Antibacterial activity of oleanolic and ursolic acids and their derivatives

Central European Journal of Biology

Volumn 5, Issue 5, 2010, Pages 543-553

  Wolska, Krystyna I ^a   Grudniak, Anna M ^a   Fiecek, Beata ^a   Kraczkiewicz Dowjat, Anna ^a   Kurek, Anna ^a  

^a UNIVERSITY OF WARSAW   (Poland)

Author keywords

Antibacterial activity; Antimutagenic effect; Cellular targets; Oleanolic acid; Ursolic acid

Indexed keywords

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM; POSIBACTERIA;

EID: 77955852363     PISSN: 1895104X     EISSN: 16443632     Source Type: Journal    
DOI: 10.2478/s11535-010-0045-x     Document Type: Review

References (93)

1. Levy S. B., The challenge of antibiotics resistance, Sci. Am., 1998, 278, 46-53.
2. Heinemann J. A., Can smart bullets penetrate magic bullet-proof vests, Drug. Discov. Today, 2001, 6, 875-878.
3. Chibani-Chennoufi S., Sidoti J., Bruttin A., Kutter E., Sarker S., Brussow H., In vitro and in vivo bacteriolytic activities of Escherichia coli phages: implications for phage therapy, Antimicrob. Agents Chemother., 2004, 48, 2558-2569.
4. Guliani A., Pirri G., Nicoletto S. F., Antimicrobial peptides: an overview of a promising class of therapeutics, Cent. Eur. J. Biol., 2007, 2, 1-3.
5. Cowan M. M., Plant products as antimicrobial agents, Clin. Microbiol. Rev., 1999, 12, 564-582.
6. Connolly J. D., Hill R. A., Triterpenoids, Nat. Prod. Rep., 2008, 25, 794-830.
7. Liu J., Oleanolic and ursolic acids: Research perspectives, J. Ethnopharmacol., 2005, 100, 92-94.
8. Farina C., Pinza M., Pifferi G., Synthesis and antiulcer activity of new derivatives of glycyrrhetic, oleanolic and ursolic acids, Pharmacology, 1998, 53, 22-32.
9. Chen Y., Liu J., Yang X., Zhao X., Xu H., Oleanolic acid nanosuspensions: preparation, in vitro characterization and enhanced hepatoprotective effect, J. Pharm. Pharmacol., 2005, 57, 259-264.
10. Li D. W., Hyun J. H., Jeong C. S., Kim Y. S., Lee E. B., Antiinflammatory activity of a-hederin methyl ester from the alkaline hydrolysate of the butanol fraction of Kalopanax pictus bark extract, Biol. Pharm. Bull., 2003, 26, 429-433.
11. Nishino H., Nishino A., Takayasu J., Hasegawa T., Iwashima A., Hitahabayashi K., Inhibition of the tumor-promoting action of 12-O-tetradecanoylphorbol 13-acetate by some oleanane-type triterpenoid compounds, Cancer Res., 1988, 48, 5210-5215.
12. Udayama M., Ohkawa M., Yoshida N., Kinjo J., Nohara T., Structures of three new oleanane glucuronides isolated from Lathyrus palustris var. pilosus and hepatoprotective activity, Chem. Pharm. Bull., 1998, 46, 1412-1415.
13. Ortiz-Andrade R. R., Garcia-Jimenez S., Castillo-Espana P., Ramirez-Avila G., Villalobos-Molina R., Estrada-Soto S., Alpha-glucosidase inhibitory activity of the methanolic extract from Tournefortia hartwegiana: an anti-hyperglycemic agent, J. Ethnopharmacol., 2007, 109, 48-53.
14. Becker H., Scher J. M., Speakman J. B., Zapp J., Bioactivity guided isolation of antimicrobial compounds from Lythrum salicaria, Fitotherapia, 2005, 76, 580-584.
15. Cunha W. R., Martins C., Ferreira de Silva D., Crotti A. E., Lopez N. P., Albuqureque S., In vitro trypanocidal activity of triterpenes from Miconia species, Planta Med., 2003, 69, 470-472.
16. Baglin I., Mitaine-Offer A. C., Nour M., Tan K., Cavé C., Lacaille-Dubois M. A., A review of natural and modified betulic, ursolic and echinocystic acid derivatives as potential antitumor and anti-HIV agents, Mini Rev. Med. Chem., 2003, 6, 525-539.
17. Kashiwada Y., Wang H. K., Nagao T., Kitanaka S., Yasuda I., Fuijoka T., et al., Anti-AIDS agents. 30. Anti-HIV activity of oleanolic acid, pomolic acid, and structurally related triterpenoids, J. Nat. Prod., 1998, 61, 1090-1095.
18. Kashiwada Y., Nagao T., Hashimoto A., Ikeshiro Y., Okabe H. Casentino L. M., Lee K. H., Anti-AIDS agents. 38. Anti-HIV activity of 3-O-acyl ursolic acid derivatives, J. Nat. Prod., 2000, 63, 1619-1622.
19. Ma C., Nakamura N., Miyashiro H., Hattori M., Shimotohno K., Inhibitory effects of constituents from Cynomorium songsricum and related triterpene derivatives on HIV-1 protease, Chem. Pharm. Bull., 1999, 47, 141-145.
20. Mengoni F., Lichtner M., Battinelli L., Marzi M., Mastoianni C. M., Vullo V., et al., In vitro anti-HIV activity of oleanolic acid on infected human mononuclear cells, Planta Med., 2002, 68, 111-114.
21. Fontanay S., Grare M., Mayer J., Finance C., Duval R. M., Ursolic, oleanolic and betulic acids: antibacterial spectra and selectivity indexes, J. Ethnopharmacol., 2008, 120, 272-276.
22. Daffe M., Draper P., The envelope layers of mycobacteria with reference to their pathogenicity, Adv. Microbiol. Physiol., 1988, 39, 131-203.
23. Zumla A., Grange J., Tuberculosis, Br. Med. J., 1998, 316, 1962-1964.
24. Bamuamba K., Gammon D. W., Meyers P., Dijoux-Franca M.-G., Scott G., Anti-mycobacterial activity of five plant species used as traditional medicines in the Western Cape Province (South Africa), J. Ethnopharmacol., 2008, 117, 385-390.
25. Mosam T., Rapid colorimetric assay for cell growth and survival: application to proliferation and cytotoxicity assays, J. Immunol. Meth., 1983, 65, 55-63.
26. Tanachatchairatana T., Bremner J. B., Chokchaisiri R., Suksamraran A., Antimycobacterial activity of cinnamate-based esters of the triterpenes betulic, oleanolic and ursolic acids, Chem. Pharm. Bull., 2008, 56, 194-198.
27. Rojas R., Caviedes L., Aponte J. C., Vaisberg A. J., Lewis W. H., Lamas G., et al., Aegicerin, the first oleanane triterpene with wide-ranging antimycobacterial activity, isolated from Clavija procera, J. Nat. Prod., 2006, 69, 845-846.
28. Horiuchi K., Shiota S., Hatano T, Yoshida T, Kuroda T., Tsuchiya T., Antimicrobial activity of oleanolic acid from Salvia officinalis and related compounds on vancomycin-resistant enterococci (VRE), Biol. Pharm. Bull., 2007, 30, 1147-1149.
29. Zheng C.-J., Sohn M.-J., Kim K.-Y., Yu H.-E., Kim W-G., Olean-27-carboxylic acid-type triterpenes with potent antibacterial activity from Aceriphyllum rossii, J. Agric. Food Chem., 2008, 56, 11752-11756.
30. Woldemichael G. M., Singh M. P., Maiese W. M., Timmermann B. N., Constituents of antibacterial extract of Caesalpinia paraguarensis Burk, Z. Naturforsch., 2003, 53, 70-75.
31. Szakiel A., Ruszkowski D., Grudniak A., Kurek A., Wolska K. I., Doligalska M., et al., Antibacterial and antiparasitic activity of oleanolic acid and its glycosides isolated from marigold (Calendula officinalis), Planta Med., 2008, 74, 1709-1715.
32. Collins L., Franzblau S. F, Microplate alarm blue assay versus BACTEC 460 system for high-throughput screening of compounds against Mycobacterium tuberculosis and Mycobacterium avium, Antimicrob. Agents Chemother., 1997, 41, 1004-1009.
33. Gu J.-Q., Wang Y., Franzblau S. G., Montenegro G., Timmermann B. N., Constituents of Quinchamalium majus with potential antitubercular activity, Z. Naturforsch., 2004, 59, 797-802.
34. Gu J.-Q., Wang Y., Franzblau S. G., Montenegro G., Yang D., Timmermann B. N., Antitubercular constituents of Valeriana laxiflora, Planta Med., 2004, 70, 509-514.
35. Jiménez-Arellanes A., Meckes M., Torres J., Luna-Herrera J., Antimycobacterial triterpenoids from Lantana hispida (Verbenaceae), J. Ethnopharmacol., 2007, 111, 202-205.
36. Caldwell C. G., Franzblau S. G., Suarez E., Timmermann B. N., Oleanane triterpenes from Junellia tridens, J. Nat. Prod., 2000, 63, 1611-1614.
37. Cantrell C. L., Lu T. S., Fronczek F. R., Fischer N. H., Adams L. B., Franzblau S. G., Antimicrobial cycloartanes from Borrichia frutescens, J. Nat. Prod., 1996, 59, 1131-1136.
38. Singh M. P., Petersen P. J., Weiss W. J., Kong F., Greenstein M., Saccharomycins, novel heptadecaglycoside antibiotics produced by Saccharothrix espanaensis: Antibacterial and mechanistic activities, Antimicrob. Agents Chemother., 2000, 44, 2154-2159.
39. National Committee for Clinical Laboratory Standards, Methods for antimicrobial susceptibility tests for bacteria that grow aerobically; Approved Standard M7-A6, NCCLS, Wayne, PA, USA, 2003.
40. Scalon Cunha L. C., Andrade e S.M. L., Cardoso F.N.A., Vinholis A. H., Gomes Martins C. H., da Silva F.A. A., et al., Antibacterial activity of triterpene acids and semi-synthetic derivatives against oral pathogens, Z. Naturforsch., 2007, 62, 668-672.
41. Timbekova A. E., Isaev M. I., Abubakirov N. K., Chemistry and biological activity of triterpenoid glycosides from Medicago sativa, Adv. Exp. Med. Biol., 1996, 405, 171-182.
42. Yadava R. N., A new biologically active triterpenoid saponin from the leaves of Lepidagathis hyalina Nees, Nat. Prod. Lett., 2001, 15, 315-322.
43. Yadava R. N., Jharbade J., A new bioactive triterpenoid saponin from the seeds of Lactuca scariola Linn, Nat. Prod. Res., 2007, 21, 500-506.
44. Kuete V., Wabo G. F., Ngameni B., Mbaveng A. T., Metuno R., Etoa F. X., et al., Antimicrobial activity of the methanolic extract, fractions and compounds from the stem bark of Irvingia gabonensis (Ixonanthaceae), J. Ethnopharmacol., 2007, 114, 54-60.
45. Cai L., Wu C. D., Compounds from Syzygium aromaticum possessing growth inhibitory activity against oral pathogens, J. Nat. Prod., 1996, 59, 987-990.
46. Djoukeng J. D., Abou-Mansour E., Tabacchi R., Tapondjou A. L., Bouda H., Lontsi D., Antibacterial triterpenes from Syzygium guineense (Myrtaceae), J. Ethnopharmacol., 2005, 101, 283-286.
47. Pannizzi L., Catalano S., Miarelli C., Cioni P. L., Campeol E., In vitro antimicrobial activity of extracts and isolated constituents of Geum rivale, Phytother. Res., 2000, 14, 561-563.
48. Clark A. M., El-Feraly E. S., Li W. S., Antimicrobial activity of phenolic constituents of Magnolia grandiflora L., J. Pharm. Sci., 1981, 70, 951-952.
49. Wächter G. A., Valcic S., Franzblau S. C., Suarez E., Timmermann B. N., Antitubercular activity of triterpenoids from Lippia turbinata, J. Nat. Prod., 2001, 64, 37-41.
50. Caliş T., Satana M. E., Yürüker A., Kelican P., Demirdamar R., Alaçam R., et al., Triterpene saponins from Cyclamen mirabile and their biological activities, J. Nat. Prod., 1997, 60, 315-318.
51. Yeung M.-F., Lau C. S. B., Chan R. C. Y., Zong Y., Che C.-T., Search for antibacterial constituents from a Tibetan medical plant, Gentianopsis paludosa, Phytother. Res., 2009, 23, 123-125.
52. Jiménez A., Meckes M., Alvarez V., Torres J., Parra R., Secondary metabolites from Chamaedora tepejilote (Palmae) are active against Mycobacterium tuberculosis, Phytother. Res., 2005, 19, 320-322.
53. da Silva Filho A. A., de Sousa J. P., Soares S., Furtado N. A., Andrade Silva M. L., Cunha W. R., et al., Antimicrobial activity of the extract and isolated compounds from Baccharis dracunculifolia D. C. (Asteraceae), Z. Naturforsch, 2008, 63, 40-46.
54. Takechi M., Tanaka Y., Structure-activity relationships of synthetic methyl ursolate glycosides, Phytochemistry, 1993, 34, 675-677.
55. Woldemichael G. M., Franzblau S. G, Zhang F., Wang Y., Timmerman B. N., Inhibitory effect of sterols from Ruprechtia triflora and diterpenes from Calceolaria pinnifolia on the growth of Mycobacterium tuberculosis, Planta Med., 2003, 69, 628-631.
56. Mallavadhani U. V., Mahapatra A., Jamil K., Reddy P. S., Antimicrobial activity of some pentacyclic triterpenes and their synthesized 3-O-lipophilic chains, Biol. Pharm. Bull., 2004, 27, 1576-1579.
57. Chattopadhyay D., Mati K., Kundu A. P., Chakraborty M. S., Bhadra R., Mandal S. C., et al., Antimicrobial activity of Alstonia macrophylla: a folklore of bay islands, J. Ethnopharmacol., 2001, 77, 49-55.
58. Chattopadhyay D., Arunachalan G., Mandal A. B., Sur T. K., Mandal S. C., Bhattacharya S. K., Antimicrobial and antiinflammatory activity of folklore: Mallotus peltatus leaf extract, J. Ethnopharmacol., 2002, 82, 229-237.
59. Zhang Y., Bao F., Hu J., Liang S., Zhang Y., Du G., et al., Antibacterial ligands and triterpenoids from Rostellularia procumbens, Planta Med., 2007, 73, 1596-1599.
60. Jaki B. U., Franzblau S. G., Chadwich L. R., Lakin D. C., Zhang F., Wang Y., et al., Purity-activity relationships of natural products: the case of anti-TB active ursolic acid, J. Nat. Prod., 2008, 71, 1742-1748.
61. Changsen C., Franzblau S. G., Palittapongarnpin P., Improved green fluorescent protein reporter genebased microplate screening for antituberculosis compounds by utilizing an acetamidase promoter, Antimicrob. Agents Chemother., 2003, 47, 3682-3687.
62. Setzer W. N., Rozmus G. F., Setzer M. C., Schmidt J. M., Vogler B., Reeb S., et al., Bioactive principles in the bark of Philidiostigma tropicum, J. Mol. Model., 2006, 12, 703-711.
63. Lee J. H., Jeong C. S., Gardenia jasminoides Ellis ethanol extract and its constituents reduce the risks of gastritis and reverse gastric lesions in rats, Food Chem. Toxicol., 2009, 47, 1127-1131.
64. Akbar E., Malik A., Antimicrobial triterpenes from Debregeasia salicifolia, Nat. Prod. Lett., 2002, 16, 339-344.
65. Chandramu C., Manohar R. D., Krupadanam D. G., Dashavantha R. V., Isolation, characterization and biological activity of betulic acid and ursolic acid from Vitex negundo L., Phytother. Res., 2003, 17, 129-134.
66. Li X. Q., Gao K., Jia Z. J., Eremophilenolides and other constituents from the roots of Ligularia sagitta, Planta Med., 2003, 69, 356-360.
67. Jovel E. M., Zhou X. L., Ming D. S., Wahabe T. R., Towers G. H., Bioactivity-guided isolation of the active compounds from Rosa nutkana and quantitative analysis of ascorbic acid by HPLC, Can. J. Physiol. Pharmacol., 2007, 85, 865-871.
68. Niikawa M., Hayashi H., Sato T., Nagase H., Kito H., Isolation of substances from glossy privet (Ligustrum lucidum Alt.) inhibiting the mutagenicity of benzo[a]pyrene in bacteria, Mutat. Res., 1993, 319, 1-9.
69. Maron D. M., Ames B. D., Revised methods for the Salmonella mutagenicity test, Mutation Res., 1983, 113, 173-215.
70. Lira Wde M., dos Santos F. V., Sannomiya M., Rodrigues C. M., Vilegas W., Varanda E. A., Modulatory effect of Byrsonima basiloba extracts on the mutagenicity of certain direct and indirect-acting mutagens in Salmonella typhimurium assays, J. Med. Food., 2008, 11, 111-119.
71. Young H. S., Chung H. Y., Lee C. K., Park K. Y., Yokozawa T., Oura H., Ursolic acid inhibits aflatoxin B1-induced mutagenicity in a Salmonella assay system, Biol. Pharm. Bull., 1994, 17, 990-992.
72. Miyazawa M., Okuno Y., Imanishi K., Suppression of the SOS-inducing activity of mutagenic heterocyclic amine, Trp-P-1, by triterpenoid from Uncaria siniensis in Salmonella typhimurium TA1535/pSK1002 Umu test, J. Agric. Food Chem., 2005, 53, 2312-2315.
73. Janion C., Inducible SOS response system of DNA repair and mutagenesis in Escherichia coli, Int. J. Biol. Sci., 2008, 23, 338-344.
74. Ohtsuka M., Fukuda K., Yano H., Kojiro M., Effect of nine active ingredients in Chinese herbal medicine sho-saiko-to on 2-(2-furyl)-3-(5-nitro-2-furyl) acrylamide mutagenicity, Jpn. J. Cancer Res., 1995, 86, 1131-1135.
75. Lee K. T., Sohn I. C., Park H. J., Kim D. W., Jung G. O., Park K. Y., Essential moiety for antimutagenic and cytotoxic activity of hederagenin monodesmosides and bidesmosides isolated from the stem bark of Kalopanax pictus, Planta Med., 2000, 66, 329-332.
76. Park K. Y., Jung G. O., Choi J., Lee K. T., Park H. J., Potent antimutagenic and their anti-lipid peroxidative effect of kaikasaponin III and tectorigenin from the flower of Pueraria thunbergiana, Arch. Pharm. Res., 2002, 25, 320-324.
77. Wei H., Ca Q., Rahn R., Zhang X., Wang Y. Lebwohl M., DNA structural integrity and base composition affect ultraviolet light-induced oxidative DNA damage, Biochemistry, 1998, 37, 6485-6490.
78. Park J. T., Uehara T., How bacteria consume their own exoskeleton (turnover and recycling of cell wall peptidoglycan), Microbiol. Mol. Biol. Rev., 2008, 72, 211-227.
79. Kurek A., Grudniak A. M., Szwed M., Klicka A., Samluk Ł., Wolska K. I., et al., Oleanolic acid and ursolic acid affect peptidoglycan metabolism in Listeria monocytogenes, Antonie van Leeuwenhoek, 2010, 97, 61-68.
80. Cossart P., Listeriology (1926-2007); the rise of a model pathogen, Microb. Infect., 2007, 9, 1143-1146.
81. Charpentier E., Courvalin P., Antibiotic resistance in Listeria spp., Antimicrob. Agents Chemother., 1999, 43, 2103-2108.
82. Kozai K., Suzuki J., Okada M., Nagasaka N., Effect of oleanolic acid-cyclodextrin inclusion compounds on dental caries by in vitro experiment and ratcaries model, Microbios, 1999, 97, 179-188.
83. Chen J.-C., Ho T.-H., Chang Y.-S., Wu S.-L., Li C.-C., Hsiang C.-Y., Identification of Escherichia coli enterotoxin inhibitors from traditional medical herbs in silico, in vitro and in vivo analyses, J. Ethnopharmacol., 2009, 121, 372-378.
84. Holmgren J., Svennerholm A. M., Bacterial enteric infections and vaccine development, Gastroenterol. Clin. North Amer., 1992, 21, 283-302.
85. Ren D., Zuo R., González Barrios A. F., Bedzyk L. A., Eldridge G. R., Pasmore M. E., et al., Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid, Appl. Environ. Microbiol., 2005, 71, 4022-4034.
86. Li Y.-H., Lau P. C., Lee J. H., Ellen R. P., Cvitkovitch D. G., Natural genetic transformation of Streptococcus mutans growing in biofilms, J. Bacteriol., 2001, 183, 897-908.
87. Potera C., Forging a link between biofilms and disease, Science, 1999, 19, 1837-1838.
88. Wei Y., Lee J.-M., Richmond C., Blatner F. R., Rafalski J. A., Larossa R. A., High-density microarray-mediated gene expression profiling of Escherichia coli, J. Bacteriol., 2001, 183, 545-556.
89. Watnick P., Kotler R., Biofilm, city of microbes, J. Bacteriol., 2000, 182, 2675-2679.
90. Ramachandran S., Prasad N. R., Effect of ursolic acid, a triterpenoid antioxidant, on ultraviolet-B radiation-induced cytotoxicity, lipid peroxidation and DNA damage in human lymphocytes, Chem. Biol. Interact., 2008, 176, 99-107.
91. Chu R., Griffin C., Staub R. D., Shoemaker M., Climent J., Leitman D., Cohen I., Shtivelman E., Fong S., Selective concomitant inhibition of mTORC1 and TORC2 activity in estrogen receptor negative breast cancer cells by BN107 and oleanolic acid, Int. J. Cancer, (in press), DOI: 10. 1002. ijc. 25116.
92. Kim J., Jang D. S., Kim H., Kim J. S., Anti-lipase and lipolytic activities of ursolic acid isolated from the roots of Actinidia arguta, Arch. Pharm. Res., 2009, 32, 983-987.
93. Xi J., Chang Q., Chan C. K., Meng Z. Y., Wang G. N., Sun J. B., Wang Y. T., Tong H. H., Zheng Y., Formulation development and bioavailability evaluation of a self-nanoemulsified drug delivery system of oleanolic acid, AAPS Pharm. Sci. Tech., 2009, 10, 172-182.