Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes

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JOURNAL ARTICLES

Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes

W Dean, L Bowden, A Aitchison, J Klose, T Moore, JJ Meneses, W Reik and R Feil
Laboratory of Developmental Genetics Programme, The Babraham Institute, Babraham Hall, Cambridge CB2 4AT, UK.

In vitro manipulation of preimplantation mammalian embryos can influence differentiation and growth at later stages of development. In the mouse, culture of embryonic stem (ES) cells affects their totipotency and may give rise to fetal abnormalities. To investigate whether this is associated with epigenetic alterations in imprinted genes, we analysed two maternally expressed genes (Igf2r, H19) and two paternally expressed genes (Igf2, U2af1-rs1) in ES cells and in completely ES cell-derived fetuses. Altered allelic methylation patterns were detected in all four genes, and these were consistently associated with allelic changes in gene expression. All the methylation changes that had arisen in the ES cells persisted on in vivo differentiation to fetal stages. Alterations included loss of methylation with biallelic expression of U2af1-rs1, maternal methylation and predominantly maternal expression of Igf2, and biallelic methylation and expression of Igf2r. In many of the ES fetuses, the levels of H19 expression were strongly reduced, and this biallelic repression was associated with biallellic methylation of the H19 upstream region. Surprisingly, biallelic H19 repression was not associated with equal levels of Igf2 expression from both parental chromosomes, but rather with a strong activation of the maternal Igf2 allele. ES fetuses derived from two of the four ES lines appeared developmentally compromised, with polyhydramnios, poor mandible development and interstitial bleeding and, in chimeric fetuses, the degree of chimerism correlated with increased fetal mass. Our study establishes a model for how early embryonic epigenetic alterations in imprinted genes persist to later developmental stages, and are associated with aberrant phenotypes.

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				A. Wagschal, H. G. Sutherland, K. Woodfine, A. Henckel, K. Chebli, R. Schulz, R. J. Oakey, W. A. Bickmore, and R. Feil G9a Histone Methyltransferase Contributes to Imprinting in the Mouse Placenta Mol. Cell. Biol., February 1, 2008; 28(3): 1104 - 1113. [Abstract] [Full Text] [PDF]

				K.-P. Kim, A. Thurston, C. Mummery, D. Ward-van Oostwaard, H. Priddle, C. Allegrucci, C. Denning, and L. Young Gene-specific vulnerability to imprinting variability in human embryonic stem cell lines Genome Res., December 1, 2007; 17(12): 1731 - 1742. [Abstract] [Full Text] [PDF]

				P. J. Rugg-Gunn, A. C. Ferguson-Smith, and R. A. Pedersen Status of genomic imprinting in human embryonic stem cells as revealed by a large cohort of independently derived and maintained lines Hum. Mol. Genet., October 15, 2007; 16(R2): R243 - R251. [Abstract] [Full Text] [PDF]

				V. Keros, K. Hultenby, B. Borgstrom, M. Fridstrom, K. Jahnukainen, and O. Hovatta Methods of cryopreservation of testicular tissue with viable spermatogonia in pre-pubertal boys undergoing gonadotoxic cancer treatment Hum. Reprod., May 1, 2007; 22(5): 1384 - 1395. [Abstract] [Full Text] [PDF]

				C. Allegrucci and L.E. Young Differences between human embryonic stem cell lines Hum. Reprod. Update, March 1, 2007; 13(2): 103 - 120. [Abstract] [Full Text] [PDF]

				S. Mitalipov, L. Clepper, H. Sritanaudomchai, A. Fujimoto, and D. Wolf Methylation Status of Imprinting Centers for H19/IGF2 and SNURF/SNRPN in Primate Embryonic Stem Cells Stem Cells, March 1, 2007; 25(3): 581 - 588. [Abstract] [Full Text] [PDF]

				S. Eckardt, N. A. Leu, H. L. Bradley, H. Kato, K. D. Bunting, and K. J. McLaughlin Hematopoietic reconstitution with androgenetic and gynogenetic stem cells Genes & Dev., February 15, 2007; 21(4): 409 - 419. [Abstract] [Full Text] [PDF]

				T. Furusawa, M. Ikeda, F. Inoue, K. Ohkoshi, T. Hamano, and T. Tokunaga Gene Expression Profiling of Mouse Embryonic Stem Cell Subpopulations Biol Reprod, October 1, 2006; 75(4): 555 - 561. [Abstract] [Full Text] [PDF]

				T. Shinohara, M. Kato, M. Takehashi, J. Lee, S. Chuma, N. Nakatsuji, M. Kanatsu-Shinohara, and M. Hirabayashi Rats produced by interspecies spermatogonial transplantation in mice and in vitro microinsemination PNAS, September 12, 2006; 103(37): 13624 - 13628. [Abstract] [Full Text] [PDF]

				T Amano, M Gertsenstein, A Nagy, H Kurihara, and H Suzuki Nuclear transfer reprogramming does not improve the low developmental potency of embryonic stem cells induced by long-term culture. Reproduction, August 1, 2006; 132(2): 257 - 263. [Abstract] [Full Text] [PDF]

				S. Kurukuti, V. K. Tiwari, G. Tavoosidana, E. Pugacheva, A. Murrell, Z. Zhao, V. Lobanenkov, W. Reik, and R. Ohlsson CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2 PNAS, July 11, 2006; 103(28): 10684 - 10689. [Abstract] [Full Text] [PDF]

				M. Kanatsu-Shinohara, M. Ikawa, M. Takehashi, N. Ogonuki, H. Miki, K. Inoue, Y. Kazuki, J. Lee, S. Toyokuni, M. Oshimura, et al. From the Cover: Production of knockout mice by random or targeted mutagenesis in spermatogonial stem cells PNAS, May 23, 2006; 103(21): 8018 - 8023. [Abstract] [Full Text] [PDF]

				A. Fujimoto, S. M. Mitalipov, H.-C. Kuo, and D. P. Wolf Aberrant Genomic Imprinting in Rhesus Monkey Embryonic Stem Cells Stem Cells, March 1, 2006; 24(3): 595 - 603. [Abstract] [Full Text] [PDF]

				J. Cai, J. Chen, Y. Liu, T. Miura, Y. Luo, J. F. Loring, W. J. Freed, M. S. Rao, and X. Zeng Assessing Self-Renewal and Differentiation in Human Embryonic Stem Cell Lines Stem Cells, March 1, 2006; 24(3): 516 - 530. [Abstract] [Full Text] [PDF]

				B. W. Sun, A. C. Yang, Y. Feng, Y. J. Sun, Y. f. Zhu, Y. Zhang, H. Jiang, C. L. Li, F. R. Gao, Z. H. Zhang, et al. Temporal and parental-specific expression of imprinted genes in a newly derived Chinese human embryonic stem cell line and embryoid bodies Hum. Mol. Genet., January 1, 2006; 15(1): 65 - 75. [Abstract] [Full Text] [PDF]

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				T. Li, T. H. Vu, G. A. Ulaner, E. Littman, J.-Q. Ling, H.-L. Chen, J.-F. Hu, B. Behr, L. Giudice, and A. R. Hoffman IVF results in de novo DNA methylation and histone methylation at an Igf2-H19 imprinting epigenetic switch Mol. Hum. Reprod., September 1, 2005; 11(9): 631 - 640. [Abstract] [Full Text] [PDF]

				P. J. Tesar Derivation of germ-line-competent embryonic stem cell lines from preblastocyst mouse embryos PNAS, June 7, 2005; 102(23): 8239 - 8244. [Abstract] [Full Text] [PDF]

				A. Fujimoto, S.M. Mitalipov, L.L. Clepper, and D.P. Wolf Development of a monkey model for the study of primate genomic imprinting Mol. Hum. Reprod., June 1, 2005; 11(6): 413 - 422. [Abstract] [Full Text] [PDF]

				T. Imamura, A. Kerjean, T. Heams, J.-J. Kupiec, C. Thenevin, and A. Paldi Dynamic CpG and Non-CpG Methylation of the Peg1/Mest Gene in the Mouse Oocyte and Preimplantation Embryo J. Biol. Chem., May 20, 2005; 280(20): 20171 - 20175. [Abstract] [Full Text] [PDF]

				T. Takeuchi, Q. V. Neri, Y. Katagiri, Z. Rosenwaks, and G. D. Palermo Effect of Treating Induced Mitochondrial Damage on Embryonic Development and Epigenesis Biol Reprod, March 1, 2005; 72(3): 584 - 592. [Abstract] [Full Text] [PDF]

				C. Allegrucci, A. Thurston, E. Lucas, and L. Young Epigenetics and the germline Reproduction, February 1, 2005; 129(2): 137 - 149. [Abstract] [Full Text] [PDF]

				C. Pantoja, L. de los Rios, A. Matheu, F. Antequera, and M. Serrano Inactivation of Imprinted Genes Induced by Cellular Stress and Tumorigenesis Cancer Res., January 1, 2005; 65(1): 26 - 33. [Abstract] [Full Text] [PDF]

				T. P. Fleming, W. Y. Kwong, R. Porter, E. Ursell, I. Fesenko, A. Wilkins, D. J. Miller, A. J. Watkins, and J. J. Eckert The Embryo and Its Future Biol Reprod, October 1, 2004; 71(4): 1046 - 1054. [Abstract] [Full Text] [PDF]

				M. R. W. Mann, S. S. Lee, A. S. Doherty, R. I. Verona, L. D. Nolen, R. M. Schultz, and M. S. Bartolomei Selective loss of imprinting in the placenta following preimplantation development in culture Development, August 1, 2004; 131(15): 3727 - 3735. [Abstract] [Full Text] [PDF]

				S. V. Dindot, P. W. Farin, C. E. Farin, J. Romano, S. Walker, C. Long, and J. A. Piedrahita Epigenetic and Genomic Imprinting Analysis in Nuclear Transfer Derived Bos gaurus/Bos taurus Hybrid Fetuses Biol Reprod, August 1, 2004; 71(2): 470 - 478. [Abstract] [Full Text] [PDF]