Disruption of the crypt niche promotes outgrowth of mutated colorectal tumor stem cells.


Journal

JCI insight
ISSN: 2379-3708
Titre abrégé: JCI Insight
Pays: United States
ID NLM: 101676073

Informations de publication

Date de publication:
08 03 2022
Historique:
received: 09 08 2021
accepted: 26 01 2022
entrez: 9 3 2022
pubmed: 10 3 2022
medline: 12 4 2022
Statut: epublish

Résumé

Recent data establish a logarithmic expansion of leucine rich repeat containing G protein coupled receptor 5-positive (Lgr5+) colonic epithelial stem cells (CESCs) in human colorectal cancer (CRC). Complementary studies using the murine 2-stage azoxymethane-dextran sulfate sodium (AOM-DSS) colitis-associated tumor model indicate early acquisition of Wnt pathway mutations drives CESC expansion during adenoma progression. Here, subdivision of the AOM-DSS model into in vivo and in vitro stages revealed DSS induced physical separation of CESCs from stem cell niche cells and basal lamina, a source of Wnt signals, within hours, disabling the stem cell program. While AOM delivery in vivo under non-adenoma-forming conditions yielded phenotypically normal mucosa and organoids derived thereof, niche injury ex vivo by progressive DSS dose escalation facilitated outgrowth of Wnt-independent dysplastic organoids. These organoids contained 10-fold increased Lgr5+ CESCs with gain-of-function Wnt mutations orthologous to human CRC driver mutations. We posit CRC originates by niche injury-induced outgrowth of normally suppressed mutated stem cells, consistent with models of adaptive oncogenesis.

Identifiants

pubmed: 35260534
pii: 153793
doi: 10.1172/jci.insight.153793
pmc: PMC8983138
doi:
pii:

Substances chimiques

Azoxymethane MO0N1J0SEN

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States

Références

Nat Rev Genet. 2016 May;17(5):284-99
pubmed: 26972587
Proc Natl Acad Sci U S A. 2016 Sep 13;113(37):E5399-407
pubmed: 27573849
Gastroenterology. 2011 Nov;141(5):1762-72
pubmed: 21889923
Am J Physiol Gastrointest Liver Physiol. 2004 Jul;287(1):G7-17
pubmed: 15194558
Genes Chromosomes Cancer. 2005 Mar;42(3):238-46
pubmed: 15609344
Virchows Arch A Pathol Anat Histopathol. 1988;413(6):499-504
pubmed: 3144085
Nature. 2013 Feb 14;494(7436):247-50
pubmed: 23354049
Nat Rev Mol Cell Biol. 2008 Aug;9(8):628-38
pubmed: 18628784
Cell. 1996 Oct 18;87(2):159-70
pubmed: 8861899
Cell. 2004 Aug 6;118(3):285-96
pubmed: 15294155
Int J Radiat Biol. 2003 Feb;79(2):71-81
pubmed: 12569011
Nature. 2011 Jun 15;474(7351):318-26
pubmed: 21677748
Cancer Sci. 2004 Jun;95(6):475-80
pubmed: 15182426
Nat Cell Biol. 2017 Jul;19(7):774-786
pubmed: 28581476
J Radiat Res. 2013 Nov 1;54(6):1161-3
pubmed: 23732771
Nature. 2009 May 14;459(7244):262-5
pubmed: 19329995
Nature. 2018 Jun;558(7710):449-453
pubmed: 29875413
Gastroenterology. 2016 Apr;150(4):808-10
pubmed: 26924087
Cancer Cell. 2009 Feb 3;15(2):91-102
pubmed: 19185844
Sci Rep. 2015 Dec 17;5:18521
pubmed: 26673743
Clin Cancer Res. 2004 Feb 15;10(4):1401-8
pubmed: 14977843
Nature. 2009 Jan 29;457(7229):608-11
pubmed: 19092804
Nat Immunol. 2017 Jul 19;18(8):843-850
pubmed: 28722707
J Carcinog. 2011 Mar 24;10:9
pubmed: 21483655
Cell. 2002 Oct 18;111(2):241-50
pubmed: 12408868
Pathology. 2018 Jan;50(1):49-59
pubmed: 29169633
Proc Natl Acad Sci U S A. 2010 Dec 14;107(50):21635-40
pubmed: 21118981
Proc Natl Acad Sci U S A. 2010 Jan 26;107(4):1565-70
pubmed: 20080688
Nat Genet. 2015 Jun;47(6):668-71
pubmed: 25938944
Gastroenterology. 2012 Nov;143(5):1266-1276
pubmed: 22841781
Carcinogenesis. 2000 Nov;21(11):1935-40
pubmed: 11062151
Carcinogenesis. 2014 Apr;35(4):849-58
pubmed: 24282287
Cancer Res. 2020 Mar 1;80(5):927-928
pubmed: 32122905
Genesis. 2007 Sep;45(9):593-605
pubmed: 17868096
Cancer Cell. 2009 Feb 3;15(2):103-13
pubmed: 19185845
J Clin Invest. 2005 Jul;115(7):1765-76
pubmed: 15965503
Nat Commun. 2013;4:2610
pubmed: 24162018
Radiat Res. 1960 Oct;13:556-93
pubmed: 13726391
Gastroenterology. 2011 May;140(6):1807-16
pubmed: 21530747
Gut. 2017 Apr;66(4):683-691
pubmed: 26818619
Med Pharm Rep. 2019 Jul;92(3):246-252
pubmed: 31460505
Curr Protoc Stem Cell Biol. 2010 May;Chapter 5:Unit5A.4
pubmed: 20443207
PLoS One. 2013 May 14;8(5):e63298
pubmed: 23691015
Acta Pharmacol Sin. 2007 Sep;28(9):1450-9
pubmed: 17723178
J Biol Chem. 2017 May 26;292(21):8569-8576
pubmed: 28389557
Science. 2012 Aug 10;337(6095):730-5
pubmed: 22855427
Gastroenterology. 2012 May;142(5):1195-1205.e6
pubmed: 22333952
Int J Oncol. 2003 Jan;22(1):145-50
pubmed: 12469197
World J Gastroenterol. 2008 Jun 28;14(24):3866-71
pubmed: 18609711
J Surg Res. 2007 Jun 1;140(1):12-9
pubmed: 17418867
Blood. 2018 Sep 20;132(12):1265-1278
pubmed: 30064973
Drug Discov Today. 2015 Dec;20(12):1422-8
pubmed: 26320725
Cell. 2012 Jun 8;149(6):1192-205
pubmed: 22682243
Genome Res. 2015 May;25(5):714-24
pubmed: 25858951
Cell Signal. 2018 Jan;42:97-105
pubmed: 28958617
Cancer Res. 2020 Mar 1;80(5):1219-1227
pubmed: 31690670
Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10779-84
pubmed: 8855257
Proc Natl Acad Sci U S A. 2013 Jul 2;110(27):11127-32
pubmed: 23776211
Cell Stem Cell. 2017 Feb 2;20(2):177-190.e4
pubmed: 27939219
Biostatistics. 2004 Oct;5(4):557-72
pubmed: 15475419
Nat Rev Immunol. 2009 Nov;9(11):799-809
pubmed: 19855405
Nature. 2007 Oct 25;449(7165):1003-7
pubmed: 17934449
Nature. 2011 Jan 20;469(7330):415-8
pubmed: 21113151
Gut. 2019 Mar;68(3):547-561
pubmed: 30297438
Nat Rev Cancer. 2013 Nov;13(11):759-71
pubmed: 24154716
Science. 2013 Jun 7;340(6137):1190-4
pubmed: 23744940
Gastroenterology. 2012 Dec;143(6):1518-1529.e7
pubmed: 22922422
Carcinogenesis. 2000 Jun;21(6):1117-20
pubmed: 10836998
Nature. 2012 Jul 18;487(7407):330-7
pubmed: 22810696
J Biomed Biotechnol. 2012;2012:718617
pubmed: 22665990
Cancer Sci. 2003 Nov;94(11):965-73
pubmed: 14611673
Elife. 2019 Apr 29;8:
pubmed: 31034356
Biochim Biophys Acta. 2013 Aug;1836(1):80-9
pubmed: 23333833
Semin Immunopathol. 2013 Mar;35(2):229-44
pubmed: 23161445
Methods Mol Biol. 2015;1267:125-44
pubmed: 25636467
Trends Cancer. 2016 Oct;2(10):552-560
pubmed: 28439564
Cancer Res. 1978 Dec;38(12):4427-30
pubmed: 719628
Gastroenterology. 2007 Feb;132(2):628-32
pubmed: 17320548
Nat Med. 2012 Mar 11;18(4):618-23
pubmed: 22406745
Inflamm Bowel Dis. 2015 Feb;21(2):409-18
pubmed: 25563695
Crit Rev Toxicol. 2002 Sep;32(5):413-44
pubmed: 12389870
World J Gastroenterol. 2017 Sep 7;23(33):6016-6029
pubmed: 28970718
Gastroenterology. 2016 Apr;150(4):931-43
pubmed: 26764183
Gastroenterology. 2007 Dec;133(6):1869-81
pubmed: 18054559
Cancer Lett. 2004 Apr 8;206(2):193-9
pubmed: 15013524
BMC Cancer. 2016 Jan 12;16:12
pubmed: 26758198
Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8683-8
pubmed: 12072559
Cell. 2017 Jun 1;169(6):985-999
pubmed: 28575679
J Mol Diagn. 2015 May;17(3):251-64
pubmed: 25801821

Auteurs

Stefan Klingler (S)

Laboratory of Signal Transduction, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Kuo-Shun Hsu (KS)

Laboratory of Signal Transduction, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Guoqiang Hua (G)

Institute of Radiation Medicine, Fudan University, Shanghai, China.

Maria Laura Martin (ML)

Laboratory of Signal Transduction, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Mohammad Adileh (M)

Laboratory of Signal Transduction, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

Timour Baslan (T)

Cancer Biology and Genetics Program.

Zhigang Zhang (Z)

Department of Surgery.

Philip B Paty (PB)

Department of Surgery.

Zvi Fuks (Z)

Department of Radiation Oncology, and.

Anthony Mc Brown (AM)

Department of Cell & Developmental Biology, Weill Cornell Medicine, New York, New York, USA.

Richard Kolesnick (R)

Laboratory of Signal Transduction, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, New York, USA.

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