A possible role for fumagillin in cellular damage during host infection by Aspergillus fumigatus

References

• Latgé JP. Aspergillus fumigatus and Aspergillosis. Clin Microbiol Rev. 1999;12:310–350.
   PubMed Web of Science ®Google Scholar
• Alastruey-Izquierdo A, Mellado E, Peláez T, et al. Population-based survey of filamentous fungi and antifungal resistance in Spain (FILPOP study). Antimicrob Agents Chemother. 2013;57:3380–3387.
   PubMed Web of Science ®Google Scholar
• Kosmidis C, Denning DW. The clinical spectrum of pulmonary aspergillosis. Thorax. 2015;70:270–277.
   PubMed Web of Science ®Google Scholar
• Bennett JW. An overview of the genus Aspergillus. In: Machida M, Gomi K, editors. Aspergillus molecular biology and genomics. Portland: Casier Academic Press; 2010. p. 1–18.
   Google Scholar
• Hope WW. Invasion of the alveolar-capillary barrier by Aspergillus spp.: therapeutic and diagnostic implications for immunocompromised patients with invasive pulmonary aspergillosis. Med Mycol. 2009;47:S291–S298.
   PubMed Web of Science ®Google Scholar
• Escobar N, Ordonez SR, Wösten HAB, et al. Hide, keep quiet, and keep low : properties that make Aspergillus fumigatus a successful lung pathogen. Front Microbiol. 2016;7:438.
   PubMed Web of Science ®Google Scholar
• Phillippe B, Ibrahim-Granet O, Prévost MC, et al. Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infect Immun. 2003;71:3034–3042.
   PubMed Web of Science ®Google Scholar
• Kerr SC, Fischer GJ, Sinha M, et al. FleA expression in Aspergillus fumigatus is recognized by fucosylated structures on mucins and macrophages to prevent lung infection. PLoS Pathog. 2016;12:e1005555.
   PubMed Web of Science ®Google Scholar
• Slesiona S, Gressler M, Mihlan M, et al. Persistence versus escape: aspergillus terreus and Aspergillus fumigatus employ different strategies during interactions with macrophages. PLoS One. 2012;7:e31223.
   PubMed Web of Science ®Google Scholar
• Tekaia F, Latgé JP. Aspergillus fumigatus: saprophyte or pathogen?. Curr Opin Microbiol. 2005;8:385–392.
   PubMed Web of Science ®Google Scholar
• Osherov N. The virulence of Aspergillus fumigatus. In: Kavanag K, editor. New Insihgts in Medical Mycology. Dordrecht: Springer; 2007. p. 185–213.
   Google Scholar
• Abad A, Victoria Fernández-Molina J, Bikandi J, et al. What makes Aspergillus fumigatus a successful pathogen? Genes and molecules involved in invasive aspergillosis. Rev Iberoam Micol. 2010;27:155–182.
   PubMed Web of Science ®Google Scholar
• Singh B, Oellerich M, Kumar R, et al. Immuno-reactive molecules identified from the secreted proteome of Aspergillus fumigatus. J Proteome Res. 2010;9:5517–5529.
   PubMed Web of Science ®Google Scholar
• Kumar A, Ahmed R, Singh PK, et al. Identification of virulence factors and diagnostic markers using immunosecretome of Aspergillus fumigatus. J Proteomics. 2011;74:1104–1112.
   PubMed Web of Science ®Google Scholar
• Virginio ED, Kubitschek-Barreira PH, Vieira Batista M, et al. Immunoproteome of Aspergillus fumigatus using sera of patients with invasive aspergillosis. Int J Mol Sci. 2014;15:14505–14530.
   PubMed Web of Science ®Google Scholar
• Bignell E, Cairns TC, Throckmorton K, et al. Secondary metabolite arsenal of an opportunistic pathogenic fungus. Phil Trans R Soc B. 2016;371:20160023.
   PubMed Web of Science ®Google Scholar
• Sueiro-Olivares M, Fernandez-Molina JV, Abad-Diaz-de-Cerio A, et al. Aspergillus fumigatus transcriptome response to a higher temperature during the earliest steps of germination monitored using a new customized expression microarray. Microbiology. 2015;161:490–502.
   PubMed Web of Science ®Google Scholar
• Barker BM, Kroll K, Vödisch M, et al. Transcriptomic and proteomic analyses of the Aspergillus fumigatus hypoxia response using an oxygen-controlled fermenter. BMC Genomics. 2012;13:62.
   PubMed Web of Science ®Google Scholar
• Irmer H, Tarazona S, Sasse C, et al. RNAseq analysis of Aspergillus fumigatus in blood reveals a just wait and see resting stage behavior. BMC Genomics. 2015;16:640.
   PubMed Web of Science ®Google Scholar
• Oosthuizen JL, Gomez P, Ruan J, et al. Dual organism transcriptomics of airway epithelial cells interacting with conidia of Aspergillus fumigatus. PLoS One. 2011;6:e20257.
   PubMed Web of Science ®Google Scholar
• Bertuzzi M, Schrettl M, Alcazar-Fuoli L, et al. The pH-responsive PacC ranscription factor of Aspergillus fumigatus governs epithelial entry and tissue invasion during pulmonary aspergillosis. PLoS Pathog. 2014;11:e1004943.
   Google Scholar
• Mcdonagh A, Fedorova ND, Crabtree J, et al. Sub-telomere directed gene expression during initiation of invasive aspergillosis. PLoS Pathog. 2008;4:e10000154.
   Web of Science ®Google Scholar
• Oda K, Bignell E, Kang SE, et al. Transcript levels of the Aspergillus fumigatus Cdc42 module, polarisome, and septin genes show little change from dormancy to polarity establishment. Med Mycol. 2016;155:445–452.
   Google Scholar
• Wiemann P, Guo C-J, Palmer JM, et al. Prototype of an intertwined secondary-metabolite supercluster. Proc Natl Acad Sci U S A. 2013;110:17065–17070.
   PubMed Web of Science ®Google Scholar
• Wallwey C, Matuschek M, Li SM. Ergot alkaloid biosynthesis in Aspergillus fumigatus: conversion of chanoclavine-I to chanoclavine-I aldehyde catalyzed by a short-chain alcohol dehydrogenase FgaDH. Arch Microbiol. 2010;192:127–134.
   PubMed Web of Science ®Google Scholar
• Dhingra S, Lind AL, Lin HC, et al. The fumagillin gene cluster, an example of hundreds of genes under veA control in Aspergillus fumigatus. PLoS One. 2013;8:e77147.
   PubMed Web of Science ®Google Scholar
• Ibrahim-Granet O, Jouvion G, Hohl TM, et al. In vivo bioluminescence imaging and histopathopathologic analysis reveal distinct roles for resident and recruited immune effector cells in defense against invasive aspergillosis. BMC Microbiol. 2010;10:105.
   PubMed Web of Science ®Google Scholar
• Cairns T, Minuzzi F, Bignell E. The host-infecting fungal transcriptome. FEMS Microbiol Lett. 2010;307:1–11.
   PubMed Web of Science ®Google Scholar
• Da Silva Ferreira ME, Malavazi I, Savoldi M, et al. Transcriptome analysis of Aspergillus fumigatus exposed to voriconazole. Curr Genet. 2006;50:32–44.
   PubMed Web of Science ®Google Scholar
• Rokas A, Gibbons JG, Zhou X, et al. The diverse applications of RNA-seq for functional genomic studies in Aspergillus fumigatus. Ann N Y Acad Sci. 2012;1273:25–34.
   PubMed Web of Science ®Google Scholar
• van de Veerdonk FL, Gresnigt MS, Romani L, et al. Aspergillus fumigatus morphology and dynamic host interactions. Nat Rev Microbiol. 2017;15:661–674.
   PubMed Web of Science ®Google Scholar
• Dagenais TRT, Keller NP. Pathogenesis of Aspergillus fumigatus in invasive aspergillosis. Clin Microbiol Rev. 2009;22:447–465.
   PubMed Web of Science ®Google Scholar
• Berthier E, Lim FY, Deng Q, et al. Low-volume toolbox for the discovery of immunosuppressive fungal secondary metabolites. PLoS Pathog. 2013;9:e1003289.
   PubMed Web of Science ®Google Scholar
• Kanno T, Uehara T, Osawa M, et al. Fumagillin, a potent angiogenesis inhibitor, induces Kaposi sarcoma-associated herpesvirus replication in primary effusion lymphoma cells. Biochem Biophys Res Commun. 2015;463:1267–1272.
   PubMed Web of Science ®Google Scholar
• Laschke MW, Menger MD. Anti-angiogenic treatment strategies for the therapy of endometriosis. Hum Reprod Update. 2012;18:682–702.
   PubMed Web of Science ®Google Scholar
• Ito JI. Enhancing Angiogenesis in Invasive Aspergillosis : A Novel therapeutic approach. J Infect Dis. 2013;207:1031–1033.
   PubMed Web of Science ®Google Scholar
• Chiang LY, Sheppard DC, Gravelat FN, et al. Aspergillus fumigatus stimulates leukocyte adhesion molecules and cytokine production by endothelial cells in vitro and during invasive pulmonary disease. Infect Immun. 2008;76:3429–3438.
   PubMed Web of Science ®Google Scholar
• Yoshida S, Ono M, Shono T, et al. Involvement of interleukin-8, vascular endothelial growth factor, and basic fibroblast growth factor in tumor necrosis factor alpha-dependent angiogenesis. Mol Cell Biol. 1997;17:4015–4023.
   PubMed Web of Science ®Google Scholar
• Ingber D, Fujita T, Kishimoto S, et al. Synthetic analogues of fumagillin that inhibit angiogenesis and suppress tumour growth. Nature. 1990;348:555–557.
   PubMed Web of Science ®Google Scholar
• Kusaka M, Sudo K, Fujita T, et al. Potent anti-angiogenic action of AGM-1470: comparison to the fumagillin parent. Biochem Biophys Res Commun. 1991;174:1070–1076.
   PubMed Web of Science ®Google Scholar
• Ben-Ami R, Albert ND, Lewis RE, et al. Proangiogenic growth factors potentiate in situ angiogenesis and enhance antifungal drug activity in murine invasive aspergillosis. J Infect Dis. 2013;207:1066–1074.
   PubMed Web of Science ®Google Scholar
• Lin HC, Chooi YH, Dhingra S, et al. The fumagillin biosynthetic gene cluster in Aspergillus fumigatus encodes a cryptic terpene cyclase involved in the formation of β-trans-bergamotene. J Am Chem Soc. 2013;135:4616–4619.
   PubMed Web of Science ®Google Scholar
• Killough JH, Magill GB, Smith RC. The Treatment of amebiasis with fumagillin. Science. 1952;115:71–72.
   PubMed Web of Science ®Google Scholar
• Jean-Michel M, Muriel T, Claudine S, et al. Fumagillin treatment of intestinal microsporidiosis. N Engl J Med. 2016;346:1963–1969.
   Google Scholar
• Sin N, Meng L, Wang MQW, et al. The anti-angiogenic agent fumagillin covalently binds and inhibits the methionine aminopeptidase, MetAP-2. Proc Natl Acad Sci U S A. 1997;94:6099–6103.
   PubMed Web of Science ®Google Scholar
• Fallon JP, Reeves EP, Kavanagh K. The Aspergillus fumigatus toxin fumagillin suppresses the immune response of Galleria mellonella larvae by inhibiting the action of haemocytes. Microbiology. 2011;157:1481–1488.
   PubMed Web of Science ®Google Scholar
• Shi YS, Zhang Y, Chen XZ, et al. Metabolites produced by the endophytic fungus Aspergillus fumigatus from the stem of Erythrophloeum fordii oliv. Molecules. 2015;20:10793–10799.
   PubMed Web of Science ®Google Scholar
• Krappmann S. How to invade a susceptible host: cellular aspects of aspergillosis. Curr Opin Microbiol. 2016;34:136–146.
   PubMed Web of Science ®Google Scholar
• Asif AR, Oellerich M, Amstrong VW, et al. Proteome of conidial surface associated proteins of Aspergillus fumigatus reflecting potential vaccine candidates and allergens. J Proteome Res. 2006;5:954–962.
   PubMed Web of Science ®Google Scholar
• Arruda LK, Mann BJ, Chapman MD. Selective expression of a major allergen and cytotoxin, Asp f I, in Aspergillus fumigatus. Implications for the immunopathogenesis of Aspergillus-related diseases. J Immunol. 1992;149:3354–3359.
   PubMed Web of Science ®Google Scholar
• Gravelat FN, Doedt T, Chiang LY, et al. In vivo analysis of Aspergillus fumigatus developmental gene expression determined by real-time reverse transcription-PCR. Infect Immun. 2008;76:3632–3639.
   PubMed Web of Science ®Google Scholar
• Jaques AK, Fukamizo T, Hall D, et al. Disruption of the gene encoding the ChiB1 chitinase of Aspergillus fumigatus and characterization of a recombinant gene product. Microbiology. 2003;149:2931–2939.
   PubMed Web of Science ®Google Scholar
• Alcazar-Fuoli L, Clavaud C, Lamarre C, et al. Functional analysis of the fungal/plant class chitinase family in Aspergillus fumigatus. Fungal Genet Biol. 2011;48:418–429.
   PubMed Web of Science ®Google Scholar
• Ramirez-Garcia A, Pellon A, Buldain I, et al. Proteomics as a tool to identify new targets against Aspergillus and Scedosporium in the context of cystic fibrosis. Mycopathologia. 2018;183:273–289.
   PubMed Web of Science ®Google Scholar
• Schmaler-Ripcke J, Sugareva V, Gebhardt P, et al. Production of pyomelanin, a second type of melanin, via the tyrosine degradation pathway in Aspergillus fumigatus. Appl Environ Microbiol. 2009;75:493–503.
   PubMed Web of Science ®Google Scholar
• Heinekamp T, Thywißen A, Macheleidt J, et al. Aspergillus fumigatus melanins: interference with the host endocytosis pathway and impact on virulence. Front Microbiol. 2012;3:440.
   PubMed Web of Science ®Google Scholar
• Bok JW, Keller NP. LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell. 2004;3:527–535.
   PubMed Web of Science ®Google Scholar
• Sambrook J, Fritsch EF, Maniatis T. Molecular cloning : a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989. p. 1–18.
   Google Scholar
• Alexander NJ, Hohn TM, Mccormick SP. The TRI11 gene of Fusarium sporotrichioides encodes a cytochrome P-450 monooxygenase required for C-15 hydroxylation in trichothecene biosynthesis. Appl Environ Microbiol. 1998;64:221–225.
   PubMed Web of Science ®Google Scholar
• López-Romero P. Pre-processing and differential expression analysis of Agilent microRNA arrays using the AgiMicroRna Bioconductor library. BMC Genomics. 2011;12:64.
   PubMed Web of Science ®Google Scholar
• Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:1–25. Article 3.
   Google Scholar
• Lopes Bezerra LM, Filler SG. Interactions of Aspergillus fumigatus with endothelial cells: internalization, injury, and stimulation of tissue factor activity. Blood. 2004;103:2143–2149.
   PubMed Web of Science ®Google Scholar
• Wiemann P, Lechner BE, Baccile JA, et al. Perturbations in small molecule synthesis uncovers an iron-responsive secondary metabolite network in Aspergillus fumigatus. Front Microbiol. 2014;5:530.
   PubMed Web of Science ®Google Scholar