scholar
• 9 Pereira RLC, Ibrahim T, Lucchetti L, Silva AJR, Moraes VLG. Immunosuppressive and anti-inflammatory effects of methanolic extract and the polyacetylene isolated from Bidens pilosa L. Immunopharmacology 1999; 43: 31-37
  CrossrefPubMedGoogle Scholar
• 10 Chang CLT, Kuo HK, Chang SL, Chiang YM, Lee TH, Wu WM, Shyur LF, Yang WC. The distinct effects of a butanol fraction of Bidens pilosa plant extract on the development of Th1-mediated diabetes and Th2-mediated airway inflammation in mice. J Biomed Sci 2005; 12: 79-89
  CrossrefPubMedGoogle Scholar
• 11 Dieamant G, Pereda MDCV, Nogueira C, Eberlin S, Facchini G, Checon JT, Cesar CK, Mussi L, Polezel MA, Martins-Oliveira jr. D, Di Stasi LC. Antiaging mechanisms of a standardized supercritical CO₂ preparation of Black Jack (Bidens pilosa L.) in human fibroblasts and skin fragments. Evid Based Complement Alternat Med 2015; 2015: 1-15
  CrossrefPubMedGoogle Scholar
• 12 Calder PC. Omega-3 fatty acids and inflammatory processes: from molecules to man. Biochem Soc Transac 2017; 45: 1105-1115
  PubMedGoogle Scholar
• 13 Hassan A, Ibrahim A, Mbodji K, Coeffier M, Ziegler F, Bounore F, Chardigny JM, Skiba M, Savoye G, Déchelotte P, Marion-Letellier R. An α-linolenic acid-rich formula reduces oxidative stress and inflammation by regulating NF-κB in rats with TNBS-induced colitis. Biochem Mol Gen Mechan 2010; 140: 1714-1721
  PubMedGoogle Scholar
• 14 Reddy VK, Naidu KA. Oleic acid, hydroxytyrosol and n-3 fatty acids collectivelly modulate colitis through reduction of oxidative stress and IL-8 synthesis; in vitro and in vivo studies. Int Immunopharmacol 2016; 35: 29-42
  CrossrefPubMedGoogle Scholar
• 15 Lee J, Moraes-Vieira PM, Castoldi A, Aryal P, Yee EU, Vickers C, Parnas O, Donaldson CJ, Saghatelian A, Kahn BB. Branched fatty acid esters of hydroxyl fatty acids (FAHFAs) protect against colitis by regulating gut innate and adapatative immune response. J Biol Chem 2016; 291: 22207-22217
  CrossrefPubMedGoogle Scholar
• 16 Balmus IM, Ciobica A, Trifan A, Stanciu C. The implications of oxidative stress and antioxidant therapies in inflammatory bowel disease: clinical aspects and animal models. Saudi J Gastroenterol 2016; 22: 3-17
  CrossrefPubMedGoogle Scholar
• 17 Nagy P, Ashby MT. Kinetics and mechanism of the oxidation of the glutathione dimer by hypochlorous acid and catalytic reduction of the chloroamine product by glutathione reductase. Chem Res Toxicol 2007; 20: 79-87
  CrossrefPubMedGoogle Scholar
• 18 Chami B, Martin NJJ, Dennis JM, Witting PK. Myeloperoxidase in the inflamed colon: A novel target for treating inflammatory bowel disease. Arch Biochem Biophys 2018; 645: 61-71
  CrossrefPubMedGoogle Scholar
• 19 Masella R, Di Benedetto R, Varì R, Filesi C, Giovannini C. Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes. J Nutr Biochem 2005; 16: 577-586
  CrossrefPubMedGoogle Scholar
• 20 Sharma M, Kaur R, Kaushik K, Kaushal N. Redox modulatory protective effects of ω-3 fatty acids rich fish oil against experimental colitis. Toxicol Mech Methods 2019; 29: 244-254
  PubMedGoogle Scholar
• 21 Silva RO, Sousa FBM, Damasceno SRB, Carvalho NS, Silva VG, Oliveira FRMA, Sousa DP, Aragão KS, Barbosa ALR, Freitas RM, Medeiros JVR. Phytol, a diterpene alcohol, inhibits the inflammatory response by reducing cytokine production and oxidative stress. Fundam Clin Pharmacol 2014; 28: 455-464
  CrossrefPubMedGoogle Scholar
• 22 Műzes G, Molnár B, Tulassay Z, Sipos F. Changes of the cytokine profile in inflammatory bowel diseases. World J Gastroenterol 2012; 18: 5848-5861
  CrossrefPubMedGoogle Scholar
• 23 Hur SJ, Kang SH, Jung HS, Kim SC, Jeon HS, Kim IH, Lee JD. Review of natural products actions on cytokines in inflammatory bowel disease. Nutr Res 2012; 32: 801-816
  CrossrefPubMedGoogle Scholar
• 24 Quaglio AEV, Castilho ACS, Di Stasi LC. Experimental evidence of heparanase, Hsp70 and NF-κB gene expression on the response of anti-inflammatory drugs in TNBS-induced colonic inflammation. Life Sci 2015; 141: 179-187
  CrossrefPubMedGoogle Scholar
• 25 Marion-Letellier R, Savoye G, Ghosh S. Polyunsaturated fatty acids and inflammation. IUBMB Life 2015; 67: 659-667
  CrossrefPubMedGoogle Scholar
• 26 Reifen R, Karlinsky A, Stark AH, Berkovich Z, Nyska A. α-Linolenic acid (ALA) is an anti-inflammatory agent in inflammatory bowel disease. J Nutr Biochem 2015; 26: 1632-1640
  CrossrefPubMedGoogle Scholar
• 27 Camuesco D, Comalada M, Concha A, Nieto A, Sierra S, Xaus J, Zarzuelo A, Gálvez J. Intestinal anti-inflammatory activity of combined quercitrin and dietary olive oil supplemented with fish oil, rich in EPA and DHA (n-3) polyunsaturated fatty acids, in rats with DSS-induced colitis. Clin Nutr 2006; 25: 466-476
  CrossrefPubMedGoogle Scholar
• 28 Medeiros-de-Moraes IM, Gonçalves-de-Albuquerque CF, Kurz ARM, Oliveira FMJ, Abreu VHP, Torres RC, Carvalho VF, Estato V, Bozza PT, Sperandio M, Castro-Faria-Neto HC, Silva AR. Omega-9 oleic acid, the main compound of olive oil, mitigates inflammation during experimental sepsis. Oxid Med Cell Longev 2018; 2018: 1-12
  PubMedGoogle Scholar
• 29 Quaglio AEV, Castilho ACS, Di Stasi LC. Experimental evidence of MAP kinase gene expression on the response of intestinal anti-inflammatory drugs. Life Sci 2015; 136: 60-66
  CrossrefPubMedGoogle Scholar
• 30 Vlodavsky I, Beckhove P, Lerner I, Pisano C, Meirovitz A, Ilan N, Elkin M. Significance of heparanase in cancer and inflammation. Cancer Microenviron 2012; 5: 115-132
  CrossrefPubMedGoogle Scholar
• 31 Lerner I, Hermano E, Zcharia E, Rodkin D, Bulvik R, Doviner V, Rubinstein AM, Ishai-Michaeli R, Atzmon R, Sherman Y, Meirovitz A, Peretz T, Vlodavsky I, Elkin M. Heparanase powers a chronic inflammatory circuit that promotes colitis-associated tumorigenesis in mice. J Clin Invest 2011; 121: 1709-1721
  CrossrefPubMedGoogle Scholar
• 32 Malago JJ, Koninkx JFJG, Van Dijk JE. The heat shock response and cytoprotection of the intestinal epithelium. Cell Stress Chaperones 2002; 7: 191-199
  CrossrefPubMedGoogle Scholar
• 33 Tomasello G, Sciumè C, Rappa F, Rodolico V, Zerilli M, Martorana A, Cicero G, De Luca R, Damiani P, Accardo FM, Romeo M, Farina F, Bonaventura G, Modica G, Zummo G, Macario EC, Macario AJL, Cappello F. Hsp10, Hsp70, and Hsp90 immunohistochemical levels change in ulcerative colitis after therapy. Eur J Histochem 2011; 55: 210-214
  PubMedGoogle Scholar
• 34 Liu X, Yang LJ, Fan SJ, Jiang H, Pan F. Swimming exercise effects on the expression of HSP70 and iNOS in hippocampus and prefrontal cortex in combined stress. Neurosci Lett 2010; 476: 99-103
  CrossrefPubMedGoogle Scholar
• 35 Borges TJ, Wieten L, van Herwijnen MJ, Broere F, van der Zee R, Bonorino C, van Eden W. The anti-inflammatory mechanisms of Hsp70. Front Immunol 2012; 3: 1-12
  PubMedGoogle Scholar
• 36 Santin AD, Hermonat PL, Ravaggi A, Bellone S, Pecorelli S, Roman JJ, Parham GP, Cannon MJ. Interleukin-10 increases Th1 cytokine production and cytotoxic potential in human papillomavirus-specific CD81 cytotoxic T lymphocytes. J Virol 2000; 74: 4729-4737
  CrossrefPubMedGoogle Scholar
• 37 Barbara G, Xing Z, Hogaboam CM, Gauldie J, Collins SM. Interleukin 10 gene transfer prevents experimental colitis in rats. Gut 2000; 46: 344-349
  CrossrefPubMedGoogle Scholar
• 38 Gutter-Kapon L, Alishekevitz D, Shaked Y, Lic JP, Aronheim A, Ilan N, Vlodavsky I. Heparanase is required for activation and function of macrophages. Proc Natl Acad Sci U S A 2016; 113: E7808-E7817
  CrossrefPubMedGoogle Scholar
• 39 Chang L, Karin M. Mammalian MAP kinase signalling cascades. Nature 2001; 410: 37-40
  CrossrefPubMedGoogle Scholar
• 40 Reverchon E, de Marco I. Supercritical fluid extraction and fractionation of natural matter. J Supercrit Fluids 2006; 38: 146-166
  CrossrefPubMedGoogle Scholar
• 41 Simopoulos AP. The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med 2008; 233: 674-688
  CrossrefPubMedGoogle Scholar
• 42 Tyagi A, Kumar U, Santos VS, Reddy S, Mohammed SB, Ibrahim A. Partial replacement of dietary linoleic acid with long chain n-3 polyunsaturated fatty acids protects against dextran sulfate sodium-induced colitis in rats. Prostaglandins Leukot Essent Fatty Acids 2014; 91: 289-297
  CrossrefPubMedGoogle Scholar
• 43 DiNicolantonio JJ, OʼKeefe JH. Importance of maintaining a low omega-6/omega-3 ratio for reducing inflammation. Open Heart 2018; 5: 1-4
  CrossrefPubMedGoogle Scholar
• 44 Morris GP, Beck PL, Herridge MS, Depew WT, Szewczuk MR, Wallace JL. Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 1989; 96: 795-803
  CrossrefPubMedGoogle Scholar
• 45 Di Stasi LC, Camuesco D, Nieto A, Vilegas W, Zarzuelo A, Gálvez J. Intestinal anti-inflammatory activity of paepalantine, an isocoumarin isolated from the capitula of Paepalanthus bromelioides, in the trinitrobenzenesulphonic acid model of rat colitis. Planta Med 2004; 70: 315-320
  Article in Thieme ConnectPubMedGoogle Scholar
• 46 Bell CJ, Gall DG, Wallace JL. Disruption of colonic electrolyte transport in experimental colitis. Am J Physiol 1995; 268: G622-G630
  PubMedGoogle Scholar
• 47 Krawisz JE, Sharon P, Stenson WF. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Gastroenterology 1984; 87: 1344-1350
  CrossrefPubMedGoogle Scholar
• 48 Anderson ME. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 1985; 113: 548-555
  PubMedGoogle Scholar
• 49 Malone MH, Robichaud RC. A Hippocratic screen for pure or crude drug materials. Lloyd 1962; 25: 320-332
  PubMedGoogle Scholar

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