XB-ART-57941
Sci Rep
January 1, 2021;
11
(1):
6607.
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Furry is required for cell movements during gastrulation and functionally interacts with NDR1.
Cervino AS
,
Moretti B
,
Stuckenholz C
,
Grecco HE
,
Davidson LA
,
Cirio MC
.
Abstract
Gastrulation is a key event in animal embryogenesis during which germ layer precursors are rearranged and the embryonic axes are established. Cell polarization is essential during gastrulation, driving asymmetric cell division, cell movements, and cell shape changes. The furry (fry) gene encodes an evolutionarily conserved protein with a wide variety of cellular functions, including cell polarization and morphogenesis in invertebrates. However, little is known about its function in vertebrate development. Here, we show that in Xenopus, Fry plays a role in morphogenetic processes during gastrulation, in addition to its previously described function in the regulation of dorsal mesoderm gene expression. Using morpholino knock-down, we demonstrate a distinct role for Fry in blastopore closure and dorsal axis elongation. Loss of Fry function drastically affects the movement and morphological polarization of cells during gastrulation and disrupts dorsal mesoderm convergent extension, responsible for head-to-tail elongation. Finally, we evaluate a functional interaction between Fry and NDR1 kinase, providing evidence of an evolutionarily conserved complex required for morphogenesis.
PubMed ID: 33758327
PMC ID: PMC7987989
Article link: Sci Rep
Grant support: [+]
Doctoral Fellowship Program Consejo Nacional de Investigaciones Científicas y Técnicas, NICHD R01 HD044750 NIH HHS , 2013-1301,2014-3658 Fondo para la Investigación Científica y Tecnológica, 20020170100755BA Secretaría de Ciencia y Técnica, Universidad de Buenos Aires, PICT-2013-0381 Agencia Nacional de Promoción Científica y Tecnológica of Argentina, R01 HD044750 NICHD NIH HHS , R01 HL136566 NHLBI NIH HHS
Species referenced: Xenopus laevis
Genes referenced: fry gsc not otx2 stk38 stk38l tbxt
Antibodies: Fn1 Ab1 Notochord Ab2 Somite Ab3
Morpholinos: fry MO1
Article Images: [+] show captions
References [+] :
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Butler, Planar cell polarity in development and disease. 2017, Pubmed
Carron, Specification of anteroposterior axis by combinatorial signaling during Xenopus development. 2016, Pubmed , Xenbase
Chiba, MST2- and Furry-mediated activation of NDR1 kinase is critical for precise alignment of mitotic chromosomes. 2009, Pubmed
Cho, Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. 1992, Pubmed , Xenbase
Cirio, Lhx1 is required for specification of the renal progenitor cell field. 2011, Pubmed , Xenbase
Cong, The furry gene of Drosophila is important for maintaining the integrity of cellular extensions during morphogenesis. 2001, Pubmed
Cook, Constitutively active NDR1-PIF kinase functions independent of MST1 and hMOB1 signalling. 2015, Pubmed
Davidson, Live imaging of cell protrusive activity, and extracellular matrix assembly and remodeling during morphogenesis in the frog, Xenopus laevis. 2008, Pubmed , Xenbase
Davidson, Mesendoderm extension and mantle closure in Xenopus laevis gastrulation: combined roles for integrin alpha(5)beta(1), fibronectin, and tissue geometry. 2002, Pubmed , Xenbase
Davidson, Patterning and tissue movements in a novel explant preparation of the marginal zone of Xenopus laevis. 2005, Pubmed , Xenbase
Davidson, Integrin alpha5beta1 and fibronectin regulate polarized cell protrusions required for Xenopus convergence and extension. 2006, Pubmed , Xenbase
Davidson, Assembly and remodeling of the fibrillar fibronectin extracellular matrix during gastrulation and neurulation in Xenopus laevis. 2005, Pubmed , Xenbase
Du, Pag1p, a novel protein associated with protein kinase Cbk1p, is required for cell morphogenesis and proliferation in Saccharomyces cerevisiae. 2002, Pubmed
Espiritu, The Lhx1-Ldb1 complex interacts with Furry to regulate microRNA expression during pronephric kidney development. 2019, Pubmed , Xenbase
Ewald, Regional requirements for Dishevelled signaling during Xenopus gastrulation: separable effects on blastopore closure, mesendoderm internalization and archenteron formation. 2005, Pubmed , Xenbase
Feroze, Mechanics of blastopore closure during amphibian gastrulation. 2015, Pubmed , Xenbase
Gallegos, Mechanosensory neurite termination and tiling depend on SAX-2 and the SAX-1 kinase. 2004, Pubmed
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Gong, Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. 2004, Pubmed
Gorny, Brachet's cleft: a model for the analysis of tissue separation in Xenopus. 2014, Pubmed , Xenbase
Goto, Xenopus furry contributes to release of microRNA gene silencing. 2010, Pubmed , Xenbase
Goto, The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. 2002, Pubmed , Xenbase
Goto, Planar cell polarity genes regulate polarized extracellular matrix deposition during frog gastrulation. 2005, Pubmed , Xenbase
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Habas, Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. 2002, Pubmed , Xenbase
Han, Integrins regulate repulsion-mediated dendritic patterning of drosophila sensory neurons by restricting dendrites in a 2D space. 2012, Pubmed
Haubold, Segmenting and Tracking Multiple Dividing Targets Using ilastik. 2016, Pubmed
He, The tricornered Ser/Thr protein kinase is regulated by phosphorylation and interacts with furry during Drosophila wing hair development. 2005, Pubmed
Heisenberg, Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. 2000, Pubmed
Hergovich, NDR kinases regulate essential cell processes from yeast to humans. 2006, Pubmed
Hergovich, Human NDR kinases are rapidly activated by MOB proteins through recruitment to the plasma membrane and phosphorylation. 2005, Pubmed
Hikasa, Wnt signaling in vertebrate axis specification. 2013, Pubmed , Xenbase
Hirata, Fission yeast Mor2/Cps12, a protein similar to Drosophila Furry, is essential for cell morphogenesis and its mutation induces Wee1-dependent G(2) delay. 2002, Pubmed
Hopwood, MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. 1989, Pubmed , Xenbase
Horne-Badovinac, A screen for round egg mutants in Drosophila identifies tricornered, furry, and misshapen as regulators of egg chamber elongation. 2013, Pubmed
Ikeda, Furry protein promotes aurora A-mediated Polo-like kinase 1 activation. 2012, Pubmed
Irie, Furry protein suppresses nuclear localization of yes-associated protein (YAP) by activating NDR kinase and binding to YAP. 2020, Pubmed
Kaufmann, Multilayer mounting enables long-term imaging of zebrafish development in a light sheet microscope. 2012, Pubmed
Keller, The function and mechanism of convergent extension during gastrulation of Xenopus laevis. 1986, Pubmed , Xenbase
Keller, Mechanisms of convergence and extension by cell intercalation. 2001, Pubmed
Keller, Shaping the vertebrate body plan by polarized embryonic cell movements. 2003, Pubmed
Keller, Dynamic determinations: patterning the cell behaviours that close the amphibian blastopore. 2008, Pubmed , Xenbase
Keller, How we are shaped: the biomechanics of gastrulation. 2004, Pubmed , Xenbase
Leptin, Gastrulation movements: the logic and the nuts and bolts. 2005, Pubmed
Luxardi, Distinct Xenopus Nodal ligands sequentially induce mesendoderm and control gastrulation movements in parallel to the Wnt/PCP pathway. 2010, Pubmed , Xenbase
Malacinski, Neural plate morphogenesis and axial stretching in "notochord-defective" Xenopus laevis embryos. 1982, Pubmed , Xenbase
Matsubara, The seven-pass transmembrane cadherin Flamingo controls dendritic self-avoidance via its binding to a LIM domain protein, Espinas, in Drosophila sensory neurons. 2011, Pubmed
Matthews, Directional migration of neural crest cells in vivo is regulated by Syndecan-4/Rac1 and non-canonical Wnt signaling/RhoA. 2008, Pubmed , Xenbase
Moretti, Compact and reflective light-sheet microscopy for long-term imaging of living embryos. 2021, Pubmed
Nagai, Multifaceted roles of Furry proteins in invertebrates and vertebrates. 2014, Pubmed
Nagai, Furry promotes acetylation of microtubules in the mitotic spindle by inhibition of SIRT2 tubulin deacetylase. 2014, Pubmed
Nelson, RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis. 2004, Pubmed
Norkett, Ser/Thr kinase Trc controls neurite outgrowth in Drosophila by modulating microtubule-microtubule sliding. 2021, Pubmed
Plouhinec, Chordin forms a self-organizing morphogen gradient in the extracellular space between ectoderm and mesoderm in the Xenopus embryo. 2014, Pubmed , Xenbase
Rozario, The physical state of fibronectin matrix differentially regulates morphogenetic movements in vivo. 2009, Pubmed , Xenbase
Sasai, Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. 1995, Pubmed , Xenbase
Scharf, Determination of the dorsal-ventral axis in eggs of Xenopus laevis: complete rescue of uv-impaired eggs by oblique orientation before first cleavage. 1980, Pubmed , Xenbase
Shawky, Multiscale analysis of architecture, cell size and the cell cortex reveals cortical F-actin density and composition are major contributors to mechanical properties during convergent extension. 2019, Pubmed , Xenbase
Shih, Patterns of cell motility in the organizer and dorsal mesoderm of Xenopus laevis. 1993, Pubmed , Xenbase
Shih, Cell motility driving mediolateral intercalation in explants of Xenopus laevis. 1993, Pubmed , Xenbase
Shindo, Models of convergent extension during morphogenesis. 2018, Pubmed , Xenbase
Shook, Large, long range tensile forces drive convergence during Xenopus blastopore closure and body axis elongation. 2019, Pubmed , Xenbase
Shook, Pattern and morphogenesis of presumptive superficial mesoderm in two closely related species, Xenopus laevis and Xenopus tropicalis. 2004, Pubmed , Xenbase
Smith, Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. 1991, Pubmed , Xenbase
Tada, Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. 2000, Pubmed , Xenbase
Takeuchi, The prickle-related gene in vertebrates is essential for gastrulation cell movements. 2004, Pubmed , Xenbase
Ulmer, A novel role of the organizer gene Goosecoid as an inhibitor of Wnt/PCP-mediated convergent extension in Xenopus and mouse. 2018, Pubmed , Xenbase
Vichalkovski, NDR kinase is activated by RASSF1A/MST1 in response to Fas receptor stimulation and promotes apoptosis. 2009, Pubmed
Wacker, Development and control of tissue separation at gastrulation in Xenopus. 2000, Pubmed , Xenbase
Wallingford, Inhibition of morphogenetic movement during Xenopus gastrulation by injected sulfatase: implications for anteroposterior and dorsoventral axis formation. 1997, Pubmed , Xenbase
Wallingford, Convergent extension: the molecular control of polarized cell movement during embryonic development. 2002, Pubmed , Xenbase
Wallingford, Dishevelled controls cell polarity during Xenopus gastrulation. 2000, Pubmed , Xenbase
Winklbauer, Fibronectin, mesoderm migration, and gastrulation in Xenopus. 1996, Pubmed , Xenbase
Winklbauer, Vegetal rotation, a new gastrulation movement involved in the internalization of the mesoderm and endoderm in Xenopus. 1999, Pubmed , Xenbase
Xiong, Structural Basis for Auto-Inhibition of the NDR1 Kinase Domain by an Atypically Long Activation Segment. 2019, Pubmed
Yokota, A novel role for a nodal-related protein; Xnr3 regulates convergent extension movements via the FGF receptor. 2003, Pubmed , Xenbase
Youn, Axial structure development in ultraviolet-irradiated (notochord-defective) amphibian embryos. 1981, Pubmed , Xenbase
Zallen, Neuronal cell shape and neurite initiation are regulated by the Ndr kinase SAX-1, a member of the Orb6/COT-1/warts serine/threonine kinase family. 2000, Pubmed
Zhou, Macroscopic stiffening of embryonic tissues via microtubules, RhoGEF and the assembly of contractile bundles of actomyosin. 2010, Pubmed , Xenbase
von Dassow, Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeo box gene. 1993, Pubmed , Xenbase
Blitz, Anterior neurectoderm is progressively induced during gastrulation: the role of the Xenopus homeobox gene orthodenticle. 1995, Pubmed , Xenbase
Butler, Planar cell polarity in development and disease. 2017, Pubmed
Carron, Specification of anteroposterior axis by combinatorial signaling during Xenopus development. 2016, Pubmed , Xenbase
Chiba, MST2- and Furry-mediated activation of NDR1 kinase is critical for precise alignment of mitotic chromosomes. 2009, Pubmed
Cho, Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. 1992, Pubmed , Xenbase
Cirio, Lhx1 is required for specification of the renal progenitor cell field. 2011, Pubmed , Xenbase
Cong, The furry gene of Drosophila is important for maintaining the integrity of cellular extensions during morphogenesis. 2001, Pubmed
Cook, Constitutively active NDR1-PIF kinase functions independent of MST1 and hMOB1 signalling. 2015, Pubmed
Davidson, Live imaging of cell protrusive activity, and extracellular matrix assembly and remodeling during morphogenesis in the frog, Xenopus laevis. 2008, Pubmed , Xenbase
Davidson, Mesendoderm extension and mantle closure in Xenopus laevis gastrulation: combined roles for integrin alpha(5)beta(1), fibronectin, and tissue geometry. 2002, Pubmed , Xenbase
Davidson, Patterning and tissue movements in a novel explant preparation of the marginal zone of Xenopus laevis. 2005, Pubmed , Xenbase
Davidson, Integrin alpha5beta1 and fibronectin regulate polarized cell protrusions required for Xenopus convergence and extension. 2006, Pubmed , Xenbase
Davidson, Assembly and remodeling of the fibrillar fibronectin extracellular matrix during gastrulation and neurulation in Xenopus laevis. 2005, Pubmed , Xenbase
Du, Pag1p, a novel protein associated with protein kinase Cbk1p, is required for cell morphogenesis and proliferation in Saccharomyces cerevisiae. 2002, Pubmed
Espiritu, The Lhx1-Ldb1 complex interacts with Furry to regulate microRNA expression during pronephric kidney development. 2019, Pubmed , Xenbase
Ewald, Regional requirements for Dishevelled signaling during Xenopus gastrulation: separable effects on blastopore closure, mesendoderm internalization and archenteron formation. 2005, Pubmed , Xenbase
Feroze, Mechanics of blastopore closure during amphibian gastrulation. 2015, Pubmed , Xenbase
Gallegos, Mechanosensory neurite termination and tiling depend on SAX-2 and the SAX-1 kinase. 2004, Pubmed
Gawantka, Gene expression screening in Xenopus identifies molecular pathways, predicts gene function and provides a global view of embryonic patterning. 1999, Pubmed , Xenbase
Gong, Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. 2004, Pubmed
Gorny, Brachet's cleft: a model for the analysis of tissue separation in Xenopus. 2014, Pubmed , Xenbase
Goto, Xenopus furry contributes to release of microRNA gene silencing. 2010, Pubmed , Xenbase
Goto, The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. 2002, Pubmed , Xenbase
Goto, Planar cell polarity genes regulate polarized extracellular matrix deposition during frog gastrulation. 2005, Pubmed , Xenbase
Gray, Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. 2011, Pubmed
Habas, Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. 2002, Pubmed , Xenbase
Han, Integrins regulate repulsion-mediated dendritic patterning of drosophila sensory neurons by restricting dendrites in a 2D space. 2012, Pubmed
Haubold, Segmenting and Tracking Multiple Dividing Targets Using ilastik. 2016, Pubmed
He, The tricornered Ser/Thr protein kinase is regulated by phosphorylation and interacts with furry during Drosophila wing hair development. 2005, Pubmed
Heisenberg, Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. 2000, Pubmed
Hergovich, NDR kinases regulate essential cell processes from yeast to humans. 2006, Pubmed
Hergovich, Human NDR kinases are rapidly activated by MOB proteins through recruitment to the plasma membrane and phosphorylation. 2005, Pubmed
Hikasa, Wnt signaling in vertebrate axis specification. 2013, Pubmed , Xenbase
Hirata, Fission yeast Mor2/Cps12, a protein similar to Drosophila Furry, is essential for cell morphogenesis and its mutation induces Wee1-dependent G(2) delay. 2002, Pubmed
Hopwood, MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. 1989, Pubmed , Xenbase
Horne-Badovinac, A screen for round egg mutants in Drosophila identifies tricornered, furry, and misshapen as regulators of egg chamber elongation. 2013, Pubmed
Ikeda, Furry protein promotes aurora A-mediated Polo-like kinase 1 activation. 2012, Pubmed
Irie, Furry protein suppresses nuclear localization of yes-associated protein (YAP) by activating NDR kinase and binding to YAP. 2020, Pubmed
Kaufmann, Multilayer mounting enables long-term imaging of zebrafish development in a light sheet microscope. 2012, Pubmed
Keller, The function and mechanism of convergent extension during gastrulation of Xenopus laevis. 1986, Pubmed , Xenbase
Keller, Mechanisms of convergence and extension by cell intercalation. 2001, Pubmed
Keller, Shaping the vertebrate body plan by polarized embryonic cell movements. 2003, Pubmed
Keller, Dynamic determinations: patterning the cell behaviours that close the amphibian blastopore. 2008, Pubmed , Xenbase
Keller, How we are shaped: the biomechanics of gastrulation. 2004, Pubmed , Xenbase
Leptin, Gastrulation movements: the logic and the nuts and bolts. 2005, Pubmed
Luxardi, Distinct Xenopus Nodal ligands sequentially induce mesendoderm and control gastrulation movements in parallel to the Wnt/PCP pathway. 2010, Pubmed , Xenbase
Malacinski, Neural plate morphogenesis and axial stretching in "notochord-defective" Xenopus laevis embryos. 1982, Pubmed , Xenbase
Matsubara, The seven-pass transmembrane cadherin Flamingo controls dendritic self-avoidance via its binding to a LIM domain protein, Espinas, in Drosophila sensory neurons. 2011, Pubmed
Matthews, Directional migration of neural crest cells in vivo is regulated by Syndecan-4/Rac1 and non-canonical Wnt signaling/RhoA. 2008, Pubmed , Xenbase
Moretti, Compact and reflective light-sheet microscopy for long-term imaging of living embryos. 2021, Pubmed
Nagai, Multifaceted roles of Furry proteins in invertebrates and vertebrates. 2014, Pubmed
Nagai, Furry promotes acetylation of microtubules in the mitotic spindle by inhibition of SIRT2 tubulin deacetylase. 2014, Pubmed
Nelson, RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis. 2004, Pubmed
Norkett, Ser/Thr kinase Trc controls neurite outgrowth in Drosophila by modulating microtubule-microtubule sliding. 2021, Pubmed
Plouhinec, Chordin forms a self-organizing morphogen gradient in the extracellular space between ectoderm and mesoderm in the Xenopus embryo. 2014, Pubmed , Xenbase
Rozario, The physical state of fibronectin matrix differentially regulates morphogenetic movements in vivo. 2009, Pubmed , Xenbase
Sasai, Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. 1995, Pubmed , Xenbase
Scharf, Determination of the dorsal-ventral axis in eggs of Xenopus laevis: complete rescue of uv-impaired eggs by oblique orientation before first cleavage. 1980, Pubmed , Xenbase
Shawky, Multiscale analysis of architecture, cell size and the cell cortex reveals cortical F-actin density and composition are major contributors to mechanical properties during convergent extension. 2019, Pubmed , Xenbase
Shih, Patterns of cell motility in the organizer and dorsal mesoderm of Xenopus laevis. 1993, Pubmed , Xenbase
Shih, Cell motility driving mediolateral intercalation in explants of Xenopus laevis. 1993, Pubmed , Xenbase
Shindo, Models of convergent extension during morphogenesis. 2018, Pubmed , Xenbase
Shook, Large, long range tensile forces drive convergence during Xenopus blastopore closure and body axis elongation. 2019, Pubmed , Xenbase
Shook, Pattern and morphogenesis of presumptive superficial mesoderm in two closely related species, Xenopus laevis and Xenopus tropicalis. 2004, Pubmed , Xenbase
Smith, Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. 1991, Pubmed , Xenbase
Tada, Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. 2000, Pubmed , Xenbase
Takeuchi, The prickle-related gene in vertebrates is essential for gastrulation cell movements. 2004, Pubmed , Xenbase
Ulmer, A novel role of the organizer gene Goosecoid as an inhibitor of Wnt/PCP-mediated convergent extension in Xenopus and mouse. 2018, Pubmed , Xenbase
Vichalkovski, NDR kinase is activated by RASSF1A/MST1 in response to Fas receptor stimulation and promotes apoptosis. 2009, Pubmed
Wacker, Development and control of tissue separation at gastrulation in Xenopus. 2000, Pubmed , Xenbase
Wallingford, Inhibition of morphogenetic movement during Xenopus gastrulation by injected sulfatase: implications for anteroposterior and dorsoventral axis formation. 1997, Pubmed , Xenbase
Wallingford, Convergent extension: the molecular control of polarized cell movement during embryonic development. 2002, Pubmed , Xenbase
Wallingford, Dishevelled controls cell polarity during Xenopus gastrulation. 2000, Pubmed , Xenbase
Winklbauer, Fibronectin, mesoderm migration, and gastrulation in Xenopus. 1996, Pubmed , Xenbase
Winklbauer, Vegetal rotation, a new gastrulation movement involved in the internalization of the mesoderm and endoderm in Xenopus. 1999, Pubmed , Xenbase
Xiong, Structural Basis for Auto-Inhibition of the NDR1 Kinase Domain by an Atypically Long Activation Segment. 2019, Pubmed
Yokota, A novel role for a nodal-related protein; Xnr3 regulates convergent extension movements via the FGF receptor. 2003, Pubmed , Xenbase
Youn, Axial structure development in ultraviolet-irradiated (notochord-defective) amphibian embryos. 1981, Pubmed , Xenbase
Zallen, Neuronal cell shape and neurite initiation are regulated by the Ndr kinase SAX-1, a member of the Orb6/COT-1/warts serine/threonine kinase family. 2000, Pubmed
Zhou, Macroscopic stiffening of embryonic tissues via microtubules, RhoGEF and the assembly of contractile bundles of actomyosin. 2010, Pubmed , Xenbase
von Dassow, Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeo box gene. 1993, Pubmed , Xenbase