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Evaluation of the bioactivities of extracts of endophytes isolated from Taiwanese herbal plants

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Abstract

The endophytic extracts from 19 endophytes, isolated from 13 species of Taiwanese plants, were evaluated for biological activity, including cytotoxicity, anti-platelet aggregation, and anti-inflammatory activity. The extracts of 12 endophytes exhibited inhibitory effects on collagen-induced platelet aggregation with IC50 values of 19.85–87.64 μg/ml. Four strains, Rahnella aquatilis, Pantoea agglomerans, Rhodotorula sp., and Penicillium paxilli, also showed inhibitory effects on thrombin-induced platelet aggregation with IC50 values of 42.80–61.54 μg/ml. Additionally 12 extracts of endophytes exhibited cytotoxicities with IC50 values of 0.12–19.83 μg/ml. However, eight extracts revealed inhibitory effects on superoxide anion generation induced by fMLP (N-formyl-l-methionyl-l-leucyl-l-phenylalanine) in human neutrophils. The extract of Rahnella aquatilis showed anti-platelet aggregation activity, and bioassay-directed fractionation led to the isolation of six compounds, including one isoalloxazine: lumichrome (1); two isoflavones: genistein (2) and daidzein (3); two cyclic peptides: cyclo-Pro-Val (4) and cyclo-Pro-Phe (5); and one benzenoid: methyl 2,4,5-trimethoxybenzoate (6). These results indicated that endophytes from Taiwanese herbal plants could be useful sources for research and development of bioactive lead compounds from nature.

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References

  • Achouak W, Pages JM, De Mot R, Molle G, Heulin T (1998) A major outer membrane protein of Rahnella aquatilis functions as a porin and root adhesin. J Bacteriol 180:909–913

    CAS  Google Scholar 

  • Aken BV, Peres CM, Doty SL, Yoon JM, Schnoor JL (2004) Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoids x nigra DN34). Int J Syst Evol Microbiol 54:1191–1196. doi:10.1099/ijs.0.02796-0

    Article  CAS  Google Scholar 

  • Bertrand H, Plassard C, Pinochet X, Touraine B, Normand P, Cleyet-Marel JC (2000) Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Can J Microbiol 46:229–236. doi:10.1139/cjm-46-3-229

    Article  CAS  Google Scholar 

  • Brady SF, Clardy J (2000) CR377, a new pentaketide antifungal agent isolated from an endophytic fungus. J Nat Prod 63:1447–1448. doi:10.1021/np990568p

    Article  CAS  Google Scholar 

  • Chang CI, Kuo CC, Chang JY, Kuo YH (2004) Three new oleanane-type triterpenes from Ludwigia octovalvis with cytotoxic activity against two human cancer cell lines. J Nat Prod 67:91–93. doi:10.1021/np030267m

    Article  CAS  Google Scholar 

  • Chang HL, Chang FR, Chen JS, Wang HP, Wu YH, Wang CC, Wu YC, Hwang TL (2008) Inhibitory effects of 16-hydroxycleroda-3, 13(14)E-dien-15-oic acid on superoxide anion and elastase release in human neutrophils through multiple mechanisms. Eur J Pharmacol 586:332–339. doi:10.1016/j.ejphar.2008.02.041

    Article  CAS  Google Scholar 

  • Chen YL, Lan YH, Hsieh PW, Wu CC, Chen SL, Yen CT, Chang FR, Hung WC, Wu YC (2008) Bioactive membrane diterpenoids of Anisomeles indica. J Nat Prod 71:1207–1212. doi:10.1021/np800147z

    Article  CAS  Google Scholar 

  • Chiang LC, Ng LT, Chiang W, Chang MY, Lin CC (2003) Immunomodulatory activities of flavonoids, monoterpenoids, triterpenoids, iridoid glycosides and phenolic compounds of Plantago species. Planta Med 69:600–604. doi:10.1055/s-2003-41113

    Article  CAS  Google Scholar 

  • Cho KM, Hong SY, Lee SM, Kim YH, Kahng GG, Lim YP, Kim H, Yun HD (2007) Endophytic bacterial communities in ginseng and their antifungal activity against pathogens. Microb Ecol 54:341–351. doi:10.1007/s00248-007-9208-3

    Article  CAS  Google Scholar 

  • Choi SY, Jung SH, Lee HS, Park KW, Yun BS, Lee KW (2008) Glycation inhibitory activity and the identification of an active compound in Plantago asiatica extract. Phytother Res 22:323–329. doi:10.1002/ptr.2316

    Article  CAS  Google Scholar 

  • Davis RA, Longden J, Avery VM, Healy PC (2008) The isolation, structure determination and cytotoxicity of the new fungal metabolite, trichodermamide C. Bioorg Med Chem Lett 18:2836–2839. doi:10.1016/j.bmcl.2008.03.090

    Article  CAS  Google Scholar 

  • Eyberger AL, Dondapati R, Porter JR (2006) Endophyte fungal isolates from Podophyllum peltatum produce podophyllotoxin. J Nat Prod 69:1121–1124. doi:10.1021/np060174f

    Article  CAS  Google Scholar 

  • Ferreres F, Pereira DM, Valentão P, Andrade PB, Seabra RM, Sottomayor M (2008) New phenolic compounds and antioxidant potential of Catharanthus roseus. J Agric Food Chem 56:9967–9974. doi:10.1021/jf8022723

    Article  Google Scholar 

  • Ge HM, Shen Y, Zhu CH, Tan SH, Ding H, Song YC, Tan RX (2008) Penicidones A-C, three cytotoxic alkaloidal metabolites of an endophytic Penicillium sp. Phytochemistry 69:571–576. doi:10.1016/j.phytochem.2007.07.014

    Article  CAS  Google Scholar 

  • Gopalakrishnan C, Dhananjayan R, Kameswaran L (1976) Studies on the pharmacological actions of Cardiospermum halicacabum. Indian J Physiol Pharmacol 20:203–206

    CAS  Google Scholar 

  • Guimaraes DO, Borges WS, Kawano CY, Ribeiro PH, Goldman GH, Nomizo A, Thiemann OH, Oliva G, Lopes NP, Pupo MT (2008) Biological activities from extracts of endophytic fugi isolated from Viguiera arenaria and Tithonia diversifolia. FEMS Immunol Med Microbiol 52:134–144

    Article  CAS  Google Scholar 

  • Gunatilaka AAL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 69:509–526. doi:10.1021/np058128n

    Article  CAS  Google Scholar 

  • Hashidoko Y (2005) Ecochemical studies of interrelationships between epiphytic bacteria and host plants via secondary metabolites. Biosci Biotechnol Biochem 69:1427–1441. doi:10.1271/bbb.69.1427

    Article  CAS  Google Scholar 

  • Hiraishi A, Furuhata K, Matsumoto A, Koike KA, Fukuyama M, Tabuchi K (1995) Phenotypic and genetic diversity of chlorine-resistant Methylobacterium strains isolated from various environments. Appl Environ Microbiol 61:2099–2107

    CAS  Google Scholar 

  • Hsieh PW, Chang FR, Wu CC, Wu KY, Li CM, Chen SL, Wu YC (2004) New cytotoxic cyclic-peptides and dianthramide from Dianthus superbus. J Nat Prod 67:1522–1527. doi:10.1021/np040036v

    Article  CAS  Google Scholar 

  • Hsieh PW, Hwang TL, Wu CC, Chiang SZ, Wu CI, Wu YC (2007) The evaluation and structure activities relationships of 2-Benzoylamino-Benzoic esters and their analogues as anti-inflammatory and anti-platelet aggregation agents. Bioorg Med Chem Lett 17:1812–1817. doi:10.1016/j.bmcl.2006.12.038

    Article  CAS  Google Scholar 

  • Hsieh PW, Chiang SZ, Wu CC, Lo YC, Shih YT, Wu YC (2008) Synthesis and anti-platelet evaluation of 2-Benzoylaminobenzoate analogs. Bioorg Med Chem 16:5803–5814. doi:10.1016/j.bmc.2008.03.071

    Article  CAS  Google Scholar 

  • Jayatilake GS, Thornton MP, Leonard AC, Grimwade JE, Baker BJ (1996) Metabolites from an antarctic sponge-associated bacterium, Pseudomonas aeruginosa. J Nat Prod 59:293–296. doi:10.1021/np960095b

    Article  CAS  Google Scholar 

  • Jiao RH, Xu S, Liu JY, Ge HM, Ding H, Xu C, Zhu HL, Tan RX (2006) Cheitominine, a cytotoxic alkaloid produced by endophytic Chaetomium sp. IFB-E015. Org Lett 8:5709–5712. doi:10.1021/ol062257t

    Article  CAS  Google Scholar 

  • Kim SY, Kim SH, Shin HY, Lim JP, Chae BS, Park JS, Hong SG, Kim MS, Jo DG, Park WH, Shin TY (2007) Effects of Prunella vulgaris on mast cell-mediated allergic reaction and inflammatory cytokine production. Exp Biol Med 232:921–926

    CAS  Google Scholar 

  • Kinjo J, Furusawa J, Baba J, Takeshita T, Yamasaki M, Nohara T (1987) Studies on the constituents of Pueraria lobata. III. Isoflavonoids and relateed compounds in the roots and the voluble stems. Chem Pharm Bull (Tokyo) 35:4846–4850

    CAS  Google Scholar 

  • Kour A, Shawl AS, Rehman S, Sultan P, Qazi PH, Suden P, Khajuria RK, Verma V (2008) Isolation and identification of an endophytic strain of Fusarium oxysporum producing podophyllotoxin from Juniperus recurva. World J Microbiol Biotechnol 24:1115–1121. doi:10.1007/s11274-007-9582-5

    Article  CAS  Google Scholar 

  • Kurihara T, Kikuchi M (1976) Studies on the constituents of flowers. VI. On the components of the flower of Pueraria thubergiana Benth. Yakugaku Zasshi 96:1486–1488

    CAS  Google Scholar 

  • Kusari S, Zühlke S, Spiteller M (2009) An endophytic fungus from Camptotheca acuminata that produces camptothecin and analogues. J Nat Prod 72:2–7. doi:10.1021/np800455b

    Article  CAS  Google Scholar 

  • Lacava PT, Li W, Araujo WL, Azevedo JL, Hartung JS (2007) The endophyte Curtobacterium flaccumfaciens reduces symptoms caused by Xylella fastidiosa in Catharanthus roseus. J Microbiol 45:388–393

    CAS  Google Scholar 

  • Lan YH, Chang FR, Yu JH, Yang YL, Chang YL, Lee SJ, Wu YC (2003) Cytotoxic styrylpyrones from Goniothalamus amuyon. J Nat Prod 66:487–490. doi:10.1021/np020441r

    Article  CAS  Google Scholar 

  • Lan YH, Chang FR, Yang YL, Wu YC (2006) New constituents from stem of Goniothalamus amuyon. Chem Pharm Bull (Tokyo) 54:1040–1043. doi:10.1248/cpb.54.1040

    Article  CAS  Google Scholar 

  • Lee SH, Kim HK, Seo JM, Kang HM, Kim JH, Son KH, Lee H, Kwon BM (2002) Arteminolides B, C, and D, new inhibitor of farnesyl protein transferase from Artemisia argyi. J Org Chem 67:7670–7675. doi:10.1021/jo020299z

    Article  CAS  Google Scholar 

  • Liaw CC, Yang YL, Chen M, Chang FR, Chen SL, Wu SH, Wu YC (2008) Mono-tetrahydrofuran annonaceous acetogenins from Annona squamosa as cytotoxic agents and calcium ion chelators. J Nat Prod 71:764–771. doi:10.1021/np0704957

    Article  CAS  Google Scholar 

  • Malech HL, Gallin JI (1987) Current concepts: immunology. Neutrophils in human diseases. N Engl J Med 317:687–694

    CAS  Google Scholar 

  • Muko KN, Ohiri FC (2000) A priliminary study on the anti-inflammatory properties of Emilia sonchifolia leaf extracts. Firoterapia 71:65–68. doi:10.1016/S0367-326X(99)00123-9

    Article  CAS  Google Scholar 

  • Nadkarni KM (1976) Indian materia medica. Popular Book Depot, Bombay, p 271

    Google Scholar 

  • Parker KA, Spero DM, Koziski KA (1987) Evaluation of some preparations of trialkoxyphthalic acid derivatives. J Org Chem 52:183–188. doi:10.1021/jo00378a005

    Article  CAS  Google Scholar 

  • Patrick GL (2005) An introduction to medicinal chemistry, 3rd edn. Oxford University Press Inc, New York

    Google Scholar 

  • Pettit GR, Du J, Pettit RK, Richert LA, Hogan F, Mukku VJ, Hoard MS (2006) Antineoplastic agents. 554. The manitoba bacterium Streptomyces sp. J Nat Prod 69:804–806. doi:10.1021/np058087v

    Article  CAS  Google Scholar 

  • Phongpaichit S, Nikom J, Rungjindamai N, Sakayaroj J, Hutadilok-Towatana N, Rukachaisirikul V, Kirtikara K (2007) Biological activities of extracts from endophytic fungi isolated from Garcinia plants. FEMS Immunol Med Microbiol 51:517–525. doi:10.1111/j.1574-695X.2007.00331.x

    Article  CAS  Google Scholar 

  • Punturee K, Wild CP, Vinitketkumneun U (2004) Thai medicinal plants modulate nitric oxide and tumor necrosis factor-α in J774.2 mouse macrophages. J Ethnopharmacol 95:183–189. doi:10.1016/j.jep.2004.06.019

    Article  Google Scholar 

  • Puri SC, Amna T, Khajuria A, Gupta A, Arora R, Spiteller M, Qazi GN (2005) Immunomodulatory activity of an extract of the novel fungal endophyte Entrophospora infrequens isolated from Nothapodytes foetida (Wight) Sleumer. Acta Microbiol Immunol Hung 54:237–260. doi:10.1556/AMicr.54.2007.3.2

    Article  CAS  Google Scholar 

  • Roos D, van Bruggen R, Meischl C (2003) Oxidative killing of microbes by neutrophils. Microbes Infect 5:1307–1315. doi:10.1016/j.micinf.2003.09.009

    Article  CAS  Google Scholar 

  • Rukachaisirikul V, Kaeobamrung J, Panwiriyarat W, Saitai P, Sukpodma Y, Phongpaichit S, Sakayaroj J (2007) A new pyrone derivative from the entophytic fungus Penicillium paxilli PSU-A71. Chem Pharm Bull (Tokyo) 55:1383–1384. doi:10.1248/cpb.55.1383

    Article  CAS  Google Scholar 

  • Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9. doi:10.1111/j.1574-6968.2007.00918.x

    Article  CAS  Google Scholar 

  • Sadique J, Chandra T, Thenmozhi V, Elango V (1987) Biochemical modes of action of Cassia occidentalis and Cardiospermum halicacabum in inflammation. J Ethnopharmacol 19:201–205. doi:10.1016/0378-8741(87)90042-0

    Article  CAS  Google Scholar 

  • Seo JM, Kang HM, Son KH, Kim JH, Lee CW, Kim HM, Chang SI, Kwon BM (2003) Antitumor activity of flavones isolated from Artemisia argyi. Planta Med 69:218–222. doi:10.1055/s-2003-38486

    Article  CAS  Google Scholar 

  • Sheeba MS, Asha VV (2006) Effect of Cardiospermum halicacabum on ethanol-induced gastric ulcers in rate. J Ethnopharmacol 106:105–110. doi:10.1016/j.jep.2005.12.009

    Article  CAS  Google Scholar 

  • Shiono Y, Tsuchinari M, Shimanuki K, Miyajima T, Murayama T, Koseki T, Laatsch H, Funakoshi T, Takanami K, Suzuki K (2007) Fusaristatins A and B, two new cyclic lipopeptides from an endophytic Fusarium sp. J Antibiot 60:309–316. doi:10.1038/ja.2007.39

    Article  CAS  Google Scholar 

  • Shylesh BS, Padikkala J (2000) In vitro cytotoxic and antitumor property of Emilia sonchifolia (L.) DC in mice. J Ethnopharmacol 73:496–500. doi:10.1016/S0378-8741(00)00317-2

    Article  Google Scholar 

  • Siripong P, Yahuafai J, Shimizu K, Ichikawa K, Yonezawa S, Asai T, Kanokmedakul K, Ruchirawat S, Oku Naoto (2006) Antitumor activity of liposomal naphthoquinone esters isolated from Thai medicinal plant: Rhinacanthus nasutus Kurz. Biol Pharm Bull 29:2279–2283. doi:10.1248/bpb.29.2279

    Article  CAS  Google Scholar 

  • Stierle A, Strobel G, Stierle D (1993) Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science 260:214–216. doi:10.1126/science.8097061

    Article  CAS  Google Scholar 

  • Takaya Y, Furukawa T, Miura S, Akutagawa T, Hotta Y, Ishikawa N, Niwa M (2007) Antioxidant constituents in distillation residue of Awamori spirits. J Agric Food Chem 55:75–79. doi:10.1021/jf062029d

    Article  CAS  Google Scholar 

  • Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459. doi:10.1039/b100918o

    Article  CAS  Google Scholar 

  • Tremaroli V, Workentine ML, Weljie AM, Vogel HJ, Ceri H, Viti C, Tatti E, Zhang P, Hynes AP, Turner RJ, Zannoni D (2009) Metabolomic investigation of the bacterial response to a metal challenge. Appl Environ Microbiol 75:719–728. doi:10.1128/AEM.01771-08

    Article  CAS  Google Scholar 

  • Trotsenko YA, Ivanova EG, Doronina NV (2001) Aerobic methylotrophic bacteria as phytosymbionts. Mikrobiologiya 70:725–736

    Google Scholar 

  • Van der Heijden R, Jacobs DI, Snoeijer W, Hallard D, Verpoorte R (2004) The Catharathus alkaloids: pharmacognosy and biotechnology. Curr Med Chem 11:607–628. doi:10.2174/0929867043455846

    Article  Google Scholar 

  • White DC, Sutton SD, Ringelberg DB (1996) The genus Sphingomonas: physiology and ecology. Curr Opin Biotechnol 7:301–306. doi:10.1016/S0958-1669(96)80034-6

    Article  CAS  Google Scholar 

  • Witko-Sarsat V, Rieu P, Descamps-Latscha B, Lesavre P, Halbwachs-Mecarelli L (2000) Neutrophils: molecules, functions and pathophysiological aspects. Lab Invest 80:617–653

    CAS  Google Scholar 

  • Wu TS, Hsu HC, Wu PL, Teng CM, Wu YC (1998) Rhinacathin-Q, a naphthoquinone from Rhinacanthus nasutus and its biological activity. Phytochemistry 49:2001–2003. doi:10.1016/S0031-9422(98)00425-7

    Article  CAS  Google Scholar 

  • Yang YL, Hua KF, Chuang PH, Wu SH, Wu KY, Chang FR, Wu YC (2008) New cyclic peptides from the seeds of Annona squamosa L. and their anti-inflammatory activities. J Agric Food Chem 56:386–392. doi:10.1021/jf072594w

    Article  CAS  Google Scholar 

  • Zhang S, Zhao M, Bai L, Hasegawa T, Wang J, Wang L, Xue H, Deng Q, Xing F, Bai Y, Sakai J, Bai J, Koyanagi R, Tsukumo Y, Kataoka T, Nagai K, Hirose K, Ando M (2006) Bioactive guainaolides from Siyekucai (Ixeris chinensis). J Nat Prod 69:1425–1428. doi:10.1021/np068015j

    Article  CAS  Google Scholar 

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Acknowledgments

We gratefully acknowledge financial support for this project from the Kaohsiung Medical University (Q-9505) and Chang Gung University (CMRPD-170431). The authors also thank the Bioresource Collection and Research Centre for support in identification of endophytes.

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Hsieh, PW., Hsu, LC., Lai, CH. et al. Evaluation of the bioactivities of extracts of endophytes isolated from Taiwanese herbal plants. World J Microbiol Biotechnol 25, 1461–1469 (2009). https://doi.org/10.1007/s11274-009-0036-0

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