Human imprinted retrogenes exhibit non-canonical imprint chromatin signatures and reside in non-imprinted host genes

David Monk; Philippe Arnaud; Jennifer M. Frost; Andrew J. Wood; Michael Cowley; Alejandro Martin-Trujillo; Amy Guillaumet-Adkins; Isabel Iglesias Platas; Cristina Camprubi; Deborah Bourc&apos;his; Robert Feil; Gudrun E. Moore; Rebecca J. Oakey

doi:10.1093/nar/gkq1230

Human imprinted retrogenes exhibit non-canonical imprint chromatin signatures and reside in non-imprinted host genes

David Monk, Philippe Arnaud, Jennifer M. Frost, Andrew J. Wood, Michael Cowley, Alejandro Martin-Trujillo, Amy Guillaumet-Adkins, Isabel Iglesias Platas, Cristina Camprubi, Deborah Bourc'his, Robert Feil, Gudrun E. Moore, Rebecca J. Oakey

Medical & Molecular Genetics

Research output: Contribution to journal › Article › peer-review

21 Citations (Scopus)

Abstract

Imprinted retrotransposed genes share a common genomic organization including a promoter-associated differentially methylated region (DMR) and a position within the intron of a multi-exonic 'host' gene. In the mouse, at least one transcript of the host gene is also subject to genomic imprinting. Human retrogene orthologues are imprinted and we reveal that human host genes are not imprinted. This coincides with genomic rearrangements that occurred during primate evolution, which increase the separation between the retrogene DMRs and the host genes. To address the mechanisms governing imprinted retrogene expression, histone modifications were assayed at the DMRs. For the mouse retrogenes, the active mark H3K4me2 was associated with the unmethylated paternal allele, while the methylated maternal allele was enriched in repressive marks including H3K9me3 and H4K20me3. Two human retrogenes showed monoallelic enrichment of active, but not of repressive marks suggesting a partial uncoupling of the relationship between DNA methylation and repressive histone methylation, possibly due to the smaller size and lower CpG density of these DMRs. Finally, we show that the genes immediately flanking the host genes in mouse and human are biallelically expressed in a range of tissues, suggesting that these loci are distinct from large imprinted clusters.

Original language	English
Pages (from-to)	4577 - 4586
Number of pages	10
Journal	Nucleic Acids Research
Volume	39
Issue number	11
DOIs	https://doi.org/10.1093/nar/gkq1230
Publication status	Published - Jun 2011

Access to Document

10.1093/nar/gkq1230

Cite this

Monk, D., Arnaud, P., Frost, J. M., Wood, A. J., Cowley, M., Martin-Trujillo, A., Guillaumet-Adkins, A., Platas, I. I., Camprubi, C., Bourc'his, D., Feil, R., Moore, G. E., & Oakey, R. J. (2011). Human imprinted retrogenes exhibit non-canonical imprint chromatin signatures and reside in non-imprinted host genes. Nucleic Acids Research, 39(11), 4577 - 4586. https://doi.org/10.1093/nar/gkq1230

@article{7542748faaf6462db56965e9ba32b026,

title = "Human imprinted retrogenes exhibit non-canonical imprint chromatin signatures and reside in non-imprinted host genes",

abstract = "Imprinted retrotransposed genes share a common genomic organization including a promoter-associated differentially methylated region (DMR) and a position within the intron of a multi-exonic 'host' gene. In the mouse, at least one transcript of the host gene is also subject to genomic imprinting. Human retrogene orthologues are imprinted and we reveal that human host genes are not imprinted. This coincides with genomic rearrangements that occurred during primate evolution, which increase the separation between the retrogene DMRs and the host genes. To address the mechanisms governing imprinted retrogene expression, histone modifications were assayed at the DMRs. For the mouse retrogenes, the active mark H3K4me2 was associated with the unmethylated paternal allele, while the methylated maternal allele was enriched in repressive marks including H3K9me3 and H4K20me3. Two human retrogenes showed monoallelic enrichment of active, but not of repressive marks suggesting a partial uncoupling of the relationship between DNA methylation and repressive histone methylation, possibly due to the smaller size and lower CpG density of these DMRs. Finally, we show that the genes immediately flanking the host genes in mouse and human are biallelically expressed in a range of tissues, suggesting that these loci are distinct from large imprinted clusters.",

author = "David Monk and Philippe Arnaud and Frost, {Jennifer M.} and Wood, {Andrew J.} and Michael Cowley and Alejandro Martin-Trujillo and Amy Guillaumet-Adkins and Platas, {Isabel Iglesias} and Cristina Camprubi and Deborah Bourc'his and Robert Feil and Moore, {Gudrun E.} and Oakey, {Rebecca J.}",

year = "2011",

month = jun,

doi = "10.1093/nar/gkq1230",

language = "English",

volume = "39",

pages = "4577 -- 4586",

journal = "Nucleic Acids Research",

issn = "1362-4962",

publisher = "Oxford Univerity Press; Oxford",

number = "11",

}

Monk, D, Arnaud, P, Frost, JM, Wood, AJ , Cowley, M, Martin-Trujillo, A, Guillaumet-Adkins, A, Platas, II, Camprubi, C, Bourc'his, D, Feil, R, Moore, GE & Oakey, RJ 2011, 'Human imprinted retrogenes exhibit non-canonical imprint chromatin signatures and reside in non-imprinted host genes', Nucleic Acids Research, vol. 39, no. 11, pp. 4577 - 4586. https://doi.org/10.1093/nar/gkq1230

TY - JOUR

T1 - Human imprinted retrogenes exhibit non-canonical imprint chromatin signatures and reside in non-imprinted host genes

AU - Monk, David

AU - Arnaud, Philippe

AU - Frost, Jennifer M.

AU - Wood, Andrew J.

AU - Cowley, Michael

AU - Martin-Trujillo, Alejandro

AU - Guillaumet-Adkins, Amy

AU - Platas, Isabel Iglesias

AU - Camprubi, Cristina

AU - Bourc'his, Deborah

AU - Feil, Robert

AU - Moore, Gudrun E.

AU - Oakey, Rebecca J.

PY - 2011/6

Y1 - 2011/6

N2 - Imprinted retrotransposed genes share a common genomic organization including a promoter-associated differentially methylated region (DMR) and a position within the intron of a multi-exonic 'host' gene. In the mouse, at least one transcript of the host gene is also subject to genomic imprinting. Human retrogene orthologues are imprinted and we reveal that human host genes are not imprinted. This coincides with genomic rearrangements that occurred during primate evolution, which increase the separation between the retrogene DMRs and the host genes. To address the mechanisms governing imprinted retrogene expression, histone modifications were assayed at the DMRs. For the mouse retrogenes, the active mark H3K4me2 was associated with the unmethylated paternal allele, while the methylated maternal allele was enriched in repressive marks including H3K9me3 and H4K20me3. Two human retrogenes showed monoallelic enrichment of active, but not of repressive marks suggesting a partial uncoupling of the relationship between DNA methylation and repressive histone methylation, possibly due to the smaller size and lower CpG density of these DMRs. Finally, we show that the genes immediately flanking the host genes in mouse and human are biallelically expressed in a range of tissues, suggesting that these loci are distinct from large imprinted clusters.

AB - Imprinted retrotransposed genes share a common genomic organization including a promoter-associated differentially methylated region (DMR) and a position within the intron of a multi-exonic 'host' gene. In the mouse, at least one transcript of the host gene is also subject to genomic imprinting. Human retrogene orthologues are imprinted and we reveal that human host genes are not imprinted. This coincides with genomic rearrangements that occurred during primate evolution, which increase the separation between the retrogene DMRs and the host genes. To address the mechanisms governing imprinted retrogene expression, histone modifications were assayed at the DMRs. For the mouse retrogenes, the active mark H3K4me2 was associated with the unmethylated paternal allele, while the methylated maternal allele was enriched in repressive marks including H3K9me3 and H4K20me3. Two human retrogenes showed monoallelic enrichment of active, but not of repressive marks suggesting a partial uncoupling of the relationship between DNA methylation and repressive histone methylation, possibly due to the smaller size and lower CpG density of these DMRs. Finally, we show that the genes immediately flanking the host genes in mouse and human are biallelically expressed in a range of tissues, suggesting that these loci are distinct from large imprinted clusters.

U2 - 10.1093/nar/gkq1230

DO - 10.1093/nar/gkq1230

M3 - Article

SN - 1362-4962

VL - 39

SP - 4577

EP - 4586

JO - Nucleic Acids Research

JF - Nucleic Acids Research

IS - 11

ER -

Human imprinted retrogenes exhibit non-canonical imprint chromatin signatures and reside in non-imprinted host genes

Abstract

Access to Document

Fingerprint

Cite this