Tissue Mechanics Determines Cell Fate in the Axial Stem Zones

Most embryos and regenerating tissues grow by the action of stem zones. Two epithelial stem zones drive axial elongation in amniotes: the mature organizer generates mesoderm, the neuralised ectoderm around it extends the neuraxis. Bipotential progenitors were also shown to exist. How are these stem cell populations organised and what controls the cell fate of bipotential progenitors? We use direct, in vivo imaging of these stem cells in the chick and find that progenitors of single and dual fates are mingled in a small region between the specialised stem zones. Divergent tissue movements surround this region. When transplanted downstream of these flows, cells from the region of mixed fates adopt the molecular identity and behaviour of the target stem zone, irrespective of normal fate. Thus, multipotent cells serve to separate the specialized stem zones, instead of a classical boundary. We propose their fate is determined extrinsically by morphogenetic shearing.

[1]  J. Martinez-Barbera,et al.  Genetic approaches in mice demonstrate that neuro-mesodermal progenitors express T/Brachyury but not Sox2 , 2018 .

[2]  M. Mallo,et al.  Deconstructing the molecular mechanisms shaping the vertebrate body plan. , 2018, Current opinion in cell biology.

[3]  Srinivas C. Turaga,et al.  In Toto Imaging and Reconstruction of Post-Implantation Mouse Development at the Single-Cell Level , 2018, Cell.

[4]  M. Gierliński,et al.  Neural differentiation, selection and transcriptomic profiling of human neuromesodermal progenitor-like cells in vitro , 2018, Development.

[5]  A. van Oudenaarden,et al.  Neuromesodermal progenitors are a conserved source of spinal cord with divergent growth dynamics , 2018, Development.

[6]  P. Andrews,et al.  Human axial progenitors generate trunk neural crest cells in vitro , 2018, bioRxiv.

[7]  R. Sambasivan,et al.  Co-expression of Tbx6 and Sox2 identifies a novel transient neuromesoderm progenitor cell state , 2017, Development.

[8]  B. Herrmann,et al.  Antagonistic Activities of Sox2 and Brachyury Control the Fate Choice of Neuro-Mesodermal Progenitors. , 2017, Developmental cell.

[9]  Valerie Wilson,et al.  A Gene Regulatory Network Balances Neural and Mesoderm Specification during Vertebrate Trunk Development , 2017, Developmental cell.

[10]  T. Kurth,et al.  The posterior neural plate in axolotl gives rise to neural tube or turns anteriorly to form somites of the tail and posterior trunk. , 2017, Developmental biology.

[11]  M. Nieto,et al.  Snail2 and Zeb2 repress P-cadherin to define embryonic territories in the chick embryo , 2017, Development.

[12]  Johannes Schindelin,et al.  TrackMate: An open and extensible platform for single-particle tracking. , 2017, Methods.

[13]  K. Kaushansky Thrombopoietin and its receptor in normal and neoplastic hematopoiesis , 2016, Thrombosis Journal.

[14]  C. Tickle,et al.  A strategy to discover new organizers identifies a putative heart organizer , 2016, Nature Communications.

[15]  Philipp J. Keller,et al.  Real-Time Three-Dimensional Cell Segmentation in Large-Scale Microscopy Data of Developing Embryos. , 2016, Developmental cell.

[16]  G. Blin,et al.  Position-dependent plasticity of distinct progenitor types in the primitive streak , 2016, eLife.

[17]  Andreas Bartschat,et al.  XPIWIT - an XML pipeline wrapper for the Insight Toolkit , 2015, Bioinform..

[18]  D. Henrique,et al.  Neuromesodermal progenitors and the making of the spinal cord , 2015, Development.

[19]  D. Elliott,et al.  Multipotent Caudal Neural Progenitors Derived from Human Pluripotent Stem Cells That Give Rise to Lineages of the Central and Peripheral Nervous System , 2015, Stem cells.

[20]  M. Lewandoski,et al.  Lineage tracing of neuromesodermal progenitors reveals novel Wnt-dependent roles in trunk progenitor cell maintenance and differentiation , 2015, Development.

[21]  J. Coon,et al.  Deterministic HOX Patterning in Human Pluripotent Stem Cell-Derived Neuroectoderm , 2015, Stem cell reports.

[22]  H. Sang,et al.  Myosin II-mediated cell shape changes and cell intercalation contribute to primitive streak formation , 2015, Nature Cell Biology.

[23]  A. Martinez Arias,et al.  Brachyury cooperates with Wnt/β-catenin signalling to elicit primitive-streak-like behaviour in differentiating mouse embryonic stem cells , 2014, BMC Biology.

[24]  L. Saúde,et al.  N-cadherin locks left-right asymmetry by ending the leftward movement of Hensen's node cells. , 2014, Developmental cell.

[25]  J. Kleinjung,et al.  In Vitro Generation of Neuromesodermal Progenitors Reveals Distinct Roles for Wnt Signalling in the Specification of Spinal Cord and Paraxial Mesoderm Identity , 2014, PLoS biology.

[26]  L. Bodenstein,et al.  Local cell interactions and self-amplifying individual cell ingression drive amniote gastrulation , 2014, eLife.

[27]  K. Kaushansky,et al.  Thrombopoietin from beginning to end , 2014, British journal of haematology.

[28]  G. Blin,et al.  Distinct Wnt-driven primitive streak-like populations reflect in vivo lineage precursors , 2014, Development.

[29]  C. Stern,et al.  Assembly of imaging chambers and high-resolution imaging of early chick embryos. , 2012, Cold Spring Harbor protocols.

[30]  M. Nieto,et al.  Mutual exclusion of transcription factors and cell behaviour in the definition of vertebrate embryonic territories. , 2012, Current opinion in genetics & development.

[31]  David R. Kelley,et al.  Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks , 2012, Nature Protocols.

[32]  D. Kimelman,et al.  Canonical Wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. , 2012, Developmental cell.

[33]  R. Lovell-Badge,et al.  Reciprocal Repression between Sox3 and Snail Transcription Factors Defines Embryonic Territories at Gastrulation , 2011, Developmental cell.

[34]  C. D. de Graaf,et al.  Thrombopoietin and hematopoietic stem cells , 2011, Cell cycle.

[35]  Donald M. Bell,et al.  Tbx6-dependent Sox2 regulation determines neural vs mesodermal fate in axial stem cells , 2010, Nature.

[36]  V. Wilson,et al.  Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. , 2009, Developmental cell.

[37]  C. Tabin,et al.  Cell Movements at Hensen’s Node Establish Left/Right Asymmetric Gene Expression in the Chick , 2009, Science.

[38]  Valerie Wilson,et al.  Stem cells, signals and vertebrate body axis extension , 2009, Development.

[39]  D. Kimelman,et al.  Wnt Signaling and the Evolution of Embryonic Posterior Development , 2009, Current Biology.

[40]  C. Stern,et al.  Spatially and temporally controlled electroporation of early chick embryos , 2008, Nature Protocols.

[41]  L. Wolpert,et al.  The amniote primitive streak is defined by epithelial cell intercalation before gastrulation , 2007, Nature.

[42]  L. Antiga Generalizing vesselness with respect to dimensionality and shape , 2007, The Insight Journal.

[43]  V. Wilson,et al.  Two distinct sources for a population of maturing axial progenitors , 2007, Development.

[44]  O. Pourquié,et al.  Dual mode of paraxial mesoderm formation during chick gastrulation , 2007, Proceedings of the National Academy of Sciences.

[45]  Tianxin Yang,et al.  Prostaglandin D2 inhibits TGF-beta1-induced epithelial-to-mesenchymal transition in MDCK cells. , 2006, American journal of physiology. Renal physiology.

[46]  R. Beare,et al.  The watershed transform in ITK - discussion and new developments , 2006, The Insight Journal.

[47]  C. Croce,et al.  Cloning and characterization of cDNAs expressed during chick development and encoding different isoforms of a putative zinc finger transcriptional regulator. , 2005, Biochimie.

[48]  Mario dos Reis,et al.  Churchill, a Zinc Finger Transcriptional Activator, Regulates the Transition between Gastrulation and Neurulation , 2003, Cell.

[49]  S. Fraser,et al.  Distinct modes of floor plate induction in the chick embryo , 2003, Development.

[50]  V. Wilson,et al.  Axial progenitors with extensive potency are localised to the mouse chordoneural hinge. , 2002, Development.

[51]  L. Szekely,et al.  Epstein-Barr virus encoded nuclear protein EBNA-3 binds a novel human uridine kinase/uracil phosphoribosyltransferase , 2002, BMC Cell Biology.

[52]  R. Behringer,et al.  The organizer of the mouse gastrula is composed of a dynamic population of progenitor cells for the axial mesoderm. , 2001, Development.

[53]  Scott E. Fraser,et al.  FGF receptor signalling is required to maintain neural progenitors during Hensen's node progression , 2001, Nature Cell Biology.

[54]  A. Streit,et al.  Combined whole-mount in situ hybridization and immunohistochemistry in avian embryos. , 2001, Methods.

[55]  K. Storey,et al.  A region of the vertebrate neural plate in which neighbouring cells can adopt neural or epidermal fates , 2000, Current Biology.

[56]  M. Kirschner,et al.  The fate of cells in the tailbud of Xenopus laevis. , 2000, Development.

[57]  C. Stern,et al.  Molecular Interactions Continuously Define the Organizer during the Cell Movements of Gastrulation , 1999, Cell.

[58]  J. Nathans,et al.  A new secreted protein that binds to Wnt proteins and inhibits their activites , 1999, Nature.

[59]  Y. Urade,et al.  Lipocalin-type Prostaglandin D Synthase (β-Trace) Is a Newly Recognized Type of Retinoid Transporter* , 1997, The Journal of Biological Chemistry.

[60]  C. Stern,et al.  Fates and migratory routes of primitive streak cells in the chick embryo. , 1996, Development.

[61]  M. Catala,et al.  Organization and development of the tail bud analyzed with the quail-chick chimaera system , 1995, Mechanisms of Development.

[62]  Karel J. Zuiderveld,et al.  Contrast Limited Adaptive Histogram Equalization , 1994, Graphics Gems.

[63]  B. Blumberg,et al.  Tail formation as a continuation of gastrulation: the multiple cell populations of the Xenopus tailbud derive from the late blastopore lip. , 1993, Development.

[64]  C. Stern,et al.  Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. , 1991, Development.

[65]  D. New A New Technique for the Cultivation of the Chick Embryo in vitro , 1955 .

[66]  D. E. Holmdahl Die Morphogenese des Vertebratorganismus vom formalen und experimentellen Gesichtspunkt , 1939, Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen.

[67]  A. Compton,et al.  THE CULTIVATION OF TISSUES IN SALINE EMBRYONIC JUICE. , 1924 .

[68]  C. Stern,et al.  Manipulating Gene Expression in the Chick Embryo. , 2017, Methods in molecular biology.

[69]  D. Kimelman Tales of Tails (and Trunks): Forming the Posterior Body in Vertebrate Embryos. , 2016, Current topics in developmental biology.

[70]  Max A. Viergever,et al.  elastix: A Toolbox for Intensity-Based Medical Image Registration , 2010, IEEE Transactions on Medical Imaging.

[71]  M. Catala,et al.  Neurulation in amniote vertebrates: a novel view deduced from the use of quail-chick chimeras. , 1998, The International journal of developmental biology.

[72]  C. Stern,et al.  Evidence for Stem Cells in the Mesoderm of Hensen’s Node and Their Role in Embryonic Pattern Formation , 1992 .

[73]  J. Brady A simple technique for making very fine, durable dissecting needles by sharpening tungsten wire electrolytically. , 1965, Bulletin of the World Health Organization.