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Planta Med 2020; 86(04): 247-254
DOI: 10.1055/a-1089-8645
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Aqueous Root Extract from Ononis spinosa Exerts Anti-adhesive Activity against Uropathogenic Escherichia coli

Melanie Deipenbrock
University of Münster, Institute of Pharmaceutical Biology and Phytochemistry, Münster, Germany
,
Jandirk Sendker
University of Münster, Institute of Pharmaceutical Biology and Phytochemistry, Münster, Germany
,
Andreas Hensel
University of Münster, Institute of Pharmaceutical Biology and Phytochemistry, Münster, Germany
› Author Affiliations
Further Information

Publication History

received 08 November 2019
revised 18 December 2019

accepted 23 December 2019

Publication Date:
22 January 2020 (online)

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Abstract

Extracts from Ononis spinosa are traditionally used for urinary tract infections due to diuretic and anti-inflammatory activity. A potential influence on the virulence of uropathogenic Escherichia coli has not been investigated until now. The following study aimed to investigate the influence of an aqueous O. spinosa extract on uropathogenic E. coli and uropathogenic E. coli host cell interaction. A hot water extract from the roots of O. spinosa (O. spinosa extract) was characterized by LC-qTOF-MS. The influence of O. spinosa extract on the proliferation of uropathogenic E. coli UTI89 and on cell viability against human T24 bladder cells was investigated. Anti-adhesive activity of O. spinosa extract was assessed by flow cytometry, evaluating the adhesion of fluorescent-labelled UTI89 to T24 bladder cells. Internalization of uropathogenic E. coli into T24 cells was monitored by an invasion assay. O. spinosa extract was characterized by the presence of isoflavones, isoflavanones, licoagrosides, pterocarpans, tartaric acid derivatives, and saponines. O. spinosa extract had no influence on the proliferation of uropathogenic E. coli (125 – 1000 µg/mL) and did not influence the cell viability of T24 cells. Bacterial adhesion to T24 cells was significantly (p > 0.001) inhibited by O. spinosa extract in a concentration-dependent manner (125 – 1000 µg/mL) during coincubation. Preincubation of uropathogenic E. coli or T24 cells with O. spinosa extract reduced bacterial adhesion, but to a lower extent than during coincubation. Consequently, the reduced bacterial adhesion also leads to a reduced internalization of uropathogenic E. coli uropathogenic E. coli into the host cell. O. spinosa extract does not interact with FimH-mediated uropathogenic E. coli adhesion to host cells. From these data, the traditional use of O. spinosa extracts for urinary tract infections seems to be rationalized.

Key words

Ononis spinosa - Fabaceae - adhesion - urinary tract infections - uropathogenic E. coli
 

  • References

  • 1 European Scientific Cooperative on Phytotherapy (ESCOP). ESCOP Monograph Ononidis radix, Restharrow root. Exeter EX1 UK: Thieme Publisher; 2015
    Google Scholar
  • 2 European Medical Agency (EMA). Community herbal monograph of HMBC working group: Ononis spinosa. Available at: http://www.ema.europa.eu/docs/en_GB/document_library/Herbal_-_Community_herbal_monograph/2014/05/WC500167795.pdf Accessed June 1, 2018
    PubMedGoogle Scholar
  • 3 Rebuelta M, San Roman L, G.-Serra Nillos M. Étude de lʼeffet diurétique de différentes préparations de lʼOnonis spinosa L. Plantes Méd Phytothér 1981; 15: 99-108
    PubMedGoogle Scholar
  • 4 Addotey JN, Lengers I, Jose J, Gampe N, Béni S, Petereit F, Hensel A. Isoflavonoids with inhibiting effects on human hyaluronidase-1 and norneolignan clitorienolactone B from Ononis spinosa L. root extract. Fitoterapia 2018; 130: 169-174
    CrossrefPubMedGoogle Scholar
  • 5 Stridh S. Regulation of renal Hyaluronan in Water Handling. Studies in vivo and in vitro [dissertation]. Uppsala: Uppsala University; 2013
    PubMedGoogle Scholar
  • 6 Bolle P, Faccendini P, Bello U, Panzironi C, Tita B. Ononis spinosa L: Pharmacological effect of ethanol extract. Pharmacol Res 1993; 27: 27-28
    CrossrefPubMedGoogle Scholar
  • 7 Dannhardt G, Schneider G, Schwell B. Identification and 5-lipoxygenase inhibiting potency of medicarpin isolated from roots of Ononis spinosa L. Pharma Pharmacol Lett 1992; 2: 161-162
    PubMedGoogle Scholar
  • 8 Spiegler V. Root Extract from Ononis spinosa exert anti-inflammatory Activity in vitro on IL-8 and TNF-alpha Release by Inhibition of TLR-4 Receptor. Front Pharmacol [submitted].
    PubMedGoogle Scholar
  • 9 Derksen A, Hensel A, Hafezi W, Herrmann F, Schmidt TJ, Ehrhardt C, Ludwig S, Kühn J. 3-O-galloylated procyanidins from Rumex acetosa L. inhibit the attachment of influenza A virus. PLoS One 2014; 9: e110089
    CrossrefPubMedGoogle Scholar
  • 10 Löhr G, Beikler T, Podbielski A, Standar K, Redanz S, Hensel A. Polyphenols from Myrothamnus flabellifolia Welw. inhibit in vitro adhesion of Porphyromonas gingivalis and exert anti-inflammatory cytoprotective effects in KB cells. J Clin Periodontol 2011; 38: 457-469
    CrossrefPubMedGoogle Scholar
  • 11 Messing J, Niehues M, Shevtsova A, Borén T, Hensel A. Antiadhesive properties of arabinogalactan protein from ribes nigrum seeds against bacterial adhesion of Helicobacter pylori . Molecules 2014; 19: 3696-3717
    CrossrefPubMedGoogle Scholar
  • 12 Messing J, Thöle C, Niehues M, Shevtsova A, Glocker E, Borén T, Hensel A. Antiadhesive properties of Abelmoschus esculentus (Okra) immature fruit extract against Helicobacter pylori adhesion. PLoS One 2014; 9: e84836
    CrossrefPubMedGoogle Scholar
  • 13 Scharf B, Sendker J, Dobrindt U, Hensel A. Influence of cranberry extract on Tamm-Horsfall protein in human urine and its antiadhesive activity against uropathogenic Escherichia coli . Planta Med 2019; 85: 126-138
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Schmuch J, Beckert S, Brandt S, Löhr G, Hermann F, Schmidt TJ, Beikler T, Hensel A. Extract from Rumex acetosa L. for prophylaxis of periodontitis: inhibition of bacterial in vitro adhesion and of gingipains of Porphyromonas gingivalis by epicatechin-3-O-(4β→8)-epicatechin-3-O-gallate (procyanidin-B2-Di-gallate). PLoS One 2015; 10: e0120130
    CrossrefPubMedGoogle Scholar
  • 15 Beydokthi SS, Sendker J, Brandt S, Hensel A. Traditionally used medicinal plants against uncomplicated urinary tract infections: Hexadecyl coumaric acid ester from the rhizomes of Agropyron repens (L.) P. Beauv. with antiadhesive activity against uropathogenic E. coli . Fitoterapia 2017; 117: 22-27
    CrossrefPubMedGoogle Scholar
  • 16 Grube K, Spiegler V, Hensel A. Antiadhesive phthalides from Apium graveolens fruits against uropathogenic E. coli . J Ethnopharmacol 2019; 237: 300-306
    CrossrefPubMedGoogle Scholar
  • 17 Sarshar S, Brandt S, Asadi Karam MR, Habibi M, Bouzari S, Lechtenberg M, Dobrindt U, Qin X, Goycoolea FM, Hensel A. Aqueous extract from Orthosiphon stamineus leaves prevents bladder and kidney infection in mice. Phytomedicine 2017; 28: 1-9
    CrossrefPubMedGoogle Scholar
  • 18 Sarshar S, Sendker J, Qin X, Goycoolea FM, Asadi Karam MR, Habibi M, Bouzari S, Dobrindt U, Hensel A. Antiadhesive hydroalcoholic extract from Apium graveolens fruits prevents bladder and kidney infection against uropathogenic E. coli . Fitoterapia 2018; 127: 237-244
    CrossrefPubMedGoogle Scholar
  • 19 Gampe N, Darcsi A, Nagyné Nedves A, Boldizsár I, Kursinszki L, Béni S. Phytochemical analysis of Ononis arvensis L. by liquid chromatography coupled with mass spectrometry. J Mass Spectrom 2019; 54: 121-133
    CrossrefPubMedGoogle Scholar
  • 20 Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55-63
    CrossrefPubMedGoogle Scholar
  • 21 Klemm P, Vejborg RM, Hancock V. Prevention of bacterial adhesion. Appl Microbiol Biotechnol 2010; 88: 451-459
    CrossrefPubMedGoogle Scholar
  • 22 Bubeník J, Baresová M, Viklický V, Jakoubková J, Sainerová H, Donner J. Established cell line of urinary bladder carcinoma (T24) containing tumour-specific antigen. Int J Cancer 1973; 11: 765-773
    CrossrefPubMedGoogle Scholar
  • 23 Miyazaki J, Ba-Thein W, Kumao T, Obata Yasuoka M, Akaza H, Hayshi H. Type 1, P and S fimbriae, and afimbrial adhesin I are not essential for uropathogenic Escherichia coli to adhere to and invade bladder epithelial cells. FEMS Immunol Med Microbiol 2002; 33: 23-26
    CrossrefPubMedGoogle Scholar
  • 24 Chen SL, Hung CS, Xu J, Reigstad CS, Magrini V, Sabo A, Blasiar D, Bieri T, Meyer RR, Ozersky P, Armstrong JR, Fulton RS, Latreille JP, Spieth J, Hooton TM, Mardis ER, Hultgren SJ, Gordon JI. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad Sci U S A 2006; 103: 5977-5982
    CrossrefPubMedGoogle Scholar
  • 25 Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55-63
    CrossrefPubMedGoogle Scholar
  • 26 Rafsanjany N, Lechtenberg M, Petereit F, Hensel A. Antiadhesion as a functional concept for protection against uropathogenic Escherichia coli: in vitro studies with traditionally used plants with antiadhesive activity against uropathogenic Escherichia coli . J Ethnopharmacol 2013; 145: 591-597
    CrossrefPubMedGoogle Scholar
  • 27 Rafsanjany N, Sendker J, Lechtenberg M, Petereit F, Scharf B, Hensel A. Traditionally used medicinal plants against uncomplicated urinary tract infections: Are unusual, flavan-4-ol- and derhamnosylmaysin derivatives responsible for the antiadhesive activity of extracts obtained from stigmata of Zea mays L. against uropathogenic E. coli and Benzethonium chloride as frequent contaminant faking potential antibacterial activities?. Fitoterapia 2015; 105: 246-253
    CrossrefPubMedGoogle Scholar
  • 28 Elsinghorst EA. Measurement of Invasion by Gentamicin Resistance. In: Clark VL, Bavoil PM. eds. Bacterial Pathogenesis Part B: Interaction of pathogenic Bacteria with Host Cells. Methods in Enzymology. Amsterdam: Elsevier; 1994: 405-420
    Google Scholar
  • 29 Lo AWH, van de Water K, Gane PJ, Chan AWE, Steadman D, Stevens K, Selwood DL, Waksman G, Remaut H. Suppression of type 1 pilus assembly in uropathogenic Escherichia coli by chemical inhibition of subunit polymerization. J Antimicrob Chemother 2014; 69: 1017-1026
    CrossrefPubMedGoogle Scholar
  • 30 Mascherpa D, Carazzone C, Marrubini G, Gazzani G, Papetti A. Identification of phenolic constituents in Cichorium endivia var. crispum and var. latifolium salads by high-performance liquid chromatography with diode array detection and electrospray ioniziation tandem mass spectrometry. J Agric Food Chem 2012; 60: 12142-12150
    CrossrefPubMedGoogle Scholar
  • 31 Ribas-Agustí A, Gratacós-Cubarsí M, Sárraga C, García-Regueiro JA, Castellari M. Analysis of eleven phenolic compounds including novel p-coumaroyl derivatives in lettuce (Lactuca sativa L.) by ultra-high-performance liquid chromatography with photodiode array and mass spectrometry detection. Phytochem Anal 2011; 22: 555-563
    CrossrefPubMedGoogle Scholar
  • 32 Mezrag A, Malafronte N, Bouheroum M, Travaglino C, Russo D, Milella L, Severino L, De Tommasi N, Braca A, Dal Piaz F. Phytochemical and antioxidant activity studies on Ononis angustissima L. aerial parts: isolation of two new flavonoids. Nat Prod Res 2017; 31: 507-514
    CrossrefPubMedGoogle Scholar