The USP46 complex deubiquitylates LRP6 to promote Wnt/β-catenin signaling.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
05 10 2023
Historique:
received: 11 03 2021
accepted: 20 09 2023
medline: 23 10 2023
pubmed: 6 10 2023
entrez: 5 10 2023
Statut: epublish

Résumé

The relative abundance of Wnt receptors plays a crucial role in controlling Wnt signaling in tissue homeostasis and human disease. While the ubiquitin ligases that ubiquitylate Wnt receptors are well-characterized, the deubiquitylase that reverses these reactions remains unclear. Herein, we identify USP46, UAF1, and WDR20 (USP46 complex) as positive regulators of Wnt signaling in cultured human cells. We find that the USP46 complex is similarly required for Wnt signaling in Xenopus and zebrafish embryos. We demonstrate that Wnt signaling promotes the association between the USP46 complex and cell surface Wnt coreceptor, LRP6. Knockdown of USP46 decreases steady-state levels of LRP6 and increases the level of ubiquitylated LRP6. In contrast, overexpression of the USP46 complex blocks ubiquitylation of LRP6 by the ubiquitin ligases RNF43 and ZNFR3. Size exclusion chromatography studies suggest that the size of the USP46 cytoplasmic complex increases upon Wnt stimulation. Finally, we show that USP46 is essential for Wnt-dependent intestinal organoid viability, likely via its role in LRP6 receptor homeostasis. We propose a model in which the USP46 complex increases the steady-state level of cell surface LRP6 and facilitates the assembly of LRP6 into signalosomes via a pruning mechanism that removes sterically hindering ubiquitin chains.

Identifiants

pubmed: 37798301
doi: 10.1038/s41467-023-41836-z
pii: 10.1038/s41467-023-41836-z
pmc: PMC10556042
doi:

Substances chimiques

beta Catenin 0
Ligases EC 6.-
Low Density Lipoprotein Receptor-Related Protein-6 0
LRP6 protein, human 0
Receptors, Wnt 0
Ubiquitin 0
ubiquitin-specific peptidase 46, human EC 3.4.-
Endopeptidases EC 3.4.-

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

6173

Subventions

Organisme : NIGMS NIH HHS
ID : P20 GM113132
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA281002
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA023108
Pays : United States
Organisme : Cancer Research UK
ID : A28592
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R35 GM136233
Pays : United States
Organisme : NIH HHS
ID : S10 OD032310
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA244188
Pays : United States

Informations de copyright

© 2023. Springer Nature Limited.

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Auteurs

Victoria H Ng (VH)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA.
Program in Cancer Biology, Vanderbilt University, Nashville, TN, 37232, USA.

Zachary Spencer (Z)

Department of Molecular and Systems Biology and the Dartmouth Cancer Center, Geisel School of Medicine at Dartmouth College, Hanover, NH, 03755, USA.

Leif R Neitzel (LR)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA.
Department of Medicine, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.

Anmada Nayak (A)

Department of Oncology, Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC, 20057, USA.

Matthew A Loberg (MA)

Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, 37232, USA.

Chen Shen (C)

Department of Oncology, Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC, 20057, USA.

Sara N Kassel (SN)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA.

Heather K Kroh (HK)

Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, 37232, USA.

Zhenyi An (Z)

UCSF Helen Diller Family Comprehensive Cancer Center, San Francisco, CA, 94158, USA.
Department of Pediatrics, University of California San Francisco, San Francisco, CA, 94158, USA.

Christin C Anthony (CC)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA.

Jamal M Bryant (JM)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA.

Amanda Lawson (A)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA.

Lily Goldsmith (L)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA.

Hassina Benchabane (H)

Department of Molecular and Systems Biology and the Dartmouth Cancer Center, Geisel School of Medicine at Dartmouth College, Hanover, NH, 03755, USA.

Amanda G Hansen (AG)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA.
STEMCELL Technologies, 1618 Station Street, Vancouver, BC, V6A 1B6, Canada.

Jingjing Li (J)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA.

Starina D'Souza (S)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA.

Andres M Lebensohn (AM)

Laboratory of Cellular and Molecular Biology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, 20892, USA.

Rajat Rohatgi (R)

Departments of Biochemistry, Stanford University School of Medicine, Stanford, CA, 94305, USA.

William A Weiss (WA)

UCSF Helen Diller Family Comprehensive Cancer Center, San Francisco, CA, 94158, USA.
Department of Pediatrics, University of California San Francisco, San Francisco, CA, 94158, USA.

Vivian L Weiss (VL)

Department of Pathology, Microbiology, and Immunology, Vanderbilt University Medical Center, Nashville, TN, 37232, USA.

Charles Williams (C)

Department of Medicine, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.

Charles C Hong (CC)

Department of Medicine, University of Maryland School of Medicine, Baltimore, MD, 21201, USA.

David J Robbins (DJ)

Department of Oncology, Lombardi Comprehensive Cancer Center, Georgetown University, Washington, DC, 20057, USA.

Yashi Ahmed (Y)

Department of Molecular and Systems Biology and the Dartmouth Cancer Center, Geisel School of Medicine at Dartmouth College, Hanover, NH, 03755, USA. yashi.ahmed@dartmouth.edu.

Ethan Lee (E)

Department of Cell & Developmental Biology, Vanderbilt University, Nashville, TN, 37232, USA. ethan.lee@vanderbilt.edu.
Program in Cancer Biology, Vanderbilt University, Nashville, TN, 37232, USA. ethan.lee@vanderbilt.edu.
Vanderbilt Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, TN, 37232, USA. ethan.lee@vanderbilt.edu.

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Classifications MeSH