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The Journal of Neuroscience, February 25, 2009, 29(8):2611-2625; doi:10.1523/JNEUROSCI.3670-08.2009

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Behavioral/Systems/Cognitive
A Dual Role for the Adaptor Protein DRK in Drosophila Olfactory Learning and Memory

Anastasios Moressis,^1,2 Anke R. Friedrich,³ Elias Pavlopoulos,^1,3 Ronald L. Davis,^4,5 and Efthimios M. C. Skoulakis^1,3

¹Institute of Molecular Biology and Genetics, Biomedical Sciences Research Centre "Alexander Fleming," Vari 16672, Greece, ²Department of Basic Sciences, School of Nursing, National and Kapodistrian University of Athens, Athens 11527, Greece, ³Department of Biology, Texas A&M University, College Station, Texas 77843, and Departments of ⁴Molecular and Cellular Biology and ⁵Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, Texas 77030

Correspondence should be addressed to Efthimios M. C. Skoulakis at the above address. Email: skoulakis{at}fleming.gr

Participation of RAS, RAF, and mitogen-activated protein kinase (MAPK) in learning and memory has been demonstrated in a number of studies, but the molecular events requisite for cascade activation and regulation have not been explored. We demonstrate that the adapter protein DRK (downstream of receptor kinase) which is essential for signaling to RAS in developmental contexts, is preferentially distributed in the adult mushroom bodies, centers for olfactory learning and memory. We demonstrate that drk mutant heterozygotes exhibit deficits in olfactory learning and memory, apparent under limited training conditions, but are not impaired in sensory responses requisite for the association of the stimuli, or brain neuroanatomy. Furthermore, we demonstrate that the protein is required acutely within mushroom body neurons to mediate efficient learning, a process that requires RAF activation. Importantly, 90 min memory remained impaired, even after differential training yielding equivalent learning in animals with compromised DRK levels and controls and did not require RAF. Sustained MAPK activation is compromised in drk mutants and surprisingly is negatively regulated by constitutive RAF activity. The data establish a role for DRK in Drosophila behavioral neuroplasticity and suggest a dual role for the protein, first in RAF activation-dependent learning and additionally in RAF-inhibition dependent sustained MAPK activation essential for memory formation or stability.

Key words: learning; memory; DRK; RAS; RAF; signaling

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Received Aug. 3, 2008; revised Dec. 24, 2008; accepted Jan. 14, 2009.

Correspondence should be addressed to Efthimios M. C. Skoulakis at the above address. Email: skoulakis{at}fleming.gr

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