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J. Biol. Chem., Vol. 279, Issue 24, 25614-25622, June 11, 2004

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Characterization of Aplysia Enticin and Temptin, Two Novel Water-borne Protein Pheromones That Act in Concert with Attractin to Stimulate Mate Attraction^*

Scott F. Cummins, Amy E. Nichols, Andinet Amare, Amanda B. Hummon, Jonathan V. Sweedler, and Gregg T. Nagle¶

From the Department of Neuroscience and Cell Biology, University of Texas Medical Branch, Galveston, Texas 77555, and the Department of Chemistry and the Beckman Institute, University of Illinois, Urbana, Illinois 61801

Mate attraction in Aplysia involves a long-distance water-borne signal (attractin) that is released during egg laying. Other pheromones are predicted to be released during egg laying that act in concert with albumen gland attractin to stimulate attraction, but their identities are unknown. To identify other candidate water-borne pheromones, we employed differential library screening of an albumen gland cDNA library, Northern blot analysis, purification, characterization, cloning, and expression of albumen gland proteins, matrix-assisted laser desorption ionization mass spectrometry, pheromone secretion assays, behavioral bioassays, immunolocalization studies, and comparative genomics. Four genes, Alb-23, Alb-24, Alb-69, and Alb-172, were highly expressed in Aplysia californica albumen glands and encoded novel proteins. The products of the Alb-24 ("enticin") and Alb-172 ("temptin") precursors were soluble and highly abundant in albumen gland extracts, whereas Alb-23 and Alb-69 were membrane-associated proteins. A comparative analysis showed that the predicted Aplysia brasiliana enticin and temptin proteins were 90 and 91% identical, respectively, to their A. californica homologs. T-maze attraction bioassay studies have previously demonstrated that egg cordons alone are attractive to Aplysia but that attractin alone is not. In the present study, however, the combination of attractin, enticin, and temptin was found to be significantly attractive to potential mates and doubled the number of animals attracted to this stimulus compared with control animals. The combined data strongly suggest that enticin and temptin are novel candidate water-borne protein pheromones that act in concert with attractin to attract Aplysia to form and maintain egglaying and mating aggregations.

Received for publication, December 11, 2003 , and in revised form, March 29, 2004.

^* This research was supported by National Science Foundation (NSF) Grant IBN-0314377, John Sealy Memorial Endowment Fund Grant 2579-02R (to G. T. N.), and National Institutes of Health Grant NS31609 (to J. V. S.). 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 additional experimental procedures, primer sequences, tables containing cDNAs identified by library screening, predicted amino acid sequences of novel precursors, and MALDI-MS of atrial gland peptides that may correspond to Alb-23 and Alb-24. The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AY161041, AY162288, AY162289, AY236850, AY162290, AY162291, AY236851, AY236852, AY162292, AY236853, AY309079, AY582744, and AY582745.

^¶ To whom correspondence should be addressed: 2.138 Medical Research Building, Galveston, TX 77555-1069; Tel.: 409-772-2834; Fax: 409-772-2789; E-mail: gtnagle{at}utmb.edu.

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