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Research Paper

The mitochondrial thiamine pyrophosphate transporter TptA promotes adaptation to low iron conditions and virulence in fungal pathogen Aspergillus fumigatus

, , , , & ORCID Icon
Pages 234-247 | Received 17 Oct 2018, Accepted 10 Mar 2019, Published online: 28 Mar 2019

References

  • Ratledge C, Dover LG. Iron metabolism in pathogenic bacteria. Annu Rev Microbiol. 2000;54:881–941.
  • Haas H. Iron – a key nexus in the virulence of Aspergillus fumigatus. Front Microbiol. 2012;3.
  • Seifert M, Nairz M, Schroll A, et al. Effects of the Aspergillus fumigatus siderophore systems on the regulation of macrophage immune effector pathways and iron homeostasis. Immunobiology. 2008;213:767–778.
  • Jung WH, Do E. Iron acquisition in the human fungal pathogen Cryptococcus neoformans. Curr Opin Microbiol. 2013;16:686–691.
  • Moore MM. The crucial role of iron uptake in Aspergillus fumigatus virulence. Curr Opin Microbiol. 2013;16:692–699.
  • Martin RB, Savory J, Brown S, et al. Transferrin binding of Al3+ and Fe3+. Clin Chem. 1987;33:405–407.
  • Halliwell B, Gutteridge JM. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J. 1984;219:1–14.
  • Tekaia F, Latge JP. Aspergillus fumigatus: saprophyte or pathogen?. Curr Opin Microbiol. 2005;8:385–392.
  • Abad A, Fernandez-Molina JV, 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.
  • Neofytos D, Treadway S, Ostrander D, et al. Epidemiology, outcomes, and mortality predictors of invasive mold infections among transplant recipients: a 10-year, single-center experience. Transpl Infect Dis. 2013;15:233–242.
  • Klingspor L, Saaedi B, Ljungman P, et al. Epidemiology and outcomes of patients with invasive mould infections: a retrospective observational study from a single centre (2005–2009). Mycoses. 2015;58:470–477.
  • Corzo-Leon DE, Satlin MJ, Soave R, et al. Epidemiology and outcomes of invasive fungal infections in allogeneic haematopoietic stem cell transplant recipients in the era of antifungal prophylaxis: a single-centre study with focus on emerging pathogens. Mycoses. 2015;58:325–336.
  • Schrettl M, Bignell E, Kragl C, et al. Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J Exp Med. 2004;200:1213–1219.
  • Schrettl M, Beckmann N, Varga J, et al. HapX-mediated adaption to iron starvation is crucial for virulence of Aspergillus fumigatus. PLoS Pathog. 2010;6:e1001124.
  • Schrettl M, Kim HS, Eisendle M, et al. SreA-mediated iron regulation in Aspergillus fumigatus. Mol Microbiol. 2008;70:27–43.
  • Marobbio CM, Vozza A, Harding M, et al. Identification and reconstitution of the yeast mitochondrial transporter for thiamine pyrophosphate. Embo J. 2002;21:5653–5661.
  • Liu YG, Whittier RF. Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics. 1995;25:674–681.
  • Schrettl M, Bignell E, Kragl C, et al. Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathog. 2007;3:1195–1207.
  • Yasmin S, Alcazar-Fuoli L, Grundlinger M, et al. Mevalonate governs interdependency of ergosterol and siderophore biosyntheses in the fungal pathogen Aspergillus fumigatus. Proc Natl Acad Sci U S A. 2012;109:E497–504.
  • Palmieri F. Diseases caused by defects of mitochondrial carriers: a review. Bba-Bioenergetics. 2008;1777:564–578.
  • Sabui S, Subramanian VS, Kapadia R, et al. Structure-function characterization of the human mitochondrial thiamin pyrophosphate transporter (hMTPPT; SLC25A19): important roles for Ile(33), Ser(34), Asp(37), His(137) and Lys(291). Bba-Biomembranes. 2016;1858:1883–1890.
  • Subramanian VS, Nabokina SM, Lin-Moshier Y, et al. Mitochondrial uptake of thiamin pyrophosphate: physiological and cell biological aspects. Plos One. 2013;8(8):e73503.
  • Philippe B, Ibrahim-Granet O, Prevost MC, et al. Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infect Immun. 2003;71:3034–3042.
  • Schobel F, Jacobsen ID, Brock M. Evaluation of lysine biosynthesis as an antifungal drug target: biochemical characterization of Aspergillus fumigatus homocitrate synthase and virulence studies. Eukaryot Cell. 2010;9:878–893.
  • Ding C, Festa RA, Sun TS, et al. Iron and copper as virulence modulators in human fungal pathogens. Mol Microbiol. 2014;93:10–23.
  • Jackson JC, Higgins LA, Lin X. Conidiation color mutants of Aspergillus fumigatus are highly pathogenic to the heterologous insect host Galleria mellonella. PLoS One. 2009;4:e4224.
  • Bettendorff L, Wins P. Thiamin diphosphate in biological chemistry: new aspects of thiamin metabolism, especially triphosphate derivatives acting other than as cofactors. FEBS J. 2009;276:2917–2925.
  • Dietl AM, Meir Z, Shadkchan Y, et al. Riboflavin and pantothenic acid biosynthesis are crucial for iron homeostasis and virulence in the pathogenic mold Aspergillus fumigatus.. Virulence. 2018;9:1036–1049.
  • Hohmann S, Meacock PA. Thiamin metabolism and thiamin diphosphate-dependent enzymes in the yeast Saccharomyces cerevisiae: genetic regulation. Biochim Biophys Acta. 1998;1385:201–219.
  • Iacopetta D, Carrisi C, De Filippis G, et al. The biochemical properties of the mitochondrial thiamine pyrophosphate carrier from Drosophila melanogaster. FEBS J. 2010;277:1172–1181.
  • Lindhurst MJ, Fiermonte G, Song S, et al. Knockout of Slc25a19 causes mitochondrial thiamine pyrophosphate depletion, embryonic lethality, CNS malformations, and anemia. Proc Natl Acad Sci U S A. 2006;103:15927–15932.
  • Hortschansky P, Eisendle M, Al-Abdallah Q, et al. Interaction of HapX with the CCAAT-binding complex–a novel mechanism of gene regulation by iron. Embo J. 2007;26:3157–3168.
  • Zhang T, Bu P, Zeng J, et al. Increased heme synthesis in yeast induces a metabolic switch from fermentation to respiration even under conditions of glucose repression. J Biol Chem. 2017;292:16942–16954.
  • Oliver JD, Kaye SJ, Tuckwell D, et al. The Aspergillus fumigatus dihydroxyacid dehydratase Ilv3A/IlvC is required for full virulence. PLoS One. 2012;7:e43559.
  • Sugui JA, Chang YC, Kwon-Chung KJ. Agrobacterium tumefaciens-mediated transformation of Aspergillus fumigatus: an efficient tool for insertional mutagenesis and targeted gene disruption. Appl Environ Microbiol. 2005;71:1798–1802.
  • Szewczyk E, Nayak T, Oakley CE, et al. Fusion PCR and gene targeting in Aspergillus nidulans. Nat Protoc. 2006;1:3111–3120.
  • Oberegger H, Schoeser M, Zadra I, et al. SREA is involved in regulation of siderophore biosynthesis, utilization and uptake in Aspergillus nidulans. Mol Microbiol. 2001;41:1077–1089.
  • Konetschny-Rapp S, Huschka HG, Winkelmann G, et al. High-performance liquid chromatography of siderophores from fungi. Biol Met. 1988;1:9–17.
  • Long N, Xu X, Qian H, et al. A putative mitochondrial iron transporter MrsA in Aspergillus fumigatus plays important roles in azole-, oxidative stress responses and virulence. Front Microbiol. 2016;7:716.
  • Gravelat FN, Beauvais A, Liu H, et al. Aspergillus galactosaminogalactan mediates adherence to host constituents and conceals hyphal beta-glucan from the immune system. PLoS Pathog. 2013;9:e1003575.
  • Lee MJ, Geller AM, Bamford NC, et al. Deacetylation of fungal exopolysaccharide mediates adhesion and biofilm formation. MBio. 2016;7:e00252–16.