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Article ; Online: Increased sugar valuation contributes to the evolutionary shift in egg-laying behavior of the fruit pest Drosophila suzukii.

Cavey, Matthieu / Charroux, Bernard / Travaillard, Solène / Manière, Gérard / Berthelot-Grosjean, Martine / Quitard, Sabine / Minervino, Caroline / Detailleur, Brice / Grosjean, Yaël / Prud'homme, Benjamin

PLoS biology

2023 Volume 21, Issue 12, Page(s) e3002432

Abstract: Behavior evolution can promote the emergence of agricultural pests by changing their ecological niche. For example, the insect pest Drosophila suzukii has shifted its oviposition (egg-laying) niche from fermented fruits to ripe, non-fermented fruits, ... ...

Abstract	Behavior evolution can promote the emergence of agricultural pests by changing their ecological niche. For example, the insect pest Drosophila suzukii has shifted its oviposition (egg-laying) niche from fermented fruits to ripe, non-fermented fruits, causing significant damage to a wide range of fruit crops worldwide. We investigate the chemosensory changes underlying this evolutionary shift and ask whether fruit sugars, which are depleted during fermentation, are important gustatory cues that direct D. suzukii oviposition to sweet, ripe fruits. We show that D. suzukii has expanded its range of oviposition responses to lower sugar concentrations than the model D. melanogaster, which prefers to lay eggs on fermented fruit. The increased response of D. suzukii to sugar correlates with an increase in the value of sugar relative to a fermented strawberry substrate in oviposition decisions. In addition, we show by genetic manipulation of sugar-gustatory receptor neurons (GRNs) that sugar perception is required for D. suzukii to prefer a ripe substrate over a fermented substrate, but not for D. melanogaster to prefer the fermented substrate. Thus, sugar is a major determinant of D. suzukii's choice of complex substrates. Calcium imaging experiments in the brain's primary gustatory center (suboesophageal zone) show that D. suzukii GRNs are not more sensitive to sugar than their D. melanogaster counterparts, suggesting that increased sugar valuation is encoded in downstream circuits of the central nervous system (CNS). Taken together, our data suggest that evolutionary changes in central brain sugar valuation computations are involved in driving D. suzukii's oviposition preference for sweet, ripe fruit.
MeSH term(s)	Animals ; Female ; Drosophila/physiology ; Drosophila melanogaster/physiology ; Oviposition ; Fruit ; Drosophila Proteins/genetics ; Sugars
Chemical Substances	Drosophila Proteins ; Sugars
Language	English
Publishing date	2023-12-11
Publishing country	United States
Document type	Journal Article
ZDB-ID	2126776-5
ISSN	1545-7885 ; 1544-9173
ISSN (online)	1545-7885
ISSN	1544-9173
DOI	10.1371/journal.pbio.3002432
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Article ; Online: Circadian rhythms in neuronal activity propagate through output circuits.

Cavey, Matthieu / Collins, Ben / Bertet, Claire / Blau, Justin

Nature neuroscience

2016 Volume 19, Issue 4, Page(s) 587–595

Abstract: Twenty-four hour rhythms in behavior are organized by a network of circadian pacemaker neurons. Rhythmic activity in this network is generated by intrinsic rhythms in clock neuron physiology and communication between clock neurons. However, it is poorly ... ...

Abstract	Twenty-four hour rhythms in behavior are organized by a network of circadian pacemaker neurons. Rhythmic activity in this network is generated by intrinsic rhythms in clock neuron physiology and communication between clock neurons. However, it is poorly understood how the activity of a small number of pacemaker neurons is translated into rhythmic behavior of the whole animal. To understand this, we screened for signals that could identify circadian output circuits in Drosophila melanogaster. We found that leucokinin neuropeptide (LK) and its receptor (LK-R) were required for normal behavioral rhythms. This LK/LK-R circuit connects pacemaker neurons to brain areas that regulate locomotor activity and sleep. Our experiments revealed that pacemaker neurons impose rhythmic activity and excitability on LK- and LK-R-expressing neurons. We also found pacemaker neuron-dependent activity rhythms in a second circadian output pathway controlled by DH44 neuropeptide-expressing neurons. We conclude that rhythmic clock neuron activity propagates to multiple downstream circuits to orchestrate behavioral rhythms.
MeSH term(s)	Animals ; Animals, Genetically Modified ; Biological Clocks/physiology ; Circadian Rhythm/physiology ; Drosophila Proteins/analysis ; Drosophila Proteins/biosynthesis ; Drosophila melanogaster ; Male ; Motor Activity/physiology ; Nerve Net/chemistry ; Nerve Net/physiology ; Neurons/chemistry ; Neurons/physiology
Chemical Substances	Drosophila Proteins
Language	English
Publishing date	2016-02-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1420596-8
ISSN	1546-1726 ; 1097-6256
ISSN (online)	1546-1726
ISSN	1097-6256
DOI	10.1038/nn.4263
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Article ; Online: Evolution of Ovipositor Length in Drosophila suzukii Is Driven by Enhanced Cell Size Expansion and Anisotropic Tissue Reorganization.

Green, Jack E / Cavey, Matthieu / Médina Caturegli, Emmanuelle / Aigouy, Benoit / Gompel, Nicolas / Prud'homme, Benjamin

Current biology : CB

2019 Volume 29, Issue 12, Page(s) 2075–2082.e6

Abstract: Morphological diversity is dominated by variation in body proportion [1], which can be described with scaling relationships and mathematical equations, following the pioneering work of D'Arcy Thompson [2] and Julian Huxley [3]. Yet, the cellular ... ...

Abstract	Morphological diversity is dominated by variation in body proportion [1], which can be described with scaling relationships and mathematical equations, following the pioneering work of D'Arcy Thompson [2] and Julian Huxley [3]. Yet, the cellular processes underlying divergence in size and shape of morphological traits between species remain largely unknown [4-8]. Here, we compare the ovipositors of two related species, Drosophila melanogaster and D. suzukii. D. suzukii has switched its egg-laying niche from rotting to ripe fruit [9]. Along with this shift, the D. suzukii ovipositor has undergone a significant change in size and shape [10]. Using an allometric approach, we find that, while adult ovipositor width has hardly changed between the species, D. suzukii ovipositor length is almost double that of D. melanogaster. We show that this difference mostly arises in a 6-h time window during pupal development. We observe that the developing ovipositors of the two species comprise an almost identical number of cells, with a similar profile of cell shapes and orientations. After cell division stops, we find that the ovipositor area continues to grow in both species through the isotropic expansion of cell apical area and the anisotropic cellular reorganization of the tissue. Remarkably, we find that the lengthening of the D. suzukii ovipositor compared to that of D. melanogaster results from the combination of the accelerated expansion of apical cell size and the enhanced anisotropic rearrangement of cells in the tissue. Therefore, the quantitative fine-tuning of morphogenetic processes can drive evolutionary changes in organ size and shape.
MeSH term(s)	Animals ; Biological Evolution ; Cell Enlargement ; Drosophila/anatomy & histology ; Drosophila/physiology ; Female ; Oviposition
Language	English
Publishing date	2019-06-06
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2019.05.020
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Article ; Online: Molecular bases of cell-cell junctions stability and dynamics.

Cavey, Matthieu / Lecuit, Thomas

Cold Spring Harbor perspectives in biology

2009 Volume 1, Issue 5, Page(s) a002998

Abstract: Epithelial cell-cell junctions are formed by apical adherens junctions (AJs), which are composed of cadherin adhesion molecules interacting in a dynamic way with the cortical actin cytoskeleton. Regulation of cell-cell junction stability and dynamics is ... ...

Abstract	Epithelial cell-cell junctions are formed by apical adherens junctions (AJs), which are composed of cadherin adhesion molecules interacting in a dynamic way with the cortical actin cytoskeleton. Regulation of cell-cell junction stability and dynamics is crucial to maintain tissue integrity and allow tissue remodeling throughout development. Actin filament turnover and organization are tightly controlled together with myosin-II activity to produce mechanical forces that drive the assembly, maintenance, and remodeling of AJs. In this review, we will discuss these three distinct stages in the lifespan of cell-cell junctions, using several developmental contexts, which illustrate how mechanical forces are generated and transmitted at junctions, and how they impact on the integrity and the remodeling of cell-cell junctions.
MeSH term(s)	Adherens Junctions/metabolism ; Animals ; Cadherins/metabolism ; Cell Adhesion ; Cell Adhesion Molecules/metabolism ; Cell Communication ; Endocytosis ; Epithelium/metabolism ; Mesoderm/metabolism ; Mice ; Models, Biological ; Myosins/metabolism ; Stress, Mechanical ; Tensile Strength
Chemical Substances	Cadherins ; Cell Adhesion Molecules ; Myosins (EC 3.6.4.1)
Language	English
Publishing date	2009-12-24
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ISSN	1943-0264
ISSN (online)	1943-0264
DOI	10.1101/cshperspect.a002998
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Article: Imaging cellular and molecular dynamics in live embryos using fluorescent proteins.

Cavey, Matthieu / Lecuit, Thomas

Methods in molecular biology (Clifton, N.J.)

2008 Volume 420, Page(s) 219–238

Abstract: With the live imaging of embryos, the dynamics of developmental processes, such as tissue remodeling, cell morphogenesis, and, campus protein dynamics can be observed and quantified. This has greatly improved the mechanistic understanding of biological ... ...

Abstract	With the live imaging of embryos, the dynamics of developmental processes, such as tissue remodeling, cell morphogenesis, and, campus protein dynamics can be observed and quantified. This has greatly improved the mechanistic understanding of biological processes. Here we describe how embryos can be prepared for imaging mainly, but not only, fluorescent proteins and probes. This chapter is a users' guide that addresses the following aspects of fluorescent embryo imaging: (1) How to handle and prepare embryos for live microscopy. (2) What microscopic setups are available for embryo imaging and what should they be used for. (3) How to practically use fluorescent imaging setups depending on the experimental context: large-scale imaging of multiple embryos, high-resolution four-dimensional imaging of single embryos, studies of protein dynamics, and so on. (4) Finally, we focus on pitfalls and how to overcome a variety of possible problems encountered during live imaging.
MeSH term(s)	Animals ; Cadherins/metabolism ; Developmental Biology/methods ; Drosophila melanogaster ; Genetic Techniques ; Green Fluorescent Proteins/metabolism ; Lasers ; Light ; Luminescent Proteins/metabolism ; Microscopy, Confocal/methods ; Microscopy, Fluorescence/methods ; Photobleaching ; Recombinant Fusion Proteins/chemistry ; Time Factors
Chemical Substances	Cadherins ; Luminescent Proteins ; Recombinant Fusion Proteins ; Green Fluorescent Proteins (147336-22-9)
Language	English
Publishing date	2008
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1064-3745
ISSN	1064-3745
DOI	10.1007/978-1-59745-583-1_13
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Article ; Online: Temporal patterning of neuroblasts controls Notch-mediated cell survival through regulation of Hid or Reaper.

Bertet, Claire / Li, Xin / Erclik, Ted / Cavey, Matthieu / Wells, Brent / Desplan, Claude

Cell

2014 Volume 158, Issue 5, Page(s) 1173–1186

Abstract: Temporal patterning of neural progenitors is one of the core mechanisms generating neuronal diversity in the central nervous system. Here, we show that, in the tips of the outer proliferation center (tOPC) of the developing Drosophila optic lobes, a ... ...

Abstract	Temporal patterning of neural progenitors is one of the core mechanisms generating neuronal diversity in the central nervous system. Here, we show that, in the tips of the outer proliferation center (tOPC) of the developing Drosophila optic lobes, a unique temporal series of transcription factors not only governs the sequential production of distinct neuronal subtypes but also controls the mode of progenitor division, as well as the selective apoptosis of Notch(OFF) or Notch(ON) neurons during binary cell fate decisions. Within a single lineage, intermediate precursors initially do not divide and generate only one neuron; subsequently, precursors divide, but their Notch(ON) progeny systematically die through Reaper activity, whereas later, their Notch(OFF) progeny die through Hid activity. These mechanisms dictate how the tOPC produces neurons for three different optic ganglia. We conclude that temporal patterning generates neuronal diversity by specifying both the identity and survival/death of each unique neuronal subtype.
MeSH term(s)	Animals ; Apoptosis ; Cell Survival ; Drosophila Proteins/metabolism ; Drosophila melanogaster/cytology ; Drosophila melanogaster/growth & development ; Drosophila melanogaster/metabolism ; Neural Stem Cells ; Neurogenesis ; Neuropeptides/metabolism ; Optic Lobe, Nonmammalian/cytology ; Optic Lobe, Nonmammalian/metabolism ; Receptors, Notch/metabolism
Chemical Substances	Drosophila Proteins ; HID protein, Drosophila ; N protein, Drosophila ; Neuropeptides ; Receptors, Notch ; rpr protein, Drosophila
Language	English
Publishing date	2014-08-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2014.07.045
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Article: Temporal Patterning of Neuroblasts Controls Notch-Mediated Cell Survival through Regulation of Hid or Reaper

Bertet, Claire / Xin Li / Ted Erclik / Matthieu Cavey / Brent Wells / Claude Desplan

Cell. 2014 Aug. 28, v. 158

2014

Abstract	Temporal patterning of neural progenitors is one of the core mechanisms generating neuronal diversity in the central nervous system. Here, we show that, in the tips of the outer proliferation center (tOPC) of the developing Drosophila optic lobes, a unique temporal series of transcription factors not only governs the sequential production of distinct neuronal subtypes but also controls the mode of progenitor division, as well as the selective apoptosis of NotchOFF or NotchON neurons during binary cell fate decisions. Within a single lineage, intermediate precursors initially do not divide and generate only one neuron; subsequently, precursors divide, but their NotchON progeny systematically die through Reaper activity, whereas later, their NotchOFF progeny die through Hid activity. These mechanisms dictate how the tOPC produces neurons for three different optic ganglia. We conclude that temporal patterning generates neuronal diversity by specifying both the identity and survival/death of each unique neuronal subtype.
Keywords	Drosophila ; apoptosis ; cell viability ; central nervous system ; death ; ganglia ; neurons ; progeny ; transcription factors
Language	English
Dates of publication	2014-0828
Size	p. 1173-1186.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2014.07.045
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Article ; Online: Evolution of Multiple Sensory Systems Drives Novel Egg-Laying Behavior in the Fruit Pest Drosophila suzukii.

Karageorgi, Marianthi / Bräcker, Lasse B / Lebreton, Sébastien / Minervino, Caroline / Cavey, Matthieu / Siju, K P / Grunwald Kadow, Ilona C / Gompel, Nicolas / Prud'homme, Benjamin

Current biology : CB

2017 Volume 27, Issue 6, Page(s) 847–853

Abstract: The rise of a pest species represents a unique opportunity to address how species evolve new behaviors and adapt to novel ecological niches [1]. We address this question by studying the egg-laying behavior of Drosophila suzukii, an invasive agricultural ... ...

Abstract	The rise of a pest species represents a unique opportunity to address how species evolve new behaviors and adapt to novel ecological niches [1]. We address this question by studying the egg-laying behavior of Drosophila suzukii, an invasive agricultural pest species that has spread from Southeast Asia to Europe and North America in the last decade [2]. While most closely related Drosophila species lay their eggs on decaying plant substrates, D. suzukii oviposits on ripening fruit, thereby causing substantial economic losses to the fruit industry [3-8]. D. suzukii has evolved an enlarged, serrated ovipositor that presumably plays a key role by enabling females to pierce the skin of ripe fruit [9]. Here, we explore how D. suzukii selects oviposition sites, and how this behavior differs from that of closely related species. We have combined behavioral experiments in multiple species with neurogenetics and mutant analysis in D. suzukii to show that this species has evolved a specific preference for oviposition on ripe fruit. Our results also establish that changes in mechanosensation, olfaction, and presumably gustation have contributed to this ecological shift. Our observations support a model in which the emergence of D. suzukii as an agricultural pest is the consequence of the progressive modification of several sensory systems, which collectively underlie a radical change in oviposition behavior.
MeSH term(s)	Animals ; Biological Evolution ; Drosophila/physiology ; Female ; Fruit/growth & development ; Introduced Species ; Mechanotransduction, Cellular ; Olfactory Perception ; Oviposition ; Species Specificity ; Taste Perception
Language	English
Publishing date	2017-03-09
Publishing country	England
Document type	Journal Article
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2017.01.055
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Article ; Online: A two-tiered mechanism for stabilization and immobilization of E-cadherin.

Cavey, Matthieu / Rauzi, Matteo / Lenne, Pierre-François / Lecuit, Thomas

Nature

2008 Volume 453, Issue 7196, Page(s) 751–756

Abstract: Epithelial tissues maintain a robust architecture which is important for their barrier function, but they are also remodelled through the reorganization of cell-cell contacts. Tissue stability requires intercellular adhesion mediated by E-cadherin, in ... ...

Abstract	Epithelial tissues maintain a robust architecture which is important for their barrier function, but they are also remodelled through the reorganization of cell-cell contacts. Tissue stability requires intercellular adhesion mediated by E-cadherin, in particular its trans-association in homophilic complexes supported by actin filaments through beta- and alpha-catenin. How alpha-catenin dynamic interactions between E-cadherin/beta-catenin and cortical actin control both stability and remodelling of adhesion is unclear. Here we focus on Drosophila homophilic E-cadherin complexes rather than total E-cadherin, including diffusing 'free' E-cadherin, because these complexes are a better proxy for adhesion. We find that E-cadherin complexes partition in very stable microdomains (that is, bona fide adhesive foci which are more stable than remodelling contacts). Furthermore, we find that stability and mobility of these microdomains depend on two actin populations: small, stable actin patches concentrate at homophilic E-cadherin clusters, whereas a rapidly turning over, contractile network constrains their lateral movement by a tethering mechanism. alpha-Catenin controls epithelial architecture mainly through regulation of the mobility of homophilic clusters and it is largely dispensable for their stability. Uncoupling stability and mobility of E-cadherin complexes suggests that stable epithelia may remodel through the regulated mobility of very stable adhesive foci.
MeSH term(s)	Actins/metabolism ; Animals ; Cadherins/chemistry ; Cadherins/metabolism ; Cell Adhesion ; Drosophila melanogaster/embryology ; Drosophila melanogaster/genetics ; Drosophila melanogaster/metabolism ; Epithelium/metabolism ; Female ; Male ; Models, Biological ; alpha Catenin/genetics ; alpha Catenin/metabolism
Chemical Substances	Actins ; Cadherins ; alpha Catenin
Language	English
Publishing date	2008-06-05
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	120714-3
ISSN	1476-4687 ; 0028-0836
ISSN (online)	1476-4687
ISSN	0028-0836
DOI	10.1038/nature06953
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Article: Drosophila valois encodes a divergent WD protein that is required for Vasa localization and Oskar protein accumulation.

Cavey, Matthieu / Hijal, Sirine / Zhang, Xiaolan / Suter, Beat

Development (Cambridge, England)

2005 Volume 132, Issue 3, Page(s) 459–468

Abstract: valois (vls) was identified as a posterior group gene in the initial screens for Drosophila maternal-effect lethal mutations. Despite its early genetic identification, it has not been characterized at the molecular level until now. We show that vls ... ...

Abstract	valois (vls) was identified as a posterior group gene in the initial screens for Drosophila maternal-effect lethal mutations. Despite its early genetic identification, it has not been characterized at the molecular level until now. We show that vls encodes a divergent WD domain protein and that the three available EMS-induced point mutations cause premature stop codons in the vls ORF. We have generated a null allele that has a stronger phenotype than the EMS mutants. The vlsnull mutant shows that vls+ is required for high levels of Oskar protein to accumulate during oogenesis, for normal posterior localization of Oskar in later stages of oogenesis and for posterior localization of the Vasa protein during the entire process of pole plasm assembly. There is no evidence for vls being dependent on an upstream factor of the posterior pathway, suggesting that Valois protein (Vls) instead acts as a co-factor in the process. Based on the structure of Vls, the function of similar proteins in different systems and our phenotypic analysis, it seems likely that vls may promote posterior patterning by facilitating interactions between different molecules.
MeSH term(s)	Adaptor Proteins, Signal Transducing/chemistry ; Amino Acid Sequence ; Animals ; Carrier Proteins/chemistry ; Carrier Proteins/genetics ; Carrier Proteins/metabolism ; Checkpoint Kinase 2 ; Cloning, Molecular ; DEAD-box RNA Helicases ; Drosophila Proteins/chemistry ; Drosophila Proteins/genetics ; Drosophila Proteins/metabolism ; Drosophila melanogaster/cytology ; Drosophila melanogaster/embryology ; Drosophila melanogaster/genetics ; Drosophila melanogaster/metabolism ; Female ; Humans ; Molecular Sequence Data ; Mutation/genetics ; Oogenesis ; Ovary/cytology ; Ovary/metabolism ; Protein Structure, Tertiary ; Protein Transport ; Protein-Serine-Threonine Kinases/metabolism ; RNA Helicases/metabolism ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; Sequence Alignment
Chemical Substances	Adaptor Proteins, Signal Transducing ; Carrier Proteins ; Drosophila Proteins ; MEP50 protein, human ; RNA, Messenger ; osk protein, Drosophila ; vls protein, Drosophila ; Checkpoint Kinase 2 (EC 2.7.1.11) ; Protein-Serine-Threonine Kinases (EC 2.7.11.1) ; lok protein, Drosophila (EC 2.7.11.1) ; DDX4 protein, human (EC 3.6.1.-) ; vas protein, Drosophila (EC 3.6.1.-) ; DEAD-box RNA Helicases (EC 3.6.4.13) ; RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2005-01-05
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	90607-4
ISSN	1477-9129 ; 0950-1991
ISSN (online)	1477-9129
ISSN	0950-1991
DOI	10.1242/dev.01590
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