Abstract
DIO3 and DIO3OS are two imprinted genes identified in mouse and humans. The DIO3 gene, which encodes for the type 3 deiodinase, is preferentially expressed from the paternal allele, while the DIO3OS transcript is transcribed in opposite orientation to DIO3, multiple noncoding and alternatively splicing isoforms from maternal allele. In this study, the five splice variants of DIO3OS were identified in Holstein cattle and had complex, tissue-specific expression patterns observed in eight tissues, including heart, liver, spleen, lung, kidney, muscle, fat and brain. In the G+C rich region, upstream from the cattle DIO3 gene, there were three small conserved regions and some promoter elements similar to those observed in mouse and humans. An allele-specific expression analysis-based SNP method revealed that DIO3 and DIO3OS genes exhibited monoallelic expression in the eight tissues, indicating that DIO3 and DIO3OS are imprinted in cattle.
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References
Amaral P. P. and Mattick J. S. 2008 Noncoding RNA in development. Mamm. Genome 19, 454–492.
Arnaud P., Monk D., Hitchins M., Gordon E., Dean W., Beechey C. V. et al. 2003 Conserved methylation imprints in the human and mouse GRB10 genes with divergent allelic expression suggests differential reading of the same mark. Hum. Mol. Genet. 12, 1005–1019.
Autuoro J. M., Pirnie S. P. and Carmichael G. G. 2014 Long noncoding RNAs in imprinting and X chromosome inactivation. Biomolecules 4, 76–100.
Carninci P., Kasukawa T., Katayama S., Gough J., Frith M. C., Maeda N. et al. 2005 The transcriptional landscape of the mammalian genome. Science 309, 1559–1563.
Carr M. S., Yevtodiyenko A., Schmidt C. L. and Schmidt J. V. 2007 Allele-specific histone modifications regulate expression of the Dlk1-Gtl2 imprinted domain. Genomics 89, 280–290.
Connor E. E., Laiakis E. C., Fernandes V. M., Williams J. L. and Capuco A.V. 2005 Molecular cloning, expression and radiation hybrid mapping of the cattle deiodinase type II (DIO2) and deiodinase type III (DIO3) genes. Anim. Genet. 36, 240–243.
Dietz W. H., Masterson K., Sittig L. J., Redei E. E. and Herzing L. B. 2012 Imprinting and expression of Dio3os mirrors Dio3 in rat. Front. Genet. 3, 279–279.
Hagan J. P., O’Neill B. L., Stewart C. L., Kozlov S. V. and Croce C. M. 2009 At least ten genes define the imprinted Dlk1-Dio3 cluster on mouse chromosome 12qF1. PLoS One 4, e4352.
Hernandez A. 2005 Structure and function of the type 3 deiodinase gene. Thyroid 15, 865–874.
Hernandez A., Fiering S., Martinez E., Galton V. A. and St Germain D. 2002 The gene locus encoding iodothyronine deiodinase type 3 (Dio3) is imprinted in the fetus and expresses antisense transcripts. Endocrinology 143, 4483–4486.
Hernandez A., Martinez M. E., Croteau W. and St Germain D. L. 2004 Complex organization and structure of sense and antisense transcripts expressed from the DIO3 imprinted locus. Genomics 83, 413–424.
Hou X. H., Li D. J., Su H., Hu J. Q., Li N. and Li S. J. 2011 Molecular cloning, expression, and imprinting status of maternally expressed gene 8 (MEG8) in dairy cattle. Russ. J. Genet. 47, 994–998.
Huang R., Jaritz M., Guenzl P., Vlatkovic I., Sommer A., Tamir I. M. et al. 2011 An RNA-seq strategy to detect the complete coding and non-coding transcriptome including full-length imprinted macro ncRNAs. PLoS One 6, e27288.
Kanduri C. 2016 Long noncoding RNAs: lessons from genomic imprinting. Biochim. Biophys. Acta 1859, 102–111.
Katayama S., Tomaru Y., Kasukawa T., Waki K., Nakanishi M., Nakamura M. et al. 2005 Antisense transcription in the mammalian genome. Science 309, 1564–1566.
Khalil A. M., Guttman M., Huarte M., Garber M., Raj A., Hagan J. P. et al. 2009 At least ten genes define the imprinted Dlk1-Dio3 cluster on mouse chromosome 12qF1. PLoS One 4, e4352.
Kozak M. 1987 At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J. Mol. Biol. 196, 947–950.
Martinez M. E., Charalambous M., Saferali A., Fiering S., Naumova A. K., St Germain D. et al. 2014 Genomic imprinting variations in the mouse type 3 deiodinase gene between tissues and brain regions. Mol. Endocrinol. 28, 1875–1886.
Numata K., Kohama C., Abe K. and Kiyosawa H. 2010 Highly parallel SNP genotyping reveals high-resolution landscape of mono-allelic Ube3a expression associated with locus-wide antisense transcription. Nucleic Acids Res. 39, 2649–2657.
O’Neill M. J. 2005 The influence of non-coding RNAs on allele-specific gene expression in mammals. Hum. Mol. Genet. 14, 113–120.
Peters J. and Robson J. E. 2008 Imprinted noncoding RNAs. Mamm. Genome 19, 493–502.
Plagge A. and Kelsey G. 2006 Imprinting the Gnas locus. Cytogenet. Genome Res. 113, 178–187.
Su H., Li D., Hou X., Tan B., Hu J., Zhang C. et al. 2011 Molecular structure of cattle Gtl2 gene and DNA methylation status of Dlk1-Gtl2 imprinted domain in cloned cattles. Anim. Reprod. Sci. 127, 23–30.
St Germain D. L. and Galton V. A. 1997 The deiodinase family of selenoproteins. Thyroid 7, 655–668.
Takada S., Tevendale M., Baker J., Georgiades P., Campbell E., Freeman T. et al. 2000 Delta-like and Gtl2 are reciprocally expressed, differentially methylated linked imprinted genes on mouse chromosome 12. Curr. Biol. 10, 1135–1138.
Tsai C., Lin S. P., Ito M., Takagi N., Takada S. and Ferguson-Smith A. C. 2002 Genomic imprinting contributes to thyroid hormone metabolism in the mouse embryo. Curr. Biol. 12, 1221–1226.
Zhang K., Li D., Wang M., Wu G., Shi Y. and Li S. 2014 The differential expression of alternatively spliced transcripts and imprinting status of MEG9 gene in cows. Anim. Genet. 45, 660–664.
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This study was supported by the National Natural Science Foundation of China (31372312).
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[Yang W., Li D., Wang G., Wu X., Zhang M., Zhang C., Cui Y. and Li S. 2017 Expression and imprinting of DIO3 and DIO3OS genes in Holstein cattle. J. Genet. 96, xx–xx]
Corresponding editor: Indrajit Nanda
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Yang, W., Li, D., Wang, G. et al. Expression and imprinting of DIO3 and DIO3OS genes in Holstein cattle. J Genet 96, 333–339 (2017). https://doi.org/10.1007/s12041-017-0780-0
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DOI: https://doi.org/10.1007/s12041-017-0780-0