Activation of leukotriene B

BLT1 Complement receptor 3 Fungi LTA4H Phagocytosis

Journal

Cellular & molecular immunology
ISSN: 2042-0226
Titre abrégé: Cell Mol Immunol
Pays: China
ID NLM: 101242872

Informations de publication

Date de publication:
31 Jan 2024
Historique:
received: 08 06 2023
accepted: 31 12 2023
medline: 1 2 2024
pubmed: 1 2 2024
entrez: 31 1 2024
Statut: aheadofprint

Résumé

Invasive fungal infections are life-threatening, and neutrophils are vital cells of the innate immune system that defend against them. The role of LTA4H-LTB

Identifiants

pubmed: 38297112
doi: 10.1038/s41423-024-01130-4
pii: 10.1038/s41423-024-01130-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 31930039
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 31821003
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 91942303
Organisme : Postdoctoral Research Foundation of China (China Postdoctoral Research Foundation)
ID : 2019YFA0508502

Informations de copyright

© 2024. The Author(s), under exclusive licence to CSI and USTC.

Références

Lionakis MS, Hohl TM. Call to action: how to tackle emerging nosocomial fungal infections. Cell Host Microbe. 2020;27:859–62.
pubmed: 32526182 pmcid: 7543769 doi: 10.1016/j.chom.2020.04.011
Salazar F, Bignell E, Brown GD, Cook PC, Warris A. Pathogenesis of respiratory viral and fungal coinfections. Clin Microbiol Rev. 2022;35:e0009421.
pubmed: 34788127 doi: 10.1128/CMR.00094-21
Lionakis MS, Drummond RA, Hohl TM. Immune responses to human fungal pathogens and therapeutic prospects. Nat Rev Immunol. 2023;23:1–20.
doi: 10.1038/s41577-022-00826-w
Hoenigl M, Seidel D, Sprute R, Cunha C, Oliverio M, Goldman GH, et al. COVID-19-associated fungal infections. Nat Microbiol. 2022;7:1127–40.
pubmed: 35918423 pmcid: 9362108 doi: 10.1038/s41564-022-01172-2
Gangneux JP, Dannaoui E, Fekkar A, Luyt CE, Botterel F, De Prost N, et al. Fungal infections in mechanically ventilated patients with COVID-19 during the first wave: the French multicentre MYCOVID study. Lancet Respir Med. 2022;10:180–90.
pubmed: 34843666 doi: 10.1016/S2213-2600(21)00442-2
Qu J, Lv X. Cryptococcal meningitis in apparently immunocompetent patients. Crit Rev Microbiol. 2022:1–11.
Schwartz S, Kontoyiannis DP, Harrison T, Ruhnke M. Advances in the diagnosis and treatment of fungal infections of the CNS. Lancet Neurol. 2018;17:362–72.
pubmed: 29477506 doi: 10.1016/S1474-4422(18)30030-9
Rao SD. Invasive fungal infections: a comprehensive review. Am J Infect Dis. 2013;1:64–9.
Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, White TC. Hidden killers: human fungal infections. Sci Transl Med. 2012;4:165rv113.
doi: 10.1126/scitranslmed.3004404
Alastruey-Izquierdo A, World Health Organization. WHO Fungal Priority Pathogens List to Guide Research, Development and Public Health Action. Geneva, Switzerland: World Health Organization; 2022.
Casadevall A. Immunity to invasive fungal diseases. Annu Rev Immunol. 2022;40:121–41.
pubmed: 35007128 doi: 10.1146/annurev-immunol-101220-034306
Patin EC, Thompson A, Orr SJ. Pattern recognition receptors in fungal immunity. Semin Cell Dev Biol. 2019;89:24–33.
Hünniger K, Kurzai O. Phagocytes as central players in the defence against invasive fungal infection. Semin Cell Dev Biol. 2019;89:3–15.
pubmed: 29601862 doi: 10.1016/j.semcdb.2018.03.021
Lionakis MS, Iliev ID, Hohl TM. Immunity against fungi. JCI insight. 2017;2:e93156.
Erwig LP, Gow NA. Interactions of fungal pathogens with phagocytes. Nat Rev Microbiol. 2016;14:163–76.
pubmed: 26853116 doi: 10.1038/nrmicro.2015.21
Vazquez-Torres A, Jones-Carson J, Balish E. Peroxynitrite contributes to the candidacidal activity of nitric oxide-producing macrophages. Infect Immun. 1996;64:3127–33.
pubmed: 8757843 pmcid: 174197 doi: 10.1128/iai.64.8.3127-3133.1996
Cheng SC, Joosten LA, Kullberg BJ, Netea MG. Interplay between Candida albicans and the mammalian innate host defense. Infect Immun. 2012;80:1304–13.
pubmed: 22252867 pmcid: 3318407 doi: 10.1128/IAI.06146-11
Branzk N, Lubojemska A, Hardison SE, Wang Q, Gutierrez MG, Brown GD, et al. Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol. 2014;15:1017–25.
pubmed: 25217981 pmcid: 4236687 doi: 10.1038/ni.2987
Peters-Golden M, Henderson WR Jr. Leukotrienes. N Engl J Med. 2007;357:1841–54.
pubmed: 17978293 doi: 10.1056/NEJMra071371
He R, Chen Y, Cai Q. The role of the LTB4-BLT1 axis in health and disease. Pharmacol Res. 2020;158:104857.
pubmed: 32439596 doi: 10.1016/j.phrs.2020.104857
Orning L, Fitzpatrick F. Albumins activate peptide hydrolysis by the bifunctional enzyme LTA4 hydrolase/aminopeptidase. Biochemistry. 1992;31:4218–23.
pubmed: 1314659 doi: 10.1021/bi00132a010
Orning L, Gierse J, Fitzpatrick F. The bifunctional enzyme leukotriene-A4 hydrolase is an arginine aminopeptidase of high efficiency and specificity. J Biol Chem. 1994;269:11269–73.
pubmed: 8157657 doi: 10.1016/S0021-9258(19)78120-4
Tobin DM, Vary JC Jr, Ray JP, Walsh GS, Dunstan SJ, Bang ND, et al. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell. 2010;140:717–30.
pubmed: 20211140 pmcid: 2907082 doi: 10.1016/j.cell.2010.02.013
Zhou LH, Zhao HZ, Wang X, Wang RY, Jiang YK, Huang LP, et al. Immune reconstitution inflammatory syndrome in non‐HIV cryptococcal meningitis: cross‐talk between pathogen and host. Mycoses. 2021;64:1402–11.
pubmed: 34390048 pmcid: 9290805 doi: 10.1111/myc.13361
Di Gennaro A, Haeggström JZ. Targeting leukotriene B4 in inflammation. Expert Opin Ther Targets. 2014;18:79–93.
pubmed: 24090264 doi: 10.1517/14728222.2013.843671
Simard JC, Simon MM, Tessier PA, Girard D. Damage-associated molecular pattern S100A9 increases bactericidal activity of human neutrophils by enhancing phagocytosis. J Immunol. 2011;186:3622–31.
pubmed: 21325622 doi: 10.4049/jimmunol.1002956
Suchard SJ, Mansfield PJ, Boxer LA, Shayman JA. Mitogen-activated protein kinase activation during IgG-dependent phagocytosis in human neutrophils: inhibition by ceramide. J Immunol. 1997;158:4961–7.
pubmed: 9144515 doi: 10.4049/jimmunol.158.10.4961
de Oliveira SAM, Reis JN, Catão E, Amaral AC, Souza ACO, Ribeiro AM, et al. β2 integrin-mediated susceptibility to paracoccidioides brasiliensis experimental infection in mice. Front Cell Infect Microbiol. 2021;11:622899.
pubmed: 33796477 pmcid: 8007971 doi: 10.3389/fcimb.2021.622899
Li DD, Jawale CV, Zhou C, Lin L, Trevejo-Nunez GJ, Rahman SA, et al. Fungal sensing enhances neutrophil metabolic fitness by regulating antifungal Glut1 activity. Cell Host Microbe. 2022;30:530–544.e6.
pubmed: 35316647 pmcid: 9026661 doi: 10.1016/j.chom.2022.02.017
Secatto A, Soares EM, Locachevic GA, Assis PA, Paula-Silva FW, Serezani CH, et al. The leukotriene B4/BLT1 axis is a key determinant in susceptibility and resistance to histoplasmosis. PLoS ONE. 2014;9:e85083.
pubmed: 24465479 pmcid: 3897419 doi: 10.1371/journal.pone.0085083
Santos PC, Santos DA, Ribeiro LS, Fagundes CT, de Paula TP, Avila TV, et al. The pivotal role of 5-lipoxygenase-derived LTB4 in controlling pulmonary paracoccidioidomycosis. PLoS Negl Trop Dis. 2013;7:e2390.
pubmed: 23991239 pmcid: 3749973 doi: 10.1371/journal.pntd.0002390
Bojang E, Ghuman H, Kumwenda P, Hall RA. Immune sensing of Candida albicans. J Fungi. 2021;7:119.
doi: 10.3390/jof7020119
Bonnett CR, Cornish EJ, Harmsen AG, Burritt JB. Early neutrophil recruitment and aggregation in the murine lung inhibit germination of Aspergillus fumigatus conidia. Infect Immun. 2006;74:6528–39.
pubmed: 16920786 pmcid: 1698102 doi: 10.1128/IAI.00909-06
Feldmesser M. Role of neutrophils in invasive aspergillosis. Infect Immun. 2006;74:6514–6.
pubmed: 17030575 pmcid: 1698058 doi: 10.1128/IAI.01551-06
Lionakis MS, Netea MG. Candida and host determinants of susceptibility to invasive candidiasis. PLoS Pathog. 2013;9:e1003079.
pubmed: 23300452 pmcid: 3536687 doi: 10.1371/journal.ppat.1003079
Lionakis MS, Lim JK, Lee CCR, Murphy PM. Organ-specific innate immune responses in a mouse model of invasive candidiasis. J Innate Immun. 2010;3:180–99.
pubmed: 21063074 pmcid: 3072204 doi: 10.1159/000321157
Afonso PV, Janka-Junttila M, Lee YJ, McCann CP, Oliver CM, Aamer KA, et al. LTB4 is a signal-relay molecule during neutrophil chemotaxis. Dev Cell. 2012;22:1079–91.
pubmed: 22542839 pmcid: 4141281 doi: 10.1016/j.devcel.2012.02.003
Tager AM, Dufour JH, Goodarzi K, Bercury SD, von Andrian UH, Luster AD. BLTR mediates leukotriene B4–induced chemotaxis and adhesion and plays a dominant role in eosinophil accumulation in a murine model of peritonitis. J Exp Med. 2000;192:439–46.
pubmed: 10934232 pmcid: 2193216 doi: 10.1084/jem.192.3.439
Tager AM, Bromley SK, Medoff BD, Islam SA, Bercury SD, Friedrich EB, et al. Leukotriene B4 receptor BLT1 mediates early effector T cell recruitment. Nat Immunol. 2003;4:982–90.
pubmed: 12949531 doi: 10.1038/ni970
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;4:965–73.
pubmed: 12949533 doi: 10.1038/ni972
Toda A, Terawaki K, Yamazaki S, Saeki K, Shimizu T, Yokomizo T. Attenuated Th1 induction by dendritic cells from mice deficient in the leukotriene B4 receptor 1. Biochimie. 2010;92:682–91.
pubmed: 20004699 doi: 10.1016/j.biochi.2009.12.002
Haribabu B, Verghese MW, Steeber DA, Sellars DD, Bock CB, Snyderman R. Targeted disruption of the leukotriene B4 receptor in mice reveals its role in inflammation and platelet-activating factor–induced anaphylaxis. J Exp Med. 2000;192:433–8.
pubmed: 10934231 pmcid: 2193219 doi: 10.1084/jem.192.3.433
Scott MJ, Cheadle WG, Hoth JJ, Peyton JC, Subbarao K, Shao WH, et al. Leukotriene B4 receptor (BLT-1) modulates neutrophil influx into the peritoneum but not the lung and liver during surgically induced bacterial peritonitis in mice. Clin Vaccin Immunol. 2004;11:936–41.
doi: 10.1128/CDLI.11.5.936-941.2004
Oyoshi MK, He R, Li Y, Mondal S, Yoon J, Afshar R, et al. Leukotriene B4-driven neutrophil recruitment to the skin is essential for allergic skin inflammation. Immunity. 2012;37:747–58.
pubmed: 23063331 pmcid: 3478399 doi: 10.1016/j.immuni.2012.06.018
Lee E, Gillrie MR, Li L, Arnason JW, Kim JH, Babes L, et al. Leukotriene B4-mediated neutrophil recruitment causes pulmonary capillaritis during lethal fungal sepsis. Cell Host Microbe. 2018;23:121–133.e4.
pubmed: 29290576 doi: 10.1016/j.chom.2017.11.009
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.
pubmed: 29375586 pmcid: 5768911 doi: 10.3389/fimmu.2017.01984
Hopke A, Lin T, Scherer AK, Shay AE, Timmer KD, Wilson-Mifsud B, et al. Transcellular biosynthesis of leukotriene B4 orchestrates neutrophil swarming to fungi. Iscience. 2022;25:105226.
pubmed: 36267914 pmcid: 9576560 doi: 10.1016/j.isci.2022.105226
Serezani CH, Aronoff DM, Sitrin RG, Peters-Golden M. FcγRI ligation leads to a complex with BLT1 in lipid rafts that enhances rat lung macrophage antimicrobial functions. Blood. 2009;114:3316–24.
pubmed: 19657115 pmcid: 2759654 doi: 10.1182/blood-2009-01-199919
Serezani CH, Aronoff DM, Jancar S, Mancuso P, Peters-Golden M. Leukotrienes enhance the bactericidal activity of alveolar macrophages against Klebsiella pneumoniae through the activation of NADPH oxidase. Blood. 2005;106:1067–75.
pubmed: 15718414 pmcid: 1895163 doi: 10.1182/blood-2004-08-3323
Mancuso P, Peters-Golden M. Modulation of alveolar macrophage phagocytosis by leukotrienes is Fc receptor–mediated and protein kinase C-dependent. Am J Respir Cell Mol Biol. 2000;23:727–33.
pubmed: 11104724 doi: 10.1165/ajrcmb.23.6.4246
Okamoto F, Saeki K, Sumimoto H, Yamasaki S, Yokomizo T. Leukotriene B4 augments and restores FcγRs-dependent phagocytosis in macrophages. J Biol Chem. 2010;285:41113–21.
pubmed: 20959460 pmcid: 3003409 doi: 10.1074/jbc.M110.175497
Morato-Marques M, Campos MR, Kane S, Rangel AP, Lewis C, Ballinger MN, et al. Leukotrienes target F-actin/cofilin-1 to enhance alveolar macrophage anti-fungal activity. J Biol Chem. 2011;286:28902–13.
pubmed: 21715328 pmcid: 3190697 doi: 10.1074/jbc.M111.235309
McDonough LD, Mishra AA, Tosini N, Kakade P, Penumutchu S, Liang SH, et al. Candida albicans isolates 529L and CHN1 exhibit stable colonization of the murine gastrointestinal tract. Mbio. 2021;12:e0287821.
pubmed: 34724818 doi: 10.1128/mBio.02878-21
Wu W, Lockhart SR, Pujol C, Srikantha T, Soll DR. Heterozygosity of genes on the sex chromosome regulates Candida albicans virulence. Mol Microbiol. 2007;64:1587–604.
pubmed: 17555440 doi: 10.1111/j.1365-2958.2007.05759.x
Hirakawa MP, Martinez DA, Sakthikumar S, Anderson MZ, Berlin A, Gujja S, et al. Genetic and phenotypic intra-species variation in Candida albicans. Genome Res. 2015;25:413–25.
pubmed: 25504520 pmcid: 4352881 doi: 10.1101/gr.174623.114
Schönherr FA, Sparber F, Kirchner FR, Guiducci E, Trautwein-Weidner K, Gladiator A, et al. The intraspecies diversity of C. albicans triggers qualitatively and temporally distinct host responses that determine the balance between commensalism and pathogenicity. Mucosal Immunol. 2017;10:1335–50.
pubmed: 28176789 doi: 10.1038/mi.2017.2
van Bruggen R, Drewniak A, Jansen M, van Houdt M, Roos D, Chapel H, et al. Complement receptor 3, not Dectin-1, is the major receptor on human neutrophils for β-glucan-bearing particles. Mol Immunol. 2009;47:575–81.
pubmed: 19811837 doi: 10.1016/j.molimm.2009.09.018
Mobberley-Schuman PS, Weiss AA. Influence of CR3 (CD11b/CD18) expression on phagocytosis of bordetella pertussis by human neutrophils. Infect Immun. 2005;73:7317–23.
pubmed: 16239529 pmcid: 1273866 doi: 10.1128/IAI.73.11.7317-7323.2005
Witt H, Yan Z, Henann D, Franck C, Reichner J. Mechanosensitive traction force generation is regulated by the neutrophil activation state. Sci Rep. 2023;13:11098.
pubmed: 37423937 pmcid: 10330213 doi: 10.1038/s41598-023-37997-y
Berton G, Yan SR, Fumagalli L, Lowell CA. Neutrophil activation by adhesion: mechanisms and pathophysiological implications. Int J Clin Lab Res. 1996;26:160–77.
pubmed: 8905448 doi: 10.1007/BF02592978
Allen DL, Hoffman WP, Marder P, Matchett MR, Leiter PA, Abbott DL, et al. The effects of LY293111Na, a leukotriene B4 receptor antagonist, on the pulmonary neutrophilia and CD11b expression caused by inhalation of a leukotriene B4 aerosol in rhesus monkeys. J Pharmacol Exp Ther. 1996;277:341–9.
pubmed: 8613940
Marder P, Spaethe SM, Froelich LL, Cerimele BJ, Petersen BH, Tanner T, et al. Inhibition of ex vivo neutrophil activation by oral LY293111, a novel leukotriene B4 receptor antagonist. Br J Clin Pharmacol. 1996;42:457–64.
pubmed: 8904617 pmcid: 2042691 doi: 10.1111/j.1365-2125.1996.tb00008.x
Alten R, Gromnica-Ihle E, Pohl C, Emmerich J, Steffgen J, Roscher R, et al. Inhibition of leukotriene B4-induced CD11B/CD18 (Mac-1) expression by BIIL 284, a new long acting LTB4 receptor antagonist, in patients with rheumatoid arthritis. Ann Rheum Dis. 2004;63:170–6.
pubmed: 14722206 pmcid: 1754875 doi: 10.1136/ard.2002.004499
van Pelt JP, de Jong EM, van Erp PE, Mitchell MI, Marder P, Spaethe SM, et al. The regulation of CD11b integrin levels on human blood leukocytes and leukotriene B4-stimulated skin by a specific leukotriene B4 receptor antagonist (LY293111). Biochem Pharm. 1997;53:1005–12.
pubmed: 9174114 doi: 10.1016/S0006-2952(96)00884-2
Condliffe AM, Davidson K, Anderson KE, Ellson CD, Crabbe T, Okkenhaug K, et al. Sequential activation of class IB and class IA PI3K is important for the primed respiratory burst of human but not murine neutrophils. Blood. 2005;106:1432–40.
pubmed: 15878979 doi: 10.1182/blood-2005-03-0944
van Rees DJ, Szilagyi K, Kuijpers TW, Matlung HL, van den Berg TK. Immunoreceptors on neutrophils. Semin Immunol. 2016;28:94–108.
pubmed: 26976825 pmcid: 7129252 doi: 10.1016/j.smim.2016.02.004
Cassatella MA, Östberg NK, Tamassia N, Soehnlein O. Biological roles of neutrophil-derived granule proteins and cytokines. Trends Immunol. 2019;40:648–64.
pubmed: 31155315 doi: 10.1016/j.it.2019.05.003
Nauseef WM. Human neutrophils ≠ murine neutrophils: does it matter? Immunol Rev. 2023;314:442–56.
pubmed: 36380497 doi: 10.1111/imr.13154
Wang J, An H, Ding M, Liu Y, Wang S, Jin Q, et al. Potent bacterial vaccines require FcγRIIB-mediated pathogen capture by liver sinusoidal endothelium. bioRxiv. 2022. https://doi.org/10.1101/2022.07.19.500551 .
Taylor PR, Tsoni SV, Willment JA, Dennehy KM, Rosas M, Findon H, et al. Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol. 2007;8:31–38.
pubmed: 17159984 doi: 10.1038/ni1408
Guo Y, Kasahara S, Jhingran A, Tosini NL, Zhai B, Aufiero MA, et al. During Aspergillus infection, monocyte-derived DCs, neutrophils, and plasmacytoid DCs enhance innate immune defense through CXCR3-dependent crosstalk. Cell Host Microbe. 2020;28:104–116.e4.
pubmed: 32485165 pmcid: 7263227 doi: 10.1016/j.chom.2020.05.002
Guo Y, Chang Q, Cheng L, Xiong S, Jia X, Lin X, et al. C-type lectin receptor CD23 is required for host defense against Candida albicans and Aspergillus fumigatus infection. J Immunol. 2018;201:2427–40.
pubmed: 30185519 doi: 10.4049/jimmunol.1800620
Luo Y, Dorf ME. Isolation of mouse neutrophils. Curr Protoc Immunol. 1997;22:3.20.1–3.20.6.
Voyich JM, DeLeo FR. Host-pathogen interactions: leukocyte phagocytosis and associated sequelae. Adv Flow Cytometry Appl Biol Res. 2003;24:79–90.
doi: 10.1007/978-94-017-0623-0_13
Fischer J, Gresnigt MS, Werz O, Hube B, Garscha U. Candida albicans‐induced leukotriene biosynthesis in neutrophils is restricted to the hyphal morphology. FASEB J. 2021;35:e21820.
pubmed: 34569657 doi: 10.1096/fj.202100516RR

Auteurs

Yan Xin (Y)

Institute for Immunology and School of Medicine, Tsinghua University, 100084, Beijing, China.
Tsinghua University-Peking University Center for Life Sciences, 100084, Beijing, China.

Sihan Xiong (S)

Institute for Immunology and School of Medicine, Tsinghua University, 100084, Beijing, China.

Linghong Zhou (L)

Department of Infectious Diseases, Shanghai Key Laboratory of Infectious Diseases and Biosafety Emergency Response, National Medical Center for Infectious Diseases, Huashan Hospital, Fudan University, Shanghai, 200040, China.

Xin Lin (X)

Institute for Immunology and School of Medicine, Tsinghua University, 100084, Beijing, China. linxin307@tsinghua.edu.cn.
Tsinghua University-Peking University Center for Life Sciences, 100084, Beijing, China. linxin307@tsinghua.edu.cn.

Classifications MeSH