Nonribosomal peptide synthesis in Aspergillus fumigatus and other fungi

Microbiology

Volumn 153, Issue 5, 2007, Pages 1297-1306

  Stack, Deirdre ^a   Neville, Claire ^a   Doyle, Sean ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALOID DERIVATIVE; AMINO ACID; CEPHALOSPORIN; COENZYME A; CYCLOSPORIN; FUNGAL PROTEIN; GLIOTOXIN; METHYLTRANSFERASE; PANTETHEINE PHOSPHATE; PENICILLIN G; PEPTIDE SYNTHASE; PEPTIDYL CARRIER PROTEIN; POLYKETIDE; PROTEIN FTMA; PROTEIN GLIP; PROTEIN LEAA; PROTEIN PES1; SIDEROPHORE; UNCLASSIFIED DRUG;

ADENYLATION; AFFINITY LABELING; ALTERNARIA; ASCOMYCETES; ASPERGILLUS FUMIGATUS; ASPERGILLUS NIDULANS; BEAUVERIA; COCHLIOBOLUS; COCHLIOBOLUS HETEROSTROPHUS; COMPUTER MODEL; DIAGNOSTIC VALUE; ENZYME SPECIFICITY; FUNGAL GENE; FUNGAL METABOLISM; FUNGAL VIRULENCE; FUSARIUM GRAMINEARUM; GENE CLUSTER; GENE DELETION; GENE DISRUPTION; GENE EXPRESSION; GENETIC CODE; MYCOSIS; NONHUMAN; NONRIBOSOMAL PEPTIDE SYNTHESIS; OPEN READING FRAME; OXIDATIVE STRESS; PHYLOGENY; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN POLYMERIZATION; PROTEOMICS; REVIEW;

ASPERGILLUS FUMIGATUS; FUNGI; PEPTIDE BIOSYNTHESIS, NUCLEIC ACID-INDEPENDENT; PEPTIDE SYNTHASES;

ASCOMYCOTA; ASPERGILLUS; ASPERGILLUS FUMIGATUS; COCHLIOBOLUS HETEROSTROPHUS; CORDYCEPS BASSIANA; FUNGI;

EID: 34249085909     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.2006/006908-0     Document Type: Review

References (75)

1. Balibar, C. J. & Walsh, C. T. (2006). GliP, a multimodular nonribosomal peptide synthetase in Aspergillus fumigatus, makes the diketopiperazine scaffold of gliotoxin. Biochemistry 45, 15029-15038.
2. Bok, J. W. & Keller, N. P. (2004). LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3, 527-535.
3. Bok, J. W., Balajee, S. A., Marr, K. A., Andes, D., Nielsen, K. F., Frisvad, J. C. & Keller, N. P. (2005). LaeA, a regulator of morphogenetic fungal virulence factors. Eukaryot Cell 4, 1574-1582.
4. Bok, J. W., Noordermeer, D., Kale, S. P. & Keller, N. P. (2006a). Secondary metabolic gene cluster silencing in Aspergillus nidulans. Mol Microbiol 61, 1636-1645.
5. Bok, J. W., Hoffmeister, D., Maggio-Hall, L. A., Murillo, R., Glasner, J. D. & Keller, N. P. (2006b). Genomic mining for Aspergillus natural products. Chem Biol 13, 31-37.
6. Bok, J. W., Chung, D., Balajee, S. A., Marr, K A., Andes, D., Nielsen, K. F., Frisvad, J. C., Kirby, K. A. & Keller, N. P. (2006c). GliZ, a transcriptional regulator of gliotoxin biosynthesis, contributes to Aspergillus fumigatus virulence. Infect Immun 74, 6761-6768.
7. Brakhage, A. A. & Langfelder, K (2002). Menacing mold: the molecular biology of Aspergillus fumigatus. Annu Rev Microbiol 56, 433-455.
8. Brookman, J. L & Denning, D. W. (2000). Molecular genetics in Aspergillus fumigatus. Curr Opin Microbiol 3, 468-474.
9. Capon, R. J., Ratnayake, R., Stewart, M., Lacey, E., Tennant, S. & Gill, J. H. (2005). Aspergillazines A-E: novel heterocyclic dipeptides from an Australian strain of Aspergillus unilateralis. Org Biomol Chem 3, 123-129.
10. Challis, G. L., Ravel, J. & Townsend, C. A. (2000). Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem Biol 3, 211-224.
11. Couch, R., O'Connor, S. E., Seidle, H., Walsh, C. T. & Parry, R. (2004). Characterization of CmaA, an adenylation-thiolation didomain enzyme involved in the biosynthesis of coronatine. J Bacteriol 186, 35-42.
12. Coyle, C. M. & Panaccione, D. G. (2005). An ergot alkaloid biosynthesis gene and clustered hypothetical genes from Aspergillus fumigatus. Appl Environ Microbiol 71, 3112-3118.
13. Cramer, R. A., Jr, Gamcsik, M. P., Brooking, R. M., Najvar, L.K., Kirkpatrick W. R., Patterson, T. F., Balibar, C. J., Graybill, J. R., Perfect, J. R. & other authors (2006a). Disruption of a nonribosomal peptide synthetase in Aspergillus fumigatus eliminates gliotoxin production. Eukaryot Cell 5, 972-980.
14. Cramer, R. A., Jr, Stajich, J. S., Yamanaka, Y., Dietrich, F. E., Steinbach, W. J. & Perfect, J. R. (2006b). Phylogenomic analysis of non-ribosomal peptide synthetases in the genus Aspergillus. Gene 383, 24-32.
15. Dean, R. A., Talbot N. J., Ebbole, D. J., Farman, M. L., Mitchell, T. K., Orbach, M. J., Thon, M., Kulkarni, R., Xu, J. R. & other authors (2005). The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434, 980-986.
16. Di Vincenzo, L., Grgurina, I. & Pascarella, S. (2005). In silico analysis of the adenylation domains of the freestanding enzymes belonging to the eucaryotic nonribosomal peptide synthetase-like family. FEBS J 272, 929-941.
17. Dorrestein, P. C., Blackhall, J., Straight P. D., Fischbach, M. A, Garneau-Tsodikova, S., Edwards, D. J., McLaughlin, S., Lin, M., Gerwick, W. H. & other authors (2006). Activity screening of carrier domains within nonribosomal peptide synthetases using complex substrate mixtures and large molecule mass spectrometry. Biochemistry 45, 1537-1546.
18. 5 -monooxy-genase (sidA) and a non-ribosomal peptide synthetase (sidC). Mol Microbiol 49, 359-375.
19. Eley, K L., Halo, L. M., Song, Z., Powles, H., Cox, R. J., Bailey, A. M., Lazarus, C. M. & Simpson, T. J. (2007). Biosynthesis of the 2-pyridone tenellin in the insect pathogenic fungus Beauveria bassiana. ChemBioChem 8, 289-297.
20. Fox, M., Gray, G., Kavanagh, K., Lewis, C. & Doyle, S. (2004). Detection of Aspergillus fumigatus mycotoxins: immunogen synthesis and immunoassay development. J Microbiol Methods 56, 221-230.
21. Galagan, J. E., Calvo, S. E., Cuomo, C., Ma, L. J., Wortman, J. R., Batzoglou, S., Lee, S. I., Basturkmen, M., Spevak, C. C. & other authors (2005). Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438, 1105-1156.
22. Gardiner, D. M. & Howlett, B. J. (2005). Bioinformatic and expression analysis of the putative gliotoxin biosynthetic gene cluster of Aspergillus fumigatus. FEMS Microbiol Lett 248, 241-248.
23. Gardiner, D. M., Cozijnsen, A. J., Wilson, L. M., Pedras, M. S. & Howlett B. J. (2004). The sirodesmin biosynthetic gene cluster of the plant pathogenic fungus Leptosphaeria maculans. Mol Microbiol 53, 1307-1318.
24. Gardiner, D. M., Waring, P. & Howlett, B. J. (2005). The epipolythio-dioxopiperazine (ETP) class of fungal toxins: distribution, mode of action, functions and biosynthesis. Microbiology 151, 1021-1032.
25. Grunewald, J. & Marahiel, M. A. (2006). Chemoenzymatic and template-directed synthesis of bioactive macrocyclic peptides. Microbiol Mol Biol Rev 70, 121-146.
26. Guo, S. & Bhattacharjee, J. K. (2003). Molecular characterization of the Candida albicans LYS5 gene and site-directed mutational analysis of the PPTase (Lys5p) domains for lysine biosynthesis. FEMS Microbiol Lett 224, 261-267.
27. Guo, S., Evans, S. A., Wilkes, M. B. & Bhattacharjee, J. K (2001). Novel posttranslational activation of the LYS2-encoded alpha-aminoadipate reductase for biosynthesis of lysine and site-directed mutational analysis of conserved amino acid residues in the activation domain of Candida albicans. J Bacteriol 183, 7120-7125.
28. Haarmann, T., Machado, C., Lubbe, Y., Correia, T., Schardl, C. L., Panaccione, D. G. & Tudzynski, P. (2005). The ergot alkaloid gene cluster in Claviceps purpurea: extension of the cluster sequence and intra species evolution. Phytochemistry 66, 1312-1320.
29. Han, K H., Kim, J. H., Kim, W. S. & Han, D. M. (2005). The snpA, a temperature-sensitive suppressor of npgA1, encodes the eukaryotic translation release factor, eRF1, in Aspergillus nidulans. FEMS Microbiol Lett 251, 155-160.
30. Harrison, P., Kumar, A., Lan, N., Echols, N., Synder, M. & Gerstein, M. (2002). A small reservoir of disabled ORFs in the yeast genome and its implications for the dynamics of proteome evolution. J Mol Biol 316, 409-419.
31. Hicks, L. M., Mazur, M. T., Miller, L. M., Dorrestein, P. C., Schnarr, N. A., Khosla, C. & Kelleher, N. L. (2006). Investigating nonribosomal peptide and polyketide biosynthesis by direct detection of intermediates on >70 kDa polypeptides by using Fourier-transform mass spectrometry. ChemBioChem 7, 904-907.
32. 5-oxygenase, is required for virulence. Infect Immun 73, 5493-5503.
33. Jegorov, A., Hajduch, M., Sulc, M. & Havlicek, V. (2006). Nonribosomal cyclic peptides: specific markers of fungal infections. J Mass Spectrom 41, 563-576.
34. Kelleher, N. L & Hicks, L. M. (2005). Contemporary mass spectrometry for the direct detection of enzyme intermediates. Curr Opin Chem Biol 9, 424-430.
35. Keller, N. P. G., Turner, G. & Bennet J. W. (2005). Fungal secondary metabolism - from biochemistry to genomics. Nat Rev Microbiol 3, 937-947.
36. Keszenman-Pereyra, D., Lawrence, S., Twfieg, M. E., Price, J. & Turner, G. (2003). The npgA cfwA gene encodes a putative 4-phosphopantetheinyl transferase which is essential for penicillin biosynthesis in Aspergillus nidulans. Curr Genet 43, 186-190.
37. Khoufache, K., Puel, O., Loiseau, N., Delaforge, M., Rivollet D., Coste, A., Cordonnier, C., Escudier, E., Botterel, F. & Bretagne, S. (2007). Verruculogen associated with Aspergillus fumigatus hyphae and conidia modifies the electrophysiological properties of human nasal epithelial cells. BMC Microbiol 7, 5.
38. Kontoyiannis, D. P. & Bodey, G. P. (2002). Invasive aspergillosis in 2002: an update. Eur J Clin Microbiol Infect Dis 21, 161-172.
39. Kosalec, L, Klaric, M. S. & Pepeljnjak, S. (2005). Verruculogen production in airborne and clinical isolates of Aspergillus fumigatus. Acta Pharm 55, 357-364.
40. Krappmann, S. (2006). Tools to study molecular mechanisms of Aspergillus pathogenicity. Trends Microbiol 14, 356-364.
41. Kupfahl, C., Heinekamp, T., Geginat, G., Ruppert, T., Harti, A., Hof, H. & Brakhage, A. A. (2006). Deletion of the gliP gene of Aspergillus fumigatus results in loss of gliotoxin production but has no effect on virulence of the fungus in a low-dose mouse infection model. Mol Microbiol 62, 292-302.
42. La Clair, J. J., Foley, T. L., Schegg, T. R., Regan, C. M. & Burkart, M. D. (2004). Manipulation of carrier proteins in antibiotic biosynthesis. Chem Biol 11, 195-201.
43. Lambalot, R. H., Gehring, A. M., Flugel, R. S., Zuber, P., LaCelle, M., Marahiel, M. A., Reid, R., Khosla, C. & Walsh, C. T. (1996). A new enzyme superfamily - the phosphopantetheinyl transferases. Chem Biol 3, 923-936.
44. Lee, B. N., Kroken, S., Chou, D. Y., Robbertse, B., Yoder, O. C. & Turgeon, B. G. (2005). Functional analysis of all nonribosomal peptide synthetases in Cochliobolus heterostrophus reveals a factor, NPS6, involved in virulence and resistance to oxidative stress. Eukaryot Cell 4, 545-555.
45. Lewis, R. E., Wiederhold, N. P., Chi, J., Han, X Y., Komanduri, K. V., Kontoyiannis, D. P. & Prince, R. A. (2005). Detection of gliotoxin in experimental and human aspergillosis. Infect Immun 73, 635-637.
46. Mabey, J. E, Anderson, M. J., Giles, P. F., Miller, C. J., Attwood, T. K, Paton, N. W., Bornberg-Bauer, E, Robson, G. D., Oliver, S. G. & Denning, D. W. (2004). CADRE: the Central Aspergillus Data REpository. Nucleic Acids Res 32, 401-405.
47. Machida, M., Asai, K., Sano, M., Tanaka, T., Kumagai, T., Terai, G., Kusumoto, K, Arima, T., Akita, O. & other authors (2005). Genome sequencing and analysis of Aspergillus oryzae. Nature 438, 1157-1161.
48. Maiya, S., Grundmann, A., Li, S. M. & Turner, G. (2006). The fumitremorgin gene cluster of Aspergillus fumigatus: identification of a gene encoding brevianamide F synthetase. ChemBioChem 7, 1062-1069.
49. May, J. J., Finking, R., Wiegeshoff, F., Weber, T. T., Bandur, N., Koert, U. & Marahiel, M. A. (2005). Inhibition of the D-alanine: D-alanyl carrier protein ligase from Bacillus subtilis increases the bacterium's susceptibility to antibiotics that target the cell wall. FEBS J 272, 2993-3003.
50. Mennink-Kersten, M. A., Klont, R. R., Warris, A., Op den Camp, H. J. & Verweij, P. E (2004). Bifidobacterium lipoteichoic acid and false ELISA reactivity in Aspergillus antigen detection. Lancet 363, 325-327.
51. Mootz, H. D., Schwarzer, D. & Marahiel, M. A. (2002). Ways of assembling complex natural products on modular nonribosomal peptide synthetases. ChemBioChem 3, 490-504.
52. Mouyna, I., Henry, C., Doering, T. L. & Latgé, J. P. (2004). Gene silencing with RNA interference in the human pathogenic fungus Aspergillus fumigatus. FEMS Microbiol Lett 237, 317-324.
53. Neville, C. M., Murphy, A., Kavanagh, K. & Doyle, S. (2005). A 4-phosphopantetheinyl transferase mediates non-ribosomal peptide synthetase activation in Aspergillus fumigatus. ChemBioChem 6, 679-685.
54. Nierman, W. C., Pain, A., Anderson, M. J., Wortman, J. R., Kim, H. S., Arroyo, J., Berriman, M., Abe, K, Archer, D. B. & other authors (2005). Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438, 1151-1156.
55. Oide, S., Moeder, W., Krasnoff, S., Gibson, D., Haas, H., Yoshioka, K. & Turgeon, B. G. (2006). NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18, 2836-2853.
56. Panaccione, D. G. & Coyle, C. M. (2005). Abundant respirable ergot alkaloids from the common airborne fungus Aspergillus fumigatus. Appl Environ Microbiol 71, 3106-3111.
57. Rausch, C., Weber, T., Kohlbacher, O., Wohlleben, W. & Huson, D. H. (2005). Specificity prediction of adenylation domains in nonribosomal peptide synthetases (NRPS) using transductive support vector machines (TSVMs). Nucleic Acids Res 33, 5799-5808.
58. 15N]-L-homoserine and its incorporation by the PKS-NRPS system of Fusarium moniliforme into the mycotoxin fusarin C. ChemBioChem 8, 6-50.
59. Reeves, E. P., Reiber, K., Neville, C., Scheibner, O., Kavanagh, K. & Doyle, S. (2006). A nonribosomal peptide synthetase (Pes1) confers protection against oxidative stress in Aspergillus fumigatus. FEBS J 273, 3038-3053.
60. Reiber, K., Reeves, E. P., Neville, C., Winkler, R., Geblhardt, P., Kavanagh, K. & Doyle, S. (2005). The expression of three nonribosomal peptide synthetases in Aspergillus fumigatus is mediated by the availability of free iron. FEMS Microbiol Lett 248, 83-91.
61. Sanchez, C., Du, L., Edwards, D. J., Toney, M. D. & Shen, B. (2001). Cloning and characterization of a phosphopantetheinyl transferase from Streptomyces verticillus ATCC15003, the producer of the hybrid peptide-polyketide antitumor drug bleomycin. Chem Biol 8, 725-738.
62. Schardl, C. L. (2006). A global view of metabolites. Chem Biol 13, 5-6.
63. Schrettl, M. E., Bignell, E., Kragl, C., Joechl, C., Rogers, T., Arst H. N., Jr, Haynes, K. & Haas, H. (2004). Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J Exp Med 200, 1213-1219.
64. Schwecke, T., Gottling, K., Durek, P., Duenas, I., Kaufer, N. F., Zock-Emmenthal, S., Staub, E., Neuhof, T., Dieckmann, R. & von Dohren, H. (2006). Nonribosomal peptide synthesis in Schizosaccharomyces pombe and the architectures of ferrichrome-type siderophore synthetases in fungi. ChemBioChem 7, 612-622.
65. Sheppard, D. C., Doedt, T., Chiang, L. Y., Kim, H. S., Chen, D., Nierman, W. C. & Filler, S. G. (2005). The Aspergillus fumigatus StuA protein governs the up-regulation of a discrete transcriptional program during the acquisition of developmental competence. Mol Biol Cell 16, 5866-5879.
66. Stachelhaus, T., Mootz, H. D. & Marahiel, M. A. (1999). The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem Biol 6, 493-505.
67. Tekaia, F. & Latgé J. P. (2005). Aspergillus fumigatus: saprophyte or pathogen. Curr Opin Microbiol 8, 385-392.
68. Tobiasen, C., Aahman, J., Ravnholt; K. S., Bjerrum, M. J., Grell, M. N. & Giese, H. (2007). Nonribosomal peptide synthetase (NPS) genes in Fusarium graminearum, F. culmorum and F. pseudograminearium and identification of NPS2 as the producer of ferricrocin. Curr Genet 51, 43-58.
69. Tsunawaki, S., Yoshida, L S., Nishida, S., Kobayashi, T. & Shimoyama, T. (2004). Fungal metabolite gliotoxin inhibits assembly of the human respiratory burst NADPH oxidase. Infect Immun 72, 3373-3382.
70. Varga, J., Kocsube, S., Toth, B. & Mesterhazy, A. (2005). Nonribosomal peptide synthetase genes in the genome of Fusarium graminearum, causative agent of wheat head blight. Acta Biol Hung 56, 375-388.
71. Vigushin, D. M., Mirsaidi, N., Brooke, G., Sun, C., Pace, P., Inman, L, Moody, C. J. & Coombes, R. C. (2004). Gliotoxin is a dual inhibitor of farnesyltransferase and geranylgeranyltransferase I with antitumor activity against breast cancer in vivo. Med Oncol 21, 21-30.
72. Vizcaino, J. A., Sanz, L., Cardoza, R. E., Monte, E. & Gutierrez, S. (2005). Detection of putative peptide synthetase genes in Trichoderma species: application of this method to the cloning of a gene from T. harzianum CECT 2413. FEMS Microbiol Lett 244, 139-148.
73. Walsh, C. T., Gehring, A. M., Weinreb, P. H., Quadri, L. E. & Flugel, R. S. (1997). Post-translational modification of polyketide and nonribosomal peptide synthases. Curr Opin Chem Biol 1, 309-315.
74. Weissman, K J., Hong, H., Oliynyk, M., Siskos, A. P. & Leadlay, P. F. (2004). Identification of a phosphopantetheinyl transferase for erythromycin biosynthesis in Saccharopolyspora erythraea. ChemBioChem 5, 116-125.
75. Wiest, A., Grzegorski, D., Xu, B. W., Goulard, C., Rebuffat, S., Ebbole, D. J., Bodo, B. & Kenerley, C. (2002). Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J Biol Chem 277, 20862-20868.