Phagosome resolution regenerates lysosomes and maintains the degradative capacity in phagocytes.


Journal

The Journal of cell biology
ISSN: 1540-8140
Titre abrégé: J Cell Biol
Pays: United States
ID NLM: 0375356

Informations de publication

Date de publication:
06 09 2021
Historique:
received: 14 05 2020
revised: 05 05 2021
accepted: 14 06 2021
entrez: 28 6 2021
pubmed: 29 6 2021
medline: 10 11 2021
Statut: ppublish

Résumé

Phagocytes engulf unwanted particles into phagosomes that then fuse with lysosomes to degrade the enclosed particles. Ultimately, phagosomes must be recycled to help recover membrane resources that were consumed during phagocytosis and phagosome maturation, a process referred to as "phagosome resolution." Little is known about phagosome resolution, which may proceed through exocytosis or membrane fission. Here, we show that bacteria-containing phagolysosomes in macrophages undergo fragmentation through vesicle budding, tubulation, and constriction. Phagosome fragmentation requires cargo degradation, the actin and microtubule cytoskeletons, and clathrin. We provide evidence that lysosome reformation occurs during phagosome resolution since the majority of phagosome-derived vesicles displayed lysosomal properties. Importantly, we show that clathrin-dependent phagosome resolution is important to maintain the degradative capacity of macrophages challenged with two waves of phagocytosis. Overall, our work suggests that phagosome resolution contributes to lysosome recovery and to maintaining the degradative power of macrophages to handle multiple waves of phagocytosis.

Identifiants

pubmed: 34180943
pii: 212440
doi: 10.1083/jcb.202005072
pmc: PMC8241537
pii:
doi:

Substances chimiques

Actins 0
Clathrin 0
Green Fluorescent Proteins 147336-22-9

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : CIHR
ID : 123373
Pays : Canada

Informations de copyright

© 2021 Lancaster et al.

Références

Exp Cell Res. 2003 Sep 10;289(1):152-61
pubmed: 12941613
Annu Rev Cell Dev Biol. 2017 Oct 6;33:127-144
pubmed: 28613937
Immunol Rev. 2016 Sep;273(1):156-79
pubmed: 27558334
J Biol Chem. 1999 Jun 18;274(25):17794-805
pubmed: 10364223
Trends Immunol. 2017 Jun;38(6):407-422
pubmed: 28416446
J Cell Biol. 2013 Dec 23;203(6):1081-97
pubmed: 24368810
Traffic. 2016 Oct;17(10):1139-49
pubmed: 27392092
Nature. 2016 Aug 11;536(7615):229-33
pubmed: 27487210
Trends Immunol. 2012 Aug;33(8):397-405
pubmed: 22560866
Mol Biol Cell. 2013 Dec;24(23):3736-45
pubmed: 24088573
Cell. 2014 Nov 20;159(5):1027-1041
pubmed: 25416943
Nature. 2010 Apr 1;464(7289):778-82
pubmed: 20305638
FEBS J. 2017 Apr;284(7):1021-1039
pubmed: 27863012
J Cell Biol. 1996 Dec;135(6 Pt 2):1801-14
pubmed: 8991092
J Cell Sci. 2020 Jun 24;133(12):
pubmed: 32501286
J Cell Biol. 1992 Nov;119(3):531-42
pubmed: 1400590
J Biol Chem. 1972 Apr 25;247(8):2439-46
pubmed: 5019957
Curr Biol. 2006 Nov 7;16(21):2156-60
pubmed: 17084701
J Cell Biol. 2018 Aug 6;217(8):2709-2726
pubmed: 29875258
Nat Cell Biol. 2012 Sep;14(9):924-34
pubmed: 22885770
J Exp Med. 1968 Sep 1;128(3):415-35
pubmed: 5666958
Curr Biol. 2006 Nov 7;16(21):2161-5
pubmed: 17084702
Mol Biol Cell. 2016 Jan 15;27(2):321-33
pubmed: 26582390
J Cell Biol. 1996 Jan;132(1-2):21-33
pubmed: 8567724
J Cell Sci. 2012 Dec 15;125(Pt 24):5937-43
pubmed: 23038769
PLoS Biol. 2019 Dec 4;17(12):e3000535
pubmed: 31800587
Mol Biol Cell. 2002 Oct;13(10):3508-20
pubmed: 12388753
J Cell Sci. 2009 Aug 15;122(Pt 16):2935-45
pubmed: 19638408
Science. 2011 Nov 4;334(6056):678-83
pubmed: 22053050
Traffic. 2013 Feb;14(2):135-52
pubmed: 23127154
Biochem Soc Trans. 2009 Oct;37(Pt 5):1022-6
pubmed: 19754444
ACS Biomater Sci Eng. 2017 Nov 13;3(11):2727-2732
pubmed: 29250592
J Cell Biol. 2000 Dec 25;151(7):1353-68
pubmed: 11134066
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Dev Cell. 2016 Sep 12;38(5):536-47
pubmed: 27623384
Traffic. 2003 Jan;4(1):1-5
pubmed: 12535269
J Cell Biol. 2018 Jan 2;217(1):329-346
pubmed: 29089378
Curr Biol. 2016 Sep 12;26(17):2233-45
pubmed: 27498570
Cold Spring Harb Perspect Biol. 2014 Mar 01;6(3):
pubmed: 24591520
J Cell Sci. 1992 Apr;101 ( Pt 4):907-13
pubmed: 1527185
Arch Dermatol Res. 2004 Jun;296(1):30-41
pubmed: 15127211
Immunity. 2011 Aug 26;35(2):182-93
pubmed: 21802320
Mol Cell Biol. 2003 Sep;23(18):6494-506
pubmed: 12944476
Cell Struct Funct. 2008;33(1):1-12
pubmed: 18256512
J Cell Biol. 1972 Jan;52(1):117-30
pubmed: 4331294
Biochem Cell Biol. 2019 Feb;97(1):21-29
pubmed: 29791809
Nature. 2010 Jun 17;465(7300):942-6
pubmed: 20526321
Cell. 2011 Aug 5;146(3):471-84
pubmed: 21816279
Dev Cell. 2010 Feb 16;18(2):324-31
pubmed: 20159602
J Cell Sci. 2002 Jul 15;115(Pt 14):2893-905
pubmed: 12082150
J Med Chem. 2009 Jun 25;52(12):3762-73
pubmed: 19459681
Trends Cell Biol. 2019 Aug;29(8):635-646
pubmed: 31171420
J Cell Biol. 1997 Apr 21;137(2):335-45
pubmed: 9128246
J Cell Biol. 2019 Aug 5;218(8):2619-2637
pubmed: 31235480
J Cell Sci. 2013 May 1;126(Pt 9):2102-13
pubmed: 23532825
Curr Biol. 2001 Oct 30;11(21):1680-5
pubmed: 11696325
EMBO J. 1994 Aug 1;13(15):3430-7
pubmed: 8062819
Nat Cell Biol. 2019 Oct;21(10):1234-1247
pubmed: 31570833
Curr Protoc Cell Biol. 2013 Dec 02;61:15.20.1-7
pubmed: 24510805
J Biol Chem. 2013 Dec 13;288(50):35769-80
pubmed: 24174532
Traffic. 2017 Nov;18(11):747-757
pubmed: 28857423
Curr Biol. 2005 Feb 22;15(4):360-5
pubmed: 15723798
Cell Microbiol. 2010 Mar;12(3):343-61
pubmed: 19863556
Cold Spring Harb Perspect Biol. 2014 May 01;6(5):a016725
pubmed: 24789820
J Cell Biol. 2015 May 11;209(3):329-37
pubmed: 25963816
Cell Rep. 2014 Feb 13;6(3):445-54
pubmed: 24462287
Dev Cell. 2016 May 23;37(4):326-336
pubmed: 27219061
Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):7877-82
pubmed: 12060735
J Immunol. 1999 Mar 15;162(6):3263-72
pubmed: 10092778
Curr Biol. 2016 Aug 8;26(15):1955-1964
pubmed: 27397893
J Innate Immun. 2010;2(3):204-15
pubmed: 20375558
Dev Cell. 2013 Aug 12;26(3):279-91
pubmed: 23891661
Methods Mol Biol. 2017;1519:1-16
pubmed: 27815869
Proc Natl Acad Sci U S A. 2014 Oct 28;111(43):15508-13
pubmed: 25313083
Traffic. 2013 Dec;14(12):1272-89
pubmed: 24025110
Cell. 2018 Sep 20;175(1):254-265.e14
pubmed: 30220460
Curr Biol. 1998 Mar 12;8(6):343-6
pubmed: 9512420
Front Cell Dev Biol. 2019 Jun 20;7:113
pubmed: 31281815
Cell. 2016 Mar 24;165(1):153-164
pubmed: 26972053
J Biol Chem. 2000 May 26;275(21):15717-27
pubmed: 10748188

Auteurs

Charlene E Lancaster (CE)

Department of Biological Sciences, University of Toronto at Scarborough, Toronto, Ontario, Canada.
Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario, Canada.

Aaron Fountain (A)

Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada.
Graduate Program in Molecular Science, Ryerson University, Toronto, Ontario, Canada.

Roaya M Dayam (RM)

Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada.
Graduate Program in Molecular Science, Ryerson University, Toronto, Ontario, Canada.

Elliott Somerville (E)

Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada.

Javal Sheth (J)

Department of Biological Sciences, University of Toronto at Scarborough, Toronto, Ontario, Canada.

Vanessa Jacobelli (V)

Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada.

Alex Somerville (A)

Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada.

Mauricio R Terebiznik (MR)

Department of Biological Sciences, University of Toronto at Scarborough, Toronto, Ontario, Canada.
Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario, Canada.

Roberto J Botelho (RJ)

Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada.
Graduate Program in Molecular Science, Ryerson University, Toronto, Ontario, Canada.

Articles similaires

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
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH