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J. Biol. Chem., Vol. 281, Issue 41, 30551-30560, October 13, 2006

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Allelic Gene Regulation of Pcdh- and Pcdh- Clusters Involving Both Monoallelic and Biallelic Expression in Single Purkinje Cells^*

Ryosuke Kaneko¹, Hiroyuki Kato¹, Yoshimi Kawamura¹, Shigeyuki Esumi, Teruyoshi Hirayama, Takahiro Hirabayashi, and Takeshi Yagi²

From the KOKORO Biology Group, Laboratories for Integrated Biology, Graduate School of Frontier Biosciences, Osaka University 1-3 Yamadaoka, Suita, Osaka 565-0871, Japan, and the Department of Morphological Neural Science, Graduate School of Medical Science, Kumamoto University, Kumamoto 860-8556, Japan

The molecular basis for providing the identity and diversity of single neurons is a key for realizing the brain system. Diverse protocadherin isoforms encoded by the Pcdh- and Pcdh- gene clusters are expressed in all of the vertebrates studied. For the Pcdh- isoforms, differential expression patterns have been found in single Purkinje cells by unusual monoallelic and combinatorial types of gene regulation. Here we investigated total allelic gene regulation in the Pcdh- and - clusters, including the C-type variable exons (C1 to C5) and the Pcdh-A and -B variable exons in single Purkinje cells. Using split single-cell reverse transcription-PCR analysis, almost all of the Purkinje cells at postnatal day 21 biallelically expressed all the C-type isoforms, whereas the Pcdh- isoforms showed both monoallelic and combinatorial expression. The Pcdh-A and -B isoforms also showed differential regulation in each cell with both monoallelic and combinatorial gene regulation. These data indicated that different types of allelic gene regulation (monoallelic versus biallelic) occurred in the Pcdh- and - clusters, although they were spliced into the same constant exons. It has been reported that each C-type Pcdh- or - transcript has a different expression pattern during brain development, suggesting that the different C-type variable exons may code temporal diversity, although the Pcdh-, -A, and -B isoforms were differential and combinatorial gene regulation within a single cell. Thus, the multiple gene regulations in the Pcdh- and - clusters had a potential mechanism for increasing the diversity of individual neurons in the brain.

Received for publication, June 14, 2006 , and in revised form, July 25, 2006.

^* This work was supported by Grants-in-Aid from the Ministry of Education, Science, Sports, and Culture of Japan (to T. Y.), the Uehara Memorial Foundation, the Takeda Foundation, and CREST (Core Research for Evolutional Science and Technology) of the Japan Science and Technology Agency. 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 supplemental Table S1 and Fig. S1.

¹ These authors contributed equally to this work.

² To whom correspondence should be addressed: Graduate School of Frontier Biosciences, Osaka University 1-3 Yamadaoka, Suita, Osaka 565-0871, Japan. Tel.: 81-6-6879-7990; Fax: 81-6-6877-1922; E-mail: yagi{at}fbs.osaka-u.ac.jp.

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