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Proc Natl Acad Sci U S A
2014 May 20;11120:7337-42.
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Smad1 transcription factor integrates BMP2 and Wnt3a signals in migrating cardiac progenitor cells.
Song J
,
McColl J
,
Camp E
,
Kennerley N
,
Mok GF
,
McCormick D
,
Grocott T
,
Wheeler GN
,
Münsterberg AE
.
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In vertebrate embryos, cardiac progenitor cells (CPCs) undergo long-range migration after emerging from the primitive streak during gastrulation. Together with other mesoderm progenitors, they migrate laterally and then toward the ventral midline, where they form the heart. Signals controlling the migration of different progenitor cell populations during gastrulation are poorly understood. Several pathways are involved in the epithelial-to-mesenchymal transition and ingression of mesoderm cells through the primitive streak, including fibroblast growth factors and wingless-type family members (Wnt). Here we focus on early CPC migration and use live video microscopy in chicken embryos to demonstrate a role for bone morphogenetic protein (BMP)/SMA and MAD related (Smad) signaling. We identify an interaction of BMP and Wnt/glycogen synthase kinase 3 beta (GSK3β) pathways via the differential phosphorylation of Smad1. Increased BMP2 activity altered migration trajectories of prospective cardiac cells and resulted in their lateral displacement and ectopic differentiation, as they failed to reach the ventral midline. Constitutively active BMP receptors or constitutively active Smad1 mimicked this phenotype, suggesting a cell autonomous response. Expression of GSK3β, which promotes the turnover of active Smad1, rescued the BMP-induced migration phenotype. Conversely, expression of GSK3β-resistant Smad1 resulted in aberrant CPC migration trajectories. De-repression of GSK3β by dominant negative Wnt3a restored normal migration patterns in the presence of high BMP activity. The data indicate the convergence of BMP and Wnt pathways on Smad1 during the early migration of prospective cardiac cells. Overall, we reveal molecular mechanisms that contribute to the emerging paradigm of signaling pathway integration in embryo development.
Alarcón,
Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways.
2009, Pubmed
Alarcón,
Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways.
2009,
Pubmed
Alsan,
Regulation of avian cardiogenesis by Fgf8 signaling.
2002,
Pubmed
,
Xenbase
Andrée,
BMP-2 induces ectopic expression of cardiac lineage markers and interferes with somite formation in chicken embryos.
1998,
Pubmed
Augsburger,
BMPs as mediators of roof plate repulsion of commissural neurons.
1999,
Pubmed
Baeg,
The Wingless morphogen gradient is established by the cooperative action of Frizzled and Heparan Sulfate Proteoglycan receptors.
2004,
Pubmed
Bartscherer,
Regulation of Wnt protein secretion and its role in gradient formation.
2008,
Pubmed
Camp,
Fate mapping identifies the origin of SHF/AHF progenitors in the chick primitive streak.
2012,
Pubmed
Camp,
Ingression, migration and early differentiation of cardiac progenitors.
2011,
Pubmed
Chapman,
Improved method for chick whole-embryo culture using a filter paper carrier.
2001,
Pubmed
Cohen,
Wnt signaling: an essential regulator of cardiovascular differentiation, morphogenesis and progenitor self-renewal.
2008,
Pubmed
Cui,
Dynamic positional fate map of the primary heart-forming region.
2009,
Pubmed
Cunningham,
Osteogenin and recombinant bone morphogenetic protein 2B are chemotactic for human monocytes and stimulate transforming growth factor beta 1 mRNA expression.
1992,
Pubmed
Foletta,
Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1.
2003,
Pubmed
Fuentealba,
Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal.
2007,
Pubmed
,
Xenbase
Gamell,
BMP2 induction of actin cytoskeleton reorganization and cell migration requires PI3-kinase and Cdc42 activity.
2008,
Pubmed
Gao,
Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2.
2011,
Pubmed
Garcia-Martinez,
Primitive-streak origin of the cardiovascular system in avian embryos.
1993,
Pubmed
Hamburger,
A series of normal stages in the development of the chick embryo. 1951.
1992,
Pubmed
Klaus,
Distinct roles of Wnt/beta-catenin and Bmp signaling during early cardiogenesis.
2007,
Pubmed
Kretzschmar,
Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1.
1997,
Pubmed
Lai,
Osteoblasts-derived BMP-2 enhances the motility of prostate cancer cells via activation of integrins.
2008,
Pubmed
Lee,
SMAD-mediated modulation of YY1 activity regulates the BMP response and cardiac-specific expression of a GATA4/5/6-dependent chick Nkx2.5 enhancer.
2004,
Pubmed
Lee-Hoeflich,
Activation of LIMK1 by binding to the BMP receptor, BMPRII, regulates BMP-dependent dendritogenesis.
2004,
Pubmed
Lenhart,
Integration of nodal and BMP signals in the heart requires FoxH1 to create left-right differences in cell migration rates that direct cardiac asymmetry.
2013,
Pubmed
Lickert,
Formation of multiple hearts in mice following deletion of beta-catenin in the embryonic endoderm.
2002,
Pubmed
Marvin,
Inhibition of Wnt activity induces heart formation from posterior mesoderm.
2001,
Pubmed
,
Xenbase
Mulligan,
Secreted Wingless-interacting molecule (Swim) promotes long-range signaling by maintaining Wingless solubility.
2012,
Pubmed
Pandur,
Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis.
2002,
Pubmed
,
Xenbase
Redkar,
Fate map of early avian cardiac progenitor cells.
2001,
Pubmed
,
Xenbase
Ridley,
Cell migration: integrating signals from front to back.
2003,
Pubmed
Sapkota,
Balancing BMP signaling through integrated inputs into the Smad1 linker.
2007,
Pubmed
,
Xenbase
Schlange,
BMP2 is required for early heart development during a distinct time period.
2000,
Pubmed
Schneider,
Wnt antagonism initiates cardiogenesis in Xenopus laevis.
2001,
Pubmed
,
Xenbase
Schultheiss,
A role for bone morphogenetic proteins in the induction of cardiac myogenesis.
1997,
Pubmed
Shi,
Mechanisms of TGF-beta signaling from cell membrane to the nucleus.
2003,
Pubmed
Shieh,
Heart malformation: what are the chances it could happen again?
2009,
Pubmed
Sieber,
Recent advances in BMP receptor signaling.
2009,
Pubmed
Smith,
Bmp and nodal independently regulate lefty1 expression to maintain unilateral nodal activity during left-right axis specification in zebrafish.
2011,
Pubmed
Song,
Time-lapse imaging of chick cardiac precursor cells.
2011,
Pubmed
Steinfeld,
RPE specification in the chick is mediated by surface ectoderm-derived BMP and Wnt signalling.
2013,
Pubmed
Streit,
Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo.
1998,
Pubmed
Stuhlmiller,
FGF/MAPK signaling is required in the gastrula epiblast for avian neural crest induction.
2012,
Pubmed
Tzahor,
Wnt/beta-catenin signaling and cardiogenesis: timing does matter.
2007,
Pubmed
Veerkamp,
Unilateral dampening of Bmp activity by nodal generates cardiac left-right asymmetry.
2013,
Pubmed
Yang,
Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8.
2002,
Pubmed
Yue,
Wnt3a-mediated chemorepulsion controls movement patterns of cardiac progenitors and requires RhoA function.
2008,
Pubmed
Yutzey,
Diversification of cardiomyogenic cell lineages in vitro.
1995,
Pubmed
Zhu,
IGFBP-4 is an inhibitor of canonical Wnt signalling required for cardiogenesis.
2008,
Pubmed
,
Xenbase