XB-ART-46881
Dev Biol
June 1, 2013;
378
(1):
1-12.
Different thresholds of Wnt-Frizzled 7 signaling coordinate proliferation, morphogenesis and fate of endoderm progenitor cells.
Abstract
Wnt signaling has multiple dynamic roles during development of the gastrointestinal and respiratory systems. Differential Wnt signaling is thought to be a critical step in Xenopus endoderm patterning such that during late gastrula and early somite stages of embryogenesis, Wnt activity must be suppressed in the anterior to allow the specification of foregut progenitors. However, the foregut endoderm also expresses the Wnt-receptor Frizzled 7 (Fzd7) as well as several Wnt ligands suggesting that the current model may be too simple. In this study, we show that Fzd7 is required to transduce a low level of Wnt signaling that is essential to maintain foregut progenitors. Foregut-specific Fzd7-depletion from the Xenopus foregut resulted in liver and pancreas agenesis. Fzd7-depleted embryos failed to maintain the foregut progenitor marker hhex and exhibited decreased proliferation; in addition the foregut cells were enlarged with a randomized orientation. We show that in the foregut Fzd7 signals via both the Wnt/β-catenin and Wnt/JNK pathways and that different thresholds of Wnt-Fzd7 activity coordinate progenitor cell fate, proliferation and morphogenesis.
PubMed ID: 23562607
PMC ID: PMC4263287
Article link: Dev Biol
Grant support: [+]
Species referenced: Xenopus
Genes referenced: a2m actl6a casp3.2 cat.2 cdc42 cdh1 cdh3 ctnnb1 dkk1 fos fzd7 gsk3b hhex jun mapk8 pcyt1a pdx1 rac1 sfrp5 tbx2 ventx1.2 ventx2.2 wnt11 wnt8a
Phenotypes: Xla Wt + BIO (fig.7.a) [+]
Xla Wt + BIO
(fig.7.b)
Xla Wt + Casin (fig.S7.e)
Xla Wt + Go 6976 (fig.S7.k)
Xla Wt + Mmu.lef1-Mmu.ctnnb1-GR + fzd7 MO + DEX (fig.6.k)
Xla Wt + NSC 23766 (fig.S7.j)
Xla Wt + SP600125 (fig.6.a)
Xla Wt + SP600125 (fig.6.h)
Xla Wt + SP600125 (fig.6.n)
Xla Wt + XAV939 (fig.S2.b)
Xla Wt + XAV939 (fig.S2.c)
Xla Wt + XAV939 (fig.S2.d)
Xla Wt + XAV939 (fig.S2.f)
Xla Wt + XAV939 (fig.S2.f)
Xla Wt + XAV939 (fig.S2.h)
Xla Wt + dkk1 (fig.6.a)
Xla Wt + dkk1 (fig.6.a)
Xla Wt + dkk1 (fig.6.m)
Xla Wt + fzd7 MO (fig.1.b-d)
Xla Wt + fzd7 MO (fig.1.b-d)
Xla Wt + fzd7 MO (fig.1.g-j)
Xla Wt + fzd7 MO (fig.2.f)
Xla Wt + fzd7 MO (fig.2.i)
Xla Wt + fzd7 MO (fig.2.o)
Xla Wt + fzd7 MO (fig.2.q)
Xla Wt + fzd7 MO (fig.2.s)
Xla Wt + fzd7 MO (fig.3.b,d,f,h,j)
Xla Wt + fzd7 MO (fig.3.b,d,f,h,j,m)
Xla Wt + fzd7 MO (fig.3.d)
Xla Wt + fzd7 MO (fig.3.l,l^1)
Xla Wt + fzd7 MO (fig.4.b,e)
Xla Wt + fzd7 MO (fig.4.d,e)
Xla Wt + fzd7 MO (fig.5.b)
Xla Wt + fzd7 MO (fig.5.c,e)
Xla Wt + fzd7 MO (fig.6.b)
Xla Wt + fzd7 MO (fig.6.d)
Xla Wt + fzd7 MO (fig.6.j)
Xla Wt + fzd7 MO (fig.7.e)
Xla Wt + fzd7 MO (fig.7.f)
Xla Wt + fzd7 MO (fig.7.g)
Xla Wt + fzd7 MO (fig.7.h)
Xla Wt + fzd7 MO (fig.S3.d)
Xla Wt + fzd7 MO (fig.S3.f)
Xla Wt + fzd7 MO (fig.S3.i)
Xla Wt + fzd7 MO (fig.S4.c,c^1,g)
Xla Wt + fzd7 MO (fig.S4.d,d^1,h)
Xla Wt + fzd7 MO (fig.S7.c)
Xla Wt + fzd7 MO (fig.S7.d)
Xla Wt + fzd7 MO + BIO (fig.7.k)
Xla Wt + fzd7 MO + BIO (fig.7.l)
Xla Wt + hydroxyurea (fig.S4.d,d^1,h)
Xla Wt + hydroxyurea (fig.S4.e,e^1,g)
Xla Wt + hydroxyurea (fig.S4.o)
Xla Wt + hydroxyurea (fig.S4.o,p)
Xla Wt + {ca}Hsa.MAPK8 + fzd7 MO + DEX (fig.6.e)
Xla Wt + Casin (fig.S7.e)
Xla Wt + Go 6976 (fig.S7.k)
Xla Wt + Mmu.lef1-Mmu.ctnnb1-GR + fzd7 MO + DEX (fig.6.k)
Xla Wt + NSC 23766 (fig.S7.j)
Xla Wt + SP600125 (fig.6.a)
Xla Wt + SP600125 (fig.6.h)
Xla Wt + SP600125 (fig.6.n)
Xla Wt + XAV939 (fig.S2.b)
Xla Wt + XAV939 (fig.S2.c)
Xla Wt + XAV939 (fig.S2.d)
Xla Wt + XAV939 (fig.S2.f)
Xla Wt + XAV939 (fig.S2.f)
Xla Wt + XAV939 (fig.S2.h)
Xla Wt + dkk1 (fig.6.a)
Xla Wt + dkk1 (fig.6.a)
Xla Wt + dkk1 (fig.6.m)
Xla Wt + fzd7 MO (fig.1.b-d)
Xla Wt + fzd7 MO (fig.1.b-d)
Xla Wt + fzd7 MO (fig.1.g-j)
Xla Wt + fzd7 MO (fig.2.f)
Xla Wt + fzd7 MO (fig.2.i)
Xla Wt + fzd7 MO (fig.2.o)
Xla Wt + fzd7 MO (fig.2.q)
Xla Wt + fzd7 MO (fig.2.s)
Xla Wt + fzd7 MO (fig.3.b,d,f,h,j)
Xla Wt + fzd7 MO (fig.3.b,d,f,h,j,m)
Xla Wt + fzd7 MO (fig.3.d)
Xla Wt + fzd7 MO (fig.3.l,l^1)
Xla Wt + fzd7 MO (fig.4.b,e)
Xla Wt + fzd7 MO (fig.4.d,e)
Xla Wt + fzd7 MO (fig.5.b)
Xla Wt + fzd7 MO (fig.5.c,e)
Xla Wt + fzd7 MO (fig.6.b)
Xla Wt + fzd7 MO (fig.6.d)
Xla Wt + fzd7 MO (fig.6.j)
Xla Wt + fzd7 MO (fig.7.e)
Xla Wt + fzd7 MO (fig.7.f)
Xla Wt + fzd7 MO (fig.7.g)
Xla Wt + fzd7 MO (fig.7.h)
Xla Wt + fzd7 MO (fig.S3.d)
Xla Wt + fzd7 MO (fig.S3.f)
Xla Wt + fzd7 MO (fig.S3.i)
Xla Wt + fzd7 MO (fig.S4.c,c^1,g)
Xla Wt + fzd7 MO (fig.S4.d,d^1,h)
Xla Wt + fzd7 MO (fig.S7.c)
Xla Wt + fzd7 MO (fig.S7.d)
Xla Wt + fzd7 MO + BIO (fig.7.k)
Xla Wt + fzd7 MO + BIO (fig.7.l)
Xla Wt + hydroxyurea (fig.S4.d,d^1,h)
Xla Wt + hydroxyurea (fig.S4.e,e^1,g)
Xla Wt + hydroxyurea (fig.S4.o)
Xla Wt + hydroxyurea (fig.S4.o,p)
Xla Wt + {ca}Hsa.MAPK8 + fzd7 MO + DEX (fig.6.e)
Article Images: [+] show captions
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Ulrich, Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. 2005, Pubmed
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Vaezi, Actin cable dynamics and Rho/Rock orchestrate a polarized cytoskeletal architecture in the early steps of assembling a stratified epithelium. 2002, Pubmed
Vasioukhin, Directed actin polymerization is the driving force for epithelial cell-cell adhesion. 2000, Pubmed
Verzi, Wnt signaling in gut organogenesis. 2009, Pubmed
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Wandzioch, Dynamic signaling network for the specification of embryonic pancreas and liver progenitors. 2009, Pubmed
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Winklbauer, Frizzled-7 signalling controls tissue separation during Xenopus gastrulation. 2001, Pubmed , Xenbase
Witzel, Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane. 2006, Pubmed
Zaret, Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation. 2008, Pubmed
Zorn, Molecular basis of vertebrate endoderm development. 2007, Pubmed , Xenbase
Zorn, Anterior endomesoderm specification in Xenopus by Wnt/beta-catenin and TGF-beta signalling pathways. 1999, Pubmed , Xenbase
Zorn, Vertebrate endoderm development and organ formation. 2009, Pubmed , Xenbase
Bovolenta, Frizzled/RYK mediated signalling in axon guidance. 2006, Pubmed
Brown, The maternal Xenopus beta-catenin signaling pathway, activated by frizzled homologs, induces goosecoid in a cell non-autonomous manner. 2000, Pubmed , Xenbase
Cha, Wnt5a and Wnt11 interact in a maternal Dkk1-regulated fashion to activate both canonical and non-canonical signaling in Xenopus axis formation. 2008, Pubmed , Xenbase
Cha, Wnt11/5a complex formation caused by tyrosine sulfation increases canonical signaling activity. 2009, Pubmed , Xenbase
Cheyette, Dapper, a Dishevelled-associated antagonist of beta-catenin and JNK signaling, is required for notochord formation. 2002, Pubmed , Xenbase
Chu, Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. 2004, Pubmed
Clevers, Wnt/beta-catenin signaling in development and disease. 2006, Pubmed
Djiane, Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. 2000, Pubmed , Xenbase
Domingos, The Wnt/beta-catenin pathway posteriorizes neural tissue in Xenopus by an indirect mechanism requiring FGF signalling. 2002, Pubmed , Xenbase
Goessling, APC mutant zebrafish uncover a changing temporal requirement for wnt signaling in liver development. 2008, Pubmed
Goss, Wnt2/2b and beta-catenin signaling are necessary and sufficient to specify lung progenitors in the foregut. 2009, Pubmed
Grumolato, Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. 2010, Pubmed
Huang, Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. 2009, Pubmed
Kim, JNK and ROKalpha function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements. 2005, Pubmed , Xenbase
Kim, Ryk cooperates with Frizzled 7 to promote Wnt11-mediated endocytosis and is essential for Xenopus laevis convergent extension movements. 2008, Pubmed , Xenbase
Kroon, Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. 2008, Pubmed
Lade, Beta-catenin signaling in hepatic development and progenitors: which way does the WNT blow? 2011, Pubmed , Xenbase
Lee, JNK regulates binding of alpha-catenin to adherens junctions and cell-cell adhesion. 2011, Pubmed
Li, Sfrp5 coordinates foregut specification and morphogenesis by antagonizing both canonical and noncanonical Wnt11 signaling. 2008, Pubmed , Xenbase
Liao, Jun NH2-terminal kinase (JNK) prevents nuclear beta-catenin accumulation and regulates axis formation in Xenopus embryos. 2006, Pubmed , Xenbase
MacDonald, Wnt/beta-catenin signaling: components, mechanisms, and diseases. 2009, Pubmed
McLin, Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. 2007, Pubmed , Xenbase
Medina, Interaction of Frizzled 7 and Dishevelled in Xenopus. 2000, Pubmed , Xenbase
Medina, Xenopus frizzled 7 can act in canonical and non-canonical Wnt signaling pathways: implications on early patterning and morphogenesis. 2000, Pubmed , Xenbase
Medina, Xenopus paraxial protocadherin has signaling functions and is involved in tissue separation. 2004, Pubmed , Xenbase
Mii, Secreted Frizzled-related proteins enhance the diffusion of Wnt ligands and expand their signalling range. 2009, Pubmed , Xenbase
Mii, Secreted Wnt "inhibitors" are not just inhibitors: regulation of extracellular Wnt by secreted Frizzled-related proteins. 2011, Pubmed
Mikels, Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. 2006, Pubmed
Moody, Fates of the blastomeres of the 32-cell-stage Xenopus embryo. 1987, Pubmed , Xenbase
Murtaugh, The what, where, when and how of Wnt/β-catenin signaling in pancreas development. 2011, Pubmed
Nagy, Wnt-11 signalling controls ventricular myocardium development by patterning N-cadherin and beta-catenin expression. 2009, Pubmed
Nemeth, Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. 2007, Pubmed
Ober, Mesodermal Wnt2b signalling positively regulates liver specification. 2006, Pubmed
Ohnuma, p27Xic1, a Cdk inhibitor, promotes the determination of glial cells in Xenopus retina. 1999, Pubmed , Xenbase
Poulain, Interplay between Wnt2 and Wnt2bb controls multiple steps of early foregut-derived organ development. 2011, Pubmed
Rankin, A gene regulatory network controlling hhex transcription in the anterior endoderm of the organizer. 2011, Pubmed , Xenbase
Reed, Morphogenesis of the primitive gut tube is generated by Rho/ROCK/myosin II-mediated endoderm rearrangements. 2009, Pubmed , Xenbase
Rozario, The physical state of fibronectin matrix differentially regulates morphogenetic movements in vivo. 2009, Pubmed , Xenbase
Sato, Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. 2004, Pubmed
Schambony, Wnt-5A/Ror2 regulate expression of XPAPC through an alternative noncanonical signaling pathway. 2007, Pubmed , Xenbase
Schier, Molecular genetics of axis formation in zebrafish. 2005, Pubmed
Schlessinger, Wnt signaling pathways meet Rho GTPases. 2009, Pubmed , Xenbase
Seifert, Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. 2007, Pubmed
Serls, Different thresholds of fibroblast growth factors pattern the ventral foregut into liver and lung. 2004, Pubmed
Shin, Restriction of hepatic competence by Fgf signaling. 2011, Pubmed
Si-Tayeb, Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. 2009, Pubmed
Sinner, Sox17 and beta-catenin cooperate to regulate the transcription of endodermal genes. 2004, Pubmed , Xenbase
Spence, Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. 2011, Pubmed , Xenbase
Sumanas, The putative wnt receptor Xenopus frizzled-7 functions upstream of beta-catenin in vertebrate dorsoventral mesoderm patterning. 2000, Pubmed , Xenbase
Sumanas, Xenopus frizzled-7 morphant displays defects in dorsoventral patterning and convergent extension movements during gastrulation. 2001, Pubmed , Xenbase
Tao, G-protein-coupled signals control cortical actin assembly by controlling cadherin expression in the early Xenopus embryo. 2007, Pubmed , Xenbase
Tao, Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. 2005, Pubmed , Xenbase
Topol, Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent beta-catenin degradation. 2003, Pubmed
Ulrich, Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. 2005, Pubmed
Usui, Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. 1999, Pubmed
Vaezi, Actin cable dynamics and Rho/Rock orchestrate a polarized cytoskeletal architecture in the early steps of assembling a stratified epithelium. 2002, Pubmed
Vasioukhin, Directed actin polymerization is the driving force for epithelial cell-cell adhesion. 2000, Pubmed
Verzi, Wnt signaling in gut organogenesis. 2009, Pubmed
Wallingford, The developmental biology of Dishevelled: an enigmatic protein governing cell fate and cell polarity. 2005, Pubmed
Wandzioch, Dynamic signaling network for the specification of embryonic pancreas and liver progenitors. 2009, Pubmed
Wheeler, Two novel Xenopus frizzled genes expressed in developing heart and brain. 1999, Pubmed , Xenbase
Winklbauer, Frizzled-7 signalling controls tissue separation during Xenopus gastrulation. 2001, Pubmed , Xenbase
Witzel, Wnt11 controls cell contact persistence by local accumulation of Frizzled 7 at the plasma membrane. 2006, Pubmed
Zaret, Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation. 2008, Pubmed
Zorn, Molecular basis of vertebrate endoderm development. 2007, Pubmed , Xenbase
Zorn, Anterior endomesoderm specification in Xenopus by Wnt/beta-catenin and TGF-beta signalling pathways. 1999, Pubmed , Xenbase
Zorn, Vertebrate endoderm development and organ formation. 2009, Pubmed , Xenbase