Extraembryonic Endoderm cells as a model of endoderm development

In recent years the multipotent extraembryonic endoderm (XEN) stem cells have been the center of much attention. In vivo, XEN cells contribute to the formation of the extraembryonic endoderm, visceral and parietal endoderm and later on, the yolk sac. Recent data have shown that the distinction between embryonic and extraembryonic endoderm is not as strict as previously thought due to the integration, and not the displacement, of the visceral endoderm into the definitive embryonic endoderm. Therefore, cells from the extraembryonic endoderm also contribute to definitive endoderm. Many research groups focused on unraveling the potential and ability of XEN cells to both support differentiation and/or differentiate into endoderm‐like tissues as an alternative to embryonic stem (ES) cells. Moreover, the conversion of ES to XEN cells, shown recently without genetic manipulations, uncovers significant and novel molecular mechanisms involved in extraembryonic endoderm and definitive endoderm development. XEN cell lines provide a unique model for an early mammalian lineage that complements the established ES and trophoblast stem cell lines. Through the study of essential genes and signaling requirements for XEN cells in vitro, insights will be gained about the developmental program of the extraembryonic and embryonic endodermal lineage in vivo. This review will provide an overview on the current literature focusing on XEN cells as a model for primitive endoderm and possibly definitive endoderm as well as the potential of using these cells for therapeutic applications.

[1]  M. Zernicka-Goetz,et al.  The anterior visceral endoderm of the mouse embryo is established from both preimplantation precursor cells and by de novo gene expression after implantation. , 2007, Developmental biology.

[2]  V. Chapman,et al.  Cell lineage-specific undermethylation of mouse repetitive DNA , 1984, Nature.

[3]  Kit T. Rodolfa,et al.  Sox17 promotes differentiation in mouse embryonic stem cells by directly regulating extraembryonic gene expression and indirectly antagonizing self-renewal. , 2010, Genes & development.

[4]  H. Hamada,et al.  Origin and role of distal visceral endoderm, a group of cells that determines anterior–posterior polarity of the mouse embryo , 2011, Nature Cell Biology.

[5]  M. Manzanares,et al.  An early developmental role for miRNAs in the maintenance of extraembryonic stem cells in the mouse embryo. , 2010, Developmental cell.

[6]  J. Rossant,et al.  Promotion of trophoblast stem cell proliferation by FGF4. , 1998, Science.

[7]  K. McGrath,et al.  Hematopoiesis in the yolk sac: more than meets the eye. , 2005, Experimental hematology.

[8]  J. Rossant.  Stem cells and lineage development in the mammalian blastocyst. , 2007, Reproduction, fertility, and development.

[9]  Q. Al-Awqati,et al.  Conversion of ES cells to columnar epithelia by hensin and to squamous epithelia by laminin , 2004, The Journal of cell biology.

[10]  P. Robson,et al.  Sall4 regulates distinct transcription circuitries in different blastocyst-derived stem cell lineages. , 2008, Cell stem cell.

[11]  C. Senner,et al.  Coordination of cell proliferation and anterior-posterior axis establishment in the mouse embryo , 2011, Development.

[12]  R. Beddington,et al.  Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo , 1996, Current Biology.

[13]  M. Dziadek,et al.  In vitro production of Reichert's membrane by mouse embryo-derived parietal endoderm cell lines. , 1990, Experimental cell research.

[14]  R. Beddington,et al.  An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. , 1989, Development.

[15]  Ucrf Developmental,et al.  An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo , 1989 .

[16]  A. McMahon,et al.  Hedgehog is required for murine yolk sac angiogenesis. , 2002, Development.

[17]  S. Lehnert,et al.  Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. , 1987, Development.

[18]  Kazuwa Nakao,et al.  Differentiation of embryonic stem cells is induced by GATA factors. , 2002, Genes & development.

[19]  Jennifer Nichols,et al.  Differential plasticity of epiblast and primitive endoderm precursors within the ICM of the early mouse embryo , 2012, Development.

[20]  L. Postovit,et al.  Developmental potential of rat extraembryonic stem cells. , 2009, Stem cells and development.

[21]  R. Sherwood,et al.  Conversion from mouse embryonic to extra-embryonic endoderm stem cells reveals distinct differentiation capacities of pluripotent stem cell states , 2012, Development.

[22]  K. Anderson,et al.  Rac1-Dependent Collective Cell Migration Is Required for Specification of the Anterior-Posterior Body Axis of the Mouse , 2010, PLoS biology.

[23]  E. Lacy,et al.  Anterior visceral endoderm directs ventral morphogenesis and placement of head and heart via BMP2 expression. , 2011, Developmental cell.

[24]  A. Hadjantonakis,et al.  eXtraembryonic ENdoderm (XEN) Stem Cells Produce Factors that Activate Heart Formation , 2010, PloS one.

[25]  J. Rossant,et al.  Establishment of endoderm progenitors by SOX transcription factor expression in human embryonic stem cells. , 2008, Cell stem cell.

[26]  M. Clements,et al.  Crosstalk between Nodal/Activin and MAPK p38 Signaling Is Essential for Anterior-Posterior Axis Specification , 2011, Current Biology.

[27]  A. Califano,et al.  Regulation of extra-embryonic endoderm stem cell differentiation by Nodal and Cripto signaling , 2011, Development.

[28]  R. Beddington,et al.  Active cell migration drives the unilateral movements of the anterior visceral endoderm , 2004, Development.

[29]  B. Hogan,et al.  Incorporation into Reichert's membrane of laminin-like extracellular proteins synthesized by parietal endoderm cells of the mouse embryo. , 1980, Developmental biology.

[30]  J. Rossant,et al.  The mouse embryo autonomously acquires anterior-posterior polarity at implantation. , 2006, Developmental cell.

[31]  A. Nagy,et al.  Insufficient VEGFA activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation. , 2002, Development.

[32]  Tony Pawson,et al.  Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. , 2006, Developmental cell.

[33]  Hitoshi Niwa,et al.  Extra-embryonic endoderm cells derived from ES cells induced by GATA Factors acquire the character of XEN cells , 2007, BMC Developmental Biology.

[34]  M. Clements,et al.  Nodal Dependent Differential Localisation of Dishevelled-2 Demarcates Regions of Differing Cell Behaviour in the Visceral Endoderm , 2011, PLoS biology.

[35]  D. Chui,et al.  Hemopoietic stem cells in murine embryonic yolk sac and peripheral blood. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[36]  T. Magnuson,et al.  Dynamic morphogenetic events characterize the mouse visceral endoderm. , 2003, Developmental biology.

[37]  C. Mummery,et al.  BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo. , 2004, Genes & development.

[38]  Janet Rossant,et al.  Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo , 2010, Proceedings of the National Academy of Sciences.

[39]  R. Khanin,et al.  A Comparative Analysis of Extra-Embryonic Endoderm Cell Lines , 2010, PloS one.

[40]  A. Hadjantonakis,et al.  BMP4 signaling directs primitive endoderm-derived XEN cells to an extraembryonic visceral endoderm identity. , 2012, Developmental biology.

[41]  B. Hogan,et al.  Bmp4 is required for the generation of primordial germ cells in the mouse embryo. , 1999, Genes & development.

[42]  J. Rossant,et al.  BMP signaling induces visceral endoderm differentiation of XEN cells and parietal endoderm. , 2012, Developmental biology.

[43]  G. Pan,et al.  MicroRNA-145 Regulates OCT4, SOX2, and KLF4 and Represses Pluripotency in Human Embryonic Stem Cells , 2009, Cell.

[44]  Megan F. Cole,et al.  Connecting microRNA Genes to the Core Transcriptional Regulatory Circuitry of Embryonic Stem Cells , 2008, Cell.

[45]  J. Rossant,et al.  Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts , 2005, Development.

[46]  John E. Reid,et al.  Nodal cis-regulatory elements reveal epiblast and primitive endoderm heterogeneity in the peri-implantation mouse embryo. , 2011, Developmental biology.

[47]  M. Surani,et al.  Proximal visceral endoderm and extraembryonic ectoderm regulate the formation of primordial germ cell precursors , 2007, BMC Developmental Biology.

[48]  A. Hadjantonakis,et al.  The endoderm of the mouse embryo arises by dynamic widespread intercalation of embryonic and extraembryonic lineages. , 2008, Developmental cell.

[49]  E. Morrisey,et al.  GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. , 1998, Genes & development.

[50]  M. Dyer,et al.  Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. , 2001, Development.

[51]  W. Woodward,et al.  Isolation of Oct4-Expressing Extraembryonic Endoderm Precursor Cell Lines , 2009, PloS one.