Fungal sensing enhances neutrophil metabolic fitness by regulating antifungal Glut1 activity.

Animals CARD Signaling Adaptor Proteins / metabolism Candida albicans Candidiasis / immunology Glucose / metabolism Glucose Transporter Type 1 / metabolism Mice Neutrophils / immunology beta-Glucans / metabolism
Candida albicans fungus glucose glucose transporter 1 immunometabolism kidney neutrophils

Journal

Cell host & microbe
ISSN: 1934-6069
Titre abrégé: Cell Host Microbe
Pays: United States
ID NLM: 101302316

Informations de publication

Date de publication:
13 04 2022
Historique:
received: 23 09 2021
revised: 10 12 2021
accepted: 16 02 2022
pubmed: 23 3 2022
medline: 19 4 2022
entrez: 22 3 2022
Statut: ppublish

Résumé

Combating fungal pathogens poses metabolic challenges for neutrophils, key innate cells in anti-Candida albicans immunity, yet how host-pathogen interactions cause remodeling of the neutrophil metabolism is unclear. We show that neutrophils mediate renal immunity to disseminated candidiasis by upregulating glucose uptake via selective expression of glucose transporter 1 (Glut1). Mechanistically, dectin-1-mediated recognition of β-glucan leads to activation of PKCδ, which triggers phosphorylation, localization, and early glucose transport by a pool of pre-formed Glut1 in neutrophils. These events are followed by increased Glut1 gene transcription, leading to more sustained Glut1 accumulation, which is also dependent on the β-glucan/dectin-1/CARD9 axis. Card9-deficient neutrophils show diminished glucose incorporation in candidiasis. Neutrophil-specific Glut1-ablated mice exhibit increased mortality in candidiasis caused by compromised neutrophil phagocytosis, reactive oxygen species (ROS), and neutrophil extracellular trap (NET) formation. In human neutrophils, β-glucan triggers metabolic remodeling and enhances candidacidal function. Our data show that the host-pathogen interface increases glycolytic activity in neutrophils by regulating Glut1 expression, localization, and function.

Identifiants

DOI: 10.1016/j.chom.2022.02.017 PMID: 35316647 PMC: PMC9026661
pubmed: 35316647
pii: S1931-3128(22)00103-2
doi: 10.1016/j.chom.2022.02.017
pmc: PMC9026661
mid: NIHMS1791537
pii:
doi:

Substances chimiques

CARD Signaling Adaptor Proteins 0
Card9 protein, mouse 0
Glucose Transporter Type 1 0
Slc2a1 protein, mouse 0
beta-Glucans 0
Glucose IY9XDZ35W2

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

530-544.e6

Subventions

Organisme : NIDCR NIH HHS
ID : R01 DE022550
Pays : United States
Organisme : NIDCR NIH HHS
ID : R37 DE022550
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK104680
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI145242
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI147383
Pays : United States
Organisme : NIH HHS
ID : S10 OD023402
Pays : United States
Organisme : NHLBI NIH HHS
ID : K01 HL135476
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI153549
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI159058
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI142354
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests

Références

Am J Physiol Cell Physiol. 2008 Sep;295(3):C836-43
pubmed: 18650261
Am J Physiol Endocrinol Metab. 2010 Feb;298(2):E141-5
pubmed: 20009031
Dis Model Mech. 2018 Mar 28;11(3):
pubmed: 29590639
Crit Rev Immunol. 2014;34(5):433-54
pubmed: 25404048
Sci Transl Med. 2020 Jun 17;12(548):
pubmed: 32554707
J Clin Invest. 1978 Feb;61(2):480-8
pubmed: 202614
PLoS Pathog. 2015 Dec 17;11(12):e1005293
pubmed: 26679537
J Biol Chem. 1999 Feb 26;274(9):5532-6
pubmed: 10026167
Immune Netw. 2020 Dec 24;20(6):e46
pubmed: 33425431
Rev Esp Quimioter. 2017 Sep;30 Suppl 1:22-25
pubmed: 28882010
Eur J Clin Microbiol Infect Dis. 2008 Nov;27(11):1071-8
pubmed: 18548295
EMBO J. 2001 Aug 15;20(16):4467-77
pubmed: 11500374
Nature. 2021 Mar;591(7851):645-651
pubmed: 33589820
Acta Haematol. 1997;97(4):211-5
pubmed: 9158663
J Exp Med. 1994 Mar 1;179(3):1047-52
pubmed: 8113673
PLoS Pathog. 2013 Jan;9(1):e1003079
pubmed: 23300452
J Cell Biol. 2015 Sep 28;210(7):1153-64
pubmed: 26416965
Cell Microbiol. 2006 Apr;8(4):668-76
pubmed: 16548892
Curr Clin Microbiol Rep. 2018 Sep;5(3):181-189
pubmed: 31552161
J Leukoc Biol. 2016 Oct;100(4):801-810
pubmed: 27154356
J Antimicrob Chemother. 2008 Jan;61 Suppl 1:i19-30
pubmed: 18063600
Semin Hematol. 1968 Apr;5(2):109-33
pubmed: 5690198
Genomics. 2002 Dec;80(6):553-7
pubmed: 12504846
Immunol Rev. 2020 May;295(1):5-14
pubmed: 32320073
J Biol Chem. 2014 Mar 14;289(11):7884-96
pubmed: 24492615
Cell Death Differ. 2004 Feb;11(2):143-53
pubmed: 14576767
Clin Infect Dis. 2001 Jun 15;32(12):1713-7
pubmed: 11360213
Annu Rev Immunol. 2011;29:1-21
pubmed: 20936972
J Leukoc Biol. 2016 Sep;100(3):581-8
pubmed: 26965632
Immunity. 2013 Apr 18;38(4):633-43
pubmed: 23601682
Nat Rev Dis Primers. 2018 May 11;4:18026
pubmed: 29749387
J Immunol Methods. 2014 Jun;408:89-100
pubmed: 24857755
Nat Rev Immunol. 2009 Jul;9(7):465-79
pubmed: 19521399
J Clin Invest. 2006 Jun;116(6):1642-50
pubmed: 16710478
J Immunol. 2014 Feb 15;192(4):1745-52
pubmed: 24442441
Nat Rev Mol Cell Biol. 2012 May 23;13(6):383-96
pubmed: 22617471
Front Immunol. 2019 Sep 20;10:2099
pubmed: 31616403
Nat Immunol. 2007 Jan;8(1):31-8
pubmed: 17159984
Nat Rev Immunol. 2015 Oct;15(10):630-42
pubmed: 26388329
Biochem Biophys Res Commun. 2004 Jun 11;318(4):977-82
pubmed: 15147968
Clin Infect Dis. 2005 Nov 1;41(9):1232-9
pubmed: 16206095
Infect Immun. 2014 Mar;82(3):1173-80
pubmed: 24379290
Front Cell Infect Microbiol. 2021 Jun 18;11:648988
pubmed: 34222036
Science. 2014 Sep 26;345(6204):1250684
pubmed: 25258083
Curr Opin Microbiol. 2020 Dec;58:32-40
pubmed: 32781324
Am J Physiol Endocrinol Metab. 2008 Aug;295(2):E227-37
pubmed: 18398011
Am J Physiol Cell Physiol. 2006 Feb;290(2):C337-44
pubmed: 16162661
Mol Cell. 2019 Oct 3;76(1):148-162.e7
pubmed: 31447391
Science. 2006 Dec 15;314(5806):1792-5
pubmed: 17170310
Nat Rev Immunol. 2016 Sep;16(9):553-65
pubmed: 27396447
Nat Rev Immunol. 2011 Jul 25;11(8):519-31
pubmed: 21785456
J Immunol. 2003 Feb 15;170(4):1964-72
pubmed: 12574365
Annu Rev Immunol. 2018 Apr 26;36:461-488
pubmed: 29677474
Cell Metab. 2014 Jul 1;20(1):61-72
pubmed: 24930970
Clin Infect Dis. 2009 Jun 15;48(12):1695-703
pubmed: 19441981
Cancer Res. 2021 May 1;81(9):2345-2357
pubmed: 33753374
Immunity. 2021 Jul 13;54(7):1377-1391
pubmed: 34260886
PLoS Pathog. 2012;8(8):e1002865
pubmed: 22916017
Mol Membr Biol. 2005 Jul-Aug;22(4):339-51
pubmed: 16154905
Mol Cell. 2015 Jun 4;58(5):845-53
pubmed: 25982116
Nat Immunol. 2014 Feb;15(2):143-51
pubmed: 24362892
J Exp Med. 2017 May 1;214(5):1249-1258
pubmed: 28385925
Annu Rev Pathol. 2014;9:181-218
pubmed: 24050624
FEBS Lett. 2019 Jan;593(2):195-208
pubmed: 30431159
Nat Protoc. 2012 Mar 08;7(4):637-42
pubmed: 22402633

Auteurs

De-Dong Li (DD)

Division of Rheumatology & Clinical Immunology, Department of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.

Chetan V Jawale (CV)

Division of Rheumatology & Clinical Immunology, Department of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.

Chunsheng Zhou (C)

Division of Rheumatology & Clinical Immunology, Department of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.

Li Lin (L)

Division of Rheumatology & Clinical Immunology, Department of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.

Giraldina J Trevejo-Nunez (GJ)

Division of Infectious Diseases, Department of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.

Syed A Rahman (SA)

Center for Systems Immunology, Departments of Immunology and Computational & Systems Biology, University of Pittsburgh, Pittsburgh, PA, USA.

Steven J Mullet (SJ)

Department of Immunology, University of Pittsburgh, Pittsburgh, PA, USA.

Jishnu Das (J)

Center for Systems Immunology, Departments of Immunology and Computational & Systems Biology, University of Pittsburgh, Pittsburgh, PA, USA.

Stacy G Wendell (SG)

Department of Immunology, University of Pittsburgh, Pittsburgh, PA, USA.

Greg M Delgoffe (GM)

Department of Pharmacology & Chemical Biology, University of Pittsburgh, Pittsburgh, PA, USA.

Michail S Lionakis (MS)

Fungal Pathogenesis Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD, USA.

Sarah L Gaffen (SL)

Division of Rheumatology & Clinical Immunology, Department of Medicine, University of Pittsburgh, Pittsburgh, PA, USA.

Partha S Biswas (PS)

Division of Rheumatology & Clinical Immunology, Department of Medicine, University of Pittsburgh, Pittsburgh, PA, USA. Electronic address: psb13@pitt.edu.

Articles similaires

Evaluating the efficacy of telesurgery with dual console SSI Mantra Surgical Robotic System: experiment on animal model and clinical trials.

Sudhir Prem Srivastava, Vishwajyoti Pascual Srivastava, Avinesh Singh et al.
1.00
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell

FBXO22 inhibits colitis and colorectal carcinogenesis by regulating the degradation of the S2448-phosphorylated form of mTOR.

Minle Li, Xuan Chen, Pengfei Qu et al.
1.00
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Use of organic material provided by an automatic enrichment device by weaner pigs and its influence on tail lesions.

Philipp Heseker, Jeanette Probst, Stefanie Ammer et al.
1.00
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH

Recherchemedicale.com › Eucaryotes › Animaux › Fungal sensing enhances neutrophil metabolic...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Protéines régulatrices de l'apoptose › Protéines adaptatrices de signalisation CARD › Fungal sensing enhances neutrophil metabolic...
Recherchemedicale.com › Eucaryotes › Champignons › Levures › Candida › Candida albicans › Fungal sensing enhances neutrophil metabolic...
Recherchemedicale.com › Infection › Infections bactériennes et mycoses › Mycoses › Candidose › Fungal sensing enhances neutrophil metabolic...
Recherchemedicale.com › Glucides › Sucres › Oses › Hexose › Glucose › Fungal sensing enhances neutrophil metabolic...
Recherchemedicale.com › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Protéines de transport membranaire › Protéines transporteurs de solutés › Transporteurs de glucose par diffusion facilitée › Transporteur de glucose de type 1 › Fungal sensing enhances neutrophil metabolic...
Recherchemedicale.com › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Fungal sensing enhances neutrophil metabolic...
Recherchemedicale.com › Systèmes sanguin et immunitaire › Système immunitaire › Phagocytes › Granulocytes neutrophiles › Fungal sensing enhances neutrophil metabolic...
Recherchemedicale.com › Glucides › Polyosides › Glucanes › bêta-Glucanes › Fungal sensing enhances neutrophil metabolic...