Candida albicans-induced leukotriene biosynthesis in neutrophils is restricted to the hyphal morphology.
5-lipoxygenase
fungi
immune response
inflammation
lipid mediator
oxylipins
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
revised:
09
07
2021
received:
28
03
2021
accepted:
12
07
2021
entrez:
27
9
2021
pubmed:
28
9
2021
medline:
21
10
2021
Statut:
ppublish
Résumé
Neutrophils are the most abundant leukocytes in circulation playing a key role in acute inflammation during microbial infections. Phagocytosis, one of the crucial defence mechanisms of neutrophils against pathogens, is amplified by chemotactic leukotriene (LT)B
Identifiants
pubmed: 34569657
doi: 10.1096/fj.202100516RR
doi:
Substances chimiques
Leukotrienes
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e21820Informations de copyright
© 2021 The Authors. The FASEB Journal published by Wiley Periodicals LLC on behalf of Federation of American Societies for Experimental Biology.
Références
Davies LC, Jenkins SJ, Allen JE, Taylor PR. Tissue-resident macrophages. Nat Immunol. 2013;14:986-995.
Desai JV, Lionakis MS. The role of neutrophils in host defense against invasive fungal infections. Curr Clin Microbiol Rep. 2018;5:181-189.
Nauseef WM, Borregaard N. Neutrophils at work. Nat Immunol. 2014;15:602-611.
Radmark O, Werz O, Steinhilber D, Samuelsson B. 5-Lipoxygenase, a key enzyme for leukotriene biosynthesis in health and disease. Biochim Biophys Acta. 2015;1851:331-339.
Gerstmeier J, Weinigel C, Rummler S, Radmark O, Werz O, Garscha U. Time-resolved in situ assembly of the leukotriene-synthetic 5-lipoxygenase/5-lipoxygenase-activating protein complex in blood leukocytes. FASEB J. 2016;30:276-285.
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;286:264-265.
Goodarzi K, Goodarzi M, Tager AM, Luster AD, von Andrian UH. Leukotriene B4 and BLT1 control cytotoxic effector T cell recruitment to inflamed tissues. Nat Immunol. 2003;4:965-973.
Lammermann T, Afonso PV, Angermann BR, et al. Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature. 2013;498(7454):371-375. http://dx.doi.org/10.1038/nature12175
Lee SP, Serezani CH, Medeiros AI, Ballinger MN, Peters-Golden M. Crosstalk between prostaglandin E2 and leukotriene B4 regulates phagocytosis in alveolar macrophages via combinatorial effects on cyclic AMP. J Immunol. 2009;182:530-537.
Okamoto F, Saeki K, Sumimoto H, Yamasaki S, Yokomizo T. Leukotriene B4 augments and restores FcγRs-dependent phagocytosis in macrophages. J Biol Chem. 2010;285(52):41113-41121. http://dx.doi.org/10.1074/jbc.m110.175497
Hopke A, Scherer A, Kreuzburg S, et al. Neutrophil swarming delays the growth of clusters of pathogenic fungi. Nat Commun. 2020;11:2031.
Tan SY, Weninger W. Neutrophil migration in inflammation: intercellular signal relay and crosstalk. Curr Opin Immunol. 2017;44:34-42.
Flamand L, Tremblay MJ, Borgeat P. Leukotriene B4 triggers the in vitro and in vivo release of potent antimicrobial agents. J Immunol. 2007;178:8036-8045.
Wan M, Sabirsh A, Wetterholm A, Agerberth B, Haeggstrom JZ. Leukotriene B4 triggers release of the cathelicidin LL-37 from human neutrophils: novel lipid-peptide interactions in innate immune responses. FASEB J. 2007;21:2897-2905.
Devchand PR, Keller H, Peters JM, Vazquez M, Gonzalez FJ, Wahli W. The PPARalpha-leukotriene B4 pathway to inflammation control. Nature. 1996;384:39-43.
Palmer RM, Salmon JA. Release of leukotriene B4 from human neutrophils and its relationship to degranulation induced by N-formyl-methionyl-leucyl-phenylalanine, serum-treated zymosan and the ionophore A23187. Immunology. 1983;50:65-73.
Claesson HE, Lindgren JA, Gustafsson B. Opsonized bacteria stimulate leukotriene synthesis in human leukocytes. Biochim Biophys Acta. 1985;836:361-367.
Romp E, Arakandy V, Fischer J, et al. Exotoxins from Staphylococcus aureus activate 5-lipoxygenase and induce leukotriene biosynthesis. Cell Mol Life Sci. 2020;77:3841-3858.
Parti RP, Loper R, Brown GD, et al. Cytosolic phospholipase a2 activation by Candida albicans in alveolar macrophages: role of dectin-1. Am J Respir Cell Mol Biol. 2010;42:415-423.
Suram S, Gangelhoff TA, Taylor PR, et al. Pathways regulating cytosolic phospholipase A2 activation and eicosanoid production in macrophages by Candida albicans. J Biol Chem. 2010;285:30676-30685.
Yun B, Lee H, Jayaraja S, Suram S, Murphy RC, Leslie CC. Prostaglandins from cytosolic phospholipase A2alpha/cyclooxygenase-1 pathway and mitogen-activated protein kinases regulate gene expression in Candida albicans-infected macrophages. J Biol Chem. 2016;291:7070-7086.
Nikou SA, Kichik N, Brown R, et al. Candida albicans interactions with mucosal surfaces during health and disease. Pathogens. 2019;8(2):53.
Morgan J, Meltzer MI, Plikaytis BD, et al. Excess mortality, hospital stay, and cost due to candidemia: a case-control study using data from population-based candidemia surveillance. Infect Control Hosp Epidemiol. 2005;26:540-547.
Pappas PG, Rex JH, Lee J, et al. A prospective observational study of candidemia: epidemiology, therapy, and influences on mortality in hospitalized adult and pediatric patients. Clin Infect Dis. 2003;37:634-643.
Mejia-Chew C, O'Halloran JA, Olsen MA, et al. Effect of infectious disease consultation on mortality and treatment of patients with candida bloodstream infections: a retrospective, cohort study. Lancet Infect Dis. 2019;19:1336-1344.
Kullberg BJ, Arendrup MC. Invasive candidiasis. New Engl J Med. 2015;373:1445-1456.
Yapar N. Epidemiology and risk factors for invasive candidiasis. Ther Clin Risk Manag. 2014;10:95-105.
Bougnoux ME, Diogo D, Francois N, et al. Multilocus sequence typing reveals intrafamilial transmission and microevolutions of Candida albicans isolates from the human digestive tract. J Clin Microbiol. 2006;44:1810-1820.
Mayer FL, Wilson D, Hube B. Candida albicans pathogenicity mechanisms. Virulence. 2013;4:119-128.
Boyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Inv. 1968;97:77-89.
Gillum AM, Tsay EY, Kirsch DR. Isolation of the Candida albicans gene for orotidine-5'-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet. 1984;198:179-182.
Mayer FL, Wilson D, Jacobsen ID, Miramon P, Grosse K, Hube B. The novel Candida albicans transporter Dur31 Is a multi-stage pathogenicity factor. PLoS Pathog. 2012;8:e1002592. http://dx.doi.org/10.1371/journal.ppat.1002592
Fonzi WA, Irwin MY. Isogenic strain construction and gene mapping in Candida albicans. Genetics. 1993;134:717-728.
Zheng X, Wang Y, Wang Y. Hgc1, a novel hypha-specific G1 cyclin-related protein regulates Candida albicans hyphal morphogenesis. EMBO J. 2004;23:1845-1856.
Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, Fink GR. Nonfilamentous C. albicans mutants are avirulent. Cell. 1997;90:939-949.
Moyes DL, Wilson D, Richardson JP, et al. Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature. 2016;532:64-68.
Steinhilber D, Herrmann T, Roth HJ. Separation of lipoxins and leukotrienes from human granulocytes by high-performance liquid chromatography with a Radial-Pak cartridge after extraction with an octadecyl reversed-phase column. J Chromatogr. 1989;493:361-366.
Werner M, Jordan PM, Romp E, et al. Targeting biosynthetic networks of the proinflammatory and proresolving lipid metabolome. FASEB J. 2019;33:6140-6153.
Evans JH, Spencer DM, Zweifach A, Leslie CC. Intracellular calcium signals regulating cytosolic phospholipase A2 translocation to internal membranes. J Biol Chem. 2001;276:30150-30160.
Aharony D, Stein RL. Kinetic mechanism of guinea pig neutrophil 5-lipoxygenase. J Biol Chem. 1986;261:11512-11519.
Werz O, Klemm J, Samuelsson B, Radmark O. 5-lipoxygenase is phosphorylated by p38 kinase-dependent MAPKAP kinases. Proc Natl Acad Sci U S A. 2000;97:5261-5266.
Werz O, Burkert E, Fischer L, et al. Extracellular signal-regulated kinases phosphorylate 5lipoxygenase and stimulate 5-lipoxygenase product formation in leukocytes. FASEB J. 2002;16(11):1441-1443. http://dx.doi.org/10.1096/fj.01-0909fje
Koeberle SC, Romir J, Fischer S, et al. Skepinone-L is a selective p38 mitogen-activated protein kinase inhibitor. Nat Chem Biol. 2011;8:141-143.
Favata MF, Horiuchi KY, Manos EJ, et al. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem. 1998;273:18623-18632.
Seno K, Okuno T, Nishi K, et al. Pyrrolidine inhibitors of human cytosolic phospholipase A(2). J Med Chem. 2000;43:1041-1044.
Gillard J, Ford-Hutchinson AW, Chan C, et al. L-663,536 (MK-886) (3-[1-(4-chlorobenzyl)-3-t-butyl-thio-5-isopropylindol-2-yl]-2,2 - dimethylpropanoic acid), a novel, orally active leukotriene biosynthesis inhibitor. Can J Physiol Pharmacol. 1989;67:456-464.
Werz O, Burkert E, Samuelsson B, Radmark O, Steinhilber D. Activation of 5-lipoxygenase by cell stress is calcium independent in human polymorphonuclear leukocytes. Blood. 2002;99(3):1044-1052. http://dx.doi.org/10.1182/blood.v99.3.1044
Wheeler RT, Fink GR. A drug-sensitive genetic network masks fungi from the immune system. PLoS Pathog. 2006;2:e35.
Ferwerda G, Meyer-Wentrup F, Kullberg BJ, Netea MG, Adema GJ. Dectin-1 synergizes with TLR2 and TLR4 for cytokine production in human primary monocytes and macrophages. Cell Microbiol. 2008;10:2058-2066.
McGreal EP, Rosas M, Brown GD, et al. The carbohydrate-recognition domain of Dectin-2 is a C-type lectin with specificity for high mannose. Glycobiology. 2006;16:422-430.
Becker KL, Aimanianda V, Wang X, et al. Aspergillus cell wall chitin induces anti- and proinflammatory cytokines in human PBMCs via the Fc-gamma receptor/Syk/PI3K pathway. mBio. 2016;7(3):e01823-15.
Hirschfeld M, Kirschning CJ, Schwandner R, et al. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol. 1999;163:2382-2386.
Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem. 1999;274:10689-10692.
Okusawa T, Fujita M, Nakamura J, et al. Relationship between structures and biological activities of mycoplasmal diacylated lipopeptides and their recognition by toll-like receptors 2 and 6. Infect Immun. 2004;72:1657-1665.
Lee EKS, Gillrie MR, Li L, et al. Leukotriene B4-mediated neutrophil recruitment causes pulmonary capillaritis during lethal fungal sepsis. Cell Host Microbe. 2018;23(1):121-133.e4.
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;178:1347-1355.
Doerfler ME, Danner RL, Shelhamer JH, Parrillo JE. Bacterial lipopolysaccharides prime human neutrophils for enhanced production of leukotriene B4. J Clin Investig. 1989;83:970-977.
Jordan PM, Gerstmeier J, Pace S, et al. Staphylococcus aureus-derived alpha-hemolysin evokes generation of specialized pro-resolving mediators promoting inflammation resolution. Cell Rep. 2020;33:108247.
Jayaraja S, Dakhama A, Yun B, et al. Cytosolic phospholipase A2 contributes to innate immune defense against Candida albicans lung infection. BMC Immunol. 2016;17:27.
Jacobsen ID, Wilson D, Wachtler B, Brunke S, Naglik JR, Hube B. Candida albicans dimorphism as a therapeutic target. Expert Rev Anti Infect Ther. 2012;10:85-93.
Wozniok I, Hornbach A, Schmitt C, et al. Induction of ERK-kinase signalling triggers morphotype-specific killing of Candida albicans filaments by human neutrophils. Cell Microbiol. 2008;10:807-820.
Kramer RM, Roberts EF, Um SL, et al. p38 mitogen-activated protein kinase phosphorylates cytosolic phospholipase A2 (cPLA2) in thrombin-stimulated platelets. Evidence that proline-directed phosphorylation is not required for mobilization of arachidonic acid by cPLA2. J Biol Chem. 1996;271:27723-27729.
Niemiec MJ, Grumaz C, Ermert D, et al. Dual transcriptome of the immediate neutrophil and Candida albicans interplay. BMC Genom. 2017;18:696.
Sudbery PE. Growth of Candida albicans hyphae. Nat Rev Microbiol. 2011;9:737-748.
Nantel A, Dignard D, Bachewich C, et al. Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol Biol Cell. 2002;13:3452-3465.
Lowman DW, Greene RR, Bearden DW, et al. Novel structural features in Candida albicans hyphal glucan provide a basis for differential innate immune recognition of hyphae versus yeast. J Biol Chem. 2014;289:3432-3443.
Lavigne LM, Albina JE, Reichner JS. Beta-glucan is a fungal determinant for adhesion-dependent human neutrophil functions. J Immunol. 2006;177:8667-8675.
Gow NA, Netea MG, Munro CA, et al. Immune recognition of Candida albicans beta-glucan by dectin-1. J Infect Dis. 2007;196:1565-1571.
Jouault T, Ibata-Ombetta S, Takeuchi O, et al. Candida albicans phospholipomannan is sensed through toll-like receptors. J Infect Dis. 2003;188:165-172.
Tada H, Nemoto E, Shimauchi H, et al. Saccharomyces cerevisiae- and Candida albicans-derived mannan induced production of tumor necrosis factor alpha by human monocytes in a CD14- and Toll-like receptor 4-dependent manner. Microbiol Immunol. 2002;46:503-512.
Mukaremera L, Lee KK, Mora-Montes HM, Gow NAR. Candida albicans yeast, pseudohyphal, and hyphal morphogenesis differentially affects immune recognition. Front Immunol. 2017;8:629.
Dillon S, Agrawal S, Banerjee K, et al. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J Clin Investig. 2006;116:916-928.
Tsuchimori N, Sharkey LL, Fonzi WA, French SW, Edwards JE, Filler SG. Reduced virulence of HWP1-deficient mutants of Candida albicans and their interactions with host cells. Infect Immun. 2000;68:1997-2002.
Liu YP, Filler SG. Candida albicans Als3, a Multifunctional Adhesin and Invasin. Eukaryot Cell. 2011;10:168-173.
Naglik JR, Challacombe SJ, Hube B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol R. 2003;67:400-428.
Hube B, Monod M, Schofield DA, Brown AJP, Gow NAR. Expression of 7 members of the gene family encoding secretory aspartyl proteinases in Candida-Albicans. Mol Microbiol. 1994;14:87-99.