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J. Biol. Chem., Vol. 279, Issue 51, 53798-53805, December 17, 2004

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Tachykinin and Tachykinin Receptor of an Ascidian, Ciona intestinalis

EVOLUTIONARY ORIGIN OF THE VERTEBRATE TACHYKININ FAMILY^*

Honoo Satake, Michio Ogasawara¶, Tsuyoshi Kawada, Katsuyoshi Masuda, Masato Aoyama, Hiroyuki Minakata, Takuto Chiba||, Hitoe Metoki||, Yutaka Satou||, and Nori Satoh||

From the Suntory Institute for Bioorganic Research, Wakayamadai 1-1-1, Shimamoto-cho, Mishima-gun, Osaka 618-8503, Japan, the ^¶Department of Biology, Faculty of Science, Chiba University, 1-33 Yaoi-cho, Inage-ku, Chiba 263-8522, Japan, and the ^||Department of Zoology, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto 606-8502, Japan

Tachykinins (TKs) are the most prevalent vertebrate brain/gut peptides. In this study, we originally identified authentic TKs and their receptor from a protochordate, Ciona intestinalis. The Ciona TK (Ci-TK) precursor, like mammalian -preprotachykinin A (-PPTA), encodes two TKs, Ci-TK-I and -II, including the -FXGLM-NH₂ vertebrate TK consensus. Mass spectrometry of the neural extract revealed the production of both Ci-TKs. Ci-TK-I contains several Substance P (SP)-typical amino acids, whereas a Thr is exceptionally located at position 4 from the C terminus of Ci-TK-II. The Ci-TK gene encodes both Ci-TKs in the same exon, indicating no alternative generation of Ci-TKs, unlike the PPTA gene. These results suggested that the alternative splicing of the PPTA gene was established during evolution of vertebrates. The only Ci-TK receptor, Ci-TK-R, was equivalently activated by Ci-TK-I, SP, and neurokinin A at physiological concentrations, whereas Ci-TK-II showed 100-fold less potent activity, indicating that the ligand selectivity of Ci-TK-R is distinct from those of vertebrate TK receptors. Ci-TK-I, like SP, also elicited the typical contraction on the guinea pig ileum. The Ci-TK gene was expressed in neurons of the brain ganglion, small cells in the intestine, and the zone 7 in the endostyle, which corresponds to the vertebrate thyroid gland. Furthermore, the Ci-TK-R mRNA was distributed in these three tissues plus the gonad. These results showed that Ci-TKs play major roles in sexual behavior and feeding in protochordates as brain/gut peptides and endocrine/paracrine molecules. Taken together, our data revealed the biochemical and structural origins of vertebrate TKs and their receptors.

Received for publication, July 19, 2004 , and in revised form, September 24, 2004.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AB175738 and AB175739.

^* 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.

To whom correspondence should be addressed: Wakayamadai 1-1-1, Shimamoto-cho, Mishima-gun, Osaka 618-8503, Japan. Tel.: 81-75-962-6092; Fax: 81-75-962-2115; E-mail: satake{at}sunbor.or.jp.

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