The evolution of the DLK1-DIO3 imprinted domain in mammals

Carol A. Edwards; Andrew J. Mungall; Lucy Matthews; Edward Ryder; Dionne J. Gray; Andrew J. Pask; Geoffrey Shaw; Jennifer A.M. Graves; Jane Rogers; Ian Dunham; Marilyn B. Renfree; Anne C. Ferguson-Smith; Alex Bateman; Chao Kung Chen; John Collins; James Gilbert; Elizabeth Huckle; Sam Griffith-Jones; Jennifer Harrow; Matthew Jones; Mustapha Larbaoui; Karen Oliver; Carol Scott; Sarah Sims; Charles Steward; Jennie Yang; Guillaume Smits; Simon Andrews; Delphine Beury; Christel Krueger; Elena Ivanova; Iain McKendrick; Paul Smith; Gavin Kelsey; Wolf Reik

doi:10.1371/journal.pbio.0060135

The evolution of the DLK1-DIO3 imprinted domain in mammals

Carol A. Edwards, Andrew J. Mungall, Lucy Matthews, Edward Ryder, Dionne J. Gray, Andrew J. Pask, Geoffrey Shaw, Jennifer A.M. Graves, Jane Rogers, Ian Dunham, Marilyn B. Renfree, Anne C. Ferguson-Smith, Alex Bateman, Chao Kung Chen, John Collins, James Gilbert, Elizabeth Huckle, Sam Griffith-Jones, Jennifer Harrow, Matthew JonesMustapha Larbaoui, Karen Oliver, Carol Scott, Sarah Sims, Charles Steward, Jennie Yang, Guillaume Smits, Simon Andrews, Delphine Beury, Christel Krueger, Elena Ivanova, Iain McKendrick, Paul Smith, Gavin Kelsey, Wolf Reik

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156 Citations (Scopus)

Abstract

A comprehensive, domain-wide comparative analysis of genomic imprinting between mammals that imprint and those that do not can provide valuable information about how and why imprinting evolved. The imprinting status, DNA methylation, and genomic landscape of the Dlk1-Dio3 cluster were determined in eutherian, metatherian, and prototherian mammals including tammar wallaby and platypus. Imprinting across the whole domain evolved after the divergence of eutherian from marsupial mammals and in eutherians is under strong purifying selection. The marsupial locus at 1.6 megabases, is double that of eutherians due to the accumulation of LINE repeats. Comparative sequence analysis of the domain in seven vertebrates determined evolutionary conserved regions common to particular subgroups and to all vertebrates. The emergence of Dlk1-Dio3 imprinting in eutherians has occurred on the maternally inherited chromosome and is associated with region-specific resistance to expansion by repetitive elements and the local introduction of noncoding transcripts including microRNAs and C/D small nucleolar RNAs. A recent mammal-specific retrotransposition event led to the formation of a completely new gene only in the eutherian domain, which may have driven imprinting at the cluster.

Original language	English
Article number	e135
Pages (from-to)	1292-1305
Number of pages	14
Journal	PLoS Biology
Volume	6
Issue number	6
DOIs	https://doi.org/10.1371/journal.pbio.0060135
Publication status	Published - Jun 2008

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Edwards, C. A., Mungall, A. J., Matthews, L., Ryder, E., Gray, D. J., Pask, A. J., Shaw, G., Graves, J. A. M., Rogers, J., Dunham, I., Renfree, M. B., Ferguson-Smith, A. C., Bateman, A., Chen, C. K., Collins, J., Gilbert, J., Huckle, E., Griffith-Jones, S., Harrow, J., ... Reik, W. (2008). The evolution of the DLK1-DIO3 imprinted domain in mammals. PLoS Biology, 6(6), 1292-1305. Article e135. https://doi.org/10.1371/journal.pbio.0060135

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title = "The evolution of the DLK1-DIO3 imprinted domain in mammals",

abstract = "A comprehensive, domain-wide comparative analysis of genomic imprinting between mammals that imprint and those that do not can provide valuable information about how and why imprinting evolved. The imprinting status, DNA methylation, and genomic landscape of the Dlk1-Dio3 cluster were determined in eutherian, metatherian, and prototherian mammals including tammar wallaby and platypus. Imprinting across the whole domain evolved after the divergence of eutherian from marsupial mammals and in eutherians is under strong purifying selection. The marsupial locus at 1.6 megabases, is double that of eutherians due to the accumulation of LINE repeats. Comparative sequence analysis of the domain in seven vertebrates determined evolutionary conserved regions common to particular subgroups and to all vertebrates. The emergence of Dlk1-Dio3 imprinting in eutherians has occurred on the maternally inherited chromosome and is associated with region-specific resistance to expansion by repetitive elements and the local introduction of noncoding transcripts including microRNAs and C/D small nucleolar RNAs. A recent mammal-specific retrotransposition event led to the formation of a completely new gene only in the eutherian domain, which may have driven imprinting at the cluster.",

author = "Edwards, {Carol A.} and Mungall, {Andrew J.} and Lucy Matthews and Edward Ryder and Gray, {Dionne J.} and Pask, {Andrew J.} and Geoffrey Shaw and Graves, {Jennifer A.M.} and Jane Rogers and Ian Dunham and Renfree, {Marilyn B.} and Ferguson-Smith, {Anne C.} and Alex Bateman and Chen, {Chao Kung} and John Collins and James Gilbert and Elizabeth Huckle and Sam Griffith-Jones and Jennifer Harrow and Matthew Jones and Mustapha Larbaoui and Karen Oliver and Carol Scott and Sarah Sims and Charles Steward and Jennie Yang and Guillaume Smits and Simon Andrews and Delphine Beury and Christel Krueger and Elena Ivanova and Iain McKendrick and Paul Smith and Gavin Kelsey and Wolf Reik",

year = "2008",

month = jun,

doi = "10.1371/journal.pbio.0060135",

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Edwards, CA, Mungall, AJ, Matthews, L, Ryder, E, Gray, DJ, Pask, AJ, Shaw, G, Graves, JAM, Rogers, J, Dunham, I, Renfree, MB, Ferguson-Smith, AC, Bateman, A, Chen, CK, Collins, J, Gilbert, J, Huckle, E, Griffith-Jones, S, Harrow, J, Jones, M, Larbaoui, M, Oliver, K, Scott, C, Sims, S, Steward, C, Yang, J, Smits, G, Andrews, S, Beury, D, Krueger, C, Ivanova, E, McKendrick, I, Smith, P, Kelsey, G & Reik, W 2008, 'The evolution of the DLK1-DIO3 imprinted domain in mammals', PLoS Biology, vol. 6, no. 6, e135, pp. 1292-1305. https://doi.org/10.1371/journal.pbio.0060135

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AU - Huckle, Elizabeth

AU - Griffith-Jones, Sam

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AU - Steward, Charles

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The evolution of the DLK1-DIO3 imprinted domain in mammals

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