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Molecular and Cellular Biology, January 2007, p. 732-742, Vol. 27, No. 2
0270-7306/07/$08.00+0     doi:10.1128/MCB.01329-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Role of DNA Methylation and Histone H3 Lysine 27 Methylation in Tissue-Specific Imprinting of Mouse Grb10{triangledown}

Yoko Yamasaki-Ishizaki,1,2,8 Tomohiko Kayashima,1 Christophe K. Mapendano,1 Hidenobu Soejima,3 Tohru Ohta,4,8 Hideaki Masuzaki,2 Akira Kinoshita,1,8 Takeshi Urano,5 Ko-ichiro Yoshiura,1,8 Naomichi Matsumoto,6 Tadayuki Ishimaru,2 Tsunehiro Mukai,3 Norio Niikawa,1,8 and Tatsuya Kishino7,8*

Departments of Human Genetics,1 Obstetrics and Gynecology, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki, Japan,2 Department of Biomolecular Sciences, Saga University, Saga, Japan,3 The Research Institute of Personalized Health Sciences, Health Sciences University of Hokkaido, Hokkaido, Japan,4 Department of Biochemistry II, Graduate School of Medicine, Nagoya University, Nagoya, Japan,5 Department of Human Genetics, Graduate School of Medicine, Yokohama City University, Yokohama, Japan,6 Division of Functional Genomics, Center for Frontier Life Sciences, Nagasaki University, Nagasaki, Japan,7 CREST, Japan Science and Technology Agency, Kawaguchi, Japan8

Received 19 July 2006/ Accepted 24 October 2006

Mouse Grb10 is a tissue-specific imprinted gene with promoter-specific expression. In most tissues, Grb10 is expressed exclusively from the major-type promoter of the maternal allele, whereas in the brain, it is expressed predominantly from the brain type promoter of the paternal allele. Such reciprocally imprinted expression in the brain and other tissues is thought to be regulated by DNA methylation and the Polycomb group (PcG) protein Eed. To investigate how DNA methylation and chromatin remodeling by PcG proteins coordinate tissue-specific imprinting of Grb10, we analyzed epigenetic modifications associated with Grb10 expression in cultured brain cells. Reverse transcriptase PCR analysis revealed that the imprinted paternal expression of Grb10 in the brain implied neuron-specific and developmental stage-specific expression from the paternal brain type promoter, whereas in glial cells and fibroblasts, Grb10 was reciprocally expressed from the maternal major-type promoter. The cell-specific imprinted expression was not directly related to allele-specific DNA methylation in the promoters because the major-type promoter remained biallelically hypomethylated regardless of its activity, whereas gametic DNA methylation in the brain type promoter was maintained during differentiation. Histone modification analysis showed that allelic methylation of histone H3 lysine 4 and H3 lysine 9 were associated with gametic DNA methylation in the brain type promoter, whereas that of H3 lysine 27 regulated by the Eed PcG complex was detected in the paternal major-type promoter, corresponding to its allele-specific silencing. Here, we propose a molecular model that gametic DNA methylation and chromatin remodeling by PcG proteins during cell differentiation cause tissue-specific imprinting in embryonic tissues.

* Corresponding author. Mailing address: Division of Functional Genomics, Center for Frontier Life Sciences, Nagasaki University, Sakamoto 1-12-4, Nagasaki 852-8523, Japan. Phone: 81-95-849-7120. Fax: 81-95-849-7178. E-mail: kishino{at}net.nagasaki-u.ac.jp.

{triangledown} Published ahead of print on 13 November 2006.

Molecular and Cellular Biology, January 2007, p. 732-742, Vol. 27, No. 2
0270-7306/07/$08.00+0     doi:10.1128/MCB.01329-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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