Top

BMC Complementary Medicine and Therapies

Published in:

Open Access 01-12-2017 | Research article

Oral administration of taheebo (Tabebuia avellanedae Lorentz ex Griseb.) water extract prevents DSS-induced colitis in mice by up-regulating type II T helper immune responses

Authors: Hyun Jung Park, Sung Won Lee, Dong-Joo Kwon, Seong-Il Heo, Se-Ho Park, Sun Young Kim, Seokmann Hong

Published in: BMC Complementary Medicine and Therapies | Issue 1/2017

Abstract

Background

Inflammatory bowel diseases (IBDs) are chronic inflammatory disorders that are mediated by pathogenic Th1 and Th17 cells. Previous studies have demonstrated that taheebo water extract (TWE) derived from Tabebuia avellanedae Lorentz ex Griseb., as folk remedy, has been used to treat various inflammatory diseases. Although TWE has been previously shown to display anti-inflammatory activities, the in vivo effects of TWE on mucosal immune responses remain unclear.

Methods

We examined the anti-inflammatory effects of TWE on innate immune cells such as dendritic cells (DCs) and macrophages and also on the differentiation of T helper cells. Lastly, adopting a method for dextran sulfate sodium (DSS)-induced colitis, we investigated whether the oral administration of TWE can modulate mucosal inflammatory responses.

Results

We found that TWE could activate DCs to produce immunosuppressive IL10 and polarize macrophages toward an anti-inflammatory phenotype in the mesenteric lymph node (MLN). Such alterations in DCs and macrophages resulted in a significant increase in anti-inflammatory Th2 and Foxp3⁺ Treg cells and a dramatic decrease in pro-inflammatory Th1 and Th17 cells in the MLN. Upon induction of colitis with DSS treatment, TWE significantly reduced the clinical symptoms, including body weight loss and colonic tissue inflammation, by up-regulating type II T helper immune responses.

Conclusions

Taken together, these data suggest that TWE is an excellent natural product with therapeutic effects to help improve inflammatory disorders such as colitis.

Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature. 2011;474(7351):298–306.CrossRefPubMed

Kosiewicz MM, Zirnheld AL, Alard P. Gut microbiota, immunity, and disease: a complex relationship. Front Microbiol. 2011;2:180.CrossRefPubMedPubMedCentral

Cerovic V, Bain CC, Mowat AM, Milling SW. Intestinal macrophages and dendritic cells: what's the difference? Trends Immunol. 2014;35(6):270–7.CrossRefPubMed

Mucida D, Park Y, Kim G, Turovskaya O, Scott I, Kronenberg M, Cheroutre H. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science. 2007;317(5835):256–60.CrossRefPubMed

Bain CC, Mowat AM. Intestinal macrophages - specialised adaptation to a unique environment. Eur J Immunol. 2011;41(9):2494–8.CrossRefPubMed

Ueda S, Umemura T, Dohguchi K, Matsuzaki T, Tokuda H, Nishino H, Iwashima A. Production of anti-tumour-promoting furanonaphthoquinones in Tabebuia avellanedae cell cultures. Phytochemistry. 1994;36(2):323–5.CrossRefPubMed

Gomez Castellanos JR, Prieto JM, Heinrich M. Red Lapacho (Tabebuia impetiginosa)--a global ethnopharmacological commodity? J Ethnopharmacol. 2009;121(1):1–13.CrossRefPubMed

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(1):145–52.CrossRefPubMed

Lee MH, Choi HM, Hahm DH, Her E, Yang HI, Yoo MC, Kim KS. Analgesic and anti-inflammatory effects in animal models of an ethanolic extract of Taheebo, the inner bark of Tabebuia avellanedae. Mol Med Rep. 2012;6(4):791–6.CrossRefPubMed

10.

Park BS, Lee HK, Lee SE, Piao XL, Takeoka GR, Wong RY, Ahn YJ, Kim JH. Antibacterial activity of Tabebuia impetiginosa Martius ex DC (Taheebo) against helicobacter pylori. J Ethnopharmacol. 2006;105(1–2):255–62.CrossRefPubMed

11.

Pereira IT, Burci LM, da Silva LM, Baggio CH, Heller M, Micke GA, Pizzolatti MG, Marques MC, Werner MF. Antiulcer effect of bark extract of Tabebuia avellanedae: activation of cell proliferation in gastric mucosa during the healing process. Phytother Res. 2013;27(7):1067–73.CrossRefPubMed

12.

Nakano K, Maruyama K, Murakami K, Takaishi Y, Tomimatsu T. Iridoids from Tabebuia-Avellanedae. Phytochemistry. 1993;32(2):371–3.CrossRef

13.

Shouval DS, Biswas A, Goettel JA, McCann K, Conaway E, Redhu NS, Mascanfroni ID, Al Adham Z, Lavoie S, Ibourk M, et al. Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity. 2014;40(5):706–19.CrossRefPubMedPubMedCentral

14.

Al-Sheraji SH, Ismail A, Manap MY, Mustafa S, Yusof RM, Hassan FA. Prebiotics as functional foods: a review. J Funct Foods. 2013;5(4):1542–53.CrossRef

15.

Pulendran B, Tang H, Manicassamy S. Programming dendritic cells to induce T(H)2 and tolerogenic responses. Nat Immunol. 2010;11(8):647–55.CrossRefPubMed

16.

Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B. Lamina Propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol. 2007;8(10):1086–94.CrossRefPubMed

17.

Hadis U, Wahl B, Schulz O, Hardtke-Wolenski M, Schippers A, Wagner N, Muller W, Sparwasser T, Forster R, Pabst O. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria. Immunity. 2011;34(2):237–46.CrossRefPubMed

18.

Schreiber HA, Loschko J, Karssemeijer RA, Escolano A, Meredith MM, Mucida D, Guermonprez P, Nussenzweig MC. Intestinal monocytes and macrophages are required for T cell polarization in response to Citrobacter rodentium. J Exp Med. 2013;210(10):2025–39.CrossRefPubMedPubMedCentral

19.

Buckner JH. Mechanisms of impaired regulation by CD4(+)CD25(+)FOXP3(+) regulatory T cells in human autoimmune diseases. Nat Rev Immunol. 2010;10(12):849–59.CrossRefPubMedPubMedCentral

20.

Boehm F, Martin M, Kesselring R, Schiechl G, Geissler EK, Schlitt HJ, Fichtner-Feigl S. Deletion of Foxp3+ regulatory T cells in genetically targeted mice supports development of intestinal inflammation. BMC Gastroenterol. 2012;12:97.CrossRefPubMedPubMedCentral

21.

Takahata M, Fremont M, Desreumaux P, Roussemaux C, Dubuquoy C, Shimomiya Y, Nakamura Y, Miyake Y. Evaluation of therapeutic properties of fermented vegetables extract (OM-X (R)) in the model of colitis induced by Citrobacter rodentium in mice. J Funct Foods. 2014;10:117–27.CrossRef

22.

Mishra PK, Palma M, Bleich D, Loke P, Gause WC. Systemic impact of intestinal helminth infections. Mucosal Immunol. 2014;7(4):753–62.PubMed

23.

Broadhurst MJ, Ardeshir A, Kanwar B, Mirpuri J, Gundra UM, Leung JM, Wiens KE, Vujkovic-Cvijin I, Kim CC, Yarovinsky F, et al. Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathog. 2012;8(11):e1003000.CrossRefPubMedPubMedCentral

24.

Lin Y, Yang X, Yue W, Xu X, Li B, Zou L, He R. Chemerin aggravates DSS-induced colitis by suppressing M2 macrophage polarization. Cell Mol Immunol. 2014;11(4):355–66.CrossRefPubMedPubMedCentral

25.

Weisser SB, Brugger HK, Voglmaier NS, McLarren KW, van Rooijen N, Sly LM. SHIP-deficient, alternatively activated macrophages protect mice during DSS-induced colitis. J Leukoc Biol. 2011;90(3):483–92.CrossRefPubMed

26.

Fairweather D, Cihakova D. Alternatively activated macrophages in infection and autoimmunity. J Autoimmun. 2009;33(3–4):222–30.CrossRefPubMedPubMedCentral

27.

Jang SE, Hyam SR, Han MJ, Kim SY, Lee BG, Kim DH. Lactobacillus brevis G-101 ameliorates colitis in mice by inhibiting NF-kappaB, MAPK and AKT pathways and by polarizing M1 macrophages to M2-like macrophages. J Appl Microbiol. 2013;115(3):888–96.CrossRefPubMed

28.

Jang SE, Han MJ, Kim SY, Kim DH. Lactobacillus plantarum CLP-0611 ameliorates colitis in mice by polarizing M1 to M2-like macrophages. Int Immunopharmacol. 2014;21(1):186–92.CrossRefPubMed

29.

Park BS, Kim JR, Lee SE, Kim KS, Takeoka GR, Ahn YJ, Kim JH. Selective growth-inhibiting effects of compounds identified in Tabebuia impetiginosa inner bark on human intestinal bacteria. J Agric Food Chem. 2005;53(4):1152–7.CrossRefPubMed

30.

Pinho BR, Sousa C, Valentao P, Andrade PB: Is nitric oxide decrease observed with naphthoquinones in LPS stimulated RAW 264.7 macrophages a beneficial property? PLoS One 2011, 6(8):e24098.

31.

Inoue K, Takano H, Ichinose T, Tomura S, Yanagisawa R, Sakurai M, Sumi D, Cho AK, Hiyoshi K, Kumagai Y. Effects of naphthoquinone on airway responsiveness in the presence or absence of antigen in mice. Arch Toxicol. 2007;81(8):575–81.CrossRefPubMed

32.

Inoue K, Takano H, Hiyoshi K, Ichinose T, Sadakane K, Yanagisawa R, Tomura S, Kumagai Y. Naphthoquinone enhances antigen-related airway inflammation in mice. Eur Respir J. 2007;29(2):259–67.CrossRefPubMed

33.

Xu J, Wagoner G, Douglas JC. Drew PD: beta-Lapachone ameliorization of experimental autoimmune encephalomyelitis. J Neuroimmunol. 2013;254(1–2):46–54.CrossRefPubMed

34.

Cheng HH, Kuo SC, Lin WC. Pharmacodynamic and pharmacokinetic studies of anthraquinone 2-carboxylic acid on passive cutaneous anaphylaxis in rats. Res Commun Mol Pathol Pharmacol. 1999;105(1–2):97–103.PubMed

35.

Santangelo C, Vari R, Scazzocchio B, Di Benedetto R, Filesi C, Masella R. Polyphenols, intracellular signalling and inflammation. Ann Ist Super Sanita. 2007;43(4):394–405.PubMed

36.

Hunter MM, Wang A, McKay DM. Helminth infection enhances disease in a murine TH2 model of colitis. Gastroenterology. 2007;132(4):1320–30.CrossRefPubMed

37.

Tordesillas L, Goswami R, Benede S, Grishina G, Dunkin D, Jarvinen KM, Maleki SJ, Sampson HA, Berin MC. Skin exposure promotes a Th2-dependent sensitization to peanut allergens. J Clin Invest. 2014;124(11):4965–75.CrossRefPubMedPubMedCentral

38.

Han H, Thelen TD, Comeau MR, Ziegler SF. Thymic stromal lymphopoietin-mediated epicutaneous inflammation promotes acute diarrhea and anaphylaxis. J Clin Invest. 2014;124(12):5442–52.CrossRefPubMedPubMedCentral

39.

Choi WH, Um MY, Ahn J, Jung CH, Park MK, Ha TY. Ethanolic extract of Taheebo attenuates increase in body weight and fatty liver in mice fed a high-fat diet. Molecules. 2014;19(10):16013–23.CrossRefPubMed

Title: Oral administration of taheebo (Tabebuia avellanedae Lorentz ex Griseb.) water extract prevents DSS-induced colitis in mice by up-regulating type II T helper immune responses
Authors: Hyun Jung Park
Sung Won Lee
Dong-Joo Kwon
Seong-Il Heo
Se-Ho Park
Sun Young Kim
Seokmann Hong
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: BMC Complementary Medicine and Therapies / Issue 1/2017
Electronic ISSN: 2662-7671
DOI: https://doi.org/10.1186/s12906-017-1952-4

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Oral administration of taheebo (Tabebuia avellanedae Lorentz ex Griseb.) water extract prevents DSS-induced colitis in mice by up-regulating type II T helper immune responses

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2017

Inhibition of influenza virus via a sesquiterpene fraction isolated from Laggera pterodonta by targeting the NF-κB and p38 pathways

Herbal formula SC-E1 suppresses lipopolysaccharide-stimulated inflammatory responses through activation of Nrf2/HO-1 signaling pathway in RAW 264.7 macrophages

Mature leaf concentrate of Sri Lankan wild type Carica papaya Linn. modulates nonfunctional and functional immune responses of rats

Antihyperlipidaemic and hepatoprotective activities of acidic and enzymatic hydrolysis exopolysaccharides from Pleurotus eryngii SI-04

Withania somnifera leaf alleviates cognitive dysfunction by enhancing hippocampal plasticity in high fat diet induced obesity model

Evaluation of the anti-diarrheal activity of the aqueous stem extract of Lantana camara Linn (Verbenaceae) in mice