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131 Publications

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    10/25/12 | A survey of 6,300 genomic fragments for cis-regulatory activity in the imaginal discs of Drosophila melanogaster.
    Jory A, Estella C, Giorgianni MW, Slattery M, Laverty TR, Rubin GM, Mann RS
    Cell Reports. 2012 Oct 25;2(4):1014-24. doi: 10.1016/j.celrep.2012.09.010

    Over 6,000 fragments from the genome of Drosophila melanogaster were analyzed for their ability to drive expression of GAL4 reporter genes in the third-instar larval imaginal discs. About 1,200 reporter genes drove expression in the eye, antenna, leg, wing, haltere, or genital imaginal discs. The patterns ranged from large regions to individual cells. About 75% of the active fragments drove expression in multiple discs; 20% were expressed in ventral, but not dorsal, discs (legs, genital, and antenna), whereas \~{}23% were expressed in dorsal but not ventral discs (wing, haltere, and eye). Several patterns, for example, within the leg chordotonal organ, appeared a surprisingly large number of times. Unbiased searches for DNA sequence motifs suggest candidate transcription factors that may regulate enhancers with shared activities. Together, these expression patterns provide a valuable resource to the community and offer a broad overview of how transcriptional regulatory information is distributed in the Drosophila genome.

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    08/23/12 | A subset of dopamine neurons signals reward for odour memory in Drosophila.
    Liu C, Placais P, Yamagata N, Pfeiffer BD, Aso Y, Friedrich AB, Siwanowicz I, Rubin GM, Preat T, Tanimoto H
    Nature. 2012 Aug 23;488(7412):512-6. doi: 10.1038/nature11304

    Animals approach stimuli that predict a pleasant outcome. After the paired presentation of an odour and a reward, Drosophila melanogaster can develop a conditioned approach towards that odour. Despite recent advances in understanding the neural circuits for associative memory and appetitive motivation, the cellular mechanisms for reward processing in the fly brain are unknown. Here we show that a group of dopamine neurons in the protocerebral anterior medial (PAM) cluster signals sugar reward by transient activation and inactivation of target neurons in intact behaving flies. These dopamine neurons are selectively required for the reinforcing property of, but not a reflexive response to, the sugar stimulus. In vivo calcium imaging revealed that these neurons are activated by sugar ingestion and the activation is increased on starvation. The output sites of the PAM neurons are mainly localized to the medial lobes of the mushroom bodies (MBs), where appetitive olfactory associative memory is formed. We therefore propose that the PAM cluster neurons endow a positive predictive value to the odour in the MBs. Dopamine in insects is known to mediate aversive reinforcement signals. Our results highlight the cellular specificity underlying the various roles of dopamine and the importance of spatially segregated local circuits within the MBs.

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    07/01/12 | Organization and metamorphosis of glia in the Drosophila visual system.
    Edwards TN, Nuschke AC, Nern A, Meinertzhagen IA
    The Journal of Comparative Neurology. 2012 Jul 1;520(10):2067-85. doi: 10.1002/cne.23071

    The visual system of Drosophila is an excellent model for determining the interactions that direct the differentiation of the nervous system’s many unique cell types. Glia are essential not only in the development of the nervous system, but also in the function of those neurons with which they become associated in the adult. Given their role in visual system development and adult function we need to both accurately and reliably identify the different subtypes of glia, and to relate the glial subtypes in the larval brain to those previously described for the adult. We viewed driver expression in subsets of larval eye disc glia through the earliest stages of pupal development to reveal the counterparts of these cells in the adult. Two populations of glia exist in the lamina, the first neuropil of the adult optic lobe: those that arise from precursors in the eye-disc/optic stalk and those that arise from precursors in the brain. In both cases, a single larval source gives rise to at least three different types of adult glia. Furthermore, analysis of glial cell types in the second neuropil, the medulla, has identified at least four types of astrocyte-like (reticular) glia. Our clarification of the lamina’s adult glia and identification of their larval origins, particularly the respective eye disc and larval brain contributions, begin to define developmental interactions which establish the different subtypes of glia.

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    04/09/12 | Using translational enhancers to increase transgene expression in Drosophila.
    Pfeiffer BD, Truman JW, Rubin GM
    Proceedings of the National Academy of Sciences of the United States of America. 2012 Apr 9;109(17):6626-31. doi: 10.1073/pnas.1204520109

    The ability to specify the expression levels of exogenous genes inserted in the genomes of transgenic animals is critical for the success of a wide variety of experimental manipulations. Protein production can be regulated at the level of transcription, mRNA transport, mRNA half-life, or translation efficiency. In this report, we show that several well-characterized sequence elements derived from plant and insect viruses are able to function in Drosophila to increase the apparent translational efficiency of mRNAs by as much as 20-fold. These increases render expression levels sufficient for genetic constructs previously requiring multiple copies to be effective in single copy, including constructs expressing the temperature-sensitive inactivator of neuronal function Shibire(ts1), and for the use of cytoplasmic GFP to image the fine processes of neurons.

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    12/01/11 | Associative learning between odorants and mechanosensory punishment in larval Drosophila.
    Eschbach C, Cano C, Haberkern H, Schraut K, Guan C, Triphan T, Gerber B
    Journal of Expiremental Biology. 2011 Dec 1;214(Pt 23):3897-905. doi: 10.1242/jeb.060533

    We tested whether Drosophila larvae can associate odours with a mechanosensory disturbance as a punishment, using substrate vibration conveyed by a loudspeaker (buzz:). One odour (A) was presented with the buzz, while another odour (B) was presented without the buzz (A/B training). Then, animals were offered the choice between A and B. After reciprocal training (A/B), a second experimental group was tested in the same way. We found that larvae show conditioned escape from the previously punished odour. We further report an increase of associative performance scores with the number of punishments, and an increase according to the number of training cycles. Within the range tested (between 50 and 200 Hz), however, the pitch of the buzz does not apparently impact associative success. Last, but not least, we characterized odour-buzz memories with regard to the conditions under which they are behaviourally expressed--or not. In accordance with what has previously been found for associative learning between odours and bad taste (such as high concentration salt or quinine), we report that conditioned escape after odour-buzz learning is disabled if escape is not warranted, i.e. if no punishment to escape from is present during testing. Together with the already established paradigms for the association of odour and bad taste, the present assay offers the prospect of analysing how a relatively simple brain orchestrates memory and behaviour with regard to different kinds of 'bad' events.

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    Svoboda LabRubin Lab
    08/23/11 | Multiple new site-specific recombinases for use in manipulating animal genomes.
    Nern A, Pfeiffer BD, Svoboda K, Rubin GM
    Proceedings of the National Academy of Sciences of the United States of America. 2011 Aug 23;108(34):14198-203. doi: 10.1073/pnas.1111704108

    Site-specific recombinases have been used for two decades to manipulate the structure of animal genomes in highly predictable ways and have become major research tools. However, the small number of recombinases demonstrated to have distinct specificities, low toxicity, and sufficient activity to drive reactions to completion in animals has been a limitation. In this report we show that four recombinases derived from yeast-KD, B2, B3, and R-are highly active and nontoxic in Drosophila and that KD, B2, B3, and the widely used FLP recombinase have distinct target specificities. We also show that the KD and B3 recombinases are active in mice.

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    06/19/11 | Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila.
    Séjourné J, Placais P, Aso Y, Siwanowicz I, Trannoy S, Thoma V, Tedjakumala SR, Rubin GM, Tchénio P, Ito K, Isabel G, Tanimoto H, Preat T
    Nature Neuroscience. 2011 Jun 19;14(7):903-10. doi: 10.1038/nn.2846

    Aversive olfactory memory is formed in the mushroom bodies in Drosophila melanogaster. Memory retrieval requires mushroom body output, but the manner in which a memory trace in the mushroom body drives conditioned avoidance of a learned odor remains unknown. To identify neurons that are involved in olfactory memory retrieval, we performed an anatomical and functional screen of defined sets of mushroom body output neurons. We found that MB-V2 neurons were essential for retrieval of both short- and long-lasting memory, but not for memory formation or memory consolidation. MB-V2 neurons are cholinergic efferent neurons that project from the mushroom body vertical lobes to the middle superiormedial protocerebrum and the lateral horn. Notably, the odor response of MB-V2 neurons was modified after conditioning. As the lateral horn has been implicated in innate responses to repellent odorants, we propose that MB-V2 neurons recruit the olfactory pathway involved in innate odor avoidance during memory retrieval.

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    Simpson LabRubin Lab
    06/01/11 | BrainAligner: 3D registration atlases of Drosophila brains.
    Peng H, Chung P, Long F, Qu L, Jenett A, Seeds AM, Myers EW, Simpson JH
    Nature Methods. 2011 Jun;8:493-500. doi: 10.1038/nmeth.1602

    Analyzing Drosophila melanogaster neural expression patterns in thousands of three-dimensional image stacks of individual brains requires registering them into a canonical framework based on a fiducial reference of neuropil morphology. Given a target brain labeled with predefined landmarks, the BrainAligner program automatically finds the corresponding landmarks in a subject brain and maps it to the coordinate system of the target brain via a deformable warp. Using a neuropil marker (the antibody nc82) as a reference of the brain morphology and a target brain that is itself a statistical average of data for 295 brains, we achieved a registration accuracy of 2 μm on average, permitting assessment of stereotypy, potential connectivity and functional mapping of the adult fruit fly brain. We used BrainAligner to generate an image pattern atlas of 2954 registered brains containing 470 different expression patterns that cover all the major compartments of the fly brain.

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    10/01/10 | Refinement of tools for targeted gene expression in Drosophila.
    Pfeiffer BD, Ngo TB, Hibbard KL, Murphy C, Jenett A, Truman JW, Rubin GM
    Genetics. 2010 Oct;186(2):735-55. doi: 10.1534/genetics.110.119917

    A wide variety of biological experiments rely on the ability to express an exogenous gene in a transgenic animal at a defined level and in a spatially and temporally controlled pattern. We describe major improvements of the methods available for achieving this objective in Drosophila melanogaster. We have systematically varied core promoters, UTRs, operator sequences, and transcriptional activating domains used to direct gene expression with the GAL4, LexA, and Split GAL4 transcription factors and the GAL80 transcriptional repressor. The use of site-specific integration allowed us to make quantitative comparisons between different constructs inserted at the same genomic location. We also characterized a set of PhiC31 integration sites for their ability to support transgene expression of both drivers and responders in the nervous system. The increased strength and reliability of these optimized reagents overcome many of the previous limitations of these methods and will facilitate genetic manipulations of greater complexity and sophistication.

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    04/13/10 | Visual targeting of motor actions in climbing Drosophila.
    Triphan T, Poeck B, Neuser K, Strauss R
    Current Biology. 2010 Apr 13;20(7):663-8. doi: 10.1016/j.cub.2010.02.055

    Drosophila melanogaster flies cross surmountable gaps in their walkway of widths exceeding their body length with an astounding maneuver but avoid attempts at insurmountable gaps by visual width estimation. Different mutant lines affect specific aspects of this maneuver, indicating a high complexity and modularity of the underlying motor control. Here we report on two mutants, ocelliless(1) and tay bridge(1), that, although making a correct decision to climb, fail dramatically in aiming at the right direction. Both mutants show structural defects in the protocerebral bridge, a central complex neuropil formed like a handlebar spanning the brain hemispheres. The bridge has been implicated in step-length control in walking flies and celestial E-vector orientation in locusts. In rescue experiments using tay bridge(1) flies, the integrity of the bridge was reestablished, concomitantly leading to a significant improvement of their orientation at the gap. Although producing directional scatter, their attempts were clearly aimed at the landing site. However, this partial rescue was lost in these flies at a reduced-visibility landing site. We therefore conclude that the protocerebral bridge is an essential part of a visual targeting network that transmits directional clues to the motor output via a known projection system.

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