Essential long-range action of Wingless/Wnt in adult intestinal compartmentalization.


Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
06 2019
Historique:
received: 12 07 2018
accepted: 26 03 2019
entrez: 14 6 2019
pubmed: 14 6 2019
medline: 7 11 2019
Statut: epublish

Résumé

Signal transduction activated by Wingless/Wnt ligands directs cell proliferation and fate specification in metazoans, and its overactivation underlies the development of the vast majority of colorectal cancers. In the conventional model, the secretion and movement of Wingless to cells distant from its source of synthesis are essential for long-range signaling in tissue patterning. However, this model was upended recently by an unanticipated finding: replacement of wild-type Drosophila Wingless with a membrane-tethered form produced viable adults with largely normal external morphology, which suggested that Wingless secretion and movement are dispensable for tissue patterning. Herein, we tested this foundational principle in the adult intestine, where Wingless signaling gradients coincide with all major boundaries between compartments. We find that the critical roles of Wingless during adult intestinal development, which include regulation of target gene activation, boundary formation, stem cell proliferation, epithelial cell fate specification, muscle differentiation, gut folding, and signaling crosstalk with the Decapentaplegic pathway, are all disrupted by Wingless tethering. These findings provide new evidence that supports the requirement for the direct, long-range action of Wingless in tissue patterning, with relevance for animal development, tissue homeostasis and Wnt-driven disease.

Identifiants

pubmed: 31194729
doi: 10.1371/journal.pgen.1008111
pii: PGENETICS-D-18-01420
pmc: PMC6563961
doi:

Substances chimiques

Drosophila Proteins 0
Wnt1 Protein 0
dpp protein, Drosophila 0
wg protein, Drosophila 0

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1008111

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM122222
Pays : United States
Organisme : NIGMS NIH HHS
ID : P20 GM113132
Pays : United States
Organisme : NIH HHS
ID : P40 OD018537
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA023108
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM121421
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM084947
Pays : United States

Commentaires et corrections

Type : CommentIn

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Nature. 2013 Jun 27;498(7455):456-62
pubmed: 23783517
Cell Tissue Res. 2001 Oct;306(1):167-78
pubmed: 11683178
Gene Expr Patterns. 2007 Jan;7(3):323-31
pubmed: 17008134
Development. 2013 May;140(9):1903-11
pubmed: 23571215
Cell Rep. 2013 Jul 11;4(1):10-8
pubmed: 23810561
Proc Natl Acad Sci U S A. 2014 Jul 22;111(29):E2967-76
pubmed: 25002478
Trends Genet. 1994 Nov;10(11):383-5
pubmed: 7809941
Mech Dev. 2000 Mar 1;91(1-2):427-31
pubmed: 10704878
Dev Biol. 2004 Apr 15;268(2):481-92
pubmed: 15063183
Nature. 2016 Feb 18;530(7590):340-3
pubmed: 26863187
Science. 2008 Jan 18;319(5861):333-6
pubmed: 18202290
Cell. 2006 May 5;125(3):523-33
pubmed: 16678096
Gene Expr Patterns. 2011 Jan-Feb;11(1-2):12-21
pubmed: 20804858
J Cell Biol. 2013 Jun 10;201(6):945-61
pubmed: 23733344
Science. 2014 Feb 21;343(6173):1244624
pubmed: 24385607
Genes Dev. 1990 Aug;4(8):1322-31
pubmed: 1977661
Cell. 1996 Nov 29;87(5):833-44
pubmed: 8945511
Genes Dev. 2004 Dec 15;18(24):2985-97
pubmed: 15601817
Dev Biol. 2016 Aug 15;416(2):347-60
pubmed: 27321560
Dev Biol. 2018 Mar 15;435(2):97-108
pubmed: 29339095
Elife. 2018 Aug 10;7:
pubmed: 30095068
Nat Commun. 2018 Jun 12;9(1):2295
pubmed: 29895891
Nature. 2014 Jan 9;505(7482):162-3
pubmed: 24390347
J Cell Sci. 2016 Feb 15;129(4):665-72
pubmed: 26823607
Nature. 2008 Oct 23;455(7216):1119-23
pubmed: 18806781
EMBO J. 1995 Oct 16;14(20):5016-26
pubmed: 7588630
Dev Dyn. 2012 Jan;241(1):85-91
pubmed: 21972080
J Cell Biol. 1999 Sep 20;146(6):1303-18
pubmed: 10491393
Development. 2006 Dec;133(24):4901-11
pubmed: 17108000
Elife. 2014 Mar 11;3:e01857
pubmed: 24618900
Nature. 2014 Jan 9;505(7482):180-5
pubmed: 24390349
Elife. 2018 Aug 15;7:
pubmed: 30106379
J Cell Biol. 1986 Oct;103(4):1517-25
pubmed: 3095337
Cell. 1998 Jun 26;93(7):1171-82
pubmed: 9657150
Annu Rev Cell Dev Biol. 2011;27:377-407
pubmed: 21801015
Dev Cell. 2002 May;2(5):667-76
pubmed: 12015973
Philos Trans R Soc Lond B Biol Sci. 2015 Apr 19;370(1666):
pubmed: 25750229
Science. 2014 Oct 3;346(6205):1248012
pubmed: 25278615
Growth Factors. 2013 Feb;31(1):1-31
pubmed: 23256519
Development. 1998 Apr;125(8):1421-32
pubmed: 9502723
Dev Cell. 2016 Mar 7;36(5):485-6
pubmed: 26954543
Development. 2016 Jul 15;143(14):2482-93
pubmed: 27436038
Cell Cycle. 2011 Apr 1;10(7):1109-20
pubmed: 21403464
Cell Stem Cell. 2013 Oct 3;13(4):375-6
pubmed: 24094316
Nat Cell Biol. 2016 Apr;18(4):451-7
pubmed: 26974662
Development. 1997 Feb;124(4):871-80
pubmed: 9043068
EMBO Rep. 2011 Sep 30;12(10):1047-54
pubmed: 21869817
Bioessays. 1997 Aug;19(8):721-9
pubmed: 9264255
Development. 1995 Aug;121(8):2265-78
pubmed: 7671794
Cell. 2006 May 5;125(3):509-22
pubmed: 16678095
Cell Rep. 2013 May 30;3(5):1725-38
pubmed: 23643535
EMBO J. 1987 Jun;6(6):1765-73
pubmed: 16453776
J Cell Biol. 1987 Nov;105(5):2095-102
pubmed: 3680372
Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15050-5
pubmed: 11742088
Development. 2017 Nov 15;144(22):4091-4102
pubmed: 28947534
Elife. 2013 Aug 27;2:e00886
pubmed: 23991285
Nature. 2015 Mar 12;519(7542):187-192
pubmed: 25731175
Development. 2016 May 15;143(10):1710-20
pubmed: 27190037
Neuron. 2001 Nov 8;32(3):415-24
pubmed: 11709153
Nat Commun. 2015 Jan 05;6:5846
pubmed: 25556612
Elife. 2015 May 07;4:e06114
pubmed: 25951303
Nat Cell Biol. 1999 Jul;1(3):144-51
pubmed: 10559900
Nature. 1996 May 30;381(6581):387-93
pubmed: 8632795
Development. 1996 May;122(5):1555-65
pubmed: 8625842
Development. 1999 Oct;126(20):4421-30
pubmed: 10498678
Cell. 1997 Mar 21;88(6):789-99
pubmed: 9118222
Cell. 2009 Oct 16;139(2):393-404
pubmed: 19837038
Trends Neurosci. 2001 May;24(5):251-4
pubmed: 11311363
Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):242-7
pubmed: 8990193
J Cell Biol. 1989 Nov;109(5):2157-67
pubmed: 2509482
Genes Dev. 2002 May 1;16(9):1055-9
pubmed: 12000788
Development. 2012 Dec;139(24):4524-35
pubmed: 23172913
J Dev Biol. 2018 Mar 28;6(2):
pubmed: 29615557
Proc Natl Acad Sci U S A. 2011 Oct 25;108(43):17696-701
pubmed: 21984734
Development. 2010 Mar;137(6):845-57
pubmed: 20179091
Nature. 2006 Jan 26;439(7075):470-4
pubmed: 16340960
Cell. 1996 May 3;85(3):357-68
pubmed: 8616891
Nature. 2008 Jul 31;454(7204):651-5
pubmed: 18633350
Curr Opin Cell Biol. 2015 Aug;35:69-77
pubmed: 26001269
Annu Rev Genet. 2013;47:377-404
pubmed: 24016187
Cell Stem Cell. 2009 Sep 4;5(3):290-7
pubmed: 19699165
PLoS Genet. 2016 Feb 04;12(2):e1005822
pubmed: 26845150
Mech Dev. 2001 Mar;101(1-2):79-90
pubmed: 11231061
Development. 1994 Jun;120(6):1661-70
pubmed: 8050372
Nature. 2006 Jan 26;439(7075):475-9
pubmed: 16340959
Dev Biol. 2016 Dec 1;420(1):43-59
pubmed: 27765651
Dev Dyn. 2010 Jan;239(1):16-33
pubmed: 19544585
Exp Cell Res. 2011 Nov 15;317(19):2711-8
pubmed: 21802415
Development. 1994 Oct;120(10):2957-66
pubmed: 7607085
Nature. 2000 Feb 17;403(6771):789-95
pubmed: 10693810
Development. 2007 Aug;134(16):3011-20
pubmed: 17634191
Curr Biol. 2001 Oct 30;11(21):R851-4
pubmed: 11696339
Development. 1995 Dec;121(12):4215-25
pubmed: 8575321
Proc Natl Acad Sci U S A. 2011 Nov 15;108(46):18702-7
pubmed: 22049341
Cell. 1990 Nov 2;63(3):549-60
pubmed: 2225066
Cell. 1994 Aug 12;78(3):437-48
pubmed: 8062386
Dev Cell. 2015 Mar 23;32(6):719-30
pubmed: 25771893
Nat Cell Biol. 2012 Oct;14(10):1036-45
pubmed: 22983114
Development. 2013 Dec;140(23):4818-25
pubmed: 24154526
Trends Cell Biol. 2016 Oct;26(10):756-765
pubmed: 27325141
Cell. 1987 Mar 27;48(6):975-88
pubmed: 3548998
Cell. 1993 Feb 26;72(4):527-40
pubmed: 8440019
Cell. 2017 Jun 1;169(6):985-999
pubmed: 28575679
Nat Cell Biol. 2002 May;4(5):367-73
pubmed: 11988739
Elife. 2018 May 01;7:
pubmed: 29714689
Development. 2015 Apr 1;142(7):1203-11
pubmed: 25804733

Auteurs

Ai Tian (A)

Department of Molecular and Systems Biology and the Norris Cotton Cancer Center, Geisel School of Medicine at Dartmouth College, Hanover, NH, United States of America.

Deepesh Duwadi (D)

Department of Molecular and Systems Biology and the Norris Cotton Cancer Center, Geisel School of Medicine at Dartmouth College, Hanover, NH, United States of America.

Hassina Benchabane (H)

Department of Molecular and Systems Biology and the Norris Cotton Cancer Center, Geisel School of Medicine at Dartmouth College, Hanover, NH, United States of America.

Yashi Ahmed (Y)

Department of Molecular and Systems Biology and the Norris Cotton Cancer Center, Geisel School of Medicine at Dartmouth College, Hanover, NH, United States of America.

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