Establishment and Organization of Germ Layers in the Gastrulating Mouse Embryo

Establishment and Organization of Germ Layers in the Gastrulating Mouse Embryo P. P. L. Tam, P. P. L. Tam The Children's Medical Research Foundation, PO Box 61, Camperdown, New South Wales 2050, AustraliaSearch for more papers by this authorR. S. P. Beddington, R. S. P. Beddington RAFRC Centre for Genome Research, Thc Old ABRO Building, King's Building, West Mains Road, Edinburgh EH9 3JQ, UKSearch for more papers by this author P. P. L. Tam, P. P. L. Tam The Children's Medical Research Foundation, PO Box 61, Camperdown, New South Wales 2050, AustraliaSearch for more papers by this authorR. S. P. Beddington, R. S. P. Beddington RAFRC Centre for Genome Research, Thc Old ABRO Building, King's Building, West Mains Road, Edinburgh EH9 3JQ, UKSearch for more papers by this author Book Editor(s):Derek J. Chadwick, Derek J. ChadwickSearch for more papers by this authorJoan Marsh, Joan MarshSearch for more papers by this author First published: 28 September 2007 https://doi.org/10.1002/9780470514221.ch3Citations: 9Book Series:Novartis Foundation Symposia AboutPDFPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShareShare a linkShare onEmailFacebookTwitterLinkedInRedditWechat Summary By following the distribution of wheat germ agglutinin–gold-labelled cells in primitive streak stage embryos, we obtained direct evidence for a continuous recruitment of the embryonic ectoderm cells to the definitive endoderm and to the embryonic and extraembryonic mesoderm during gastrulation. The majority of the definitive endodermal cells ingressed through the anterior end of the primitive streak and were incorporated initially into the midline endoderm at the archenteron, but a small population of endodermal cells may he recruited by direct delamination from the embryonic ectoderm. The pre-existing visceral embryonic endoderm was progressively replaced, but not totally, by the newly recruited population which colonized the embryonic foregut and the notochord. The developmental fate of the recruited endoderm and that of cells in the embryonic ectoderm and the mesoderm of late primitive streak stage embryos indicate that concomitant with the establishment of the germ layers, an orderly allocation of prospective fetal tissues to specific parts of the body occurs simultaneously in all three germ layers. References Batten BE, Haar JL 1979 Fine structural differentiation of germ layers in the mouse at the time of mesoderm formation. Anat Rec 194: 125–142 10.1002/ar.1091940109 CASPubMedWeb of Science®Google Scholar Beddington RSP 1981 An autoradiographic analysis of the potency of embryonic ectoderm in the 8th day postimplantation mouse embryo. J Embryol Exp Morphol 64: 87–104 CASPubMedWeb of Science®Google Scholar Beddington RSP 1983 The origin of foetal tissues during gastrulation in the rodent. In: MH Johnson (ed) Development in mammals. Elsevier, Amsterdam p 1–32 Google Scholar Bellairs R 1986 The primitive streak. Anat Embryol 174: 1–14 10.1007/BF00318331 CASPubMedWeb of Science®Google Scholar Cockroft DL, Gardner RL 1987 Clonal analysis of the developmental potential of 6th and 7th day visceral endoderm in the mouse. Development 101: 143–155 PubMedGoogle Scholar Cooke J, Wong A 1991 Growth factor-related proteins that are inducers in early amphibian development may mediate similar steps in amniote (bird) embryogenesis. Development 111: 197–212 CASPubMedWeb of Science®Google Scholar Enders AC, Given RL, Schlafke S 1978 Differentiation and migration of endoderm in the rat and mouse at implantation. Anat Rec 190: 65–78 10.1002/ar.1091900107 PubMedWeb of Science®Google Scholar Fontaine J, Le Douarin NM 1977 Analysis of endoderm formation in the chick embryo at the primitive streak stage as determined by radioautography mapping. Dev Biol 26: 323–335 Google Scholar Frohman MA, Boyle M, Martin GR 1990 Isolation of the mouseHox-2.9 gene; analysis of embryonic expression suggests that positional information along the anterior-posterior axis is specified by mesoderm. Development 110: 589–608 CASPubMedWeb of Science®Google Scholar Gardner RL, Beddington RSP 1988 Multi-lineage 'stem' cells in the mammalian embryo. J Cell Sci Suppl 10: 11–27 10.1242/jcs.1988.Supplement_10.2 CASPubMedGoogle Scholar Hashimoto K, Nakatsuji N 1989 Formation of the primitive streak and mesoderm cells in mouse embryos—detailed scanning electron microscopical study. Dev Growth & Differ 31: 209–218 10.1111/j.1440-169X.1989.00209.x Web of Science®Google Scholar Kimber SJ 1986 Distribution of lectin receptors in postimplantation mouse embryo at 6–8 days gestation. Am J Anat 177: 203–219 10.1002/aja.1001770207 CASPubMedWeb of Science®Google Scholar Lamers WH, Spliet WGM, Langemeyer RATM 1987 The lining of the gut in the developing rat embryo. Its relation to the hypoblast (primary endoderm) and the notochord. Anat Embryol 176: 259–265 10.1007/BF00310060 CASPubMedWeb of Science®Google Scholar Lawson KA, Pedersen RA 1987 Cell fate, morphogenetic movement and population kinetics of embryonic endoderm at the time of germ layer formation in the mouse. Development 101: 627–652 PubMedWeb of Science®Google Scholar Lawson KA, Meneses J J, Pedersen RA 1986 Cell fate and cell lineage in the endoderm of the presomite mouse embryo, studied with an intracellular tracer. Dev Biol 115: 325–339 10.1016/0012-1606(86)90253-8 CASPubMedWeb of Science®Google Scholar Meier S, Tam PPL 1982 Metameric pattern development in the embryonic axis of the mouse. I. Differentiation of the cranial segments. Differentiation 21: 95–108 10.1111/j.1432-0436.1982.tb01202.x PubMedWeb of Science®Google Scholar Mitrani E, Ziv T, Thomsen G, Shimoni Y, Melton DA, Bril A 1990 Activin can induce the formation of axial structures and is expressed in the hypoblast of the chick. Cell 63: 495–501 10.1016/0092-8674(90)90446-L CASPubMedWeb of Science®Google Scholar Nakatsuji N, Snow MHL, Wylie CC 1986 Cinematographic study of the cell movement in the primitive-streak stage mouse embryo. J Embryol Exp Morphol 96: 99–100 PubMedWeb of Science®Google Scholar Poelmann RE 1981a The formation of the embryonic mesoderm in the early postimplantation mouse embryo. Anat Embryol 162: 29–40 10.1007/BF00318092 CASPubMedWeb of Science®Google Scholar Poelmann RE 1981b The head process and the formation of the definitive endoderm in the mouse embryo. Anat Embryol 162: 41–49 10.1007/BF00318093 CASPubMedWeb of Science®Google Scholar Sanders EJ, Bellairs R, Portch PA 1978 In vivo and in vitro studies on the hypoblast and definitive endoblast of avian embryos. J Embryol Exp Morphol 46: 187–205 CASPubMedWeb of Science®Google Scholar Snell GD, Stevens LC 1966 Early embryology. In: L Green (ed) Biology of the laboratory mouse. Dover, New York p 205–245 Google Scholar Snow MHL 1976 Embryo growth during the immediate postimplantation period. In: Embryogenesis in mammals. Elsevier, Amsterdam (Ciba Found Symp 40) p 53–70 10.1002/9780470720226.ch5 Google Scholar Stern CD 1990 The marginal zone and its contribution to the hypoblast and primitive streak of the chick embryo. Development 109: 667–682 10.1242/dev.109.3.667 CASPubMedWeb of Science®Google Scholar Stern CD, Canning DR 1990 Origin of cells giving rise to mesoderm and endoderm in chick embryo. Nature (Lond) 343: 273–275 10.1038/343273a0 PubMedWeb of Science®Google Scholar Sundin OH, Busse HG, Rogers MB, Gudas LJ, Eichele G 1990 Region-specific expression in early chick and mouse embryos of Ghox-lab and Hox 1.6, vertebrate homeobox-containing genes related toDrosophila labial. Development 108: 47–58 CASPubMedWeb of Science®Google Scholar Takeichi M 1988 The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102: 639–655 10.1242/dev.102.4.639 CASPubMedWeb of Science®Google Scholar Tam PPL 1984 The histogenetic capacity of tissues in the caudal end of the embryonic axis of the mouse. J Embryol Exp Morphol 82: 253–266 CASPubMedWeb of Science®Google Scholar Tam PPL 1989 Regionalisation of the mouse embryonic ectoderm: allocation of prospective ectodermal tissues during gastrulation. Development 101: 55–67 Google Scholar Tam PPL, Beddington RSP 1987 The formation of mesodermal tissues in the mouse embryo during gastrulation and early organogenesis. Development 99: 109–126 10.1242/dev.99.1.109 CASPubMedWeb of Science®Google Scholar Tam PPL, Meier S 1982 The establishment of a somitomeric pattern in the mesoderm of the gastrulating mouse embryo. Am J Anat 164: 209–225 10.1002/aja.1001640303 CASPubMedWeb of Science®Google Scholar Wilkinson DG, Bhatt S, Herrmann BG 1990 Expression pattern of the mouseT gene and its role in mesoderm formation. Nature (Lond) 343: 657–659 10.1038/343657a0 CASPubMedWeb of Science®Google Scholar Wilkinson DG, Peters G, Dickson C, McMahon AP 1988 Expression of the FGF-related proto-oncogeneint-2 during gastrulation and neurulation in the mouse. EMBO (Eur Mol Biol Organ) J 7: 691–695 10.1002/j.1460-2075.1988.tb02864.x CASPubMedWeb of Science®Google Scholar Evans MJ, Martin GR 1975 The differentiation of clonal teratocarcinoma cell culture in vitro. In: D Solter, M Sherman (eds) Roche symposium on teratomas and differentiation. Academic Press, New York Google Scholar Gardner RL, Rossant J 1979 Investigation of the fate of 4.5 day post coitum mouse inner cell mass cells by blastocyst injection. J Embryol Exp Morphol 52: 141–152 CASPubMedWeb of Science®Google Scholar Martin GR, Evans MJ 1975 Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci USA 72: 1441–1445 10.1073/pnas.72.4.1441 CASPubMedWeb of Science®Google Scholar Martin GR, Wiley LM, Damjanov I 1977 The development of cystic embryoid bodiesin vitro from clonal teratocarcinoma stem cells. Dev Biol 61: 230–244 10.1016/0012-1606(77)90294-9 CASPubMedWeb of Science®Google Scholar Meunier H, Rivier C, Evans RM, Vale W 1988 Gonadal and extragonadal expression of inhibin α, b̃A and b̃B subunits in various tissues predicts diverse functions. Proc Natl Acad Sci USA 85: 247–251 10.1073/pnas.85.1.247 CASPubMedWeb of Science®Google Scholar Takeichi M 1988 The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102: 639–655 10.1242/dev.102.4.639 CASPubMedWeb of Science®Google Scholar Tam PPL, Beddington RSP 1987 The formation of mesodermal tissues in the mouse embryo during gastrulation and early organogenesis. Development 99: 109–126 10.1242/dev.99.1.109 CASPubMedWeb of Science®Google Scholar Beddington RSP 1983 The origin of the foetal tissues during gastrulation in the rodent. In: MH Johnson (ed) Development in mammals. Elsevier, Amsterdam p 1–32 Google Scholar Blumberg B, Wright CVE, de Robertis EM, Cho KWY 1991 Organizer-specific homeobox genes inXenopus laevis embryos. Science (Wash DC) 253: 194–196 10.1126/science.1677215 CASPubMedWeb of Science®Google Scholar Hogan B, Tilly R 1978 In vitro development of inner cell masses isolated immunosurgically from mouse blastocysts. J Embryol Exp Morphol 45: 93–105 CASPubMedWeb of Science®Google Scholar Jat PS, Noble MD, Ataliotis P et al 1991 Direct derivation of conditionally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc Natl Acad Sci USA 88: 5096–5101 10.1073/pnas.88.12.5096 CASPubMedWeb of Science®Google Scholar Lawson KA, Pedersen RA 1992 Clonal analysis of cell fate during gastrulation and early neurulation in the mouse. In: Postimplantation development in the mouse. Wiley, Chichester (Ciba Found Symp 165) p 3–26 10.1002/9780470514221.ch2 Google Scholar New DAT 1990 Introduction. In: AJ Copp, DL Cockcroft (eds) Postimplantation mammalian embryos: a practical approach. IRL Press, Oxford p 1–14 Google Scholar Saxén L, Thesleff I 1992 Epithelial-mesenchymal interactions in murine organogenesis. In: Postimplantation development in the mouse. Wiley, Chichester (Ciba Found Symp 165) p 183–198 Google Scholar Tam PPL 1989 Regionalisation of the mouse embryonic ectoderm: allocation of prospective ectodermal tissues during gastrulation. Development 107: 55–67 CASPubMedWeb of Science®Google Scholar Tam PPL, Beddington RSP 1987 The formation of mesodermal tissues in the mouse embryo during gastrulation and early organogenesis. Development 99: 109–126 10.1242/dev.99.1.109 CASPubMedWeb of Science®Google Scholar Citing Literature Ciba Foundation Symposium 165 ‐ Postimplantation Development in the Mouse: Postimplantation Development in the Mouse: Ciba Foundation Symposium 165 ReferencesRelatedInformation