A proteomic approach to investigating gene cluster expression and secondary metabolite functionality in Aspergillus fumigatus

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Owens, Rebecca A ^a   Hammel, Stephen ^a   Sheridan, Kevin J ^a   Jones, Gary W ^a   Doyle, Sean ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

CHITINASE; CYCLINE; FUNGAL PROTEIN; GLIOTOXIN; GLIT PROTEIN; HEAT SHOCK PROTEIN; HYDROGEN PEROXIDE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; LAEA PROTEIN; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (QUINONE); REGULATOR PROTEIN; UNCLASSIFIED DRUG; XPT1 PROTEIN; PROTEOME;

ARTICLE; ASPERGILLUS FUMIGATUS; CONTROLLED STUDY; FUNGUS GROWTH; GENE CLUSTER; GENE EXPRESSION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLOMICS; MYCELIUM; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEOMICS; PURINE SYNTHESIS; SECONDARY METABOLISM; FLUORESCENCE MICROSCOPY; FUNGAL GENE; GENETICS; METABOLISM; MULTIGENE FAMILY; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ASPERGILLUS FUMIGATUS; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FUNGAL PROTEINS; GENES, FUNGAL; MICROSCOPY, FLUORESCENCE; MULTIGENE FAMILY; PROTEOME; TANDEM MASS SPECTROMETRY;

EID: 84908610784     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106942     Document Type: Article

References (71)

1. 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.
2. Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, et al. (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4: e1000046.
3. Kniemeyer O, Lessing F, Scheibner O, Hertweck C, Brakhage AA (2006) Optimisation of a 2-D gel electrophoresis protocol for the human-pathogenic fungus Aspergillus fumigatus. Curr Genet 49: 178-189.
4. Carberry S, Neville CM, Kavanagh K, Doyle S (2006) Analysis of major intracellular proteins of Aspergillus fumigatus by MALDI mass spectrometry: identification and characterisation of an elongation factor 1B protein with glutathione transferase activity. Biochem Biophys Res Commun 341: 1096-1104.
5. Asif AR, Oellerich M, Amstrong VW, Riemenschneider B, Monod M, et al. (2006) Proteome of Conidial Surface Associated Proteins of Aspergillus fumigatus Reflecting Potential Vaccine Candidates and Allergens. J Proteome Res 5: 954-962.
6. Vödisch M, Albrecht D, Lessing F, Schmidt AD, Winkler R, et al. (2009) Twodimensional proteome reference maps for the human pathogenic filamentous fungus aspergillus fumigatus. Proteomics 9: 1407-1415.
7. Teutschbein J, Albrecht D, Po M, Guthke R, Aimanianda V, et al. (2010) Proteome Profiling and Functional Classification of Intracellular Proteins from Conidia of the Human-Pathogenic Mold Aspergillus fumigatus research articles. J Proteome Res 9: 3427-3442.
8. Wartenberg D, Lapp K, Jacobsen ID, Dahse H-M, Kniemeyer O, et al. (2011) Secretome analysis of Aspergillus fumigatus reveals Asp-hemolysin as a major secreted protein. J Clin Microbiol 301: 602-611.
9. Cagas SE, Jain MR, Li H, Perlin DS (2011) The Proteomic Signature of Aspergillus fumigatus During Early Development. Mol Cell proteomics 10: M111.010108.
10. Suh M-J, Fedorova ND, Cagas SE, Hastings S, Fleischmann RD, et al. (2012) Development stage-specific proteomic profiling uncovers small, lineage specific proteins most abundant in the Aspergillus fumigatus conidial proteome. Proteome Sci 10: 30.
11. Kniemeyer O, Schmidt AD, Vo?disch M, Wartenberg D, Brakhage AA (2011) Identification of virulence determinants of the human pathogenic fungi Aspergillus fumigatus and Candida albicans by proteomics. Int J Med Microbiol 301: 368-377.
12. Link AJ, Eng J, Schieltz DM, Carmack E, Mize GJ, et al. (1999) Direct analysis of protein complexes using mass spectrometry. Nat Biotechnol 17: 676-682.
13. Washburn MP, Wolters D, Yates JR (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19: 242-247.
14. McCormack AL, Schieltz DM, Goode B, Yang S, Barnes G, et al. (1997) Direct analysis and identification of proteins in mixtures by LC/MS/MS and database searching at the low-femtomole level. Anal Chem 69: 767-776.
15. Aebersold R, Mann M (2003) Mass spectrometry-based proteomics. Nature 422: 198-207.
16. Ouyang H, Luo Y, Zhang L, Li Y, Jin C (2010) Proteome analysis of Aspergillus fumigatus total membrane proteins identifies proteins associated with the glycoconjugates and cell wall biosynthesis using 2D LC-MS/MS. Mol Biotechnol 44: 177-189.
17. Rabilloud T (2009) Membrane proteins and proteomics: love is possible, but so difficult. Electrophoresis 30 Suppl 1: S174-80.
18. Wiedner SD, Burnum KE, Pederson LM, Anderson LN, Fortuin S, et al. (2012) Multiplexed activity-based protein profiling of the human pathogen Aspergillus fumigatus reveals large functional changes upon exposure to human serum. J Biol Chem: 10.1074/jbc.M112.394106.
19. Gubbens J, Zhu H, Girard G, Song L, Florea BI, et al. (2014) Natural product proteomining, a quantitative proteomics platform, allows rapid discovery of biosynthetic gene clusters for different classes of natural products. Chem Biol 21: 707-718.
20. Carberry S, Molloy E, Hammel S, O'Keeffe G, Jones GW, et al. (2012) Gliotoxin effects on fungal growth: Mechanisms and exploitation. Fungal Genet Biol 49: 302-312.
21. Vödisch M, Scherlach K, Winkler R, Hertweck C, Braun H-P, et al. (2011) Analysis of the Aspergillus fumigatus proteome reveals metabolic changes and the activation of the pseurotin A biosynthesis gene cluster in response to hypoxia. J Proteome Res 10: 2508-2524.
22. Barker BM, Kroll K, Vo?disch M, Mazurie A, Kniemeyer O, et al. (2012) Transcriptomic and proteomic analyses of the Aspergillus fumigatus hypoxia response using an oxygen-controlled fermenter. BMC Genomics 13: 62.
23. Lessing F, Kniemeyer O, Wozniok I, Loeffler J, Kurzai O, et al. (2007) The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot Cell 6: 2290-2302.
24. Albrecht D, Guthke R, Brakhage AA, Kniemeyer O (2010) Integrative analysis of the heat shock response in Aspergillus fumigatus. BMC Genomics 11: 32.
25. Gautam P, Shankar J, Madan T, Sirdeshmukh R, Sundaram CS, et al. (2008) Proteomic and transcriptomic analysis of Aspergillus fumigatus on exposure to amphotericin B. Antimicrob Agents Chemother 52: 4220-4227.
26. Gautam P, Upadhyay SK, Hassan W, Madan T, Sirdeshmukh R, et al. (2011) Transcriptomic and proteomic profile of Aspergillus fumigatus on exposure to artemisinin. Mycopathologia 172: 331-346.
27. Singh S, Gupta S, Singh B, Sharma SK, Gupta VK, et al. (2012) Proteomic Characterization of Aspergillus fumigatus Treated with an Antifungal Coumarin for Identification of Novel Target Molecules of Key Pathways. J Proteome Res 11: 3259-3268.
28. Schrettl M, Carberry S, Kavanagh K, Haas H, Jones GW, et al. (2010) Selfprotection against gliotoxin-a component of the gliotoxin biosynthetic cluster, GliT, completely protects Aspergillus fumigatus against exogenous gliotoxin. PLoS Pathog 6: e1000952.
29. Pardo J, Urban C, Galvez EM, Ekert PG, Mu? ller U, et al. (2006) The mitochondrial protein Bak is pivotal for gliotoxin-induced apoptosis and a critical host factor of Aspergillus fumigatus virulence in mice. J Cell Biol 174: 509-519.
30. Gallagher L, Owens RA, O' Keeffe G, Dolan SK, Schrettl M, et al. (2012) The Aspergillus fumigatus Protein GliK Protects Against Oxidative Stress and is Essential for Gliotoxin Biosynthesis. Eukaryot Cell 11: 1226-1238.
31. Collins C, Keane TM, Turner DJ, O'Keeffe G, Fitzpatrick DA, et al. (2013) Genomic and Proteomic Dissection of the Ubiquitous Plant Pathogen, Armillaria mellea: Toward a New Infection Model System. J Proteome Res 12: 2552-2570.
32. Arnaud M, Cerquiera G, Inglis D, Skrzypek M, Binkley J, et al. (n.d.) Aspergillus Genome Database.
33. Priebe S, Linde J, Albrecht D, Guthke R, Brakhage AA (2011) FungiFun: A web-based application for functional categorization of fungal genes and proteins. Fungal Genet Biol 48: 353-358.
34. Davis C, Carberry S, Schrettl M, Singh I, Stephens JC, et al. (2011) The role of glutathione S-transferase GliG in gliotoxin biosynthesis in Aspergillus fumigatus. Chem Biol 18: 542-552.
35. O'Hanlon KA, Cairns T, Stack D, Schrettl M, Bignell EM, et al. (2011) Targeted Disruption of Nonribosomal Peptide Synthetase pes3 Augments the Virulence of Aspergillus fumigatus . Infect Immun 79: 3978-3992.
36. O'Keeffe G, Jo?chl C, Kavanagh K, Doyle S (2013) Extensive proteomic remodeling is induced by eukaryotic translation elongation factor 1Bc deletion in Aspergillus fumigatus. Protein Sci 22: 1612-1622.
37. Shevchenko A, Tomas H, Havlis J, Olsen J V, Mann M (2007) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856-2860.
38. 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: e50.
39. Grundmann A, Li S-M (2005) Overproduction, purification and characterization of FtmPT1, a brevianamide F prenyltransferase from Aspergillus fumigatus. Microbiology 151: 2199-2207.
40. Maiya S, Grundmann A, Li X, Li S-M, Turner G (2007) Identification of a hybrid PKS/NRPS required for pseurotin A biosynthesis in the human pathogen Aspergillus fumigatus. Chembiochem 8: 1736-1743.
41. Lin H-C, Chooi Y-H, Dhingra S, Xu W, Calvo AM, et al. (2013) The Fumagillin Biosynthetic Gene Cluster in Aspergillus fumigatus Encodes a Cryptic Terpene Cyclase Involved in the Formation of b-trans-Bergamotene. J Am Chem Soc 135: 4616-4619.
42. Wiemann P, Keller NP (2013) Strategies for mining fungal natural products. J Ind Microbiol Biotechnol.
43. Gardiner DM, Howlett BJ (2005) Bioinformatic and expression analysis of the putative gliotoxin biosynthetic gene cluster of Aspergillus fumigatus. FEMS Microbiol Lett 248: 241-248.
44. 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.
45. Tsunematsu Y, Ishikawa N, Wakana D, Goda Y, Noguchi H, et al. (2013) Distinct mechanisms for spiro-carbon formation reveal biosynthetic pathway crosstalk. Nat Chem Biol 9: 818-825.
46. Wiemann P, Guo C, Palmer JM, Sekonyela R, Wang CCC (2013) Prototype of an intertwined secondary- metabolite supercluster. Proc Natl Acad Sci U S A 110: 17065-17070.
47. Scharf DH, Remme N, Heinekamp T, Hortschansky P, Brakhage AA, et al. (2010) Transannular Disulfide Formation in Gliotoxin Biosynthesis and Its Role in Self-Resistance of the Human Pathogen Aspergillus fumigatus. J Am Chem Soc 132: 10136-10141.
48. Burkovics P, Hajdu? I, Szukacsov V, Unk I, Haracska L (2009) Role of PCNAdependent stimulation of 3 9-phosphodiesterase and 39-59 exonuclease activities of human Ape2 in repair of oxidative DNA damage. Nucleic Acids Res 37: 4247-4255.
49. Baumer M, Kunzler M, Steigemann P, Braus GH, Irniger S (2000) Yeast Ranbinding Protein Yrb1p Is Required for Efficient Proteolysis of Cell Cycle Regulatory Proteins Pds1p and Sic1p. J Biol Chem 275: 38929-38937.
50. Valerius O, Draht O, Ku? bler E, Adler K, Hoffmann B, et al. (2001) Regulation of hisHF transcription of Aspergillus nidulans by adenine and amino acid limitation. Fungal Genet Biol 32: 21-31.
51. Sieńko M, Natorff R, Zieliński Z, Hejduk A, Paszewski A (2007) Two Aspergillus nidulans genes encoding methylenetetrahydrofolate reductases are up-regulated by homocysteine. Fungal Genet Biol 44: 691-700.
52. Yamazaki H, Yamazaki D, Takaya N, Takagi M, Ohta A (2007) A chitinase gene, chiB, involved in the autolytic process of Aspergillus nidulans. Curr Genet 51: 89-91.
53. Vödisch M, Albrecht D, Lessing F, Schmidt AD, Winkler R, et al. (2009) Twodimensional proteome reference maps for the human pathogenic filamentous fungus Aspergillus fumigatus. Proteomics 9: 1407-1415.
54. Stack D, Neville C, Doyle S (2007) Nonribosomal peptide synthesis in Aspergillus fumigatus and other fungi. Microbiology 153: 1297-1306.
55. O' Hanlon KA, Gallagher L, Schrettl M, Jo?chl C, Kavanagh K, et al. (2012) Nonribosomal Peptide Synthetase Genes pesL and pes1 Are Essential for Fumigaclavine C Production in Aspergillus fumigatus. Appl Environ Microbiol 78: 3166-3176.
56. Steffan N, Grundmann A, Afiyatullov S, Ruan H, Li S (2009) FtmOx1, a nonheme Fe(II) and alpha-ketoglutarate-dependent dioxygenase, catalyses the endoperoxide formation of verruculogen in Aspergillus fumigatus. Org Biomol Chem 7: 4082-4087.
57. Kato N, Suzuki H, Takagi H, Uramoto M, Takahashi S, et al. (2011) Gene disruption and biochemical characterization of verruculogen synthase of Aspergillus fumigatus. Chembiochem 12: 711-714.
58. Khoufache K, Puel O, Loiseau N, Delaforge M, Rivollet D, et al. (2007)Verruculogen associated with Aspergillus fumigatus hyphae and conidia modifies the electrophysiological properties of human nasal epithelial cells. BMC Microbiol 7: 5.
59. Sin N, Meng L, Wang MQ, Wen JJ, Bornmann WG, et al. (1997) The antiangiogenic agent fumagillin covalently binds and inhibits the methionine aminopeptidase, MetAP-2. Proc Natl Acad Sci U S A 94: 6099-6103.
60. Fallon JP, Reeves EP, Kavanagh K (2010) Inhibition of neutrophil function following exposure to the Aspergillus fumigatus toxin fumagillin. J Med Microbiol 59: 625-633.
61. McDonagh A, Fedorova ND, Crabtree J, Yu Y, Kim S, et al. (2008) Subtelomere directed gene expression during initiation of invasive aspergillosis. PLoS Pathog 4: e1000154.
62. Choi HS, Shim JS, Kim J-A, Kang SW, Kwon HJ (2007) Discovery of gliotoxin as a new small molecule targeting thioredoxin redox system. Biochem Biophys Res Commun 359: 523-528.
63. Zamir L, Zaretsky M, Fridman Y, Ner-Gaon H, Rubin E, et al. (2012) Tight coevolution of proliferating cell nuclear antigen (PCNA)-partner interaction networks in fungi leads to interspecies network incompatibility. Proc Natl Acad Sci U S A 109: E406-14.
64. Fraczek MG, Rashid R, Denson M, Denning DW, Bowyer P (2010) Aspergillus fumigatus allergen expression is coordinately regulated in response to hydrogen peroxide and cyclic AMP. Clin Mol Allergy 8: 15.
65. Franzosa EA, Albanese V, Frydman J, Xia Y, McClellan AJ (2011) Heterozygous yeast deletion collection screens reveal essential targets of Hsp90. PLoS One 6: e28211.
66. Brace JL, Vanderweele DJ, Rudin CM (2005) Svf1 inhibits reactive oxygen species generation and promotes survival under conditions of oxidative stress in Saccharomyces cerevisiae. Yeast 22: 641-652.
67. Hartl L, Zach S, Seidl-Seiboth V (2012) Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Appl Microbiol Biotechnol 93: 533-543.
68. Alcazar-Fuoli L, Clavaud C, Lamarre C, Aimanianda V, Seidl-Seiboth V, et al. (2011) Functional analysis of the fungal/plant class chitinase family in Aspergillus fumigatus. Fungal Genet Biol 48: 418-429.
69. Guetsova ML, Crother TR, Taylor MW, Daignan-Fornier B (1999) Isolation and Characterization of the Saccharomyces cerevisiae XPT1 Gene Encoding Xanthine Phosphoribosyl Transferase. J Bacteriol 181: 2984.
70. Mackenzie DA, Guillemette T, Al-Sheikh H, Watson AJ, Jeenes DJ, et al. (2005) UPR-independent dithiothreitol stress-induced genes in Aspergillus niger . Mol Genet Genomics 274: 410-418.
71. Mabey JE, Anderson MJ, Giles PF, Miller CJ, Attwood TK, et al. (2004) CADRE: the Central Aspergillus Data REpository. Nucleic Acids Res 32: D401-5.