dictyNews
Electronic Edition
Volume 40, number 21
August 29, 2014
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Abstracts
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Arrestins function in cAR1 GPCR-mediated signaling and cAR1
internalization in the development of D. discoideum
Xiumei Cao1, #, Jianshe Yan1, 2, #, *, Shi Shu3, Joseph A. Brzostowski4,
and Tian Jin2, *
Mol. Biol. Cell mbc.E14-03-0834;
First Published on August 20, 2014;doi:10.1091/mbc.E14-03-0834
1. Shanghai Institute of Immunology, Shanghai Jiao Tong University
School of Medicine, Shanghai, 200025, China
2. Chemotaxis Signal Section, Laboratory of Immunogenetics, National
Institute of Allergy and Infectious Diseases, National Institutes of Health,
Rockville, MD 20852, USA
3. Laboratory of Cell Biology, National Heart, Lung and Blood Institute,
National Institutes of Health, Bethesda, MD 20892, USA
4. Laboratory of Immunogenetics Imaging Facility, National Institute of
Allergy and Infectious Diseases, National Institutes of Health, Rockville,
MD 20852, USA
Oscillation of chemical signals is a common biological phenomenon but
its regulation is poorly understood. At the aggregation stage of Dictyostelium
discoideum development, the chemoattractant cAMP is synthesized and
released at 6 min intervals, directing cell migration. Although the G protein-
coupled cAMP receptor cAR1 and ERK2 are both implicated in regulating the
oscillation, the signaling circuit remains unknown. Here, we report that
D. discoideum arrestins regulate the frequency of cAMP oscillation and may
link cAR1 signaling to oscillatory ERK2 activity. Cells lacking arrestins (adcB-C-)
display cAMP oscillations during the aggregation stage that are twice as frequent
as wild type cells. The adcB-C- cells also have a shorter period of transient
ERK2 activity and precociously reactivate ERK2 in response to cAMP stimulation.
We show that AdcC associates with ERK2 and that activation of cAR1 promotes
the transient membrane recruitment of AdcC and interaction with cAR1, indicating
that arrestins function in cAR1-controlled periodic ERK2 activation and oscillatory
cAMP signaling in the aggregation stage of D. discoideum development. In
addition, ligand-induced cAR1 internalization is compromised in adcB-C- cells,
suggesting that arrestins are involved in elimination of high-affinity cAR1 receptors
from cell surface after the aggregation stage of multicellular development.
Submitted by Jianshe Yan [[log in to unmask]]
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An evolutionarily significant unicellular strategy in response to starvation
stress in Dictyostelium social amoebae
Darja Dubravcic [1,2], Minus van Baalen [2], Clément Nizak [1,3]
1 CNRS, LIPHY, F-38000 Grenoble, France
2 Laboratory of Ecology and Evolution, CNRS UMR7625, Ecole Normale
Supérieure, Université Pierre et Marie Curie, Paris Universitas, CNRS,
Paris, France
3 Laboratory of Biochemistry, UMR 8231 ESPCI ParisTech/CNRS,
PSL Research University, Paris, France
F1000research, accepted
http://f1000research.com/articles/3-133/v1#article-reports
The social amoeba Dictyostelium discoideum is widely studied for its
multicellular development program as a response to starvation and constitutes
a model of choice in microbial cooperation studies. Aggregates of up to 106
cells form fruiting bodies containing two cell types: (i) dormant spores (~80%)
that can persist for months in the absence of nutrients, and (ii) dead stalk cells
(~20%) that promote the dispersion of the spores towards nutrient-rich areas.
It is often overlooked that not all cells aggregate upon starvation. Using a new
quantitative approach based on time-lapse fluorescence microscopy and a low
ratio of reporting cells, we have quantified this fraction of non-aggregating cells.
In realistic starvation conditions, up to 15% of cells do not aggregate, which
makes this third cell fate a significant component of the population-level response
of social amoebae to starvation. Non-aggregating cells have an advantage over
cells in aggregates since they resume growth earlier upon arrival of new nutrients,
but have a shorter lifespan under prolonged starvation. We find that phenotypic
heterogeneities linked to cell nutritional state bias the representation of cells in the
aggregating vs. non-aggregating fractions, and thus regulate population partitioning.
Next, we report that the fraction of non-aggregating cells depends on genetic factors
that regulate the timing of starvation, signal sensing efficiency and aggregation
efficiency. In addition, interactions between clones in mixtures of non-isogenic
cells affect the partitioning of each clone into both fractions. We further test the
evolutionary significance of the non-aggregating cell fraction. The partitioning of
cells into aggregating and non-aggregating fractions is optimal in fluctuating
environments with an unpredictable duration of starvation periods. D. discoideum
thus constitutes a model system lying at the intersection of microbial cooperation
and bet hedging, defining a new frontier in microbiology and evolution studies
Submitted by Clement Nizak [[log in to unmask]]
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Evolutionary reconstruction of pattern formation in 98 Dictyostelium species
reveals that cell-type specialization by lateral inhibition is a derived trait
Christina Schilde, Anna Skiba and Pauline Schaap
College of Life Sciences, University of Dundee, UK
EvoDevo, in press
BACKGROUND Multicellularity provides organisms with opportunities for
cell-type specialization, but requires novel mechanisms to position correct
proportions of different cell types throughout the organism. Dictyostelid social
amoebas display an early form of multicellularity, where amoebas aggregate
to form fruiting bodies, which contain only spores or up to four additional cell-
types. These cell types will form the stalk and support structures for the stalk
and spore head. Phylogenetic inference subdivides Dictyostelia into four
major groups, with the model organism D.discoideum residing in group 4.
Differentiation of its five cell types is dominated in D.discoideum by lateral
inhibition-type mechanisms that trigger scattered cell differentiation, with
tissue patterns being formed by cell sorting.
RESULTS To reconstruct the evolution of pattern formation in Dictyostelia, we
used cell-type specific antibodies and promoter-reporter fusion constructs to
investigate pattern formation in 98 species that represent all groupings. Our
results indicate that in all early diverging Dictyostelia and most members of
groups 1-3, cells differentiate into maximally two cell types, prestalk and
prespore cells, with pattern formation being dominated by position-dependent
transdifferentiation of prespore cells into prestalk cells. In clade 2A, prestalk and
stalk cell differentiation are lost and the prespore cells construct an acellular stalk.
Group 4 species set aside correct proportions of prestalk and prespore cells early
in development, and differentiate into up to three more supporting cell types.
CONCLUSIONS Our experiments show that positional transdifferentiation is the
ancestral mode of pattern formation in Dictyostelia. The early specification of a
prestalk population equal to the number of stalk cells is a derived trait that
emerged in group 4 and a few late diverging species in the other groups.
Group 4 spore masses are larger than those of other groups and the differentiation
of supporting cell types by lateral inhibition may have facilitated this increase in
size. The signal DIF-1, which is secreted by prespore cells, triggers differentiation
of supporting cell types. The synthesis and degradation of DIF-1 were shown to
be restricted to group 4. This suggests that the emergence of DIF-1 signalling
caused increased cell-type specialization in this group.
Submitted by Christina Schilde [[log in to unmask]]
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[End dictyNews, volume 40, number 21]
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