Stochastic imprinting in the progeny of Dnmt3L−/− females

The cis-acting regulatory sequences of imprinted genes are subject to germline-specific epigenetic modifications, the imprints, so that this class of genes is exclusively expressed from either the paternal or maternal allele in offspring. How genes are differentially marked in the germlines remains...

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Published in	Human molecular genetics Vol. 15; no. 4; pp. 589 - 598
Main Authors	Arnaud, Philippe, Hata, Kenichiro, Kaneda, Masahiro, Li, En, Sasaki, Hiroyuki, Feil, Robert, Kelsey, Gavin
Format	Journal Article
Language	English
Published	Oxford Oxford University Press 15.02.2006 Oxford Publishing Limited (England) Oxford University Press (OUP)
Subjects	Animals Biochemistry, Molecular Biology Biological and medical sciences Cancer DNA (Cytosine-5-)-Methyltransferases DNA (Cytosine-5-)-Methyltransferases - deficiency DNA Methylation Embryo, Mammalian Embryo, Mammalian - cytology Epistasis, Genetic Female Fundamental and applied biological sciences. Psychology Genetic Diseases, Inborn Genetic Diseases, Inborn - genetics Genetics of eukaryotes. Biological and molecular evolution Genomic Imprinting Genomic Imprinting - genetics Genomics Humans Life Sciences Mice Mice, Knockout Molecular and cellular biology Molecular biology Molecular Networks Oocytes Oocytes - cytology Progeny Female Genetics Genomic imprinting
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ISSN	0964-6906 1460-2083
DOI	10.1093/hmg/ddi475

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Abstract	The cis-acting regulatory sequences of imprinted genes are subject to germline-specific epigenetic modifications, the imprints, so that this class of genes is exclusively expressed from either the paternal or maternal allele in offspring. How genes are differentially marked in the germlines remains largely to be elucidated. Although the exact nature of the mark is not fully known, DNA methylation [at differentially methylated regions (DMRs)] appears to be a major, functional component. Recent data in mice indicate that Dnmt3a, an enzyme with de novo DNA methyltransferase activity, and the related protein Dnmt3L are required for methylation of imprinted loci in germ cells. Maternal methylation imprints, in particular, are strictly dependent on the presence of Dnmt3L. Here, we show that, unexpectedly, methylation imprints can be present in some progeny of Dnmt3L−/− females. This incomplete penetrance of the effect of Dnmt3L deficiency in oocytes is neither embryo nor locus specific, but stochastic. We establish that, when it occurs, methylation is present in both embryo and extra-embryonic tissues and results in a functional imprint. This suggests that this maternal methylation is inherited, directly or indirectly, from the gamete. Our results indicate that in the absence of Dnmt3L, factors such as Dnmt3a and possibly others can act alone to mark individual DMRs. However, establishment of appropriate maternal imprints at all loci does require a combination of all factors. This observation can provide a basis to understand mechanisms involved in some sporadic cases of imprinting-related diseases and polymorphic imprinting in human.
AbstractList	The cis-acting regulatory sequences of imprinted genes are subject to germline-specific epigenetic modifications, the imprints, so that this class of genes is exclusively expressed from either the paternal or maternal allele in offspring. How genes are differentially marked in the germlines remains largely to be elucidated. Although the exact nature of the mark is not fully known, DNA methylation [at differentially methylated regions (DMRs)] appears to be a major, functional component. Recent data in mice indicate that Dnmt3a, an enzyme with de novo DNA methyltransferase activity, and the related protein Dnmt3L are required for methylation of imprinted loci in germ cells. Maternal methylation imprints, in particular, are strictly dependent on the presence of Dnmt3L. Here, we show that, unexpectedly, methylation imprints can be present in some progeny of Dnmt3L−/− females. This incomplete penetrance of the effect of Dnmt3L deficiency in oocytes is neither embryo nor locus specific, but stochastic. We establish that, when it occurs, methylation is present in both embryo and extra-embryonic tissues and results in a functional imprint. This suggests that this maternal methylation is inherited, directly or indirectly, from the gamete. Our results indicate that in the absence of Dnmt3L, factors such as Dnmt3a and possibly others can act alone to mark individual DMRs. However, establishment of appropriate maternal imprints at all loci does require a combination of all factors. This observation can provide a basis to understand mechanisms involved in some sporadic cases of imprinting-related diseases and polymorphic imprinting in human. The cis-acting regulatory sequences of imprinted genes are subject to germline-specific epigenetic modifications, the imprints, so that this class of genes is exclusively expressed from either the paternal or maternal allele in offspring. How genes are differentially marked in the germlines remains largely to be elucidated. Although the exact nature of the mark is not fully known, DNA methylation [at differentially methylated regions (DMRs)] appears to be a major, functional component. Recent data in mice indicate that Dnmt3a, an enzyme with de novo DNA methyltransferase activity, and the related protein Dnmt3L are required for methylation of imprinted loci in germ cells. Maternal methylation imprints, in particular, are strictly dependent on the presence of Dnmt3L. Here, we show that, unexpectedly, methylation imprints can be present in some progeny of Dnmt3L(-/-) females. This incomplete penetrance of the effect of Dnmt3L deficiency in oocytes is neither embryo nor locus specific, but stochastic. We establish that, when it occurs, methylation is present in both embryo and extra-embryonic tissues and results in a functional imprint. This suggests that this maternal methylation is inherited, directly or indirectly, from the gamete. Our results indicate that in the absence of Dnmt3L, factors such as Dnmt3a and possibly others can act alone to mark individual DMRs. However, establishment of appropriate maternal imprints at all loci does require a combination of all factors. This observation can provide a basis to understand mechanisms involved in some sporadic cases of imprinting-related diseases and polymorphic imprinting in human. The cis-acting regulatory sequences of imprinted genes are subject to germline-specific epigenetic modifications, the imprints, so that this class of genes is exclusively expressed from either the paternal or maternal allele in offspring. How genes are differentially marked in the germlines remains largely to be elucidated. Although the exact nature of the mark is not fully known, DNA methylation [at differentially methylated regions (DMRs)] appears to be a major, functional component. Recent data in mice indicate that Dnmt3a, an enzyme with de novo DNA methyltransferase activity, and the related protein Dnmt3L are required for methylation of imprinted loci in germ cells. Maternal methylation imprints, in particular, are strictly dependent on the presence of Dnmt3L. Here, we show that, unexpectedly, methylation imprints can be present in some progeny of Dnmt3L(-/-) females. This incomplete penetrance of the effect of Dnmt3L deficiency in oocytes is neither embryo nor locus specific, but stochastic. We establish that, when it occurs, methylation is present in both embryo and extra-embryonic tissues and results in a functional imprint. This suggests that this maternal methylation is inherited, directly or indirectly, from the gamete. Our results indicate that in the absence of Dnmt3L, factors such as Dnmt3a and possibly others can act alone to mark individual DMRs. However, establishment of appropriate maternal imprints at all loci does require a combination of all factors. This observation can provide a basis to understand mechanisms involved in some sporadic cases of imprinting-related diseases and polymorphic imprinting in human.The cis-acting regulatory sequences of imprinted genes are subject to germline-specific epigenetic modifications, the imprints, so that this class of genes is exclusively expressed from either the paternal or maternal allele in offspring. How genes are differentially marked in the germlines remains largely to be elucidated. Although the exact nature of the mark is not fully known, DNA methylation [at differentially methylated regions (DMRs)] appears to be a major, functional component. Recent data in mice indicate that Dnmt3a, an enzyme with de novo DNA methyltransferase activity, and the related protein Dnmt3L are required for methylation of imprinted loci in germ cells. Maternal methylation imprints, in particular, are strictly dependent on the presence of Dnmt3L. Here, we show that, unexpectedly, methylation imprints can be present in some progeny of Dnmt3L(-/-) females. This incomplete penetrance of the effect of Dnmt3L deficiency in oocytes is neither embryo nor locus specific, but stochastic. We establish that, when it occurs, methylation is present in both embryo and extra-embryonic tissues and results in a functional imprint. This suggests that this maternal methylation is inherited, directly or indirectly, from the gamete. Our results indicate that in the absence of Dnmt3L, factors such as Dnmt3a and possibly others can act alone to mark individual DMRs. However, establishment of appropriate maternal imprints at all loci does require a combination of all factors. This observation can provide a basis to understand mechanisms involved in some sporadic cases of imprinting-related diseases and polymorphic imprinting in human.
Author	Arnaud, Philippe Li, En Sasaki, Hiroyuki Feil, Robert Kelsey, Gavin Kaneda, Masahiro Hata, Kenichiro
Author_xml	– sequence: 1 givenname: Philippe surname: Arnaud fullname: Arnaud, Philippe organization: Institute of Molecular Genetics, CNRS UMR-5535 and University of Montpellier-II, 1919, Route de Mende, 34090 Montpellier, France – sequence: 2 givenname: Kenichiro surname: Hata fullname: Hata, Kenichiro organization: Division of Human Genetics, Department of Integrated Genetics, National Institute of Genetics, Research Organization of Information and Systems, 1111 Yata, Mishima 411-8540, Japan – sequence: 3 givenname: Masahiro surname: Kaneda fullname: Kaneda, Masahiro organization: Division of Human Genetics, Department of Integrated Genetics, National Institute of Genetics, Research Organization of Information and Systems, 1111 Yata, Mishima 411-8540, Japan – sequence: 4 givenname: En surname: Li fullname: Li, En organization: Department of Medicine, Cardiovascular Research Center, Massachusetts General Hospital, Harvard Medical School, Charleston, MA 02129, USA and – sequence: 5 givenname: Hiroyuki surname: Sasaki fullname: Sasaki, Hiroyuki organization: Division of Human Genetics, Department of Integrated Genetics, National Institute of Genetics, Research Organization of Information and Systems, 1111 Yata, Mishima 411-8540, Japan – sequence: 6 givenname: Robert surname: Feil fullname: Feil, Robert organization: Institute of Molecular Genetics, CNRS UMR-5535 and University of Montpellier-II, 1919, Route de Mende, 34090 Montpellier, France – sequence: 7 givenname: Gavin surname: Kelsey fullname: Kelsey, Gavin organization: Laboratory of Developmental Genetics and Imprinting, The Babraham Institute, Cambridge, UK
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Snippet	The cis-acting regulatory sequences of imprinted genes are subject to germline-specific epigenetic modifications, the imprints, so that this class of genes is...
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SubjectTerms	Animals Biochemistry, Molecular Biology Biological and medical sciences Cancer DNA (Cytosine-5-)-Methyltransferases DNA (Cytosine-5-)-Methyltransferases - deficiency DNA Methylation Embryo, Mammalian Embryo, Mammalian - cytology Epistasis, Genetic Female Fundamental and applied biological sciences. Psychology Genetic Diseases, Inborn Genetic Diseases, Inborn - genetics Genetics of eukaryotes. Biological and molecular evolution Genomic Imprinting Genomic Imprinting - genetics Genomics Humans Life Sciences Mice Mice, Knockout Molecular and cellular biology Molecular biology Molecular Networks Oocytes Oocytes - cytology
Title	Stochastic imprinting in the progeny of Dnmt3L−/− females
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