Adhesion of bacteria to epithelial tissue is an essential step in the progression of the urinary tract infections. Reduction of virulence factors responsible for microbial attachment may help to decrease or inhibit colonization of the host organism by pathogens. In the age of increasing bacterial antibiotic resistance, more and more attention is being paid to the use of plants and/or their bioactive components in the prevention and treatment of human infections. Asiatic acid (AA) and ursolic acid (UA), two plant secondary metabolites, were used as potential antibacterial agents. The current study aimed to determine the possible impact of AA and UA on morphology, hydrophobicity, and adhesion of clinical uropathogenic Escherichia coli strains (UPEC) to the uroepithelial cells. Our work describes for the first time the effects exerted by AA and UA on virulence factors of UPECs. The impact of both acids on the cell surface hydrophobicity of the investigated strains was very weak. The results clearly show the influence of AA and UA on the presence of P fimbriae and curli fibers, morphology of the UPECs cells and their adhesion to epithelium; however, some differences between activities of AA and UA were found.

Department of Biology and Medical Parasitology Wroclaw Medical University Mikulicza Radeckiego 9 50 367 Wroclaw Poland

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Anuuk H, Hirmo S, Turi E, Mikelsaar M, Arak E, Wadstrom T. Effect on cell surface hydrophobicity and susceptibility of Helicobacter pylori strains to medicinal plant extracts. FEMS Microbiol Lett. 1999;172:41–45. doi: 10.1111/j.1574-6968.1999.tb13447.x. PubMed DOI

Barnabas CG, Nagarajan S (1988) Antimicrobial activity of flavonoids of some medicinal plants. Fitoterapia 3:508–510

Cho CW, Choi DS, Cardone MH, Kim CW, Sinskey AJ, Rha C. Glioblastoma cell death induced by asiatic acid. Cell Biol Toxicol. 2006;22:393–408. doi: 10.1007/s10565-006-0104-2. PubMed DOI

Chung PY, Navaratnam P, Chung LY. Synergistic antimicrobial activity between pentacyclic triterpenoids and antibiotics against Staphylococcus aureus strains. Ann Clin Microbiol Antimicrob. 2011;10:25–30. doi: 10.1186/1476-0711-10-25. PubMed DOI PMC

Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol. 2000;66:4555–4558. doi: 10.1128/AEM.66.10.4555-4558.2000. PubMed DOI PMC

Clinical and Laboratory Standards Institute . M100-S18. Performance standards for antimicrobial susceptibility testing. Wayne: Seventeenth Informational Supplement Clinical Laboratory Standards Institute; 2008.

Cunningham DG, Vannozzi SA, Turk R, Roderick R, O’Shea E, Brilliant K. Cranberry phytochemicals and their health benefits. In: Shahidi F, Weerasinghe DK, editors. Nutraceutical beverages: Chemistry, nutrition, and health effects. Washington: American Chemical Society; 2004. pp. 35–51.

Dykes GA, Amarowicz R, Pegg RB. An antioxidant bearberry (Arctostaphylos uva-ursi) extractmodulates surface hydrophobicity of a wide range of food-related bacteria: implications for functional food safety. Food Control. 2003;14:515–518. doi: 10.1016/S0956-7135(02)00110-X. DOI

Evans DJ, Evans DG, Young LS, Pitt J. Hemagglutination typing of Escherichia coli: definition of seven hemagglutination types. J Clin Microbiol. 1980;12:235–242. PubMed PMC

Filocamo A, Bisignano C, D’Arrigo M, Ginestra G, Mandalari G, Galati EM. Norfloxacin and ursolic acid: in vitro association and postantibiotic effect against Staphylococcus aureus. Lett Appl Microbiol. 2011;53:193–197. doi: 10.1111/j.1472-765X.2011.03090.x. PubMed DOI

Fontanay S, Grare M, Mayer J, Finance C, Duval RE. Ursolic, oleanolic and betulinic acids: antibacterial spectra and selectivity indexes. J Ethnopharmacol. 2008;120:272–276. doi: 10.1016/j.jep.2008.09.001. PubMed DOI

Foo LY, Lu Y, Howell AB, Vorsa N. A-type proanthocyanidin trimers from cranberry that inhibit adherence of uropathogenic P-fimbriated Escherichia coli. J Nat Prod. 2000;63:1225–1228. doi: 10.1021/np000128u. PubMed DOI

Hammar M, Arnqvist A, Bian Z, Olsen A, Normark S. Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol. 1995;18:661–670. doi: 10.1111/j.1365-2958.1995.mmi_18040661.x. PubMed DOI

Ikeda Y, Murakami A, Ohigashi H. Ursolic acid: an anti- and pro-inflammatory triterpenoid. Mol Nutr Food Res. 2008;52:26–42. doi: 10.1002/mnfr.200700389. PubMed DOI

Jahanshahi M, Azad S, Aslanbeigi B, Rahbar M. Effect of subinhibitory concentrations of antibiotics and antibodies on the adherence of Escherichia coli to human uroepithelial cells in vitro. Res J Biol Sci. 2010;5:326–329. doi: 10.3923/rjbsci.2010.326.329. DOI

Johnson-White B, Buquo L, Zeinali M, Ligler FS. Prevention of nonspecific bacterial cell adhesion in immunoassays by use of cranberry juice. Anal Chem. 2006;78:853–857. doi: 10.1021/ac051700v. PubMed DOI

Justice SS, Hunstad DA, Seed PC, Hultgren SJ. Filamentation by Escherichia coli subverts innate defenses during urinary tract infection. PNAS. 2006;103:19884–19889. doi: 10.1073/pnas.0606329104. PubMed DOI PMC

Kurek A, Grudniak AM, Szwed M, Klicka A, Samluk Ł, Wolska KI, Janiszowska W, Popowska M. Oleanolic acid and ursolic acid affect peptidoglycan metabolism in Listeria monocytogenes. Antonie van Leeuwenhoek. 2010;97:61–68. doi: 10.1007/s10482-009-9388-6. PubMed DOI

Lindahl M, Faris A, Wadstrom T, Hjerten S. A new test based on “salting out” to measure relative surface hydrophobicity of bacterial cells. Biochim Biophys Acta. 1981;77:471–476. doi: 10.1016/0304-4165(81)90261-0. PubMed DOI

Melican K, Sandoval RM, Kader A, Josefsson L, Tanner GA, Molitoris BA, Richter-Dahlfors A. Uropathogenic Escherichia coli P and Type 1 fimbriae act in synergy in a living host to facilitate renal colonization leading to nephron obstruction. PLoS Pathog. 2011;7:e1001298. doi: 10.1371/journal.ppat.1001298. PubMed DOI PMC

Moodley R, Chenia H, Jonnalagadda SB, Koorbanally N. Antibacterial and anti-adhesion activity of the pentacyclic triterpenoids isolated from the leaves and edible fruits of Carissa macrocarpa. J Med Plants Res. 2011;5:4851–4858.

Mulvey MA. Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol. 2002;4:257–271. doi: 10.1046/j.1462-5822.2002.00193.x. PubMed DOI

Najar AG, Nejad MM, Mansouri S. The comparison between virulence factors of Escherichia coli isolated from urinary tract infections and faecal flora. Res Pharm Sci. 2007;2:99–103.

Nishino C, Enoki N, Tawata S, Mori A, Kobayashi K, Fukushima M (1987) Antibacterial activity of flavonoids against Staphylococcus epidermidis, a skin bacterium. Agric Biol Chem 51:139–143

Nostro A, Cannatelli MA, Crisafi G, Musolino AD, Procopio F, Alonzo V. Modifications of hydrophobicity, in vitro adherence and cellular aggregation of Streptococcus mutans by Helichrysum italicum extract. Lett Appl Microbiol. 2004;38:423–427. doi: 10.1111/j.1472-765X.2004.01509.x. PubMed DOI

Pizarro-Cerda J, Cossart P. Bacterial adhesion and entry into host cells. Cell. 2006;124:715–727. doi: 10.1016/j.cell.2006.02.012. PubMed DOI

Prades J, Vogler O, Alemany R, Gomez-Florit M, Funari SS, Ruiz-Gutierrez V, Barcelo F. Plant pentacyclic triterpenic acids as modulators of lipid membrane physical properties. Biochim Biophys Acta. 2011;1808:752–760. doi: 10.1016/j.bbamem.2010.12.007. PubMed DOI

Rafat M, Fonga KW, Goldsipe A, Stephenson BC, Coradetti ST, Sambandan TG, Sinskey AJ, Rha C. Association (micellization) and partitioning of aglycon triterpenoids. J Colloid Interface Sci. 2008;325:324–330. doi: 10.1016/j.jcis.2008.05.046. PubMed DOI

Rahim ZH, Khan HB. Comparative studies on the effect of crude aqueous (CA) and solvent (CM) extracts of clove on the cariogenic properties of Streptococcus mutans. J Oral Sci. 2006;48:117–123. doi: 10.2334/josnusd.48.117. PubMed DOI

Raksha R, Srinivasa H, Macaden RS. Occurrence and characterization of uropathogenic Escherichia coli in urinary tract infections. Indian J Med Microbiol. 2003;21:102–107. PubMed

Rauha JP, Remes S, Heinonen M, Hopia A, Kähkönen M, Kujala T, Pihlaja K, Vuorela H, Vuorela P (2000) Antimicrobial effects of Finnish plant extracts containing flavonoids and other phenolic compounds. Int J Food Microbiol 56:3–12 PubMed

Razak FA, Rahim ZH. The anti-adherence effect of Piper betle and Psidium guajava extracts on the adhesion of early settlers in dental plaque to saliva-coated glass surfaces. J Oral Sci. 2003;45:201–206. doi: 10.2334/josnusd.45.201. PubMed DOI

Saralaya V, Bhat G, Kamath A, Shivananda PG. Effect of trace elements on surface hydrophobicity and adherence of Escherichia coli to uroepithelial cells. Indian J Exp Biol. 2004;42:681–685. PubMed

Sunman E, Gopalkrishna Bhat K, Hegde BM. Bacterial adherence and immune response in recurrent UTI. Int J Gynaecol Obstet. 2001;75:263–268. doi: 10.1016/S0020-7292(01)00480-5. PubMed DOI

Szakiel A, Ruszkowski D, Grudniak A, Kurek A, Wolska KI, Doligalska M, Janiszowska W. Antibacterial and antiparasitic activity of oleanolic acid and its glycosides isolated from marigold (Calendula officinalis) Planta Med. 2008;74:1709–1715. doi: 10.1055/s-0028-1088315. PubMed DOI

Turi E, Turi M, Anuuk H, Arak E. Action of aqueous extracts of bearberry and cowberry leaves and wild camomile and pineapple-weed flowers on Escherichia coli surface structures. Pharm Biol. 1999;37:127–133. doi: 10.1076/phbi.37.2.127.6086. DOI

Wen X, Sun H, Liu J, Wu G, Zhang L, Wu X, Ni P (2005) Pentacyclic triterpenes. Part 1: The first examples of naturally occurring pentacyclic triterpenes as a new class of inhibitors of glycogen phosphorylases. Bioorg Med Chem Lett 15:4944–4948 PubMed

Wojnicz D, Jankowski S. Effects of subinhibitory concentrations of amikacin and ciprofloxacin on the hydrophobicity and adherence to epithelial cells of uropathogenic Escherichia coli strains. Int J Antimicrob Agents. 2007;29:700–704. doi: 10.1016/j.ijantimicag.2007.01.007. PubMed DOI

Wojnicz D, Sycz Z, Walkowski S, Gabrielska J, Aleksandra W, Alicja K, Anna SL, Hendrich AB. Study on the influence of cranberry extract Żuravit SOS(®) on the properties of uropathogenic Escherichia coli strains, their ability to form biofilm and its antioxidant properties. Phytomedicine. 2012;19:506–514. doi: 10.1016/j.phymed.2011.12.013. PubMed DOI

Yamanaka A, Kimizuka R, Kato T, Okuda K. Inhibitory effects of cranberry juice on attachment of oral streptococci and biofilm formation. Oral Microbiol Immunol. 2004;9:150–154. doi: 10.1111/j.0902-0055.2004.00130.x. PubMed DOI

Yatsuda R, Rosalen PL, Cury JA, Murata RM, Rehder VL, Melo LV, Koo H. Effects of Mikania genus plants on growth and cell adherence of mutans streptococci. J Ethnopharmacol. 2005;97:183–189. doi: 10.1016/j.jep.2004.09.042. PubMed DOI