Trypacidin, a spore-borne toxin from Aspergillus fumigatus, is cytotoxic to lung cells

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Gauthier, Thierry ^a   Wang, Xiaodi ^a   Dos Santos, Joice ^a   Fysikopoulos, Athanasios ^a   Tadrist, Souria ^a   Canlet, Cécile ^a   Artigot, Marie Pierre ^a   Loiseau, Nicolas ^a   Oswald, Isabelle P ^a   Puel, Olivier ^a  

^a TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; FUMAGACLAVINE A; FUMAGILLIN; HELVOLIC ACID; MONOMETHYLSULOCHRIN; QUESTIN; REACTIVE OXYGEN METABOLITE; TRYPACIDIN; UNCLASSIFIED DRUG; VERRUCULOGEN; MYCOTOXIN;

APOPTOSIS; ARTICLE; ASPERGILLUS FUMIGATUS; BRONCHUS MUCOSA; CANCER CELL CULTURE; CELL CYCLE; CELL CYCLE G0 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL DEATH; CELL FRACTIONATION; CELL VIABILITY; CONIDIUM; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; DOSE RESPONSE; EPITHELIUM CELL; FLOW CYTOMETRY; FUNGAL STRAIN; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; LUNG ALVEOLUS CELL; LUNG ASPERGILLOSIS; MASS SPECTROMETRY; MITOCHONDRIAL MEMBRANE POTENTIAL; NUCLEAR MAGNETIC RESONANCE; OXIDATIVE STRESS; TOXIN STRUCTURE; ULTRAVIOLET SPECTROSCOPY; BRONCHUS; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; FUNGUS SPORE; LUNG DISEASE; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY;

ASPERGILLUS FUMIGATUS;

APOPTOSIS; ASPERGILLUS FUMIGATUS; BRONCHI; CELL LINE; EPITHELIAL CELLS; HUMANS; LUNG DISEASES; MOLECULAR STRUCTURE; MYCOTOXINS; OXIDATIVE STRESS; SPORES, FUNGAL;

EID: 84863045978     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029906     Document Type: Article

References (49)

1. Samson RA, Flannigan B, Flannigan ME, Verhoeff AP, Adan OCG, et al. (1994) Health implications of fungi in indoor air environments. Air quality monographs, vol. 2. Elsevier Science B.V pp. 531-538.
2. Zielinska-Jankiewicz K, Kozajda A, Piotrowska M, Szadkowska-Stanczyk I, (2008) Microbiological contamination with moulds in work environment in libraries and archive storage facilities. Ann Agric Environ Med 15: 71-78.
3. Matysik S, Herbarth O, Mueller A, (2008) Determination of volatile metabolites originating from mould growth on wall paper and synthetic media. J Microbiol Methods 75: 182-187.
4. Eduard W, (2009) Fungal spores: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting. Crit Rev Toxicol 39: 799-864.
5. Araujo R, Amorim A, Gusmao L, (2010) Genetic diversity of Aspergillus fumigatus in indoor hospital environments. Med Mycol 48: 832-838.
6. Karvala K, Nordman H, Luukkonen R, Nykyri E, Lappalainen S, et al. (2008) Occupational rhinitis in damp and moldy workplaces. Am J Rhinol 22: 457-462.
7. Latge JP, (1999) Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12: 310-350.
8. Arendrup MC, O'driscoll BR, Petersen E, Denning DW, (2006) Acute pulmonary aspergillosis in immunocompetent subjects after exposure to bark chippings. Scand J Infect Dis 38: 945-949.
9. Batard E, Renaudin K, Morin O, Desjars P, Germaud P, (2003) Fatal acute granulomatous pulmonary aspergillosis in a healthy subject after inhalation of vegetal dust. Eur J Clin Microbiol Infect Dis 22: 357-359.
10. Russell K, Broadbridge C, Murray S, Waghorn D, Mahoney A, (2008) Gardening can seriously damage your health. Lancet 371: 2056.
11. Dagenais, TR, Keller NP, (2009) Pathogenesis of Aspergillus fumigatus in Invasive Aspergillosis. Clin Microbiol Rev 22: 447-465.
12. Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, et al. (2005) Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438: 1151-1156.
13. Perrin RM, Fedorova ND, Bok JW, Cramer RA, Wortman JR, et al. (2007) Transcriptional regulation of chemical diversity in Aspergillus fumigatus by LaeA. PLoS Pathog 3: 508-517.
14. Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, et al. (2010) SMURF: Genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol 47: 736-741.
15. Frisvad JC, Rank C, Nielsen KF, Larsen TO, (2009) Metabolomics of Aspergillus fumigatus. Med Mycol 47: S53-71.
16. Lewis RE, Wiederhold NP, Chi J, Han XY, Komanduri KV, et al. (2005) Detection of gliotoxin in experimental and human aspergillosis. Infect Immun 73: 635-637.
17. Kwon-Chung KJ, Sugui JA, (2009) What do we know about the role of gliotoxin in the pathobiology of Aspergillus fumigatus? Med Mycol 47: S97-103.
18. Mitchell CG, Slight J, Donaldson K, (1997) Diffusible component from the spore surface of the fungus Aspergillus fumigatus which inhibits the macrophage oxidative burst is distinct from gliotoxin and other hyphal toxins. Thorax 52: 796-801.
19. Panaccione DG, Coyle CM, (2005) Abundant respirable ergot alkaloids from the common airborne fungus Aspergillus fumigatus. Appl Environ Microbiol 71: 3106-3111.
20. Fischer G, Müller T, Schwalbe R, Ostrowski R, Dott W, (2000) Species-specific profiles of mycotoxins produced in cultures and associated with conidia of airborne fungi derived from biowaste. Int J Hyg Environ Health 203: 105-116.
21. Fischer G, Müller T, Ostrowski R, Dott W, (1999) Mycotoxins of Aspergillus fumigatus in pure culture and in native bioaerosols from compost facilities. Chemosphere 38: 1745-1755.
22. Balan J, Ebringer L, Nemec P, Kovacs S, Dobias J, (1963) Antiprotozoal antibiotics. Isolation and characterization of trypacidin, a new antibiotic, active against trypanosoma cruzi and toxoplasma gondii. J Antibiot 16: 157-160.
23. Turner WB, (1965) The production of trypacidin and monomethylsulochrin by Aspergillus fumigatus. J Chem Soc Perkin 1: 6658-6659.
24. Balan J, Kjaera A, Kovacs S, Shapiro RH, (1965) The structure of trypacidin. Acta Chem Scand 19: 528-530.
25. Khoufache K, Puel O, Loiseau N, Delaforge M, Rivollet, et al. (2007) Verruculogen associated with Aspergillus fumigatus hyphae and conidia modifies the electrophysiological properties of human nasal epithelial cells. BMC Microbiol 7: 5.
26. Coyle CM, Kenaley SC, Rittenour WR, Panaccione DG, (2007) Association of ergot alkaloids with conidiation in Aspergillus fumigatus. Mycologia 99: 804-811.
27. Rabinovitch PS, (1994) DNA content histogram and cell-cycle analysis. Methods Cell Biol 41: 263-296.
28. Green DR, Reed JC, (1998) Mitochondria and apoptosis. Science 281: 1309-1312.
29. Twumasi-Boateng K, Yu Y, Chen D, Gravelat FN, Nierman WC, et al. (2009) Transcriptional profiling identifies a role for BrlA in the response to nitrogen depletion and for StuA in the regulation of secondary metabolite clusters in Aspergillus fumigatus. Eukaryot Cell 8: 104-115.
30. Ames BD, Haynes SW, Gao X, Evans BS, Kelleher NL, et al. (2011) Complexity Generation in Fungal Peptidyl Alkaloid Biosynthesis: Oxidation of Fumiquinazoline A to the Heptacyclic Hemiaminal Fumiquinazoline C by the Flavoenzyme Af12070 from Aspergillus fumigatus. Biochemistry 50: 8756-8769.
31. Ames BD, Liu X, Walsh CT, (2010) Enzymatic processing of fumiquinazoline F: a tandem oxidative-acylation strategy for the generation of multicyclic scaffolds in fungal indole alkaloid biosynthesis. Biochemistry 49: 8564-8576.
32. Maiya S, Grundmann A, Li SM, Turner G, (2006) The fumitremorgin gene cluster of Aspergillus fumigatus: identification of a gene encoding brevianamide F synthetase. Chembiochem 7: 1062-1069.
33. Larsen TO, Smedsgaard J, Nielsen KF, Hansen MAE, Samson RA, et al. (2007) Production of mycotoxins by Aspergillus lentulus and other medically important and closely related species in section Fumigati. Med Mycol 45: 225-232.
34. Geiser DM, Frisvad JC, Taylor JW, (1998) Evolutionary Relationships in Aspergillus Section Fumigati Inferred from Partial β-Tubulin and Hydrophobin DNA Sequences. Mycologia 90: 831-845.
35. Hong SB, Go SJ, Shin HD, Frisvad JC, Samson RA, (2005) Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia 97: 1316-1329.
36. Tepsic K, Gunde-Cimerman N, Frisvad JC, (1997) Growth and mycotoxin production by Aspergillus fumigatus strains isolated from a saltern. FEMS Microbiol Lett 157: 9-12.
37. Afiyatullov SS, Kalinovskii AI, Pivkin MV, Dmitrenok PS, Kuznetsova TA, (2004) Fumitremorgins from the marine isolate of the fungus Aspergillus fumigatus. Chem Nat Comp 40: 615-619.
38. Chomcheon P, Wiyakrutta S, Sriubolmas N, Ngamrojanavanich N, Mahidol C, et al. (2009) Metabolites from the endophytic mitosporic Dothideomycete sp. LRUB20. Phytochemistry 70: 121-127.
39. Zhou X, Zhao A, Goping G, Hirszel P, (2000) Gliotoxin-induced cytotoxicity proceeds via apoptosis and is mediated by caspases and reactive oxygen species in LLC-PK1 cells. Toxicol Sci 54: 194-202.
40. Kweon Y-O, Paik Y-H, Schnabl B, Qian T, Lemasters JJ, et al. (2003) Gliotoxin-mediated apoptosis of activated human hepatic stellate cells. J Hepatol 39: 38-46.
41. Shen HM, Shi C-Y, Shen Y, Ong CN, (1996) Detection of elevated reactive oxygen species level in cultured rat hepatocytes treated with aflatoxin B1. Free Radical Bio Med 21: 139-146.
42. Zhang L, Zhang J, Hu C, Cao J, Zhou X, et al. (2009) Efficient activation of p53 pathway in A549 cells exposed to L2, a novel compound targeting p53-MDM2 interaction. Anticancer Drugs 20: 416-424.
43. Krishnaswamy R, Devaraj SN, Padma VV, (2010) Lutein protects HT29 cells against deoxynivalenol-induced oxidative stress and apoptosis: prevention of NF-kB nuclear localization and down regulation of NF-kB and cyclo-oxygenase-2 expression. Free Radical Bio Med 49: 50-60.
44. Daly P, Verhaegen S, Clynes M, Kavanagh K, (1999) Culture filtrates of Aspergillus fumigatus induce different modes of cell death in human cancer cell lines. Mycopathologia 146: 67-74.
45. Féménia F, Huet D, Lair-Fulleringer S, Wagner MC, Sarfati J, et al. (2009) Effects of conidia of various Aspergillus species on apoptosis of human pneumocytes and bronchial epithelial cells. Mycopathologia 167: 249-262.
46. Hertweck C, (2009) Hidden biosynthetic treasures brought to light. Nat Chem Biol 5: 450-452.
47. Brakhage AA, Schroeckh V, (2011) Fungal secondary metabolites- strategies to activate silent gene clusters. Fungal Genet Biol 48: 15-22.
48. Miller JD, Sun M, Gilyan A, Roy J, TG Rand, (2010) Inflammation-associated gene transcription and expression in mouse lungs induced by low molecular weight compounds from fungi from the built environment. Chem-Biol Interact 183: 113-124.
49. Flemming J, Hudson B, Rand TG, (2004) Comparison of inflammatory and cytotoxic lung responses in mice after intratracheal exposure to spores of two different Stachybotrys chartarum strains. Toxicol Sci 78: 267-275.