Local glycolysis fuels actomyosin contraction during axonal retraction.


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:
04 12 2023
Historique:
received: 27 06 2022
revised: 04 04 2023
accepted: 02 10 2023
pmc-release: 30 04 2024
medline: 31 10 2023
pubmed: 30 10 2023
entrez: 30 10 2023
Statut: ppublish

Résumé

In response to repulsive cues, axonal growth cones can quickly retract. This requires the prompt activity of contractile actomyosin, which is formed by the non-muscle myosin II (NMII) bound to actin filaments. NMII is a molecular motor that provides the necessary mechanical force at the expense of ATP. Here, we report that this process is energetically coupled to glycolysis and is independent of cellular ATP levels. Induction of axonal retraction requires simultaneous generation of ATP by glycolysis, as shown by chemical inhibition and genetic knock-down of GAPDH. Co-immunoprecipitation and proximal-ligation assay showed that actomyosin associates with ATP-generating glycolytic enzymes and that this association is strongly enhanced during retraction. Using microfluidics, we confirmed that the energetic coupling between glycolysis and actomyosin necessary for axonal retraction is localized to the growth cone and near axonal shaft. These results indicate a tight coupling between on-demand energy production by glycolysis and energy consumption by actomyosin contraction suggesting a function of glycolysis in axonal guidance.

Identifiants

pubmed: 37902728
pii: 276367
doi: 10.1083/jcb.202206133
pmc: PMC10616508
pii:
doi:

Substances chimiques

Actomyosin 9013-26-7
Adenosine Triphosphate 8L70Q75FXE

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023 Santos et al.

Références

Science. 2007 May 25;316(5828):1212-6
pubmed: 17525344
J Biochem. 2015 Sep;158(3):245-52
pubmed: 25922200
Nat Methods. 2005 Aug;2(8):599-605
pubmed: 16094385
Cell Motil Cytoskeleton. 1988;9(1):48-59
pubmed: 2895686
Cell. 2013 Jun 20;153(7):1510-25
pubmed: 23791179
Cold Spring Harb Perspect Biol. 2010 Jun;2(6):a001917
pubmed: 20463002
Trends Neurosci. 2014 Oct;37(10):572-82
pubmed: 25167775
F1000Res. 2017 May 18;6:724
pubmed: 28663786
Nat Commun. 2022 Jul 13;13(1):4043
pubmed: 35831314
FEBS Lett. 2018 Jun;592(11):1763-1776
pubmed: 29749605
Development. 2016 Sep 1;143(17):3037-44
pubmed: 27578174
J Cell Sci. 2001 May;114(Pt 9):1643-53
pubmed: 11309196
Science. 2001 Apr 20;292(5516):504-7
pubmed: 11283355
Annu Rev Cell Dev Biol. 2021 Oct 6;37:285-310
pubmed: 34314591
Biophys J. 2006 Feb 15;90(4):1371-84
pubmed: 16326908
J Biol Chem. 2003 Feb 21;278(8):5929-40
pubmed: 12488440
Nat Cell Biol. 2021 May;23(5):457-466
pubmed: 33972734
Crit Rev Biochem Mol Biol. 2020 Aug;55(4):354-371
pubmed: 32646244
Nat Commun. 2018 May 30;9(1):2136
pubmed: 29849027
Cell Biol Int. 2002;26(2):155-64
pubmed: 11846445
Cell Calcium. 2010 Jun;47(6):507-13
pubmed: 20510449
J Neurosci Res. 2019 Aug;97(8):883-889
pubmed: 30575090
Eur J Neurosci. 2010 Sep;32(5):693-706
pubmed: 21050275
Semin Cell Dev Biol. 2014 Nov;35:147-55
pubmed: 25020201
J Cell Biol. 2000 Apr 17;149(2):263-70
pubmed: 10769020
Cell. 2013 Jan 31;152(3):479-91
pubmed: 23374344
Biochem Int. 1990;21(1):53-60
pubmed: 2143653
PLoS One. 2011;6(8):e24284
pubmed: 21904624
Cell. 2001 Apr 20;105(2):233-44
pubmed: 11336673
Antioxid Redox Signal. 2019 Aug 1;31(4):275-317
pubmed: 30585734
Elife. 2022 Oct 12;11:
pubmed: 36222651
J Comp Neurol. 2021 Jul 1;529(10):2517-2538
pubmed: 33438755
Annu Rev Neurosci. 2005;28:127-56
pubmed: 16022592
Elife. 2014 Sep 15;3:e03159
pubmed: 25225054
Curr Top Cell Regul. 1992;33:15-30
pubmed: 1499331
Nat Genet. 2000 May;25(1):25-9
pubmed: 10802651
Proc Natl Acad Sci U S A. 2008 Jun 24;105(25):8760-5
pubmed: 18562289
J Allergy Clin Immunol. 2016 Jan;137(1):231-245.e4
pubmed: 26100081
Development. 2018 Oct 2;145(19):
pubmed: 30177526
Nat Metab. 2021 May;3(5):714-727
pubmed: 34031595
Neural Dev. 2010 Jun 22;5:16
pubmed: 20569485
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
EBioMedicine. 2021 Jul;69:103474
pubmed: 34256347
Nature. 2020 Feb;578(7796):621-626
pubmed: 32051585
Nat Biotechnol. 2002 May;20(5):473-7
pubmed: 11981560
Lancet Neurol. 2015 May;14(5):532-46
pubmed: 25769423
Curr Protoc Immunol. 2018 Nov;123(1):e58
pubmed: 30238640
Development. 2020 Apr 20;147(8):
pubmed: 32265198
Science. 1998 Nov 20;282(5393):1508-11
pubmed: 9822385
Biol Chem. 2013 Nov;394(11):1399-410
pubmed: 23950574
Mol Biol Cell. 2009 Feb;20(4):1167-79
pubmed: 19109430
Nat Methods. 2009 Feb;6(2):161-6
pubmed: 19122669
Annu Rev Cell Dev Biol. 2016 Oct 6;32:577-608
pubmed: 27576119
Curr Opin Neurobiol. 2021 Feb;66:22-29
pubmed: 33039927
Nucleic Acids Res. 2021 Jan 8;49(D1):D325-D334
pubmed: 33290552
EMBO J. 2014 Apr 1;33(7):668-85
pubmed: 24469251
Curr Opin Neurobiol. 2006 Feb;16(1):52-8
pubmed: 16387488
Biopolymers. 2016 Aug;105(8):483-91
pubmed: 27061920
Dev Neurobiol. 2018 Mar;78(3):221-237
pubmed: 29030922
Curr Opin Cell Biol. 2020 Apr;63:11-19
pubmed: 31927278
Nat Commun. 2016 Oct 24;7:13233
pubmed: 27775035
J Cell Biol. 1984 Jul;99(1 Pt 2):222s-225s
pubmed: 6746730
Nature. 2021 Jul;595(7865):120-124
pubmed: 34079125
Biol Psychiatry. 2020 Mar 15;87(6):559-569
pubmed: 31604519
J Neurosci. 2021 Aug 4;41(31):6637-6651
pubmed: 34252036
Antioxid Redox Signal. 2021 Oct 1;35(10):788-807
pubmed: 32368925
Nature. 2016 Nov 24;539(7630):555-559
pubmed: 27828947
J Biol Chem. 2002 Feb 22;277(8):6214-22
pubmed: 11739394
Neuroimage. 2019 Jan 15;185:825-835
pubmed: 29654875
J Cell Sci. 2006 Aug 15;119(Pt 16):3413-23
pubmed: 16899819
Neuron. 2012 Mar 8;73(5):911-24
pubmed: 22405202
Eur J Pharmacol. 2000 Apr 21;395(1):1-7
pubmed: 10781666
Cold Spring Harb Perspect Biol. 2010 Mar;2(3):a001784
pubmed: 20300212
Front Mol Neurosci. 2017 Oct 10;10:317
pubmed: 29066950
Nat Rev Mol Cell Biol. 2021 Mar;22(3):215-235
pubmed: 33169001
Science. 1984 Sep 21;225(4668):1258-65
pubmed: 6474175
Amino Acids. 2021 Apr;53(4):507-515
pubmed: 33651246
Cell Metab. 2005 Aug;2(2):119-29
pubmed: 16098829
Cell Metab. 2017 Aug 1;26(2):361-374.e4
pubmed: 28768175
Front Cell Neurosci. 2018 Nov 26;12:447
pubmed: 30534055
Pharmacology. 2012;90(1-2):19-39
pubmed: 22776780
Nucleic Acids Res. 2019 Jan 8;47(D1):D419-D426
pubmed: 30407594
Nat Commun. 2014 Nov 21;5:5566
pubmed: 25412762
Neural Plast. 2019 Apr 14;2019:1719829
pubmed: 31097955
Cold Spring Harb Protoc. 2012 Mar 01;2012(3):335-9
pubmed: 22383652
Nat Methods. 2008 Jul;5(7):605-7
pubmed: 18536722
Neurochem Res. 2009 May;34(5):807-18
pubmed: 18751889
Neuron. 2003 Dec 4;40(5):931-44
pubmed: 14659092
Cytoskeleton (Hoboken). 2010 Sep;67(9):545-54
pubmed: 20803696
J Cell Biol. 2018 Jul 2;217(7):2235-2246
pubmed: 29752396
Nat Rev Neurosci. 2014 Dec;15(12):786-801
pubmed: 25409697
J Neurosci. 2006 Mar 22;26(12):3141-53
pubmed: 16554465
Lab Chip. 2011 Nov 7;11(21):3663-73
pubmed: 21922081
Mol Biol Cell. 2003 Nov;14(11):4654-66
pubmed: 12960431

Auteurs

Renata Santos (R)

Université Paris Cité, Institute of Psychiatry and Neuroscience of Paris, INSERM U1266, Laboratory of Dynamics of Neuronal Structure in Health and Disease, Paris, France.
Institut des Sciences Biologiques, Centre national de la recherche scientifique , Paris, France.

Ludmilla Lokmane (L)

Institut de Biologie de l'Ecole Normale Supérieure, École Normale Supérieure, Centre national de la recherche scientifique, Paris Sciences et Lettres Research University , Paris, France.

Dersu Ozdemir (D)

Université Paris Cité, Institute of Psychiatry and Neuroscience of Paris, INSERM U1266, Laboratory of Dynamics of Neuronal Structure in Health and Disease, Paris, France.

Clément Traoré (C)

Brain Plasticity Unit, École Supérieure de Physique et de Chimie Industrielles-ParisTech , Paris, France.

Annabelle Agesilas (A)

Brain Plasticity Unit, École Supérieure de Physique et de Chimie Industrielles-ParisTech , Paris, France.

Coralie Hakibilen (C)

Brain Plasticity Unit, École Supérieure de Physique et de Chimie Industrielles-ParisTech , Paris, France.

Zsolt Lenkei (Z)

Université Paris Cité, Institute of Psychiatry and Neuroscience of Paris, INSERM U1266, Laboratory of Dynamics of Neuronal Structure in Health and Disease, Paris, France.
Brain Plasticity Unit, École Supérieure de Physique et de Chimie Industrielles-ParisTech , Paris, France.
GHU-Paris Psychiatrie et Neurosciences, Hôpital Sainte Anne, Paris, France.

Diana Zala (D)

Université Paris Cité, Institute of Psychiatry and Neuroscience of Paris, INSERM U1266, Laboratory of Dynamics of Neuronal Structure in Health and Disease, Paris, France.
Brain Plasticity Unit, École Supérieure de Physique et de Chimie Industrielles-ParisTech , Paris, France.

Articles similaires

Adenosine Triphosphate Adenosine Diphosphate Mitochondrial ADP, ATP Translocases Binding Sites Mitochondria
Animals Astrocytes Amyloid beta-Protein Precursor Mice Mice, Transgenic

Glucose and glutamine drive hepatitis E virus replication.

Shaheen Khan, Suruchi Aggarwal, Pooja Bhatia et al.
1.00
Glutamine Virus Replication Hepatitis E virus Glucose Glycolysis
Animals Hypoxia-Inducible Factor 1, alpha Subunit Glycolysis Interferon-gamma Humans

Classifications MeSH