The DOI matches its Crossref record.
Cell shape changes during gastrulation in Drosophila
Abstract
The first morphogenetic movement during Drosophila development is the invagination of the mesoderm, an event that folds a one-layered epithelium into a multilayered structure. In this paper, we describe the shape changes and behaviour of the cells participating in this process and show how mutations that change cell fate affect this behaviour. We divide the formation of the mesodermal germ layer into two phases. During the first phase, the ventral epithelium folds into a tube by a series of concerted cell shape changes (ventral furrow formation). Based on the behaviour of cells in this phase, we conclude that the prospective mesoderm is not a homogeneous cell population, but consists of two subpopulations. Each subpopulation goes through a distinctive sequence of specific cell shape changes which together mediate the invagination of the ventral furrow. In the second phase, the invaginated tube of mesoderm loses its epithelial character, the mesoderm cells disperse, divide and then spread out along the ectoderm to form a single cell layer. To test how ventral furrow formation depends on cell fates in the mesoderm and in neighbouring cells we alter these fates genetically using maternal and zygotic mutations. These experiments show that some of the aspects of cell behaviour specific for ventral furrow cells are part of an autonomous differentiation programme. The force driving the invagination is generated within the region of the ventral furrow, with the lateral and dorsal cell populations contributing little or none of the force. Two known zygotic genes that are required for the formation of the mesoderm, twist and snail, are expressed in ventral furrow cells, and the correct execution of cell shape changes in the mesoderm depends on both. Finally, we show that the region where the ventral furrow forms is determined by the expression of mesoderm-specific genes, and not by mechanical or other epigenetic properties of the egg.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cited by
Nieto, M. A., Huang, R. Y.-J., Jackson, R. A., & Thiery, J. P. (2016) · Cell · doi:10.1016/j.cell.2016.06.028 · Cited by 4,492
Batlle, E., Sancho, E., Francí, C., Domínguez, D., Monfar, M., Baulida, J., & García de Herreros, A. (2000) · Nature Cell Biology · doi:10.1038/35000034 · Cited by 2,666
The origin of pattern and polarity in the Drosophila embryo
Johnston, D. S., & Nüsslein-Volhard, C. (1992) · Cell · doi:10.1016/0092-8674(92)90466-p · Cited by 1,361
Pulsed contractions of an actin–myosin network drive apical constriction
Martin, A. C., Kaschube, M., & Wieschaus, E. F. (2009) · Nature · doi:10.1038/nature07522 · Cited by 1,245
Mechanotransduction in development: a growing role for contractility
Wozniak, M. A., & Chen, C. S. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2592 · Cited by 818
Rhyu, M. S., Jan, L. Y., & Jan, Y. N. (1994) · Cell · doi:10.1016/0092-8674(94)90112-0 · Cited by 767
Epithelial-mesenchymal transitions: insights from development
Lim, J., & Thiery, J. P. (2012) · Development · doi:10.1242/dev.071209 · Cited by 661
Force Generation, Transmission, and Integration during Cell and Tissue Morphogenesis
Lecuit, T., Lenne, P.-F., & Munro, E. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100109-104027 · Cited by 621
twist and snail as positive and negative regulators during Drosophila mesoderm development.
Leptin, M. (1991) · Genes & Development · doi:10.1101/gad.5.9.1568 · Cited by 566
Self-citationHow we are shaped: The biomechanics of gastrulation
Keller, R., Davidson, L. A., & Shook, D. R. (2003) · Differentiation · doi:10.1046/j.1432-0436.2003.710301.x · Cited by 494
Irvine, K. D., & Wieschaus, E. (1994) · Development · doi:10.1242/dev.120.4.827 · Cited by 466
Apical constriction: A cell shape change that can drive morphogenesis
Sawyer, J. M., Harrell, J. R., Shemer, G., Sullivan-Brown, J., Roh-Johnson, M., & Goldstein, B. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2009.09.009 · Cited by 448
Transitions between epithelial and mesenchymal states in development and disease
Baum, B., Settleman, J., & Quinlan, M. P. (2008) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2008.02.001 · Cited by 398
The dorsal morphogen gradient regulates the mesoderm determinant twist in early Drosophila embryos.
Jiang, J., Kosman, D., Ip, Y. T., & Levine, M. (1991) · Genes & Development · doi:10.1101/gad.5.10.1881 · Cited by 365
The drosophila gastrulation gene concertina encodes a Gα-like protein
Parks, S., & Wieschaus, E. (1991) · Cell · doi:10.1016/0092-8674(91)90652-f · Cited by 327
Programmed and self-organized flow of information during morphogenesis
Collinet, C., & Lecuit, T. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-00318-6 · Cited by 322
Costa, M., Wilson, E. T., & Wieschaus, E. (1994) · Cell · doi:10.1016/0092-8674(94)90384-0 · Cited by 318
Exploring a New Twist on Tumor Metastasis
Yang, J., Mani, S. A., & Weinberg, R. A. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3850 · Cited by 297
Fehon, R. G., Johansen, K., Rebay, I., & Artavanis-Tsakonas, S. (1991) · The Journal of cell biology · doi:10.1083/jcb.113.3.657 · Cited by 295
Gisselbrecht, S., Skeath, J. B., Doe, C. Q., & Michelson, A. M. (1996) · Genes & Development · doi:10.1101/gad.10.23.3003 · Cited by 292
A core transcriptional network for early mesoderm development in Drosophila melanogaster
Sandmann, T., Girardot, C., Brehme, M., Tongprasit, W., Stolc, V., & Furlong, E. E. M. (2007) · Genes & Development · doi:10.1101/gad.1509007 · Cited by 286
Chapter 30 In Situ Hybridization to RNA
Lehmann, R., & Tautz, D. (1994) · Methods in Cell Biology · doi:10.1016/s0091-679x(08)60933-4 · Cited by 282
Myogenesis: A View from Drosophila
Baylies, M. K., Bate, M., & Gomez, M. R. (1998) · Cell · doi:10.1016/s0092-8674(00)81198-8 · Cited by 274
Rutledge, B. J., Zhang, K., Bier, E., Jan, Y. N., & Perrimon, N. (1992) · Genes & Development · doi:10.1101/gad.6.8.1503 · Cited by 274
Oncogenic cooperation between H-Twist and N-Myc overrides failsafe programs in cancer cells
Valsesia-Wittmann, S., Magdeleine, M., Dupasquier, S., Garin, E., Jallas, A.-C., Combaret, V., Krause, A., Leissner, P., & Puisieux, A. (2004) · Cancer Cell · doi:10.1016/j.ccr.2004.09.033 · Cited by 270
Establishment of the Mesoderm-Neuroectoderm Boundary in the Drosophila Embryo
Kosman, D., Ip, Y. T., Levine, M., & Arora, K. (1991) · Science · doi:10.1126/science.1925551 · Cited by 243
Graded dorsal and differential gene regulation in the Drosophila embryo.
Reeves, G. T., & Stathopoulos, A. (2009) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a000836 · Cited by 119
msh may play a conserved role in dorsoventral patterning of the neuroectoderm and mesoderm
D'Alessio, M., & Frasch, M. (1996) · Mechanisms of Development · doi:10.1016/s0925-4773(96)00583-7 · Cited by 126
Steiner, F. A., Talbert, P. B., Kasinathan, S., Deal, R. B., & Henikoff, S. (2012) · Genome Research · doi:10.1101/gr.131748.111 · Cited by 123
Raz, E., & Shilo, B. Z. (1993) · Genes & Development · doi:10.1101/gad.7.10.1937 · Cited by 113
Kadam, S., McMahon, A., Tzou, P., & Stathopoulos, A. (2009) · Development · doi:10.1242/dev.027904 · Cited by 83
Hecht, P. M., & Anderson, K. V. (1993) · Genetics · doi:10.1093/genetics/135.2.405 · Cited by 80
Ventralizing signal determined by protease activation in Drosophila embryogenesis
Smith, C. L., & DeLotto, R. (1994) · Nature · doi:10.1038/368548a0 · Cited by 75
Spätzle regulates the shape of the Dorsal gradient in the Drosophila embryo
Morisato, D. (2001) · Development · doi:10.1242/dev.128.12.2309 · Cited by 46
Regulation of spatiotemporal limits of developmental gene expression via enhancer grammar
Keller, S. H., Jena, S. G., Yamazaki, Y., & Lim, B. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1917040117 · Cited by 36
Metadata
- Authors
- Leptin, M., & Grunewald, B.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 1990-09-01
- Volume
- 110
- Issue
- 1
- Pages
- 73-84
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W1866991157
- Cited by
- 518
- References
- 0
- FWCI
- 7.29
- Type
- journal article
- Language
- en
- Open access
- closed
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.
