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J. Biol. Chem., Vol. 280, Issue 15, 14948-14955, April 15, 2005

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Two Functional but Noncomplementing Drosophila Tyrosine Decarboxylase Genes

DISTINCT ROLES FOR NEURAL TYRAMINE AND OCTOPAMINE IN FEMALE FERTILITY^*

Shannon H. Cole¶, Ginger E. Carney||, Colleen A. McClung**, Stacey S. Willard, Barbara J. Taylor, and Jay Hirsh¶¶

From the Department of Biology and Neuroscience Graduate Program, University of Virginia, Charlottesville, Virginia 22903, the ^||Department of Biology, Texas A&M University, College Station, Texas 77843-3258, and the Department of Zoology, Oregon State University, Corvallis, Oregon 97331-2914

The trace biogenic amine tyramine is present in the nervous systems of animals ranging in complexity from nematodes to mammals. Tyramine is synthesized from tyrosine by the enzyme tyrosine decarboxylase (TDC), a member of the aromatic amino acid family, but this enzyme has not been identified in Drosophila or in higher animals. To further clarify the roles of tyramine and its metabolite octopamine, we have cloned two TDC genes from Drosophila melanogaster, dTdc1 and dTdc2. Although both gene products have TDC activity in vivo, dTdc1 is expressed nonneurally, whereas dTdc2 is expressed neurally. Flies with a mutation in dTdc2 lack neural tyramine and octopamine and are female sterile due to egg retention. Although other Drosophila mutants that lack octopamine retain eggs completely within the ovaries, dTdc2 mutants release eggs into the oviducts but are unable to deposit them. This specific sterility phenotype can be partially rescued by driving the expression of dTdc2 in a dTdc2-specific pattern, whereas driving the expression of dTdc1 in the same pattern results in a complete rescue. The disparity in rescue efficiencies between the ectopically expressed Tdc genes may reflect the differential activities of these gene products. The egg retention phenotype of the dTdc2 mutant and the phenotypes associated with ectopic dTdc expression contribute to a model in which octopamine and tyramine have distinct and separable neural activities.

Received for publication, December 17, 2004 , and in revised form, January 13, 2005.

^* This work was supported in part by National Institutes of Health Grants R01 GM 27318 (to J. H.) and R01 GM 56920A (to B. J. T.) and by National Science Foundation Grant IBN-0321473 (to G. C.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains an additional table and two additional figures.

^¶ Recipient of Ruth L. Kirschstein Memorial National Research Service Award 1 F31 DA15265-03.

^** Current address: Department of Psychiatry and Center for Basic Neuroscience, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9070.

Recipient of Ruth L. Kirschstein Memorial National Research Service Award 1 F31 DA06063-01.

^¶¶ To whom correspondence should be addressed: Dept. of Biology, Rm. 262, Gilmer Hall, P.O. Box 400328, University of Virginia, Charlottesville, VA 22903. Tel.: 434-982-5607; Fax: 434-982-5626; E-mail: jh6u{at}virginia.edu.

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