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First published online December 22, 2008
doi: 10.1242/10.1242/dev.028407
Meeting Review |
1 Institut Curie, CNRS, UMR144, 26 rue d'Ulm, 75248 Paris Cedex 05,
France.
2 Center for Cell Dynamics, Friday Harbor Labs, University of Washington, 620
University Road, Friday Harbor, WA 98250, USA.
e-mail: yohanns.bellaiche{at}curie.fr and munroem{at}u.washington.edu
SUMMARY
A joint meeting of the Japanese and French societies for Developmental Biology, entitled `Frontiers in Developmental Biology', was recently held in Giens, France. The organizers, Patrick Lemaire and Shinichi Aizawa, showcased some of the rapid progress in the field that has been made possible through the use of modern large-scale network analyses, and of an increasingly sophisticated array of tools and ideas from microscopy, mathematics and computer science.
Introduction
This is an exciting time for developmental biologists as we move in earnest beyond describing gene expression patterns and gene functions to considering how gene networks specify cellular machinery, how this machinery operates within living cells to orchestrate the complex dynamics of animal development, and how it is tuned by evolution to carry out different tasks in different contexts. Armed with an ever-growing array of new technical capabilities and with influences from other scientific disciplines, we are venturing towards new frontiers in every direction. To highlight and promote this amazing progress, Patrick Lemaire (IBDML, Marseille France) and Shinichi Aizawa (Riken Center for Developmental Biology, Kobe, Japan) organized a special joint meeting of the Japanese and French Societies for Developmental Biology. For 4 days, participants gathered on a remote Mediterranean peninsula near the small French town of Hyeres to look into the future together and to describe what they see there. The themes that emerged most clearly were genetic regulatory networks (GRNs), morphogenesis and the interdisciplinary study of evolution and development.
Genetic networks and signaling pathways
The study of GRNs and signaling pathways is a central theme in developmental biology, and important findings were reported at the meeting that shed new light on the mechanisms by which GRNs and signaling cascades are employed during axis specification, somitogenesis and stem cell determination.
Axis specification
The specification of body axes is a process that is crucial for the correct
patterning of the embryonic body plan. Hiroshi Hamada (Osaka University,
Osaka, Japan) gave a keynote presentation on the mechanisms of anteroposterior
(AP) axis determination in mice. He illustrated that within the inner cell
mass of the early mouse embryo, the expression of Nodal, a transforming growth
factor β (TGFβ) family member, is sufficient to induce the
expression of its antagonist Lefty (Lefty1) in a cell population marked by the
presence of the transcription factor GATA6. This population then contributes
to the proximal region of the anterior visceral endoderm (AVE) and thereby
defines the AP axis of the mouse embryo. The interplay between Nodal and Lefty
was also shown to be important for the specification of the dorsoventral (DV)
axis in sea urchins. Thierry Lepage (Université Pierre et Marie Curie,
Villefranche-sur-Mer, France) convincingly illustrated that Nodal, which is
expressed early in the presumptive ventral ectoderm, controls DV patterning
(Duboc et al., 2004
). He
further described how its restricted expression could be explained by a
reaction diffusion model in which Nodal activates both its own expression and
that of its antagonist Lefty (Duboc et
al., 2008). Both Hamada's and Lepage's results suggest that
regulatory interactions between Nodal and Lefty provide a simple mechanism by
which a weak asymmetry in Nodal expression can be amplified and maintained to
stably define an embryonic axis. In further investigations of the mechanisms
of asymmetry in early mouse development, Naoto Ueno (National Institute for
Basic Biology, Okazaki, Japan) reported a novel and surprising function for
the planar cell polarity (PCP) gene Prickle1 in the regulation of
apicobasal polarity in the epiblast. Finally, Hidehiko Inomata (RIKEN Center
for Developmental Biology, Kobe, Japan) considered the mechanisms that
underlie the robustness of DV patterning in frog embryos. Recent work
implicates the local inhibition of chordin, a bone morphogenetic protein (BMP)
antagonist, by dorsally expressed BMP proteases in the regulation of DV
patterning. Inomata showed that the scaffold protein olfactomedin 1 (ONT1)
binds chordin and the chordin-degrading enzyme BMP1 through distinct domains,
with this binding enhancing chordin degradation. His work suggests that stable
axis formation depends on two compensatory regulatory pathways involving ONT1
and BMP1, on the one hand, and dorsally expressed BMPs (ADMP and BMP2), on the
other (Inomata et al.,
2008).
The molecular mechanisms that underlie left-right (LR) axis specification
were addressed in three talks, two of which highlighted the role of cilia in
this process. Hiroyuki Takeda (University of Tokyo, Tokyo, Japan), whose group
studies medaka development, described the characterization of the
kintoun (ktu) medaka mutant, which is defective in both
ciliary motility and LR axis specification
(Omran et al., 2009).
Positional cloning of the ktu gene identified a novel gene that is
essential for ciliary motility from algae to humans. ktu encodes a
protein that is required in the cytoplasm for the pre-assembly of dynein arm
complexes, the mutation of which causes primary ciliary dyskinesia. Moving
from fish to mice, Hamada showed in his keynote address that PCP signaling
determines the posterior positioning of basal bodies in the epithelial cells
of the node, which in turn determines the posterior tilt of nodal cilia
required for directed flows and LR axis specification. Finally,
Stéphane Noselli (Université de Nice, Nice, France) presented
his recent findings on LR axis specification in Drosophila. Here, the
LR axis is manifested by the direction of the 360° rotation of the male
genitalia. Using time-lapse imaging, Noselli and his colleagues showed that
the 360° genitalia rotation can be decomposed into two concomitant
180° rotations of the anterior and posterior regions of the genitalia A8
segment, with the directions of both rotations being controlled by the LR
determinant myosin 1D.
Global control mechanisms
A trio of talks dealt with mechanisms that coordinate the expression of
multiple genes during development. Two of these focused on Hox transcription
factor genes, which are arranged in clusters in the genome. Hox gene
transcription can be activated according to the spatial arrangement of the
genes on the chromosomes, a phenomenon known as colinearity. The expression of
Hox genes is tightly regulated, with the Polycomb Group (PcG) family of
proteins being one of the most prominent repressors. Denis Duboule (University
of Geneva, Geneva, Switzerland; Federal Institute of Technology, Lausanne,
Switzerland) discussed the developmental and evolutionary significance of Hox
gene colinearity. He illustrated how a global control region (GCR) located
proximal to one of the Hox gene clusters acts as a module to drive the
expression of Hox genes according to their position within the Hox cluster
during vertebrate AP axis specification, digit determination and external
genitalia development (Montavon et al.,
2008; Tarchini et al.,
2006; Cobb and Duboule,
2005). Giacomo Cavalli (Institute of Human Genetics, Montpellier,
France) reported important findings on the mechanisms that maintain Hox gene
expression patterns during Drosophila embryogenesis. He showed that
Hox genes from different clusters, located on different chromosomes,
colocalize within nuclear PcG bodies when they are co-repressed, but localize
to different nuclear positions when differentially expressed. His work
illustrates how the binding of a PcG repressor to PcG response elements can
promote the long-range chromosome organization necessary for the maintenance
of Hox expression patterns during embryogenesis. Finally, Mirana Ramialison
(European Molecular Biology Laboratory, Heidelberg, Germany) reported the
systematic identification of groups of spatially co-expressed genes, so-called
synexpression groups, and their corresponding cis-regulatory regions through a
bioinformatics analysis of the Medaka Expression Pattern Database. Her
analysis also revealed the chromosomal clustering of co-expressed genes,
hinting at the existence of novel GCRs that could play a fundamental role
during development.
|
;
Dequeant et al., 2006), has
emerged as a central model for studying how temporal information (the
segmentation clock) is transformed into spatial regulation (the formation of
somites along the AP axis). Emilie Delaune (Laboratory of Sharon Amacher,
University of California at Berkeley, CA, USA) reported the development and
use of a Notch target GFP reporter in zebrafish to visualize the segmentation
clock at cellular resolution, enabling a detailed analysis of how neighboring
cells, which express Notch target genes, are coordinated to form a somite.
Yumiko Saga (National Institute of Genetics, Mishima, Japan) presented her
recent findings on how interactions among Notch and the transcription factors
Mesp2 and Tbx6 iteratively define segmental borders and rostrocaudal pattern
within forming somites. She showed that Notch signaling (a temporal factor)
and Tbx6 (a spatial factor) cooperate to promote Mesp2 expression within a
domain that prefigures the somite. Mesp2, in turn, suppresses Tbx6 expression
via the ubiquitin-proteasome pathway to define the anterior border of the next
Mesp2 domain (Fig. 1)
(Oginuma et al., 2008). From
these data, Yumiko Saga proposed Mesp2 to be the final output signal through
which the translation from temporal information into spatial regulation
occurs.
Stem cells
Several talks dealt with GRNs in the context of stem cell specification
and/or maintenance. The elegant work of Cédric Maurange and colleagues
(National Institute for Medical Research, London, UK) addressed the
fundamental issue of how stem cells `decide' to stop dividing once sufficient
numbers of neurons have been produced
(Maurange et al., 2008). In
Drosophila, neural progenitors express a temporal sequence of
distinct transcription factors that endow their progeny neurons with different
identities. Maurange reported that progression to the end of this sequence is
necessary to promote cell cycle exit and stem cell apoptosis, explaining how
the correct number of neurons with a given fate is produced during development
(Fig. 2). Moving from
Drosophila to mice, Daijiro Konno (RIKEN Center for Developmental
Biology, Kobe, Japan) addressed the long-standing issue of the role of mitotic
spindle orientation in brain neurogenesis in mice
(Konno et al., 2008).
Combining time-lapse microscopy with genetic perturbations of spindle
orientation in the mouse cortex, he showed that during asymmetric divisions of
neural progenitors, the maintenance of progenitor identity and proliferative
potential correlates with the inheritance of the basal process.
Large-scale genetic network analysis
Four talks illustrated ways in which large-scale network analyses can yield
fundamental insights into developmental mechanisms. Norbert Perrimon (Harvard
Medical School, Boston, MA, USA) reviewed his ongoing work on the structure
and complexity of signaling networks, suggesting that the notion of discrete
modular pathways (Wnt, Hedgehog, Notch, etc.) may be overly simplified.
Instead, he argued that the transmission of an external signal involves
hundreds of satellite proteins surrounding the more limited `canonical' sets
identified by classical genetic approaches, with these satellite members of
signaling networks making quantitative contributions to the network output.
Whereas mutations with the highest contribution lead to a complete collapse of
network function, the effects of mutations in components associated with more
subtle functions are compensated. This model has implications: (1) for
understanding how the genetic background influences variation in expressivity;
(2) for the characterization of susceptibility loci associated with complex
diseases such as cancer, diabetes and neurodegeneration; and (3) for the
robustness and evolvability of signaling networks. Marc Vidal (Harvard
University, Cambridge, MA, USA) described his ongoing efforts towards the
construction and analysis of comprehensive protein-protein interaction
networks, drawing on examples from humans, yeast and worms. He illustrated
some of the ways in which this analysis can yield fundamental biological
insights. For example, he showed how combining global network analysis with
protein and transcription profiling can help to identify susceptibility loci
associated with cancer.
|
). He
showed that cardiac cell migration is controlled through the transcriptional
regulation of effector genes involved in most cellular processes that are
required for directed migration, including polarity, membrane protrusion and
cell-matrix adhesion. His work hints at how complex morphogenetic behaviors
could arise through the combinatorial activation of conserved cellular modules
by tissue-specific GRNs.
Asymmetric cell division in C. elegans
Understanding the cellular dynamics that underlie the asymmetrical
inheritance of developmental potential is an important issue in the
development of multicellular organisms, and three talks focused on the C.
elegans zygote as a model system in which to analyze this. Asako Sugimoto
(RIKEN Center for Developmental Biology, Kobe, Japan) presented a beautiful
analysis of P-granule (germ granule) assembly in C. elegans. She
showed that among 14 previously identified P-granule components, two (PGL-1
and PGL-3) are sufficient to form granules when expressed in cultured
mammalian cells. The granules that formed contained endogenous poly(A)-binding
protein and mRNA, sequestered some of the other co-expressed P-granule
components and had a layered structure that is also found in C.
elegans P-granules. These studies provide an exciting first glimpse of
the dynamic principles that govern germ granule self-assembly in C.
elegans and in other organisms. Francois Nedelec (EMBL, Heidelberg,
Germany) described elegant work in which he and his colleagues used direct
high-resolution observations of microtubule dynamics in the C.
elegans zygote to identify novel feedback interactions between
microtubule dynamics and spindle pole motions (Koslowski et al., 2007). They
then used detailed computer simulations to show how these feedback
interactions could explain the spindle pole oscillations and AP displacements
that are observed during asymmetric cell divisions. Ed Munro (Center for Cell
Dynamics, University of Washington, WA, USA) described using a similar
synthesis of models and experiments to explore how a system of biochemical and
mechanical interactions among the generally asymmetrically localized Par
proteins, small GTPases and the actomyosin cytoskeleton could explain the
zygote's ability to form and stabilize polarized cortical domains in response
to a transient polarizing cue. These studies emphasize how the factors that
regulate force generation in embryonic cells are often redistributed by the
very forces they control.
Morphogenesis and pattern formation
Morphogenesis remains one of the most fascinating but poorly understood
processes in developmental biology. However, new efforts and approaches are
beginning to lead towards a more functional and mechanistic understanding of
the underlying processes. Bénédicte Charrier (UPMC, Paris,
France) and Bernard Billoud (Centre National de la Recherche Scientifique
(CNRS), Roscoff, France) described the use of a simple cellular automata model
- in which a finite number of states are assigned to the cells of a grid and
through which interactions between groups of grid cells can be studied - to
explore how different empirically derived rules or hypotheses about local cell
growth, division and differentiation, and their modulation by cell-cell
communication could explain multicellular patterns observed during the
development of the filamentous brown alga Ectocarpus siliculosus. In
plants, Jan Traas (Ecole Normale Supérieure de Lyon, CNRS-Institut
National de la Recherche Agronomique, Lyon, France) illustrated how growth
seems to be partially coordinated by a cytoskeleton-based sensing of stress in
tissues. Computer simulations show that such a mechanism would be sufficient
to generate the shape changes observed during organogenesis in plants.
Anne-Gaëlle Rolland-Lagan (University of Ottawa, Ottawa, Canada)
emphasized the need for quantitative descriptions of pattern formation as a
starting point for the construction and analysis of theoretical models. To
this end, she described a suite of algorithms that she is developing to
quantify and analyze leaf vein patterns at high spatial resolution. Moving
from plants to animals, Thomas Lecuit (CNRS-Institut de Biologie du
Développement de Marseille Luminy, Marseille, France) described recent
collaborative work with physicist Pierre-François Lenne (CNRS-Institut
Fresnel, Marseille, France) that combines computer simulations and physical
perturbations to show how anisotropic tension governed by the local bipolar
recruitment of Myosin 2 could explain cell intercalation and tissue elongation
during Drosophila gastrulation
(Rauzi et al., 2008). He
emphasized a key role for dynamic adhesive contacts during cell rearrangement
(Cavey et al., 2008) and showed
that bipolar recruitment of Myosin relies on a spatial bias in branched versus
unbranched actin network assembly mediated by Scar and Diaphanous, two
regulators of actin polymerization. Francois Robin (IBDML, Marseille, France)
described joint work with Kristin Sherrard (Center for Cell Dynamics,
University of Washington, WA, USA) that identifies a two-step mechanism for
ascidian endoderm invagination: apical constriction and columnarization
followed by basolateral shortening around tight apical collars. This is
accompanied by the sequential accumulation of active myosin at apical and then
basolateral surfaces. Using a detailed computational model, they showed that
this two-step mechanism could account robustly for the dynamics of cell shape
change and tissue deformation that are seen during invagination. Yohanns
Bellaïche (Institut Curie, Paris, France) analyzed the mechanisms that
coordinate growth and morphogenesis in proliferating epithelia. Using novel
mathematical tools to quantify the morphometric effects of cell division and
cell growth. This work underscores an essential need to understand the
interplay between cell cycle control and morphogenesis.
Finally, Shigeru Kondo (Nagoya University, Nagoya, Japan) presented an elegant analysis of pigmentation patterns in zebrafish. He showed that empirically determined rules for interactions among distinct pigment cell types (melanophores and xanthophores) fulfill all the requirements for a classical Turing-style pattern-formation mechanism. He showed further that this basic mechanism can explain the dynamics of pattern formation observed in wild-type and in many mutant embryos or hybrid combinations.
Evolutionary developmental biology
Last, but not least, a very exciting session showcased some new approaches
and recent progress in understanding the evolution of developmental
mechanisms. Per Ahlberg (Uppsala University, Uppsala, Sweden) discussed how
fossil data can be used to sharpen inferences about the evolution of
developmental mechanisms made from the comparative study of living taxa,
drawing on his recent studies of digit homologies and the neural crest origins
of the neck and shoulder (Boisvert et al.,
2008; Matsuoka et al.,
2005). He highlighted the need to reconstruct soft anatomy from
fossil data as a key challenge, because it is the soft anatomy, not bone
morphology, that correlates most strongly with developmental boundaries. He
presented a novel and exciting approach that uses sub-micron resolution
synchrotron scans to map muscle attachments to fossil bones in 3D that holds
great promise for soft-tissue reconstructions in many other contexts. Shigeru
Kuratani (RIKEN Center for Developmental Biology, Kobe, Japan) discussed the
rib-derived turtle carapace as an evolutionary novelty, which results from the
arrest and dorsolateral confinement of rib growth, leading to a
turtle-specific infolding of the lateral body wall
(Nagashima et al., 2007). He
showed that the carapacial ridge - a turtle-specific structure that lies along
the line of infolding - does not play an inductive role in carapace patterning
as previously thought, but instead appears to have co-opted elements of the
Wnt signaling pathway for the control of carapace growth.
Marie-Anne Félix (Institut Jacques Monod. INRS-UPMC, Paris, France)
described an elegant quantitative analysis of robustness and evolvability of
vulval patterning in C. elegans and related species. She showed that
vulval patterning is buffered against both genetic and environmental
variation; the errors that do occur depend on both genotype and environmental
conditions. This buffering appears to have allowed extensive cryptic evolution
of the vulval patterning network within the Caenorhabditis genus,
associated with quantitative changes in the Notch and EGF signaling pathways
(Félix, 2007;
Braendle and Félix,
2008; Milloz et al.,
2008). Claude Desplan (New York University, New York, NY, USA)
presented his beautiful work on AP patterning in the wasp Nasonia.
Nasonia, like most insects, lacks the morphogen Bicoid, which establishes
anterior identity in Drosophila. He showed that several highly
conserved genes (orthodenticle, caudal and giant) are
localized as mRNA in the Nasonia egg and that together they subsume
the various functions of Bicoid (Brent et
al., 2007; Lynch et al.,
2006). Both talks emphasized how, by tinkering with the same
toolkit of genes and preserving most of their interactions, nature tunes GRNs
to preserve similar functions under different conditions.
Other talks emphasized how similar tinkering can lead to evolutionary
innovation. Benjamin Prud'homme (IBDML, Marseille, France) discussed his
recent work with colleagues Nicolas Gompel and Sean Carroll, which identifies
the molecular bases for the evolution of male specific Drosophila
wing pigmentation patterns (Prud'homme et
al., 2006). He showed how these patterns have been modified by
changing specific cis-regulatory elements of pigmentation gene, leading to the
co-option of pre-patterned regulatory inputs from wing-development genes such
as engrailed. Jessica Cande (UC Berkeley, Berkeley, CA, USA) reported
two changes in the GRN that underlies heart formation in beetles: one is a
gain in an expression domain of tinman; the other is a switch in the
expression patterns of two neighboring genes that appears to be
morphologically silent. Francois Parcy (CNRS Grenoble, France) discussed
insights into the origins of angiospermy that were gained from the analysis of
LEAFY - a key regulator of floral development whose DNA-bound structure has
recently been determined (Hamès et
al., 2008). Homology modeling and biochemical analyses suggest
that variations in the DNA-binding specificities of LEAFY and its interactions
with other binding partners may have contributed to the appearance of
flowers.
Conclusions
The future challenge in developmental biology is obvious: to integrate the increasingly sophisticated characterizations of GRNs and signaling pathways with the emerging physical descriptions of the cell behaviors that underlie pattern formation and morphogenesis. Using genome-wide gene profiling to identify points of regulatory control across this interface is a key step. But it will be equally important to understand the targets of this control - to understand the dynamics of embryonic cell behavior from a physical perspective and how local cell behaviors are integrated across tissue scales during pattern formation and morphogenesis. This meeting highlighted some of the many ways in which researchers are beginning to take a more interdisciplinary approach to developmental biology, combining classical molecular genetics with novel methods for imaging and physical perturbation, quantitative analysis, physical modeling and computer simulation, thus offering a glimpse of how the field is likely to develop in the near future.
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