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The membrane raft protein Flotillin-1 is essential in dopamine neurons for amphetamine-induced behavior in Drosophila

Molecular Psychiatry volume 18, pages 824–833 (2013)Cite this article

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Abstract

The dopamine transporter (DAT) is the primary molecular target responsible for the rewarding properties of the psychostimulants amphetamine (AMPH) and cocaine. AMPH increases extracellular dopamine (DA) by promoting its nonexocytotic release via DAT-mediated efflux. Previous studies in heterologous cells have shown that phosphorylation of the amino terminus of DAT is required for AMPH-induced DA efflux but not for DA uptake. However, the identity of many of the modulatory proteins and the molecular mechanisms that coordinate efflux and the ensuing behavioral effects remain poorly defined. Here, we establish a robust assay for AMPH-induced hyperlocomotion in Drosophila melanogaster larvae. Using a variety of genetic and pharmacological approaches, we demonstrate that this behavioral response is dependent on DA and on DAT and its phosphorylation. We also show that methylphenidate (MPH), which competitively inhibits DA uptake but does not induce DAT-mediated DA efflux, also leads to DAT-dependent hyperlocomotion, but this response is independent of DAT phosphorylation. Moreover, we demonstrate that the membrane raft protein Flotillin-1 is required for AMPH-induced, but not MPH-induced, hyperlocomotion. These results are the first evidence of a role for a raft protein in an AMPH-mediated behavior. Thus, using our assay we are able to translate molecular and cellular findings to a behavioral level and to differentiate in vivo the distinct mechanisms of two psychostimulants.

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Acknowledgements

This work was supported by PO1 DA12408 and K05 DA022413 (JAJ), T32 MH018870 (CSK, ZF) and the Lieber Center for Schizophrenia Research and Treatment. We thank Dr Rex Kerr and Nicholas Swierczek for providing us with the MWT software, Dr Marta Zlatic for help in setting up the MWT hardware, Dr Wesley Grueber for sharing his MWT system for the initial MWT/DIAS comparison.

Author Contribution:

ABP, CSK and JAJ designed the experiments, analyzed the data, discussed the results, and wrote the manuscript. ABP generated the hDAT mutant transgenic flies, developed the experimental protocol and implemented hardware setups for the behavioral tests. ABP, CSK and YZ performed the experiments. HY generated the hFlot1 and hFlot1 (C34A) transgenic flies. RF performed the statistical analyses. DSK developed the code that automates Choreography. BDM provided advice on fly genetics and the development of the behavioral assay. ZF, AY and BDM discussed the results and commented on the manuscript.

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  1. A B Pizzo and C S Karam: These authors contributed equally to this work.

Authors and Affiliations

  1. Center for Molecular Recognition, Columbia University College of Physicians and Surgeons, New York, NY, USA

    A B Pizzo, C S Karam, Y Zhang, H Yano, Z Freyberg & J A Javitch

  2. Department of Psychiatry, Columbia University College of Physicians and Surgeons, New York, NY, USA

    A B Pizzo, C S Karam, Y Zhang, H Yano, Z Freyberg & J A Javitch

  3. Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY, USA

    A B Pizzo, C S Karam, Y Zhang, H Yano, Z Freyberg & J A Javitch

  4. Department of Pharmacology, Columbia University College of Physicians and Surgeons, New York, NY, USA

    H Yano & J A Javitch

  5. Department of Psychology, Stern College for Women, Yeshiva University, New York, NY, USA

    R J Freyberg

  6. Department of Computational Sciences and Engineering, Institute for Computer Sciences, Technical University of Munich, Garching, Germany

    D S Karam

  7. Department of Neurology, Columbia University College of Physicians and Surgeons, New York, NY, USA

    A Yamamoto

  8. Department of Pathology and Cell Biology, Columbia University College of Physicians and Surgeons, New York, NY, USA

    A Yamamoto & B D McCabe

  9. Department of Neuroscience, Columbia University College of Physicians and Surgeons, New York, NY, USA

    B D McCabe

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Pizzo, A., Karam, C., Zhang, Y. et al. The membrane raft protein Flotillin-1 is essential in dopamine neurons for amphetamine-induced behavior in Drosophila. Mol Psychiatry 18, 824–833 (2013). https://doi.org/10.1038/mp.2012.82

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