Optimized human intestinal organoid model reveals interleukin-22-dependency of paneth cell formation.


Journal

Cell stem cell
ISSN: 1875-9777
Titre abrégé: Cell Stem Cell
Pays: United States
ID NLM: 101311472

Informations de publication

Date de publication:
01 09 2022
Historique:
received: 11 02 2022
revised: 01 07 2022
accepted: 05 08 2022
pubmed: 25 8 2022
medline: 9 9 2022
entrez: 24 8 2022
Statut: ppublish

Résumé

Opposing roles have been proposed for IL-22 in intestinal pathophysiology. We have optimized human small intestinal organoid (hSIO) culturing, constitutively generating all differentiated cell types while maintaining an active stem cell compartment. IL-22 does not promote the expansion of stem cells but rather slows the growth of hSIOs. In hSIOs, IL-22 is required for formation of Paneth cells, the prime producers of intestinal antimicrobial peptides (AMPs). Introduction of inflammatory bowel disease (IBD)-associated loss-of-function mutations in the IL-22 co-receptor gene IL10RB resulted in abolishment of Paneth cells in hSIOs. Moreover, IL-22 induced expression of host defense genes (such as REG1A, REG1B, and DMBT1) in enterocytes, goblet cells, Paneth cells, Tuft cells, and even stem cells. Thus, IL-22 does not directly control the regenerative capacity of crypt stem cells but rather boosts Paneth cell numbers, as well as the expression of AMPs in all cell types.

Identifiants

pubmed: 36002022
pii: S1934-5909(22)00338-1
doi: 10.1016/j.stem.2022.08.002
pmc: PMC9438971
pii:
doi:

Substances chimiques

Calcium-Binding Proteins 0
DMBT1 protein, human 0
DNA-Binding Proteins 0
Interleukins 0
Tumor Suppressor Proteins 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1333-1345.e6

Commentaires et corrections

Type : ErratumIn

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests H.C. is an inventor of several patents related to organoid technology; his full disclosure is given at https://www.uu.nl/staff/JCClevers/.

Références

Immunity. 2008 Dec 19;29(6):947-57
pubmed: 19100701
Gastroenterology. 2011 Nov;141(5):1762-72
pubmed: 21889923
Cell Death Dis. 2015 Feb 05;6:e1631
pubmed: 25654764
Nat Biotechnol. 2018 Oct;36(9):843-846
pubmed: 29813047
Mucosal Immunol. 2014 Jan;7(1):143-54
pubmed: 23715173
N Engl J Med. 2009 Nov 19;361(21):2033-45
pubmed: 19890111
Cell Mol Gastroenterol Hepatol. 2018 Jul 04;7(1):1-17
pubmed: 30364840
Cell Rep. 2021 Feb 16;34(7):108757
pubmed: 33596425
Nat Rev Microbiol. 2011 May;9(5):356-68
pubmed: 21423246
Clin Pharmacol Ther. 2019 Jan;105(1):177-189
pubmed: 29952004
Nat Cell Biol. 2020 Mar;22(3):321-331
pubmed: 32123335
Cell Rep. 2021 Mar 9;34(10):108819
pubmed: 33691112
Nat Rev Drug Discov. 2014 Jan;13(1):21-38
pubmed: 24378801
BMC Genomics. 2018 Jun 19;19(1):477
pubmed: 29914354
Bioinformatics. 2016 Apr 15;32(8):1241-3
pubmed: 26668002
Stem Cell Reports. 2015 Nov 10;5(5):908-917
pubmed: 26527385
Annu Rev Physiol. 2013;75:289-311
pubmed: 23398152
Cell. 2020 Aug 20;182(4):1062-1064
pubmed: 32822568
Biochem Pharmacol. 2018 Jun;152:224-235
pubmed: 29608910
Science. 2015 Jan 23;347(6220):1260419
pubmed: 25613900
Sci Immunol. 2020 Oct 2;5(52):
pubmed: 33008915
Science. 2016 Oct 21;354(6310):358-362
pubmed: 27846573
Mucosal Immunol. 2021 Mar;14(2):389-401
pubmed: 33060802
Nature. 2009 May 14;459(7244):262-5
pubmed: 19329995
Nature. 2015 Dec 24;528(7583):560-564
pubmed: 26649819
Nat Biotechnol. 2020 Dec;38(12):1408-1414
pubmed: 32747759
Cell Mol Gastroenterol Hepatol. 2022;13(5):1554-1589
pubmed: 35176508
Nat Protoc. 2015 Oct;10(10):1474-85
pubmed: 26334867
J Clin Invest. 2008 Feb;118(2):534-44
pubmed: 18172556
Cell Stem Cell. 2020 Oct 1;27(4):646-662.e7
pubmed: 32693086
Genome Biol. 2019 Dec 23;20(1):296
pubmed: 31870423
Am J Gastroenterol. 2011 Aug;106(8):1544-55
pubmed: 21519361
Immunity. 2014 Oct 16;41(4):620-32
pubmed: 25367575
Nature. 2012 Jun 28;486(7404):490-5
pubmed: 22722868
PLoS Pathog. 2016 Apr 07;12(4):e1005481
pubmed: 27055194
J Exp Med. 2020 Feb 13;217(3):e20192195
pubmed: 32997932
J Gastroenterol. 2018 Apr;53(4):465-474
pubmed: 29075900
Elife. 2021 Oct 11;10:
pubmed: 34633285
Cell Stem Cell. 2018 Dec 6;23(6):787-793.e6
pubmed: 30526881
Proc Natl Acad Sci U S A. 2018 Oct 2;115(40):10118-10123
pubmed: 30217896
Nature. 2011 Jan 20;469(7330):415-8
pubmed: 21113151
Inflamm Bowel Dis. 2008 Feb;14(2):204-12
pubmed: 18022867
PLoS One. 2020 Oct 22;15(10):e0240802
pubmed: 33091031
Cell. 2019 Jun 13;177(7):1888-1902.e21
pubmed: 31178118
Cell Mol Gastroenterol Hepatol. 2019;7(2):255-274
pubmed: 30686779
Curr Protoc Immunol. 2020 Sep;130(1):e106
pubmed: 32940424
Science. 2016 Apr 8;352(6282):189-96
pubmed: 27124452
Nat Commun. 2022 Feb 15;13(1):874
pubmed: 35169117
Mucosal Immunol. 2012 Jan;5(1):99-109
pubmed: 22089030
Science. 2001 Dec 7;294(5549):2155-8
pubmed: 11739954
Nat Immunol. 2009 Jan;10(1):83-91
pubmed: 19029903
Nat Immunol. 2011 May;12(5):383-90
pubmed: 21502992
PLoS Pathog. 2013;9(10):e1003698
pubmed: 24130494

Auteurs

Gui-Wei He (GW)

Oncode Institute, Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center, Uppsalalaan 8, Utrecht, 3584 CT, the Netherlands.

Lin Lin (L)

Oncode Institute, Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center, Uppsalalaan 8, Utrecht, 3584 CT, the Netherlands; The Princess Maxima Center for Pediatric Oncology, 3584 CS Utrecht, the Netherlands.

Jeff DeMartino (J)

The Princess Maxima Center for Pediatric Oncology, 3584 CS Utrecht, the Netherlands.

Xuan Zheng (X)

AMOLF, Amsterdam, the Netherlands.

Nadzeya Staliarova (N)

Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands; Netherlands Proteomics Centre, Padualaan 8, 3584 CH Utrecht, the Netherlands.

Talya Dayton (T)

Oncode Institute, Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center, Uppsalalaan 8, Utrecht, 3584 CT, the Netherlands.

Harry Begthel (H)

Oncode Institute, Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center, Uppsalalaan 8, Utrecht, 3584 CT, the Netherlands.

Willine J van de Wetering (WJ)

The Maastricht Multimodal Molecular Imaging Institute, Maastricht University, 6229 ER Maastricht, the Netherlands.

Eduard Bodewes (E)

The Princess Maxima Center for Pediatric Oncology, 3584 CS Utrecht, the Netherlands.

Jeroen van Zon (J)

AMOLF, Amsterdam, the Netherlands.

Sander Tans (S)

AMOLF, Amsterdam, the Netherlands.

Carmen Lopez-Iglesias (C)

The Maastricht Multimodal Molecular Imaging Institute, Maastricht University, 6229 ER Maastricht, the Netherlands.

Peter J Peters (PJ)

The Maastricht Multimodal Molecular Imaging Institute, Maastricht University, 6229 ER Maastricht, the Netherlands.

Wei Wu (W)

Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands; Netherlands Proteomics Centre, Padualaan 8, 3584 CH Utrecht, the Netherlands; Singapore Immunology Network (SIgN), ASTAR (Agency for Science, Technology and Research), Singapore.

Daniel Kotlarz (D)

Department of Pediatrics, Dr. von Hauner Children's Hospital, University Hospital, Ludwig Maximilian University Munich, Munich, Germany.

Christoph Klein (C)

Department of Pediatrics, Dr. von Hauner Children's Hospital, University Hospital, Ludwig Maximilian University Munich, Munich, Germany.

Thanasis Margaritis (T)

The Princess Maxima Center for Pediatric Oncology, 3584 CS Utrecht, the Netherlands.

Frank Holstege (F)

The Princess Maxima Center for Pediatric Oncology, 3584 CS Utrecht, the Netherlands.

Hans Clevers (H)

Oncode Institute, Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences and University Medical Center, Uppsalalaan 8, Utrecht, 3584 CT, the Netherlands; The Princess Maxima Center for Pediatric Oncology, 3584 CS Utrecht, the Netherlands. Electronic address: h.clevers@hubrecht.eu.

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Classifications MeSH