Parental origin-specific expression of Mash2 is established at the time of implantation with its imprinting mechanism highly resistant to genome-wide demethylation

Mechanisms of Development

Volumn 87, Issue 1-2, 1999, Pages 129-142

  Tanaka, Mika ^a   Puchyr, Martina ^a   Gertsenstein, Marina ^a   Harpal, Kendraprasad ^a   Jaenisch, Rudolf ^c   Rossant, Janet ^a,b   Nagy, Andras ^a,b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Dnmt1; Genomic imprinting; Mash2; Methylation; Mouse; Placenta; Trophoblast

Indexed keywords

DNA METHYLTRANSFERASE; TRANSCRIPTION FACTOR;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHORIOALLANTOIS; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; EMBRYO; FATHER; FEMALE; GENE CASSETTE; GENE EXPRESSION; GENE INSERTION; GENOME IMPRINTING; IMPLANTATION; MALE; MOTHER; MOUSE; MUTANT; NONHUMAN; PARENT; PLACENTA; PRIORITY JOURNAL; TIME; TROPHOBLAST;

ANIMALS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CPG ISLANDS; DNA METHYLATION; DNA-BINDING PROTEINS; ECTODERM; EMBRYO IMPLANTATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; GENOMIC IMPRINTING; HUMANS; IN SITU HYBRIDIZATION; LAC OPERON; MALE; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, NUCLEIC ACID; TIME FACTORS; TRANSCRIPTION FACTORS; TROPHOBLASTS;

EID: 0032878170     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0925-4773(99)00158-6     Document Type: Article

References (52)

1. Alders M., Hodges M., Hadjantonakis A.K., Postmus J., van Wijk I., Bliek J., de Meulemeester M., Westerveld A., Guillemot F. The human Achaete-Scute homologue 2 (ASCL2,HASH2) maps to chromosome 11p15.5, close to IGF2 and is expressed in extravillus trophoblasts. Hum. Mol. Genet. 6:1997;859-867.
2. Bartolomei M.S., Zemel S., Tilghman S.M. Parental imprinting of the mouse H19 gene. Nature. 351:1991;153-155.
3. Bartolomei M.S., Webber A.L., Brunkow M.E., Tilghman S.M. Epigenetic mechanisms underlying the imprinting of the mouse H19 gene. Genes Dev. 7:1993;1663-1673.
4. Beard C., Li E., Jaenisch R. Loss of methylation activates Xist in somatic but not in embryonic cells. Genes Dev. 9:1995;2325-2334.
5. Bestor T.H. Cloning of a mammalian DNA methyltransferase. Gene. 74:1988;9-12.
6. Calzonetti T., Stevenson L., Rossant J. A novel regulatory region is required for trophoblast-specific transcription in transgenic mice. Dev. Biol. 171:1995;615-626.
7. Campuzano S., Modolell J. Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet. 8:1992;202-208.
8. Caspary T., Cleary M.A., Baker C.C., Guan X.J., Tilghman S.M. Multiple mechanisms regulate imprinting of the mouse distal chromosome 7 gene cluster. Mol. Cell Biol. 18:1998;3466-3474.
9. Chapman V., Forrester L., Sanford J., Hastie N., Rossant J. Cell lineage-specific undermethylation of mouse repetitive DNA. Nature. 307:1984;284-286.
10. Conlon R.A., Rossant J. Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development. 116:1992;357-368.
11. Ferguson-Smith A.C., Cattanach B.M., Barton S.C., Beechey C.V., Surani M.A. Embryological and molecular investigations of parental imprinting on mouse chromosome 7 [see comments]. Nature. 351:1991;667-670.
12. Ferguson-Smith A.C., Sasaki H., Cattanach B.M., Surani M.A. Parental-origin-specific epigenetic modification of the mouse H19 gene. Nature. 362:1993;751-755.
13. Ghysen A., Dambly-Chaudiere C. From DNA to form: the achaete-scute complex. Genes Dev. 2:1988;495-501.
14. Giddings S.J., King C.D., Harman K.W., Flood J.F., Carnaghi L.R. Allele specific inactivation of insulin 1 and 2, in the mouse yolk sac, indicates imprinting. Nat. Genet. 6:1994;310-313.
15. Gould T.D., Pfeifer K. Imprinting of mouse Kvlqt1 is developmentally regulated. Hum. Mol. Genet. 7:1998;483-487.
16. Guillemot F., Nagy A., Auerbach A., Rossant J., Joyner A.L. Essential role of Mash-2 in extraembryonic development. Nature. 371:1994;333-336.
17. Guillemot F., Caspary T., Tilghman S.M., Copeland N.G., Gilbert D.J., Jenkins N.A., Anderson D.J., Joyner A.L., Rossant J., Nagy A. Genomic imprinting of Mash2, a mouse gene required for trophoblast development. Nat. Genet. 9:1995;235-241.
18. Hatada I., Mukai T. Genomic imprinting of p57KIP2, a cyclin-dependent kinase inhibitor, in mouse. Nat. Genet. 11:1995;204-206.
19. Henry I., Jeanpierre M., Couillin P., Barichard F., Serre J.L., Journel H., Lamouroux A., Turleau C., de Grouchy J. Molecular definition of the 11p15.5 region involved in Beckwith- Wiedemann syndrome and probably in predisposition to adrenocortical carcinoma. Hum. Genet. 81:1989;273-277.
20. Jaenisch R. DNA methylation and imprinting: why bother? [see comments]. Trends Genet. 13:1997;323-329.
21. Jang S.K., Krausslich H.G., Nicklin M.J., Duke G.M., Palmenberg A.C., Wimmer E. A segment of the 5' nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62:1988;2636-2643.
22. Johnson J.E., Birren S.J., Anderson D.J. Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature. 346:1990;858-861.
23. Kusuda J., Hirata M., Yoshizaki N., Kameoka Y., Takahashi I., Hashimoto K. Over 80% of NotI sites are associated with CpG rich islands in the sequenced human DNA. Jinrui Idengaku Zasshi. 35:1990;277-282.
24. Lei H., Oh S.P., Okano M., Juttermann R., Goss K.A., Jaenisch R., Li E. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development. 122:1996;3195-3205.
25. Lescisin K.R., Varmuza S., Rossant J. Isolation and characterization of a novel trophoblast-specific cDNA in the mouse. Genes Dev. 2:1988;1639-1646.
26. Li E., Bestor T.H., Jaenish R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell. 69:1992;915-926.
27. Li E., Beard C., Jaenisch R. Role for DNA methylation in genomic imprinting. Nature. 366:1993;362-365.
28. Martinez C., Modolell J. Cross-regulatory interactions between the proneural achaete and scute genes of Drosophila. Science. 251:1991;1485-1487.
29. Miquerol L., Gertsenstein M., Harpal K., Rossant J., Nagy A. Multiple developmental roles of VEGF suggested by a LacZ-tagged allele. Dev. Biol. 1999.
30. Moens C.B., Stanton B.R., Parada L.F., Rossant J. Defects in heart and lung development in compound heterozygotes for two different targeted mutations at the N-myc locus. Development. 119:1993;485-499.
31. Monk M., Boubelik M., Lehnert S. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development. 99:1987;371-382.
32. Nagy A., Rossant J., Nagy R., Abramow-Newerly W., Roder J.C. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA. 90:1993;8424-8428.
33. Nagy A., Moens C., Ivanyi E., Pawling J., Gertsenstein M., Hadjantonakis A.K., Pirity M., Rossant J. Dissecting the role of N-myc in development using a single targeting vector to generate a series of alleles [In Process Citation]. Curr. Biol. 8:1998;661-664.
34. Obata Y., Kaneko-Ishino T., Koide T., Takai Y., Ueda T., Domeki I., Shiroishi T., Ishino F., Kono T. Disruption of primary imprinting during oocyte growth leads to the modified expression of imprinted genes during embryogenesis. Development. 125:1998;1553-1560.
35. Okano M., Xie S., Li E. Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells [In Process Citation]. Nucleic Acids Res. 26:1998;2536-2540.
36. Ping A.J., Reeve A.E., Law D.J., Young M.R., Boehnke M., Feinberg A.P. Genetic linkage of Beckwith-Wiedemann syndrome to 11p15. Am. J. Hum. Genet. 44:1989;720-723.
37. Razin A., Cedar H. DNA methylation and genomic imprinting. Cell. 77:1994;473-476.
38. Rossant J., Sanford J.P., Chapman V.M., Andrews G.K. Undermethylation of structural gene sequences in extraembryonic lineages of the mouse. Dev. Biol. 117:1986;567-573.
39. Rossant J., Guillemot F., Tanaka M., Latham K., Gertenstein M., Nagy A. Mash2 is expressed in oogenesis and preimplantation development but is not required for blastocyst formation. Mech. Dev. 73:1998;183-191.
40. Shemer R., Birger Y., Riggs A.D., Razin A. Structure of the imprinted mouse Snrpn gene and establishment of its parental-specific methylation pattern. Proc. Natl. Acad. Sci. USA. 94:1997;10267-10272.
41. Stoger R., Kubicka P., Liu C.G., Kafri T., Razin A., Cedar H., Barlow D.P. Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell. 73:1993;61-71.
42. Sutcliffe J.S., Nakao M., Christian S., Orstavik K.H., Tommerup N., Ledbetter D.H., Beaudet A.L. Deletions of a differentially methylated CpG island at the SNRPN gene define a putative imprinting control region [see comments]. Nat. Genet. 8:1994;52-58.
43. Szabo P.E., Mann J.R. Allele-specific expression and total expression levels of imprinted genes during early mouse development: implications for imprinting mechanisms. Genes Dev. 9:1995;3097-3108.
44. Takeuchi T., Yamazaki Y., Katoh-Fukui Y., Tsuchiya R., Kondo S., Motoyama J., Higashinakagawa T. Gene trap capture of a novel mouse gene, jumonji, required for neural tube formation. Genes Dev. 9:1995;1211-1222.
45. Tanaka M., Gertsenstein M., Rossant J., Nagy A. Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev. Biol. 190:1997;55-65.
46. Tremblay K.D., Saam J.R., Ingram R.S., Tilghman S.M., Bartolomei M.S. A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat. Genet. 9:1995;407-413.
47. Tremblay K.D., Duran K.L., Bartolomei M.S. A 5' 2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol. Cell Biol. 17:1997;4322-4329.
48. Tucker K.L., Beard C., Dausmann J., Jackson-Grusby L., Laird P.W., Lei H., Li E., Jaenisch R. Germ-line passage is required for establishment of methylation and expression patterns of imprinted but not of nonimprinted genes. Genes Dev. 10:1996;1008-1020.
49. Villares R., Cabrera C.V. The achaete-scute gene complex of D. melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc. Cell. 50:1987;415-424.
50. Wilkinson D.G., Bailes J.A., McMahon A.P. Expression of the proto-oncogene int-1 is restricted to specific neural cells in the developing mouse embryo. Cell. 50:1987;79-88.
51. Wood S.A., Allen N.D., Rossant J., Auerbach A., Nagy A. Non-injection methods for the production of embryonic stem cell-embryo chimeras. Nature. 365:1993;87-89.
52. Yoder J.A., Bestor T.H. A candidate mammalian DNA methyltransferase related to pmt1p of fission yeast. Hum. Mol. Genet. 7:1998;279-284.