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A molecular atlas of the developing ectoderm defines neural, neural crest, placode, and nonneural progenitor identity in vertebrates
- Source :
- PLoS Biology, PLoS Biology, Public Library of Science, 2017, 15 (10), ⟨10.1371/journal.pbio.2004045⟩, PLoS biology, vol 15, iss 10, PLoS Biology, Vol 15, Iss 10, p e2004045 (2017)
- Publication Year :
- 2017
- Publisher :
- HAL CCSD, 2017.
-
Abstract
- During vertebrate neurulation, the embryonic ectoderm is patterned into lineage progenitors for neural plate, neural crest, placodes and epidermis. Here, we use Xenopus laevis embryos to analyze the spatial and temporal transcriptome of distinct ectodermal domains in the course of neurulation, during the establishment of cell lineages. In order to define the transcriptome of small groups of cells from a single germ layer and to retain spatial information, dorsal and ventral ectoderm was subdivided along the anterior-posterior and medial-lateral axes by microdissections. Principal component analysis on the transcriptomes of these ectoderm fragments primarily identifies embryonic axes and temporal dynamics. This provides a genetic code to define positional information of any ectoderm sample along the anterior-posterior and dorsal-ventral axes directly from its transcriptome. In parallel, we use nonnegative matrix factorization to predict enhanced gene expression maps onto early and mid-neurula embryos, and specific signatures for each ectoderm area. The clustering of spatial and temporal datasets allowed detection of multiple biologically relevant groups (e.g., Wnt signaling, neural crest development, sensory placode specification, ciliogenesis, germ layer specification). We provide an interactive network interface, EctoMap, for exploring synexpression relationships among genes expressed in the neurula, and suggest several strategies to use this comprehensive dataset to address questions in developmental biology as well as stem cell or cancer research.<br />Author summary Vertebrate embryo germ layers become progressively regionalized by evolutionarily conserved molecular processes. Catching the early steps of this dynamic spatial cell diversification at the scale of the transcriptome was challenging, even with the advent of efficient RNA sequencing. We have microdissected complementary and defined areas of a single germ layer, the developing ectoderm, and explored how the transcriptome changes over time and space in the ectoderm during the differentiation of frog epidermis, neural plate, and neural crest. We have created EctoMap, a searchable interface using these regional transcriptomes, to predict the expression of the 31 thousand genes expressed in neurulae and their networks of co-expression, predictive of functional relationships. Through several examples, we illustrate how these data provide insights in development, cancer, evolution and stem cell biology.
- Subjects :
- Xenopus
Gene Identification and Analysis
Xenopus laevis
Cell Signaling
Databases, Genetic
Biology (General)
Neurulation
WNT Signaling Cascade
ComputingMilieux_MISCELLANEOUS
Neurons
Stem Cells
Methods and Resources
Neural crest
Eukaryota
Genomics
[SDV.BIBS]Life Sciences [q-bio]/Quantitative Methods [q-bio.QM]
Neural Crest
Physical Sciences
Frogs
Stem Cell Research - Nonembryonic - Non-Human
General Agricultural and Biological Sciences
Neural plate
Microdissection
Statistics (Mathematics)
Network Analysis
QH301-705.5
1.1 Normal biological development and functioning
General Biochemistry, Genetics and Molecular Biology
Amphibians
03 medical and health sciences
Genetic
Genetics
Humans
Statistical Methods
Neural fold
Internet
Embryos
Gastrulation
Organisms
Biology and Life Sciences
Computational Biology
Wnt Proteins
030104 developmental biology
Neuroscience
Mathematics
Developmental Biology
0301 basic medicine
Embryology
Time Factors
Gene Expression
Ectoderm
Genetic Networks
Medical and Health Sciences
Mathematical and Statistical Techniques
Neoplasms
Cluster Analysis
Developmental
Gene Regulatory Networks
Pediatric
Principal Component Analysis
General Neuroscience
Gene Expression Regulation, Developmental
Animal Models
Biological Sciences
Signaling Cascades
medicine.anatomical_structure
Experimental Organism Systems
Vertebrates
embryonic structures
Transcriptome Analysis
Algorithms
Signal Transduction
Computer and Information Sciences
animal structures
Germ layer
Biology
Research and Analysis Methods
Databases
Model Organisms
Underpinning research
medicine
Animals
General Immunology and Microbiology
Agricultural and Veterinary Sciences
Gene Expression Profiling
Neurosciences
Cell Biology
Stem Cell Research
Genome Analysis
Gene Ontology
Neurula
Gene Expression Regulation
Multivariate Analysis
Transcriptome
Developmental biology
Subjects
Details
- Language :
- English
- ISSN :
- 15449173 and 15457885
- Database :
- OpenAIRE
- Journal :
- PLoS Biology, PLoS Biology, Public Library of Science, 2017, 15 (10), ⟨10.1371/journal.pbio.2004045⟩, PLoS biology, vol 15, iss 10, PLoS Biology, Vol 15, Iss 10, p e2004045 (2017)
- Accession number :
- edsair.doi.dedup.....4c29c8498f3ed3f9e48c63abcf2ec5de
- Full Text :
- https://doi.org/10.1371/journal.pbio.2004045⟩