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Gastrulation: Making and Shaping Germ Layers CB28CH11-SolnicaKrezel ARI 29 June 2012 17:12 V I E E W R S Review in Advance first posted online on July 9, 2012. (Changes may still occur before final publication online and in print.) I E N C N A D V A Gastrulation: Making and Shaping Germ Layers Lila Solnica-Krezel and Diane S. Sepich Department of Developmental Biology, Washington University School of Medicine in St. Louis, St. Louis, Missouri 63110; email: [email protected], [email protected] Annu. Rev. Cell Dev. Biol. 2012. 28:11.1–11.31 Keywords The Annual Review of Cell and Developmental Biology is online at cellbio.annualreviews.org cell migration, cell intercalation, adhesion, chemotaxis, planar polarity This article’s doi: Abstract 10.1146/annurev-cellbio-092910-154043 Gastrulation is a fundamental phase of animal embryogenesis during Copyright c 2012 by Annual Reviews. All rights reserved which germ layers are specified, rearranged, and shaped into a body plan with organ rudiments. Gastrulation involves four evolutionar- 1081-0706/12/1110-0001$20.00 ily conserved morphogenetic movements, each of which results in a specific morphologic transformation. During emboly, mesodermal and endodermal cells become internalized beneath the ectoderm. Epibolic by Universidad de Los Andes - Colombia on 10/04/12. For personal use only. Annu. Rev. Cell Dev. Biol. 2012.28. Downloaded from www.annualreviews.org movements spread and thin germ layers. Convergence movements nar- row germ layers dorsoventrally, while concurrent extension movements elongate them anteroposteriorly. Each gastrulation movement can be achieved by single or multiple motile cell behaviors, including cell shape changes, directed migration, planar and radial intercalations, and cell divisions. Recent studies delineate cyclical and ratchet-like behaviors of the actomyosin cytoskeleton as a common mechanism underlying vari- ous gastrulation cell behaviors. Gastrulation movements are guided by differential cell adhesion, chemotaxis, chemokinesis, and planar polar- ity. Coordination of gastrulation movements with embryonic polarity involves regulation by anteroposterior and dorsoventral patterning sys- tems of planar polarity signaling, expression of chemokines, and cell adhesion molecules. 11.1 Changes may still occur before final publication online and in print CB28CH11-SolnicaKrezel ARI 29 June 2012 17:12 INTRODUCTION Contents Animals have bodies of diverse shapes with INTRODUCTION . 11.2 internal collections of organs of unique mor- COMPONENT GASTRULATION phology and function. Such sophisticated body MOVEMENTS: architecture is elaborated during embryonic de- MORPHOGENETIC velopment, whereby a fertilized egg undergoes OUTCOMES AND a program of cell divisions, fate specification, UNDERLYING CELL and movements. One key process of embryo- BEHAVIORS . 11.3 genesis is determination of the anteroposterior Emboly . 11.3 (AP), dorsoventral (DV), and left-right (LR) Epiboly. 11.5 embryonic axes. Other aspects of embryo- Convergence and Extension . 11.5 genesis are specification of the germ layers, GASTRULATION MOVEMENTS endoderm, mesoderm, and ectoderm, as well as IN MODEL ORGANISMS. 11.7 their subsequent patterning and diversification Caenorhabditis elegans . 11.7 of cell fates along the embryonic axes. These Drososophila melanogaster ............ 11.7 processes occur very early during development Sea Urchin . 11.9 when most embryos consist of a relatively Zebrafish . 11.9 small number of morphologically similar cells Frog . .11.10 arranged in simple structures, such as cell balls Chick . .11.11 or sheets, which can be flat or cup shaped. Mouse. .11.12 The term gastrulation, derived from the Greek MECHANICS OF POLARIZATION word gaster, denoting stomach or gut, is a fun- OF CELL ARCHITECTURE damental process of animal embryogenesis that AND ACTIVITY DURING employs cellular rearrangements and move- GASTRULATION................11.13 ments to reposition and shape the germ layers, Cell Shape and Motility Depend on thus creating the internal organization as well Adhesion and Cytoskeleton. .11.13 as the external form of developing animals. Apical Constriction and Pulsed Here we discuss both the differences in Actomyosin Contraction . .11.14 the cellular and molecular mechanisms of gas- Cell Intercalation . .11.16 trulation as well as the many similarities that Directed Migration . .11.17 emerge as we learn more about this fascinating MOLECULAR CUES GUIDING process in model organisms. First, we discuss POLARIZED GASTRULATION the four evolutionarily conserved gastrulation CELL BEHAVIORS . .11.18 movements, epiboly, internalization, conver- by Universidad de Los Andes - Colombia on 10/04/12. For personal use only. Annu. Rev. Cell Dev. Biol. 2012.28. Downloaded from www.annualreviews.org Cell-Cell Adhesion. .11.18 gence, and extension, each of which drives de- Cell-Matrix Adhesion . .11.20 fined morphological tissue transformation. Sec- Planar Polarity. .11.20 ond, we survey cellular mechanisms underlying Chemotaxis . .11.21 these gastrulation movements, including cell Chemokinesis. .11.22 migration, intercalation, epithelial mesenchy- COORDINATION OF mal transition, and cell shape changes. Next, we GASTRULATION discuss the process of gastrulation as it occurs MOVEMENTS WITH BODY in several model organisms, highlighting how AXES . .11.22 they employ epiboly, internalization, conver- OUTLOOK. .11.24 gence, and extension movements as well as the specific cellular mechanisms deployed. Then we provide a short review of the basic cell prop- erties, including cell adhesion, cortical tension, 11.2 Solnica-Krezel · Sepich Changes may still occur before final publication online and in print CB28CH11-SolnicaKrezel ARI 29 June 2012 17:12 and cytoskeletal systems, that mediate various structure central to the process of gastrulation, gastrulation cell behaviors. The essence of var- also known as blastoderm margin in fish and ious gastrulation cell movements is their po- primitive streak in amniotes (Keller & David- AP: anteroposterior larized and directional nature that affords the son 2004). Internalization is usually followed by transformation of an amorphous cellular mass migration of endodermal and mesodermal pro- DV: dorsoventral or cell sheet into highly asymmetric and struc- genitors away from the blastopore as individ- LR: left-right tured body rudiment. We review the significant ual cells (Solnica-Krezel 2005). At the onset of EMT: epithelial to progress achieved in recent years in delineat- gastrulation, prospective mesodermal and en- mesenchymal ing various molecular mechanisms that mediate doderm cells reside in epithelium (Drosophila transition and instruct asymmetric cellular behaviors dur- melanogaster, Caenorhabditis elegans, chick, SMO: ing gastrulation and coordinate morphogenetic mouse) or within tightly packed and adherent Spemann-Mangold organizer movements with embryonic polarity. mesenchymal tissue (frog, fish). Thus, emboly and migration of internalized mesodermal and endodermal cells must involve some form of ep- COMPONENT GASTRULATION ithelial to mesenchymal transition (EMT) (Wu MOVEMENTS: et al. 2007). In this process, epithelial junctions MORPHOGENETIC OUTCOMES are disassembled and cell adhesion molecules AND UNDERLYING CELL are downregulated, while intermediate filament BEHAVIORS network is formed and microtubule network is The process of gastrulation entails a set rearranged from acentrosomal to that radiating of evolutionarily conserved morphogenetic from a centrosome (Thiery et al. 2009). movements, emboly/internalization, epiboly, The variations in the cellular mechanisms convergence, and extension, which are defined that drive internalization include the position by their morphogenetic outcome (Keller of the blastopore in the gastrula and the timing et al. 1991). Emboly, or internalization, is of the EMT with respect to the internaliza- the defining gastrulation movement, which tion (preceding or following it) (Figure 1). transports the prospective mesodermal and Invagination is one type of emboly that occurs endodermal cells beneath the future ectoderm during gastrulation in D. melanogaster. Apical (Figure 1a–j). Epibolic movements spread constriction of ventral midline epithelial cells and thin germ layers (Figure 1d,e,k,l,m). creates a furrow where mesoderm folds inward Convergence movements narrow germ layers (Figure 1b,c) (Kam et al. 1991, Leptin & dorsolaterally/mediolaterally, whereas con- Roth 1994). As the ventral furrow (blastopore) current extension movements elongate them deepens, taking the nascent mesoderm deep anteroposteriorly (Figures 2 and 3). Impor- inside the embryo, cells break away from the by Universidad de Los Andes - Colombia on 10/04/12. For personal use only. tantly, the same morphogenetic transformation epithelium and start migrating on the internal Annu. Rev. Cell Dev. Biol. 2012.28. Downloaded from www.annualreviews.org of tissue, or each of these gastrulation move- layer of the future ectoderm. Involution is ments, can be achieved by various motile cell another example of internalization that pre- behaviors or a combination of cell behaviors. cedes EMT. In the extensively studied example Consequently, involvement of a specific gastru- of involution during frog gastrulation, the lation movement in a given animal species does prospective mesoderm and part of endoderm not imply the underlying cellular mechanism, form a cohesive tissue above the prospective which must be experimentally determined. blastopore (Keller 1981). Involution is heralded by apical constriction of so-called bottle
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