TY - JOUR
T1 - Evolutionary acquisition of promoter-associated non-coding RNA (pancRNA) repertoires diversifies species-dependent gene activation mechanisms in mammals
AU - Uesaka, Masahiro
AU - Agata, Kiyokazu
AU - Oishi, Takao
AU - Nakashima, Kinichi
AU - Imamura, Takuya
N1 - Funding Information:
This work was supported in part by Grant-in-aid Nos. 21688021, 24380158, and 15H04603 (to T. I.), Global COE program A06 (to Kyoto University), the Grants to Excellent Graduate Schools (MEXT) program of Kyoto University, Grant-in-aid Nos. 221S0002 and 16H06279 for Scientific Research on Innovative Areas “Genome Science” from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and by the Asahi Glass Foundation (to T. I.), and Grant-in-Aid for JSPS Research Fellow Nos. 12J01645 and 15J06414 (to M. U.).
Funding Information:
We thank the Great Ape Information Network (GAIN) and Kumamoto Sanctuary, Wildlife Research Center, Kyoto University for chimpanzee and macaque samples. This study was conducted by the Cooperative Research Program of the Primate Research Institute, Kyoto University. We thank Atsushi Toyoda, Yutaka Suzuki and Sumio Sugano for directional RNA sequencing, Hiroo Imai for primate sample preparation, and Osamu Nishimura, Nobuhiko Hamazaki and Naoki Yamamoto for useful discussions. We thank the National Institute of Genetics (NIG) and the Graduate School of Frontier Sciences in the University of Tokyo for technical assistance. We thank Elizabeth Nakajima for proofreading the manuscript. We thank the Mouse ENCODE Consortium for the mouse directional RNA-seq and ChIP-seq data.
Publisher Copyright:
© 2017 The Author(s).
PY - 2017/4/7
Y1 - 2017/4/7
N2 - Background: Recent transcriptome analyses have shown that long non-coding RNAs (ncRNAs) play extensive roles in transcriptional regulation. In particular, we have reported that promoter-associated ncRNAs (pancRNAs) activate the partner gene expression via local epigenetic changes. Results: Here, we identify thousands of genes under pancRNA-mediated transcriptional activation in five mammalian species in common. In the mouse, 1) pancRNA-partnered genes confined their expression pattern to certain tissues compared to pancRNA-lacking genes, 2) expression of pancRNAs was significantly correlated with the enrichment of active chromatin marks, H3K4 trimethylation and H3K27 acetylation, at the promoter regions of the partner genes, 3) H3K4me1 marked the pancRNA-partnered genes regardless of their expression level, and 4) C- or G-skewed motifs were exclusively overrepresented between-200 and-1bp relative to the transcription start sites of the pancRNA-partnered genes. More importantly, the comparative transcriptome analysis among five different mammalian species using a total of 25 counterpart tissues showed that the overall pancRNA expression profile exhibited extremely high species-specificity compared to that of total mRNA, suggesting that interspecies difference in pancRNA repertoires might lead to the diversification of mRNA expression profiles. Conclusions: The present study raises the interesting possibility that the gain and/or loss of gene-activation-associated pancRNA repertoires, caused by formation or disruption of the genomic GC-skewed structure in the course of evolution, finely shape the tissue-specific pattern of gene expression according to a given species.
AB - Background: Recent transcriptome analyses have shown that long non-coding RNAs (ncRNAs) play extensive roles in transcriptional regulation. In particular, we have reported that promoter-associated ncRNAs (pancRNAs) activate the partner gene expression via local epigenetic changes. Results: Here, we identify thousands of genes under pancRNA-mediated transcriptional activation in five mammalian species in common. In the mouse, 1) pancRNA-partnered genes confined their expression pattern to certain tissues compared to pancRNA-lacking genes, 2) expression of pancRNAs was significantly correlated with the enrichment of active chromatin marks, H3K4 trimethylation and H3K27 acetylation, at the promoter regions of the partner genes, 3) H3K4me1 marked the pancRNA-partnered genes regardless of their expression level, and 4) C- or G-skewed motifs were exclusively overrepresented between-200 and-1bp relative to the transcription start sites of the pancRNA-partnered genes. More importantly, the comparative transcriptome analysis among five different mammalian species using a total of 25 counterpart tissues showed that the overall pancRNA expression profile exhibited extremely high species-specificity compared to that of total mRNA, suggesting that interspecies difference in pancRNA repertoires might lead to the diversification of mRNA expression profiles. Conclusions: The present study raises the interesting possibility that the gain and/or loss of gene-activation-associated pancRNA repertoires, caused by formation or disruption of the genomic GC-skewed structure in the course of evolution, finely shape the tissue-specific pattern of gene expression according to a given species.
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U2 - 10.1186/s12864-017-3662-1
DO - 10.1186/s12864-017-3662-1
M3 - Article
C2 - 28388877
AN - SCOPUS:85018624289
SN - 1471-2164
VL - 18
JO - BMC Genomics
JF - BMC Genomics
IS - 1
M1 - 285
ER -