Modulation of imprinted gene network in placenta results in normal development of in vitro manipulated mouse embryos

Human Molecular Genetics

Volumn 19, Issue 9, 2010, Pages 1779-1790

  Fauque, Patricia ^a,b   Ripoche, Marie Anne ^b   Tost, Jörg ^c   Journot, Laurent ^d   Gabory, Anne ^b   Busato, Florence ^c   Le Digarcher, Anne ^d   Mondon, Françoise ^b   Gut, Ivo ^c   Jouannet, Pierre ^a   Vaiman, Daniel ^b   Dandolo, Luisa ^b   Jammes, Hélène ^b,e  

^a INSERM   (France)

^b INSTITUT COCHIN   (France)

^c CENTRE NATIONAL DE GÉNOTYPAGE   (France)

^d INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^e ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; MESSENGER RNA; PROTEIN DIO3; PROTEIN DLK1; RNA H19; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; EMBRYO CULTURE; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION; GENOME IMPRINTING; IN VITRO STUDY; MALE; MATING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLACENTA; PRIORITY JOURNAL; PSEUDOPREGNANCY; PYROSEQUENCING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; DNA METHYLATION; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; GENE COMPONENTS; GENE REGULATORY NETWORKS; GENOMIC IMPRINTING; INSULIN-LIKE GROWTH FACTOR II; MICE; PLACENTA; PREGNANCY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, UNTRANSLATED;

EID: 77952516401     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq059     Document Type: Article

References (62)

1. Andersen, A.N., Goossens, V., Ferraretti, A.P., Bhattacharya, S., Felberbaum, R., de Mouzon, J. and Nygren, K.G. (2008) Assisted reproductive technology in Europe, 2004: results generated from European registers by ESHRE. Hum. Reprod, 23, 756-771.
2. Wright, V.C., Chang, J., Jeng, G. and Macaluso, M. (2008) Assisted reproductive technology surveillance-United States, 2005. MMWR Surveill. Summ., 57, 1-23.
3. Hansen, M., Kurinczuk, J.J., Bower, C. and Webb, S. (2002) The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization. N. Engl. J. Med., 346, 725-730.
4. Schieve, L.A., Meikle, S.F., Ferre, C., Peterson, H.B., Jeng, G. and Wilcox, L.S. (2002) Low and very low birth weight in infants conceived with use of assisted reproductive technology. N. Engl. J. Med., 346, 731-737.
5. DeBaun, M.R., Niemitz, E.L. and Feinberg, A.P. (2003) Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am. J. Hum. Genet., 72, 156-160.
6. Gicquel, C., Gaston, V., Mandelbaum, J., Siffroi, J.P., Flahault, A. and Le Bouc, Y. (2003) In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene. Am. J. Hum. Genet., 72, 1338-1341.
7. Maher, E.R., Brueton, L.A., Bowdin, S.C., Luharia, A., Cooper, W., Cole, T.R., Macdonald, F., Sampson, J.R., Barratt, C.L., Reik, W. et al. (2003) Beckwith-Wiedemann syndrome and assisted reproduction technology (ART). J. Med. Genet., 40, 62-64.
8. Ludwig, H. (2005) Archives of gynecology and obstetrics: 135 years. Arch. Gynecol. Obstet., 271,1-5.
9. Halliday, J., Oke, K., Breheny, S., Algar, E. and J. Amor, D. (2004) Beckwith-Wiedemann syndrome and IVF: a case-control study. Am. J. Hum. Genet., 75, 526-528.
10. Orstavik, K.H., Eiklid, K., van der Hagen, C.B., Spetalen, S., Kierulf, K., Skjeldal, O. and Buiting, K. (2003) Another case of imprinting defect in a girl with Angelman syndrome who was conceived by intracytoplasmic semen injection. Am. J. Hum. Genet., 72, 218-219.
11. Cox, G.F., Burger, J., Lip, V., Mau, U.A., Sperling, K., Wu, B.L. and Horsthemke, B. (2002) Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am. J. Hum. Genet., 71, 162-164.
12. Bliek, J., Terhal, P., van den Bogaard, M.J., Maas, S., Hamel, B., Salieb-Beugelaar, G., Simon, M., Letteboer, T., van der Smagt, J., Kroes, H. et al. (2006) Hypomethylation of the H19 gene causes not only Silver-Russell syndrome (SRS) but also isolated asymmetry or an SRS-like phenotype. Am. J. Hum. Genet., 78, 604-614.
13. Kagami, M., Nagai, T., Fukami, M., Yamazawa, K. and Ogata, T. (2007) Silver-Russell syndrome in a girl born after in vitro fertilization: partial hypermethylation at the differentially methylated region of PEG1/MEST. J. Assist. Reprod. Genet., 24, 131-136.
14. Holmes, R. and Soloway, P.D. (2006) Regulation of imprinted DNA methylation. Cytogenet. Genome Res., 113, 122-129.
15. Lewis, A. and Reik, W. (2006) How imprinting centres work. Cytogenet. Genome Res., 113, 81-89.
16. Beechey, C.V., Blake, A. and Peters, J. (2008) Mouse imprinting data and references. http://www.har.mrc.ac.uk/research/genomic_imprinting/.
17. Reik, W. and Walter, J. (2001) Evolution of imprinting mechanisms: the battle of the sexes begins in the zygote. Nat. Genet., 27, 255-256.
18. Fauque, P., Jouannet, P., Lesaffre, C., Ripoche, M.A., Dandolo, L., Vaiman, D. and Jammes, H. (2007) Assisted Reproductive Technology affects developmental kinetics, H19 Imprinting Control Region methylation and H19 gene expression in individual mouse embryos. BMC Dev. Biol., 7, 116.
19. Doherty, A.S., Mann, M.R., Tremblay, K.D., Bartolomei, M.S. and Schultz, R.M. (2000) Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod., 62, 1526-1535.
20. Sasaki, H., Ferguson-Smith, A.C., Shum, A.S., Barton, S.C. and Surani, M.A. (1995) Temporal and spatial regulation of H19 imprinting in normal and uniparental mouse embryos. Development, 121, 4195-4202.
21. Varrault, A., Gueydan, C., Delalbre, A., Bellmann, A., Houssami, S., Aknin, C., Severac, D., Chotard, L., Kahli, M., Le Digarcher, A. et al. (2006) Zac1 regulates an imprinted gene network critically involved in the control of embryonic growth. Dev. Cell, 11, 711-722.
22. Gabory, A., Ripoche, M.A., Le Digarcher, A., Watrin, F., Ziyyat, A., Forne, T., Jammes, H., Ainscough, J.F., Surani, M.A., Journot, L. et al. (2009) H19 acts as a trans regulator of the imprinted gene network controlling growth in mice. Development, 136, 3413-3421.
23. Nagy, A., Vintersten, K. and Behringer, R. (2003) Manipulating the Mouse Embryo: a Laboratory Manual., 3rd edn.
24. Laissue, P., Burgio, G., l'Hote, D., Renault, G., Marchiol-Fournigault, C., Fradelizi, D., Fellous, M., Serres, C., Montagutelli, X., Monget, P. et al. (2009) Identification of Quantitative Trait Loci responsible for embryonic lethality in mice assessed by ultrasonography. Int. J. Dev. Biol., 53, 623-629.
25. Tost, J. and Gut, I.G. (2007) DNA methylation analysis by pyrosequencing. Nat. Protoc., 2, 2265-2275.
26. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol., 3, RESEARCH0034.
27. Leighton, P.A., Ingram, R.S., Eggenschwiler, J., Efstratiadis, A. and Tilghman, S.M. (1995) Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature, 375, 34-39.
28. Eggenschwiler, J., Ludwig, T., Fisher, P., Leighton, P.A., Tilghman, S.M. and Efstratiadis, A. (1997) Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith-Wiedemann and Simpson-Golabi-Behmel syndromes. Genes Dev., 11, 3128-3142.
29. Reik, W., Constancia, M., Fowden, A., Anderson, N., Dean, W., Ferguson-Smith, A., Tycko, B. and Sibley, C. (2003) Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J. Physiol., 547, 35-44.
30. Khosla, S., Dean, W., Brown, D., Reik, W. and Feil, R. (2001) Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol. Reprod., 64, 918-926.
31. Li, T., Vu, T.H., Ulaner, G.A., Littman, E., Ling, J.Q., Chen, H.L., Hu, J.F., Behr, B., Giudice, L. and Hoffman, A.R. (2005) IVF results in de novo DNA methylation and histone methylation at an Igf2-H19 imprinting epigenetic switch. Mol. Hum. Reprod., 11, 631-640.
32. Mann, M.R., Chung, Y.G., Nolen, L.D., Verona, R.I., Latham, K.E. and Bartolomei, M.S. (2003) Disruption of imprinted gene methylation and expression in cloned preimplantation stage mouse embryos. Biol. Reprod., 69, 902-914.
33. Rivera, R.M., Stein, P., Weaver, J.R., Mager, J., Schultz, R.M. and Bartolomei, M.S. (2008) Manipulations of mouse embryos prior to implantation result in aberrant expression of imprinted genes on day 9.5 of development. Hum. Mol. Genet., 17, 1-14.
34. Tost, J., El Abdalaoui, H. and Gut, I.G. (2006) Serial pyrosequencing for quantitative DNA methylation analysis. Biotechniques, 40, 721-722. 724, 726.
35. Moore, T., Constancia, M., Zubair, M., Bailleul, B., Feil, R., Sasaki, H. and Reik, W. (1997) Multiple imprinted sense and antisense transcripts, differential methylation and tandem repeats in a putative imprinting control region upstream of mouse Igf2. Proc. Natl Acad. Sci. USA, 94, 12509-12514.
36. Murrell, A., Ito, Y., Verde, G., Huddleston, J., Woodfine, K., Silengo, M.C., Spreafico, F., Perotti, D., De Crescenzo, A., Sparago, A. et al. (2008) Distinct methylation changes at the IGF2-H19 locus in congenital growth disorders and cancer. PLoS ONE, 3, e1849.
37. Lopes, S., Lewis, A., Hajkova, P., Dean, W., Oswald, J., Forne, T., Murrell, A., Constancia, M., Bartolomei, M., Walter, J. et al. (2003) Epigenetic modifications in an imprinting cluster are controlled by a hierarchy of DMRs suggesting long-range chromatin interactions. Hum. Mol. Genet., 12, 295-305.
38. Umlauf, D., Goto, Y., Cao, R., Cerqueira, F., Wagschal, A., Zhang, Y. and Feil, R. (2004) Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat. Genet., 36, 1296-1300.
39. Mann, M.R., Lee, S.S., Doherty, A.S., Verona, R.I., Nolen, L.D., Schultz, R.M. and Bartolomei, M.S. (2004) Selective loss of imprinting in the placenta following preimplantation development in culture. Development, 131, 3727-3735.
40. Buffat, C., Boubred, F., Mondon, F., Chelbi, S.T., Feuerstein, J.M., Lelievre-Pegorier, M., Vaiman, D. and Simeoni, U. (2007) Kidney gene expression analysis in a rat model of intrauterine growth restriction reveals massive alterations of coagulation genes. Endocrinology, 148, 5549-5557.
41. Leighton, P.A., Saam, J.R., Ingram, R.S., Stewart, C.L. and Tilghman, S.M. (1995) An enhancer deletion affects both H19 and Igf2 expression. Genes Dev., 9, 2079-2089.
42. Poirier, F., Chan, C.T., Timmons, P.M., Robertson, E.J., Evans, M.J. and Rigby, P.W. (1991) The murine H19 gene is activated during embryonic stem cell differentiation in vitro and at the time of implantation in the developing embryo. Development, 113, 1105-1114.
43. DeChiara, T.M., Efstratiadis, A. and Robertson, E.J. (1990) A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature, 345, 78-80.
44. Coan, P.M., Fowden, A.L., Constancia, M., Ferguson-Smith, A.C., Burton, G.J. and Sibley, C.P. (2008) Disproportional effects of Igf2 knockout on placental morphology and diffusional exchange characteristics in the mouse. J. Physiol., 586, 5023-5032.
45. Ludwig, T., Eggenschwiler, J., Fisher, P., D'Ercole, A.J., Davenport, M.L. and Efstratiadis, A. (1996) Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev. Biol., 177, 517-535.
46. Lau, M.M., Stewart, C.E., Liu, Z., Bhatt, H., Rotwein, P. and Stewart, C.L. (1994) Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev., 8, 2953-2963.
47. Wang, Z.Q., Fung, M.R., Barlow, D.P. and Wagner, E.F. (1994) Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature, 372, 464-467.
48. Fortier, A.L., Lopes, F.L., Darricarrere, N., Martel, J. and Trasler, J.M. (2008) Superovulation alters the expression of imprinted genes in the midgestation mouse placenta. Hum. Mol. Genet., 17, 1653-1665.
49. Constancia, M., Angiolini, E., Sandovici, I., Smith, P., Smith, R., Kelsey, G., Dean, W., Ferguson-Smith, A., Sibley, C.P., Reik, W. et al. (2005) Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. Proc. Natl Acad. Sci. USA, 102, 19219-19224.
50. Li, L., Keverne, E.B., Aparicio, S.A., Ishino, F., Barton, S.C. and Surani, M.A. (1999) Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science, 284, 330-333.
51. Takahashi, K., Kobayashi, T. and Kanayama, N. (2000) p57(Kip2) regulates the proper development of labyrinthine and spongiotrophoblasts. Mol. Hum. Reprod., 6, 1019-1025.
52. Kawahara, M., Wu, Q., Yaguchi, Y., Ferguson-Smith, A.C. and Kono, T. (2006) Complementary roles of genes regulated by two paternally methylated imprinted regions on chromosomes 7 and 12 in mouse placentation. Hum. Mol. Genet., 15, 2869-2879.
53. Sekita, Y., Wagatsuma, H., Nakamura, K., Ono, R., Kagami, M., Wakisaka, N., Hino, T., Suzuki-Migishima, R., Kohda, T., Ogura, A. et al. (2008) Role of retrotransposon-derived imprinted gene, Rtl1, in the feto-maternal interface of mouse placenta. Nat. Genet., 40, 243-248.
54. Smallwood, A., Papageorghiou, A., Nicolaides, K., Alley, M.K., Jim, A., Nargund, G., Ojha, K., Campbell, S. and Banerjee, S. (2003) Temporal regulation of the expression of syncytin (HERV-W), maternally imprinted PEG10, and SGCE in human placenta. Biol. Reprod., 69, 286-293.
55. Ono, R., Shiura, H., Aburatani, H., Kohda, T., Kaneko-Ishino, T. and Ishino, F. (2003) Identification of a large novel imprinted gene cluster on mouse proximal chromosome 6. Genome Res., 13, 1696-1705.
56. Iacob, D., Cai, J., Tsonis, M., Babwah, A., Chakraborty, C., Bhattacharjee, R.N. and Lala, P.K. (2008) Decorin-mediated inhibition of proliferation and migration of the human trophoblast via different tyrosine kinase receptors. Endocrinology, 149, 6187-6197.
57. Sandell, L.L., Guan, X.J., Ingram, R. and Tilghman, S.M. (2003) Gatm, a creatine synthesis enzyme, is imprinted in mouse placenta. Proc. Natl Acad. Sci. USA, 100, 4622-4627.
58. McMinn, J., Wei, M., Schupf, N., Cusmai, J., Johnson, E.B., Smith, A.C., Weksberg, R., Thaker, H.M. and Tycko, B. (2006) Unbalanced placental expression of imprinted genes in human intrauterine growth restriction. Placenta, 27, 540-549.
59. Mizuno, Y., Sotomaru, Y., Katsuzawa, Y., Kono, T., Meguro, M., Oshimura, M., Kawai, J., Tomaru, Y., Kiyosawa, H., Nikaido, I. et al. (2002) Asb4, Ata3, and Dcn are novel imprinted genes identified by high-throughput screening using RIKEN cDNA microarray. Biochem. Biophys. Res. Commun., 290, 1499-1505.
60. Xu, G., Guimond, M.J., Chakraborty, C. and Lala, P.K. (2002) Control of proliferation, migration, and invasiveness of human extravillous trophoblast by decorin, a decidual product. Biol. Reprod., 67, 681-689.
61. Guerif, F., Le Gouge, A., Giraudeau, B., Poindron, J., Bidault, R., Gasnier, O. and Royere, D. (2007) Limited value of morphological assessment at days 1 and 2 to predict blastocyst development potential: a prospective study based on 4042 embryos. Hum. Reprod., 22, 1973-1981.
62. Dupont, J.M., Tost, J., Jammes, H. and Gut, I.G. (2004) De novo quantitative bisulfite sequencing using the pyrosequencing technology. Anal. Biochem., 333, 119-127.