Kinetics of phagosome maturation is coupled to their intracellular motility.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
26 09 2022
26 09 2022
Historique:
received:
23
03
2022
accepted:
12
09
2022
entrez:
27
9
2022
pubmed:
28
9
2022
medline:
1
10
2022
Statut:
epublish
Résumé
Immune cells degrade internalized pathogens in phagosomes through sequential biochemical changes. The degradation must be fast enough for effective infection control. The presumption is that each phagosome degrades cargos autonomously with a distinct but stochastic kinetic rate. However, here we show that the degradation kinetics of individual phagosomes is not stochastic but coupled to their intracellular motility. By engineering RotSensors that are optically anisotropic, magnetic responsive, and fluorogenic in response to degradation activities in phagosomes, we monitored cargo degradation kinetics in single phagosomes simultaneously with their translational and rotational dynamics. We show that phagosomes that move faster centripetally are more likely to encounter and fuse with lysosomes, thereby acidifying faster and degrading cargos more efficiently. The degradation rates increase nearly linearly with the translational and rotational velocities of phagosomes. Our results indicate that the centripetal motion of phagosomes functions as a clock for controlling the progression of cargo degradation.
Identifiants
pubmed: 36163370
doi: 10.1038/s42003-022-03988-4
pii: 10.1038/s42003-022-03988-4
pmc: PMC9512794
doi:
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1014Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM124918
Pays : United States
Informations de copyright
© 2022. The Author(s).
Références
EMBO J. 2007 Jan 24;26(2):313-24
pubmed: 17245426
J Biol Chem. 2009 Dec 18;284(51):35926-38
pubmed: 19837664
J Cell Biol. 2002 Mar 4;156(5):855-65
pubmed: 11864991
Proc Natl Acad Sci U S A. 2021 Oct 12;118(41):
pubmed: 34607961
Proc Natl Acad Sci U S A. 2010 Nov 30;107(48):20726-31
pubmed: 21071675
Cell Rep. 2018 Jun 19;23(12):3591-3606
pubmed: 29925001
Trends Immunol. 2017 Jun;38(6):407-422
pubmed: 28416446
J Cell Biol. 2015 Aug 17;210(4):595-611
pubmed: 26261180
Cell. 2013 Jan 17;152(1-2):172-82
pubmed: 23332753
J Cell Biol. 2005 Apr 11;169(1):139-49
pubmed: 15809313
J Cell Biol. 1994 Mar;124(5):677-88
pubmed: 8120091
J Biol Chem. 2015 May 29;290(22):14166-80
pubmed: 25903133
Biochem Soc Trans. 2007 Nov;35(Pt 5):1083-7
pubmed: 17956285
J Exp Med. 2002 Aug 19;196(4):529-40
pubmed: 12186844
Nat Cell Biol. 2016 Apr;18(4):404-17
pubmed: 26950892
Front Biosci. 2006 May 01;11:1479-90
pubmed: 16368530
Eur J Cell Biol. 2000 Oct;79(10):735-49
pubmed: 11089922
Curr Opin Cell Biol. 2010 Apr;22(2):124-31
pubmed: 20034776
J Vis Exp. 2016 Sep 05;(115):
pubmed: 27684087
Curr Biol. 1998 May 21;8(11):R394-7
pubmed: 9635187
Sci Rep. 2017 Jun 15;7(1):3558
pubmed: 28620230
Mol Biol Cell. 2018 Feb 15;29(4):452-465
pubmed: 29237821
Methods Mol Biol. 2008;445:311-25
pubmed: 18425459
J Cell Biol. 2015 Oct 26;211(2):359-72
pubmed: 26504171
J Cell Biol. 1983 Sep;97(3):692-702
pubmed: 6885916
J Cell Biol. 1997 Apr 7;137(1):113-29
pubmed: 9105041
J Biol Chem. 1998 Apr 17;273(16):9842-51
pubmed: 9545324
Mol Biol Cell. 2002 Oct;13(10):3508-20
pubmed: 12388753
Proc Natl Acad Sci U S A. 2020 Feb 25;117(8):3944-3952
pubmed: 32041870
J Cell Sci. 2016 Dec 1;129(23):4329-4339
pubmed: 27799357
ACS Nano. 2018 Dec 26;12(12):11871-11880
pubmed: 30421608
Cold Spring Harb Perspect Biol. 2014 Aug 01;6(8):
pubmed: 25085912
Sci Rep. 2017 Dec 6;7(1):17068
pubmed: 29213131
J Cell Sci. 1998 Feb;111 ( Pt 3):303-12
pubmed: 9427679
Methods Mol Biol. 2017;1519:227-239
pubmed: 27815883
Int J Environ Res Public Health. 2017 Jan 24;14(2):
pubmed: 28125027
Mol Biosyst. 2010 May;6(5):888-93
pubmed: 20567775
J Cell Biol. 2018 Jan 2;217(1):329-346
pubmed: 29089378
Mol Biol Cell. 2014 Nov 1;25(21):3330-41
pubmed: 25165138
Cell Microbiol. 2013 Jun;15(6):843-59
pubmed: 23253353
Mol Pharm. 2005 Nov-Dec;2(6):440-8
pubmed: 16323951
J Cell Biol. 2016 Mar 14;212(6):677-92
pubmed: 26975849
Biophys Rep (N Y). 2022 Mar 9;2(1):
pubmed: 35382229
J Biol Chem. 1996 Feb 16;271(7):3803-11
pubmed: 8631997
Mol Cell Biol. 2003 Sep;23(18):6494-506
pubmed: 12944476
Biochem Cell Biol. 2002;80(5):509-15
pubmed: 12440692
Mol Biol Cell. 2001 Sep;12(9):2742-55
pubmed: 11553713
Mol Biol Cell. 2002 Feb;13(2):402-11
pubmed: 11854399
Nat Methods. 2012 Jun 10;9(7):724-6
pubmed: 22688415
PLoS One. 2009 Nov 20;4(11):e7919
pubmed: 19936232
J Vis Exp. 2015 Dec 07;(106):e53402
pubmed: 26710109
Cell. 2016 Feb 11;164(4):722-34
pubmed: 26853472
J Biol Chem. 1997 Jun 27;272(26):16147-51
pubmed: 9195911
Nat Cell Biol. 2002 Dec;4(12):945-54
pubmed: 12447391
Plant Physiol. 1992 Feb;98(2):673-9
pubmed: 16668694
Nat Cell Biol. 2020 Nov;22(11):1292-1294
pubmed: 33139938
J Cell Sci. 2009 Jul 15;122(Pt 14):2504-13
pubmed: 19549681
Nat Nanotechnol. 2013 Mar;8(3):193-8
pubmed: 23455985
Trends Cell Biol. 2004 Jul;14(7):343-51
pubmed: 15246427
Cell. 2006 Jul 14;126(1):205-18
pubmed: 16839887
J Cell Biol. 2004 Jan 19;164(2):185-94
pubmed: 14718518
Rev Sci Instrum. 2016 Aug;87(8):084304
pubmed: 27587135
Traffic. 2016 Jul;17(7):786-802
pubmed: 27020146
Proc Natl Acad Sci U S A. 2012 Nov 6;109(45):18447-52
pubmed: 23091040
Proc Natl Acad Sci U S A. 2015 Jul 14;112(28):E3699-708
pubmed: 26124111
Mol Cell Biol. 2014 Nov 15;34(22):4186-99
pubmed: 25225330
J Biol Chem. 2000 Nov 10;275(45):35432-41
pubmed: 10945978
Proc Natl Acad Sci U S A. 2003 May 27;100(11):6481-6
pubmed: 12743369
Nanoscale. 2017 Jan 07;9(1):288-297
pubmed: 27909711
J Cell Sci. 2006 Feb 15;119(Pt 4):659-70
pubmed: 16434478
J Colloid Interface Sci. 2021 Apr;587:64-78
pubmed: 33370664
Traffic. 2005 May;6(5):413-20
pubmed: 15813751
EMBO J. 2012 Feb 15;31(4):932-44
pubmed: 22157818
Biophys J. 2022 Feb 1;121(3):459-469
pubmed: 34968424
Biochem Soc Trans. 2013 Apr;41(2):475-90
pubmed: 23514140
Proc Natl Acad Sci U S A. 2015 Nov 24;112(47):E6486-95
pubmed: 26604306
Langmuir. 2018 Jan 23;34(3):1151-1158
pubmed: 28946746
Biophys J. 2018 Jun 19;114(12):2900-2909
pubmed: 29925026
ACS Nano. 2013 Oct 22;7(10):8634-44
pubmed: 23971739
Naunyn Schmiedebergs Arch Pharmacol. 2011 Mar;383(3):263-73
pubmed: 21136248
Cold Spring Harb Protoc. 2010 Nov 01;2010(11):pdb.prot5527
pubmed: 21041400
Proc Natl Acad Sci U S A. 2015 Apr 14;112(15):4636-41
pubmed: 25825728
Curr Protoc Immunol. 2013 Oct 01;102:14.34.1-14.34.14
pubmed: 24510516
J Cell Sci. 2013 Mar 15;126(Pt 6):1307-16
pubmed: 23645161