Aspergillus fumigatus-derived gliotoxin impacts innate immune cell activation through modulating lipid mediator production in macrophages.
Aspergillus fumigatus
gliotoxin
leukotriene
lipid mediators
macrophages
prostaglandin
Journal
Immunology
ISSN: 1365-2567
Titre abrégé: Immunology
Pays: England
ID NLM: 0374672
Informations de publication
Date de publication:
13 Sep 2024
13 Sep 2024
Historique:
received:
15
03
2024
accepted:
20
08
2024
medline:
13
9
2024
pubmed:
13
9
2024
entrez:
13
9
2024
Statut:
aheadofprint
Résumé
Gliotoxin (GT), a secondary metabolite and virulence factor of the fungal pathogen Aspergillus fumigatus, suppresses innate immunity and supports the suppression of host immune responses. Recently, we revealed that GT blocks the formation of the chemotactic lipid mediator leukotriene (LT)B
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : 210879364
Organisme : Deutsche Forschungsgemeinschaft
ID : 239748522
Organisme : Deutsche Forschungsgemeinschaft
ID : 316213987
Informations de copyright
© 2024 The Author(s). Immunology published by John Wiley & Sons Ltd.
Références
Meena DS, Kumar D, Bohra GK, Kumar G. Clinical manifestations, diagnosis, and treatment outcome of CNS aspergillosis: A systematic review of 235 cases. Infect Dis Now. 2021;51(8):654–660.
Denning DW, Bromley MJ. How to bolster the antifungal pipeline. Science. 2015;347(6229):1414–1416.
Lockhart SR, Chowdhary A, Gold JAW. The rapid emergence of antifungal‐resistant human‐pathogenic fungi. Nat Rev Microbiol. 2023;21(12):818–832.
Maitre T, Cottenet J, Godet C, Roussot A, Abdoul Carime N, Ok V, et al. Chronic pulmonary aspergillosis: prevalence, favouring pulmonary diseases and prognosis. Eur Respir J. 2021;58(2):2003345.
Eichner RD, Al Salami M, Wood PR, Müllbacher A. The effect of gliotoxin upon macrophage function. Int J Immunopharmacol. 1986;8(7):789–797.
Scharf DH, Brakhage AA, Mukherjee PK. Gliotoxin—bane or boon? Environ Microbiol. 2016;18(4):1096–1109.
Chen H, Zhao R, Ge M, Sun Y, Li Y, Shan L. Gliotoxin, a natural product with ferroptosis inducing properties. Bioorg Chem. 2023;133:106415.
Pahl HL, Krauss B, Schulze‐Osthoff K, Decker T, Traenckner EB, Vogt M, et al. The immunosuppressive fungal metabolite gliotoxin specifically inhibits transcription factor NF‐kappaB. J Exp Med. 1996;183(4):1829–1840.
Orciuolo E, Stanzani M, Canestraro M, Galimberti S, Carulli G, Lewis R, et al. Effects of Aspergillus fumigatus gliotoxin and methylprednisolone on human neutrophils: implications for the pathogenesis of invasive aspergillosis. J Leukoc Biol. 2007;82(4):839–848.
Scharf DH, Heinekamp T, Brakhage AA. Human and plant fungal pathogens: the role of secondary metabolites. PLoS Pathog. 2014;10(1):e1003859.
König S, Pace S, Pein H, Heinekamp T, Kramer J, Romp E, et al. Gliotoxin from Aspergillus fumigatus abrogates leukotriene B4 formation through inhibition of leukotriene A4 hydrolase. Cell Chem Biol. 2019;26(4):524–534.e5.
Coméra C, André K, Laffitte J, Collet X, Galtier P, Maridonneau‐Parini I. Gliotoxin from Aspergillus fumigatus affects phagocytosis and the organization of the actin cytoskeleton by distinct signalling pathways in human neutrophils. Microbes Infect. 2007;9(1):47–54.
Waringt P. Gliotoxin induces apoptosis in macrophages unrelated to its phagocytic properties. J Biol Chem. 1988;263:18493–18499.
Jordan PM, Werz O. Specialized pro‐resolving mediators: biosynthesis and biological role in bacterial infections. FEBS J. 2022;289(14):4212–4227.
Schwab JM, Chiang N, Arita M, Serhan CN. Resolvin E1 and protectin D1 activate inflammation‐resolution programmes. Nature. 2007;447(7146):869–874.
Haeggström JZ, Funk CD. Lipoxygenase and leukotriene pathways: biochemistry, biology, and roles in disease. Chem Rev. 2011;111(10):5866–5898.
Werz O, Gerstmeier J, Libreros S, De la Rosa X, Werner M, Norris PC, et al. Human macrophages differentially produce specific resolvin or leukotriene signals that depend on bacterial pathogenicity. Nat Commun. 2018;9(1):59.
Werner M, Jordan PM, Romp E, Czapka A, Rao Z, Kretzer C, et al. Targeting biosynthetic networks of the proinflammatory and proresolving lipid metabolome. FASEB J. 2019;33(5):6140–6153.
Rådmark O, Werz O, Steinhilber D, Samuelsson B. 5‐Lipoxygenase, a key enzyme for leukotriene biosynthesis in health and disease. Bioch Biophys Acta (BBA)—Mol Cell Biol Lipids. 2015;1851(4):331–339.
Martin TR, Pistorese BP, Chi EY, Goodman RB, Matthay MA. Effects of leukotriene B4 in the human lung. Recruitment of neutrophils into the alveolar spaces without a change in protein permeability. J Clin Invest. 1989;84(5):1609–1619.
Rola‐Pleszczynski M, Stankova J. Leukotriene B4 enhances interleukin‐6 (IL‐6) production and IL‐6 messenger rna accumulation in human monocytes in vitro: transcriptional and posttranscriptional mechanisms. Blood. 1992;80(4):1004–1011.
Crooks SW, Stockley RA. Leukotriene B4. Int J Biochem Cell Biol. 1998;30(2):173–178.
Surette ME, Palmantier R, Gosselin J, Borgeat P. Lipopolysaccharides prime whole human blood and isolated neutrophils for the increased synthesis of 5‐lipoxygenase products by enhancing arachidonic acid availability: involvement of the CD14 antigen. J Exp Med. 1993;178(4):1347–1355.
Czop JK, Austen KF. Generation of leukotrienes by human monocytes upon stimulation of their beta‐glucan receptor during phagocytosis. Proc Natl Acad Sci. 1985;82(9):2751–2755.
Caffrey‐Carr AK, Hilmer KM, Kowalski CH, Shepardson KM, Temple RM, Cramer RA, et al. Host‐derived leukotriene B4 is critical for resistance against invasive pulmonary aspergillosis. Front Immunol. 2018;8:1984.
Askonas LJ, Kachur JF, Villani‐Price D, Liang CD, Russell MA, Smith WG. Pharmacological characterization of SC‐57461A (3‐[methyl[3‐[4‐(phenylmethyl)phenoxy]propyl]amino]propanoic acid HCl), a potent and selective inhibitor of leukotriene A(4) hydrolase I: in vitro studies. J Pharmacol Exp Ther. 2002;300(2):577–582.
Stanzani M, Orciuolo E, Lewis R, Kontoyiannis DP, Martins SLR, St. John LS, et al. Aspergillus fumigatus suppresses the human cellular immune response via gliotoxin‐mediated apoptosis of monocytes. Blood. 2005;105(6):2258–2265.
Suen YK, Fung KP, Lee CY, Kong SK. Gliotoxin induces apoptosis in cultured macrophages via production of reactive oxygen species and cytochrome c release without mitochondrial depolarization. Free Radic Res. 2001;35(1):1–10.
Jordan PM, Gerstmeier J, Pace S, Bilancia R, Rao Z, Börner F, et al. Staphylococcus aureus‐derived α‐hemolysin evokes generation of specialized pro‐resolving mediators promoting inflammation resolution. Cell Rep. 2020;33(2):108247.
Ford‐Hutchinson AW, Bray MA, Doig MV, Shipley ME, Smith MJ. Leukotriene B, a potent chemokinetic and aggregating substance released from polymorphonuclear leukocytes. Nature. 1980;286(5770):264–265.
Wirth JJ, Kierszenbaum F. Stimulatory effects of leukotriene B4 on macrophage association with and intracellular destruction of Trypanosoma cruzi. J Immunol. 1985;134(3):1989–1993.
Gijon MA, Spencer DM, Siddiqi AR, Bonventre JV, Leslie CC. Cytosolic phospholipase A2 is required for macrophage arachidonic acid release by agonists that Do and Do not mobilize calcium. Novel role of mitogen‐activated protein kinase pathways in cytosolic phospholipase A2 regulation. J Biol Chem. 2000;275(26):20146–20156.
Liu T, Zhang L, Joo D, Sun SC. NF‐kappaB signaling in inflammation. Signal Transduct Target Ther. 2017;2:17023.
Arias M, Santiago L, Vidal‐Garcia M, Redrado S, Lanuza P, Comas L, et al. Preparations for invasion: modulation of host lung immunity during pulmonary aspergillosis by gliotoxin and other fungal secondary metabolites. Front Immunol. 2018;9:2549.
Joshi N, Walter JM, Misharin AV. Alveolar Macrophages. Cell Immunol. 2018;330:86–90.
Wang Z, Brandt S, Medeiros A, Wang S, Wu H, Dent A, et al. MicroRNA 21 is a homeostatic regulator of macrophage polarization and prevents prostaglandin E2‐mediated M2 generation. PLoS One. 2015;10(2):e0115855.
Rao Z, Pace S, Jordan PM, Bilancia R, Troisi F, Börner F, et al. Vacuolar (H(+))‐ATPase critically regulates specialized proresolving mediator pathways in human M2‐like monocyte‐derived macrophages and has a crucial role in resolution of inflammation. J Immunol. 2019;203(4):1031–1043.
Jones CN, Dimisko L, Forrest K, Judice K, Poznansky MC, Markmann JF, et al. Human neutrophils are primed by chemoattractant gradients for blocking the growth of Aspergillus fumigatus. J Infect Dis. 2016;213(3):465–475.
Caffrey‐Carr AK, Hilmer KM, Kowalski CH, Shepardson KM, Temple RM, Cramer RA, et al. Host‐derived leukotriene B(4) is critical for resistance against invasive pulmonary aspergillosis. Front Immunol. 2017;8:1984.
Leslie CC. Cytosolic phospholipase A(2): physiological function and role in disease. J Lipid Res. 2015;56(8):1386–1402.
Norris PC, Gosselin D, Reichart D, Glass CK, Dennis EA. Phospholipase A2 regulates eicosanoid class switching during inflammasome activation. Proc Natl Acad Sci USA. 2014;111(35):12746–12751.
Pueringer RJ, Hunninghake GW. Lipopolysaccharide stimulates de novo synthesis of PGH synthase in human alveolar macrophages. Am J Physiol. 1992;262(1 Pt 1):L78–L85.
Miek L, Jordan PM, Gunther K, Pace S, Beyer T, Kowalak D, et al. Staphylococcus aureus controls eicosanoid and specialized pro‐resolving mediator production via lipoteichoic acid. Immunology. 2022;166(1):47–67.
Park SJ, Mehrad B. Innate immunity to Aspergillus species. Clin Microbiol Rev. 2009;22(4):535–551.
Kroll M, Arenzana‐Seisdedos F, Bachelerie F, Thomas D, Friguet B, Conconi M. The secondary fungal metabolite gliotoxin targets proteolytic activities of the proteasome. Chem Biol. 1999;6(10):689–698.
Gupta SC, Sundaram C, Reuter S, Aggarwal BB. Inhibiting NF‐κB activation by small molecules as a therapeutic strategy. Biochim Biophys Acta. 2010;1799(10–12):775–787.
Devillier P, Bessard G. Thromboxane A2 and related prostaglandins in airways. Fundam Clin Pharmacol. 1997;11(1):2–18.
Lopez‐Vidriero MT, Das I, Smith AP, Picot R, Reid L. Bronchial secretion from normal human airways after inhalation of prostaglandin F2alpha, acetylcholine, histamine, and citric acid. Thorax. 1977;32(6):734–739.
Thrikawala S, Niu M, Keller NP, Rosowski EE. Cyclooxygenase production of PGE2 promotes phagocyte control of A. fumigatus hyphal growth in larval zebrafish. PLoS Pathog. 2022;18(3):e1010040.
Liu H, Zheng M, Qiao J, Dang Y, Zhang P, Jin X. Role of prostaglandin D2 /CRTH2 pathway on asthma exacerbation induced by Aspergillus fumigatus. Immunology. 2014;142(1):78–88.
Oga T, Matsuoka T, Yao C, Nonomura K, Kitaoka S, Sakata D, et al. Prostaglandin F(2alpha) receptor signaling facilitates bleomycin‐induced pulmonary fibrosis independently of transforming growth factor‐beta. Nat Med. 2009;15(12):1426–1430.
Maehara T, Fujimori K. Inhibition of prostaglandin F(2)(alpha) receptors exaggerates HCl‐induced lung inflammation in mice. Int J Mol Sci. 2021;22(23):12843.
Ricciotti E, FitzGerald GA. Prostaglandins and inflammation. Arterioscler Thromb Vasc Biol. 2011;31(5):986–1000.
Dunne K, Reece E, McClean S, Doyle S, Rogers TR, Murphy P, et al. Aspergillus fumigatus supernatants disrupt bronchial epithelial monolayers: potential role for enhanced invasion in cystic fibrosis. J Fungi. 2023;9(4):490.
Speth C, Hagleitner M, Ott HW, Würzner R, Lass‐Flörl C, Rambach G. Aspergillus fumigatus activates thrombocytes by secretion of soluble compounds. J Infect Dis. 2013;207(5):823–833.
Ye W, Liu T, Zhang W, Zhang W. The toxic mechanism of gliotoxins and biosynthetic strategies for toxicity prevention. Int J Mol Sci. 2021;22(24):13510.
Johannessen LN, Nilsen AM, Løvik M. The mycotoxins citrinin and gliotoxin differentially affect production of the pro‐inflammatory cytokines tumour necrosis factor‐alpha and interleukin‐6, and the anti‐inflammatory cytokine interleukin‐10. Clin Exp Allergy. 2005;35(6):782–789.
Murray PJ, Allen JE, Biswas SK, Fisher EA, Gilroy DW, Goerdt S, et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 2014;41(1):14–20.
Colas RA, Shinohara M, Dalli J, Chiang N, Serhan CN. Identification and signature profiles for pro‐resolving and inflammatory lipid mediators in human tissue. Am J Physiol Cell Physiol. 2014;307(1):C39–C54.
Peltner LK, Gluthmann L, Börner F, Pace S, Hoffstetter RK, Kretzer C, et al. Cannabidiol acts as molecular switch in innate immune cells to promote the biosynthesis of inflammation‐resolving lipid mediators. Cell Chem Biol. 2023;30(12):1508–1524.e7.
Ikeda M, Futami M, Chanda B, Kobayashi M, Izawa K, Tojo A. The mouse homolog of the mutant WASp responsible for human X‐linked neutropenia renders granulopoiesis ineffective. Biochem Biophys Res Commun. 2022;622:177–183.
Gerst R, Cseresnyés Z, Figge MT. JIPipe: visual batch processing for ImageJ. Nat Methods. 2023;20(2):168–169.
Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–675.
Schindelin J, Arganda‐Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open‐source platform for biological‐image analysis. Nat Methods. 2012;9(7):676–682.
Stringer C, Wang T, Michaelos M, Pachitariu M. Cellpose: a generalist algorithm for cellular segmentation. Nat Methods. 2021;18(1):100–106.
Tinevez JY, Perry N, Schindelin J, Hoopes GM, Reynolds GD, Laplantine E, et al. TrackMate: an open and extensible platform for single‐particle tracking. Methods. 2017;115:80–90.
Hoang TNM, Cseresnyés Z, Hartung S, Blickensdorf M, Saffer C, Rennert K, et al. Invasive aspergillosis‐on‐chip: a quantitative treatment study of human Aspergillus fumigatus infection. Biomaterials. 2022;283:121420.
Wessel D, Flügge UI. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem. 1984;138(1):141–143.