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PMID: 16614068 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Limited evolutionary conservation of imprinting in the human placenta.

Monk D, Arnaud P, Apostolidou S, Hills FA, Kelsey G, Stanier P, Feil R, Moore GE

Abstract

The epigenetic phenomenon of genomic imprinting provides an additional level of gene regulation that is confined to a limited number of genes, frequently, but not exclusively, important for embryonic development. The evolution and maintenance of imprinting has been linked to the balance between the allocation of maternal resources to the developing fetus and the mother's well being. Genes that are imprinted in both the embryo and extraembryonic tissues show extensive conservation between a mouse and a human. Here we examine the human orthologues of mouse genes imprinted only in the placenta, assaying allele-specific expression and epigenetic modifications. The genes from the KCNQ1 domain and the isolated human orthologues of the imprinted genes Gatm and Dcn all are expressed biallelically in the human, from first-trimester trophoblast through to term. This lack of imprinting is independent of promoter CpG methylation and correlates with the absence of the allelic histone modifications dimethylation of lysine-9 residue of H3 (H3K9me2) and trimethylation of lysine-27 residue of H3 (H3K27me3). These specific histone modifications are thought to contribute toward regulation of imprinting in the mouse. Genes from the IGF2R domain show polymorphic concordant expression in the placenta, with imprinting demonstrated in only a minority of samples. Together these findings have important implications for understanding the evolution of mammalian genomic imprinting. Because most human pregnancies are singletons, this absence of competition might explain the comparatively relaxed need in the human for placental-specific imprinting.

MeSH Terms
Alleles Amidinotransferases/genetics Animals Base Sequence DNA/genetics,metabolism DNA Methylation Decorin Epigenesis, Genetic Evolution, Molecular Extracellular Matrix Proteins/genetics Female Gene Expression Regulation, Developmental Genomic Imprinting Histones/metabolism Humans KCNQ1 Potassium Channel/genetics Male Mice Multigene Family Placenta/metabolism Polymorphism, Genetic Pregnancy Proteoglycans/genetics Receptor, IGF Type 2/genetics
Chemicals
DCN protein, human Dcn protein, mouse Decorin Extracellular Matrix Proteins Histones KCNQ1 Potassium Channel KCNQ1 protein, human Proteoglycans Receptor, IGF Type 2 DNA Amidinotransferases glycine amidinotransferase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Monk D
Institute of Reproductive and Developmental Biology, Imperial College London, London W12 0NN, United Kingdom. dmonk@imperial.ac.uk
Arnaud P
Apostolidou S
Hills F A
Kelsey G
Stanier P
Feil R
Moore G E
References (41)
41 references, click to expand
  1. Allelic IGF2R repression does not correlate with expression of antisense RNA in human extraembryonic tissues.
    Genomics. 2001 May 1;73(3):331-7 PMID: 11350125
  2. Domain regulation of imprinting cluster in Kip2/Lit1 subdomain on mouse chromosome 7F4/F5: large-scale DNA methylation analysis reveals that DMR-Lit1 is a putative imprinting control region.
    Genome Res. 2002 Dec;12(12):1860-70 PMID: 12466290
  3. The histone code regulating expression of the imprinted mouse Igf2r gene.
    Endocrinology. 2003 Dec;144(12):5658-70 PMID: 12975326
  4. Resourceful imprinting.
    Nature. 2004 Nov 4;432(7013):53-7 PMID: 15525980
  5. A differentially methylated region within the gene Kcnq1 functions as an imprinted promoter and silencer.
    Hum Mol Genet. 2003 Feb 1;12(3):283-94 PMID: 12554682
  6. M6P/IGF2R imprinting evolution in mammals.
    Mol Cell. 2000 Apr;5(4):707-16 PMID: 10882106
  7. Absence of an obvious molecular imprinting mechanism in a human fetus with monoallelic IGF2R expression.
    Biochem Biophys Res Commun. 1998 Apr 7;245(1):272-7 PMID: 9535821
  8. Functional polymorphism in the parental imprinting of the human IGF2R gene.
    Biochem Biophys Res Commun. 1993 Dec 15;197(2):747-54 PMID: 8267611
  9. Regulation of supply and demand for maternal nutrients in mammals by imprinted genes.
    J Physiol. 2003 Feb 15;547(Pt 1):35-44 PMID: 12562908
  10. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation.
    Nat Genet. 2004 Dec;36(12):1291-5 PMID: 15516931
  11. Lsh controls silencing of the imprinted Cdkn1c gene.
    Development. 2005 Feb;132(4):635-44 PMID: 15647320
  12. Genomic imprinting of Mash2, a mouse gene required for trophoblast development.
    Nat Genet. 1995 Mar;9(3):235-42 PMID: 7773285
  13. X-inactivation patterns in human embryonic and extra-embryonic tissues.
    Placenta. 2003 Feb-Mar;24(2-3):270-5 PMID: 12566254
  14. Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal.
    Cell. 1993 Apr 9;73(1):61-71 PMID: 8462104
  15. The non-coding Air RNA is required for silencing autosomal imprinted genes.
    Nature. 2002 Feb 14;415(6873):810-3 PMID: 11845212
  16. An antisense RNA regulates the bidirectional silencing property of the Kcnq1 imprinting control region.
    Mol Cell Biol. 2004 Sep;24(18):7855-62 PMID: 15340049
  17. Beckwith-Wiedemann syndrome demonstrates a role for epigenetic control of normal development.
    Hum Mol Genet. 2003 Apr 1;12 Spec No 1:R61-8 PMID: 12668598
  18. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1.
    Nat Genet. 2002 Nov;32(3):426-31 PMID: 12410230
  19. Imprinted expression of the Igf2r gene depends on an intronic CpG island.
    Nature. 1997 Oct 16;389(6652):745-9 PMID: 9338788
  20. Syntenic organization of the mouse distal chromosome 7 imprinting cluster and the Beckwith-Wiedemann syndrome region in chromosome 11p15.5.
    Hum Mol Genet. 1998 Jul;7(7):1149-59 PMID: 9618174
  21. Allele-specific histone lysine methylation marks regulatory regions at imprinted mouse genes.
    EMBO J. 2002 Dec 2;21(23):6560-70 PMID: 12456662
  22. A census of mammalian imprinting.
    Trends Genet. 2005 Aug;21(8):457-65 PMID: 15990197
  23. XIST expression in human oocytes and preimplantation embryos.
    Am J Hum Genet. 1997 Jul;61(1):33-9 PMID: 9245982
  24. Epimutation of the telomeric imprinting center region on chromosome 11p15 in Silver-Russell syndrome.
    Nat Genet. 2005 Sep;37(9):1003-7 PMID: 16086014
  25. DNA methylation is linked to deacetylation of histone H3, but not H4, on the imprinted genes Snrpn and U2af1-rs1.
    Mol Cell Biol. 2001 Aug;21(16):5426-36 PMID: 11463825
  26. Genomic imprinting in mammalian development: a parental tug-of-war.
    Trends Genet. 1991 Feb;7(2):45-9 PMID: 2035190
  27. Bidirectional action of the Igf2r imprint control element on upstream and downstream imprinted genes.
    Genes Dev. 2001 Sep 15;15(18):2361-6 PMID: 11562346
  28. Imprinting of PEG1/MEST isoform 2 in human placenta.
    Placenta. 2006 Feb-Mar;27(2-3):119-26 PMID: 16338457
  29. Promoter-restricted histone code, not the differentially methylated DNA regions or antisense transcripts, marks the imprinting status of IGF2R in human and mouse.
    Hum Mol Genet. 2004 Oct 1;13(19):2233-45 PMID: 15294879
  30. Asb4, Ata3, and Dcn are novel imprinted genes identified by high-throughput screening using RIKEN cDNA microarray.
    Biochem Biophys Res Commun. 2002 Feb 8;290(5):1499-505 PMID: 11820791
  31. Genomic imprinting of IGF2, p57(KIP2) and PEG1/MEST in a marsupial, the tammar wallaby.
    Mech Dev. 2005 Feb;122(2):213-22 PMID: 15652708
  32. Molecular links between X-inactivation and autosomal imprinting: X-inactivation as a driving force for the evolution of imprinting?
    Curr Biol. 2003 Mar 18;13(6):R242-54 PMID: 12646153
  33. Multipoint analysis of human chromosome 11p15/mouse distal chromosome 7: inclusion of H19/IGF2 in the minimal WT2 region, gene specificity of H19 silencing in Wilms' tumorigenesis and methylation hyper-dependence of H19 imprinting.
    Hum Mol Genet. 1999 Jul;8(7):1337-52 PMID: 10369881
  34. Gatm, a creatine synthesis enzyme, is imprinted in mouse placenta.
    Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4622-7 PMID: 12671064
  35. Expression of Xist during mouse development suggests a role in the initiation of X chromosome inactivation.
    Cell. 1993 Jan 29;72(2):171-82 PMID: 8425217
  36. Co-evolution of X-chromosome inactivation and imprinting in mammals.
    Nat Rev Genet. 2005 May;6(5):403-10 PMID: 15818385
  37. Site-specific analysis of histone methylation and acetylation.
    Methods Mol Biol. 2004;287:99-120 PMID: 15273407
  38. Genome imprinting regulated by the mouse Polycomb group protein Eed.
    Nat Genet. 2003 Apr;33(4):502-7 PMID: 12627233
  39. Genomic imprinting: intricacies of epigenetic regulation in clusters.
    Annu Rev Cell Dev Biol. 2003;19:237-59 PMID: 14570570
  40. Parental origin-specific expression of Mash2 is established at the time of implantation with its imprinting mechanism highly resistant to genome-wide demethylation.
    Mech Dev. 1999 Sep;87(1-2):129-42 PMID: 10495277
  41. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes.
    Nat Genet. 2004 Dec;36(12):1296-300 PMID: 15516932
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2006-04-25
Epub
2006-00-13
Pages
6623-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1564202
Subset
IM
Grants
Wellcome Trust · United Kingdom
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