The temporal dynamics of differential gene expression in Aspergillus fumigatus interacting with human immature dendritic cells in vitro

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Morton, Charles O ^a   Varga, John J ^b   Hornbach, Anke ^c   Mezger, Markus ^c   Sennefelder, Helga ^c   Kneitz, Susanne ^d   Kurzai, Oliver ^e   Krappmann, Sven ^f   Einsele, Hermann ^c   Nierman, William C ^b   Rogers, Thomas R ^a   Loeffler, Juergen ^c  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b J CRAIG VENTER INSTITUTE   (United States)

^c UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^d Interdisziplinäres Zentrum für Klinische Forschung   (Germany)

^e FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^f UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRATE AMINOTRANSFERASE; ABC TRANSPORTER; ALDEHYDE DEHYDROGENASE; ALDEHYDE REDUCTASE; ALKALINE PHOSPHATASE; AMINO ACID TRANSPORTER; BUTYRYL COENZYME A DEHYDROGENASE; CATALASE; CATALASE A; CD83 ANTIGEN; CD86 ANTIGEN; CHAPERONE; COPPER EXPORTING ADENOSINE TRIPHOSPHATASE; CYTOCHROME C PEROXIDASE; EXONUCLEASE; FARNESYL TRANS TRANSFERASE; FLAVINE MONONUCLEOTIDE REDUCTASE; GLIOTOXIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 12; INOSITOL OXYGENASE; MALATE DEHYDROGENASE (DECARBOXYLATING); MANNOSIDASE; MITOCHONDRIAL PROTEIN; PERMEASE; RIBONUCLEASE P; RIBOSOME PROTEIN; TRANSFER RNA METHYLTRANSFERASE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GLUCOSE 4 EPIMERASE;

ADAPTIVE IMMUNITY; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; ASPERGILLUS FUMIGATUS; CELL DEATH; CONIDIUM; CONTROLLED STUDY; CYTOTOXICITY; DENDRITIC CELL; DOWN REGULATION; FERMENTATION; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; INNATE IMMUNITY; MICROARRAY ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PHAGOCYTOSIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; TOXIN SYNTHESIS; UPREGULATION; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; IMMUNE EVASION; IMMUNOLOGY; MICROBIOLOGY;

ASPERGILLUS FUMIGATUS;

ASPERGILLUS FUMIGATUS; CELLS, CULTURED; DENDRITIC CELLS; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; INFLAMMATION; PHAGOCYTOSIS;

EID: 79251569265     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016016     Document Type: Article

References (80)

1. O'Gorman CM, Fuller HT, Dyer PS (2009) Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457: 471-474.
2. Gugnani HC (2003) Ecology and taxonomy of pathogenic aspergilli. Front Biosci 8: s346-357.
3. Latge JP (1999) Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12: 310-350.
4. Neofytos D, Horn D, Anaissie E, Steinbach W, Olyaei A, et al. (2009) Epidemiology and outcome of invasive fungal infection in adult hematopoietic stem cell transplant recipients: analysis of Multicenter Prospective Antifungal Therapy (PATH) Alliance registry. Clin Infect Dis 48: 265-273.
5. Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K, et al. (2009) Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460: 1117-1121.
6. Hope WW (2009) Invasion of the alveolar-capillary barrier by Aspergillus spp.: therapeutic and diagnostic implications for immunocompromised patients with invasive pulmonary aspergillosis. Med Mycol 47 Suppl 1: S291-298.
7. Chignard M, Balloy V, Sallenave JM, Si-Tahar M (2007) Role of Toll-like receptors in lung innate defense against invasive aspergillosis. Distinct impact in immunocompetent and immunocompromized hosts. Clin Immunol 124: 238-243.
8. Wang JE, Warris A, Ellingsen EA, Jorgensen PF, Flo TH, et al. (2001) Involvement of CD14 and toll-like receptors in activation of human monocytes by Aspergillus fumigatus hyphae. Infect Immun 69: 2402-2406.
9. Dagenais TR, Keller NP (2009) Pathogenesis of Aspergillus fumigatus in Invasive Aspergillosis. Clin Microbiol Rev 22: 447-465.
10. Steele C, Rapaka RR, Metz A, Pop SM, Williams DL, et al. (2005) The betaglucan receptor dectin-1 recognizes specific morphologies of Aspergillus fumigatus. PLoS Pathog 1: e42.
11. Cortez KJ, Lyman CA, Kottilil S, Kim HS, Roilides E, et al. (2006) Functional genomics of innate host defense molecules in normal human monocytes in response to Aspergillus fumigatus. Infect Immun 74: 2353-2365.
12. Gafa V, Lande R, Gagliardi MC, Severa M, Giacomini E, et al. (2006) Human dendritic cells following Aspergillus fumigatus infection express the CCR7 receptor and a differential pattern of interleukin-12 (IL-12), IL-23, and IL-27 cytokines, which lead to a Th1 response. Infect Immun 74: 1480-1489.
13. Mezger M, Kneitz S, Wozniok I, Kurzai O, Einsele H, et al. (2008) Proinflammatory response of immature human dendritic cells is mediated by dectin-1 after exposure to Aspergillus fumigatus germ tubes. J Infect Dis 197: 924-931.
14. 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.
15. Bozza S, Gaziano R, Spreca A, Bacci A, Montagnoli C, et al. (2002) Dendritic cells transport conidia and hyphae of Aspergillus fumigatus from the airways to the draining lymph nodes and initiate disparate Th responses to the fungus. J Immunol 168: 1362-1371.
16. Tekaia F, Latge JP (2005) Aspergillus fumigatus: saprophyte or pathogen? Curr Opin Microbiol 8: 385-392.
17. Askew DS (2008) Aspergillus fumigatus: virulence genes in a street-smart mold. Curr Opin Microbiol 11: 331-337.
18. Willger SD, Grahl N, Cramer RA, Jr. (2009) Aspergillus fumigatus metabolism: clues to mechanisms of in vivo fungal growth and virulence. Med Mycol 47 Suppl 1: S72-79.
19. Kwon-Chung KJ, Sugui JA (2009) What do we know about the role of gliotoxin in the pathobiology of Aspergillus fumigatus? Med Mycol 47 Suppl 1: S97-103.
20. Penalva MA, Tilburn J, Bignell E, Arst HN, Jr. (2008) Ambient pH gene regulation in fungi: making connections. Trends Microbiol 16: 291-300.
21. Schrettl M, Bignell E, Kragl C, Sabiha Y, Loss O, et al. (2007) Distinct roles forintra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathog 3: 1195-1207.
22. Grahl N, Cramer RA, Jr. (2009) Regulation of hypoxia adaptation: an overlooked virulence attribute of pathogenic fungi? Med Mycol. pp 1-16.
23. Sugui JA, Kim HS, Zarember KA, Chang YC, Gallin JI, et al. (2008) Genes differentially expressed in conidia and hyphae of Aspergillus fumigatus upon exposure to human neutrophils. PLoS ONE 3: e2655.
24. Sabatte J, Maggini J, Nahmod K, Amaral MM, Martinez D, et al. (2007) Interplay of pathogens, cytokines and other stress signals in the regulation of dendritic cell function. Cytokine Growth Factor Rev 18: 5-17.
25. Willment JA, Brown GD (2008) C-type lectin receptors in antifungal immunity. Trends Microbiol 16: 27-32.
26. Ruepp A, Zollner A, Maier D, Albermann K, Hani J, et al. (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32: 5539-5545.
27. Hosack DA, Dennis G, Jr., Sherman BT, Lane HC, Lempicki RA (2003) Identifying biological themes within lists of genes with EASE. Genome Biol 4: R70.
28. Brown JS, Aufauvre-Brown A, Brown J, Jennings JM, Arst H, Jr., et al. (2000) Signature-tagged and directed mutagenesis identify PABA synthetase as essential for Aspergillus fumigatus pathogenicity. Mol Microbiol 36: 1371-1380.
29. Loeffler J, Haddad Z, Bonin M, Romeike N, Mezger M, et al. (2009) Interaction analyses of human monocytes co-cultured with different forms of Aspergillus fumigatus. J Med Microbiol 58: 49-58.
30. Kang MW, Jang JY, Choi JY, Kim SH, Oh J, et al. (2008) Induction of IFNgamma gene expression by thioredoxin: positive feed-back regulation of Th1 response by thioredoxin and IFN-gamma. Cell Physiol Biochem 21: 215-224.
31. Xie D, Bai H, Liu L, Xie X, Ayello J, et al. (2009) Apoptosis of lymphocytes and monocytes infected with influenza virus might be the mechanism of combating virus and causing secondary infection by influenza. Int Immunol 21: 1251-1262.
32. Palucka K, Banchereau J (2002) How dendritic cells and microbes interact to elicit or subvert protective immune responses. Curr Opin Immunol 14: 420-431.
33. Ok M, Latge JP, Baeuerlein C, Ebel F, Mezger M, et al. (2009) Immune responses of human immature dendritic cells can be modulated by the recombinant Aspergillus fumigatus antigen Aspf1. Clin Vaccine Immunol 16: 1485-1492.
34. Stanzani M, Orciuolo E, Lewis R, Kontoyiannis DP, Martins SL, et al. (2005) Aspergillus fumigatus suppresses the human cellular immune response via gliotoxin-mediated apoptosis of monocytes. Blood 105: 2258-2265.
35. Pardo J, Urban C, Galvez EM, Ekert PG, Muller 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.
36. Teutschbein J, Albrecht D, Potsch 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. J Proteome Res 9: 3427-3442.
37. Malicev E, Chowdhury HH, Macek P, Sepcic K (2007) Effect of ostreolysin, an Asp-hemolysin isoform, on human chondrocytes and osteoblasts, and possible role of Asp-hemolysin in pathogenesis. Med Mycol 45: 123-130.
38. Kamei K, Watanabe A (2005) Aspergillus mycotoxins and their effect on the host. Med Mycol 43 Suppl 1: S95-99.
39. Watts C (2006) Phagosome neutrality in host defense. Cell 126: 17-19.
40. Savina A, Jancic C, Hugues S, Guermonprez P, Vargas P, et al. (2006) NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126: 205-218.
41. Serrano-Gomez D, Dominguez-Soto A, Ancochea J, Jimenez-Heffernan JA, Leal JA, et al. (2004) Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J Immunol 173: 5635-5643.
42. Romani L, Bistoni F, Puccetti P (2002) Fungi, dendritic cells and receptors: a host perspective of fungal virulence. Trends Microbiol 10: 508-514.
43. Huang Q, Liu D, Majewski P, Schulte LC, Korn JM, et al. (2001) The plasticity of dendritic cell responses to pathogens and their components. Science 294: 870-875.
44. Serrano-Gomez D, Leal JA, Corbi AL (2005) DC-SIGN mediates the binding of Aspergillus fumigatus and keratinophylic fungi by human dendritic cells. Immunobiology 210: 175-183.
45. Balloy V, Chignard M (2009) The innate immune response to Aspergillus fumigatus. Microbes Infect 11: 919-927.
46. Krappmann S, Bignell EM, Reichard U, Rogers T, Haynes K, et al. (2004) The Aspergillus fumigatus transcriptional activator CpcA contributes significantly to the virulence of this fungal pathogen. Mol Microbiol 52: 785-799.
47. Braus GH, Sasse C, Krappmann S (2006) Amino acid acquisition, cross-pathway control, and virulence in Aspergillus. Med Mycol 44: S91-S94.
48. Sasse C, Bignell EM, Hasenberg M, Haynes K, Gunzer M, et al. (2008) Basal expression of the Aspergillus fumigatus transcriptional activator CpcA is sufficient to support pulmonary aspergillosis. Fungal Genet Biol 45: 693-704.
49. Lamarre C, Sokol S, Debeaupuis JP, Henry C, Lacroix C, et al. (2008) Transcriptomic analysis of the exit from dormancy of Aspergillus fumigatus conidia. BMC Genomics 9: 417.
50. Ibrahim-Granet O, Dubourdeau M, Latge JP, Ave P, Huerre M, et al. (2008) Methylcitrate synthase from Aspergillus fumigatus is essential for manifestation of invasive aspergillosis. Cell Microbiol 10: 134-148.
51. Miskei M, Karanyi Z, Pocsi I (2009) Annotation of stress-response proteins in the aspergilli. Fungal Genet Biol 46 Suppl 1: S105-120.
52. 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.
53. de Gouvea PF, Soriani FM, Malavazi I, Savoldi M, Goldman MH, et al. (2008) Functional characterization of the Aspergillus fumigatusPHO80 homologue. Fungal Genet Biol 45: 1135-1146.
54. Lambou K, Lamarre C, Beau R, Dufour N, Latge JP Functional analysis of the superoxide dismutase family in Aspergillus fumigatus. Mol Microbiol.
55. Paris S, Wysong D, Debeaupuis JP, Shibuya K, Philippe B, et al. (2003) Catalases of Aspergillus fumigatus. Infect Immun 71: 3551-3562.
56. Shibuya K, Paris S, Ando T, Nakayama H, Hatori T, et al. (2006) Catalases of Aspergillus fumigatus and inflammation in aspergillosis. Nippon Ishinkin Gakkai Zasshi 47: 249-255.
57. Schmaler-Ripcke J, Sugareva V, Gebhardt P, Winkler R, Kniemeyer O, et al. (2009) Production of pyomelanin, a second type of melanin, via the tyrosine degradation pathway in Aspergillus fumigatus. Appl Environ Microbiol 75: 493-503.
58. Valiante V, Jain R, Heinekamp T, Brakhage AA (2009) The MpkA MAP kinase module regulates cell wall integrity signaling and pyomelanin formation in Aspergillus fumigatus. Fungal Genet Biol 46: 909-918.
59. Beauvais A, Schmidt C, Guadagnini S, Roux P, Perret E, et al. (2007) An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus. Cell Microbiol 9: 1588-1600.
60. Langfelder K, Philippe B, Jahn B, Latge JP, Brakhage AA (2001) Differential expression of the Aspergillus fumigatus pksP gene detected in vitro and in vivo with green fluorescent protein. Infect Immun 69: 6411-6418.
61. Pihet M, Vandeputte P, Tronchin G, Renier G, Saulnier P, et al. (2009) Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol 9: 177.
62. Martinez-Ruiz A, Kao R, Davies J, Martinez del Pozo A (1999) Ribotoxins are a more widespread group of proteins within the filamentous fungi than previously believed. Toxicon 37: 1549-1563.
63. Lacadena J, Alvarez-Garcia E, Carreras-Sangra N, Herrero-Galan E, Alegre-Cebollada J, et al. (2007) Fungal ribotoxins: molecular dissection of a family of natural killers. FEMS Microbiol Rev 31: 212-237.
64. Li SM, Unsold IA (2006) Post-genome research on the biosynthesis of ergot alkaloids. Planta Med 72: 1117-1120.
65. Romani L (2008) Cell mediated immunity to fungi: a reassessment. Med Mycol. pp 1-15.
66. Bonifazi P, D'Angelo C, Zagarella S, Zelante T, Bozza S, et al. (2009) Intranasally delivered siRNA targeting PI3K/Akt/mTOR inflammatory pathways protects from aspergillosis. Mucosal Immunol.
67. Burns S, Thrasher AJ (2004) Dendritic cells: the bare bones of immunity. Curr Biol 14: R965-967.
68. Phadke AP, Mehrad B (2005) Cytokines in host defense against Aspergillus: recent advances. Med Mycol 43 Suppl 1: S173-176.
69. Baldwin AS, Jr. (1996) The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 14: 649-683.
70. Mezger M, Steffens M, Beyer M, Manger C, Eberle J, et al. (2008) Polymorphisms in the chemokine (C-X-C motif) ligand 10 are associated with invasive aspergillosis after allogeneic stem-cell transplantation and influence CXCL10 expression in monocyte-derived dendritic cells. Blood 111: 534-536.
71. Repetto G, del Peso A, Zurita JL (2008) Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc 3: 1125-1131.
72. Luther K, Ebel F (2006) Toll-like receptors: Recent advances, open questions and implications for aspergillosis control. Med Mycol 44: S219-S227.
73. 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.
74. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, opensource system for microarray data management and analysis. Biotechniques 34: 374-378.
75. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
76. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, et al. (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35: W71-74.
77. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
78. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M (2002) Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18 Suppl 1: S96-104.
79. Smyth GK, Speed TP (2003) Normalization of cDNA microarray data. Methods 31: 265-273.
80. Smyth GK, Michaud J, Scott HS (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21: 2067-2075.