Intestinal Paneth cell differentiation relies on asymmetric regulation of Wnt signaling by Daam1/2.


Journal

Science advances
ISSN: 2375-2548
Titre abrégé: Sci Adv
Pays: United States
ID NLM: 101653440

Informations de publication

Date de publication:
24 11 2023
Historique:
medline: 27 11 2023
pubmed: 24 11 2023
entrez: 24 11 2023
Statut: ppublish

Résumé

The mammalian intestine is one of the most rapidly self-renewing tissues, driven by stem cells residing at the crypt bottom. Paneth cells form a major element of the niche microenvironment providing various growth factors to orchestrate intestinal stem cell homeostasis, such as Wnt3. Different Wnt ligands can selectively activate β-catenin-dependent (canonical) or -independent (noncanonical) signaling. Here, we report that the Dishevelled-associated activator of morphogenesis 1 (Daam1) and its paralogue Daam2 asymmetrically regulate canonical and noncanonical Wnt (Wnt/PCP) signaling. Daam1/2 interacts with the Wnt inhibitor RNF43, and Daam1/2 double knockout stimulates canonical Wnt signaling by preventing RNF43-dependent degradation of the Wnt receptor, Frizzled (Fzd). Single-cell RNA sequencing analysis revealed that Paneth cell differentiation is impaired by Daam1/2 depletion because of defective Wnt/PCP signaling. Together, we identified Daam1/2 as an unexpected hub molecule coordinating both canonical and noncanonical Wnt, which is fundamental for specifying an adequate number of Paneth cells.

Identifiants

pubmed: 38000028
doi: 10.1126/sciadv.adh9673
pmc: PMC10672176
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

eadh9673

Subventions

Organisme : Czech Science Foundation
ID : GX19-28347X
Organisme : National Institute for Cancer Research
ID : LX22NPO5102
Organisme : Dutch Cancer Society
ID : 13112

Références

Nature. 2012 Aug 30;488(7413):665-9
pubmed: 22895187
Proc Natl Acad Sci U S A. 2007 Apr 17;104(16):6708-13
pubmed: 17412835
EMBO Rep. 2021 May 5;22(5):e52970
pubmed: 33938624
Small GTPases. 2014;5:e29513
pubmed: 24914801
Int J Stem Cells. 2023 Aug 30;:
pubmed: 37643759
Proc Natl Acad Sci U S A. 2015 Jun 16;112(24):7548-50
pubmed: 26023187
Development. 2015 Jan 1;142(1):99-107
pubmed: 25480917
Exp Mol Med. 2022 Sep;54(9):1367-1378
pubmed: 36117218
J Biol Chem. 2020 Apr 10;295(15):5124-5135
pubmed: 32107310
EMBO J. 1999 Feb 1;18(3):578-85
pubmed: 9927417
Nature. 2016 Jul 21;535(7612):430-4
pubmed: 27398620
Annu Rev Physiol. 2013;75:289-311
pubmed: 23398152
Development. 2016 Dec 1;143(23):4509-4520
pubmed: 27789627
Nature. 2016 Feb 18;530(7590):340-3
pubmed: 26863187
PLoS One. 2016 Oct 19;11(10):e0163915
pubmed: 27760153
Nature. 2011 Jul 04;476(7360):293-7
pubmed: 21727895
Nat Cell Biol. 2021 Jan;23(1):23-31
pubmed: 33398177
J Cell Biol. 2006 Nov 20;175(4):555-62
pubmed: 17101698
Dev Biol. 2022 Feb;482:1-6
pubmed: 34818531
Nat Rev Mol Cell Biol. 2021 Jan;22(1):39-53
pubmed: 32958874
Proc Natl Acad Sci U S A. 2008 Jan 8;105(1):210-5
pubmed: 18162551
Nature. 2012 Apr 29;485(7397):195-200
pubmed: 22575959
Genome Biol. 2014;15(12):550
pubmed: 25516281
Proc Natl Acad Sci U S A. 2018 Sep 25;115(39):E9135-E9144
pubmed: 30209221
Nat Methods. 2019 Dec;16(12):1289-1296
pubmed: 31740819
Cell. 2021 Jun 24;184(13):3573-3587.e29
pubmed: 34062119
Proc Natl Acad Sci U S A. 2012 Jul 17;109(29):11717-22
pubmed: 22753465
Cell. 2001 Dec 28;107(7):843-54
pubmed: 11779461
J Vis Exp. 2020 Jun 5;(160):
pubmed: 32568249
Dev Biol. 2016 Dec 15;420(2):271-277
pubmed: 27983963
Nat Commun. 2020 Sep 15;11(1):4586
pubmed: 32934222
Gene Expr Patterns. 2020 Dec;38:119153
pubmed: 33186756
Nature. 1998 Jan 22;391(6665):357-62
pubmed: 9450748
Mol Cell Biol. 2017 Aug 28;37(18):
pubmed: 28674183
Cell Stem Cell. 2018 Dec 6;23(6):787-793.e6
pubmed: 30526881
Int J Mol Sci. 2020 Nov 27;21(23):
pubmed: 33261128
Cell Syst. 2019 Apr 24;8(4):329-337.e4
pubmed: 30954475
Sci Rep. 2020 Dec 9;10(1):21555
pubmed: 33299006
Elife. 2021 Oct 27;10:
pubmed: 34702444
EMBO Rep. 2021 May 5;22(5):e51415
pubmed: 33786993
Nature. 2011 Jan 20;469(7330):415-8
pubmed: 21113151
Anal Chem. 1996 Mar 1;68(5):850-8
pubmed: 8779443
Br J Pharmacol. 2017 Dec;174(24):4701-4715
pubmed: 28703283
Differentiation. 2014 Jul;88(1):17-26
pubmed: 24798204
EMBO J. 2007 May 16;26(10):2513-26
pubmed: 17476309
Nature. 2022 Oct;610(7930):182-189
pubmed: 36131013
Curr Biol. 2013 Jul 22;23(14):1373-9
pubmed: 23850281
EMBO Rep. 2011 Sep 30;12(10):1055-61
pubmed: 21909076
ACS Chem Biol. 2018 Feb 16;13(2):467-474
pubmed: 28892606
J Vis Exp. 2017 Jul 12;(125):
pubmed: 28745625
Dev Growth Differ. 2021 Apr;63(3):199-218
pubmed: 33619734
Cancers (Basel). 2016 Jun 08;8(6):
pubmed: 27338477
Dev Biol. 2017 Jun 15;426(2):176-187
pubmed: 27016259
Nat Commun. 2017 Jan 16;8:14049
pubmed: 28091601
Nature. 2016 Oct 19;538(7625):336-343
pubmed: 27762356
Genes Dev. 2014 Feb 15;28(4):305-16
pubmed: 24532711
Bioinformatics. 2021 Apr 1;36(22-23):5535-5536
pubmed: 33313640
Mol Cell. 2015 May 7;58(3):522-33
pubmed: 25891077
Cell. 2017 Jun 1;169(6):985-999
pubmed: 28575679
Annu Rev Cell Dev Biol. 2021 Oct 6;37:369-389
pubmed: 34196570

Auteurs

Gabriele Colozza (G)

Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), 1030 Vienna, Austria.

Heetak Lee (H)

Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), 1030 Vienna, Austria.
Center for Genome Engineering, Institute for Basic Science, 55, Expo-ro, Yuseong-gu, Daejeon 34126, Republic of Korea.

Alessandra Merenda (A)

HUB Organoids, Utrecht, Netherlands.

Szu-Hsien Sam Wu (SS)

Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), 1030 Vienna, Austria.

Andrea Català-Bordes (A)

Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), 1030 Vienna, Austria.

Tomasz W Radaszkiewicz (TW)

Department of Experimental Biology, Faculty of Science, Masaryk University, Brno, Czech Republic.

Ingrid Jordens (I)

Oncode Institute and Centre for Molecular Medicine, University Medical Centre Utrecht, Utrecht, Netherlands.

Ji-Hyun Lee (JH)

Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), 1030 Vienna, Austria.
Center for Genome Engineering, Institute for Basic Science, 55, Expo-ro, Yuseong-gu, Daejeon 34126, Republic of Korea.

Aileen-Diane Bamford (AD)

Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), 1030 Vienna, Austria.
Department of Biosystems Science and Engineering, ETH Zurich, Mattenstrasse 26, 4058 Basel, Switzerland.

Fiona Farnhammer (F)

Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), 1030 Vienna, Austria.
Division of Metabolism and Division of Oncology, University Children's Hospital Zurich and Children's Research Center, University of Zurich, 8032 Zurich, Switzerland.

Teck Yew Low (TY)

UKM Medical Molecular Biology Institute (UMBI), University Kebangsaan Malaysia (UKM), Jalan Yaacob Latiff, Bandar Tun Razak, 56000 Kuala Lumpur, Malaysia.

Madelon M Maurice (MM)

Oncode Institute and Centre for Molecular Medicine, University Medical Centre Utrecht, Utrecht, Netherlands.

Vítězslav Bryja (V)

Department of Experimental Biology, Faculty of Science, Masaryk University, Brno, Czech Republic.
Department of Cytokinetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, Brno, Czech Republic.

Jihoon Kim (J)

Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), 1030 Vienna, Austria.
Department of Medical and Biological Sciences, The Catholic University of Korea, Bucheon, Republic of Korea.

Bon-Kyoung Koo (BK)

Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), 1030 Vienna, Austria.
Center for Genome Engineering, Institute for Basic Science, 55, Expo-ro, Yuseong-gu, Daejeon 34126, Republic of Korea.
Department of Life Sciences, Pohang University of Science and Technology (POSTECH), Pohang, Republic of Korea.

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