XB-ART-49645
Stem Cells
2015 Mar 01;333:674-85. doi: 10.1002/stem.1877.
Show Gene links
Show Anatomy links
Neural crest specification by inhibition of the ROCK/Myosin II pathway.
Kim K
,
Ossipova O
,
Sokol SY
.
???displayArticle.abstract???
Neural crest is a population of multipotent progenitor cells that form at the border of neural and non-neural ectoderm in vertebrate embryos, and undergo epithelial-mesenchymal transition and migration. According to the traditional view, the neural crest is specified in early embryos by signaling molecules including BMP, FGF, and Wnt proteins. Here, we identify a novel signaling pathway leading to neural crest specification, which involves Rho-associated kinase (ROCK) and its downstream target nonmuscle Myosin II. We show that ROCK inhibitors promote differentiation of human embryonic stem cells (hESCs) into neural crest-like progenitors (NCPs) that are characterized by specific molecular markers and ability to differentiate into multiple cell types, including neurons, chondrocytes, osteocytes, and smooth muscle cells. Moreover, inhibition of Myosin II was sufficient for generating NCPs at high efficiency. Whereas Myosin II has been previously implicated in the self-renewal and survival of hESCs, we demonstrate its role in neural crest development during ESC differentiation. Inhibition of this pathway in Xenopus embryos expanded neural crest in vivo, further indicating that neural crest specification is controlled by ROCK-dependent Myosin II activity. We propose that changes in cell morphology in response to ROCK and Myosin II inhibition initiate mechanical signaling leading to neural crest fates.
???displayArticle.pubmedLink??? 25346532
???displayArticle.pmcLink??? PMC4428345
???displayArticle.link??? Stem Cells
???displayArticle.grants??? [+]
Species referenced: Xenopus laevis
Genes referenced: rho rho.2
References [+] :
Acloque,
Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease.
2009, Pubmed
Acloque, Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. 2009, Pubmed
Aragona, A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. 2013, Pubmed
Bajpai, CHD7 cooperates with PBAF to control multipotent neural crest formation. 2010, Pubmed , Xenbase
Barberi, Derivation of multipotent mesenchymal precursors from human embryonic stem cells. 2005, Pubmed
Berndt, Rho-kinase and myosin II affect dynamic neural crest cell behaviors during epithelial to mesenchymal transition in vivo. 2008, Pubmed
Betters, Analysis of early human neural crest development. 2010, Pubmed
Blauwkamp, Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. 2012, Pubmed
Broders-Bondon, Regulation of XSnail2 expression by Rho GTPases. 2007, Pubmed , Xenbase
Bronner-Fraser, Cell lineage analysis reveals multipotency of some avian neural crest cells. 1988, Pubmed
Brunet, Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria. 2013, Pubmed
Chambers, Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. 2009, Pubmed
Chang, Rho kinases regulate the renewal and neural differentiation of embryonic stem cells in a cell plating density-dependent manner. 2010, Pubmed
Chen, Molecular basis of pluripotency. 2008, Pubmed
Chen, Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells. 2010, Pubmed
Cheung, Neural crest development is regulated by the transcription factor Sox9. 2003, Pubmed
Cimadamore, Human ESC-derived neural crest model reveals a key role for SOX2 in sensory neurogenesis. 2011, Pubmed
Clark, Myosin II and mechanotransduction: a balancing act. 2007, Pubmed
Crane, Neural crest stem and progenitor cells. 2006, Pubmed
Curchoe, Early acquisition of neural crest competence during hESCs neuralization. 2010, Pubmed
de Crozé, Reiterative AP2a activity controls sequential steps in the neural crest gene regulatory network. 2011, Pubmed , Xenbase
Dupont, Role of YAP/TAZ in mechanotransduction. 2011, Pubmed
Engler, Matrix elasticity directs stem cell lineage specification. 2006, Pubmed
Enver, Stem cell states, fates, and the rules of attraction. 2009, Pubmed
Eyckmans, A hitchhiker's guide to mechanobiology. 2011, Pubmed
Farge, Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium. 2003, Pubmed
Gee, Yes-associated protein 65 (YAP) expands neural progenitors and regulates Pax3 expression in the neural plate border zone. 2011, Pubmed , Xenbase
Groysman, A negative modulatory role for rho and rho-associated kinase signaling in delamination of neural crest cells. 2008, Pubmed
Guémar, The small GTPase RhoV is an essential regulator of neural crest induction in Xenopus. 2007, Pubmed , Xenbase
Harb, The Rho-Rock-Myosin signaling axis determines cell-cell integrity of self-renewing pluripotent stem cells. 2008, Pubmed
Harland, In situ hybridization: an improved whole-mount method for Xenopus embryos. 1991, Pubmed , Xenbase
Hopwood, MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. 1989, Pubmed , Xenbase
Hotta, Small-molecule induction of neural crest-like cells derived from human neural progenitors. 2009, Pubmed
Huang, Induction of the neural crest and the opportunities of life on the edge. 2004, Pubmed , Xenbase
Itoh, GEF-H1 functions in apical constriction and cell intercalations and is essential for vertebrate neural tube closure. 2014, Pubmed , Xenbase
Itoh, Axis determination in Xenopus involves biochemical interactions of axin, glycogen synthase kinase 3 and beta-catenin. 1998, Pubmed , Xenbase
Jaffe, Rho GTPases: biochemistry and biology. 2005, Pubmed
Jiang, Isolation and characterization of neural crest stem cells derived from in vitro-differentiated human embryonic stem cells. 2009, Pubmed
Joo, ROCK suppression promotes differentiation and expansion of endothelial cells from embryonic stem cell-derived Flk1(+) mesodermal precursor cells. 2012, Pubmed
Kim, Rab11 regulates planar polarity and migratory behavior of multiciliated cells in Xenopus embryonic epidermis. 2012, Pubmed , Xenbase
Kreitzer, A robust method to derive functional neural crest cells from human pluripotent stem cells. 2013, Pubmed
Kuriyama, Molecular analysis of neural crest migration. 2008, Pubmed , Xenbase
Kurosawa, Application of Rho-associated protein kinase (ROCK) inhibitor to human pluripotent stem cells. 2012, Pubmed
Langer, Ajuba LIM proteins are snail/slug corepressors required for neural crest development in Xenopus. 2008, Pubmed , Xenbase
Le Douarin, Multipotentiality of the neural crest. 2003, Pubmed
Lee, Derivation of neural crest cells from human pluripotent stem cells. 2010, Pubmed
Lee, Actomyosin contractility and microtubules drive apical constriction in Xenopus bottle cells. 2007, Pubmed , Xenbase
Lee, Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. 2007, Pubmed
Levayer, Biomechanical regulation of contractility: spatial control and dynamics. 2012, Pubmed
Li, Integrated biochemical and mechanical signals regulate multifaceted human embryonic stem cell functions. 2010, Pubmed
Li, Nuclear myosin II regulates the assembly of preinitiation complex for ICAM-1 gene transcription. 2009, Pubmed
Lo, Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities. 1995, Pubmed
Ludwig, Derivation of human embryonic stem cells in defined conditions. 2006, Pubmed
Marchant, The inductive properties of mesoderm suggest that the neural crest cells are specified by a BMP gradient. 1998, Pubmed , Xenbase
Marlow, Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. 2002, Pubmed , Xenbase
McBeath, Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. 2004, Pubmed
Menendez, Wnt signaling and a Smad pathway blockade direct the differentiation of human pluripotent stem cells to multipotent neural crest cells. 2011, Pubmed
Menke, Regulation of adherens junctions by Rho GTPases and p120-catenin. 2012, Pubmed
Mica, Modeling neural crest induction, melanocyte specification, and disease-related pigmentation defects in hESCs and patient-specific iPSCs. 2013, Pubmed
Milet, Embryonic stem cell strategies to explore neural crest development in human embryos. 2012, Pubmed
Mizuseki, Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. 1998, Pubmed , Xenbase
Monsoro-Burq, Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. 2003, Pubmed , Xenbase
Newport, A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. 1982, Pubmed , Xenbase
Nieto, Control of cell behavior during vertebrate development by Slug, a zinc finger gene. 1994, Pubmed
Nieuwkoop, The "organization centre". 3. Segregation and pattern formation in morphogenetic fields. 1967, Pubmed
Noisa, Notch signaling regulates the differentiation of neural crest from human pluripotent stem cells. 2014, Pubmed
O'Donnell, Functional analysis of Sox8 during neural crest development in Xenopus. 2006, Pubmed , Xenbase
Ohgushi, Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. 2010, Pubmed
Ohgushi, Lonely death dance of human pluripotent stem cells: ROCKing between metastable cell states. 2011, Pubmed
Olson, Linking actin dynamics and gene transcription to drive cellular motile functions. 2010, Pubmed
Ossipova, Neural crest specification by noncanonical Wnt signaling and PAR-1. 2011, Pubmed , Xenbase
Pevny, SOX genes and neural progenitor identity. 2005, Pubmed
Phillips, Neural crest cell survival is dependent on Rho kinase and is required for development of the mid face in mouse embryos. 2012, Pubmed
Prasad, Induction of the neural crest state: control of stem cell attributes by gene regulatory, post-transcriptional and epigenetic interactions. 2012, Pubmed , Xenbase
Rauskolb, Cytoskeletal tension inhibits Hippo signaling through an Ajuba-Warts complex. 2014, Pubmed
Riento, Rocks: multifunctional kinases in cell behaviour. 2003, Pubmed
Sasai, Requirement of FoxD3-class signaling for neural crest determination in Xenopus. 2001, Pubmed , Xenbase
Sauka-Spengler, A gene regulatory network orchestrates neural crest formation. 2008, Pubmed
Selleck, Origins of the avian neural crest: the role of neural plate-epidermal interactions. 1995, Pubmed
Singh, Cell-cycle control of developmentally regulated transcription factors accounts for heterogeneity in human pluripotent cells. 2013, Pubmed
Skoglund, Convergence and extension at gastrulation require a myosin IIB-dependent cortical actin network. 2008, Pubmed , Xenbase
Sordella, Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. 2003, Pubmed
Straight, Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. 2003, Pubmed
Street, Rho kinase proteins--pleiotropic modulators of cell survival and apoptosis. 2011, Pubmed
Sun, Forcing stem cells to behave: a biophysical perspective of the cellular microenvironment. 2012, Pubmed
Sun, Hippo/YAP-mediated rigidity-dependent motor neuron differentiation of human pluripotent stem cells. 2014, Pubmed
Taneyhill, To adhere or not to adhere: the role of Cadherins in neural crest development. 2008, Pubmed
Thiery, Epithelial-mesenchymal transitions in development and disease. 2009, Pubmed
Vicente-Manzanares, Non-muscle myosin II takes centre stage in cell adhesion and migration. 2009, Pubmed
Walker, Non-muscle myosin II regulates survival threshold of pluripotent stem cells. 2010, Pubmed
Watanabe, A ROCK inhibitor permits survival of dissociated human embryonic stem cells. 2007, Pubmed
Wozniak, Mechanotransduction in development: a growing role for contractility. 2009, Pubmed
Wu, The tight junction scaffolding protein cingulin regulates neural crest cell migration. 2011, Pubmed
Yim, Force-dependent cell signaling in stem cell differentiation. 2012, Pubmed
Zhang, Pax6 is a human neuroectoderm cell fate determinant. 2010, Pubmed