Endophytic fungi found in association with Smallanthus sonchifolius (Asteraceae) as resourceful producers of cytotoxic bioactive natural products

Journal of Basic Microbiology

Volumn 49, Issue 2, 2009, Pages 142-151

  Gallo, Margareth B C ^a   Chagas, Fernanda O ^a   Almeida, Marília O ^a   Macedo, Cláudia C ^a   Cavalcanti, Bruno C ^b   Barros, Francisco W A ^b   De Moraes, Manoel O ^b   Costa Lotufo, Letícia V ^b   Pessoa, Cláudia ^b   Bastos, Jairo K ^a   Pupo, Mônica T ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

Author keywords

Aphidicolin; Isocoumarin; Nigrospora sphaerica; Phoma betae; Yacon

Indexed keywords

8 HYDROXY 6 METHOXY 3 METHYLISOCOUMARIN; 8-HYDROXY-6-METHOXY-3-METHYLISOCOUMARIN; ABIETANE DERIVATIVE; ANTINEOPLASTIC AGENT; CHOLEST 4 EN 3 ONE; ERGOSTA 4,6,8(14),22 TETRAEN 3 ONE; ERGOSTA-4,6,8(14),22-TETRAEN-3-ONE; ISOCOUMARIN DERIVATIVE;

ARTICLE; ASCOMYCETES; ASTERACEAE; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG DEVELOPMENT; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; ASCOMYCOTA; ASTERACEAE; CELL LINE, TUMOR; CHOLESTENONES; DITERPENES, ABIETANE; DRUG DISCOVERY; HUMANS; ISOCOUMARINS; MOLECULAR STRUCTURE;

ASTERACEAE; FUNGI; NIGROSPORA SPHAERICA; PHOMA BETAE; POLYMNIA SONCHIFOLIA; SMALLANTHUS SONCHIFOLIUS;

EID: 65349180144     PISSN: 0233111X     EISSN: 15214028     Source Type: Journal    
DOI: 10.1002/jobm.200800093     Document Type: Article

References (56)

1. Valentová, K., Truong, N.T., Moncion, A., Waziers, I. and Ulrichová, J., 2007. Induction of glucokinase mRNA by dietary phenolic compounds in rat liver cells in vitro. J. Agric. Food Chem., 55, 7726-7731.
2. Schorr, K., Merfort, I. and Costa, F.B., 2007. A novel dimeric melampolide and further terpenoids from Smallanthus sonchifolius (Asteraceae) and the inhibition of the transcription factor NF-kappa B. Nat. Prod. Communic., 4, 367-374.
3. Lin, F., Morifumi, H. and Kodama, O., 2003. Purification and identification of antimicrobial sesquiterpene lactones from Yacon (Smallanthus sonchifolius) leaves. Biosci. Biotechnol. Biochem., 67, 2154-2159.
4. Neves, V.A. and Silva, M.A., 2007. Polyphenol oxidase from Yacon Roots (Smallanthus sonchifolius). J. Agric. Food Chem., 55, 2424-2430.
5. Valentová, K., Lebeda, A., Doležalová, I., Jirovskỳ, D., Simonovska, B., Vovk, I., Kosina, P., Gasmanová, N., Dziechciarková, M. and Ulrichová, J., 2006. The biological and chemical variability of Yacon. J. Agric. Food Chem., 54, 1347-1352.
6. Genta, S.B., Cabrera, W.M., Grau, A. and Sánchez, S.S., 2005. Subchronic 4-month oral toxicity study of dried Smallanthus sonchifolius (yacon) roots as a diet supplement in rats. Food Chem. Toxicol., 43, 1657-1665.
7. Pedreschi, R., Campos, D., Noratto, G., Chirinos, R. and Cisneros-Zevallos, L., 2003. Andean yacon root (Smallanthus sonchifolius Poepp. Endl.) fructooligosaccharides as a potential novel source of prebiotics. J. Agric. Food Chem., 51, 5278-5284.
8. Gallo, M.B.C., Guimarães, D.O., Momesso, L.S. and Pupo, M.T., 2008. Natural Products from endophytic fungi. In: Saikai, R., Bezbaruah, R.L. and Bora, T.C. (eds.), Microbial Biotechnology, pp. 139-168. New India Publishing Agency, New Delhi, India.
9. Firáková, S., Šturdíková, M. and Múčková, M., 2007. Bioactive secondary metabolites produced by microorganisms associated with plants. Biologia, 62, 251 -257.
10. Guimarães, D.O., Borges, W.S., Kawano, C.Y., Ribeiro, P.H., Goldman, G.H., Nomizo, A., Thiemann, O.H., Lopes, N.P. and Pupo, M.T., 2008. Biological activities from extracts of endophytic fungi isolated from Viguiera arenaria and Tithonia diversifolia. FEMS Immunol. Med. Microbiol., 52, 134-144.
11. Borges, K.B., Borges, W.S., Pupo, M.T. and Bonato, P.S., 2008. Stereoselective analysis of thioridazine-2-sulfoxide and thioridazine-5- sulfoxide: An investigation of rac-thio-ridazine biotransformation by some endophytic fungi. J. Pharm. Biomed. Anal., 46, 945-952.
12. Borges, K.B., Borges, W.S., Pupo, M.T. and Bonato, P.S., 2007. Endophytic fungi as models for the stereoselective biotransformation of thioridazide. Appl. Microbiol. Biotechnol., 77, 669 -674.
13. Borges, W.S. and Pupo, M.T., 2006. Novel anthraquinone derivatives produced by Phoma sorghina, an endophyte found in association with the medicinal plant Tithonia diversifolia (Asteraceae). J. Braz. Chem. Soc., 17, 929-934.
14. Jackson, M., Karwowski, J.P., Humphrey, P.E., Kohl, W.L., Barlow, G.J. and Tanaka, S.K., 1993. Calbistrins, novel an-tifungal agents produced by Penicillium restrictum. 1. Production, taxonomy of the producing organism and biological activity. J. Antibiotics, 46, 34- 38.
15. Atlas, R.M., 1995. Handbook of Microbiological Media for the Examination of Food, 310 pp. CRC Press, Boca Raton.
16. Mosman, T., 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 65, 55-63.
17. Pohlit, A.M., Tigre, R.F., Cavalcanti, B.C., Moraes, M.O., Costa- Lotufo, L.V., Moraes, M.E.A., Santos, E.V.M., Morais, S.K.R., Nunomura, S.M. and Pessoa, C., 2007. Cytotoxic fractions from the leaves of Tachia grandiflora. Pharm. Biol., 45, 429-433.
18. Gannibal, P.B., Klemsdal, S.S. and Levitin, M.M., 2007. AFPL analysis of Russian Alternaria tenuissima populations from wheat kernels and other hosts. Eur. J. Plant Pathol., 119, 175-182.
19. Chrysayi-Tokousbalides, M. and Kastanias, M.A., 2003. Cynodontin: a fungal metabolite with antifungal properties. J. Agric. Food Chem., 51, 4920-4923.
20. Garcia-Pajón, C.M. and Collado, I.G., 2003. Secondary metabolites isolated from Colletotrichum species. Nat. Prod. Rep., 20, 426- 431.
21. Gond, S.K., Verma, V.C., Kumar, A., Kumar, V. and Kharwar, R.N., 2007. Study of endophytic fungal community from different parts of Aegle marmelos Correae (Rutaceae) from Varanasi (India). World J. Microbiol. Biotechnol., 23, 1371-1375.
22. Verma, V.C., Gond, S.K., Kumar, A., Kharvar, R.N. and Strobel, G., 2007. The endophytic mycoflora of bark, leaf, and stem tissues of Azadirachta indica A. Juss (Neem) from Varanasi (India). Microbial Ecol., 54, 119-125.
23. White, I.R. and Backhouse, D., 2007. Comparison of fungal endophyte communities in the invasive panicoid grass Hyparrhenia hirta and the native grass Bothriochloa macra. Aust. J. Bot., 55, 178-185.
24. Raviraja, N.S., Maria, G.L. and Sridhar, K.R., 2006. Antimicrobial evaluation of endophytic fungi inhabiting medicinal plants of the Western Ghats of India. Eng. Life Sci., 5, 515-520.
25. O'Callaghan, M., Gerard, E.M., Waipara, N.W., Young, S.D., Glare, T.R., Barrell, P.J. and Conner, A.J., 2004. Mic-robial communities of Solanum tuberosum and magainin-producing transgenic lines. Plant Soil, 266, 47 - 56.
26. Liu, J.Y., Song, Y.C., Zhang, Z., Wang, L., Guo, Z.J., Zou, W.X. and Tan, R.X., 2004. Aspergillus fumigatus CY018, an endophytic fungus in Cynodon dactylon as a versatile producer of new and bioactive metabolites. J. Biotechnol., 114, 279-287.
27. Kogel, K., Franken, P. and Hückelhoven, R., 2006. Endo-phyte or parasite - What decides? Curr. Opin. Plant Biol., 9, 358-363.
28. Katyal, P., Khanna, P.K. and Kapoor, S., 2006. Toxicity of fungicides against Agaricus bisporus and its mycopathogens. J. Mycol. Plant Pathol., 36, 296 - 298.
29. Fudo, R., Ando, T., Sato, S., Kameyama, T. and Yamanaka, S., 1997. Isolation of isoeugenitin as a fruiting body in-ducer for Stigmatella aurantiaca from a soil fungus Papulaspora sp. Biosci. Biotechnol. Biochem., 61, 183-184.
30. Bayman, P., Angulo-Sandoval, P., Báez-Ortiz, Z. and Lodge, D.J., 1998. Distribution and dispersal of Xylaria endophytes in two tree species in Puerto Rico. Mycol. Res., 102, 944-948.
31. Hu, K., Tan, F., Tang, K., Zhu, S. and Wang, W., 2006. Isolation and screening of endophytic fungi synthesizing taxol from Taxus chinensis var. mairei. Ziran Kexueban, 31, 134-137.
32. Bussaban, B., Lumyong, S., Lumyong, P., McKenzie, E.H.C. and Hyde, K.D., 2001. Endophytic fungi from Amomum siamense. Can. J. Microbiol., 47, 943- 948.
33. Weber, H.A. and Gloer, J.B., 1988. Interference competition among natural fungal competitors: an antifungal metabolite from the coprophilous fungus Preussia fleischhakii. J. Nat. Prod., 51, 879-883.
34. Johnson, J.H., Meyers, E., O'Sullivan, J., Phillipson, D.W., Robinson, G., Trejo, W.H. and Wells, J.S., 1989. Culpin, a novel hydroquinone antibiotic of fungal origin. J. Antibiotics, 42, 1515-1517.
35. Bok, J.W., Lermer, L., Chilton, J., Klingeman, H.G. and Towers, G.H.N., 1999. Antitumor sterols from the mycelia of Cordyceps sinensis. Phytochemistry, 51, 891-898.
36. Tian, G., Li, B., Wang, W., Wang, C. and Gong, K., 2005. Components of the essential oil of Isidon henryi (hemsi) Kudo. Xibei Zhiwu Xuebao, 25, 2543-2548.
37. Rizzo, C.J. and Smith, A.B., 1991. Aphidicolin synthetic studies: a stereocontrolled end game. J. Chem. Soc. Perkin Trans. I, 969-979.
38. Palin, A.H., Critcher, R., Fitzgerald, D.J., Anderson, J.N. and Farr, C.J., 1998. Direct cloning and analysis of DNA sequences from a region of the Chinese hamster genome associated with aphidicolin-sensitivity fragility. J. Cell Sci., 111, 1623-1634.
39. Michaelis, M., Zimmer, A., Handjou, N., Cinatl, J. and Cinatl, J.Jr., 2005. Increased systemic efficacy of aphidico-lin encapsulated in liposomes. Oncol. Rep., 13, 157 - 160.
40. Oikawa, H., Toshima, H., Ohashi, S., König, W.A., Kenmoku, H. and Sassa, T., 2001. Diversity of diterpene hydrocarbons in fungus Phoma betae. Tetrahedron Lett., 42, 2329-2332.
41. Ichihara, A., Oikawa, H., Hayashi, K., Hashimoto, M., Sakamura, S. and Sakai, R., 1984. 3-deoxyaphidicolin and aphidicolin analogues as phytotoxins from Phoma betae. Agric. Biol. Chem., 48, 1687-1689.
42. Chenot, E., Bernardi, D., Comel, A. and Kirsh, G., 2007. Preparation of monoalkylterephthalates: an overview. Synth. Commun., 37, 483-490.
43. Fujimoto, H., Nakamura, E., Okuyama, E. and Ishibashi, M., 2004. Six immunosuppressive features from an Ascomycete, Zopfiella longicauda, found in a screening study monitored by immunomodulatory activity. Chem. Pharm. Bull., 52, 1005-1008.
44. Kumagai, H., Amemiya, M., Naganawa, H., Sawa, T., Ishizuka, M. and Takeuchi, T., 1994. Biosynthesis of antitumor antibiotic, cytogenin. J. Antibiotics, 47, 440-446.
45. Chen, J.-J., Chou, E.-T., Duh, C.-Y., Yang, S.-Z. and Chen, I.-S., 2006. New cytotoxic tetrahydrofuran- and dihydro-furan-type lignans from the stem bark of Beilschmiedia tsangii. Planta Med., 72, 351-357.
46. Kwon, H.C., Zee, S.D., Cho, S.Y., Choi, S.U. and Lee, K.R., 2002. Cytotoxic ergosterols from Paecilomyces sp. J300. Arch. Pharmacol., Res., 25, 851 -855.
47. Yuan, H., Junker, B., Helquist, P. and Taylor, R.E., 2004. Synthesis of anti-angiogenic isocoumarins. Curr. Org. Chem., 1, 1-9.
48. Agata, N., Nogi, H., Milhollen, M., Kharbanda, S. and Kufe, D.W., 2004. 2-(8-hydroxy-6-methoxy-1-oxo-1H-2-benzopy-ran-3-yl)propionic acid, a small molecule isocoumarin, potentiates dexamethasone-induced apoptosis of human multiple myeloma cells. Cancer Res., 64, 8512-8516.
49. Salloum, R.M., Jaskowiak, N.T., Mauceri, H.J., Seetharam, S., Beckett, M.A., Koons, A.M., Hari, D.M., Gupta, V.K., Reimer, C., Kalluri, R., Posner, M.C., Hellman, S., Kufe, D.W. and Weichselbaum, R.R., 2000. NM-3, an isocouma-rin, increases the antitumor effects of radiotherapy without toxicity. Cancer Res., 60, 6958 -6963.
50. Inoue, A., Tamogami, S., Kato, H., Nakazato, Y., Akiyama, M., Kodama, O., Akatsuka, T. and Hashidoko, Y., 1995. Antifungal melampolides from leaf extracts of Smallanthus sonchifolius. Phytochemistry, 39, 845 - 848.
51. Kakuta, H., Seiki, T., Hashidoko, Y. and Mizutani, J., 1992. Ent-kaurenic acid and its related compounds from glandular trichome exudate and leaf extracts of Polymnia sonchifolia. Biosci. Biotech. Biochem., 56, 1562-1564.
52. Oikawa, H., Nakamura, K., Toshima, H., Tayamasu, T. and Sassa, T., 2002. Proposed mechanism for the reaction catalyzed by a diterpene cyclase, aphidicolan-16-beta-ol synthase: experimental results on biomimetic cyclization and examination of the cyclization pathway by ab initio calculations. J. Am. Chem. Soc., 124, 9145-9153.
53. Yao, Q., 2007. Biosynthetic Studies of Fungal Diterpenes Antibiotics. Master Dissertation. Oregon State University. 203 pp.
54. Perello, A., Simon, M.R. and Arambarri, A.M., 2002. Interactions between foliar pathogens and the saprophytic microflora of the wheat (Triticum aestivum L.) phylloplane. J. Phytophatol., 150, 232-243.
55. Szewczuk, V., Kita, W., Jarosz, B., Truszkowska, W. and Siewinsk, A., 1991. Metabolites of Nigrospora - growth inhibition of some phytopathogenic fungi by organic extracts from Nigrospora orizae (Berkeley and Broome) Petch. J. Basic Microbiol., 31, 69-73.
56. Kim, J.-C., Choi, G.J., Park, J.-H., Kim, H.T. and Cho, K.Y., 2001. Activity against plant pathogenic fungi of phomo-lactone isolated from Nigrospora sphaerica. Pest Manag. Sci., 57, 554-559.