DNA methyltransferase is actively retained in the cytoplasm during early development

Journal of Cell Biology

Volumn 147, Issue 1, 1999, Pages 25-32

  Cardoso, M Cristina ^a   Leonhardt, Heinrich ^a,b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b FRANZ VOLHARD CLINIC   (Germany)

Author keywords

Cytoplasmic retention; DNA methylation; DNA methyltransferase; Genomic imprinting; Preimplantation development

Indexed keywords

DNA METHYLTRANSFERASE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BLASTOCYST; CELL STRAIN COS1; CONTROLLED STUDY; DNA BINDING; DNA METHYLATION; GENOME IMPRINTING; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; ZYGOTE;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BLASTOCYST; CELL LINE; CELL NUCLEUS; CYTOPLASM; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; MICE, INBRED C57BL; MOLECULAR WEIGHT; NUCLEAR LOCALIZATION SIGNALS; PROTEIN ISOFORMS; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; ZYGOTE;

ANIMALIA; MAMMALIA;

EID: 0033523760     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.147.1.25     Document Type: Article

References (42)

1. Bestor, T., A. Laudano, R. Mattaliano, and V. Ingram. 1988. Cloning and sequencing of a cDNA encoding DNA melhyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J. Mol. Biol. 203:971-983.
2. Bestor, T.H. 1992. Activation of mammalian DNA methyltransferase by cleavage of a Zn binding regulatory domain. EMBO (Eur. Mol. Biol. Organ.) J. 11:2611-2617.
3. Bhattacharya, S. K., S. Ramchandani, N. Cervoni, and M. Szyf. 1999. A mammalian protein with specific demethylase activity for mCpG DNA. Nature. 397:579-583.
4. Birger, Y., R. Shemer, J. Perk, and A. Razin. 1999. The imprinting box of the mouse Igf2r gene. Nature. 397:84-88.
5. Cardoso, M.C., C. Joseph, H.P. Rahn, R. Reusch, B. Nadal-Ginard, and H. Leonhardt. 1997. Mapping and use of a sequence that targets DNA ligase I to sites of DNA replication in vivo. J. Cell Biol. 139:579-587.
6. Cardoso, M.C., and H. Leonhardt. 1995. Immunofluorescence techniques in cell cycle studies. In Cell Cycle: Materials and Methods. M. Pagano, editor. Springer-Verlag, Heidelberg. 15-28.
7. Cardoso, M.C., H. Leonhardt, and B. Nadal-Ginard. 1993. Reversal of terminal differentiation and control of DNA replication: cyclin A and Cdk2 specifically localize at subnuclear sites of DNA replication. Cell. 74:979-992.
8. Carlson, L.L., A.W. Page, and T.H. Bestor. 1992. Properties and localization of DNA methyltransferase in preimplantation mouse embryos: implications for genomic imprinting. Genes Dev. 6:2536-2541.
9. Constancia, M., B. Pickard, G. Kelsey, and W. Reik. 1998. Imprinting mechanisms. Genome Res. 8:881-900.
10. Czank, A., R. Hauselmann, A.W. Page, H. Leonhardt, T.H. Bestor, W. Schaffner, and M. Hergersberg. 1991. Expression in mammalian cells of a cloned gene encoding murine DNA methyltransferase. Gene. 109:259-263.
11. Dabauvalle, M.C., and W.W. Franke. 1984. Karyophobic proteins. A category of abundant soluble proteins which accumulate in the cytoplasm. Exp. Cell Res. 153:308-326.
12. Dreyer, C. 1987. Differential accumulation of oocyte nuclear proteins by embryonic nuclei of Xenopus. Development. 101:829-846.
13. Gaudet, F., D. Talbot, H. Leonhardt, and R. Jaenisch. 1998. A short DNA methyltransferase isoform restores methylation in vivo. J. Biol. Chem. 273: 32725-32729.
14. Hogan, B., R. Beddington, F. Constantini, and E. Lacy. 1994. Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
15. Howlett, S.K., and W. Reik. 1991. Methylation levels of maternal and paternal genomes during preimplantation development. Development. 113:119-127.
16. Latham, K.E., J.I. Garrels, and D. Solter. 1994. Alterations in protein synthesis following transplantation of mouse 8-cell stage nuclei to enucleated 1-cell embryos. Dev. Biol. 163:341-350.
17. Latham, K.E., J. McGrath, and D. Solter. 1995. Mechanistic and developmental aspects of genetic imprinting in mammals. Int. Rev. Cytol. 160:53-98.
18. Lawitts, J.A., and J.D. Biggers. 1993. Culture of preimplantation embryos. Methods Enzymol. 225:153-164.
19. Leonhardt, H., and T.H. Bestor. 1993. Structure, function and regulation of mammalian DNA methyltransferase. In DNA Methylation: Molecular Biology and Biological Significance. Vol. 64. J.P. Jost and H.P. Saluz, editors. Birkäuser Verlag, Basel, Switzerland. 109-119.
20. Leonhardt, H., A.W. Page, H.U. Weier, and T.H. Bestor. 1992. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell. 71:865-873.
21. Li, E., C. Beard, and R. Jaenisch. 1993. Role for DNA methylation in genomic imprinting. Nature. 366:362-365.
22. Li, E., T.H. Bestor, and R. Jaenisch. 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell. 69:915-926.
23. Li, X., W. Shou, M. Kloc, B.A. Reddy, and L.D. Etkin. 1994. Cytoplasmic retention of Xenopus nuclear factor 7 before the mid blastula transition uses a unique anchoring mechanism involving a retention domain and several phosphorylalion sites. J. Cell Biol. 124:7-17.
24. Mertineit, C., J.A. Yoder, T. Taketo, D.W. Laird, J.M. Trasler, and T.H. Bestor. 1998. Sex-specific exons control DNA methyltransferase in mammalian germ cells. Development. 125:889-897.
25. Monk, M., R.L. Adams, and A. Rinaldi. 1991. Decrease in DNA methylase activity during preimplantation development in the mouse. Development. 112: 189-192.
26. Monk, M., M. Boubelik, and S. Lehnert. 1987. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development. 99:371-382.
27. Okano, M., S. Xie, and E. Li. 1998a. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat. Genet. 19: 219-220.
28. Okano, M., S. Xie, and E. Li. 1998b. Dnmt2 is not required for de novo and maintenance methylation of viral DNA in embryonic stem cells. Nucleic Acids Res. 26:2536-2540.
29. Olek, A., and J. Walter. 1997. The preimplantation ontogeny of the H19 methylation imprint. Nat. Genet. 17:275-276.
30. Paine, P.L. 1984. Diffusive and nondiffusive proteins in vivo. J. Cell Biol. 99: 188-195.
31. Panning, B., and R. Jaenisch. 1996. DNA hypomethylation can activate Xist expression and silence X-linked genes. Genes Dev. 10:1991-2002.
32. Razin, A., and R. Shemer. 1995. DNA methylation in early development. Hum. Mol. Genet. 4:1751-1755.
33. Sanford, J.P., H.J. Clark, V.M. Chapman, and J. Rossant. 1987. Differences in DNA methylation during oogenesis and spcrmatogenesis and their persistence during early embryogenesis in the mouse. Genes Dev. 1:1039-1046.
34. Taylor, D.L., and E.D. Salmon. 1989. Basic fluorescence microscopy. In Fluorescence Microscopy of Living Cells in Culture. Vol. 29. Y.-L. Wang and D.L. Taylor, editors. Academic Press, San Diego, CA, 207-237.
35. Tremblay, K.D., K.L. Duran, and M.S. Bartolomei. 1997. A 5′ 2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol. Cell Biol. 17:4322-4329.
36. Tucker, K.L., D. Talbot, M.A. Lee, H. Leonhardt, and R. Jaenisch. 1996. Complementation of methylation deficiency in embryonic stem cells by a DNA methyltransferase minigene. Proc. Natl. Acad. Sci. USA. 93:12920-12925.
37. Van den Wyngaert, I., J. Sprengel, S.U. Kass, and W.H. Luyten. 1998. Cloning and analysis of a novel human putative DNA methyltransferase. FEBS Lett. 426:283-289.
38. Veenstra, G.J., M.T. Mathu, and O.H. Destree. 1999. The Oct-1 POU domain directs developmentally regulated nuclear translocalion in Xenopus embryos. Biol. Chem. 380:253-257.
39. Walsh, C.P., J.R. Chaillet, and T.H. Bestor. 1998. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20: 116-117.
40. Yoder, J.A., and T.H. Bestor. 1998. A candidate mammalian DNA methyltransferase related to pmt 1p of fission yeast. Hum. Mol. Genet. 7:279-284.
41. Yoder, J.A., R.W.C. Yen, P.M. Vertino, T.H. Bestor, and S.B. Baylin. 1996. New 5′ regions of the murine and human genes for DNA (cytosine-5)-methyltransferase. J. Biol. Chem. 271:31092-31097.
42. Zimmermann, C., E. Guhl, and A. Graessmann. 1997. Mouse DNA methyltransferase (MTase) deletion mutants that retain the catalytic domain display neither de novo nor maintenance methylation activity in vivo. Biol. Chem. 378:393-405.