CRB1 is required for recycling by RAB11A+ vesicles in human retinal organoids.


Journal

Stem cell reports
ISSN: 2213-6711
Titre abrégé: Stem Cell Reports
Pays: United States
ID NLM: 101611300

Informations de publication

Date de publication:
12 09 2023
Historique:
received: 22 12 2021
revised: 03 07 2023
accepted: 04 07 2023
medline: 15 9 2023
pubmed: 5 8 2023
entrez: 4 8 2023
Statut: ppublish

Résumé

CRB1 gene mutations can cause early- or late-onset retinitis pigmentosa, Leber congenital amaurosis, or maculopathy. Recapitulating human CRB1 phenotypes in animal models has proven challenging, necessitating the development of alternatives. We generated human induced pluripotent stem cell (iPSC)-derived retinal organoids of patients with retinitis pigmentosa caused by biallelic CRB1 mutations and evaluated them against autologous gene-corrected hiPSCs and hiPSCs from healthy individuals. Patient organoids show decreased levels of CRB1 and NOTCH1 expression at the retinal outer limiting membrane. Proximity ligation assays show that human CRB1 and NOTCH1 can interact via their extracellular domains. CRB1 patient organoids feature increased levels of WDFY1+ vesicles, fewer RAB11A+ recycling endosomes, decreased VPS35 retromer complex components, and more degradative endolysosomal compartments relative to isogenic control organoids. Taken together, our data demonstrate that patient-derived retinal organoids enable modeling of retinal degeneration and highlight the importance of CRB1 in early endosome maturation receptor recycling in the retina.

Identifiants

pubmed: 37541258
pii: S2213-6711(23)00263-1
doi: 10.1016/j.stemcr.2023.07.001
pmc: PMC10545476
pii:
doi:

Substances chimiques

Eye Proteins 0
CRB1 protein, human 0
Membrane Proteins 0
Nerve Tissue Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1793-1810

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interests The authors declare no competing interests. The LUMC is holder of patent number PCT/NL2014/050549, which describes the potential clinical use of CRB2; J.W. and L.P.P. are listed as co-inventor of this patent, and J.W. is an employee of the LUMC.

Références

PLoS Biol. 2014 Apr 29;12(4):e1001847
pubmed: 24781186
Hum Mol Genet. 2018 Sep 15;27(18):3137-3153
pubmed: 29893966
J Cell Sci. 2004 Aug 15;117(Pt 18):4169-77
pubmed: 15316081
Front Cell Dev Biol. 2021 Feb 09;8:608112
pubmed: 33634099
Development. 2010 Feb;137(4):641-50
pubmed: 20110329
Nature. 1998 Jul 30;394(6692):432-3
pubmed: 9697764
Hum Reprod. 2019 Mar 1;34(3):519-529
pubmed: 30597006
Neuron. 2011 Jan 27;69(2):215-30
pubmed: 21262462
Hum Mol Genet. 2013 Jan 1;22(1):35-50
pubmed: 23001562
Glia. 2007 Nov 1;55(14):1486-97
pubmed: 17705196
PLoS One. 2019 Dec 13;14(12):e0220220
pubmed: 31834921
Curr Biol. 2011 Jul 12;21(13):1111-7
pubmed: 21700461
Nat Chem Biol. 2018 Aug;14(8):801-810
pubmed: 29915378
Dev Cell. 2011 Dec 13;21(6):1171-8
pubmed: 22172677
Stem Cell Reports. 2023 May 9;18(5):1123-1137
pubmed: 37084726
Cell Rep. 2017 Apr 11;19(2):351-363
pubmed: 28402857
Stem Cell Reports. 2019 May 14;12(5):906-919
pubmed: 30956116
Cell Rep. 2019 Jul 2;28(1):51-64.e4
pubmed: 31269450
Eur J Cell Biol. 2015 Nov;94(11):513-21
pubmed: 26220253
PLoS One. 2013 Dec 06;8(12):e82532
pubmed: 24324803
Elife. 2019 Nov 07;8:
pubmed: 31697234
Dev Cell. 2012 Jun 12;22(6):1261-74
pubmed: 22579223
Hum Mol Genet. 2015 Jun 1;24(11):3104-18
pubmed: 25701872
Cell Rep. 2022 Sep 13;40(11):111349
pubmed: 36103833
J Biol Chem. 2008 Mar 14;283(11):6783-9
pubmed: 18174161
Am J Ophthalmol. 2022 Feb;234:37-48
pubmed: 34320374
Hum Mol Genet. 2006 Sep 15;15(18):2659-72
pubmed: 16885194
J Neurochem. 2021 Apr;157(2):263-296
pubmed: 32964462
Dev Biol. 2020 Mar 15;459(2):126-137
pubmed: 31881198
Dev Biol. 2011 Dec 1;360(1):87-95
pubmed: 21958744
J Cell Sci. 2001 Nov;114(Pt 22):3991-4000
pubmed: 11739631
EMBO Rep. 2006 Mar;7(3):297-302
pubmed: 16440003
Sci Rep. 2021 Jul 15;11(1):14525
pubmed: 34267251
PLoS Genet. 2013;9(12):e1003976
pubmed: 24339791
Mol Ther Methods Clin Dev. 2020 Dec 25;20:423-441
pubmed: 33575434
Nat Rev Mol Cell Biol. 2013 May;14(5):307-14
pubmed: 23609509
Front Cell Neurosci. 2019 Aug 13;13:368
pubmed: 31456666
Front Neurosci. 2020 Aug 14;14:860
pubmed: 32922261
Hum Mol Genet. 2019 Jan 1;28(1):105-123
pubmed: 30239717
Hum Mol Genet. 2014 Jul 15;23(14):3759-71
pubmed: 24565864
Transgenic Res. 2006 Apr;15(2):255-9
pubmed: 16604465
J Biomed Biotechnol. 2011;2011:868217
pubmed: 21912482
Development. 2016 Dec 1;143(23):4543-4553
pubmed: 27899511

Auteurs

Thilo M Buck (TM)

Department of Ophthalmology, Leiden University Medical Center (LUMC), Leiden 2333 ZA, the Netherlands.

Peter M J Quinn (PMJ)

Department of Ophthalmology, Leiden University Medical Center (LUMC), Leiden 2333 ZA, the Netherlands.

Lucie P Pellissier (LP)

Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences (KNAW), Amsterdam 1105 BA, the Netherlands.

Aat A Mulder (AA)

Department of Cell & Chemical Biology, Leiden University Medical Center (LUMC), Leiden 2300 RC, the Netherlands.

Aldo Jongejan (A)

Bioinformatics Laboratory, Epidemiology & Data Science, Amsterdam University Medical Centers, Amsterdam 1105 AZ, the Netherlands.

Xuefei Lu (X)

Department of Ophthalmology, Leiden University Medical Center (LUMC), Leiden 2333 ZA, the Netherlands.

Nanda Boon (N)

Department of Ophthalmology, Leiden University Medical Center (LUMC), Leiden 2333 ZA, the Netherlands.

Daniëlle Koot (D)

Department of Ophthalmology, Leiden University Medical Center (LUMC), Leiden 2333 ZA, the Netherlands.

Hind Almushattat (H)

Department of Ophthalmology, Leiden University Medical Center (LUMC), Leiden 2333 ZA, the Netherlands.

Christiaan H Arendzen (CH)

Leiden University Medical Center hiPSC Hotel, Leiden 2333 ZA, the Netherlands.

Rogier M Vos (RM)

Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences (KNAW), Amsterdam 1105 BA, the Netherlands.

Edward J Bradley (EJ)

Department of Genome Analysis, Amsterdam University Medical Centers, Amsterdam 1105 AZ, the Netherlands.

Christian Freund (C)

Leiden University Medical Center hiPSC Hotel, Leiden 2333 ZA, the Netherlands.

Harald M M Mikkers (HMM)

Department of Cell & Chemical Biology, Leiden University Medical Center (LUMC), Leiden 2300 RC, the Netherlands; Leiden University Medical Center hiPSC Hotel, Leiden 2333 ZA, the Netherlands.

Camiel J F Boon (CJF)

Department of Ophthalmology, Leiden University Medical Center (LUMC), Leiden 2333 ZA, the Netherlands; Department of Ophthalmology, Amsterdam University Medical Centers, Academic Medical Center, University of Amsterdam, Amsterdam 1000 AE, the Netherlands.

Perry D Moerland (PD)

Bioinformatics Laboratory, Epidemiology & Data Science, Amsterdam University Medical Centers, Amsterdam 1105 AZ, the Netherlands.

Frank Baas (F)

Department of Genome Analysis, Amsterdam University Medical Centers, Amsterdam 1105 AZ, the Netherlands; Department of Clinical Genetics/LDGA, Leiden University Medical Center, Leiden 2333 ZA, the Netherlands.

Abraham J Koster (AJ)

Department of Cell & Chemical Biology, Leiden University Medical Center (LUMC), Leiden 2300 RC, the Netherlands.

Jacques Neefjes (J)

Department of Cell & Chemical Biology, Leiden University Medical Center (LUMC), Leiden 2300 RC, the Netherlands.

Ilana Berlin (I)

Department of Cell & Chemical Biology, Leiden University Medical Center (LUMC), Leiden 2300 RC, the Netherlands.

Carolina R Jost (CR)

Department of Cell & Chemical Biology, Leiden University Medical Center (LUMC), Leiden 2300 RC, the Netherlands.

Jan Wijnholds (J)

Department of Ophthalmology, Leiden University Medical Center (LUMC), Leiden 2333 ZA, the Netherlands; Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences (KNAW), Amsterdam 1105 BA, the Netherlands. Electronic address: j.wijnholds@lumc.nl.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH