Phosphorylation of axin within biomolecular condensates counteracts its tankyrase-mediated degradation.


Journal

Journal of cell science
ISSN: 1477-9137
Titre abrégé: J Cell Sci
Pays: England
ID NLM: 0052457

Informations de publication

Date de publication:
15 10 2023
Historique:
received: 31 03 2023
accepted: 08 09 2023
medline: 30 10 2023
pubmed: 18 9 2023
entrez: 18 9 2023
Statut: ppublish

Résumé

Axin (also known as AXIN1) is a central negative regulator of the proto-oncogenic Wnt/β-catenin signaling pathway, as axin condensates provide a scaffold for the assembly of a multiprotein complex degrading β-catenin. Axin, in turn, is degraded through tankyrase. Consequently, tankyrase small-molecule inhibitors block Wnt signaling by stabilizing axin, revealing potential for cancer therapy. Here, we discovered that axin is phosphorylated by casein kinase 1 alpha 1 (CSNK1A1, also known as CK1α) at an N-terminal casein kinase 1 consensus motif, and that this phosphorylation is antagonized by the catalytic subunit alpha of protein phosphatase 1 (PPP1CA, hereafter referred to as PP1). Axin condensates promoted phosphorylation by enriching CK1α over PP1. Importantly, the phosphorylation took place within the tankyrase-binding site, electrostatically and/or sterically hindering axin-tankyrase interaction, and counteracting tankyrase-mediated degradation of axin. Thus, the presented data propose a novel mechanism regulating axin stability, with implications for Wnt signaling, cancer therapy and self-organization of biomolecular condensates.

Identifiants

pubmed: 37721093
pii: 329027
doi: 10.1242/jcs.261214
pmc: PMC10652037
pii:
doi:

Substances chimiques

Axin Protein 0
Tankyrases EC 2.4.2.30
beta Catenin 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. Published by The Company of Biologists Ltd.

Déclaration de conflit d'intérêts

Competing interests The authors declare no competing or financial interests.

Références

Nat Rev Mol Cell Biol. 2017 May;18(5):285-298
pubmed: 28225081
EMBO J. 2007 Mar 21;26(6):1511-21
pubmed: 17318175
EMBO J. 1998 Mar 2;17(5):1371-84
pubmed: 9482734
J Cell Sci. 2007 Jul 15;120(Pt 14):2402-12
pubmed: 17606995
Genes Dev. 1999 Jul 15;13(14):1768-73
pubmed: 10421629
Eur J Cancer. 2022 Sep;173:41-51
pubmed: 35849876
Nat Commun. 2019 Sep 18;10(1):4251
pubmed: 31534175
Proc Natl Acad Sci U S A. 2011 Feb 1;108(5):1937-42
pubmed: 21245303
Mol Syst Biol. 2011 Oct 11;7:539
pubmed: 21988835
Mol Biol Cell. 2014 Nov 1;25(21):3424-36
pubmed: 25208568
Science. 1998 Apr 24;280(5363):596-9
pubmed: 9554852
Nucleic Acids Res. 2015 Jan;43(Database issue):D512-20
pubmed: 25514926
J Microbiol. 2019 Feb;57(2):93-100
pubmed: 30706340
J Med Chem. 2021 Dec 23;64(24):17936-17949
pubmed: 34878777
Nature. 2009 Oct 1;461(7264):614-20
pubmed: 19759537
J Cell Sci. 2015 Jan 1;128(1):33-9
pubmed: 25380820
J Biol Chem. 1999 Apr 16;274(16):10681-4
pubmed: 10196136
Cell. 2009 Dec 11;139(6):1056-68
pubmed: 20005801
J Cell Biol. 1999 May 17;145(4):741-56
pubmed: 10330403
Cell. 2007 Jun 1;129(5):969-82
pubmed: 17540176
J Clin Invest. 2015 Apr;125(4):1401-18
pubmed: 25798617
Protein Sci. 2018 Jan;27(1):112-128
pubmed: 28836357
Nat Commun. 2022 Feb 3;13(1):674
pubmed: 35115535
J Cell Sci. 2005 Nov 15;118(Pt 22):5269-77
pubmed: 16263762
Cold Spring Harb Perspect Biol. 2013 Jan 01;5(1):a007898
pubmed: 23169527
Cell. 2012 Jun 8;149(6):1192-205
pubmed: 22682243
Mol Cell. 2008 Dec 5;32(5):652-61
pubmed: 19061640
Biochem Biophys Res Commun. 1999 Dec 9;266(1):28-35
pubmed: 10581160
Mol Cell Biol. 1999 Jun;19(6):4414-22
pubmed: 10330181
Development. 2017 Jun 15;144(12):2234-2247
pubmed: 28506997
J Cell Biol. 2018 Apr 2;217(4):1383-1394
pubmed: 29438981
Mol Cell Biol. 2002 Feb;22(4):1184-93
pubmed: 11809809
J Biol Chem. 2002 Jun 14;277(24):21657-65
pubmed: 11940574
Cancer Cell. 2004 Feb;5(2):127-36
pubmed: 14998489
Cell. 1997 Jul 11;90(1):181-92
pubmed: 9230313
Nat Struct Mol Biol. 2007 Jun;14(6):484-92
pubmed: 17529994
J Biol Chem. 1984 Feb 10;259(3):1834-41
pubmed: 6229539
Proc Natl Acad Sci U S A. 2012 Jan 31;109(5):1500-5
pubmed: 22307604
Open Biol. 2011 Nov;1(3):110013
pubmed: 22645652
Mol Cell Biol. 2002 Feb;22(4):1172-83
pubmed: 11809808
Cancer Res. 2005 Sep 15;65(18):8183-92
pubmed: 16166293
Cold Spring Harb Perspect Biol. 2012 Dec 01;4(12):
pubmed: 23209147
J Cell Biol. 2021 Apr 5;220(4):
pubmed: 33651074

Auteurs

Katharina Klement (K)

Experimental Medicine II, Nikolaus-Fiebiger-Center, Friedrich-Alexander University Erlangen-Nürnberg, 91054 Erlangen, Germany.

Martina Brückner (M)

Experimental Medicine II, Nikolaus-Fiebiger-Center, Friedrich-Alexander University Erlangen-Nürnberg, 91054 Erlangen, Germany.

Dominic B Bernkopf (DB)

Experimental Medicine II, Nikolaus-Fiebiger-Center, Friedrich-Alexander University Erlangen-Nürnberg, 91054 Erlangen, Germany.

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Classifications MeSH