Architectural reorganization of the nuclei upon transfer into oocytes accompanies genome reprogramming

Molecular Reproduction and Development

Volumn 73, Issue 9, 2006, Pages 1102-1111

  Martin, Catherine ^a,b   Brochard, Vincent ^a   Migné, Carole ^a   Zink, Daniele ^b   Debey, Pascale ^a,c   Beaujean, Nathalie ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

^b UNIVERSITY OF MUNICH   (Germany)

^c MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Chromatin; Chromocenters; Mouse embryo; Nuclear transfer; Nuclear ultrastucture

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTOCYST; CELL NUCLEUS; CELL NUCLEUS TRANSPLANTATION; CENTROMERE; CHROMATIN; CHROMOSOME NOR; CHROMOSOME REARRANGEMENT; CLONING; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENOME; GENOME ANALYSIS; HETEROCHROMATIN; METAPHASE CHROMOSOME; MOUSE; NONHUMAN; NUCLEOLUS; OOCYTE; PRIORITY JOURNAL; SOMATIC CELL GENETICS;

ANIMALS; CELL NUCLEUS; CELLS, CULTURED; CHROMATIN; CHROMOSOMES, MAMMALIAN; CYTOPLASM; EMBRYO; EMBRYO, MAMMALIAN; FEMALE; GENOME; MICE; MICROSCOPY, ELECTRON; MITOSIS; NUCLEAR TRANSFER TECHNIQUES; OOCYTES; TIME FACTORS;

EID: 33746631685     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20506     Document Type: Article

References (51)

1. Adenot PG, Szollosi MS, Geze M, Renard JP, Debey P. 1991. Dynamics of paternal chromatin changes in live one-cell mouse embryo after natural fertilization. Mol Reprod Dev 28:23-34.
2. Adenot PG, Mercier Y, Renard JP, Thompson EM. 1997. Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124:4615-4625.
3. Aoki F, Worrad DM, Schultz RM. 1997. Regulation of transcriptional activity during the first and second cycles in the preimplantation mouse embryo. Dev Biol 181:296-307.
4. Arney KL, Bao S, Bannister AJ, Kouzarides T, Surani MA. 2002. Histone methylation defines epigenetic asymmetry in the mouse zygote. Int J Dev Biol 46:317-320.
5. Beaujean N, Bouniol-Baly C, Monod C, Kissa K, Jullien D, Aulner N, Amirand C, Debey P, Kas E. 2000. Induction of early transcription in one-cell mouse embryos by microinjection of the nonhistone chromosomal protein HMG-I. Dev Biol 221:337-354.
6. Beaujean N, Taylor J, Gardner J, Wilmut I, Meehan R, Young L. 2004. Effect of limited DNA methylation reprogramming in the normal sheep embryo on somatic cell nuclear transfer. Biol Reprod 71:185-193.
7. Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K, Fauth C, Muller S, Eils R, Cremer C, Speicher MR, Cremer T. 2005. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol 5:57.
8. Bouniol C, Nguyen E, Debey P. 1995. Endogenous transcription occurs at the 1-cell stage in the mouse embryo. Exp Cell Res 218:57-62.
9. Brown KE, Guest SS, Smale ST, Hahm K, Merkenschlager M, Fisher AG. 1997. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 91:845-854.
10. Brown KE, Baxter J, Graf D, Merkenschlager M, Fisher AG. 1999. Dynamic repositioning of genes in the nucleus of lymphocytes preparing for cell division. Mol Cell 3:207-217.
11. Gerda MC, Berrios S, Fernandez-Donoso R, Garagna S, Redi C. 1999. Organisation of complex nuclear domains in somatic mouse cells. Biol Cell 91:55-65.
12. Clegg KB, Piko L. 1983. Quantitative aspects of RNA synthesis and polyadenylation in 1-cell and 2-cell mouse embryos. J Embryol Exp Morphol 74:169-182.
13. Cremer T, Kurz A, Zirbel R, Dietzel S, Rinke B, Schrock E, Speicher MR, Mathieu U, Jauch A, Emmerich P, Scherthan H, Ried T, Cremer C, Lichter P. 1993. Role of chromosome territories in the functional compartmentalization of the cell nucleus. Cold Spring Harb Symp Quant Biol 58:777-792.
14. Cremer T, Cremer C. 2001. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 4:292-301.
15. Cremer M, Kupper K, Wagler B, Wizelman L, von Hase J, Weiland Y, KrejaL, Diebold J, Speicher MR, Cremer T. 2003. Inheritance of gene density-related higher order chromatin arrangements in normal and tumor cell nuclei. J Cell Biol 162:809-820.
16. Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA. 1999. Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 145:1119-1131.
17. Dean W, Lucifero D, Santos F. 2005. DNA methylation in mammalian development and disease. Birth Defects Res C Embryo Today 75:98-111.
18. Debey P, Renard JP, Coppey-Moisan M, Monnot I, Geze M. 1989. Dynamics of chromatin changes in live one-cell mouse embryos: A continuous follow-up by fluorescence microscopy. Exp Cell Res 183:413-433.
19. Dozortsev D, Coleman A, Nagy P, Diamond MP, Ermilov A, Weier U, Liyanage M, Reid T. 2000. Nucleoli in a pronuclei-stage mouse embryo are represented by major satellite DNA of interconnecting chromosomes. Fertil Steril 73:366-371.
20. Dundr M, Misteli T. 2001. Functional architecture in the cell nucleus. Biochem J 356:297-310.
21. Fakan S, Odartchenko N. 1980. Ultrastructural organization of the cell nucleus in early mouse embryos. Biol Cell 37:211-218.
22. Flechon JE, Kopecny V. 1998. The nature of the 'nucleolus precursor body' in early preimplantation embryos: A review of fine-structure cytochemical, immunocytochemical and autoradiographic data related to nucleolar function. Zygote 6:183-191.
23. Francastel C, Walters MC, Groudine M, Martin DI. 1999. A functional enhancer suppresses silencing of a transgene and prevents its localization close to centrometric heterochromatin. Cell 99:259-269.
24. Geuskens M, Alexandre H. 1984. Ultrastructural and autoradiographic studies of nucleolar development and rDNA transcription in preimplantation mouse embryos. Cell Differ 14:125-134.
25. Grewal SI, Rice JC. 2004. Regulation of heterochromatin by histone methylation and small RNAs. Curr Opin Cell Biol 16:230-238.
26. Haaf T, Schmid M. 1991. Chromosome topology in mammalian interphase nuclei. Exp Cell Res 192:325-332.
27. Hayakawa T, Haraguchi T, Masumoto H, Hiraoka Y. 2003. Cell cycle behavior of human HP1 subtypes: Distinct molecular domains of HP1 are required for their centromeric localization during interphase and metaphase. J Cell Sci 116:3327-3338.
28. Latham KE. 1999. Mechanisms and control of embryonic genome activation in mammalian embryos. Int Rev Cytol 193:71-124.
29. Latham KE, Garrels JI, Chang C, Solter D. 1991a. Quantitative analysis of protein synthesis in mouse embryos. I. Extensive reprogramming at the one- and two-cell stages. Development 112:921-932.
30. Latham KE, Solter D, Schultz RM. 1991b. Activation of a two-cell stage-specific gene following transfer of heterologous nuclei into enucleated mouse embryos. Mol Reprod Dev 30:182-186.
31. Manuelidis L. 1985. Individual interphase chromosome domains revealed by in situ hybridization. Hum Genet 71:288-293.
32. Manuelidis L, Borden J. 1988. Reproducible compartmentalization of individual chromosome domains in human CNS cells revealed by in situ hybridization and three-dimensional reconstruction. Chromosoma 96:397-410.
33. Martin C, Beaujean N, Brochard V, Audouard C, Zink D, Debey P. 2006. Genome restructuring in mouse embryos during reprogramming and early development. Dev Biol 292:317-332.
34. Mayer W, Smith A, Fundele R, Haaf T. 2000. Spatial separation of parental genomes in preimplantation mouse embryos. J Cell Biol 148:629-634.
35. McLay DW, Clarke HJ. 2003. Remodelling the paternal chromatin at fertilization in mammals. Reproduction 125:625-633.
36. Mine E, Allory Y, Worman HJ, Courvalin JC, Buendia B. 1999. Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma 108:220-234.
37. Misteli T. 2004. Spatial positioning; a new dimension in genome function. Cell 119:153-156.
38. Nothias JY, Majumder S, Kaneko KJ, DePamphilis ML. 1995. Regulation of gene expression at the beginning of mammalian development. J Biol Chem 270:22077-22080.
39. Parada LA, McQueen PG, Munson PJ, Misteli T. 2002. Conservation of relative chromosome positioning in normal and cancer cells. Curr Biol 12:1692-1697.
40. Reik W, Walter J. 2001. Genomic imprinting: Parental influence on the genome. Nat Rev Genet 2:21-32.
41. Reik W, Dean W, Walter J. 2001. Epigenetic reprogramming in mammalian development. Science 293:1089-1093.
42. Santos F, Hendrich B, Reik W, Dean W. 2002. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 241:172-182.
43. Schubeler D, Francastel C, Cimbora DM, Reik A, Martin DI, Groudine M. 2000. Nuclear localization and histone acetylation: A pathway for chromatin opening and transcriptional activation of the human beta-globin locus. Genes Dev 14:940-950.
44. Schultz RM, Worrad DM. 1995. Role of chromatin structure in zygotic gene activation in the mammalian embryo. Semin Cell Biol 6:201-208.
45. Shaw PJ, Abranches R, Paula Santos A, Beven AF, Stoger E, Wegel E, Gonzalez-Melendi P. 2002. The architecture of interphase chromosomes and nucleolar transcription sites in plants. J Struct Biol 140:31-38.
46. Taddei A, Hediger F, Neumann FR, Gasser SM. 2004. The function of nuclear architecture: A genetic approach. Annu Rev Genet 38:305-345.
47. Takeuchi IK, Takeuchi YK. 1986. Ultrastructural localization of Ag-NOR proteins in full-grown oocytes and preimplantation embryos of mice. J Electron Microsc (Tokyo) 35:280-287.
48. Tanabe H, Habermann FA, Solovei I, Cremer M, Cremer T. 2002. Non-random radial arrangements of interphase chromosome territories: Evolutionary considerations and functional implications. Mutat Res 504:37-45.
49. Zatsepina O, Baly C, Chebrout M, Debey P. 2003. The step-wise assembly of a functional nucleolus in preimplantation mouse embryos involves the cajal (coiled) body. Dev Biol 253:66-83.
50. Zhou Q, Jouneau A, Brochard V, Adenot P, Renard JP. 2001. Developmental potential of mouse embryos reconstructed from metaphase embryonic stem cell nuclei. Biol Reprod 65:412-419.
51. Zirbel RM, Mathieu UR, Kurz A, Cremer T, Lichter P. 1993. Evidence for a nuclear compartment of transcription and splicing located at chromosome domain boundaries. Chromosome Res 1:93-106.